Current developments of pharmacotherapy targeting heme oxygenase 1 in cancer (Review)
- Authors:
- Xiaohu Ouyang
- Jingbo Wang
- Xiaoyuan Qiu
- Desheng Hu
- Jing Cui
-
Affiliations: Department of Integrated Traditional Chinese and Western Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430022, P.R. China, Health Management Center, Hubei Provincial Hospital of Integrated Chinese & Western Medicine, Wuhan, Hubei 430015, P.R. China - Published online on: February 18, 2025 https://doi.org/10.3892/ijo.2025.5732
- Article Number: 26
This article is mentioned in:
Abstract
![]() |
![]() |
![]() |
Bray F, Laversanne M, Sung H, Ferlay J, Siegel RL, Soerjomataram I and Jemal A: Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 74:229–263. 2024. View Article : Google Scholar : PubMed/NCBI | |
Tenhunen R, Marver HS and Schmid R: Microsomal heme oxygenase. Characterization of the enzyme. J Biol Chem. 244:6388–6394. 1969. View Article : Google Scholar : PubMed/NCBI | |
Keyse SM and Tyrrell RM: Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci USA. 86:99–103. 1989. View Article : Google Scholar : PubMed/NCBI | |
Maines MD, Trakshel GM and Kutty RK: Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J Biol Chem. 261:411–419. 1986. View Article : Google Scholar : PubMed/NCBI | |
Shibahara S, Müller R, Taguchi H and Yoshida T: Cloning and expression of cDNA for rat heme oxygenase. Proc Natl Acad Sci USA. 82:7865–7869. 1985. View Article : Google Scholar : PubMed/NCBI | |
Kim HP, Wang X, Galbiati F, Ryter SW and Choi AM: Caveolae compartmentalization of heme oxygenase-1 in endothelial cells. FASEB J. 18:1080–1089. 2004. View Article : Google Scholar : PubMed/NCBI | |
Bindu S, Pal C, Dey S, Goyal M, Alam A, Iqbal MS, Dutta S, Sarkar S, Kumar R, Maity P and Bandyopadhyay U: Translocation of heme oxygenase-1 to mitochondria is a novel cytoprotective mechanism against non-steroidal anti-inflammatory drug-induced mitochondrial oxidative stress, apoptosis, and gastric mucosal injury. J Biol Chem. 286:39387–39402. 2011. View Article : Google Scholar : PubMed/NCBI | |
Lin Q, Weis S, Yang G, Weng YH, Helston R, Rish K, Smith A, Bordner J, Polte T, Gaunitz F and Dennery PA: Heme oxygenase-1 protein localizes to the nucleus and activates transcription factors important in oxidative stress. J Biol Chem. 282:20621–20633. 2007. View Article : Google Scholar : PubMed/NCBI | |
Tenhunen R, Marver HS and Schmid R: The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA. 61:748–755. 1967. View Article : Google Scholar | |
Jozkowicz A, Huk I, Nigisch A, Weigel G, Weidinger F and Dulak J: Effect of prostaglandin-J(2) on VEGF synthesis depends on the induction of heme oxygenase-1. Antioxid Redox Signal. 4:577–585. 2002. View Article : Google Scholar : PubMed/NCBI | |
Li Volti G, Tibullo D, Vanella L, Giallongo C, Di Raimondo F, Forte S, Di Rosa M, Signorelli SS and Barbagallo I: The heme oxygenase system in hematological malignancies. Antioxid Redox Signal. 27:363–377. 2017. View Article : Google Scholar : PubMed/NCBI | |
Acharya R, Deb PK and attanayak SP: An azomethine derivative, 1-(4-nitrophenyl)-N-phenylmethanimine (BCS2) ameliorated 7,12-dimethylbenz(a)anthracene-induced mammary carcinoma through Nrf2-keap1-HO-1 pathway. Curr Med Chem. Jan 6–2025.(Epub ahead of print). View Article : Google Scholar | |
Sadiq A, Chen P and Fert-Bober J: Silencing PADI-2 induces antitumor effects by downregulating NF-κB, Nrf2/HO-1 and AKT1 in A549 lung cancer cells. Int Immunopharmacol. 146:1138302025. View Article : Google Scholar : PubMed/NCBI | |
Becker JC, Fukui H, Imai Y, Sekikawa A, Kimura T, Yamagishi H, Yoshitake N, Pohle T, Domschke W and Fujimori T: Colonic expression of heme oxygenase-1 is associated with a better long-term survival in patients with colorectal cancer. Scand J Gastroenterol. 42:852–858. 2007. View Article : Google Scholar : PubMed/NCBI | |
Goswami B, Rajappa M, Sharma M and Sharma A: Inflammation: its role and interplay in the development of cancer, with special focus on gynecological malignancies. Int J Gynecol Cancer. 18:591–599. 2008. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Chen M, Yu H, Yuan G, Luo L, Xu X, Xu Y, Sui X, Leung EL and Wu Q: The role and mechanisms of action of natural compounds in the prevention and treatment of cancer and cancer metastasis. Front Biosci (Landmark Ed). 27:1922022. View Article : Google Scholar : PubMed/NCBI | |
Wei Z, Chen J, Zuo F, Guo J, Sun X, Liu D and Liu C: Traditional Chinese medicine has great potential as candidate drugs for lung cancer: A review. J Ethnopharmacol. 300:1157482023. View Article : Google Scholar : PubMed/NCBI | |
Xu Y, Cai Q, Zhao C, Zhang W, Xu X, Lin H, Lin Y, Chen D, Lin S, Jia P, et al: Gegen qinlian decoction attenuates colitis-associated colorectal cancer via suppressing TLR4 signaling pathway based on network pharmacology and in vivo/in vitro experimental validation. Pharmaceuticals (Basel). 18:122024. View Article : Google Scholar : PubMed/NCBI | |
Zhang T, Yuan J, Ju X, Zhou J, Zhai X, Chu C, Tan M, Ju G, Gu J and Xu D: Modified shenqi dihuang decoction inhibits prostate cancer metastasis by disrupting TCA cycle energy metabolism via NF-kB/p65-mediated OGDH regulation. Phytomedicine. 138:1564052025.(Epub ahead of print). View Article : Google Scholar : PubMed/NCBI | |
Wang W, Lin F, Shi S, Yu Y, Lin M, Lian W, Chen B and Qi X: Investigating the role of quercetin, an active ingredient in bazhen decoction, in targeting CXCL8 to inhibit macrophage M2 polarization and reshape the immunological microenvironment of colorectal cancer. Chem Biol Drug Des. 105:e700472025. View Article : Google Scholar : PubMed/NCBI | |
Singh M, Sharma P, Singh PK, Singh TG and Saini B: Medicinal potential of heterocyclic compounds from diverse natural sources for the management of cancer. Mini Rev Med Chem. 20:942–957. 2020. View Article : Google Scholar : PubMed/NCBI | |
Morse D and Choi AMK: Heme oxygenase-1: From bench to bedside. Am J Respir Crit Care Med. 172:660–670. 2005. View Article : Google Scholar : PubMed/NCBI | |
Detsika MG, Theochari E, Palamaris K, Gakiopoulou H and Lianos EA: Effect of heme oxygenase-1 depletion on complement regulatory proteins expression in the rat. Antioxidants (Basel). 12:612022. View Article : Google Scholar : PubMed/NCBI | |
Onyiah JC, Sheikh SZ, Maharshak N, Otterbein LE and Plevy SE: Heme oxygenase-1 and carbon monoxide regulate intestinal homeostasis and mucosal immune responses to the enteric microbiota. Gut Microbes. 5:220–224. 2014. View Article : Google Scholar : PubMed/NCBI | |
Waza AA, Hamid Z, Ali S, Bhat SA and Bhat MA: A review on heme oxygenase-1 induction: Is it a necessary evil. Inflamm Res. 67:579–588. 2018. View Article : Google Scholar : PubMed/NCBI | |
Kutty RK, Nagineni CN, Kutty G, Hooks JJ, Chader GJ and Wiggert B: Increased expression of heme oxygenase-1 in human retinal pigment epithelial cells by transforming growth factor-beta. J Cell Physiol. 159:371–378. 1994. View Article : Google Scholar : PubMed/NCBI | |
Bian C, Zhong M, Nisar MF, Wu Y, Ouyang M, Bartsch JW and Zhong JL: A novel heme oxygenase-1 splice variant, 14 kDa HO-1, promotes cell proliferation and increases relative telomere length. Biochem Biophys Res Commun. 500:429–434. 2018. View Article : Google Scholar : PubMed/NCBI | |
Durante W: Targeting heme oxygenase-1 in the arterial response to injury and disease. Antioxidants (Basel). 9:8292020. View Article : Google Scholar : PubMed/NCBI | |
