Corruption of homeostatic mechanisms in the guanylyl cyclase C signaling pathway underlying colorectal tumorigenesis

Cancer Biology and Therapy

Volumn 10, Issue 3, 2010, Pages 211-218

  Li, Peng ^a   Waldman, Scott A ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

APC; Apoptosis; CDX2; Chromosomal instability; Colon cancer; Guanylyl cyclase C; Homeostasis; Migration and adhesion; p53; Proliferation

Indexed keywords

CARCINOGEN; GUANYLATE CYCLASE; GUANYLYL CYCLASE C; TRANSCRIPTION FACTOR CDX2; UNCLASSIFIED DRUG;

APC GENE; APOPTOSIS; CANCER GROWTH; CARCINOGENESIS; CELL ADHESION; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL REGENERATION; CELL TRANSFORMATION; COLORECTAL CANCER; COLORECTAL TUMORIGENESIS; GENE MUTATION; GENE OVEREXPRESSION; GENE SILENCING; GENOMICS; HOMEOSTASIS; HUMAN; INTESTINE CRYPT; INTESTINE EPITHELIUM CELL; INTESTINE VILLUS; MALIGNANT TRANSFORMATION; NONHUMAN; ONCOGENE; REGULATORY MECHANISM; REVIEW; TUMOR SUPPRESSOR GENE;

ANIMALS; CELL GROWTH PROCESSES; CELL TRANSFORMATION, NEOPLASTIC; COLORECTAL NEOPLASMS; HOMEOSTASIS; HUMANS; RECEPTORS, GUANYLATE CYCLASE-COUPLED; RECEPTORS, PEPTIDE; SIGNAL TRANSDUCTION;

EID: 77955504104     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.10.3.12539     Document Type: Review

References (80)

