Adipocyte‑rich microenvironment promotes chemoresistance via upregulation of peroxisome proliferator‑activated receptor gamma/ABCG2 in epithelial ovarian cancer
- Authors:
- Siqi Chen
- Zixuan Liu
- Haixia Wu
- Bo Wang
- Yuqing Ouyang
- Junru Liu
- Xiaoyan Zheng
- Haoke Zhang
- Xueying Li
- Xiaofan Feng
- Yan Li
- Yangyang Shen
- Hong Zhang
- Bo Xiao
- Chunyan Yu
- Weimin Deng
-
Affiliations: Department of Immunology, Tianjin Institute of Immunology, Tianjin Key Laboratory of Cellular and Molecular Immunology, Key Laboratory of Diseases and Microenvironment of Ministry of Education of China, Tianjin Medical University, Tianjin 300070, P.R. China, Department of Pathology, Tianjin Central Hospital of Obstetrics and Gynecology, Tianjin 300100, P.R. China, Department of Blood Transfusion, Qilu Hospital of Shandong University Dezhou Hospital, Dezhou, Shandong 253000, P.R. China, Department of Laboratory, Shanxi Eye Hospital, Taiyuan, Shanxi 030002, P.R. China, Department of Family Planning, The Second Hospital of Tianjin Medical University, Tianjin 300211, P.R. China, Department of Clinical Laboratory, The Affiliated Eye Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325027, P.R. China - Published online on: February 27, 2024 https://doi.org/10.3892/ijmm.2024.5361
- Article Number: 37
-
Copyright: © Chen et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Miller KD, Nogueira L, Devasia T, Mariotto AB, Yabroff KR, Jemal A, Kramer J and Siegel RL: Cancer treatment and survivorship statistics, 2022. CA Cancer J Clin. 72:409–436. 2022. View Article : Google Scholar : PubMed/NCBI | |
Raghavan S, Winter PS, Navia AW, Williams HL, DenAdel A, Lowder KE, Galvez-Reyes J, Kalekar RL, Mulugeta N, Kapner KS, et al: Microenvironment drives cell state, plasticity, and drug response in pancreatic cancer. Cell. 184:6119–6137.e26. 2021. View Article : Google Scholar : PubMed/NCBI | |
Lin F, Li X and Wang X, Sun H, Wang Z and Wang X: Stanniocalcin 1 promotes metastasis, lipid metabolism and cisplatin chemoresistance via the FOXC2/ITGB6 signaling axis in ovarian cancer. J Exp Clin Cancer Res. 41:1292022. View Article : Google Scholar : PubMed/NCBI | |
Mukherjee A, Chiang CY, Daifotis HA, Nieman KM, Fahrmann JF, Lastra RR, Romero IL, Fiehn O and Lengyel E: Adipocyte-induced FABP4 expression in ovarian cancer cells promotes metastasis and mediates carboplatin resistance. Cancer Res. 80:1748–1761. 2020. View Article : Google Scholar : PubMed/NCBI | |
Liu X, Zhang P, Xu J, Lv G and Li Y: Lipid metabolism in tumor microenvironment: Novel therapeutic targets. Cancer Cell Int. 22:2242022. View Article : Google Scholar : PubMed/NCBI | |
Vasseur S and Guillaumond F: Lipids in cancer: A global view of the contribution of lipid pathways to metastatic formation and treatment resistance. Oncogenesis. 11:462022. View Article : Google Scholar : PubMed/NCBI | |
Mukherjee A, Bilecz AJ and Lengyel E: The adipocyte microenvironment and cancer. Cancer Metastasis Rev. 41:575–587. 2022. View Article : Google Scholar : PubMed/NCBI | |