Huber WJ III and Backes WL: Expression and characterization of full-length human heme oxygenase-1: The presence of intact membrane-binding region leads to increased binding affinity for NADPH cytochrome P450 reductase. Biochemistry. 46:12212–12219. 2007. View Article : Google Scholar : PubMed/NCBI | |
Jung NH, Kim HP, Kim BR, Cha SH, Kim GA, Ha H, Na YE and Cha YN: Evidence for heme oxygenase-1 association with caveolin-1 and −2 in mouse mesangial cells. IUBMB Life. 55:525–532. 2003. View Article : Google Scholar : PubMed/NCBI | |
Slebos DJ, Ryter SW, van der Toorn M, Liu F, Guo F, Baty CJ, Karlsson JM, Watkins SC, Kim HP, Wang X, et al: Mitochondrial localization and function of heme oxygenase-1 in cigarette smoke-induced cell death. Am J Respir Cell Mol Biol. 36:409–417. 2007. View Article : Google Scholar : PubMed/NCBI | |
Nitti M, Ivaldo C, Traverso N and Furfaro AL: Clinical significance of heme oxygenase 1 in tumor progression. Antioxidants (Basel). 10:7892021. View Article : Google Scholar : PubMed/NCBI | |
Signorelli SS, Li Volsi G, Fiore V, Mangiafico M, Barbagallo I, Parenti R, Rizzo M and Li Volti G: Plasma heme oxygenase-1 is decreased in peripheral artery disease patients. Mol Med Rep. 14:3459–3463. 2016. View Article : Google Scholar : PubMed/NCBI | |
Alam J, Stewart D, Touchard C, Boinapally S, Choi AM and Cook JL: Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem. 274:26071–26078. 1999. View Article : Google Scholar : PubMed/NCBI | |
Khalil HS, Langdon SP, Kankia IH, Bown J and Deeni YY: NRF2 regulates HER2 and HER3 signaling pathway to modulate sensitivity to targeted immunotherapies. Oxid Med Cell Longev. 2016:41487912016. View Article : Google Scholar : PubMed/NCBI | |
Kang MI, Kobayashi A, Wakabayashi N, Kim SG and Yamamoto M: Scaffolding of Keap1 to the actin cytoskeleton controls the function of Nrf2 as key regulator of cytoprotective phase 2 genes. Proc Natl Acad Sci USA. 101:2046–2051. 2004. View Article : Google Scholar : PubMed/NCBI | |
Zipper LM and Mulcahy RT: The keap1 BTB/POZ dimerization function is required to sequester Nrf2 in cytoplasm. J Biol Chem. 277:36544–36552. 2002. View Article : Google Scholar : PubMed/NCBI | |
Itoh K, Wakabayashi N, Katoh Y, Ishii T, O'Connor T and Yamamoto M: Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells. 8:379–391. 2003. View Article : Google Scholar : PubMed/NCBI | |
Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD and Yamamoto M: Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13:76–86. 1999. View Article : Google Scholar : PubMed/NCBI | |
Xia MH, Yan XY, Zhou L, Xu L, Zhang LC, Yi HW and Su J: p62 suppressed VK3-induced oxidative damage through keap1/Nrf2 pathway in human ovarian cancer cells. J Cancer. 11:1299–1307. 2020. View Article : Google Scholar : PubMed/NCBI | |
Alam J and Cook JL: How many transcription factors does it take to turn on the heme oxygenase-1 gene? Am J Respir Cell Mol Biol. 36:166–174. 2007. View Article : Google Scholar : PubMed/NCBI | |
Kim H, Yin K, Falcon DM and Xue X: The interaction of Hemin and Sestrin2 modulates oxidative stress and colon tumor growth. Toxicol Appl Pharmacol. 374:77–85. 2019. View Article : Google Scholar : PubMed/NCBI | |
Lu JJ, Abudukeyoumu A, Zhang X, Liu LB, Li MQ and Xie F: Heme oxygenase 1: A novel oncogene in multiple gynecological cancers. Int J Biol Sci. 17:2252–2261. 2021. View Article : Google Scholar : PubMed/NCBI | |
Kitamuro T, Takahashi K, Ogawa K, Udono-Fujimori R, Takeda K, Furuyama K, Nakayama M, Sun J, Fujita H, Hida W, et al: Bach1 functions as a hypoxia-inducible repressor for the heme oxygenase-1 gene in human cells. J Biol Chem. 278:9125–9133. 2003. View Article : Google Scholar : PubMed/NCBI | |
Igarashi K and Sun J: The heme-Bach1 pathway in the regulation of oxidative stress response and erythroid differentiation. Antioxid Redox Signal. 8:107–118. 2006. View Article : Google Scholar : PubMed/NCBI | |
Sun J, Brand M, Zenke Y, Tashiro S, Groudine M and Igarashi K: Heme regulates the dynamic exchange of Bach1 and NF-E2-related factors in the Maf transcription factor network. Proc Natl Acad Sci USA. 101:1461–1466. 2004. View Article : Google Scholar : PubMed/NCBI | |
Alam J, Killeen E, Gong P, Naquin R, Hu B, Stewart D, Ingelfinger JR and Nath KA: Heme activates the heme oxygenase-1 gene in renal epithelial cells by stabilizing Nrf2. Am J Physiol Renal Physiol. 284:F743–F752. 2003. View Article : Google Scholar : PubMed/NCBI | |
Sudan K, Vijayan V, Madyaningrana K, Gueler F, Igarashi K, Foresti R, Motterlini R and Immenschuh S: TLR4 activation alters labile heme levels to regulate BACH1 and heme oxygenase-1 expression in macrophages. Free Radic Biol Med. 137:131–142. 2019. View Article : Google Scholar : PubMed/NCBI | |
Ali FF, Abdelzaher WY, Ibrahim RA and Elroby Ali DM: Amelioration of estrogen-induced endometrial hyperplasia in female rats by hemin via heme-oxygenase-1 expression, suppression of iNOS, p38 MAPK, and Ki67. Can J Physiol Pharmacol. 97:1159–1168. 2019. View Article : Google Scholar : PubMed/NCBI | |
Alam J, Igarashi K, Immenschuh S, Shibahara S and Tyrrell RM: Regulation of heme oxygenase-1 gene transcription: Recent advances and highlights from the international conference (Uppsala, 2003) on heme oxygenase. Antioxid Redox Signal. 6:924–933. 2004. View Article : Google Scholar : PubMed/NCBI | |
Morse D, Lin L, Choi AMK and Ryter SW: Heme oxygenase-1, a critical arbitrator of cell death pathways in lung injury and disease. Free Radic Biol Med. 47:1–12. 2009. View Article : Google Scholar : PubMed/NCBI | |
Trakshel GM, Kutty RK and Maines MD: Purification and characterization of the major constitutive form of testicular heme oxygenase. The noninducible isoform. J Biol Chem. 261:11131–11137. 1986. View Article : Google Scholar : PubMed/NCBI | |
Hayashi S, Omata Y, Sakamoto H, Higashimoto Y, Hara T, Sagara Y and Noguchi M: Characterization of rat heme oxygenase-3 gene. Implication of processed pseudogenes derived from heme oxygenase-2 gene. Gene. 336:241–250. 2004. View Article : Google Scholar : PubMed/NCBI | |
Abraham NG and Kappas A: Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev. 60:79–127. 2008. View Article : Google Scholar : PubMed/NCBI | |
Ryter SW, Alam J and Choi AMK: Heme oxygenase-1/carbon monoxide: From basic science to therapeutic applications. Physiol Rev. 86:583–650. 2006. View Article : Google Scholar : PubMed/NCBI | |
O'Rourke SA, Shanley LC and Dunne A: The Nrf2-HO-1 system and inflammaging. Front Immunol. 15:14570102024. View Article : Google Scholar : PubMed/NCBI | |
Tenhunen R, Ross ME, Marver HS and Schmid R: Reduced nicotinamide-adenine dinucleotide phosphate dependent biliverdin reductase: Partial purification and characterization. Biochemistry. 9:298–303. 1970. View Article : Google Scholar : PubMed/NCBI | |
Motterlini R and Otterbein LE: The therapeutic potential of carbon monoxide. Nat Rev Drug Discov. 9:728–743. 2010. View Article : Google Scholar : PubMed/NCBI | |
Knauert M, Vangala S, Haslip M and Lee PJ: Therapeutic applications of carbon monoxide. Oxid Med Cell Longev. 2013:3608152013. View Article : Google Scholar : PubMed/NCBI | |
Li MH, Jang JH, Na HK, Cha YN and Surh YJ: Carbon monoxide produced by heme oxygenase-1 in response to nitrosative stress induces expression of glutamate-cysteine ligase in PC12 cells via activation of phosphatidylinositol 3-kinase and Nrf2 signaling. J Biol Chem. 282:28577–28586. 2007. View Article : Google Scholar : PubMed/NCBI | |
Vitek L and Tiribelli C: Bilirubin, intestinal integrity, the microbiome, and inflammation. N Engl J Med. 383:684–686. 2020. View Article : Google Scholar : PubMed/NCBI | |
