Inhibitor of DNA binding 1 (Id1) mediates stemness of colorectal cancer cells through the Id1-c-Myc-PLAC8 axis via the Wnt/β-catenin and Shh signaling pathways

References

• Brenner H, Kloor M, Pox CP. Colorectal cancer. Lancet. 2014;383(9927):1490–1502. doi:10.1016/S0140-6736(13)61612-824225001
   PubMed Web of Science ®Google Scholar
• Siegel RL, Miller KD, Fedewa SA, et al. Colorectal cancer statistics, 2017. CA Cancer J Clin. 2017;67(3):177–193. doi:10.3322/caac.2139528248415
   PubMed Web of Science ®Google Scholar
• Ciombor KK, Wu C, Goldberg RM. Recent therapeutic advances in the treatment of colorectal cancer. Annu Rev Med. 2015;66:83–95. doi:10.1146/annurev-med-051513-10253925341011
   PubMed Web of Science ®Google Scholar
• Bashir B, Snook AE. Immunotherapy regimens for metastatic colorectal carcinomas. Hum Vaccin Immunother. 2018;14(2):250–254. doi:10.1080/21645515.2017.139724429083978
   PubMed Web of Science ®Google Scholar
• Takayama T, Miyanishi K, Hayashi T, Sato Y, Niitsu Y. Colorectal cancer: genetics of development and metastasis. J Gastroenterol. 2006;41(3):185–192. doi:10.1007/s00535-006-1801-616699851
   PubMed Web of Science ®Google Scholar
• Mathonnet M, Perraud A, Christou N, et al. Hallmarks in colorectal cancer: angiogenesis and cancer stem-like cells. World J Gastroenterol. 2014;20(15):4189–4196. doi:10.3748/wjg.v20.i15.418924764657
   PubMed Web of Science ®Google Scholar
• Crea F, Nobili S, Paolicchi E, et al. Epigenetics and chemoresistance in colorectal cancer: an opportunity for treatment tailoring and novel therapeutic strategies. Drug Resist Updat. 2011;14(6):280–296. doi:10.1016/j.drup.2011.08.00121955833
   PubMed Web of Science ®Google Scholar
• Fanale D, Castiglia M, Bazan V, Russo A. Involvement of non-coding RNAs in chemo- and radioresistance of colorectal cancer. Adv Exp Med Biol. 2016;937:207–228.27573902
   PubMed Web of Science ®Google Scholar
• Debeb BG 1, Xu W, Woodward WA. Radiation resistance of breast cancer stem cells: understanding the clinical framework. J Mammary Gland Biol Neoplasia. 2009;14(1):11–17. doi:10.1007/s10911-009-9114-z19252973
   PubMed Web of Science ®Google Scholar
• Crea F, Danesi R, Farrar WL. Cancer stem cell epigenetics and chemoresistance. Epigenomics. 2009;1(1):63–79. doi:10.2217/epi.09.422122637
   PubMed Web of Science ®Google Scholar
• Hittelman WN, Liao Y, Wang L, Milas L. Are cancer stem cells radioresistant? Future Oncol. 2010;6(10):1563–1576. doi:10.2217/fon.10.12121062156
   PubMed Web of Science ®Google Scholar
• Pranatharthi A, Ross C, Srivastava S. Cancer stem cells and radioresistance: rho/ROCK pathway plea attention. Stem Cells Int. 2016;2016:5785786. doi:10.1155/2016/124365927597870
   PubMed Web of Science ®Google Scholar
• Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell. 1990;61(1):49–59. doi:10.1016/0092-8674(90)90214-Y2156629
   PubMed Web of Science ®Google Scholar
• Ling F, Kang B, Sun XH. Id proteins: small molecules, mighty regulators. Curr Top Dev Biol. 2014;110:189–216.25248477
   PubMed Web of Science ®Google Scholar
• Lasorella A, Uo T, Iavarone A. Id proteins at the cross-road of development and cancer. Oncogene. 2001;20(58):8326–8333. doi:10.1038/sj.onc.120509311840325
   PubMed Web of Science ®Google Scholar
• Ling MT, Wang X, Zhang X, Wong YC. The multiple roles of Id-1 in cancer progression. Differentiation. 2006;74(9–10):481–487. doi:10.1111/j.1432-0436.2006.00083.x17177845
   PubMed Web of Science ®Google Scholar
• Schoppmann SF, Schindl M, Bayer G, et al. Overexpression of Id-1 is associated with poor clinical outcome in node negative breast cancer. Int J Cancer. 2003;104(6):677–682. doi:10.1002/ijc.1100912640673
   PubMed Web of Science ®Google Scholar
• Forootan SS, Wong YC, Dodson A, et al. Increased Id-1 expression is significantly associated with poor survival of patients with prostate cancer. Human Pathol. 2007;38(9):1321–1329. doi:10.1016/j.humpath.2007.02.01117599389
   PubMed Web of Science ®Google Scholar
• Yang HY, Liu HL, Liu GY, et al. Expression and prognostic values of Id-1 and Id-3 in gastric adenocarcinoma. J Surg Res. 2011;167(2):258–266. doi:10.1016/j.jss.2009.08.00620080245