Vlachostergios PJ: Loss of tumor suppressive properties of lipid metabolism enzyme CPT2 in ovarian carcinoma: Comment on 'CPT2 down-regulation promotes tumor growth and metastasis through inducing ROS/NFκB pathway in ovarian cancer' by Zhang et al. Transl Oncol. 14:1010672021. View Article : Google Scholar | |
Siegel RL, Miller KD and Jemal A: Cancer statistics, 2020. CA Cancer J Clin. 70:7–30. 2020. View Article : Google Scholar : PubMed/NCBI | |
Gilks CB and Prat J: Ovarian carcinoma pathology and genetics: Recent advances. Hum Pathol. 40:1213–1223. 2009. View Article : Google Scholar : PubMed/NCBI | |
Montaigne D, Butruille L and Staels B: PPAR control of metabolism and cardiovascular functions. Nat Rev Cardiol. 18:809–823. 2021. View Article : Google Scholar : PubMed/NCBI | |
Luo X, Xu J, Yu J and Yi P: Shaping immune responses in the tumor microenvironment of ovarian cancer. Front Immunol. 12:6923602021. View Article : Google Scholar : PubMed/NCBI | |
Tian W, Lei N, Zhou J, Chen M, Guo R, Qin B, Li Y and Chang L: Extracellular vesicles in ovarian cancer chemoresistance, metastasis, and immune evasion. Cell Death Dis. 13:642022. View Article : Google Scholar : PubMed/NCBI | |
Li Y, Yu C and Deng W: Roles and mechanisms of adipokines in drug resistance of tumor cells. Eur J Pharmacol. 899:1740192021. View Article : Google Scholar : PubMed/NCBI | |
Dai L, Song K and Di W: Adipocytes: Active facilitators in epithelial ovarian cancer progression? J Ovarian Res. 13:1152020. View Article : Google Scholar : PubMed/NCBI | |
Chehade H, Tedja R, Ramos H, Bawa TS, Adzibolosu N, Gogoi R, Mor G and Alvero AB: Regulatory role of the adipose microenvironment on ovarian cancer progression. Cancers (Basel). 14:22672022. View Article : Google Scholar : PubMed/NCBI | |
Duan C, Yu M, Xu J, Li BY, Zhao Y and Kankala RK: Overcoming cancer multi-drug resistance (MDR): Reasons, mechanisms, nanotherapeutic solutions, and challenges. Biomed Pharmacother. 162:1146432023. View Article : Google Scholar : PubMed/NCBI | |
Pote MS and Gacche RN: ATP-binding cassette efflux transporters and MDR in cancer. Drug Discov Today. 28:1035372023. View Article : Google Scholar : PubMed/NCBI | |
Dean M, Moitra K and Allikmets R: The human ATP-binding cassette (ABC) transporter superfamily. Hum Mutat. 43:1162–1182. 2022. View Article : Google Scholar : PubMed/NCBI | |
Kukal S, Guin D, Rawat C, Bora S, Mishra MK, Sharma P, Paul PR, Kanojia N, Grewal GK, Kukreti S, et al: Multidrug efflux transporter ABCG2: Expression and regulation. Cell Mol Life Sci. 78:6887–6939. 2021. View Article : Google Scholar : PubMed/NCBI | |
Li B, Jiang J, Assaraf YG, Xiao H, Chen ZS and Huang C: Surmounting cancer drug resistance: New insights from the perspective of N6-methyladenosine RNA modification. Drug Resist Updat. 53:1007202020. View Article : Google Scholar | |
Mirza AZ, Althagafi II and Shamshad H: Role of PPAR receptor in different diseases and their ligands: Physiological importance and clinical implications. Eur J Med Chem. 166:502–513. 2019. View Article : Google Scholar : PubMed/NCBI | |
Ma S, Zhou B, Yang Q, Pan Y, Yang W, Freedland SJ, Ding LW, Freeman MR, Breunig JJ, Bhowmick NA, et al: A transcriptional regulatory loop of master regulator transcription factors, PPARG, and fatty acid synthesis promotes esophageal adenocarcinoma. Cancer Res. 81:1216–1229. 2021. View Article : Google Scholar : PubMed/NCBI | |