Maruhashi T, Kihara Y and Higashi Y: Bilirubin and endothelial function. J Atheroscler Thromb. 26:688–696. 2019. View Article : Google Scholar : PubMed/NCBI | |
Baylor JL and Butler MW: Immune challenge-induced oxidative damage may be mitigated by biliverdin. J Exp Biol. 222:jeb2000552019. View Article : Google Scholar : PubMed/NCBI | |
Kajarabille N and Latunde-Dada GO: Programmed cell-death by ferroptosis: Antioxidants as mitigators. Int J Mol Sci. 20:49682019. View Article : Google Scholar : PubMed/NCBI | |
Ryter SW and Choi AMK: Targeting heme oxygenase-1 and carbon monoxide for therapeutic modulation of inflammation. Transl Res. 167:7–34. 2016. View Article : Google Scholar : PubMed/NCBI | |
Ryter SW: Heme oxgenase-1, a cardinal modulator of regulated cell death and inflammation. Cells. 10:5152021. View Article : Google Scholar : PubMed/NCBI | |
Dennery PA: Signaling function of heme oxygenase proteins. Antioxid Redox Signal. 20:1743–1753. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wang X, Wang Y, Kim HP, Nakahira K, Ryter SW and Choi AMK: Carbon monoxide protects against hyperoxia-induced endothelial cell apoptosis by inhibiting reactive oxygen species formation. J Biol Chem. 282:1718–1726. 2007. View Article : Google Scholar : PubMed/NCBI | |
Suttner DM, Sridhar K, Lee CS, Tomura T, Hansen TN and Dennery PA: Protective effects of transient HO-1 overexpression on susceptibility to oxygen toxicity in lung cells. Am J Physiol. 276:L443–L451. 1999.PubMed/NCBI | |
Boname JM, Bloor S, Wandel MP, Nathan JA, Antrobus R, Dingwell KS, Thurston TL, Smith DL, Smith JC, Randow F and Lehner PJ: Cleavage by signal peptide peptidase is required for the degradation of selected tail-anchored proteins. J Cell Biol. 205:847–862. 2014. View Article : Google Scholar : PubMed/NCBI | |
Mascaro M, Alonso EN, Alonso EG, Lacunza E, Curino AC and Facchinetti MM: Nuclear localization of heme oxygenase-1 in pathophysiological conditions: Does it explain the dual role in cancer? Antioxidants (Basel). 10:872021. View Article : Google Scholar : PubMed/NCBI | |
Biswas C, Shah N, Muthu M, La P, Fernando AP, Sengupta S, Yang G and Dennery PA: Nuclear heme oxygenase-1 (HO-1) modulates subcellular distribution and activation of Nrf2, impacting metabolic and anti-oxidant defenses. J Biol Chem. 289:26882–26894. 2014. View Article : Google Scholar : PubMed/NCBI | |
Yu D, Sun R, Shen D, Ge L, Xue T and Cao Y: Nuclear heme oxygenase-1 improved the hypoxia-mediated dysfunction of blood-spinal cord barrier via the miR-181c-5p/SOX5 signaling pathway. Neuroreport. 32:112–120. 2021. View Article : Google Scholar : PubMed/NCBI | |
Gandini NA, Alonso EN, Fermento ME, Mascaró M, Abba MC, Coló GP, Arévalo J, Ferronato MJ, Guevara JA, Núñez M, et al: Heme oxygenase-1 has an antitumor role in breast cancer. Antioxid Redox Signal. 30:2030–2049. 2019. View Article : Google Scholar : PubMed/NCBI | |
Converso DP, Taillé C, Carreras MC, Jaitovich A, Poderoso JJ and Boczkowski J: HO-1 is located in liver mitochondria and modulates mitochondrial heme content and metabolism. FASEB J. 20:1236–1238. 2006. View Article : Google Scholar : PubMed/NCBI | |
Matsushima M, Nose H, Tsuzuki H, Takekoshi M, Kusatsugu Y, Taniguchi H, Ohdachi T, Hashimoto N, Sato M and Kawabe T: Decrease in cholesterol in the cell membrane is essential for Nrf2 activation by quercetin. J Nutr Biochem. 116:1093292023. View Article : Google Scholar : PubMed/NCBI | |
Fahrer J, Wittmann S, Wolf AC and Kostka T: Heme oxygenase-1 and its role in colorectal cancer. Antioxidants (Basel). 12:19892023. View Article : Google Scholar : PubMed/NCBI | |
Nitti M, Piras S, Marinari UM, Moretta L, Pronzato MA and Furfaro AL: HO-1 induction in cancer progression: A matter of cell adaptation. Antioxidants (Basel). 6:292017. View Article : Google Scholar : PubMed/NCBI | |
Jagadeesh ASV, Fang X, Kim SH, Guillen-Quispe YN, Zheng J, Surh YJ and Kim SJ: Non-canonical vs canonical functions of heme oxygenase-1 in cancer. J Cancer Prev. 27:7–15. 2022. View Article : Google Scholar : PubMed/NCBI | |
Gao Y, Wan L, Li M, Wang B and Ma Y: NRF2/HO-1 axis, BIRC5, and TP53 expression in ESCC and its correlation with clinical pathological characteristics and prognosis. Int J Biol Markers. 38:174–184. 2023. View Article : Google Scholar : PubMed/NCBI | |
Dennery PA: Heme oxygenase in neonatal lung injury and repair. Antioxid Redox Signal. 21:1881–1892. 2014. View Article : Google Scholar : PubMed/NCBI | |
Loboda A, Damulewicz M, Pyza E, Jozkowicz A and Dulak J: Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: An evolutionarily conserved mechanism. Cell Mol Life Sci. 73:3221–3247. 2016. View Article : Google Scholar : PubMed/NCBI | |
Tossetta G and Marzioni D: Natural and synthetic compounds in ovarian cancer: A focus on NRF2/KEAP1 pathway. Pharmacol Res. 183:1063652022. View Article : Google Scholar : PubMed/NCBI | |
Rejhová A, Opattová A, Čumová A, Slíva D and Vodička P: Natural compounds and combination therapy in colorectal cancer treatment. Eur J Med Chem. 144:582–594. 2018. View Article : Google Scholar : PubMed/NCBI | |
Wang H, Guo S, Kim SJ, Shao F, Ho JWK, Wong KU, Miao Z, Hao D, Zhao M, Xu J, et al: Cisplatin prevents breast cancer metastasis through blocking early EMT and retards cancer growth together with paclitaxel. Theranostics. 11:2442–2459. 2021. View Article : Google Scholar : PubMed/NCBI | |
Lang W, Zhang J, Xiao X, Cheng M, Zheng X, Gong H, Ali I, Zhao Y, Jia F, Wang Z, et al: Forsythiaside A ameliorates inflammation by regulating the autophagy in methotrexate-induced intestinal mucositis. Comb Chem High Throughput Screen. January 29–2025.(Epub ahead of print). View Article : Google Scholar : PubMed/NCBI | |
Green DR: The coming decade of cell death research: Five riddles. Cell. 177:1094–1107. 2019. View Article : Google Scholar : PubMed/NCBI | |
Bedoui S, Herold MJ and Strasser A: Emerging connectivity of programmed cell death pathways and its physiological implications. Nat Rev Mol Cell Biol. 21:678–695. 2020. View Article : Google Scholar : PubMed/NCBI | |
Sun Z, Ding C, Wang Y, Lu T and Song W: Plasma-activated medium inhibited the proliferation and migration of non-small cell lung cancer A549 cells in 3D culture. Int J Mol Sci. 25:132622024. View Article : Google Scholar : PubMed/NCBI | |
Wang C, You Z, Zhou G, Dong J, Tong S and Sun G: Amarogentin suppresses cell proliferation and EMT process through inducing ferroptosis in colorectal cancer. BMC Gastroenterol. 25:462025. View Article : Google Scholar : PubMed/NCBI | |
Kerr JF, Wyllie AH and Currie AR: Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 26:239–257. 1972. View Article : Google Scholar : PubMed/NCBI | |
Galluzzi L, Vitale I, Aaronson SA, Abrams JM, Adam D, Agostinis P, Alnemri ES, Altucci L, Amelio I, Andrews DW, et al: Molecular mechanisms of cell death: Recommendations of the nomenclature committee on cell death 2018. Cell Death Differ. 25:486–541. 2018. View Article : Google Scholar : PubMed/NCBI | |
Sharma P, Sharma V, Ahluwalia TS, Dogra N, Kumar S and Singh S: Let-7a induces metabolic reprogramming in breast cancer cells via targeting mitochondrial encoded ND4. Cancer Cell Int. 21:6292021. View Article : Google Scholar : PubMed/NCBI | |
Nagata S: Apoptosis and clearance of apoptotic cells. Annu Rev Immunol. 36:489–517. 2018. View Article : Google Scholar : PubMed/NCBI | |
