LGR5 is a negative regulator of tumourigenicity, antagonizes wnt signalling and regulates cell adhesion in colorectal cancer cell lines

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Walker, Francesca ^a   Zhang, Hui Hua ^a   Odorizzi, Annalisa ^a   Burgess, Antony W ^a  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

LEUCINE RICH REPEAT CONTAINING G PROTEIN COUPLED RECEPTOR 5; ONCOPROTEIN; UNCLASSIFIED DRUG; WNT3A PROTEIN; G PROTEIN COUPLED RECEPTOR; LGR5 PROTEIN, HUMAN; MESSENGER RNA; SMALL INTERFERING RNA; TUMOR MARKER; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL ADHESION; CELL MOTILITY; CELL PROLIFERATION; CLONOGENESIS; COLORECTAL CANCER; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME SPECIFICITY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; HETEROZYGOSITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; UPREGULATION; ANIMAL; CELL MOTION; CLONOGENIC ASSAY; COLORECTAL TUMOR; DNA MICROARRAY; DRUG ANTAGONISM; DRUG SCREENING; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE; WESTERN BLOTTING; WOUND HEALING;

ANIMALS; BLOTTING, WESTERN; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; COLONY-FORMING UNITS ASSAY; COLORECTAL NEOPLASMS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; HUMANS; MICE; MICE, NUDE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, G-PROTEIN-COUPLED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL; WNT PROTEINS; WOUND HEALING; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 79960885004     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022733     Document Type: Article

References (65)