Mannan A, Garg N, Singh TG and Kang HK: Peroxisome proliferator-activated receptor-gamma (PPAR-γ): Molecular effects and its importance as a novel therapeutic target for cerebral ischemic injury. Neurochem Res. 46:2800–2831. 2021. View Article : Google Scholar : PubMed/NCBI | |
Szatmari I, Vámosi G, Brazda P, Balint BL, Benko S, Széles L, Jeney V, Ozvegy-Laczka C, Szántó A, Barta E, et al: Peroxisome proliferator-activated receptor gamma-regulated ABCG2 expression confers cytoprotection to human dendritic cells. J Biol Chem. 281:23812–23823. 2006. View Article : Google Scholar : PubMed/NCBI | |
Lin Y, Bircsak KM, Gorczyca L, Wen X and Aleksunes LM: Regulation of the placental BCRP transporter by PPAR gamma. J Biochem Mol Toxicol. 31: View Article : Google Scholar : 2017. | |
Kim CE, Park HY, Won HJ, Kim M, Kwon B, Lee SJ, Kim DH, Shin JG and Seo SK: Repression of PPARγ reduces the ABCG2-mediated efflux activity of M2 macrophages. Int J Biochem Cell Biol. 130:1058952021. View Article : Google Scholar | |
Yu Z, Cai Y, Deng M, Li D, Wang X, Zheng H, Xu Y, Li W and Zhang W: Fat extract promotes angiogenesis in a murine model of limb ischemia: A novel cell-free therapeutic strategy. Stem Cell Res Ther. 9:2942018. View Article : Google Scholar : PubMed/NCBI | |
Yu C, Niu X, Du Y, Chen Y, Liu X, Xu L, Iwakura Y, Ma X, Li Y, Yao Z and Deng W: IL-17A promotes fatty acid uptake through the IL-17A/IL-17RA/p-STAT3/FABP4 axis to fuel ovarian cancer growth in an adipocyte-rich microenvironment. Cancer Immunol Immunother. 69:115–126. 2020. View Article : Google Scholar | |
Xu S, Yu C, Ma X, Li Y, Shen Y, Chen Y, Huang S, Zhang T, Deng W and Wang Y: IL-6 promotes nuclear translocation of HIF-1α to aggravate chemoresistance of ovarian cancer cells. Eur J Pharmacol. 894:1738172021. View Article : Google Scholar | |
Shen M, Xu Z, Xu W, Jiang K, Zhang F, Ding Q, Xu Z and Chen Y: Inhibition of ATM reverses EMT and decreases metastatic potential of cisplatin-resistant lung cancer cells through JAK/STAT3/PD-L1 pathway. J Exp Clin Cancer Res. 38:1492019. View Article : Google Scholar : PubMed/NCBI | |
Li D, Wang Y, Dong C, Chen T, Dong A, Ren J, Li W, Shu G, Yang J, Shen W, et al: CST1 inhibits ferroptosis and promotes gastric cancer metastasis by regulating GPX4 protein stability via OTUB1. Oncogene. 42:83–98. 2023. View Article : Google Scholar : | |
Christofides A, Konstantinidou E, Jani C and Boussiotis VA: The role of peroxisome proliferator-activated receptors (PPAR) in immune responses. Metabolism. 114:1543382021. View Article : Google Scholar | |
Hamilton TC, Young RC, McKoy WM, Grotzinger KR, Green JA, Chu EW, Whang-Peng J, Rogan AM, Green WR and Ozols RF: Characterization of a human ovarian carcinoma cell line (NIH:OVCAR-3) with androgen and estrogen receptors. Cancer Res. 43:5379–5389. 1983.PubMed/NCBI | |
Mitra AK, Davis DA, Tomar S, Roy L, Gurler H, Xie J, Lantvit DD, Cardenas H, Fang F, Liu Y, et al: In vivo tumor growth of high-grade serous ovarian cancer cell lines. Gynecol Oncol. 138:372–377. 2015. View Article : Google Scholar : PubMed/NCBI | |