1. Cho KR, Vogelstein B. Suppressor gene alterations in the colorectal adenoma-carcinoma sequence. J Cell Biochem Suppl 1992; 16:137-41.
2. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, Kinzler KW. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in betacatenin or APC. Science 1997; 275:1787-90. (Pubitemid 27136715)
3. Mahmoud NN, Boolbol SK, Bilinski RT, Martucci C, Chadburn A, Bertagnolli MM. Apc gene mutation is associated with a dominant-negative effect upon intestinal cell migration. Cancer Res 1997; 57:5045-50. (Pubitemid 27498118)
4. Caldwell CM, Kaplan KB. The role of APC in mitosis and in chromosome instability. Adv Exp Med Biol 2009; 656:51-64.
5. Rudolph KL, Millard M, Bosenberg MW, DePinho RA. Telomere dysfunction and evolution of intestinal carcinoma in mice and humans. Nat Genet 2001; 28:155-9. (Pubitemid 32538061)
6. Sansom OJ, Reed KR, Hayes AJ, Ireland H, Brinkmann H, Newton IP, et al. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation and migration. Genes Dev 2004; 18:1385-90.
7. + myeloid cells that promote invasion. Nat Genet 2007; 39:467-75.
8. Biswas S, Chytil A, Washington K, Romero-Gallo J, Gorska AE, Wirth PS, et al. Transforming growth factor beta receptor type II inactivation promotes the establishment and progression of colon cancer. Cancer Res 2004; 64:4687-92.
9. Waldman T, Zhang Y, Dillehay L, Yu J, Kinzler K, Vogelstein B, Williams J. Cell cycle arrest versus cell death in cancer therapy. Nat Med 1997; 3:1034-6. (Pubitemid 27391962)
10. el-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, et al. WAF1, a potential mediator of p53 tumor suppression. Cell 1993; 75:817-25.
11. Symonds H, Krall L, Remington L, Saenz-Robles M, Lowe S, Jacks T, Van Dyke T. p53-dependent apoptosis suppresses tumor growth and progression in vivo. Cell 1994; 78:703-11. (Pubitemid 24268592)
12. Lozano G, Elledge SJ. p53 sends nucleotides to repair DNA. Nature 2000; 404:24-5.
13. Sivagnanasundaram S, Islam I, Talbot I, Drummond F, Walters JR, Edwards YH. The homeobox gene CDX2 in colorectal carcinoma: a genetic analysis. Br J Cancer 2001; 84:218-25. (Pubitemid 32113449)
14. da Costa LT, He TC, Yu J, Sparks AB, Morin PJ, Polyak K, et al. CDX2 is mutated in a colorectal cancer with normal APC/beta-catenin signaling. Oncogene 1999; 18:5010-4.
15. Chawengsaksophak K, James R, Hammond VE, Kontgen F, Beck F. Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 1997; 386:84-7.
16. Park J, Schulz S, Waldman SA. Intestine-specific activity of the human guanylyl cyclase C promoter is regulated by Cdx2. Gastroenterology 2000; 119:89-96. (Pubitemid 30452582)
17. Notterman DA, Alon U, Sierk AJ, Levine AJ. Transcriptional gene expression profiles of colorectal adenoma, adenocarcinoma, and normal tissue examined by oligonucleotide arrays. Cancer Res 2001; 61:3124-30.
18. Zhang L, Zhou W, Velculescu VE, Kern SE, Hruban RH, Hamilton SR, et al. Gene expression profiles in normal and cancer cells. Science 1997; 276:1268-72.
19. Lin JE, Li P, Snook AE, Schulz S, Dasgupta A, Hyslop TM, et al. The hormone receptor GUCY2C suppresses intestinal tumor formation by inhibiting AKT signaling. Gastroenterology 138:241-54.
20. Li P, Schulz S, Bombonati A, Palazzo JP, Hyslop TM, Xu Y, et al. Guanylyl cyclase C suppresses intestinal tumorigenesis by restricting proliferation and maintaining genomic integrity. Gastroenterology 2007; 133:599-607.
21. Montgomery RK, Mulberg AE, Grand RJ. Development of the human gastrointestinal tract: twenty years of progress. Gastroenterology 1999; 116:702-31.
22. Potten CS, Loeffler M. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 1990; 110:1001-20.
23. Nordgaard I, Mortensen PB. Digestive processes in the human colon. Nutrition 1995; 11:37-45.
24. Bach SP, Renehan AG, Potten CS. Stem cells: the intestinal stem cell as a paradigm. Carcinogenesis 2000; 21:469-76.
25. Secor SM. Gastric function and its contribution to the postprandial metabolic response of the Burmese python Python molurus. J Exp Biol 2003; 206:1621-30.
26. Koldovsky O, Dobiasova M, Hahn P, Kolinska J, Kraml J, Pacha J. Development of gastrointestinal functions. Physiol Res 1995; 44:341-8.
27. Schonhoff SE, Giel-Moloney M, Leiter AB. Minireview: Development and differentiation of gut endocrine cells. Endocrinology 2004; 145:2639-44. (Pubitemid 38686209)
28. Bry L, Falk P, Huttner K, Ouellette A, Midtvedt T, Gordon JI. Paneth cell differentiation in the developing intestine of normal and transgenic mice. Proc Natl Acad Sci USA 1994; 91:10335-9.
