Wnt signaling and colon tumorigenesis - A view from the periphery

Experimental Cell Research

Volumn 317, Issue 19, 2011, Pages 2748-2758

  Burgess, Antony W ^a   Faux, Maree C ^a   Layton, Meredith J ^b   Ramsay, Robert G ^c,d  

^a OLIVIA NEWTON JOHN CANCER RESEARCH INSTITUTE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c PETER MACCALLUM CANCER CENTRE   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Apc; E cadherin; Myb; Myc; Phospho catenin

Indexed keywords

APC PROTEIN; BETA CATENIN; PROTEASOME; PROTEIN MYB; WNT PROTEIN;

CANCER CELL; CARCINOGENESIS; CELL ADHESION; CELL MIGRATION; CELLULAR DISTRIBUTION; COLON MUCOSA; COLON TUMOR; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

EID: 80455173856     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2011.08.010     Document Type: Review

References (142)

1. Rowan A., et al. APC mutations in sporadic colorectal tumors: a mutational "hotspot" and interdependence of the "two hits". Proc. Natl. Acad. Sci. U.S.A. 2000, 97(7):3352.
2. Jones S., et al. Comparative lesion sequencing provides insights into tumor evolution. Proc. Natl Acad. Sci. 2008, 105(11):4283.
3. Kinzler K.W., Vogelstein B. Cancer-susceptibility genes. Gatekeepers and caretakers. Nature 1997, 386:761-763.
4. Nusse R. Wnt signaling and stem cell control. Cell Res. 2008, 18:523-527.
5. Brabletz T., et al. Nuclear overexpression of the oncoprotein beta-catenin in colorectal cancer is localized predominantly at the invasion front. Pathol. Res. Pract. 1998, 194(10):701-704.
6. Brabletz T., et al. Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc. Natl. Acad. Sci. U.S.A. 2001, 98(18):10356-10361.
7. Anderson C.B., Neufeld K.L., White R.L. Subcellular distribution of Wnt pathway proteins in normal and neoplastic colon. Proc. Natl. Acad. Sci. U.S.A. 2002, 99(13):8683-8688.
8. Phelps R.A., et al. A two-step model for colon adenoma initiation and progression caused by APC loss. Cell 2009, 137(4):623-634.
9. Pollard P., et al. The Apc 1322T mouse develops severe polyposis associated with submaximal nuclear beta-catenin expression. Gastroenterology 2009, 136(7):2204-2213. e1-13.
10. Blaker H., et al. Somatic mutations in familial adenomatous polyps. Nuclear translocation of beta-catenin requires more than biallelic APC inactivation. Am. J. Clin. Pathol. 2003, 120(3):418-423.
11. Sansom O.J., et al. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev. 2004, 18(12):1385-1390.
12. Kroboth K., et al. Lack of adenomatous polyposis coli protein correlates with a decrease in cell migration and overall changes in microtubule stability. Mol. Biol. Cell 2007, 18(3):910-918.
13. Faux M.C., et al. Restoration of full-length adenomatous polyposis coli (APC) protein in a colon cancer cell line enhances cell adhesion. J. Cell Sci. 2004, 117(Pt 3):427-439.
14. Barker N., et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449(7165):1003-1007.
15. Hedman H., Henriksson R. LRIG inhibitors of growth factor signalling - double-edged swords in human cancer?. Eur. J. Cancer 2007, 43(4):676-682.
16. Sato T., et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 2011, 469(7330):415-418.
17. Buske P., et al. A comprehensive model of the spatio-temporal stem cell and tissue organisation in the intestinal crypt. PLoS Comput. Biol. 2011, 7(1):e1001045.
18. van Leeuwen I.M., et al. An integrative computational model for intestinal tissue renewal. Cell Prolif. 2009, 42(5):617-636.
19. Kuhnert F., et al. Essential requirement for Wnt signaling in proliferation of adult small intestine and colon revealed by adenoviral expression of Dickkopf-1. Proc. Natl. Acad. Sci. U.S.A. 2004, 101(1):266-271.
20. Zeki S.S., Graham T.A., Wright N.A. Stem cells and their implications for colorectal cancer. Nat. Rev. Gastroenterol. Hepatol. 2011, 8(2):90-100.