Zhao G, Tan Y, Cardenas H, Vayngart D, Wang Y, Huang H, Keathley R, Wei JJ, Ferreira CR, Orsulic S, et al: Ovarian cancer cell fate regulation by the dynamics between saturated and unsaturated fatty acids. Proc Natl Acad Sci USA. 119:e22034801192022. View Article : Google Scholar : PubMed/NCBI | |
Šrámek J, Němcová-Fürstová V and Kovář J: Molecular mechanisms of apoptosis induction and its regulation by fatty acids in pancreatic β-cells. Int J Mol Sci. 22:42852021. View Article : Google Scholar | |
Krümmel B, von Hanstein AS, Plötz T, Lenzen S and Mehmeti I: Differential effects of saturated and unsaturated free fatty acids on ferroptosis in rat β-cells. J Nutr Biochem. 106:1090132022. View Article : Google Scholar | |
Hoy AJ, Nagarajan SR and Butler LM: Tumour fatty acid metabolism in the context of therapy resistance and obesity. Nat Rev Cancer. 21:753–766. 2021. View Article : Google Scholar : PubMed/NCBI | |
Aggarwal S, Verma SS, Aggarwal S and Gupta SC: Drug repurposing for breast cancer therapy: Old weapon for new battle. Semin Cancer Biol. 68:8–20. 2021. View Article : Google Scholar | |
Chen HJ, Chung YL, Li CY, Chang YT, Wang CCN, Lee HY, Lin HY and Hung CC: Taxifolin Resensitizes multidrug resistance cancer cells via uncompetitive inhibition of P-glycoprotein function. Molecules. 23:30552018. View Article : Google Scholar : PubMed/NCBI | |
Engle K and Kumar G: Cancer multidrug-resistance reversal by ABCB1 inhibition: A recent update. Eur J Med Chem. 239:1145422022. View Article : Google Scholar : PubMed/NCBI | |
Modi A, Roy D, Sharma S, Vishnoi JR, Pareek P, Elhence P, Sharma P and Purohit P: ABC transporters in breast cancer: Their roles in multidrug resistance and beyond. J Drug Target. 30:927–947. 2022. View Article : Google Scholar : PubMed/NCBI | |
Wang J, Yang DH, Yang Y, Wang JQ, Cai CY, Lei ZN, Teng QX, Wu ZX, Zhao L and Chen ZS: Overexpression of ABCB1 transporter confers resistance to mTOR inhibitor WYE-354 in cancer cells. Int J Mol Sci. 21:13872020. View Article : Google Scholar : PubMed/NCBI | |
Bukowski K, Kciuk M and Kontek R: Mechanisms of multidrug resistance in cancer chemotherapy. Int J Mol Sci. 21:32332020. View Article : Google Scholar : PubMed/NCBI | |
He ZX, Zhao TQ, Gong YP, Zhang X, Ma LY and Liu HM: Pyrimidine: A promising scaffold for optimization to develop the inhibitors of ABC transporters. Eur J Med Chem. 200:1124582020. View Article : Google Scholar : PubMed/NCBI | |
Miyata H, Takada T, Toyoda Y, Matsuo H, Ichida K and Suzuki H: Identification of febuxostat as a new strong ABCG2 inhibitor: Potential applications and risks in clinical situations. Front Pharmacol. 7:5182016. View Article : Google Scholar | |
Deng F, Sjostedt N, Santo M, Neuvonen M, Niemi M and Kidron H: Novel inhibitors of breast cancer resistance protein (BCRP, ABCG2) among marketed drugs. Eur J Pharm Sci. 181:1063622023. View Article : Google Scholar | |
Cao Y: Adipocyte and lipid metabolism in cancer drug resistance. J Clin Invest. 129:3006–3017. 2019. View Article : Google Scholar : PubMed/NCBI | |
