Role of ENPP1 in cancer pathogenesis: Mechanisms and clinical implications (Review)
- Authors:
- Lujie Zhao
- Yu Zhang
- Yahui Tian
- Xin Ding
- Runling Lin
- Lin Xiao
- Fujun Peng
- Kai Zhang
- Zhongfa Yang
-
Affiliations: School of Basic Medical Sciences, Shandong Second Medical University, Weifang, Shandong 261021, P.R. China, School of Clinical Medical Sciences, Shandong Second Medical University, Weifang, Shandong 261021, P.R. China, Genetic Testing Centre, Qingdao University Women's and Children's Hospital, Qingdao, Shandong 266000, P.R. China - Published online on: October 3, 2024 https://doi.org/10.3892/ol.2024.14722
- Article Number: 590
-
Copyright: © Zhao et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
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|
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 | |
|
Sana H and Pigeolet M: The role of surgery in global cancer services. Lancet. 403:1237–1238. 2024. View Article : Google Scholar : PubMed/NCBI | |
|
Paul S, Konig MF, Pardoll DM, Bettegowda C, Papadopoulos N, Wright KM, Gabelli SB, Ho M, van Elsas A and Zhou S: Cancer therapy with antibodies. Nat Rev Cancer. 24:399–426. 2024. View Article : Google Scholar : PubMed/NCBI | |
|
Jin H, Wang L and Bernards R: Rational combinations of targeted cancer therapies: Background, advances and challenges. Nat Rev Drug Discov. 22:213–234. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Terai M and Sato T: Individualised neoantigen cancer vaccine therapy. Lancet. 403:590–591. 2024. View Article : Google Scholar : PubMed/NCBI | |
|
Awwad SW, Serrano-Benitez A, Thomas JC, Gupta V and Jackson SP: Revolutionizing DNA repair research and cancer therapy with CRISPR-Cas screens. Nat Rev Mol Cell Biol. 24:477–494. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Wu X, Liu J, Wang J, Wang L, Lin Z, Wang X, Zhu J, Kong B, Fei J, Tang Y, et al: Senaparib as First-line maintenance therapy in advanced ovarian cancer: A randomized phase 3 trial. Nat Med. 30:1612–1621. 2024. View Article : Google Scholar : PubMed/NCBI | |
|
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 | |
|
Li Y, Zhang L, Xu T, Zhao X, Jiang X, Xiao F, Sun H and Wang L: Aberrant ENPP2 expression promotes tumor progression in multiple myeloma. Leuk Lymphoma. 63:963–974. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Hu M, Guo W, Liao Y, Xu D, Sun B, Song H, Wang T, Kuang Y, Jing B, Li K, et al: Dysregulated ENPP1 increases the malignancy of human lung cancer by inducing epithelial-mesenchymal transition phenotypes and stem cell features. Am J Cancer Res. 9:134–144. 2019.PubMed/NCBI | |
|
Bageritz J and Goidts V: Functional characterization of ENPP1 reveals a link between cell cycle progression and stem-like phenotype in glioblastoma. Mol Cell Oncol. 1:e9640282014. View Article : Google Scholar : PubMed/NCBI | |
|
Takahashi T, Old LJ and Boyse EA: Surface alloantigens of plasma cells. J Exp Med. 131:1325–1341. 1970. View Article : Google Scholar : PubMed/NCBI | |
|
Goding JW, Grobben B and Slegers H: Physiological and pathophysiological functions of the Ecto-nucleotide pyrophosphatase/phosphodiesterase family. Biochim Biophys Acta. 1638:1–19. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Stefan C, Jansen S and Bollen M: NPP-type ectophosphodiesterases: Unity in diversity. Trends Biochem Sci. 30:542–550. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Ruf N, Uhlenberg B, Terkeltaub R, Nurnberg P and Rutsch F: The mutational spectrum of ENPP1 as arising after the analysis of 23 unrelated patients with generalized arterial calcification of infancy (GACI). Hum Mutat. 25:982005. View Article : Google Scholar : PubMed/NCBI | |
|
