Importance of the niche: Wnt signaling and stem cell plasticity in intestinal homeostasis and disease

Molecular Pathogenesis of Colorectal Cancer

Volumn , Issue , 2013, Pages 107-120

  Sansom, Owen J ^a   Näthke, Inke ^b  

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84929573872     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-8412-7_4     Document Type: Chapter

References (68)

1. Albuquerque C, Breukel C, van der Luijt R, Fidalgo P, Lage P, Slors FJ, Leitao CN, Fodde R, Smits R (2002) The 'just-right' signaling model: APC somatic mutations are selected based on a specifi c level of activation of the beta-catenin signaling cascade. Hum Mol Genet 11:1549-1560
2. Appleton PL, Quyn AJ, Swift S, Nathke I (2009) Preparation of wholemount mouse intestine for high-resolution three-dimensional imaging using two-photon microscopy. J Microsc 234:196-204
3. 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 (2007) Identifi cation of stem cells in small intestine and colon by marker gene Lgr5. Nature 449:1003-1007
4. 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 (2009) Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457:608-611
5. Bejsovec A (1999) Signal transduction: Wnt signalling shows its versatility. Curr Biol 9:R684-R687
6. Brabletz T, Jung A, Hermann K, Gunther K, Hohenberger W, Kirchner T (1998) Nuclear overexpression of the oncoprotein beta-catenin in colorectal cancer is localized predominantly at the invasion front. Pathol Res Pract 194:701-704
7. Brabletz T, Jung A, Reu S, Porzner M, Hlubek F, Kunz-Schughart LA, Knuechel R, Kirchner T (2001) Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc Natl Acad Sci U S A 98:10356-10361
8. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T (2005) Opinion: migrating cancer stem cells-an integrated concept of malignant tumour progression. Nat Rev Cancer 5:744-749
9. Brocardo M, Lei Y, Tighe A, Taylor SS, Mok MT, Henderson BR (2008) Mitochondrial targeting of adenomatous polyposis coli protein is stimulated by truncating cancer mutations: regulation of Bcl-2 and implications for cell survival. J Biol Chem 283:5950-5959
10. Buchert M, Athineos D, Abud HE, Burke ZD, Faux MC, Samuel MS, Jarnicki AG, Winbanks CE, Newton IP, Meniel VS, Suzuki H, Stacker SA, Nathke IS, Tosh D, Huelsken J, Clarke AR, Heath JK, Sansom OJ, Ernst M (2010) Genetic dissection of differential signaling threshold requirements for the Wnt/beta-catenin pathway in vivo. PLoS Genet 6:e1000816
11. Cheng H, Bjerknes M (1983) Cell production in mouse intestinal epithelium measured by stathmokinetic fl ow cytometry and Coulter particle counting. Anat Rec 207:427-434
12. Cheung AF, Carter AM, Kostova KK, Woodruff JF, Crowley D, Bronson RT, Haigis KM, Jacks T (2010) Complete deletion of Apc results in severe polyposis in mice. Oncogene 29:1857-1864
13. Crosnier C, Stamataki D, Lewis J (2006) Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet 7:349-359
14. de Sousa EMF, Colak S, Buikhuisen J, Koster J, Cameron K, de Jong JH, Tuynman JB, Prasetyanti PR, Fessler E, van den Bergh SP, Rodermond H, Dekker E, van der Loos CM, Pals ST, van de Vijver MJ, Versteeg R, Richel DJ, Vermeulen L, Medema JP (2011) Methylation of cancerstem-cell-associated Wnt target genes predicts poor prognosis in colorectal cancer patients. Cell Stem Cell 9:476-485
15. Dikovskaya D, Newton IP, Näthke IS (2004) The adenomatous polyposis coli protein is required for the formation of robust spindles formed in CSF Xenopus extracts. Mol Biol Cell 15:2978-2991
16. Dikovskaya D, Schiffmann D, Newton IP, Oakley A, Kroboth K, Sansom O, Jamieson TJ, Meniel V, Clarke A, Näthke IS (2007) Loss of APC induces polyploidy as a result of a combination of defects in mitosis and apoptosis. J Cell Biol 176:183-195
17. Draviam VM, Shapiro I, Aldridge B, Sorger PK (2006) Misorientation and reduced stretching of aligned sister kinetochores promote chromosome missegregation in EB1- or APC-depleted cells. EMBO J 25:2814-2827
18. Fearon ER, Vogelstein B (1990) A genetic model for colorectal tumorigenesis. Cell 61:759-767
19. Gaspar C, Franken P, Molenaar L, Breukel C, van der Valk M, Smits R, Fodde R (2009) A targeted constitutive mutation in the APC tumor suppressor gene underlies mammary but not intestinal tumorigenesis. PLoS Genet 5:e1000547
20. Itzkovitz S, Blat IC, Jacks T, Clevers H, van Oudenaarden A (2012) Optimality in the development of intestinal crypts. Cell 148:608-619