Zhou X, Zhang J, Lv W, Zhao C, Xia Y, Wu Y and Zhang Q: The pleiotropic roles of adipocyte secretome in remodeling breast cancer. J Exp Clin Cancer Res. 41:2032022. View Article : Google Scholar : PubMed/NCBI | |
Dumas JF and Brisson L: Interaction between adipose tissue and cancer cells: Role for cancer progression. Cancer Metastasis Rev. 40:31–46. 2021. View Article : Google Scholar | |
Brown KA and Scherer PE: Update on adipose tissue and cancer. Endocr Rev. 44:961–974. 2023. View Article : Google Scholar : PubMed/NCBI | |
Tewari S, Vargas R and Reizes O: The impact of obesity and adipokines on breast and gynecologic malignancies. Ann N Y Acad Sci. 1518:131–150. 2022. View Article : Google Scholar : PubMed/NCBI | |
Clemente-Suárez VJ, Redondo-Flórez L, Beltrán-Velasco AI, Martín-Rodríguez A, Martínez-Guardado I, Navarro-Jiménez E, Laborde-Cárdenas CC and Tornero-Aguilera JF: The role of adipokines in health and disease. Biomedicines. 11:12902023. View Article : Google Scholar : PubMed/NCBI | |
Rybinska I, Mangano N, Tagliabue E and Triulzi T: Cancer-associated adipocytes in breast cancer: Causes and consequences. Int J Mol Sci. 22:37752021. View Article : Google Scholar : PubMed/NCBI | |
Wróblewski M, Szewczyk-Golec K, Hołyńska-Iwan I, Wróblewska J and Woźniak A: Characteristics of selected adipokines in ascites and blood of ovarian cancer patients. Cancers (Basel). 13:47022021. View Article : Google Scholar : PubMed/NCBI | |
Rajesh Y and Sarkar D: Association of adipose tissue and adipokines with development of obesity-induced liver cancer. Int J Mol Sci. 22:21632021. View Article : Google Scholar : PubMed/NCBI | |
Conze D, Weiss L, Regen PS, Bhushan A, Weaver D, Johnson P and Rincon M: Autocrine production of interleukin 6 causes multidrug resistance in breast cancer cells. Cancer Res. 61:8851–8858. 2001.PubMed/NCBI | |
Lipsey CC, Harbuzariu A, Robey RW, Huff LM, Gottesman MM and Gonzalez-Perez RR: Leptin signaling affects survival and chemoresistance of estrogen receptor negative breast cancer. Int J Mol Sci. 21:37942020. View Article : Google Scholar : PubMed/NCBI | |
Weng C, Dong H, Bai R, Sheng J, Chen G, Ding K, Lin W, Chen J and Xu Z: Angiogenin promotes angiogenesis via the endonucleolytic decay of miR-141 in colorectal cancer. Mol Ther Nucleic Acids. 27:1010–1022. 2022. View Article : Google Scholar : PubMed/NCBI | |
Lehuédé C, Li X, Dauvillier S, Vaysse C, Franchet C, Clement E, Esteve D, Longué M, Chaltiel L, Le Gonidec S, et al: Adipocytes promote breast cancer resistance to chemotherapy, a process amplified by obesity: Role of the major vault protein (MVP). Breast Cancer Res. 21:72019. View Article : Google Scholar | |
Sarkanen JR, Kaila V, Mannerström B, Räty S, Kuokkanen H, Miettinen S and Ylikomi T: Human adipose tissue extract induces angiogenesis and adipogenesis in vitro. Tissue Eng Part A. 18:17–25. 2012. View Article : Google Scholar | |
Amor S, Iglesias-de la Cruz MC, Ferrero E, Garcia-Villar O, Barrios V, Fernandez N, Monge L, García-Villalón AL and Granado M: Peritumoral adipose tissue as a source of inflammatory and angiogenic factors in colorectal cancer. Int J Colorectal Dis. 31:365–375. 2016. View Article : Google Scholar | |