Rutsch F, Vaingankar S, Johnson K, Goldfine I, Maddux B, Schauerte P, Kalhoff H, Sano K, Boisvert WA, Superti-Furga A and Terkeltaub R: PC-1 nucleoside triphosphate pyrophosphohydrolase deficiency in idiopathic infantile arterial calcification. Am J Pathol. 158:543–554. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Thakkar AD, Raj H, Chakrabarti D, Ravishankar Saravanan N, Muthuvelan B, Balakrishnan A and Padigaru M: Identification of gene expression signature in estrogen receptor positive breast carcinoma. Biomark Cancer. 2:1–15. 2010.PubMed/NCBI | |
|
Lau WM, Doucet M, Stadel R, Huang D, Weber KL and Kominsky SL: Enpp1: A potential facilitator of breast cancer bone metastasis. PLoS One. 8:e667522013. View Article : Google Scholar : PubMed/NCBI | |
|
Aerts I, Martin JJ, De Deyn PP, Van Ginniken C, Van Ostade X, Kockx M, Dua G and Slegers H: The expression of ecto-nucleotide pyrophosphatase/phosphodiesterase 1 (E-NPP1) is correlated with astrocytic tumor grade. Clin Neurol Neurosurg. 113:224–229. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Huhn S, Bevier M, Rudolph A, Pardini B, Naccarati A, Hein R, Hoffmeister M, Vodickova L, Novotny J, Brenner H, et al: Shared ancestral susceptibility to colorectal cancer and other nutrition related diseases. BMC Med Genet. 13:942012. View Article : Google Scholar : PubMed/NCBI | |
|
Attalla SS, Boucher J, Proud H, Taifour T, Zuo D, Sanguin-Gendreau V, Ling C, Johnson G, Li V, Luo RB, et al: HER2Delta16 engages ENPP1 to promote an Immune-Cold microenvironment in breast cancer. Cancer Immunol Res. 11:1184–1202. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Wang S, Bohnert V, Joseph AJ, Sudaryo V, Skariah G, Swinderman JT, Yu FB, Subramanyam V, Wolf DM, Lyu X, et al: ENPP1 is an innate immune checkpoint of the anticancer cGAMP-STING pathway in breast cancer. Proc Natl Acad Sci USA. 120:e23136931202023. View Article : Google Scholar : PubMed/NCBI | |
|
Duangiad P, Nutho B, Chaijarasphong T, Morales NP, Pongtharangkul T, Hamachi I, Ojida A and Wongkongkatep J: Naturally occurring quercetin and myricetin as potent inhibitors for human ectonucleotide pyrophosphatase/phosphodiesterase 1. Sci Rep. 14:1252024. View Article : Google Scholar : PubMed/NCBI | |
|
Sun Y, Chen M, Han Y, Li W, Ma X, Shi Z, Zhou Y, Xu L, Yu L, Wang Y, et al: Discovery of Pyrido[2,3-d]pyrimidin-7-one derivatives as highly potent and efficacious ectonucleotide pyrophosphatase/phosphodiesterase 1 (ENPP1) inhibitors for cancer treatment. J Med Chem. 67:3986–4006. 2024. View Article : Google Scholar : PubMed/NCBI | |
|
Ruiz-Fernandez de Cordoba B, Moreno H, Valencia K, Perurena N, Ruedas P, Walle T, Pezonaga-Torres A, Hinojosa J, Guruceaga E, Pineda-Lucena A, et al: Tumor ENPP1 (CD203a)/Haptoglobin axis exploits Myeloid-derived suppressor cells to promote Post-radiotherapy local recurrence in breast cancer. Cancer Discov. 12:1356–1377. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Li Z, He Q, Peng J, Yan Y and Fu C: Identification of downregulated Exosome-associated gene ENPP1 as a novel lipid metabolism and Immune-Associated biomarker for hepatocellular carcinoma. J Oncol. 2022:48347912022. View Article : Google Scholar : PubMed/NCBI | |
|
Kato K, Nishimasu H, Okudaira S, Mihara E, Ishitani R, Takagi J, Aoki J and Nureki O: Crystal structure of Enpp1, an extracellular glycoprotein involved in bone mineralization and insulin signaling. Proc Natl Acad Sci USA. 109:16876–16881. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Stefan C, Jansen S and Bollen M: Modulation of purinergic signaling by NPP-type ectophosphodiesterases. Purinergic Signal. 2:361–370. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Linden J, Koch-Nolte F and Dahl G: Purine release, metabolism, and signaling in the inflammatory response. Annu Rev Immunol. 37:325–347. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Li S, Yokota T, Wang P, Ten Hoeve J, Ma F, Le TM, Abt ER, Zhou Y, Wu R, Nanthavongdouangsy M, et al: Cardiomyocytes disrupt pyrimidine biosynthesis in nonmyocytes to regulate heart repair. J Clin Invest. 132:e1497112022. View Article : Google Scholar : PubMed/NCBI | |