21. Zhang H.H., et al. Selective inhibition of proliferation in colorectal carcinoma cell lines expressing mutant APC or activated B-Raf. Int. J. Cancer 2009, 125(2):297-307.
22. Manolagas S.C., Almeida M. Gone with the Wnts: beta-catenin, T-cell factor, forkhead box O, and oxidative stress in age-dependent diseases of bone, lipid, and glucose metabolism. Mol. Endocrinol. 2007, 21(11):2605-2614.
23. Malaterre J., et al. c-Myb is required for progenitor cell homeostasis in colonic crypts. Proc. Natl. Acad. Sci. U.S.A. 2007, 104(10):3829-3834.
24. Ramsay R.G., Gonda T.J. MYB function in normal and cancer cells. Nat. Rev. Cancer 2008, 8(7):523-534.
25. Ramsay R.G., Malaterre J. Insights into c-Myb functions through investigating colonic crypts. Blood Cells Mol. Dis. 2007, 39(3):287-291.
26. Bienz M., Clevers H. Linking colorectal cancer to Wnt signaling. Cell 2000, 103:311.
27. Radtke F., Clevers H., Riccio O. From gut homeostasis to cancer. Curr. Mol. Med. 2006, 6:275-289.
28. Buchert M., et al. Genetic dissection of differential signaling threshold requirements for the Wnt/beta-catenin pathway in vivo. PLoS Genet. 2010, 6(1):e1000816.
29. Carothers A.M., et al. Progressive changes in adherens junction structure during intestinal adenoma formation in Apc mutant mice. J. Biol. Chem. 2001, 276(42):39094-39102.
30. Albuquerque C., et al. The 'just-right' signaling model: APC somatic mutations are selected based on a specific level of activation of the beta-catenin signaling cascade. Hum. Mol. Genet. 2002, 11(13):1549-1560.
31. Inomata M., et al. Alteration of beta-catenin expression in colonic epithelial cells of familial adenomatous polyposis patients. Cancer Res. 1996, 56(9):2213-2217.
32. Shibata H., et al. Rapid colorectal adenoma formation initiated by conditional targeting of the Apc gene. Science 1997, 278(5335):120-123.
33. Vermeulen, L., et al., Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol. 12 (5) (2010) 468-476.
34. Aberle H., et al. beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 1997, 16(13):3797-3804.
35. Winston J.T., et al. The SCFbeta-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IkappaBalpha and beta-catenin and stimulates IkappaBalpha ubiquitination in vitro. Genes Dev. 1999, 13(3):270-283.
36. Jiang J., Struhl G. Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature 1998, 391(6666):493-496.
37. van Kerkhof P., Putters J., Strous G.J. The ubiquitin ligase SCF(betaTrCP) regulates the degradation of the growth hormone receptor. J. Biol. Chem. 2007, 282(28):20475-20483.
38. Liu C., et al. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 2002, 108(6):837-847.
39. Rubinfeld B., et al. Association of the APC gene product with beta-catenin. Science 1993, 262(5140):1731-1734.
40. Su L.K., Vogelstein B., Kinzler K.W. Association of the APC tumor suppressor protein with catenins. Science 1993, 262(5140):1734-1737.
41. Kishida S., et al. Axin, a negative regulator of the wnt signaling pathway, directly interacts with adenomatous polyposis coli and regulates the stabilization of beta-catenin. J. Biol. Chem. 1998, 273(18):10823-10826.
42. Nakamura T., et al. Axin, an inhibitor of the Wnt signalling pathway, interacts with beta-catenin, GSK-3beta and APC and reduces the beta-catenin level. Genes Cells 1998, 3(6):395-403.
43. Ha N.C., et al. Mechanism of phosphorylation-dependent binding of APC to beta-catenin and its role in beta-catenin degradation. Mol. Cell 2004, 15(4):511-521.
44. Kimelman D., Xu W. Beta-catenin destruction complex: insights and questions from a structural perspective. Oncogene 2006, 25(57):7482-7491.
45. Gail R., Frank R., Wittinghofer A. Systematic peptide array-based delineation of the differential beta-catenin interaction with Tcf4, E-cadherin, and adenomatous polyposis coli. J. Biol. Chem. 2005, 280(8):7107-7117.