Bejarano L, Jordāo MJC and Joyce JA: Therapeutic targeting of the tumor microenvironment. Cancer Discov. 11:933–959. 2021. View Article : Google Scholar : PubMed/NCBI | |
Huang M, Lin Y, Wang C, Deng L, Chen M, Assaraf YG, Chen ZS, Ye W and Zhang D: New insights into antiangiogenic therapy resistance in cancer: Mechanisms and therapeutic aspects. Drug Resist Updat. 64:1008492022. View Article : Google Scholar : PubMed/NCBI | |
Qi S, Deng S, Lian Z and Yu K: Novel Drugs with high efficacy against tumor angiogenesis. Int J Mol Sci. 23:69342022. View Article : Google Scholar : PubMed/NCBI | |
Iwamoto H, Abe M, Yang Y, Cui D, Seki T, Nakamura M, Hosaka K, Lim S, Wu J, He X, et al: Cancer lipid metabolism confers antiangiogenic drug resistance. Cell Metab. 28:104–117.e5. 2018. View Article : Google Scholar : PubMed/NCBI | |
Mentoor I, Engelbrecht AM, van Jaarsveld PJ and Nell T: Chemoresistance: Intricate interplay between breast tumor cells and adipocytes in the tumor microenvironment. Front Endocrinol (Lausanne). 9:7582018. View Article : Google Scholar | |
Bougaret L, Delort L, Billard H, Le Huede C, Boby C, De la Foye A, Rossary A, Mojallal A, Damour O, Auxenfans C, et al: Adipocyte/breast cancer cell crosstalk in obesity interferes with the anti-proliferative efficacy of tamoxifen. PLoS One. 13:e01915712018. View Article : Google Scholar : PubMed/NCBI | |
Yang J, Zaman MM, Vlasakov I, Roy R, Huang L, Martin CR, Freedman SD, Serhan CN and Moses MA: Adipocytes promote ovarian cancer chemoresistance. Sci Rep. 9:133162019. View Article : Google Scholar : PubMed/NCBI | |
Kasonga A, Kruger MC and Coetzee M: Activation of PPARs modulates signalling pathways and expression of regulatory genes in osteoclasts derived from human CD14+ monocytes. Int J Mol Sci. 20:17982019. View Article : Google Scholar : PubMed/NCBI | |
Li G, Li X, Mahmud I, Ysaguirre J, Fekry B, Wang S, Wei B, Eckel-Mahan KL, Lorenzi PL, Lehner R and Sun K: Interfering with lipid metabolism through targeting CES1 sensitizes hepatocellular carcinoma for chemotherapy. JCI Insight. 8:e1636242023. View Article : Google Scholar : | |
Schlotterbeck J, Cebo M, Kolb A and Lämmerhofer M: Quantitative analysis of chemoresistance-inducing fatty acid in food supplements using UHPLC-ESI-MS/MS. Anal Bioanal Chem. 411:479–491. 2019. View Article : Google Scholar | |
Zou Y, Watters A, Cheng N, Perry CE, Xu K, Alicea GM, Parris JLD, Baraban E, Ray P, Nayak A, et al: Polyunsaturated fatty acids from astrocytes activate PPARγ signaling in cancer cells to promote brain metastasis. Cancer Discov. 9:1720–1735. 2019. View Article : Google Scholar : PubMed/NCBI | |
Liotti A, Cosimato V, Mirra P, Cali G, Conza D, Secondo A, Luongo G, Terracciano D, Formisano P, Beguinot F, et al: Oleic acid promotes prostate cancer malignant phenotype via the G protein-coupled receptor FFA1/GPR40. J Cell Physiol. 233:7367–7378. 2018. View Article : Google Scholar : PubMed/NCBI | |
Zhang M, Di Martino JS, Bowman RL, Campbell NR, Baksh SC, Simon-Vermot T, Kim IS, Haldeman P, Mondal C, Yong-Gonzales V, et al: Adipocyte-derived lipids mediate melanoma progression via FATP proteins. Cancer Discov. 8:1006–1025. 2018. View Article : Google Scholar : PubMed/NCBI | |