21. Kaur P, Potten CS (2011) The interfollicular epidermal stem cell saga: sensationalism versus reality check. Exp Dermatol 20:697-702
22. Kim TH, Escudero S, Shivdasani RA (2012) Intact function of Lgr5 receptor-expressing intestinal stem cells in the absence of Paneth cells. Proc Natl Acad Sci U S A 109(10):3932-3937
23. Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, Peters PJ, Clevers H (1998) Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 1998(19):379-383
24. Kroboth K, Newton IP, Kita K, Dikovskaya D, Zumbrunn J, Waterman-Storer CM, Näthke IS (2007) Lack of adenomatous polyposis coli protein correlates with a decrease in cell migration and overall changes in microtubule stability. Mol Biol Cell 18:910-918
25. Lewis A, Segditsas S, Deheragoda M, Pollard P, Jeffery R, Nye E, Lockstone H, Davis H, Clark S, Stamp G, Poulsom R, Wright N, Tomlinson I (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
26. Lewis A, Davis H, Deheragoda M, Pollard P, Nye E, Jeffery R, Segditsas S, East P, Poulsom R, Stamp G, Wright N, Tomlinson I (2012) The C-terminus of Apc does not infl uence intestinal adenoma development or progression. J Pathol 226:73-83
27. Li Z, Kroboth K, Newton IP, Nathke IS (2008) Novel self-association of the APC molecule affects APC clusters and cell migration. J Cell Sci 121:1916-1925
28. Luongo C, Moser AR, Gledhill S, Dove WF (1994) Loss of APC in intestinal adenomas from Min mice. Cancer Res 54:5947-5952
29. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA (2008) The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 133:704-715
30. March HN, Rust AG, Wright NA, ten Hoeve J, de Ridder J, Eldridge M, van der Weyden L, Berns A, Gadiot J, Uren A, Kemp R, Arends MJ, Wessels LF, Winton DJ, Adams DJ (2011) Insertional mutagenesis identifi es multiple networks of cooperating genes driving intestinal tumorigenesis. Nat Genet 43:1202-1209
31. McCartney BM, Näthke IS (2008) Cell regulation by the Apc protein Apc as master regulator of epithelia. Curr Opin Cell Biol 20:186-193
32. Merlos-Suarez A, Barriga FM, Jung P, Iglesias M, Cespedes MV, Rossell D, Sevillano M, Hernando-Momblona X, da Silva-Diz V, Munoz P, Clevers H, Sancho E, Mangues R, Batlle E (2011) The intestinal stem cell signature identifi es colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 8:511-524
33. Miyoshi Y, Nagase H, Ando H, Horii A, Ichii S, Nakatsuru S, Aoki T, Miki Y, Mori T, Nakamura Y (1992) Somatic mutations of the APC gene in colorectal tumors: mutation cluster region in the APC gene. Hum Mol Genet 1:229-233
34. Moser AR, Dove WF, Roth KA, Gordon JI (1992) The Min (multiple intestinal neoplasia) mutation: its effect on gut epithelial cell differentiation and interaction with a modifi er system. J Cell Biol 116:1517-1526
35. Muncan V, Sansom OJ, Tertoolen L, Phesse TJ, Begthel H, Sancho E, Cole AM, Gregorieff A, de Alboran IM, Clevers H, Clarke AR (2006) Rapid loss of intestinal crypts upon conditional deletion of the Wnt/Tcf-4 target gene c-Myc. Mol Cell Biol 26:8418-8426
36. Murawala P, Tripathi MM, Vyas P, Salunke A, Joseph J (2009) Nup358 interacts with APC and plays a role in cell polarization. J Cell Sci 122:3113-3122
37. Näthke IS, Adams CL, Polakis P, Sellin JH, Nelson WJ (1996) The adenomatous polyposis coli tumor suppressor protein localizes to plasma membrane sites involved in active cell migration. J Cell Biol 134:165-179
38. Neal JV, Potten CS (1981) Description and basic cell kinetics of the murine pericryptal fi broblast sheath. Gut 22:19-24
39. Nelson SA, Li Z, Newton IP, Fraser D, Milne RE, Martin DM, Schiffmann D, Yang X, Dormann D, Weijer CJ, Appleton PL, Nathke IS (2012) Tumorigenic fragments of APC cause dominant defects in directional cell migration in multiple model systems. Dis Model Mech 5(6):940-947
40. O'Brien LE, Soliman SS, Li X, Bilder D (2011) Altered modes of stem cell division drive adaptive intestinal growth. Cell 147:603-614
41. Polakis P (1999) The oncogenic activation of b-catenin. Curr Opin Genet Dev 9:15-21
42. Polakis P (2007) The many ways of Wnt in cancer. Curr Opin Genet Dev 17:45-51
43. Polakis P (2012) Wnt signaling in cancer. Cold Spring Harb Perspect Biol 4(5). pii: a008052
44. Pollard P, Deheragoda M, Segditsas S, Lewis A, Rowan A, Howarth K, Willis L, Nye E, McCart A, Mandir N, Silver A, Goodlad R, Stamp G, Cockman M, East P, Spencer-Dene B, Poulsom R, Wright N, Tomlinson I (2009) The Apc 1322T mouse develops severe polyposis associated with submaximal nuclear beta-catenin expression. Gastroenterology 136:2204-2213. e1-13