|
Cimpean A, Stefan C, Gijsbers R, Stalmans W and Bollen M: Substrate-specifying determinants of the nucleotide pyrophosphatases/phosphodiesterases NPP1 and NPP2. Biochem J. 381:71–77. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Ferreira CR, Carpenter TO and Braddock DT: ENPP1 in blood and bone: Skeletal and soft tissue diseases induced by ENPP1 deficiency. Annu Rev Pathol. 19:507–540. 2024. View Article : Google Scholar : PubMed/NCBI | |
|
Novais EJ, Narayanan R, Canseco JA, van de Wetering K, Kepler CK, Hilibrand AS, Vaccaro AR and Risbud MV: A new perspective on intervertebral disc Calcification-from bench to bedside. Bone Res. 12:32024. View Article : Google Scholar : PubMed/NCBI | |
|
Okawa A, Nakamura I, Goto S, Moriya H, Nakamura Y and Ikegawa S: Mutation in Npps in a mouse model of ossification of the posterior longitudinal ligament of the spine. Nat Genet. 19:271–273. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Brampton C, Pomozi V, Le Corre Y, Zoll J, Kauffenstein G, Ma C, Hoffmann PR, Martin L and Le Saux O: Bone marrow-derived ABCC6 is an essential regulator of ectopic calcification in pseudoxanthoma elasticum. J Invest Dermatol. 144:1772–1783.e3. 2024. View Article : Google Scholar : PubMed/NCBI | |
|
Harmey D, Hessle L, Narisawa S, Johnson KA, Terkeltaub R and Millan JL: Concerted regulation of inorganic pyrophosphate and osteopontin by akp2, enpp1, and ank: An integrated model of the pathogenesis of mineralization disorders. Am J Pathol. 164:1199–1209. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Pillai ICL, Li S, Romay M, Lam L, Lu Y, Huang J, Dillard N, Zemanova M, Rubbi L, Wang Y, et al: Cardiac fibroblasts adopt osteogenic fates and can be targeted to attenuate pathological heart calcification. Cell Stem Cell. 20:218–232.e5. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Abate N, Carulli L, Cabo-Chan A Jr, Chandalia M, Snell PG and Grundy SM: Genetic polymorphism PC-1 K121Q and ethnic susceptibility to insulin resistance. J Clin Endocrinol Metab. 88:5927–5934. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Maddux BA and Goldfine ID: Membrane glycoprotein PC-1 inhibition of insulin receptor function occurs via direct interaction with the receptor alpha-subunit. Diabetes. 49:13–19. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Maddux BA, Sbraccia P, Kumakura S, Sasson S, Youngren J, Fisher A, Spencer S, Grupe A, Henzel W and Stewart TA: Membrane glycoprotein PC-1 and insulin resistance in non-insulin-dependent diabetes mellitus. Nature. 373:448–451. 1995. View Article : Google Scholar : PubMed/NCBI | |
|
Besic V, Stubbs RS and Hayes MT: Liver ENPP1 protein increases with remission of type 2 diabetes after gastric bypass surgery. BMC Gastroenterol. 14:2222014. View Article : Google Scholar : PubMed/NCBI | |
|
Meyre D, Bouatia-Naji N, Tounian A, Samson C, Lecoeur C, Vatin V, Ghoussaini M, Wachter C, Hercberg S, Charpentier G, et al: Variants of ENPP1 are associated with childhood and adult obesity and increase the risk of glucose intolerance and type 2 diabetes. Nat Genet. 37:863–867. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Chourabi M, Liew MS, Lim S, H'mida-Ben Brahim D, Boussofara L, Dai L, Wong PM, Foo JN, Sriha B, Robinson KS, et al: ENPP1 mutation causes recessive cole disease by altering melanogenesis. J Invest Dermatol. 138:291–300. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Eytan O, Morice-Picard F, Sarig O, Ezzedine K, Isakov O, Li Q, Ishida-Yamamoto A, Shomron N, Goldsmith T, Fuchs-Telem D, et al: Cole disease results from mutations in ENPP1. Am J Hum Genet. 