1. Jordan CT, (2004) Cancer stem cell biology: from leukemia to solid tumours. Curr Opin Cell Biol 16: 708-712.
2. Donnenberg VS, Donnenberg AD, (2005) Multiple drug resistance in cancer revisited: the cancer stem cell hypothesis. J Clin Pharmacol 45: 872-877.
3. Essers MA, Trumpp A, Targeting leukemic stem cells by breaking their dormancy. Mol Oncol 4: 443-450.
4. O'Brien CA, Pollett A, Gallinger S, Dick JE, (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445: 106-110.
5. Chen ZG, (2009) The cancer stem cell concept in progression of head and neck cancer. J Oncol 2009: 894064.
6. Visvader JE, Lindeman GJ, (2008) Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8: 755-768.
7. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, et al. (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445: 111-115.
8. Levin TG, Powell AE, Davies PS, Silk AD, Dismuke AD, et al. (2010) Characterization of the intestinal cancer stem cell marker, CD166/ALCAM, in the human and mouse gastrointestinal tract. Gastroenterology 139: 2072-2082.
9. Chu P, Clanton DJ, Snipas TS, Lee J, Mitchell E, et al. (2009) Characterization of a subpopulation of colon cancer cells with stem cell-like properties. Int J Cancer 124: 1312-1321.
10. Vermeulen L, Todaro M, de Sousa Mello F, Sprick MR, Kemper K, et al. (2008) Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc Natl Acad Sci U S A 105: 13427-13432.
11. Todaro M, Francipane MG, Medema JP, Stassi G, (2010) Colon cancer stem cells: promise of targeted therapy. Gastroenterology 138: 2151-2162.
12. Nishimura S, Wakabayashi N, Toyoda K, Kashima K, Mitsufuji S, (2003) Expression of Musashi-1 in human normal colon crypt cells: a possible stem cell marker of human colon epithelium. Dig Dis Sci 48: 1523-1529.
13. Sureban SM, May R, George RJ, Dieckgraefe BK, McLeod HL, et al. (2008) Knockdown of RNA binding protein musashi-1 leads to tumour regression in vivo. Gastroenterology 134: 1448-1458.
14. Li DW, Tang HM, Fan JW, Yan DW, Zhou CZ, et al. (2010) Expression level of Bmi-1 oncoprotein is associated with progression and prognosis in colon cancer. J Cancer Res Clin Oncol 136: 997-1006.
15. Carpentino JE, Hynes MJ, Appelman HD, Zheng T, Steindler DA, et al. (2009) Aldehyde dehydrogenase-expressing colon stem cells contribute to tumourigenesis in the transition from colitis to cancer. Cancer Res 69: 8208-8215.
16. Alison MR, Lim SM, Nicholson LJ, (2011) Cancer stem cells: problems for therapy? J Pathol 223: 148-162.
17. Hsu SY, Liang SG, Hsueh AJ, (1998) Characterization of two LGR genes homologous to gonadotropin and thyrotropin receptors with extracellular leucine-rich repeats and a G protein-coupled, seven-transmembrane region. Mol Endocrinol 12: 1830-1845.
18. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, et al. (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007.
19. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, et al. (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459: 262-265.
20. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, et al. (2010) Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature.
21. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, et al. (2009) Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457: 608-611.
22. Uchida H, Yamazaki K, Fukuma M, Yamada T, Hayashida T, et al. Overexpression of leucine-rich repeat-containing G protein-coupled receptor 5 in colorectal cancer. Cancer Sci 101: 1731-1737.
23. Van der Flier LG, Sabates-Bellver J, Oving I, Haegebarth A, De Palo M, et al. (2007) The Intestinal Wnt/TCF Signature. Gastroenterology 132: 628-632.
24. Schneikert J, Behrens J, (2007) The canonical Wnt signalling pathway and its APC partner in colon cancer development. Gut 56: 417-425.
25. McDonald T, Wang R, Bailey W, Xie G, Chen F, et al. (1998) Identification and cloning of an orphan G protein-coupled receptor of the glycoprotein hormone receptor subfamily. Biochem Biophys Res Commun 247: 266-270.
26. McClanahan T, Koseoglu S, Smith K, Grein J, Gustafson E, et al. (2006) Identification of overexpression of orphan G protein-coupled receptor GPR49 in human colon and ovarian primary tumours. Cancer Biol Ther 5: 419-426.
27. Morita H, Mazerbourg S, Bouley DM, Luo CW, Kawamura K, et al. (2004) Neonatal lethality of LGR5 null mice is associated with ankyloglossia and gastrointestinal distension. Mol Cell Biol 24: 9736-9743.
28. Garcia MI, Ghiani M, Lefort A, Libert F, Strollo S, et al. (2009) LGR5 deficiency deregulates Wnt signaling and leads to precocious Paneth cell differentiation in the fetal intestine. Dev Biol 331: 58-67.
29. Whitehead RH, Macrae FA, St John DJ, Ma J, (1985) A colon cancer cell line (LIM1215) derived from a patient with inherited nonpolyposis colorectal cancer. J Natl Cancer Inst 74: 759-765.
30. Andrew SM, Teh JG, Johnstone RW, Russell SM, Whitehead RH, et al. (1990) Tumour localization by combinations of monoclonal antibodies in a new human colon carcinoma cell line (LIM1899). Cancer Res 50: 5225-5230.
31. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, et al. (1997) Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275: 1787-1790.
32. Behrens J, (2005) The role of the Wnt signalling pathway in colorectal tumourigenesis. Biochem Soc Trans 33: 672-675.
33. Zhang HH, Walker F, Kiflemariam S, Whitehead RH, Williams D, et al. (2009) Selective inhibition of proliferation in colorectal carcinoma cell lines expressing mutant APC or activated B-Raf. Int J Cancer 125: 297-307.
34. Uchida H, Yamazaki K, Fukuma M, Yamada T, Hayashida T, et al. (2010) Overexpression of leucine-rich repeat-containing G protein-coupled receptor 5 in colorectal cancer. Cancer Sci 101: 1731-1737.