29. Hall PA, Coates PJ, Ansari B, Hopwood D. Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J Cell Sci 1994; 107:3569-77.
30. Duprey P, Chowdhury K, Dressler GR, Balling R, Simon D, Guenet JL, Gruss P. A mouse gene homologous to the Drosophila gene caudal is expressed in epithelial cells from the embryonic intestine. Genes Dev 1988; 2:1647-54.
31. Subramanian V, Meyer B, Evans GS. The murine Cdx1 gene product localises to the proliferative compartment in the developing and regenerating intestinal epithelium. Differentiation 1998; 64:11-8.
32. Lorentz O, Duluc I, Arcangelis AD, Simon-Assmann P, Kedinger M, Freund JN. Key role of the Cdx2 homeobox gene in extracellular matrix-mediated intestinal cell differentiation. J Cell Biol 1997; 139:1553-65.
33. Suh E, Chen L, Taylor J, Traber PG. A homeodomain protein related to caudal regulates intestine-specific gene transcription. Mol Cell Biol 1994; 14:7340-51. (Pubitemid 24326399)
34. Beck F, Chawengsaksophak K, Waring P, Playford RJ, Furness JB. Reprogramming of intestinal differentiation and intercalary regeneration in Cdx2 mutant mice. Proc Natl Acad Sci USA 1999; 96:7318-23.
35. +/- compound mutant mice. Nat Genet 2003; 35:323-30.
36. Li P, Lin JE, Chervoneva I, Schulz S, Waldman SA, Pitari GM. Homeostatic control of the crypt-villus axis by the bacterial enterotoxin receptor guanylyl cyclase C restricts the proliferating compartment in intestine. Am J Pathol 2007; 171:1847-58.
37. Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, Peters PJ, Clevers H. Depletion of epithelial stemcell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 1998; 19:379-83.
38. -/- colon carcinoma. Science 1997; 275:1784-7.
39. Su LK, Kinzler KW, Vogelstein B, Preisinger AC, Moser AR, Luongo C, et al. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 1992; 256:668-70.
40. Fodde R, Edelmann W, Yang K, van Leeuwen C, Carlson C, Renault B, et al. A targeted chain-termination mutation in the mouse Apc gene results in multiple intestinal tumors. Proc Natl Acad Sci USA 1994; 91:8969-73.
41. Notterman DA, Alon U, Sierk AJ, Levine AJ. Transcriptional gene expression profiles of colorectal adenoma, adenocarcinoma and normal tissue examined by oligonucleotide arrays. Cancer Research 2001; 61:3124-30. (Pubitemid 32691964)
42. Steinbrecher KA, Wowk SA, Rudolph JA, Witte DP, Cohen MB. Targeted inactivation of the mouse guanylin gene results in altered dynamics of colonic epithelial proliferation. Am J Pathol 2002; 161:2169-78.
43. Zeng Q, Phukan S, Xu Y, Sadim M, Rosman DS, Pennison M, et al. Tgfbr1 haploinsufficiency is a potent modifier of colorectal cancer development. Cancer Res 2009; 69:678-86.
44. Hamamoto T, Beppu H, Okada H, Kawabata M, Kitamura T, Miyazono K, Kato M. Compound disruption of smad2 accelerates malignant progression of intestinal tumors in apc knockout mice. Cancer Res 2002; 62:5955-61.
45. Kinzler KW, Vogelstein B. Lessons from hereditary colorectal cancer. Cell 1996; 87:159-70.
46. Lengauer C, Kinzler KW, Vogelstein B. Genetic instability in colorectal cancers. Nature 1997; 386:623-7.
47. Corpet DE, Tache S, Archer MC, Bruce WR. Dehydroalanine and lysinoalanine in thermolyzed casein do not promote colon cancer in the rat. Food Chem Toxicol 2008; 46:3037-42.
48. Bingham SA, Pignatelli B, Pollock JR, Ellul A, Malaveille C, Gross G, et al. Does increased endogenous formation of N-nitroso compounds in the human colon explain the association between red meat and colon cancer? Carcinogenesis 1996; 17:515-23.
49. Spruck CH, Won KA, Reed SI. Deregulated cyclin E induces chromosome instability. Nature 1999; 401:297-300. (Pubitemid 129515546)
50. Caldwell CM, Green RA, Kaplan KB. APC mutations lead to cytokinetic failures in vitro and tetraploid genotypes in Min mice. J Cell Biol 2007; 178:1109-20.
51. Kaplan KB, Burds AA, Swedlow JR, Bekir SS, Sorger PK, Nathke IS. A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nat Cell Biol 2001; 3:429-32.
52. Morrison EE, Wardleworth BN, Askham JM, Markham AF, Meredith DM. EB1, a protein which interacts with the APC tumour suppressor, is associated with the microtubule cytoskeleton throughout the cell cycle. Oncogene 1998; 17:3471-7.
53. Strohmeyer R, Ramirez M, Cole GJ, Mueller K, Rogers J. Association of factor H of the alternative pathway of complement with agrin and complement receptor 3 in the Alzheimer's disease brain. J Neuroimmunol 2002; 131:135-46.