46. Kohler E.M., et al. Contribution of the 15 amino acid repeats of truncated APC to beta-catenin degradation and selection of APC mutations in colorectal tumours from FAP patients. Oncogene 2009, 29(11):1663-1671.
47. Su Y., et al. APC is essential for targeting phosphorylated beta-catenin to the SCFbeta-TrCP ubiquitin ligase. Mol. Cell 2008, 32(5):652-661.
48. Roberts D.M., et al. Deconstructing the sscatenin destruction complex: mechanistic roles for the tumor suppressor APC in regulating Wnt signaling. Mol. Biol. Cell. 2011, 22(11):1845-1863.
49. Smits R., et al. Apc1638T: a mouse model delineating critical domains of the adenomatous polyposis coli protein involved in tumorigenesis and development. Genes Dev. 1999, 13(10):1309-1321.
50. Oshima M., et al. Loss of Apc heterozygosity and abnormal tissue building in nascent intestinal polyps in mice carrying a truncated Apc gene. Proc. Natl. Acad. Sci. U.S.A. 1995, 92(10):4482-4486.
51. Cheung A.F., et al. Complete deletion of Apc results in severe polyposis in mice. Oncogene 2010, 29(12):1857-1864.
52. Faux M.C., et al. Recruitment of adenomatous polyposis coli and beta-catenin to axin-puncta. Oncogene 2008, 27(44):5808-5820.
53. Nathke I.S., et al. The adenomatous polyposis coli tumor suppressor protein localizes to plasma membrane sites involved in active cell migration. J. Cell Biol. 1996, 134(1):165-179.
54. Kita K., et al. Adenomatous polyposis coli on microtubule plus ends in cell extensions can promote microtubule net growth with or without EB1. Mol. Biol. Cell 2006, 17(5):2331-2345.
55. Mogensen M.M., et al. The adenomatous polyposis coli protein unambiguously localizes to microtubule plus ends and is involved in establishing parallel arrays of microtubule bundles in highly polarized epithelial cells. J. Cell Biol. 2002, 157(6):1041-1048.
56. McCartney B.M., Nathke I.S. Cell regulation by the Apc protein Apc as master regulator of epithelia. Curr. Opin. Cell Biol. 2008, 20(2):186-193.
57. Nathke I. Cytoskeleton out of the cupboard: colon cancer and cytoskeletal changes induced by loss of APC. Nat. Rev. Cancer 2006, 6(12):967-974.
58. Etienne-Manneville S., Hall A. Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 2003, 421(6924):753-756.
59. Etienne-Manneville S., et al. Cdc42 and Par6-PKCzeta regulate the spatially localized association of Dlg1 and APC to control cell polarization. J. Cell Biol. 2005, 170(6):895-901.
60. Moseley J.B., et al. Regulated binding of adenomatous polyposis coli protein to actin. J. Biol. Chem. 2007, 282(17):12661-12668.
61. Munemitsu S., et al. The APC gene product associates with microtubules in vivo and promotes their assembly in vitro. Cancer Res. 1994, 54(14):3676-3681.
62. Smith K.J., et al. Wild-type but not mutant APC associates with the microtubule cytoskeleton. Cancer Res. 1994, 54(14):3672-3675.
63. Jimbo T., et al. Identification of a link between the tumour suppressor APC and the kinesin superfamily. Nat. Cell Biol. 2002, 4(4):323-327.
64. Kawasaki Y., et al. Asef, a link between the tumor suppressor APC and G-protein signaling. Science 2000, 289(5482):1194-1197.
65. Watanabe T., et al. Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev. Cell 2004, 7(6):871-883.
66. Wen Y., et al. EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat. Cell Biol. 2004, 6(9):820-830.
67. Su L.K., et al. APC binds to the novel protein EB1. Cancer Res. 1995, 55(14):2972-2977.
68. Matsumine A., et al. Binding of APC to the human homolog of the Drosophila discs large tumor suppressor protein. Science 1996, 272(5264):1020-1023.
69. Harris E.S., Nelson W.J. Adenomatous polyposis coli regulates endothelial cell migration independent of roles in beta-catenin signaling and cell-cell adhesion. Mol. Biol. Cell 2010, 21(15):2611-2623.
70. Fiedler M., et al. Dishevelled interacts with the DIX domain polymerization interface of Axin to interfere with its function in down-regulating beta-catenin. Proc. Natl. Acad. Sci. U.S.A. 2011, 108(5):1937-1942.
