Lgr5 methylation in cancer stem cell differentiation and prognosis-prediction in colorectal cancer

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Su, Shasha ^a   Hong, Feng ^b   Liang, Yanling ^a   Zhou, Jieqiong ^a   Liang, Yan ^a   Chen, Kequan ^a   Wang, Xinying ^a   Wang, Zhongqiu ^a   Wang, Zhiqing ^a   Chang, Cassie ^c   Han, Weihua ^d   Gong, Wei ^a   Qin, Haitao ^a   Jiang, Bo ^a   Xiong, Huabao ^c   Peng, Liang ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b JINING MEDICAL UNIVERSITY   (China)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d Xingtai Medical College   (China)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL INTERFERING RNA; G PROTEIN COUPLED RECEPTOR; LGR5 PROTEIN, HUMAN;

ADULT; ARTICLE; CANCER DIAGNOSIS; CANCER GRADING; CANCER PROGNOSIS; CANCER STEM CELL; CANCER SURVIVAL; CANCER TISSUE; CELL DIFFERENTIATION; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; DISTANT METASTASIS; DNA METHYLATION; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENE SILENCING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LGR5 GENE; MAJOR CLINICAL STUDY; MALE; ONCOGENE; PROMOTER REGION; AGED; CANCER STAGING; COLORECTAL NEOPLASMS; GENETICS; METABOLISM; METASTASIS; MIDDLE AGED; MORTALITY; PATHOLOGY; PROGNOSIS; TUMOR CELL LINE;

ADULT; AGED; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DNA METHYLATION; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; MALE; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM METASTASIS; NEOPLASM STAGING; NEOPLASTIC STEM CELLS; PROGNOSIS; PROMOTER REGIONS, GENETIC; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84963787591     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0143513     Document Type: Article

References (52)

1. Yamamoto M, Taguchi Y, Ito-Kureha T, Semba K, Yamaguchi N, Inoue J. NF-kappaB non-cell-autonomously regulates cancer stem cell populations in the basal-like breast cancer subtype. Nature communications. 2013; 4:2299. Epub 2013/08/13. doi: 10.1038/ncomms3299 PMID: 23934482.
2. Polytarchou C, Iliopoulos D, Struhl K. An integrated transcriptional regulatory circuit that reinforces the breast cancer stem cell state. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109(36):14470-5. Epub 2012/08/22. doi: 10.1073/pnas.1212811109 PMID: 22908280; PubMed Central PMCID: PMCPMC3437881.
3. Infanger DW, Cho Y, Lopez BS, Mohanan S, Liu SC, Gursel D, et al. Glioblastoma Stem Cells Are Regulated by Interleukin-8 Signaling in a Tumoral Perivascular Niche. Cancer research. 2013. Epub 2013/10/15. doi: 10.1158/0008-5472.can-13-1355 PMID: 24121485.
4. Shan J, Shen J, Liu L, Xia F, Xu C, Duan G, et al. Nanog regulates self-renewal of cancer stem cells through the insulin-like growth factor pathway in human hepatocellular carcinoma. Hepatology. 2012; 56(3):1004-14. doi: 10.1002/hep.25745 PMID: 22473773.
5. 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):106-10. doi: 10.1038/nature05372 PMID: 17122772.
6. Zhu L, Gibson P, Currle DS, Tong Y, Richardson RJ, Bayazitov IT, et al. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature. 2009; 457(7229):603-7. PMID: 19092805. doi: 10.1038/nature07589
7. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, et al. Phenotypic characterization of human colorectal cancer stem cells. Proceedings of the National Academy of Sciences of the United States of America. 2007; 104(24):10158-63. doi: 10.1073/pnas.0703478104 PMID: 17548814; PubMed Central PMCID: PMC1891215.
8. Vermeulen L, Todaro M, de Sousa Mello F, Sprick MR, Kemper K, Perez Alea M, et al. Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105(36):13427-32. PMID: 18765800. doi: 10.1073/pnas.0805706105
9. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 2007; 449(7165):1003-7. PMID: 17934449.
10. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature. 2009; 457(7229):608-11. PMID: 19092804. doi: 10.1038/nature07602
11. Hsu SY, Kudo M, Chen T, Nakabayashi K, Bhalla A, van der Spek PJ, et al. The three subfamilies of leucine-rich repeat-containing G protein-coupled receptors (LGR): identification of LGR6 and LGR7 and the signaling mechanism for LGR7. Molecular endocrinology (Baltimore, Md. 2000; 14(8):1257-71. PMID: 10935549.
12. Barker N, van Es JH, Jaks V, Kasper M, Snippert H, Toftgard R, et al. Very long-term self-renewal of small intestine, colon, and hair follicles from cycling Lgr5+ve stem cells. Cold Spring Harbor symposia on quantitative biology. 2008; 73:351-6. PMID: 19478326. doi: 10.1101/sqb.2008.72.003
13. Jaks V, Barker N, Kasper M, van Es JH, Snippert HJ, Clevers H, et al. Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nature genetics. 2008; 40(11):1291-9. PMID: 18849992. doi: 10.1038/ng.239
14. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. 2009; 459(7244):262-5. PMID: 19329995. doi: 10.1038/nature07935
15. Yui S, Nakamura T, Sato T, Nemoto Y, Mizutani T, Zheng X, et al. Functional engraftment of colon epithelium expanded in vitro from a single adult Lgr5(+) stem cell. Nature medicine. 2012; 18(4):618-23. doi: 10.1038/nm.2695 PMID: 22406745.
16. Sato T, Clevers H. Growing self-organizing mini-guts from a single intestinal stem cell: mechanism and applications. Science. 2013; 340(6137):1190-4. doi: 10.1126/science.1234852 PMID: 23744940.
17. Barker N, Huch M, Kujala P, van de Wetering M, Snippert HJ, van Es JH, et al. Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell stem cell. 2010; 6(1):25-36. Epub 2010/01/21. doi: 10.1016/j.stem.2009.11.013 PMID: 20085740.
18. Huch M, Dorrell C, Boj SF, van Es JH, Li VS, van de Wetering M, et al. In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration. Nature. 2013; 494(7436):247-50. doi: 10.1038/nature11826 PMID: 23354049; PubMed Central PMCID: PMC3634804.
19. Morita H, Mazerbourg S, Bouley DM, Luo CW, Kawamura K, Kuwabara Y, et al. Neonatal lethality of LGR5 null mice is associated with ankyloglossia and gastrointestinal distension. Molecular and cellular biology. 2004; 24(22):9736-43. PMID: 15509778.
20. Yamamoto Y, Sakamoto M, Fujii G, Tsuiji H, Kenetaka K, Asaka M, et al. Overexpression of orphan G-protein-coupled receptor, Gpr49, in human hepatocellular carcinomas with beta-catenin mutations. Hepatology (Baltimore, Md. 2003; 37(3):528-33. PMID: 12601349.
21. Fukuma M, Tanese K, Effendi K, Yamazaki K, Masugi Y, Suda M, et al. Leucine-rich repeat-containing G protein-coupled receptor 5 regulates epithelial cell phenotype and survival of hepatocellular carcinoma cells. Experimental cell research. 2013; 319(3):113-21. doi: 10.1016/j.yexcr.2012.10.011 PMID: 23127514.
22. McClanahan T, Koseoglu S, Smith K, Grein J, Gustafson E, Black S, et al. Identification of overexpression of orphan G protein-coupled receptor GPR49 in human colon and ovarian primary tumors. Cancer biology & therapy. 2006; 5(4):419-26. PMID: 16575208.
23. Tanese K, Fukuma M, Yamada T, Mori T, Yoshikawa T, Watanabe W, et al. G-protein-coupled receptor GPR49 is up-regulated in basal cell carcinoma and promotes cell proliferation and tumor formation. The American journal of pathology. 2008; 173(3):835-43. PMID: 18688030. doi: 10.2353/ajpath.2008.071091
24. Yamanoi K, Fukuma M, Uchida H, Kushima R, Yamazaki K, Katai H, et al. Overexpression of leucinerich repeat-containing G protein-coupled receptor 5 in gastric cancer. Pathology international. 2013; 63(1):13-9. Epub 2013/01/30. doi: 10.1111/pin.12013 PMID: 23356221.