Panda PK, Paschoalini Mafra AC, Bastos ACS, Cao L, Serra Bonet M, Brashears CB, Chen EY, Benedict-Hamilton HM, Ehrhardt W, Bomalaski J, et al: Bcl-Xl protects ASS1-deficient cancers from arginine starvation induced apoptosis. Clin Cancer Res. February 3–2025.(Epub ahead of print). View Article : Google Scholar : PubMed/NCBI | |
Gu Z, Deng M, Luo Q, Lin S, Yu J, Li C, Wang X, Chen L, Liu T, Li Y and He B: Harnessing HDAC-targeted oleanolic acid derivatives for combined anti-cancer and hepatoprotective effects. Int J Biol Macromol. 297:1397612025.(Epub ahead of print). View Article : Google Scholar : PubMed/NCBI | |
Chen Y, Liu X, Chen B, Zhu F, Wang Z, Cheong KL, Ye S, Zhong S and Chen J: Selenium nanoparticles decorated by fucoidan induce ferroptosis in HepG2 cells. Int J Biol Macromol. 289:1388412025. View Article : Google Scholar : PubMed/NCBI | |
Chen YT, Lin CW, Su CW, Yang WE, Chuang CY, Su SC, Hsieh MJ and Yang SF: Magnolol triggers caspase-mediated apoptotic cell death in human oral cancer cells through JNK1/2 and p38 pathways. Biomedicines. 9:12952021. View Article : Google Scholar : PubMed/NCBI | |
Hsieh MJ, Lin CC, Lo YS, Chuang YC, Ho HY and Chen MK: Chrysosplenol D triggers apoptosis through heme oxygenase-1 and mitogen-activated protein kinase signaling in oral squamous cell carcinoma. Cancers (Basel). 13:43272021. View Article : Google Scholar : PubMed/NCBI | |
Ho HY, Chen PJ, Chuang YC, Lo YS, Lin CC, Hsieh MJ and Chen MK: Picrasidine I triggers heme oxygenase-1-induced apoptosis in nasopharyngeal carcinoma cells via ERK and Akt signaling pathways. Int J Mol Sci. 23:61032022. View Article : Google Scholar : PubMed/NCBI | |
Su SC, Chen YT, Hsieh YH, Yang WE, Su CW, Chiu WY, Yang SF and Lin CW: Gambogic acid induces HO-1 expression and cell apoptosis through p38 signaling in oral squamous cell carcinoma. Am J Chin Med. 50:1663–1679. 2022. View Article : Google Scholar : PubMed/NCBI | |
DiMarco-Crook C, Rakariyatham K, Li Z, Du Z, Zheng J, Wu X and Xiao H: Synergistic anticancer effects of curcumin and 3′,4′-didemethylnobiletin in combination on colon cancer cells. J Food Sci. 85:1292–1301. 2020. View Article : Google Scholar : PubMed/NCBI | |
Elsherbiny NM, Eisa NH, El-Sherbiny M and Said E: Chemo-preventive effect of crocin against experimentally-induced hepatocarcinogenesis via regulation of apoptotic and Nrf2 signaling pathways. Environ Toxicol Pharmacol. 80:1034942020. View Article : Google Scholar : PubMed/NCBI | |
Chuang CY, Lin CW, Su CW, Chen YT, Yang WE, Yang SF and Su SC: Deoxyshikonin mediates heme oxygenase-1 induction and apoptotic response via p38 signaling in tongue cancer cell lines. Int J Mol Sci. 23:71152022. View Article : Google Scholar : PubMed/NCBI | |
Zhao X, Dong W, Gao Y, Shin DS, Ye Q, Su L, Jiang F, Zhao B and Miao J: Novel indolyl-chalcone derivatives inhibit A549 lung cancer cell growth through activating Nrf-2/HO-1 and inducing apoptosis in vitro and in vivo. Sci Rep. 7:39192017. View Article : Google Scholar : PubMed/NCBI | |
Sui X, Gao B and Zhang L, Wang Y, Ma J, Wu X, Zhou C, Liu M and Zhang L: Scutellaria barbata D.Don and Hedyotis diffusa Willd herb pair combined with cisplatin synergistically inhibits ovarian cancer progression through modulating oxidative stress via NRF2-FTH1 autophagic degradation pathway. J Ovarian Res. 17:2462024. View Article : Google Scholar : PubMed/NCBI | |
Chien MH, Yang WE, Yang YC, Ku CC, Lee WJ, Tsai MY, Lin CW and Yang SF: Dual targeting of the p38 MAPK-HO-1 axis and cIAP1/XIAP by demethoxycurcumin triggers caspase-mediated apoptotic cell death in oral squamous cell carcinoma cells. Cancers (Basel). 12:7032020. View Article : Google Scholar : PubMed/NCBI | |
Su CW, Chuang CY, Chen YT, Yang WE, Pan YP, Lin CW and Yang SF: FLLL32 triggers caspase-mediated apoptotic cell death in human oral cancer cells by regulating the p38 pathway. Int J Mol Sci. 22:118602021. View Article : Google Scholar : PubMed/NCBI | |
Harmse L, Gangat N, Martins-Furness C, Dam J and de Koning CB: Copper-imidazo[1,2-a]pyridines induce intrinsic apoptosis and modulate the expression of mutated p53, haem-oxygenase-1 and apoptotic inhibitory proteins in HT-29 colorectal cancer cells. Apoptosis. 24:623–643. 2019. View Article : Google Scholar : PubMed/NCBI | |
Acquaviva R, Tomasello B, Di Giacomo C, Santangelo R, La Mantia A, Naletova I, Sarpietro M.G, Castelli F and Malfa GA: Protocatechuic acid, a simple plant secondary metabolite, induced apoptosis by promoting oxidative stress through HO-1 downregulation and p21 upregulation in colon cancer cells. Biomolecules. 11:14852021. View Article : Google Scholar : PubMed/NCBI | |
Yang IH, Ahn CH, Cho NP, Jin B, Lee W, Jung YC, Hong SD, Shin JA and Cho SD: Heme oxygenase-1 is a key molecule underlying differential response of TW-37-induced apoptosis in human mucoepidermoid carcinoma cells. Molecules. 24:17002019. View Article : Google Scholar : PubMed/NCBI | |
Guo Y, Fang Q, Ma D, Yu K, Cheng B, Tang S, Lu T, Wang W and Wang J: Up-regulation of HO-1 promotes resistance of B-cell acute lymphocytic leukemia cells to HDAC4/5 inhibitor LMK-235 via the Smad7 pathway. Life Sci. 207:386–394. 2018. View Article : Google Scholar : PubMed/NCBI | |
Li X, Guo Y, Kuang X, Zhao L, Li H, Cheng B, Wang W, Zhang Z, Liu P and Wang J: Histone deacetylase inhibitor LMK-235-mediated HO-1 expression induces apoptosis in multiple myeloma cells via the JNK/AP-1 signaling pathway. Life Sci. 223:146–157. 2019. View Article : Google Scholar : PubMed/NCBI | |
Jia XB, Zhang Q, Xu L, Yao WJ and Wei L: Lotus leaf flavonoids induce apoptosis of human lung cancer A549 cells through the ROS/p38 MAPK pathway. Biol Res. 54:72021. View Article : Google Scholar : PubMed/NCBI | |
Yan S, Yue Y, Wang J, Li W, Sun M, Zeng L and Wang X: Banxia Xiexin decoction, a traditional Chinese medicine, alleviates colon cancer in nude mice. Ann Transl Med. 7:3752019. View Article : Google Scholar : PubMed/NCBI | |
Sun X, Li J, Li Y, Wang S and Li Q: Apatinib, a novel tyrosine kinase inhibitor, promotes ROS-dependent apoptosis and autophagy via the Nrf2/HO-1 pathway in ovarian cancer cells. Oxid Med Cell Longev. 2020:31451822020. View Article : Google Scholar : PubMed/NCBI | |
Li J, Xiong C, Xu P, Luo Q and Zhang R: Puerarin induces apoptosis in prostate cancer cells via inactivation of the Keap1/Nrf2/ARE signaling pathway. Bioengineered. 12:402–413. 2021. View Article : Google Scholar : PubMed/NCBI | |
Li X, Mu J, Lin Y, Zhao J and Meng X: Combination of cyanidin-3-O-glucoside and cisplatin induces oxidative stress and apoptosis in HeLa cells by reducing activity of endogenous antioxidants, increasing bax/bcl-2 mRNA expression ratio, and downregulating Nrf2 expression. J Food Biochem. 45:e138062021. View Article : Google Scholar : PubMed/NCBI | |
Yang Y, Tian Z, Guo R and Ren F: Nrf2 inhibitor, brusatol in combination with trastuzumab exerts synergistic antitumor activity in HER2-positive cancers by inhibiting Nrf2/HO-1 and HER2-AKT/ERK1/2 pathways. Oxid Med Cell Longev. 2020:98675952020. View Article : Google Scholar : PubMed/NCBI | |
Mondal P, Natesh J, Penta D and Meeran SM: Extract of Murraya koenigii selectively causes genomic instability by altering redox-status via targeting PI3K/AKT/Nrf2/caspase-3 signaling pathway in human non-small cell lung cancer. Phytomedicine. 104:1542722022. View Article : Google Scholar : PubMed/NCBI | |
Kuang X, Xiong J, Wang W, Li X, Lu T, Fang Q and Wang J: PIM inhibitor SMI-4a induces cell apoptosis in B-cell acute lymphocytic leukemia cells via the HO-1-mediated JAK2/STAT3 pathway. Life Sci. 219:248–256. 2019. View Article : Google Scholar : PubMed/NCBI | |