71. Faux M.C., et al. Independent interactions of phosphorylated beta-catenin with E-cadherin at cell-cell contacts and APC at cell protrusions. PLoS One 2010, 5(11):e14127.
72. Dikovskaya D., et al. Loss of APC induces polyploidy as a result of a combination of defects in mitosis and apoptosis. J. Cell Biol. 2007, 176(2):183-195.
73. Barth A.I., et al. NH2-terminal deletion of beta-catenin results in stable colocalization of mutant beta-catenin with adenomatous polyposis coli protein and altered MDCK cell adhesion. J. Cell Biol. 1997, 136(3):693-706.
74. Votin V., Nelson W.J., Barth A.I. Neurite outgrowth involves adenomatous polyposis coli protein and beta-catenin. J. Cell Sci. 2005, 118(Pt 24):5699-5708.
75. Sharma M., et al. Membrane localization of adenomatous polyposis coli protein at cellular protrusions: targeting sequences and regulation by beta-catenin. J. Biol. Chem. 2006, 281(25):17140-17149.
76. Zhou F.Q., et al. NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron 2004, 42(6):897-912.
77. Purro S.A., et al. Wnt regulates axon behavior through changes in microtubule growth directionality: a new role for adenomatous polyposis coli. J. Neurosci. 2008, 28(34):8644-8654.
78. Sparks A.B., et al. Mutational analysis of the APC/beta-catenin/Tcf pathway in colorectal cancer. Cancer Res. 1998, 58(6):1130-1134.
79. Morin P.J., et al. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 1997, 275(5307):1787-1790.
80. Wang Z., Vogelstein B., Kinzler K.W. Phosphorylation of beta-catenin at S33, S37, or T41 can occur in the absence of phosphorylation at T45 in colon cancer cells. Cancer Res. 2003, 63(17):5234-5235.
81. Chan T.A., et al. Targeted inactivation of CTNNB1 reveals unexpected effects of beta-catenin mutation. Proc. Natl. Acad. Sci. U.S.A. 2002, 99(12):8265-8270.
82. Provost E., et al. Functional correlates of mutation of the Asp32 and Gly34 residues of beta-catenin. Oncogene 2005, 24(16):2667-2676.
83. Provost E., et al. Functional correlates of mutations in beta-catenin exon 3 phosphorylation sites. J. Biol. Chem. 2003, 278(34):31781-31789.
84. Al-Fageeh M., et al. Phosphorylation and ubiquitination of oncogenic mutants of beta-catenin containing substitutions at Asp32. Oncogene 2004, 23(28):4839-4846.
85. Johnson V., et al. Exon 3 beta-catenin mutations are specifically associated with colorectal carcinomas in hereditary non-polyposis colorectal cancer syndrome. Gut 2005, 54(2):264-267.
86. Segditsas S., Tomlinson I. Colorectal cancer and genetic alterations in the Wnt pathway. Oncogene 2006, 25(57):7531-7537.
87. Medrek C., et al. Wnt-5a-CKI{alpha} signaling promotes {beta}-catenin/E-cadherin complex formation and intercellular adhesion in human breast epithelial cells. J. Biol. Chem. 2009, 284(16):10968-10979.
88. Maher M.T., et al. Activity of the beta-catenin phosphodestruction complex at cell-cell contacts is enhanced by cadherin-based adhesion. J. Cell Biol. 2009, 186(2):219-228.
89. Maher M.T., et al. Beta-catenin phosphorylated at serine 45 is spatially uncoupled from beta-catenin phosphorylated in the GSK3 domain: implications for signaling. PLoS One 2010, 5(4):e10184.
90. Sadot E., et al. Regulation of S33/S37 phosphorylated beta-catenin in normal and transformed cells. J. Cell Sci. 2002, 115(Pt 13):2771-2780.
91. Huang P., Senga T., Hamaguchi M. A novel role of phospho-beta-catenin in microtubule regrowth at centrosome. Oncogene 2007, 26(30):4357-4371.
92. Polakis P., Hart M., Rubinfeld B. Defects in the regulation of beta-catenin in colorectal cancer. Adv. Exp. Med. Biol. 1999, 470:23-32.