25. Hirsch D, Barker N, McNeil N, Hu Y, Camps J, McKinnon K, et al. LGR5 positivity defines stem-like cells in colorectal cancer. Carcinogenesis. 2013. Epub 2013/11/28. doi: 10.1093/carcin/bgt377 PMID: 24282287.
26. Rubinfeld B, Albert I, Porfiri E, Munemitsu S, Polakis P. Loss of beta-catenin regulation by the APC tumor suppressor protein correlates with loss of structure due to common somatic mutations of the gene. Cancer research. 1997; 57(20):4624-30. Epub 1997/10/23. PMID: 9377578.
27. Garcia MI, Ghiani M, Lefort A, Libert F, Strollo S, Vassart G. LGR5 deficiency deregulates Wnt signaling and leads to precocious Paneth cell differentiation in the fetal intestine. Developmental biology. 2009;331(1):58-67. Epub 2009/04/28. doi: 10.1016/j.ydbio.2009.04.020 PMID: 19394326.
28. de Lau W, Barker N, Low TY, Koo BK, Li VS, Teunissen H, et al. Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling. Nature. 2011; 476(7360):293-7. doi: 10.1038/nature10337 PMID: 21727895.
29. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. The New England journal of medicine. 2003; 349(21):2042-54. Epub 2003/11/25. doi: 10.1056/NEJMra023075 PMID: 14627790.
30. Jones PA, Baylin SB. The epigenomics of cancer. Cell. 2007; 128(4):683-92. doi: 10.1016/j.cell.2007.01.029 PMID: 17320506.
31. Ung M, Ma X, Johnson KC, Christensen BC, Cheng C. Effect of estrogen receptor alpha binding on functional DNA methylation in breast cancer. Epigenetics: official journal of the DNA Methylation Society. 2014; 9(4). Epub 2014/01/18. PMID: 24434785.
32. Mancikova V, Buj R, Castelblanco E, Inglada-Perez L, Diez A, de Cubas AA, et al. DNA methylation profiling of well-differentiated thyroid cancer uncovers markers of recurrence free survival. International journal of cancer Journal international du cancer. 2013. Epub 2014/01/03. doi: 10.1002/ijc.28703 PMID: 24382797.
33. Raggi C, Factor VM, Seo D, Holczbauer A, Gillen MC, Marquardt JU, et al. Epigenetic reprogramming modulates malignant properties of human liver cancer. Hepatology. 2014. Epub 2014/01/23. doi: 10.1002/hep.27026 PMID: 24449497.
34. de Sousa EMF, Colak S, Buikhuisen J, Koster J, Cameron K, de Jong JH, et al. Methylation of cancer-stem-cell-associated Wnt target genes predicts poor prognosis in colorectal cancer patients. Cell stem cell. 2011; 9(5):476-85. doi: 10.1016/j.stem.2011.10.008 PMID: 22056143.
35. Li LC, Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics. 2002; 18(11):1427-31. Epub 2002/11/09. PMID: 12424112.
36. Spizzo G, Gastl G, Obrist P, Fong D, Haun M, Grunewald K, et al. Methylation status of the Ep-CAM promoter region in human breast cancer cell lines and breast cancer tissue. Cancer letters. 2007; 246(1-2):253-61. doi: 10.1016/j.canlet.2006.03.002 PMID: 16624485.
37. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, et al. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell. 2007; 131(6):1109-23. doi: 10.1016/j.cell.2007.10.054 PMID: 18083101.
38. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, et al. Identification and expansion of human colon-cancer-initiating cells. Nature. 2007; 445(7123):111-5. doi: 10.1038/nature05384 PMID: 17122771.