Zhang Y, Wang D, Lv B, Hou X, Liu Q, Liao C, Xu R, Zhang Y, Xu F and Zhang P: Oleic acid and insulin as key characteristics of T2D promote colorectal cancer deterioration in xenograft mice revealed by functional metabolomics. Front Oncol. 11:6850592021. View Article : Google Scholar : PubMed/NCBI | |
Li X, Ycaza J and Blumberg B: The environmental obesogen tributyltin chloride acts via peroxisome proliferator activated receptor gamma to induce adipogenesis in murine 3T3-L1 preadipocytes. J Steroid Biochem Mol Biol. 127:9–15. 2011. View Article : Google Scholar : PubMed/NCBI | |
Hernandez-Quiles M, Broekema MF and Kalkhoven E: PPARgamma in metabolism, immunity, and cancer: Unified and diverse mechanisms of action. Front Endocrinol (Lausanne). 12:6241122021. View Article : Google Scholar : PubMed/NCBI | |
Mal S, Dwivedi AR and Kumar V, Kumar N, Kumar B and Kumar V: Role of peroxisome proliferator-activated receptor gamma (PPARγ) in different disease states: Recent updates. Curr Med Chem. 28:3193–3215. 2021. View Article : Google Scholar | |
Zhang GY, Ahmed N, Riley C, Oliva K, Barker G, Quinn MA and Rice GE: Enhanced expression of peroxisome proliferator-activated receptor gamma in epithelial ovarian carcinoma. Br J Cancer. 92:113–119. 2005. View Article : Google Scholar | |
Al-Alem L, Southard RC, Kilgore MW and Curry TE: Specific thiazolidinediones inhibit ovarian cancer cell line proliferation and cause cell cycle arrest in a PPARγ independent manner. PLoS One. 6:e161792011. View Article : Google Scholar | |
Shin SJ, Kim JY, Kwon SY, Mun KC, Cho CH and Ha E: Ciglitazone enhances ovarian cancer cell death via inhibition of glucose transporter-1. Eur J Pharmacol. 743:17–23. 2014. View Article : Google Scholar : PubMed/NCBI | |
Zhang Y, Ba Y, Liu C, Sun G, Ding L, Gao S, Hao J, Yu Z, Zhang J, Zen K, et al: PGC-1alpha induces apoptosis in human epithelial ovarian cancer cells through a PPARgamma-dependent pathway. Cell Res. 17:363–373. 2007. View Article : Google Scholar : PubMed/NCBI | |
Kim S, Lee JJ and Heo DS: PPARγ ligands induce growth inhibition and apoptosis through p63 and p73 in human ovarian cancer cells. Biochem Biophys Res Commun. 406:389–395. 2011. View Article : Google Scholar : PubMed/NCBI | |
Yokoyama Y, Xin B, Shigeto T and Mizunuma H: Combination of ciglitazone, a peroxisome proliferator-activated receptor gamma ligand, and cisplatin enhances the inhibition of growth of human ovarian cancers. J Cancer Res Clin Oncol. 137:1219–1228. 2011. View Article : Google Scholar : PubMed/NCBI | |
Cheng S, Qian K, Wang Y, Wang G, Liu X, Xiao Y and Wang X: PPARγ inhibition regulates the cell cycle, proliferation and motility of bladder cancer cells. J Cell Mol Med. 23:3724–3736. 2019. View Article : Google Scholar : PubMed/NCBI | |
Wu B, Sun X, Gupta HB, Yuan B, Li J, Ge F, Chiang HC, Zhang X, Zhang C, Zhang D, et al: Adipose PD-L1 modulates PD-1/PD-L1 checkpoint blockade immunotherapy efficacy in breast cancer. Oncoimmunology. 7:e15001072018. View Article : Google Scholar : PubMed/NCBI |