93:752–757. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Nanda A, Xiong X, AlLafi A, Cesarato N and Betz RC: Cole disease due to a novel pathogenic variant in the ENPP1 gene. J Eur Acad Dermatol Venereol. 36:e559–e561. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Arima T, Sugimoto K, Taniwaki T, Maeda K, Shibata Y, Tateyama M, Karasugi T, Tokunaga T, Sueyoshi T, Hisanaga S, et al: Cartilage tissues regulate systemic aging via ectonucleotide pyrophosphatase/phosphodiesterase 1 in mice. J Biol Chem. 300:1055122024. View Article : Google Scholar : PubMed/NCBI | |
|
Wang H, Gonzalez-Garcia I, Traba J, Jain S, Conteh S, Shin DM, Qi C, Gao Y, Sun J, Kang S, et al: ATP-degrading ENPP1 is required for survival (or persistence) of Long-lived plasma cells. Sci Rep. 7:178672017. View Article : Google Scholar : PubMed/NCBI | |
|
Watanabe R, Fujita N, Sato Y, Kobayashi T, Morita M, Oike T, Miyamoto K, Kuro-O M, Michigami T, Fukumoto S, et al: Enpp1 is an Anti-aging factor that regulates Klotho under phosphate overload conditions. Sci Rep. 7:77862017. View Article : Google Scholar : PubMed/NCBI | |
|
Shi J, Hua X, Zhu B, Ravichandran S, Wang M, Nguyen C, Brodie SA, Palleschi A, Alloisio M, Pariscenti G, et al: Somatic genomics and clinical features of lung adenocarcinoma: A retrospective study. PLoS Med. 13:e10021622016. View Article : Google Scholar : PubMed/NCBI | |
|
Crabtree TD, Puri V, Chen SB, Gierada DS, Bell JM, Broderick S, Krupnick AS, Kreisel D, Patterson GA, Meyers BF, et al: Does the method of radiologic surveillance affect survival after resection of stage I non-small cell lung cancer? J Thorac Cardiovasc Surg. 149:45–52. 53.e1–3. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Han Y, Wong FC, Wang D and Kahlert C: An in silico analysis reveals an EMT-associated gene signature for predicting recurrence of Early-Stage lung adenocarcinoma. Cancer Inform. 21:117693512211007272022. View Article : Google Scholar : PubMed/NCBI | |
|
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A and Bray F: Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 71:209–249. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Cancer Genome Atlas N: Comprehensive molecular portraits of human breast tumours. Nature. 490:61–70. 2012. View Article : Google Scholar | |
|
Nolan E, Lindeman GJ and Visvader JE: Deciphering breast cancer: From biology to the clinic. Cell. 186:1708–1728. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Awolaran O, Brooks SA and Lavender V: Breast cancer osteomimicry and its role in bone specific metastasis; an integrative, systematic review of preclinical evidence. Breast. 30:156–171. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Kurosaki M, Terao M, Liu D, Zanetti A, Guarrera L, Bolis M, Gianni' M, Paroni G, Goodall GJ and Garattini E: A DOCK1 Gene-derived circular RNA is highly expressed in luminal mammary tumours and is involved in the epithelial differentiation, growth, and motility of breast cancer cells. Cancers (Basel). 13:53252021. View Article : Google Scholar : PubMed/NCBI | |
|
Ledderose C, Hefti MM, Chen Y, Bao Y, Seier T, Li L, Woehrle T, Zhang J and Junger WG: Adenosine arrests breast cancer cell motility by A3 receptor stimulation. Purinergic Signal. 12:673–685. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Attalla S, Taifour T and Muller W: Tailoring therapies to counter the divergent immune landscapes of breast cancer. Front Cell Dev Biol. 11:11117962023. View Article : Google Scholar : PubMed/NCBI | |
|
Schettini F, Barbao P, Braso-Maristany F, Galván P, Martínez D, Paré L, De Placido S, Prat A and Guedan S: Identification of cell surface targets for CAR-T cell therapies and antibody-drug conjugates in breast cancer. ESMO Open. 6:1001022021. View Article : Google Scholar : PubMed/NCBI | |