39. Ghods AJ, Irvin D, Liu G, Yuan X, Abdulkadir IR, Tunici P, et al. Spheres isolated from 9L gliosarcoma rat cell line possess chemoresistant and aggressive cancer stem-like cells. Stem cells. 2007; 25(7):1645-53. Epub 2007/04/07. doi: 10.1634/stemcells.2006-0624 PMID: 17412894.
40. Su N, Peng L, Xia B, Zhao Y, Xu A, Wang J, et al. Lyn is involved in CD24-induced ERK1/2 activation in colorectal cancer. Molecular cancer. 2012; 11:43. doi: 10.1186/1476-4598-11-43 PMID: 22731636; PubMed Central PMCID: PMC3464950.
41. Yeung TM, Gandhi SC, Wilding JL, Muschel R, Bodmer WF. Cancer stem cells from colorectal cancer-derived cell lines. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(8):3722-7. doi: 10.1073/pnas.0915135107 PMID: 20133591; PubMed Central PMCID: PMC2840416.
42. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J, et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nature genetics. 2007; 39(2):232-6. doi: 10.1038/ng1950 PMID: 17200670.
43. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nature genetics. 2009; 41(2):178-86. doi: 10.1038/ng.298 PMID: 19151715
44. Yi JM, Tsai HC, Glockner SC, Lin S, Ohm JE, Easwaran H, et al. Abnormal DNA methylation of CD133 in colorectal and glioblastoma tumors. Cancer research. 2008; 68(19):8094-103. doi: 10.1158/0008-5472.CAN-07-6208 PMID: 18829568; PubMed Central PMCID: PMC2744404.
45. Gopisetty G, Xu J, Sampath D, Colman H, Puduvalli VK. Epigenetic regulation of CD133/PROM1 expression in glioma stem cells by Sp1/myc and promoter methylation. Oncogene. 2013; 32(26):3119-29. doi: 10.1038/onc.2012.331 PMID: 22945648; PubMed Central PMCID: PMC3820114.
46. Chen KL, Pan F, Jiang H, Chen JF, Pei L, Xie FW, et al. Highly enriched CD133(+)CD44(+) stem-like cells with CD133(+)CD44(high) metastatic subset in HCT116 colon cancer cells. Clinical & experimental metastasis. 2011; 28(8):751-63. doi: 10.1007/s10585-011-9407-7 PMID: 21750907.
47. Woodson K, O'Reilly KJ, Ward DE, Walter J, Hanson J, Walk EL, et al. CD44 and PTGS2 methylation are independent prognostic markers for biochemical recurrence among prostate cancer patients with clinically localized disease. Epigenetics: official journal of the DNA Methylation Society. 2006; 1(4):183-6. Epub 2007/11/14. PMID: 17998819.
48. Tabu K, Sasai K, Kimura T, Wang L, Aoyanagi E, Kohsaka S, et al. Promoter hypomethylation regulates CD133 expression in human gliomas. Cell research. 2008; 18(10):1037-46. doi: 10.1038/cr.2008.270 PMID: 18679414.
49. Hochedlinger K, Yamada Y, Beard C, Jaenisch R. Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell. 2005; 121(3):465-77. doi: 10.1016/j.cell.2005.02.018 PMID: 15882627.
50. Hammoud SS, Cairns BR, Jones DA. Epigenetic regulation of colon cancer and intestinal stem cells. Current opinion in cell biology. 2013; 25(2):177-83. doi: 10.1016/j.ceb.2013.01.007 PMID: 23402869; PubMed Central PMCID: PMC3615052.
51. Liu Z, Dai W, Jiang L, Cheng Y. Over-expression of LGR5 correlates with poor survival of colon cancer in mice as well as in patients. Neoplasma. 2014; 61(2):177-85. doi: 10.4149/neo-2014-016 PMID: 24063790.
52. Chen Q, Zhang X, Li WM, Ji YQ, Cao HZ, Zheng P. Prognostic value of LGR5 in colorectal cancer: a meta-analysis. PloS one. 2014; 9(9):e107013. doi: 10.1371/journal.pone.0107013 PMID: 25192390; PubMed Central PMCID: PMC4156381.