Intestinal stem cell marker LGR5 expression during gastric carcinogenesis

World Journal of Gastroenterology

Volumn 19, Issue 46, 2013, Pages 8714-8721

  Zheng, Zhi Xue ^a   Sun, Yu ^a   Bu, Zhao De ^a   Zhang, Lian Hai ^a   Li, Zi Yu ^a   Wu, Ai Wen ^a   Wu, Xiao Jiang ^a   Wang, Xiao Hong ^b   Cheng, Xiao Jing ^b   Xing, Xiao Fang ^b   Du, Hong ^a   Ji, Jia Fu ^a  

^a Department of Biochemistry and Molecular BiologyCancer Hospital of Peking University   (China)

^b PEKING UNIVERSITY CANCER HOSPITAL AND INSTITUTE   (China)

Author keywords

Cancer stem cell; Gastric cancer; Intestinal metaplasia; Leucine rich repeat containing G proteincoupled receptor 5; Tumorigenesis

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; LEUCINE-RICH REPEAT CONTAINING G PROTEIN-COUPLED RECEPTOR 5; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CANCER GROWTH; CANCER STAGING; CANCER STEM CELL; CARCINOGENESIS; CONTROLLED STUDY; DYSPLASIA; FEMALE; FOLLOW UP; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTESTINE METAPLASIA; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; PROTEIN EXPRESSION; STOMACH ADENOCARCINOMA; STOMACH CANCER; TUMOR BIOPSY; TUMOR DIFFERENTIATION; VERY ELDERLY;

CANCER STEM CELL; GASTRIC CANCER; INTESTINAL METAPLASIA; LEUCINE-RICH REPEAT-CONTAINING G PROTEIN-COUPLED RECEPTOR 5; TUMORIGENESIS;

ADENOCARCINOMA; BIOPSY; CELL DEDIFFERENTIATION; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; LIVER NEOPLASMS; MALE; METAPLASIA; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM RECURRENCE, LOCAL; NEOPLASM STAGING; NEOPLASTIC STEM CELLS; PROGNOSIS; RECEPTORS, G-PROTEIN-COUPLED; STOMACH NEOPLASMS; TUMOR MARKERS, BIOLOGICAL; UP-REGULATION;

EID: 84890392785     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v19.i46.8714     Document Type: Article

References (47)