35. Fan LF, Dong WG, Jiang CQ, Xia D, Liao F, et al. (2010) Expression of putative stem cell genes Musashi-1 and beta1-integrin in human colorectal adenomas and adenocarcinomas. Int J Colorectal Dis 25: 17-23.
36. Potten CS, Booth C, Tudor GL, Booth D, Brady G, et al. (2003) Identification of a putative intestinal stem cell and early lineage marker; musashi-1. Differentiation 71: 28-41.
37. Kayahara T, Sawada M, Takaishi S, Fukui H, Seno H, et al. (2003) Candidate markers for stem and early progenitor cells, Musashi-1 and Hes1, are expressed in crypt base columnar cells of mouse small intestine. FEBS Lett 535: 131-135.
38. Timmins NE, Dietmair S, Nielsen LK, (2004) Hanging-drop multicellular spheroids as a model of tumour angiogenesis. Angiogenesis 7: 97-103.
39. Elsaba TM, Martinez-Pomares L, Robins AR, Crook S, Seth R, et al. (2010) The stem cell marker CD133 associates with enhanced colony formation and cell motility in colorectal cancer. PLoS One 5: e10714.
40. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, et al. (2007) Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci U S A 104: 10158-10163.
41. Kremerskothen J, Stolting M, Wiesner C, Korb-Pap A, van Vliet V, et al. (2011) Zona occludens proteins modulate podosome formation and function. The FASEB journal: official publication of the Federation of American Societies for Experimental Biology 25: 505-514.
42. Van Goethem E, Guiet R, Balor S, Charriere GM, Poincloux R, et al. (2011) Macrophage podosomes go 3D. European journal of cell biology 90: 224-236.
43. Rottiers P, Saltel F, Daubon T, Chaigne-Delalande B, Tridon V, et al. (2009) TGFbeta-induced endothelial podosomes mediate basement membrane collagen degradation in arterial vessels. Journal of cell science 122: 4311-4318.
44. Turley EA, Noble PW, Bourguignon LY, (2002) Signaling properties of hyaluronan receptors. J Biol Chem 277: 4589-4592.
45. Willert J, Epping M, Pollack JR, Brown PO, Nusse R, (2002) A transcriptional response to Wnt protein in human embryonic carcinoma cells. BMC Dev Biol 2: 8.
46. Xu L, Corcoran RB, Welsh JW, Pennica D, Levine AJ, (2000) WISP-1 is a Wnt-1- and beta-catenin-responsive oncogene. Genes Dev 14: 585-595.
47. Taneyhill L, Pennica D, (2004) Identification of Wnt responsive genes using a murine mammary epithelial cell line model system. BMC Dev Biol 4: 6.
48. Kratochwil K, Galceran J, Tontsch S, Roth W, Grosschedl R, (2002) FGF4, a direct target of LEF1 and Wnt signaling, can rescue the arrest of tooth organogenesis in Lef1(-/-) mice. Genes Dev 16: 3173-3185.
49. Hovanes K, Li TW, Munguia JE, Truong T, Milovanovic T, et al. (2001) Beta-catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nat Genet 28: 53-57.
50. Tago K, Nakamura T, Nishita M, Hyodo J, Nagai S, et al. (2000) Inhibition of Wnt signaling by ICAT, a novel beta-catenin-interacting protein. Genes Dev 14: 1741-1749.
51. ten Berge D, Koole W, Fuerer C, Fish M, Eroglu E, et al. (2008) Wnt signaling mediates self-organization and axis formation in embryoid bodies. Cell Stem Cell 3: 508-518.
52. De Langhe SP, Sala FG, Del Moral PM, Fairbanks TJ, Yamada KM, et al. (2005) Dickkopf-1 (DKK1) reveals that fibronectin is a major target of Wnt signaling in branching morphogenesis of the mouse embryonic lung. Dev Biol 277: 316-331.
53. DasGupta R, Fuchs E, (1999) Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126: 4557-4568.
54. Crawford HC, Fingleton BM, Rudolph-Owen LA, Goss KJ, Rubinfeld B, et al. (1999) The metalloproteinase matrilysin is a target of beta-catenin transactivation in intestinal tumours. Oncogene 18: 2883-2891.
55. Howe LR, Watanabe O, Leonard J, Brown AM, (2003) Twist is up-regulated in response to Wnt1 and inhibits mouse mammary cell differentiation. Cancer Res 63: 1906-1913.
56. Rahmani M, Read JT, Carthy JM, McDonald PC, Wong BW, et al. (2005) Regulation of the versican promoter by the beta-catenin-T-cell factor complex in vascular smooth muscle cells. J Biol Chem 280: 13019-13028.
57. Brabletz T, Jung A, Dag S, Hlubek F, Kirchner T, (1999) beta-catenin regulates the expression of the matrix metalloproteinase-7 in human colorectal cancer. Am J Pathol 155: 1033-1038.
58. Dissanayake SK, Wade M, Johnson CE, O'Connell MP, Leotlela PD, et al. (2007) The Wnt5A/protein kinase C pathway mediates motility in melanoma cells via the inhibition of metastasis suppressors and initiation of an epithelial to mesenchymal transition. J Biol Chem 282: 17259-17271.
59. Chen YS, Mathias RA, Mathivanan S, Kapp EA, Moritz RL, et al. (2010) Proteomic profiling of MDCK plasma membranes reveals Wnt-5a involvement during oncogenic H-Ras/TGF-{beta}-mediated epithelial-mesenchymal transition. Mol Cell Proteomics.
60. Fan XS, Wu HY, Yu HP, Zhou Q, Zhang YF, et al. (2010) Expression of Lgr5 in human colorectal carcinogenesis and its potential correlation with beta-catenin. Int J Colorectal Dis 25: 583-590.
61. Yamamoto Y, Sakamoto M, Fujii G, Tsuiji H, Kenetaka K, et al. (2003) Overexpression of orphan G-protein-coupled receptor, Gpr49, in human hepatocellular carcinomas with beta-catenin mutations. Hepatology 37: 528-533.
62. van den Brink GR, Offerhaus GJ, (2007) The morphogenetic code and colon cancer development. Cancer Cell 11: 109-117.
63. Sun X, Jackson L, Dey SK, Daikoku T, (2009) In pursuit of leucine-rich repeat-containing G protein-coupled receptor-5 regulation and function in the uterus. Endocrinology 150: 5065-5073.
64. Lewis A, Segditsas S, Deheragoda M, Pollard P, Jeffery R, et al. (2010) Severe polyposis in Apc(1322T) mice is associated with submaximal Wnt signalling and increased expression of the stem cell marker Lgr5. Gut 59: 1680-1686.
65. Hlubek F, Brabletz T, Budczies J, Pfeiffer S, Jung A, et al. (2007) Heterogeneous expression of Wnt/beta-catenin target genes within colorectal cancer. Int J Cancer 121: 1941-1948.