|
Manzano RG, Martinez-Navarro EM, Forteza J and Brugarolas A: Microarray phosphatome profiling of breast cancer patients unveils a complex phosphatase regulatory role of the MAPK and PI3K pathways in estrogen Receptor-negative breast cancers. Int J Oncol. 45:2250–2266. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Takahashi RU, Miyazaki H, Takeshita F, Yamamoto Y, Minoura K, Ono M, Kodaira M, Tamura K, Mori M and Ochiya T: Loss of microRNA-27b contributes to breast cancer stem cell generation by activating ENPP1. Nat Commun. 6:73182015. View Article : Google Scholar : PubMed/NCBI | |
|
Kawaguchi M, Han X, Hisada T, Nishikawa S, Kano K, Ieda N, Aoki J, Toyama T and Nakagawa H: Development of an ENPP1 fluorescence probe for inhibitor screening, cellular imaging, and prognostic assessment of malignant breast cancer. J Med Chem. 62:9254–9269. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Goswami A, Deb B, Goyal S, Gosavi A, Mali M, Martis AM, Khurana P, Gangar M, Raykar D, Mohanty A and Kulkarni A: AVA-NP-695 selectively inhibits ENPP1 to activate STING pathway and abrogate tumor metastasis in 4T1 breast cancer syngeneic mouse model. Molecules. 27:67212022. View Article : Google Scholar : PubMed/NCBI | |
|
Carozza JA, Brown JA, Bohnert V, Fernandez D, AlSaif Y, Mardjuki RE, Smith M and Li L: Structure-aided development of Small-molecule inhibitors of ENPP1, the extracellular phosphodiesterase of the immunotransmitter cGAMP. Cell Chem Biol. 27:1347–1358.e5. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Prostate cancer, . Nat Rev Dis Primers. 7:82021. View Article : Google Scholar : PubMed/NCBI | |
|
Cai M, Song XL, Li XA, Chen M, Guo J, Yang DH, Chen Z and Zhao SC: Current therapy and drug resistance in metastatic Castration-resistant prostate cancer. Drug Resist Updat. 68:1009622023. View Article : Google Scholar : PubMed/NCBI | |
|
McKinney LP, Singh R, Jordan IK, Varambally S, Dammer EB and Lillard JW Jr: Transcriptome analysis identifies tumor immune microenvironment signaling networks supporting metastatic Castration-Resistant prostate cancer. Onco (Basel). 3:81–95. 2023.PubMed/NCBI | |
|
Wang QJ, Bin C, Xue Q, Gao Q, Huang A, Wang K and Tang N: GSTZ1 sensitizes hepatocellular carcinoma cells to sorafenib-induced ferroptosis via inhibition of NRF2/GPX4 axis. Cell Death Dis. 12:4262021. View Article : Google Scholar : PubMed/NCBI | |
|
Torre LA, Trabert B, DeSantis CE, Miller KD, Samimi G, Runowicz CD, Gaudet MM, Jemal A and Siegel RL: Ovarian cancer statistics, 2018. CA Cancer J Clin. 68:284–296. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Stella J, Buers I, van de Wetering K, Hohne W, Rutsch F and Nitschke Y: Effects of different variants in the ENPP1 gene on the functional properties of ectonucleotide pyrophosphatase/phosphodiesterase family member 1. Hum Mutat. 37:1190–1201. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Martinez-Ramirez AS, Diaz-Munoz M, Battastini AM, Campos-Contreras A, Olvera A, Bergamin L, Glaser T, Jacintho Moritz CE, Ulrich H and Vázquez-Cuevas FG: Cellular migration ability is modulated by extracellular purines in ovarian carcinoma SKOV-3 Cells. J Cell Biochem. 118:4468–4478. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang QF, Li YK, Chen CY, Zhang XD, Cao L, Quan FF, Zeng X, Wang J and Liu J: Identification and validation of a prognostic index based on a metabolic-genomic landscape analysis of ovarian cancer. Biosci Rep. 40:BSR202019372020. View Article : Google Scholar : PubMed/NCBI | |
|
Wang H, Ye F, Zhou C, Cheng Q and Chen H: High expression of ENPP1 in high-grade serous ovarian carcinoma predicts poor prognosis and as a molecular therapy target. PLoS One. 16:e02457332021. View Article : Google Scholar : PubMed/NCBI | |