93. Gottardi C.J., Gumbiner B.M. Distinct molecular forms of beta-catenin are targeted to adhesive or transcriptional complexes. J. Cell Biol. 2004, 167(2):339-349.
94. Staal F.J., et al. Wnt signals are transmitted through N-terminally dephosphorylated beta-catenin. EMBO Rep. 2002, 3(1):63-68.
95. Gottardi C.J., Peifer M. Terminal regions of beta-catenin come into view. Structure 2008, 16(3):336-338.
96. Gao Y., Wang H.Y. Inositol pentakisphosphate mediates Wnt/beta-catenin signaling. J. Biol. Chem. 2007, 282(36):26490-26502.
97. Sayat R., et al. O-GlcNAc-glycosylation of beta-catenin regulates its nuclear localization and transcriptional activity. Exp. Cell Res. 2008, 314(15):2774-2787.
98. Schramp M., et al. PIPKIgamma regulates beta-catenin transcriptional activity downstream of growth factor receptor signaling. Cancer Res. 2011, 71(4):1282-1291.
99. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006, 127(3):469-480.
100. Cavallo R.A., et al. Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 1998, 395(6702):604-608.
101. Levanon D., et al. Transcriptional repression by AML1 and LEF-1 is mediated by the TLE/Groucho corepressors. Proc. Natl. Acad. Sci. U.S.A. 1998, 95(20):11590-11595.
102. Arce L., Pate K.T., Waterman M.L. Groucho binds two conserved regions of LEF-1 for HDAC-dependent repression. BMC Cancer 2009, 9:159.
103. Mahmoudi T., et al. The leukemia-associated Mllt10/Af10-Dot1l are Tcf4/beta-catenin coactivators essential for intestinal homeostasis. PLoS Biol. 2010, 8(11):e1000539.
104. Lustig B., et al. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol. Cell. Biol. 2002, 22(4):1184-1193.
105. Yan D., et al. Elevated expression of axin2 and hnkd mRNA provides evidence that Wnt/beta-catenin signaling is activated in human colon tumors. Proc. Natl. Acad. Sci. U.S.A. 2001, 98(26):14973-14978.
106. He T.C., et al. Identification of c-MYC as a target of the APC pathway. Science 1998, 281(5382):1509-1512.
107. Hatzis P., et al. Genome-wide pattern of TCF7L2/TCF4 chromatin occupancy in colorectal cancer cells. Mol. Cell. Biol. 2008, 28(8):2732-2744.
108. Ciznadija D., et al. Intestinal adenoma formation and MYC activation are regulated by cooperation between MYB and Wnt signaling. Cell Death Differ. 2009, 16(11):1530-1538.
109. Tuupanen S., et al. The common colorectal cancer predisposition SNP rs6983267 at chromosome 8q24 confers potential to enhanced Wnt signaling. Nat. Genet. 2009, 41(8):885-890.
110. Wright J.B., Brown S.J., Cole M.D. Upregulation of c-MYC in cis through a large chromatin loop linked to a cancer risk-associated SNP in colorectal cancer cells. Mol. Cell. Biol. 2010, 30(6):1411-1420.
111. Simonis M., Kooren J., de Laat W. An evaluation of 3C-based methods to capture DNA interactions. Nat. Methods 2007, 4(11):895-901.
112. -/- colon carcinoma. Science 1997, 275(5307):1784-1787.
113. Biechele T.L., Moon R.T. Assaying beta-catenin/TCF transcription with beta-catenin/TCF transcription-based reporter constructs. Meth. Mol. Biol. 2008, 468:99-110.
114. Boman B., et al. A Tcf4-GFP reporter mouse model for monitoring effects of Apc mutations during intestinal tumorigenesis. Mol. Carcinog. 2009, 48(9):821-831.
115. Terzic J., et al. Inflammation and colon cancer. Gastroenterology 2010, 138(6):2101-2114. e5.
116. Morikawa T., et al. STAT3 expression, molecular features, inflammation patterns, and prognosis in a database of 724 colorectal cancers. Clin. Cancer Res. 2011, 17(6):1452-1462.
117. Min/+ mice due to decreases in c-Myc expression. Mol. Cancer Res. 2007, 5(12):1296-1303.
118. Nakagoshi H., et al. Transcriptional activation of the c-myc gene by the c-myb and B-myb gene products. Oncogene 1992, 7(6):1233-1240.