45. Potten CS, Loeffl er M (1990) Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110:1001-1020
46. Potten CS, Gandara R, Mahida YR, Loeffl er M, Wright NA (2009) The stem cells of small intestinal crypts: where are they? Cell Prolif 42:731-750
47. Preston SL, Wong WM, Chan AO, Poulsom R, Jeffery R, Goodlad RA, Mandir N, Elia G, Novelli M, Bodmer WF, Tomlinson IP, Wright NA (2003) Bottom-up histogenesis of colorectal adenomas: origin in the monocryptal adenoma and initial expansion by crypt fi ssion. Cancer Res 63:3819-3825
48. Rothwell PM, Wilson M, Elwin CE, Norrving B, Algra A, Warlow CP, Meade TW (2010) Longterm effect of aspirin on colorectal cancer incidence and mortality: 20-year follow-up of fi ve randomised trials. Lancet 376:1741-1750
49. Rubinfeld B, Albert I, Porfi ri E, Fiol C, Munemitsu S, Polakis P (1996) Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 272:1023-1026
50. Sangiorgi E, Capecchi MR (2008) Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 40:915-920
51. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ, Clevers H (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459:262-265
52. 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 (2010) Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469:415-418
53. Shibata H, Toyama K, Shioya H, Ito M, Hirota M, Hasegawa S, Matsumoto H, Takano H, Akiyama T, Toyoshima K, Kanamaru R, Kanegae Y, Saito I, Nakamura Y, Shiba K, Noda T (1997) Rapid colorectal adenoma formation initiated by conditional targeting of the Apc gene. Science 278:120-123
54. Shih IM, Wang TL, Traverso G, Romans K, Hamilton SR, Ben-Sasson S, Kinzler KW, Vogelstein B (2001) Top-down morphogenesis of colorectal tumors. Proc Natl Acad Sci U S A 98:2640-2645
55. Smits R, Kielman MF, Breukel C, Zurcher C, Neufeld K, Jagmohan-Changur S, Hofland N, van Dijk J, White R, Edelmann W, Kucherlapati R, Khan PM, Fodde R (1999) Apc1638T: a mouse model delineating critical domains of the adenomatous polyposis coli protein involved in tumorigenesis and development. Genes Dev 13:1309-1321
56. Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M, Kroon-Veenboer C, Barker N, Klein AM, van Rheenen J, Simons BD, Clevers H (2010) Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143:134-144
57. Spaderna S, Schmalhofer O, Hlubek F, Berx G, Eger A, Merkel S, Jung A, Kirchner T, Brabletz T (2006) A transient, EMT-linked loss of basement membranes indicates metastasis and poor survival in colorectal cancer. Gastroenterology 131:830-840
58. Steigerwald K, Behbehani GK, Combs KA, Barton MC, Groden J (2005) The APC tumor suppressor promotes transcription-independent apoptosis in vitro. Mol Cancer Res 3:78-89
59. Su LK, Kinzler KW, Vogelstein B, Preisinger AC, Moser A, Luongo C, Gould KA, Dove WF (1992) Multiple intestinal neoplasia caused by mutations in the murine homolog of the APC gene. Science 256:668-670
60. Takeda N, Jain R, LeBoeuf MR, Wang Q, Lu MM, Epstein JA (2011) Interconversion between intestinal stem cell populations in distinct niches. Science 334:1420-1424
61. Tian G, Finley D (2012) Cell biology: destruction deconstructed. Nature 482:170-171
62. Totafurno J, Bjerknes M, Cheng H (1987) The crypt cycle. Crypt and villus production in the adult intestinal epithelium. Biophys J 52:279-294
63. van Es JH, Jay P, Gregorieff A, van Gijn ME, Jonkheer S, Hatzis P, Thiele A, van den Born M, Begthel H, Brabletz T, Taketo MM, Clevers H (2005) Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol 7:381-386
64. Vermeulen L, De Sousa EMF, 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 (2010) Wnt activity defi nes colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 12:468-476
65. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A, Waldvogel B, Vannier C, Darling D, zur Hausen A, Brunton VG, Morton J, Sansom O, Schuler J, Stemmler MP, Herzberger C, Hopt U, Keck T, Brabletz S, Brabletz T (2009) The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 11:1487-1495
66. Wright NA, Alison M (1984) The biology of epithelial cell populations. Clarendon, Oxford
67. Wright NA, Irwin M (1982) The kinetics of villus cell populations in the mouse small intestine. I. Normal villi: the steady state requirement. Cell Tissue Kinet 15:595-609
68. Zhu L, Gibson P, Currle DS, Tong Y, Richardson RJ, Bayazitov IT, Poppleton H, Zakharenko S, Ellison DW, Gilbertson RJ (2009) Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature 457:603-607