|
Larjavaara S, Mantyla R, Salminen T, Haapasalo H, Raitanen J, Jääskeläinen J and Auvinen A: Incidence of gliomas by anatomic location. Neuro Oncol. 9:319–325. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Tykocki T and Eltayeb M: Ten-year survival in glioblastoma. A systematic review. J Clin Neurosci. 54:7–13. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Bageritz J, Puccio L, Piro RM, Hovestadt V, Phillips E, Pankert T, Lohr J, Herold-Mende C, Lichter P and Goidts V: Stem cell characteristics in glioblastoma are maintained by the Ecto-nucleotidase E-NPP1. Cell Death Differ. 21:929–940. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD and Rich JN: Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 444:756–760. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Roa JC, Garcia P, Kapoor VK, Maithel SK, Javle M and Koshiol J: Gallbladder cancer. Nat Rev Dis Primers. 8:692022. View Article : Google Scholar : PubMed/NCBI | |
|
Montalvo-Jave EE, Rahnemai-Azar AA, Papaconstantinou D, Deloiza ME, Tsilimigras DI, Moris D, Mendoza-Barrera GE, Weber SM and Pawlik TM: Molecular pathways and potential biomarkers in gallbladder cancer: A comprehensive review. Surg Oncol. 31:83–89. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Turgeon MK and Maithel SK: Cholangiocarcinoma: A Site-specific update on the current state of surgical management and multi-modality therapy. Chin Clin Oncol. 9:42020. View Article : Google Scholar : PubMed/NCBI | |
|
Yano Y, Hayashi Y, Sano K, Nagano H, Nakaji M, Seo Y, Ninomiya T, Yoon S, Yokozaki H and Kasuga M: Expression and localization of ecto-nucleotide pyrophosphatase/phosphodiesterase I-1 (E-NPP1/PC-1) and −3 (E-NPP3/CD203c/PD-Ibeta/B10/gp130(RB13-6)) in inflammatory and neoplastic bile duct diseases. Cancer Lett. 207:139–147. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Yang C, Chen J, Yu Z, Luo J, Li X, Zhou B and Jiang N: Mining of RNA Methylation-related genes and elucidation of their molecular biology in gallbladder carcinoma. Front Oncol. 11:6218062021. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang X, Li L, Zhang M, Zhang L, Liu S, Guo J, Jiang N, Peng Q, Wang J and Ding S: Intelligent recognition of CTCs from gallbladder cancer by ultrasensitive electrochemical cytosensor and diagnosis of chemotherapeutic resistance. Biosens Bioelectron. 228:1151832023. View Article : Google Scholar : PubMed/NCBI | |
|
Ng JH, Iyer NG, Tan MH and Edgren G: Changing epidemiology of oral squamous cell carcinoma of the tongue: A global study. Head Neck. 39:297–304. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Tan Y, Wang Z, Xu M, Li B, Huang Z, Qin S, Nice EC, Tang J and Huang C: Oral squamous cell carcinomas: State of the field and emerging directions. Int J Oral Sci. 15:442023. View Article : Google Scholar : PubMed/NCBI | |
|
Romano A, Di Stasio D, Petruzzi M, Fiori F, Lajolo C, Santarelli A, Lucchese A, Serpico R and Contaldo M: Noninvasive imaging methods to improve the diagnosis of oral carcinoma and its precursors: State of the art and proposal of a Three-step diagnostic process. Cancers (Basel). 13:28642021. View Article : Google Scholar : PubMed/NCBI | |
|
Li J, Qiao Z, Li Y, Lu X, Shao T and Lv X: Bioinformatic analysis indicated that STARD4-AS1 might be a novel Ferroptosis-related biomarker of oral squamous cell carcinoma. Heliyon. 10:e331932024. View Article : Google Scholar : PubMed/NCBI | |
|
Radaic A, Kamarajan P, Cho A, Wang S, Hung GC, Najarzadegan F, Wong DT, Ton-That H, Wang CY and Kapila YL: Biological biomarkers of oral cancer. Periodontol. 2000 Dec 10–2023.doi: 10.1111/prd.12542 (Epub ahead of print). | |
|