119. Barker N., Clevers H. Leucine-rich repeat-containing G-protein-coupled receptors as markers of adult stem cells. Gastroenterology 2010, 138(5):1681-1696.
120. Quyn A.J., et al. Spindle orientation bias in gut epithelial stem cell compartments is lost in precancerous tissue. Cell Stem Cell 2010, 6(2):175-181.
121. Wong W.M., et al. Histogenesis of human colorectal adenomas and hyperplastic polyps: the role of cell proliferation and crypt fission. Gut 2002, 50(2):212-217.
122. Barker N., et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009, 457(7229):608-611.
123. Snippert H.J., et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 2010, 143(1):134-144.
124. Lopez-Garcia C., et al. Intestinal stem cell replacement follows a pattern of neutral drift. Science 2010, 330(6005):822-825.
125. Sato T., et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 2009, 459(7244):262-265.
126. Gracz A.D., Ramalingam S., Magness S.T. Sox9 expression marks a subset of CD24-expressing small intestine epithelial stem cells that form organoids in vitro. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298(5):G590-G600.
127. Matsuda M., Chitnis A.B. Atoh1a expression must be restricted by Notch signaling for effective morphogenesis of the posterior lateral line primordium in zebrafish. Development 2010, 137(20):3477-3487.
128. Furukawa K., et al. Smad3 contributes to positioning of proliferating cells in colonic crypts by inducing EphB receptor protein expression. Biochem. Biophys. Res. Commun. 2011, 405(4):521-526.
129. Appleton P.L., et al. Preparation of wholemount mouse intestine for high-resolution three-dimensional imaging using two-photon microscopy. J. Microsc. 2009, 234(2):196-204.
130. H.J. Choi, A.H. Huber, W.I. Weis, Thermodynamics of beta-catenin-ligand interactions: the roles of the N- and C-terminal tails in modulating binding affinity. J. Biol. Chem. 281 (2006) 1027-1038.
131. Rigby R.J., et al. Suppressor of cytokine signaling 3 (SOCS3) limits damage-induced crypt hyper-proliferation and inflammation-associated tumorigenesis in the colon. Oncogene 2007, 26(33):4833-4841.
132. +/Min mice. FEBS Lett. 2008, 582(19):2911-2915.
133. Sukhotnik I., et al. Effect of transforming growth factor-alpha on enterocyte apoptosis is correlated with EGF receptor expression along the villus-crypt axis during methotrexate-induced intestinal mucositis in a rat. Apoptosis 2008, 13(11):1344-1355.
134. Vidrich A., et al. Fibroblast growth factor receptor-3 is expressed in undifferentiated intestinal epithelial cells during murine crypt morphogenesis. Dev. Dyn. 2004, 230(1):114-123.
135. McConnell B.B., et al. Kruppel-like factor 5 is important for maintenance of crypt architecture and barrier function in mouse intestine. Gastroenterology 2011, [Electronic publication ahead of print] PMID:21763241.
136. Solanas G., et al. Cleavage of E-cadherin by ADAM10 mediates epithelial cell sorting downstream of EphB signalling. Nat. Cell Biol. 2011.
137. Wong S.Y., et al. Computational model of cell positioning: directed and collective migration in the intestinal crypt epithelium. J. R. Soc. Interface 2010, 7(Suppl 3):S351-S363.
138. Kim T.H., Shivdasani R.A. Genetic evidence that intestinal Notch functions vary regionally and operate through a common mechanism of Math1 repression. J. Biol. Chem. 2011, 286(13):11427-11433.
139. Pellegrinet L., et al. Dll1- and dll4-mediated notch signaling are required for homeostasis of intestinal stem cells. Gastroenterology 2011, 140(4):1230-1240. e1-7.
140. Myant K., Sansom O. Efficient Wnt mediated intestinal hyperproliferation requires the cyclin D2-CDK4/6 complex. Cell Dev. 2011, 6(1):3.
141. Takeda K., et al. Expression of LGR5, an intestinal stem cell marker, during each stage of colorectal tumorigenesis. Anticancer Res. 2011, 31(1):263-270.
142. Walker F., et al. LGR5 is a negative regulator of tumourigenicity, antagonizes Wnt signalling and regulates cell adhesion in colorectal cancer cell lines. PLoS One 2011, 6(7):e22733.