1. Filomena A, Saieva C, Lucchetti V, Santacroce F, Falorni P, Francini V, Carrieri P, Zini E, Ridolfi B, Belli P, Orsini B, Mandi P, Palli D, Scheggi S. Gastric cancer surveillance in a high-risk population in tuscany (Central Italy): preliminary results. Digestion 2011; 84: 70-77 PMID: 21494036 DOI: 10.1159/000322689]
2. McCune K, Bhat-Nakshatri P, Thorat MA, Nephew KP, Badve S, Nakshatri H. Prognosis of hormone-dependent breast cancers: implications of the presence of dysfunctional transcriptional networks activated by insulin via the immune transcription factor T-bet. Cancer Res 2010; 70: 685-696 PMID: 20068169 DOI: 10.1158/0008-5472]
3. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process--First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 1992; 52: 6735-6740 PMID: 1458460]
4. Kemper K, Grandela C, Medema JP. Molecular identification and targeting of colorectal cancer stem cells. Oncotarget 2010; 1: 387-395 PMID: 21311095]
5. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, Pierotti MA, Daidone MG. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 2005; 65: 5506-5511 PMID: 15994920]
6. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, Conticello C, Ruco L, Peschle C, De Maria R. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008; 15: 504-514 PMID: 18049477 DOI: 10.1038/sj.cdd]
7. Curley MD, Therrien VA, Cummings CL, Sergent PA, Koulouris CR, Friel AM, Roberts DJ, Seiden MV, Scadden DT, Rueda BR, Foster R. CD133 expression defines a tumor initiating cell population in primary human ovarian cancer. Stem Cells 2009; 27: 2875-2883 PMID: 19816957 DOI: 10.1002/ stem.236]
8. Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, Ngai P, Chu PW, Lam CT, Poon RT, Fan ST. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 2008; 13: 153-166 PMID: 18242515 DOI: 10.1016/j.ccr.2008.01.013]
9. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 2005; 65: 10946-10951 PMID: 16322242 DOI: 10.1158/0008-5472.CAN-05-2018]
10. Li C, Lee CJ, Simeone DM. Identification of human pancreatic cancer stem cells. Methods Mol Biol 2009; 568: 161-173 PMID: 19582426 DOI: 10.1007/978-1-59745-280-9_10]
11. Monzani E, Facchetti F, Galmozzi E, Corsini E, Benetti A, Cavazzin C, Gritti A, Piccinini A, Porro D, Santinami M, Invernici G, Parati E, Alessandri G, La Porta C.A. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer 2007; 43: 935-946 PMID: 17320377 DOI: 10.16/j.ejca.2007.01.017]
12. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821-5828 PMID: 14522905]
13. Vermeulen L, Todaro M, de Sousa Mello F, Sprick MR, Kemper K, Perez Alea M, Richel DJ, Stassi G, Medema JP. Singlecell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc Natl Acad Sci USA 2008; 105: 13427-13432 PMID: 18765800 DOI: 10.1073/pnas.0805706105]
14. Pinson KI, Brennan J, Monkley S, Avery BJ, Skarnes WC. An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 2000; 407: 535-538 PMID: 11029008 DOI: 10.1038/35035124]
15. Van der Flier LG, Sabates-Bellver J, Oving I, Haegebarth A, De Palo M, Anti M, Van Gijn ME, Suijkerbuijk S, Van de Wetering M, Marra G, Clevers H. The Intestinal Wnt/ TCF Signature. Gastroenterology 2007; 132: 628-632 PMID: 17320548 DOI: 10.1053/j.gastro.2006.08.039]
16. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, Wu L, Lindeman GJ, Visvader JE. Generation of a functional mammary gland from a single stem cell. Nature 2006; 439: 84-88 PMID: 16397499 DOI: 10.1038/nature04372]
17. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, Danenberg E, Clarke AR, Sansom OJ, Clevers H. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009; 457: 608-611 PMID: 19092804 DOI: 10.1038/nature07935]
18. Brabletz S, Schmalhofer O, Brabletz T. Gastrointestinal stem cells in development and cancer. J Pathol 2009; 217: 307-317 PMID: 19031475 DOI: 10.1002/path.2475]
19. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, Clevers H. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007; 449: 1003-1007 PMID: 17934449 DOI: 10.1038/nature06196]
20. Becker L, Huang Q, Mashimo H. Lgr5, an intestinal stem cell marker, is abnormally expressed in Barrett's esophagus and esophageal adenocarcinoma. Dis Esophagus 2010; 23: 168-174 PMID: 19549212 DOI: 10.1111/j.1442-2050.2009.00979.x]
21. Takeda K, Kinoshita I, Shimizu Y, Matsuno Y, Shichinohe T, Dosaka-Akita H. Expression of LGR5, an intestinal stem cell marker, during each stage of colorectal tumorigenesis. Anticancer Res 2011; 31: 263-270 PMID: 21273608]
22. Uchida H, Yamazaki K, Fukuma M, Yamada T, Hayashida T, Hasegawa H, Kitajima M, Kitagawa Y, Sakamoto M. Overexpression of leucine-rich repeat-containing G protein-coupled receptor 5 in colorectal cancer. Cancer Sci 2010; 101: 1731-1737 PMID: 20384634]
23. Kleist B, Xu L, Li G, Kersten C. Expression of the adult intestinal stem cell marker Lgr5 in the metastatic cascade of colorectal cancer. Int J Clin Exp Pathol 2011; 4: 327-335 PMID: 21577318]
24. Karam SM, Li Q, Gordon JI. Gastric epithelial morphogenesis in normal and transgenic mice. Am J Physiol 1997; 272: G1209-G1220 PMID: 9176232]
25. Karam SM, Straiton T, Hassan WM, Leblond CP. Defining epithelial cell progenitors in the human oxyntic mucosa. Stem Cells 2003; 21: 322-336 PMID: 12743327 DOI: 10.1634/stem]
26. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, Clevers H. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 2011; 469: 415-418 PMID: 21113151 DOI: 10.1038/nature]
27. Hsu SY, Liang SG, Hsueh AJ. Characterization of two LGR genes homologous to gonadotropin and thyrotropin receptors with extracellular leucine-rich repeats and a G proteincoupled, seven-transmembrane region. Mol Endocrinol 1998; 12: 1830-1845 PMID: 9849958]
28. McDonald T, Wang R, Bailey W, Xie G, Chen F, Caskey CT, Liu Q. Identification and cloning of an orphan G proteincoupled receptor of the glycoprotein hormone receptor subfamily. Biochem Biophys Res Commun 1998; 247: 266-270 PMID: 9642114]
29. Rugge M, Farinati F, Baffa R, Sonego F, Di Mario F, Leandro G, Valiante F. Gastric epithelial dysplasia in the natural history of gastric cancer: a multicenter prospective follow-up study. Interdisciplinary Group on Gastric Epithelial Dysplasia. Gastroenterology 1994; 107: 1288-1296 PMID: 7926493]
30. Sun X, Jackson L, Dey SK, Daikoku T. In pursuit of leucinerich repeat-containing G protein-coupled receptor-5 regulation and function in the uterus. Endocrinology 2009; 150: 5065-5073 PMID: 19797400 DOI: 10.1210/en.2009-0690]
31. McClanahan T, Koseoglu S, Smith K, Grein J, Gustafson E, Black S, Kirschmeier P, Samatar AA. Identification of overexpression of orphan G protein-coupled receptor GPR49 in human colon and ovarian primary tumors. Cancer Biol Ther 2006; 5: 419-426 PMID: 16575208]
32. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008; 8: 755-768 PMID: 18784658]
33. Appelman HD. What is dysplasia in the gastrointestinal tract? Arch Pathol Lab Med 2005; 129: 170-173 PMID: 15679413]
34. Tosi P, Filipe MI, Luzi P, Miracco C, Santopietro R, Lio R, Sforza V, Barbini P. Gastric intestinal metaplasia type III cases are classified as low-grade dysplasia on the basis of morphometry. J Pathol 1993; 169: 73-78 PMID: 8433217 DOI: 10.1002/path.1711690112]
35. May R, Riehl TE, Hunt C, Sureban SM, Anant S, Houchen CW. Identification of a novel putative gastrointestinal stem cell and adenoma stem cell marker, doublecortin and CaM kinase-like-1, following radiation injury and in adenomatous polyposis coli/multiple intestinal neoplasia mice. Stem Cells 2008; 26: 630-637 PMID: 18055444 DOI: 10.1634/stemcells.2007-0621]
36. Sureban SM, May R, Ramalingam S, Subramaniam D, Natarajan G, Anant S, Houchen CW. Selective blockade of DCAMKL-1 results in tumor growth arrest by a Let-7a MicroRNA-dependent mechanism. Gastroenterology 2009; 137: 649-59, 659.e1-2 PMID: 19445940 DOI: 10.1053/j]
37. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Opinion: migrating cancer stem cells an integrated concept of malignant tumour progression. Nat Rev Cancer 2005; 5: 744-749 PMID: 16148886 DOI: 10.1038/nrc1694]
38. Chisholm AD. Gastrulation: Wnts signal constriction. Curr Biol 2006; 16: R874-R876 PMID: 17055968 DOI: 10.1016/ j.cub.2006.09.028]
39. Labelle M, Begum S, Hynes RO. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymallike transition and promotes metastasis. Cancer Cell 2011; 20: 576-590 PMID: 22094253 DOI: 10.1016/j.ccr.2011.09.009]
40. Fessler E, Dijkgraaf FE, De Sousa E, Melo F, Medema JP. Cancer stem cell dynamics in tumor progression and metastasis: Is the microenvironment to blame? Cancer Lett 2013; 341: 97-104 PMID: 23089245 DOI: 10.1016/j.canlet.2012.10.015]
41. de Lau W, Barker N, Low TY, Koo BK, Li VS, Teunissen H, Kujala P, Haegebarth A, Peters PJ, van de Wetering M, Stange DE, van Es JE, Guardavaccaro D, Schasfoort RB, Mohri Y, Nishimori K, Mohammed S, Heck AJ, Clevers H. Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling. Nature 2011; 476: 293-297 PMID: 21727895]
42. Vermeulen L, De Sousa E, Melo F, van der Heijden M, Cameron K, de Jong JH, Borovski T, Tuynman JB, Todaro M, Merz C, Rodermond H, Sprick MR, Kemper K, Richel DJ, Stassi G, Medema JP. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 2010; 12: 468-476 PMID: 20418870 DOI: 10.1038/ncb2048]
43. Fodde R, Brabletz T. Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol 2007; 19: 150-158 PMID: 17306971 DOI: 10.1016/j.ceb.2007.02]
44. Hattori T, Fujita S. Tritiated thymidine autoradiographic study on histogenesis and spreading of intestinal metaplasia in human stomach. Pathol Res Pract 1979; 164: 224-237 PMID: 461230 DOI: 10.1016/S0344-0338(79)80045-X]
45. McDonald SA, Greaves LC, Gutierrez-Gonzalez L, Rodriguez-Justo M, Deheragoda M, Leedham SJ, Taylor RW, Lee CY, Preston SL, Lovell M, Hunt T, Elia G, Oukrif D, Harrison R, Novelli MR, Mitchell I, Stoker DL, Turnbull DM, Jankowski JA, Wright NA. Mechanisms of field cancerization in the human stomach: the expansion and spread of mutated gastric stem cells. Gastroenterology 2008; 134: 500-510 PMID: 18242216 DOI: 10.1053/j.gastro.2007.11.035]
46. Hansson LE, Nyrén O, Hsing AW, Bergström R, Josefsson S, Chow WH, Fraumeni JF, Adami HO. The risk of stomach cancer in patients with gastric or duodenal ulcer disease. N Engl J Med 1996; 335: 242-249 PMID: 8657240 DOI: 10.1056/ NEJM199607253350404]
47. Tatematsu M, Tsukamoto T, Inada K. Stem cells and gastric cancer: role of gastric and intestinal mixed intestinal metaplasia. Cancer Sci 2003; 94: 135-141 PMID: 12708487]