Zhou Z, Fang Q, Li P, Ma D, Zhe N, Ren M, Chen B, He Z and Wang J, Zhong Q and Wang J: Entinostat combined with fludarabine synergistically enhances the induction of apoptosis in TP53 mutated CLL cells via the HDAC1/HO-1 pathway. Life Sci. 232:1165832019. View Article : Google Scholar : PubMed/NCBI | |
Wang LH, Li Y, Yang SN, Wang FY, Hou Y, Cui W, Chen K, Cao Q, Wang S, Zhang TY, et al: Gambogic acid synergistically potentiates cisplatin-induced apoptosis in non-small-cell lung cancer through suppressing NF-κB and MAPK/HO-1 signalling. Br J Cancer. 110:341–352. 2014. View Article : Google Scholar : PubMed/NCBI | |
Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM, Gleason CE, Patel DN, Bauer AJ, Cantley AM, Yang WS, et al: Ferroptosis: An iron-dependent form of nonapoptotic cell death. Cell. 149:1060–1072. 2012. View Article : Google Scholar : PubMed/NCBI | |
Qi YL, Wang HR, Chen LL, Duan YT, Yang SY and Zhu HL: Recent advances in small-molecule fluorescent probes for studying ferroptosis. Chem Soc Rev. 51:7752–7778. 2022. View Article : Google Scholar : PubMed/NCBI | |
Imai H, Matsuoka M, Kumagai T, Sakamoto T and Koumura T: Lipid peroxidation-dependent cell death regulated by GPx4 and ferroptosis. Curr Top Microbiol Immunol. 403:143–170. 2017.PubMed/NCBI | |
Hou W, Xie Y, Song X, Sun X, Lotze MT, Zeh HJ III, Kang R and Tang D: Autophagy promotes ferroptosis by degradation of ferritin. Autophagy. 12:1425–1428. 2016. View Article : Google Scholar : PubMed/NCBI | |
Wen SY, Gao RR, Chen YY, Wang YJ, Wang XT and Liu HX: Brassinin from Brassica campestris L. inhibits colorectal cancer by inducing p62/NRF2/GPX4-regulated ferroptosis. Animal Model Exp Med. Jan 23–2025.(Epub ahead of print). View Article : Google Scholar | |
Liu J, Zhou S, Chen J, Lin H, Li Y, Zhang X, Chen S, Lv X and Zhao H: Nrf2 inhibition and NCOA4-mediated ferritinophagy activation synergistically exacerbated S-3′-hydroxy-7′,2′, 4′-trimethoxyisoxane induced ferroptosis in lung cancer cells. Chem Biol Interact. 406:1113532025. View Article : Google Scholar : PubMed/NCBI | |
Zhang JJ, Ni P, Song Y, Gao MJ, Guo XY and Zhao BQ: Effective protective mechanisms of HO-1 in diabetic complications: A narrative review. Cell Death Discov. 10:4332024. View Article : Google Scholar : PubMed/NCBI | |
Zhang Y and Xie J: Targeting ferroptosis regulators by natural products in colorectal cancer. Front Pharmacol. 15:13747222024. View Article : Google Scholar : PubMed/NCBI | |
Chen L, Shen Q, Liu Y, Zhang Y, Sun L, Ma X, Song N and Xie J: Homeostasis and metabolism of iron and other metal ions in neurodegenerative diseases. Signal Transduct Target Ther. 10:312025. View Article : Google Scholar : PubMed/NCBI | |
Malfa GA, Tomasello B, Acquaviva R, Genovese C, La Mantia A, Cammarata FP, Ragusa M, Renis M and Di Giacomo C: Betula etnensis Raf. (Betulaceae) extract induced HO-1 expression and ferroptosis cell death in human colon cancer cells. Int J Mol Sci. 20:27232019. View Article : Google Scholar : PubMed/NCBI | |
Lin H, Chen X, Zhang C, Yang T, Deng Z, Song Y, Huang L, Li F, Li Q, Lin S and Jin D: EF24 induces ferroptosis in osteosarcoma cells through HMOX1. Biomed Pharmacother. 136:1112022021. View Article : Google Scholar : PubMed/NCBI | |
Li R, Zhang J, Zhou Y, Gao Q, Wang R, Fu Y, Zheng L and Yu H: Transcriptome investigation and in vitro verification of curcumin-induced HO-1 as a feature of ferroptosis in breast cancer cells. Oxid Med Cell Longev. 2020:34698402020. View Article : Google Scholar : PubMed/NCBI | |
Han S, Lin F, Qi Y, Liu C, Zhou L, Xia Y, Chen K, Xing J, Liu Z, Yu W, et al: HO-1 contributes to luteolin-triggered ferroptosis in clear cell renal cell carcinoma via increasing the labile iron pool and promoting lipid peroxidation. Oxid Med Cell Longev. 2022:38462172022. View Article : Google Scholar : PubMed/NCBI | |
Zhang Y, Zhang H, Mu J, Han M, Cao Z, Dong F, Wang T, Pan L, Luo W, Li J, et al: Eupalinolide B inhibits hepatic carcinoma by inducing ferroptosis and ROS-ER-JNK pathway. Acta Biochim Biophys Sin (Shanghai). 54:974–986. 2022. View Article : Google Scholar : PubMed/NCBI | |
Lai X, Sun Y, Zhang X, Wang D, Wang J, Wang H, Zhao Y, Liu X, Xu X, Song H, et al: Honokiol induces ferroptosis by upregulating HMOX1 in acute myeloid leukemia cells. Front Pharmacol. 13:8977912022. View Article : Google Scholar : PubMed/NCBI | |
He X, Yao Q, Fan D, Duan L, You Y, Liang W, Zhou Z, Teng S, Liang Z, Hall DD, et al: Cephalosporin antibiotics specifically and selectively target nasopharyngeal carcinoma through HMOX1-induced ferroptosis. Life Sci. 277:1194572021. View Article : Google Scholar : PubMed/NCBI | |
Feng C, Wu Y, Chen Y, Xiong X, Li P, Peng X, Li C, Weng W, Zhu Y, Zhou D and Li Y: Arsenic trioxide increases apoptosis of SK-N-BE (2) cells partially by inducing GPX4-mediated ferroptosis. Mol Biol Rep. 49:6573–6580. 2022. View Article : Google Scholar : PubMed/NCBI | |
Chen P, Li X, Zhang R, Liu S, Xiang Y, Zhang M, Chen X, Pan T, Yan L, Feng J, et al: Combinative treatment of β-elemene and cetuximab is sensitive to KRAS mutant colorectal cancer cells by inducing ferroptosis and inhibiting epithelial-mesenchymal transformation. Theranostics. 10:5107–5119. 2020. View Article : Google Scholar : PubMed/NCBI | |
Du J, Wang L, Huang X, Zhang N, Long Z, Yang Y, Zhong F, Zheng B, Lan W, Lin W and Ma W: Shuganning injection, a traditional Chinese patent medicine, induces ferroptosis and suppresses tumor growth in triple-negative breast cancer cells. Phytomedicine. 85:1535512021. View Article : Google Scholar : PubMed/NCBI | |
Xiaohu O, Wang J, Qiu X, Song S, Li J, Luo S, Chen Q and Hu D: Sophora alopecuroide-Taraxacum decoction (STD) inhibits non-small cell lung cancer via inducing ferroptosis and modulating tumor immune microenvironment. Heliyon. 10:e395642024. View Article : Google Scholar : PubMed/NCBI | |
Wei R, Zhao Y, Wang J, Yang X, Li S, Wang Y, Yang X, Fei J, Hao X, Zhao Y, et al: Tagitinin C induces ferroptosis through PERK-Nrf2-HO-1 signaling pathway in colorectal cancer cells. Int J Biol Sci. 17:2703–2717. 2021. View Article : Google Scholar : PubMed/NCBI | |
Shi H, Hou B, Li H, Zhou H and Du B: Cyclophosphamide induces the ferroptosis of tumor cells through heme oxygenase-1. Front Pharmacol. 13:8394642022. View Article : Google Scholar : PubMed/NCBI | |
Guan D, Zhou W, Wei H, Wang T, Zheng K, Yang C, Feng R, Xu R, Fu Y, Li C, et al: Ferritinophagy-mediated ferroptosis and activation of keap1/Nrf2/HO-1 pathway were conducive to emt inhibition of gastric cancer cells in action of 2,2′-di-pyridineketone hydrazone dithiocarbamate butyric acid ester. Oxid Med Cell Longev. 2022:39206642022. View Article : Google Scholar : PubMed/NCBI | |
Villalpando-Rodriguez GE, Blankstein AR, Konzelman C and Gibson SB: Lysosomal destabilizing drug siramesine and the dual tyrosine kinase inhibitor lapatinib induce a synergistic ferroptosis through reduced heme oxygenase-1 (HO-1) levels. Oxid Med Cell Longev. 2019:95612812019. View Article : Google Scholar : PubMed/NCBI | |
Cui Z, Wang H, Li S, Qin T, Shi H, Ma J, Li L, Yu G, Jiang T and Li C: Dihydroartemisinin enhances the inhibitory effect of sorafenib on HepG2 cells by inducing ferroptosis and inhibiting energy metabolism. J Pharmacol Sci. 148:73–85. 2022. View Article : Google Scholar : PubMed/NCBI | |
Lou JS, Zhao LP, Huang ZH, Chen XY, Xu JT, Tai WC, Tsim KWK, Chen YT and Xie T: Ginkgetin derived from Ginkgo biloba leaves enhances the therapeutic effect of cisplatin via ferroptosis-mediated disruption of the Nrf2/HO-1 axis in EGFR wild-type non-small-cell lung cancer. Phytomedicine. 80:1533702021. View Article : Google Scholar : PubMed/NCBI | |