Wu T, Jiao Z, Li Y, Su X, Yao F, Peng J, Chen W and Yang A: HPRT1 promotes chemoresistance in oral squamous cell carcinoma via activating MMP1/PI3K/Akt signaling pathway. Cancers (Basel). 14:8552022. View Article : Google Scholar : PubMed/NCBI | |
|
Liu Y, Wang Y, Li X, Jia Y, Wang J and Ao X: FOXO3a in cancer drug resistance. Cancer Lett. 540:2157242022. View Article : Google Scholar : PubMed/NCBI | |
|
Narayanan S, Cai CY, Assaraf YG, Guo HQ, Cui Q, Wei L, Huang JJ, Ashby CR Jr and Chen ZS: Targeting the ubiquitin-proteasome pathway to overcome Anti-cancer drug resistance. Drug Resist Updat. 48:1006632020. View Article : Google Scholar : PubMed/NCBI | |
|
Perez-Valencia JA, Prosdocimi F, Cesari IM, da Costa IR, Furtado C, Agostini M and Rumjanek FD: Angiogenesis and evading immune destruction are the main related transcriptomic characteristics to the invasive process of oral tongue cancer. Sci Rep. 8:20072018. View Article : Google Scholar : PubMed/NCBI | |
|
Ma C, Zhao J, Zhou L, Jia C, Shi Y, Li X, Jihu K and Zhang T: Targeting ENPP1 depletion may be a promising therapeutic strategy for treating oral squamous cell carcinoma via cytotoxic autophagy-related apoptosis. FASEB J. 38:e234202024. View Article : Google Scholar : PubMed/NCBI | |
|
Carozza JA, Cordova AF, Brown JA, AlSaif Y, Böhnert V, Cao X, Mardjuki RE, Skariah G, Fernandez D and Li L: ENPP1′s regulation of extracellular cGAMP is a ubiquitous mechanism of attenuating STING signaling. Proc Natl Acad Sci USA. 119:e21191891192022. View Article : Google Scholar : PubMed/NCBI | |
|
Sun L, Wu J, Du F, Chen X and Chen ZJ: Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science. 339:786–791. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Wu J, Sun L, Chen X, Du F, Shi H, Chen C and Chen ZJ: Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science. 339:826–830. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Harding SM, Benci JL, Irianto J, Discher DE, Minn AJ and Greenberg RA: Mitotic progression following DNA damage enables pattern recognition within micronuclei. Nature. 548:466–470. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Li L: Stimulating STING for cancer therapy: Taking the extracellular route. Cell Chem Biol. 31:851–861. 2024. View Article : Google Scholar : PubMed/NCBI | |
|
Mackenzie KJ, Carroll P, Martin CA, Murina O, Fluteau A, Simpson DJ, Olova N, Sutcliffe H, Rainger JK and Leitch A: cGAS surveillance of micronuclei links genome instability to innate immunity. Nature. 548:461–465. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Haag SM, Gulen MF, Reymond L, Gibelin A, Abrami L, Decout A, Heymann M, van der Goot FG, Turcatti G, Behrendt R and Ablasser A: Targeting STING with covalent small-molecule inhibitors. Nature. 559:269–273. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Kato K, Nishimasu H, Oikawa D, Hirano S, Hirano H, Kasuya G, Ishitani R, Tokunaga F and Nureki O: Structural insights into cGAMP degradation by Ecto-nucleotide pyrophosphatase phosphodiesterase 1. Nat Commun. 9:44242018. View Article : Google Scholar : PubMed/NCBI | |
|
Wang X, Lu X, Yan D, Zhou Y and Tan X: Development of Novel Ecto-nucleotide pyrophosphatase/phosphodiesterase 1 (ENPP1) inhibitors for tumor immunotherapy. Int J Mol Sci. 23:71042022. View Article : Google Scholar : PubMed/NCBI | |
|