   PubMed Web of Science ®Google Scholar
• Rothschild SI, Kappeler A, Ratschiller D, et al. The stem cell gene “inhibitor of differentiation 1” (ID1) is frequently expressed in non-small cell lung cancer. Lung Cancer. 2011;71(3):306–311. doi:10.1016/j.lungcan.2010.06.01820709421
   PubMed Web of Science ®Google Scholar
• Luo KJ, Wen J, Xie X, et al. Prognostic relevance of Id-1 expression in patients with resectable esophageal squamous cell carcinoma. Ann Thorac Surg. 2012;93(5):1682–1688. doi:10.1016/j.athoracsur.2012.01.11422480390
   PubMed Web of Science ®Google Scholar
• Zhao ZR, Zhang ZY, Zhang H, Jiang L, Wang MW, Sun XF. Overexpression of Id-1 protein is a marker in colorectal cancer progression. Oncol Rep. 2008;19(2):419–424.18202790
   PubMed Web of Science ®Google Scholar
• Li L, Wei X, Wu B, Xiao Y, Yin M, Yang Q. siRNA-mediated knockdown of ID1 disrupts Nanog- and Oct-4-mediated cancer stem cell-likeness and resistance to chemotherapy in gastric cancer cells. Oncol Lett. 2017;13(5):3014–3024. doi:10.3892/ol.2017.582828529558
   PubMed Web of Science ®Google Scholar
• Przybyła T, Sakowicz-Burkiewicz M, Maciejewska I, Bielarczyk H, Pawełczyk T. Suppression of ID1 expression in colon cancer cells increases sensitivity to 5-fluorouracil. Acta Biochim Pol. 2017;64(2):315–322. doi:10.18388/abp.2016_142128510612
   PubMed Web of Science ®Google Scholar
• Ponz-Sarvisé M, Nguewa PA, Pajares MJ, et al. Inhibitor of differentiation-1 as a novel prognostic factor in NSCLC patients with adenocarcinoma histology and its potential contribution to therapy resistance. Clin Cancer Res. 2011;17(12):4155–4166. doi:10.1158/1078-0432.CCR-10-338121540238
   PubMed Web of Science ®Google Scholar
• Hu H, Han HY, Wang YL, et al. The role of Id-1 in chemosensitivity and epirubicin-induced apoptosis in bladder cancer cells. Oncol Rep. 2009;21(4):1053–1059. doi:10.3892/or_0000032319288008
   PubMed Web of Science ®Google Scholar
• Jung S, Park RH, Kim S, et al. Id proteins facilitate self-renewal and proliferation of neural stem cells. Stem Cells Dev. 2010;19(6):831–841. doi:10.1089/scd.2009.029019757990
   PubMed Web of Science ®Google Scholar
• Romero-Lanman EE, Pavlovic S, Amlani B, Chin Y, Benezra R. Id1 maintains embryonic stem cell self-renewal by up-regulation of Nanog and repression of Brachyury expression. Stem Cells Dev. 2012;21(3):384–393. doi:10.1089/scd.2011.042822013995
   PubMed Web of Science ®Google Scholar
• O’Brien CA, Kreso A, Ryan P, et al. ID1 and ID3 regulate the self-renewal capacity of human colon cancer-initiating cells through p21. Cancer Cell. 2012;21(6):777–792. doi:10.1016/j.ccr.2012.04.03622698403
   PubMed Web of Science ®Google Scholar
• Ke J, Wu X, Wu X, et al. A subpopulation of CD24+ cells in colon cancer cell lines possess stem cell characteristics. Neoplasma. 2012;59(3):282–288. doi:10.4149/neo_2012_03622329848
   PubMed Web of Science ®Google Scholar
• Gil J, Stembalska A, Pesz KA, Sasiadek MM. Cancer stem cells: the theory and perspectives in cancer therapy. J Appl Genet. 2008;49(2):193–199. doi:10.1007/BF0319561218436993
   PubMed Web of Science ®Google Scholar
• Spillane JB, Henderson MA. Cancer stem cells: a review. ANZ J Surg. 2007;77(6):464–468. doi:10.1111/j.1445-2197.2007.04156.x17501888
   PubMed Web of Science ®Google Scholar
• Katoh Y, Katoh M. Comparative genomics on PROM1 gene encoding stem cell marker CD133. Int J Mol Med. 2007;19(6):967–970.17487431
   PubMed Web of Science ®Google Scholar
• MacDonald BT, Tamai K, He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell. 2009;17(1):9–26. doi:10.1016/j.devcel.2009.06.01619619488
   PubMed Web of Science ®Google Scholar
• Botchkina G. Colon cancer stem cells–from basic to clinical application. Cancer Lett. 2013;338(1):127–140. doi:10.1016/j.canlet.2013.03.03422537805
   PubMed Web of Science ®Google Scholar
• O’Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445(7123):106–110. doi:10.1038/nature0537217122772
   PubMed Web of Science ®Google Scholar