Li S, Zhang Y, Zhang J, Yu B, Wang W, Jia B, Chang J and Liu J: Neferine exerts ferroptosis-inducing effect and antitumor effect on thyroid cancer through Nrf2/HO-1/NQO1 inhibition. J Oncol. 2022:79337752022.PubMed/NCBI | |
Chen J, Zhou S, Zhang X and Zhao H: S-3′-hydroxy-7′, 2′, 4′-trimethoxyisoxane, a novel ferroptosis inducer, promotes NSCLC cell death through inhibiting Nrf2/HO-1 signaling pathway. Front Pharmacol. 13:9736112022. View Article : Google Scholar : PubMed/NCBI | |
Jing T, Guo Y and Wei Y: Carboxymethylated pachyman induces ferroptosis in ovarian cancer by suppressing NRF1/HO-1 signaling. Oncol Lett. 23:1612022. View Article : Google Scholar : PubMed/NCBI | |
Zhu X, Chen X, Qiu L, Zhu J and Wang J: Norcantharidin induces ferroptosis via the suppression of NRF2/HO-1 signaling in ovarian cancer cells. Oncol Lett. 24:3592022. View Article : Google Scholar : PubMed/NCBI | |
Han L, Li L and Wu G: Induction of ferroptosis by carnosic acid-mediated inactivation of Nrf2/HO-1 potentiates cisplatin responsiveness in OSCC cells. Mol Cell Probes. 64:1018212022. View Article : Google Scholar : PubMed/NCBI | |
Zychlinsky A, Prevost MC and Sansonetti PJ: Shigella flexneri induces apoptosis in infected macrophages. Nature. 358:167–169. 1992. View Article : Google Scholar : PubMed/NCBI | |
D'Souza CA and Heitman J: Dismantling the cryptococcus coat. Trends Microbiol. 9:112–113. 2001. View Article : Google Scholar : PubMed/NCBI | |
Wang X, He S, Cheng P and Pu K: A dual-locked tandem fluorescent probe for imaging of pyroptosis in cancer chemo-immunotherapy. Adv Mater. 35:e22065102023. View Article : Google Scholar : PubMed/NCBI | |
Jorgensen I and Miao EA: Pyroptotic cell death defends against intracellular pathogens. Immunol Rev. 265:130–142. 2015. View Article : Google Scholar : PubMed/NCBI | |
Yu P, Zhang X, Liu N, Tang L, Peng C and Chen X: Pyroptosis: Mechanisms and diseases. Signal Transduct Target Ther. 6:1282021. View Article : Google Scholar : PubMed/NCBI | |
Zhendong Y, Changjun C, Haocheng H, Qibin L, Dailing C, Linsong T, Xuecheng S, Gong M and Lei Z: Regulation of macrophage polarization and pyroptosis by 4-methylcatechol alleviates collagen-induced arthritis via Nrf2/HO-1 and NF-κB/NLRP3 signaling pathways. Int Immunopharmacol. 146:1138552025. View Article : Google Scholar : PubMed/NCBI | |
Ghaith WZ, Wadie W and El-Yamany MF: Crosstalk between SIRT1/Nrf2 signaling and NLRP3 inflammasome/pyroptosis as a mechanistic approach for the neuroprotective effect of linagliptin in Parkinson's disease. Int Immunopharmacol. 145:1137162025. View Article : Google Scholar : PubMed/NCBI | |
Okasha AH, Hegab II, Seleem MA, Azzam AR, Ibrahim S, Ghalwash AA and El-Gohary RM: Effects of Fisetin and Nicorandil on adjuvant-induced rheumatoid arthritis in rats: Emerging role of TLR4/NF-κB-induced pyroptosis, Nrf-2/HO-1, and OPG/RANKL pathways. Cytokine. 187:1568762025. View Article : Google Scholar : PubMed/NCBI | |
Wayal V, Wang SD and Hsieh CC: Novel bioactive peptides alleviate western diet-induced MAFLD in C57BL/6J mice by inhibiting NLRP3 inflammasome activation and pyroptosis via TLR4/NF-κB and Keap1/Nrf2/HO-1 signaling pathways. Int Immunopharmacol. 148:1141772025. View Article : Google Scholar : PubMed/NCBI | |
Hong C, Wang L, Zhou X, Zou L, Xiang X, Deng H, Li Q, Wu Y, Liu L and Li T: Protective effects of mdivi-1 on cognition disturbance following sepsis in mice via alleviating microglia activation and polarization. CNS Neurosci Ther. 31:e701492025. View Article : Google Scholar : PubMed/NCBI | |
Shi H, Qiao F, Lu W, Huang K, Wen Y, Ye L and Chen Y: Baicalin improved hepatic injury of NASH by regulating NRF2/HO-1/NRLP3 pathway. Eur J Pharmacol. 934:1752702022. View Article : Google Scholar : PubMed/NCBI | |
Zhang B, Wan S, Liu H, Qiu Q, Chen H, Chen Z, Wang L and Liu X: Naringenin alleviates renal ischemia reperfusion injury by suppressing ER stress-induced pyroptosis and apoptosis through activating Nrf2/HO-1 signaling pathway. Oxid Med Cell Longev. 2022:59924362022. View Article : Google Scholar : PubMed/NCBI | |
Yan Z, Qi W, Zhan J, Lin Z, Lin J, Xue X, Pan X and Zhou Y: Activating Nrf2 signalling alleviates osteoarthritis development by inhibiting inflammasome activation. J Cell Mol Med. 24:13046–13057. 2020. View Article : Google Scholar : PubMed/NCBI | |
Liu Y, Zhou J, Luo Y, Li J, Shang L, Zhou F and Yang S: Honokiol alleviates LPS-induced acute lung injury by inhibiting NLRP3 inflammasome-mediated pyroptosis via Nrf2 activation in vitro and in vivo. Chin Med. 16:1272021. View Article : Google Scholar : PubMed/NCBI | |
Levine B and Kroemer G: Autophagy in the pathogenesis of disease. Cell. 132:27–42. 2008. View Article : Google Scholar : PubMed/NCBI | |
Kroemer G, Marino G and Levine B: Autophagy and the integrated stress response. Mol Cell. 40:280–293. 2010. View Article : Google Scholar : PubMed/NCBI | |
Mizushima N and Komatsu M: Autophagy: Renovation of cells and tissues. Cell. 147:728–741. 2011. View Article : Google Scholar : PubMed/NCBI | |
Nam HJ: Autophagy modulators in cancer: Focus on cancer treatment. Life (Basel). 11:8392021.PubMed/NCBI | |
Fleming A, Noda T, Yoshimori T and Rubinsztein DC: Chemical modulators of autophagy as biological probes and potential therapeutics. Nat Chem Biol. 7:9–17. 2011. View Article : Google Scholar : PubMed/NCBI | |
Xu Y and Wan W: Acetylation in the regulation of autophagy. Autophagy. 19:379–387. 2023. View Article : Google Scholar : PubMed/NCBI | |
Sun Y, Xu M, Duan Q, Bryant JL and Xu X: The role of autophagy in the progression of HIV infected cardiomyopathy. Front Cell Dev Biol. 12:13725732024. View Article : Google Scholar : PubMed/NCBI | |
Satarker S, Wilson J, Kolathur KK, Mudgal J, Lewis SA, Arora D and Nampoothiri M: Spermidine as an epigenetic regulator of autophagy in neurodegenerative disorders. Eur J Pharmacol. 979:1768232024. View Article : Google Scholar : PubMed/NCBI | |
Meyer N, Zielke S, Michaelis JB, Linder B, Warnsmann V, Rakel S, Osiewacz HD, Fulda S, Mittelbronn M, Münch C, et al: AT 101 induces early mitochondrial dysfunction and HMOX1 (heme oxygenase 1) to trigger mitophagic cell death in glioma cells. Autophagy. 14:1693–1709. 2018. View Article : Google Scholar : PubMed/NCBI | |
So KY, Kim SH, Jung KT, Lee HY and Oh SH: MAPK/JNK1 activation protects cells against cadmium-induced autophagic cell death via differential regulation of catalase and heme oxygenase-1 in oral cancer cells. Toxicol Appl Pharmacol. 332:81–91. 2017. View Article : Google Scholar : PubMed/NCBI | |
Shi Y, Zhang B, Feng X, Qu F, Wang S, Wu L, Wang X, Liu Q, Wang P and Zhang K: Apoptosis and autophagy induced by DVDMs-PDT on human esophageal cancer Eca-109 cells. Photodiagnosis Photodyn Ther. 24:198–205. 2018. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Zhang J, Huang ZH, Huang XH, Zheng WB, Yin XF, Li YL, Li B and He QY: Isodeoxyelephantopin induces protective autophagy in lung cancer cells via Nrf2-p62-keap1 feedback loop. Cell Death Dis. 8:e28762017. View Article : Google Scholar : PubMed/NCBI | |
Tan Q, Wang H, Hu Y, Hu M, Li X, Aodengqimuge Ma Y, Wei C and Song L: Src/STAT3-dependent heme oxygenase-1 induction mediates chemoresistance of breast cancer cells to doxorubicin by promoting autophagy. Cancer Sci. 106:1023–1032. 2015. View Article : Google Scholar : PubMed/NCBI | |
Galluzzi L, Kepp O, Chan FK and Kroemer G: Necroptosis: Mechanisms and relevance to disease. Annu Rev Pathol. 12:103–130. 2017. View Article : Google Scholar : PubMed/NCBI | |