Wu J, Dobbs N, Yang K and Yan N: Interferon-Independent activities of mammalian STING mediate antiviral response and tumor immune evasion. Immunity. 53:115–126.e5. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Liu FF, Shi W, Done SJ, Miller N, Pintilie M, Voduc D, Nielsen TO, Nofech-Mozes S, Chang MC, Whelan TJ, et al: Identification of a Low-Risk luminal a breast cancer cohort that may not benefit from breast radiotherapy. J Clin Oncol. 33:2035–2040. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Cho Y, Kang M, Ji SH, Jeong HJ, Jung JE, Oh DH, Park S, Park YY, Choi J, Kim S, et al: Discovery of orally bioavailable phthalazinone analogues as an ENPP1 inhibitor for STING-mediated cancer immunotherapy. J Med Chem. 66:15141–15170. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Jeong HJ, Lee HL, Kim SJ, Jeong JH, Ji SH, Kim HB, Kang M, Chung HW, Park CS, Choo H, et al: Identification of novel pyrrolopyrimidine and pyrrolopyridine derivatives as potent ENPP1 inhibitors. J Enzyme Inhib Med Chem. 37:2434–2451. 2022. View Article : Google Scholar : PubMed/NCBI | |
|
Jung JE, Jang Y, Jeong HJ, Kim SJ, Park K, Oh DH, Yu A, Park CS and Han SJ: Discovery of 3,4-dihydropyrimido[4,5-d]pyrimidin-2(1H)-one and 3,4-dihydropyrido[2,3-d]pyrimidin-2(1H)-one derivatives as novel ENPP1 inhibitors. Bioorg Med Chem Lett. 75:1289472022. View Article : Google Scholar : PubMed/NCBI | |
|
Khan Jadoon MS, Pelletier J, Sevigny J and Iqbal J: Synthesis of new class of indole acetic acid sulfonate derivatives as ectonucleotidases inhibitors. RSC Adv. 13:29496–29511. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Rohilla A, Singh AK, Koleske B, Srikrishna G and Bishai WR: Structure-based virtual screening and in vitro validation of inhibitors of cyclic dinucleotide phosphodiesterases ENPP1 and CdnP. Microbiol Spectr. 12:e02012232024. View Article : Google Scholar : PubMed/NCBI | |
|
Guan D, Fang L, Feng M, Guo S, Xie L, Chen C, Sun X, Wu Q, Yuan X, Xie Z, et al: Ecto-nucleotide pyrophosphatase/phosphodiesterase 1 inhibitors: Research progress and prospects. Eur J Med Chem. 267:1162112024. View Article : Google Scholar : PubMed/NCBI | |
|
Ruiz-Fernandez de Cordoba B, Martinez-Monge R and Lecanda F: ENPP1 immunobiology as a therapeutic target. Clin Cancer Res. 29:2184–2193. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Dillon S, Suchacki K, Hsu SN, Stephen LA, Wang R, Cawthorn WP, Stewart AJ, Nudelman F, Morton NM and Farquharson C: Ablation of Enpp6 results in transient bone hypomineralization. JBMR Plus. 5:e104392021. View Article : Google Scholar : PubMed/NCBI | |
|
Yan J, Duan W, Gao Q, Mao T, Wang M, Duan J and Li J: ENPP2 inhibitor improves proliferation in AOM/DSS-induced colorectal cancer mice via remodeling the gut barrier function and gut microbiota composition. Pharmacol Res. 195:1068772023. View Article : Google Scholar : PubMed/NCBI | |
|
Masse K, Bhamra S, Paroissin C, Maneta-Peyret L, Boue-Grabot E and Jones EA: The enpp4 ectonucleotidase regulates kidney patterning signalling networks in Xenopus embryos. Commun Biol. 4:11582021. View Article : Google Scholar : PubMed/NCBI | |
|
Thompson JA, Motzer RJ, Molina AM, Choueiri TK, Heath EI, Redman BG, Sangha RS, Ernst DS, Pili R, Kim SK, et al: Phase I trials of Anti-ENPP3 Antibody-drug conjugates in advanced refractory renal cell carcinomas. Clin Cancer Res. 24:4399–4406. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Takaya K and Kishi K: Regulation of ENPP5, a senescence-associated secretory phenotype factor, prevents skin aging. Biogerontology. 25:529–542. 2024. View Article : Google Scholar : PubMed/NCBI | |
|
Boccon-Gibod L: Etiopathogenesis of benign prostatic hypertrophy. Recent acquisitions. Ann Urol (Paris). 22:3–8. 1988.(In French). PubMed/NCBI | |
|
Onyedibe KI, Wang M and Sintim HO: ENPP1, an old enzyme with new functions, and small molecule Inhibitors-A STING in the tale of ENPP1. Molecules. 24:41922019. View Article : Google Scholar : PubMed/NCBI | |
|
Ullah S, Pelletier J, Sevigny J and Iqbal J: Synthesis and biological evaluation of arylamide sulphonate derivatives as ectonucleotide Pyrophosphatase/phosphodiesterase-1 and −3 inhibitors. ACS Omega. 7:26905–26918. 2022. View Article : Google Scholar : PubMed/NCBI |