• Ricci-Vitiani L, Lombardi DG, Pilozzi E, et al. Identification and expansion of human colon-cancer-initiating cells. Nature. 2007;445(7123):111–115. doi:10.1038/nature0538417122771
   PubMed Web of Science ®Google Scholar
• Chen S, Song X, Chen Z, et al. Cd133 expression and the prognosis of colorectal cancer: a systematic review and meta-analysis. PLoS One. 2013;8(2):e56380. doi:10.1371/journal.pone.005638023409180
   PubMed Web of Science ®Google Scholar
• Yeung TM, Gandhi SC, Wilding JL, Muschel R, Bodmer WF. Cancer stem cells from colorectal cancer-derived cell lines. Proc Natl Acad Sci U S A. 2010;107(8):3722–3727. doi:10.1073/pnas.091009710720133591
   PubMed Web of Science ®Google Scholar
• Benoit YD. Identification of novel molecules targeting cancer stem cells. Methods Mol Biol. 2018;1765:333–347.29589319
   PubMedGoogle Scholar
• Karlsson H, Fryknas M, Larsson R, Nygren P. Loss of cancer drug activity in colon cancer hct-116 cells during spheroid formation in a new 3-d spheroid cell culture system. Exp Cell Res. 2012;318(13):1577–1585. doi:10.1016/j.yexcr.2012.03.02622487097
   PubMed Web of Science ®Google Scholar
• Zhang X, Ling MT, Wang X, Wong YC. Inactivation of id-1 in prostate cancer cells: a potential therapeutic target in inducing chemosensitization to taxol through activation of jnk pathway. Int J Cancer. 2006;118(8):2072–2081. doi:10.1002/ijc.2159216287090
   PubMed Web of Science ®Google Scholar
• Geng H, Rademacher BL, Pittsenbarger J, et al. Id1 enhances docetaxel cytotoxicity in prostate cancer cells through inhibition of p21. Cancer Res. 2010;70(8):3239–3248. doi:10.1158/0008-5472.CAN-09-318620388787
   PubMed Web of Science ®Google Scholar
• Kawamoto H, Yuasa T, Kubota Y, et al. Characteristics of CD133+ human colon cancer SW620 cells. Cell Transplant. 2010;19(6):857–864. doi:10.3727/096368910X50898820587144
   PubMed Web of Science ®Google Scholar
• Sgambato A, Puglisi MA, Errico F, et al. Post-translational modulation of CD133 expression during sodium butyrate-induced differentiation of HT29 human colon cancer cells: implications for its detection. J Cell Physiol. 2010;224(1):234–241.20333645
   PubMed Web of Science ®Google Scholar
• Wan L, Pantel K, Kang Y. Tumor metastasis: moving new biological insights into the clinic. Nat Med. 2013;19(11):1450–1464.24202397
   PubMed Web of Science ®Google Scholar
• Scheel C, Weinberg RA. Cancer stem cells and epithelial-mesenchymal transition: concepts and molecular links. Semin Cancer Biol. 2012;22(5–6):396–403. doi:10.1016/j.semcancer.2012.04.00122554795
   PubMed Web of Science ®Google Scholar
• Asirvatham AJ, Carey JP, Chaudhary J. ID1-, ID2-, and ID3-regulated gene expression in E2A positive or negative prostate cancer cells. Prostate. 2007;67(13):1411–1420. doi:10.1002/pros.2063317639499
   PubMed Web of Science ®Google Scholar
• Gumireddy K, Li A, Gimotty PA, et al. KLF17 is a negative regulator of epithelial-mesenchymal transition and metastasis in breast cancer. Nat Cell Biol. 2009;11(11):1297–1304. doi:10.1038/ncb182619801974
   PubMed Web of Science ®Google Scholar
• Kühl SJ, Kühl M. On the role of Wnt/β-catenin signaling in stem cells. Biochim Biophys Acta. 2013;1830(2):2297–2306. doi:10.1016/j.bbagen.2012.08.01022986148
   PubMed Web of Science ®Google Scholar
• Lee JY, Kang MB, Jang SH, et al. Id-1 activates Akt-mediated Wnt signaling and p27(Kip1) phosphorylation through PTEN inhibition. Oncogene. 2009;28(6):824–831. doi:10.1038/onc.2008.45119079342
   PubMed Web of Science ®Google Scholar
• Zhu L, Gibson P, Currle DS, et al. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature. 2009;457(7229):603–607. doi:10.1038/nature0758919092805
   PubMed Web of Science ®Google Scholar
• Yamashita T, Ji J, Budhu A, et al. Epcam-positive hepatocellular carcinoma cells are tumor-initiating cells with stem/progenitor cell features. Gastroenterology. 2009;136(3):1012–1024. doi:10.1053/j.gastro.2008.11.04919150350
   PubMed Web of Science ®Google Scholar
• Yook JI, Li XY, Ota I, et al. A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells. Nat Cell Biol. 2006;8(12):1398–1406. doi:10.1038/ncb150817072303
   PubMed Web of Science ®Google Scholar