Wu X, Gu R, Tang M, Mu X, He W and Nie X: Elucidating the dual roles of apoptosis and necroptosis in diabetic wound healing: Implications for therapeutic intervention. Burns Trauma. 13:tkae0612025. View Article : Google Scholar : PubMed/NCBI | |
Tonnus W, Meyer C, Paliege A, Belavgeni A, von Mässenhausen A, Bornstein SR, Hugo C, Becker JU and Linkermann A: The pathological features of regulated necrosis. J Pathol. 247:697–707. 2019. View Article : Google Scholar : PubMed/NCBI | |
Orozco S and Oberst A: RIPK3 in cell death and inflammation: The good, the bad, and the ugly. Immunol Rev. 277:102–112. 2017. View Article : Google Scholar : PubMed/NCBI | |
Chen J, Kos R, Garssen J and Redegeld F: Molecular insights into the mechanism of necroptosis: The necrosome as a potential therapeutic target. Cells. 8:14862019. View Article : Google Scholar : PubMed/NCBI | |
Zhang T, Shen Y, Zhu R, Shan W, Li Y, Yan M and Zhang Y: Benzo[a]pyrene exposure promotes RIP1-mediated necroptotic death of osteocytes and the JNK/IL-18 pathway activation via generation of reactive oxygen species. Toxicology. 476:1532442022. View Article : Google Scholar : PubMed/NCBI | |
Huang HJ, Wang HT, Yeh TY, Lin BW, Shiao YJ, Lo YL and Lin AMY: Neuroprotective effect of selumetinib on acrolein-induced neurotoxicity. Sci Rep. 11:124972021. View Article : Google Scholar : PubMed/NCBI | |
Luo A and Chen Y: Label-free interactome analysis revealed an essential role of CUL3-KEAP1 complex in mediating the ubiquitination and degradation of PHD2. J Proteome Res. 19:260–268. 2020. View Article : Google Scholar : PubMed/NCBI | |
Chen D, Wu YX, Qiu YB, Wan BB, Liu G, Chen JL, Lu MD and Pang QF: Hyperoside suppresses hypoxia-induced A549 survival and proliferation through ferrous accumulation via AMPK/HO-1 axis. Phytomedicine. 67:1531382020. View Article : Google Scholar : PubMed/NCBI | |
Romeo G, Ciaffaglione V, Amata E, Dichiara M, Calabrese L, Vanella L, Sorrenti V, Grosso S, D'Amico AG, D'Agata V, et al: Combination of heme oxygenase-1 inhibition and sigma receptor modulation for anticancer activity. Molecules. 26:38602021. View Article : Google Scholar : PubMed/NCBI | |
Ghimire K, Awasthi BP, Yadav K, Lee J, Kim H, Jeong BS and Kim JA: Prostate cancer-selective anticancer action of an oxindole derivative via HO-1-mediated disruption of metabolic reprogramming. Chem Biol Interact. 408:1113932025.(Epub ahead of print). View Article : Google Scholar : PubMed/NCBI | |
Castruccio Castracani C, Longhitano L, Distefano A, Di Rosa M, Pittalà V, Lupo G, Caruso M, Corona D, Tibullo D and Li Volti G: Heme Oxygenase-1 and carbon monoxide regulate growth and progression in glioblastoma cells. Mol Neurobiol. 57:2436–2446. 2020. View Article : Google Scholar : PubMed/NCBI | |
Sorrenti V, D'Amico AG, Barbagallo I, Consoli V, Grosso S and Vanella L: Tin mesoporphyrin selectively reduces non-small-cell lung cancer cell line a549 proliferation by interfering with heme oxygenase and glutathione systems. Biomolecules. 11:9172021. View Article : Google Scholar : PubMed/NCBI | |
Zhao Y, Xiao W, Peng W, Huang Q, Wu K, Evans CE, Liu X and Jin H: Oridonin-loaded nanoparticles inhibit breast cancer progression through regulation of ROS-related Nrf2 signaling pathway. Front Bioeng Biotechnol. 9:6005792021. View Article : Google Scholar : PubMed/NCBI | |
Talmadge JE and Fidler IJ: AACR centennial series: The biology of cancer metastasis: historical perspective. Cancer Res. 70:5649–5669. 2010. View Article : Google Scholar : PubMed/NCBI | |
Wirtz D, Konstantopoulos K and Searson PC: The physics of cancer: The role of physical interactions and mechanical forces in metastasis. Nat Rev Cancer. 11:512–522. 2011. View Article : Google Scholar : PubMed/NCBI | |
Luu Hoang KN, Anstee JE and Arnold JN: The diverse roles of heme oxygenase-1 in tumor progression. Front Immunol. 12:6583152021. View Article : Google Scholar : PubMed/NCBI | |
SenGupta S, Parent CA and Bear JE: The principles of directed cell migration. Nat Rev Mol Cell Biol. 22:529–547. 2021. View Article : Google Scholar : PubMed/NCBI | |
Lavoie H, Gagnon J and Therrien M: ERK signalling: A master regulator of cell behaviour, life and fate. Nat Rev Mol Cell Biol. 21:607–632. 2020. View Article : Google Scholar : PubMed/NCBI | |
Samson SC, Khan AM and Mendoza MC: ERK signaling for cell migration and invasion. Front Mol Biosci. 9:9984752022. View Article : Google Scholar : PubMed/NCBI | |
Wattanathamsan O and Pongrakhananon V: Emerging role of microtubule-associated proteins on cancer metastasis. Front Pharmacol. 13:9354932022. View Article : Google Scholar : PubMed/NCBI | |
Bonner K and Quick QA: Microtubule actin crosslinking factor 1, a brain tumor oncoprotein (Review). Mol Clin Oncol. 22:152024. View Article : Google Scholar : PubMed/NCBI | |
Li R, Zeng X, Yang M, Xu X, Feng J, Bao L, Xue B, Wang X and Huang Y: Antidiabetic agent DPP-4i facilitates murine breast cancer metastasis by oncogenic ROS-NRF2-HO-1 axis via a positive NRF2-HO-1 feedback loop. Front Oncol. 11:6798162021. View Article : Google Scholar : PubMed/NCBI | |
Du MW, Zhu XL, Zhang DX, Chen XZ, Yang LH, Xiao JZ, Fang WJ, Xue XC, Pan WH, Liao WQ and Yang T: X-Paste improves wound healing in diabetes via NF-E2-related factor/HO-1 signaling pathway. World J Diabetes. 15:1299–1316. 2024. View Article : Google Scholar : PubMed/NCBI | |
Cao Y, Zhang H, Tang J and Wang R: Ferulic acid mitigates growth and invasion of esophageal squamous cell carcinoma through inducing ferroptotic cell death. Dis Markers. 2022:46079662022. View Article : Google Scholar : PubMed/NCBI | |
He L, Zhang T, Sun W, Qin Y, Wang Z, Dong W and Zhang H: The DPP-IV inhibitor saxagliptin promotes the migration and invasion of papillary thyroid carcinoma cells via the NRF2/HO1 pathway. Med Oncol. 37:972020. View Article : Google Scholar : PubMed/NCBI | |
Yang PW, Xu PL, Cheng CS, Jiao JY, Wu Y, Dong S, Xie J and Zhu XY: Integrating network pharmacology and experimental models to investigate the efficacy of QYHJ on pancreatic cancer. J Ethnopharmacol. 297:1155162022. View Article : Google Scholar : PubMed/NCBI | |
Lim GE, Sung JY, Yu S, Kim Y, Shim J, Kim HJ, Cho ML, Lee JS and Kim YN: Pygenic acid A (PA) sensitizes metastatic breast cancer cells to anoikis and inhibits metastasis in vivo. Int J Mol Sci. 21:84442020. View Article : Google Scholar : PubMed/NCBI | |
Chou YT, Hsu FF, Hu DY, Chen YC, Hsu YH, Hsu JT and Chau LY: Identification of danthron as an isoform-specific inhibitor of HEME OXYGENASE-1/cytochrome P450 reductase interaction with anti-tumor activity. J Biomed Sci. 25:62018. View Article : Google Scholar : PubMed/NCBI | |
Jang HY, Hong OY, Youn HJ, Kim MG, Kim CH, Jung SH and Kim JS: 15d-PGJ2 inhibits NF-κB and AP-1-mediated MMP-9 expression and invasion of breast cancer cell by means of a heme oxygenase-1-dependent mechanism. BMB Rep. 53:212–217. 2020. View Article : Google Scholar : PubMed/NCBI | |
Poprac P, Jomova K, Simunkova M, Kollar V, Rhodes CJ and Valko M: Targeting free radicals in oxidative stress-related human diseases. Trends Pharmacol Sci. 38:592–607. 2017. View Article : Google Scholar : PubMed/NCBI | |
Sies H: Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: Oxidative eustress. Redox Biol. 11:613–619. 2017. View Article : Google Scholar : PubMed/NCBI | |
Seiva FRF, Agneis MLG, de Almeida MR, Caputo WL, de Souza MC, das Neves KA, Oliveira ÉN, Justulin LA Jr and Chuffa LGA: In silico analysis of non-conventional oxidative stress-related enzymes and their potential relationship with carcinogenesis. Antioxidants (Basel). 13:12792024. View Article : Google Scholar : PubMed/NCBI | |
Shokeir AA, Hussein AM, Barakat N, Abdelaziz A, Elgarba M and Awadalla A: Activation of nuclear factor erythroid 2-related factor 2 (Nrf2) and Nrf-2-dependent genes by ischaemic pre-conditioning and post-conditioning: New adaptive endogenous protective responses against renal ischaemia/reperfusion injury. Acta Physiol (Oxf). 210:342–353. 2014. View Article : Google Scholar : PubMed/NCBI | |
Zedan AMG, Sakran MI, Bahattab O, Hawsawi YM, Al-Amer O, Oyouni AAA, Nasr Eldeen SK and El-Magd MA: Oriental hornet (Vespa orientalis) larval extracts induce antiproliferative, antioxidant, anti-inflammatory, and anti-migratory effects on MCF7 cells. Molecules. 26:33032021. View Article : Google Scholar : PubMed/NCBI | |
Mizunoe Y, Kobayashi M, Sudo Y, Watanabe S, Yasukawa H, Natori D, Hoshino A, Negishi A, Okita N, Komatsu M and Higami Y: Trehalose protects against oxidative stress by regulating the Keap1-Nrf2 and autophagy pathways. Redox Biol. 15:115–124. 2018. View Article : Google Scholar : PubMed/NCBI | |
Song HC, Chen Y, Chen Y, Park J, Zheng M, Surh YJ, Kim UH, Park JW, Yu R, Chung HT and Joe Y: GSK-3β inhibition by curcumin mitigates amyloidogenesis via TFEB activation and anti-oxidative activity in human neuroblastoma cells. Free Radic Res. 54:918–930. 2020. View Article : Google Scholar : PubMed/NCBI | |
Zhang L, Zhang J, Ye Z, Manevich Y, Ball LE, Bethard JR, Jiang YL, Broome AM, Dalton AC, Wang GY, et al: Isoflavone ME-344 disrupts redox homeostasis and mitochondrial function by targeting heme oxygenase 1. Cancer Res. 79:4072–4085. 2019. View Article : Google Scholar : PubMed/NCBI | |
Dong J, Li Y, Xiao H, Luo D, Zhang S, Zhu C, Jiang M, Cui M, Lu L and Fan S: Cordycepin sensitizes breast cancer cells toward irradiation through elevating ROS production involving Nrf2. Toxicol Appl Pharmacol. 364:12–21. 2019. View Article : Google Scholar : PubMed/NCBI | |
Liang X, Wang P, Yang C, Huang F, Wu H, Shi H and Wu X: Galangin inhibits gastric cancer growth through enhancing STAT3 mediated ROS production. Front Pharmacol. 12:6466282021. View Article : Google Scholar : PubMed/NCBI | |
Binnewies M, Roberts EW, Kersten K, Chan V, Fearon DF, Merad M, Coussens LM, Gabrilovich DI, Ostrand-Rosenberg S, Hedrick CC, et al: Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat Med. 24:541–550. 2018. View Article : Google Scholar : PubMed/NCBI | |
Hanahan D and Weinberg RA: Hallmarks of cancer: The next generation. Cell. 144:646–674. 2011. View Article : Google Scholar : PubMed/NCBI | |
Muliaditan T, Caron J, Okesola M, Opzoomer JW, Kosti P, Georgouli M, Gordon P, Lall S, Kuzeva DM, Pedro L, et al: Macrophages are exploited from an innate wound healing response to facilitate cancer metastasis. Nat Commun. 9:29512018. View Article : Google Scholar : PubMed/NCBI | |
Was H, Dulak J and Jozkowicz A: Heme oxygenase-1 in tumor biology and therapy. Curr Drug Targets. 11:1551–1570. 2010. View Article : Google Scholar : PubMed/NCBI | |
Hashimoto K, Nishimura S, Ito T, Kakinoki R and Akagi M: Immunohistochemical expression and clinicopathological assessment of PD-1, PD-L1, NY-ESO-1, and MAGE-A4 expression in highly aggressive soft tissue sarcomas. Eur J Histochem. 66:33932022. View Article : Google Scholar : PubMed/NCBI | |
Muliaditan T, Opzoomer JW, Caron J, Okesola M, Kosti P, Lall S, Van Hemelrijck M, Dazzi F, Tutt A, Grigoriadis A, et al: Repurposing Tin mesoporphyrin as an immune checkpoint inhibitor shows therapeutic efficacy in preclinical models of cancer. Clin Cancer Res. 24:1617–1628. 2018. View Article : Google Scholar : PubMed/NCBI | |
Spear S, Le Saux O, Mirza H.B, Iyer N, Tyson K, Grundland Freile F, Walton JB, Woodman C, Jarvis S, Ennis DP, et al: PTEN loss shapes macrophage dynamics in high-grade serous ovarian carcinoma. Cancer Res. 84:3772–3787. 2024. View Article : Google Scholar : PubMed/NCBI | |
Yuan H, Xia P, Sun X, Ma J, Xu X, Fu C, Zhou H, Guan Y, Li Z, Zhao S, et al: Photothermal nanozymatic nanoparticles induce ferroptosis and apoptosis through tumor microenvironment manipulation for cancer therapy. Small. 18:e22021612022. View Article : Google Scholar : PubMed/NCBI | |
Gong X, Liu Y, Liang K, Chen Z, Ding K, Qiu L, Wei J and Du H: Cucurbitacin I reverses tumor-associated macrophage polarization to affect cancer cell metastasis. Int J Mol Sci. 24:159202023. View Article : Google Scholar : PubMed/NCBI | |
Magri S, Musca B, Pinton L, Orecchini E, Belladonna ML, Orabona C, Bonaudo C, Volpin F, Ciccarino P, Baro V, et al: The immunosuppression pathway of tumor-associated macrophages is controlled by heme oxygenase-1 in glioblastoma patients. Int J Cancer. 151:2265–2277. 2022. View Article : Google Scholar : PubMed/NCBI | |
Liu XM, Li Z, Wang XY, Ding BW, Wang JQ, Qiao X, Feng YK, Hao JH and Xu JY: Self-assembled HO-1i-Pt(IV) nanomedicine targeting p38/MAPK and MDR pathways for cancer chemo-immunotherapy. J Control Release. 379:797–813. 2025.(Epub ahead of print). View Article : Google Scholar : PubMed/NCBI | |
Dulak J and Jozkowicz A: Novel faces of heme oxygenase-1: Mechanisms and therapeutic potentials. Antioxid Redox Signal. 20:1673–1676. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wadowski P, Juszczak M and Woźniak K: NRF2 modulators of plant origin and their ability to overcome multidrug resistance in cancers. Int J Mol Sci. 25:115002024. View Article : Google Scholar : PubMed/NCBI | |
Ekiert HM and Szopa A: Biological activities of natural products. Molecules. 25:57692020. View Article : Google Scholar : PubMed/NCBI | |
Yagüe E, Sun H and Hu Y: East Wind, West Wind: Toward the modernization of traditional Chinese medicine. Front Neurosci. 16:10578172022. View Article : Google Scholar : PubMed/NCBI | |
Chen Z, Yu T, Wang Y, Li J, Zhang B and Zhou L: Mechanistic insights into the role of traditional Chinese medicine in treating gastric cancer. Front Oncol. 14:14436862025. View Article : Google Scholar : PubMed/NCBI | |
Liu Y, Fang C, Luo J, Gong C, Wang L and Zhu S: Traditional Chinese medicine for cancer treatment. Am J Chin Med. 52:583–604. 2024. View Article : Google Scholar : PubMed/NCBI | |
Gorrini C, Harris IS and Mak TW: Modulation of oxidative stress as an anticancer strategy. Nat Rev Drug Discov. 12:931–947. 2013. View Article : Google Scholar : PubMed/NCBI | |
Arnold JN, Magiera L, Kraman M and Fearon DT: Tumoral immune suppression by macrophages expressing fibroblast activation protein-α and heme oxygenase-1. Cancer Immunol Res. 2:121–126. 2014. View Article : Google Scholar : PubMed/NCBI | |
Zheng Z, Ke L, Ye S, Shi P and Yao H: Pharmacological mechanisms of cryptotanshinone: Recent advances in cardiovascular, cancer, and neurological disease applications. Drug Des Devel Ther. 18:6031–6060. 2024. View Article : Google Scholar : PubMed/NCBI | |
Chiang SK, Chen SE and Chang LC: A dual role of heme oxygenase-1 in cancer cells. Int J Mol Sci. 20:392018. View Article : Google Scholar : PubMed/NCBI | |
Calò LA, Pagnin E, Davis PA, Armanini D, Mormino P, Rossi GP and Pessina AC: Oxidative stress-related proteins in a Conn's adenoma tissue. Relevance for aldosterone's prooxidative and proinflammatory activity. J Endocrinol Invest. 33:48–53. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zhang C, Deng Z, Wu J, Ding C, Li Z, Xu Z, Chen W, Yang K, Wei H, He T, et al: HO-1 impairs the efficacy of radiotherapy by redistributing cGAS and STING in tumors. J Clin Invest. 134:e1810442024. View Article : Google Scholar : PubMed/NCBI |