54. Miller RK, Heller KK, Frisen L, Wallack DL, Loayza D, Gammie AE, Rose MD. The kinesin-related proteins, Kip2p and Kip3p, function differently in nuclear migration in yeast. Mol Biol Cell 1998; 9:2051-68.
55. Halberg RB, Katzung DS, Hoff PD, Moser AR, Cole CE, Lubet RA, et al. Tumorigenesis in the multiple intestinal neoplasia mouse: redundancy of negative regulators and specificity of modifiers. Proc Natl Acad Sci USA 2000; 97:3461-6.
56. 2/M-associated cell death after gamma-irradiation. Oncogene 1997; 14:2759-66.
57. Kirsch DG, Santiago PM, di Tomaso E, Sullivan JM, Hou WS, Dayton T, et al. p53 controls radiationinduced gastrointestinal syndrome in mice independent of apoptosis. Science 327:593-6.
58. Reed KR, Meniel VS, Marsh V, Cole A, Sansom OJ, Clarke AR. A limited role for p53 in modulating the immediate phenotype of Apc loss in the intestine. BMC Cancer 2008; 8:162. (Pubitemid 352003729)
59. min/+ mice. Cancer Res 2008; 68:7670-5.
60. Potten CS, Wilson JW, Booth C. Regulation and significance of apoptosis in the stem cells of the gastro-intestinal epithelium. Stem Cells 1997; 15:82-93. (Pubitemid 27152515)
61. Potten CS, Allen TD. Ultrastructure of cell loss in intestinal mucosa. J Ultrastruct Res 1977; 60:272-7.
62. Polzar B, Zanotti S, Stephan H, Rauch F, Peitsch MC, Irmler M, et al. Distribution of deoxyribonuclease I in rat tissues and its correlation to cellular turnover and apoptosis (programmed cell death). Eur J Cell Biol 1994; 64:200-10.
63. Merritt AJ, Potten CS, Kemp CJ, Hickman JA, Balmain A, Lane DP, Hall PA. The role of p53 in spontaneous and radiation-induced apoptosis in the gastrointestinal tract of normal and p53-deficient mice. Cancer Res 1994; 54:614-7. (Pubitemid 24068309)
64. Morin PJ, Vogelstein B, Kinzler KW. Apoptosis and APC in colorectal tumorigenesis. Proc Natl Acad Sci USA 1996; 93:7950-4.
65. Duckworth CA, Pritchard DM. Suppression of apoptosis, crypt hyperplasia and altered differentiation in the colonic epithelia of bak-null mice. Gastroenterology 2009; 136:943-52.
66. Mallo GV, Soubeyran P, Lissitzky JC, Andre F, Farnarier C, Marvaldi J, et al. Expression of the Cdx1 and Cdx2 homeotic genes leads to reduced malignancy in colon cancer-derived cells. J Biol Chem 1998; 273:14030-6.
67. Bonhomme C, Duluc I, Martin E, Chawengsaksophak K, Chenard MP, Kedinger M, et al. The Cdx2 homeobox gene has a tumour suppressor function in the distal colon in addition to a homeotic role during gut development. Gut 2003; 52:1465-71.
68. Mazelin L, Bernet A, Bonod-Bidaud C, Pays L, Arnaud S, Gespach C, et al. Netrin-1 controls colorectal tumorigenesis by regulating apoptosis. Nature 2004; 431:80-4. (Pubitemid 39215111)
69. Qiu W, Carson-Walter EB, Kuan SF, Zhang L, Yu J. PUMA suppresses intestinal tumorigenesis in mice. Cancer Res 2009; 69:4999-5006.
70. Yang WC, Mathew J, Velcich A, Edelmann W, Kucherlapati R, Lipkin M, et al. Targeted inactivation of the p21(WAF1/cip1) gene enhances Apc-initiated tumor formation and the tumor-promoting activity of a western-style high-risk diet by altering cell maturation in the intestinal mucosal. Cancer Res 2001; 61:565-9.
71. 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; 457:608-11.
72. Potten CS. Cell cycles in cell hierarchies. Int J Radiat Biol Relat Stud Phys Chem Med 1986; 49:257-78.
73. Carothers AM, Melstrom KA Jr, Mueller JD, Weyant MJ, Bertagnolli MM. Progressive changes in adherens junction structure during intestinal adenoma formation in Apc mutant mice. J Biol Chem 2001; 276:39094-102.
74. Westbrook AM, Wei B, Braun J, Schiestl RH. Intestinal mucosal inflammation leads to systemic genotoxicity in mice. Cancer Res 2009; 69:4827-34.
75. Boudreau F, Lussier CR, Mongrain S, Darsigny M, Drouin JL, Doyon G, et al. Loss of cathepsin L activity promotes claudin-1 overexpression and intestinal neoplasia. FASEB J 2007; 21:3853-65.
76. Velcich A, Yang W, Heyer J, Fragale A, Nicholas C, Viani S, et al. Colorectal cancer in mice genetically deficient in the mucin Muc2. Science 2002; 295:1726-9. (Pubitemid 34202910)
77. Ezaki T, Guo RJ, Li H, Reynolds AB, Lynch JP. The homeodomain transcription factors Cdx1 and Cdx2 induce E-cadherin adhesion activity by reducing beta-and p120-catenin tyrosine phosphorylation. Am J Physiol Gastrointest Liver Physiol 2007; 293:54-65.
78. Colleypriest BJ, Palmer RM, Ward SG, Tosh D. Cdx genes, inflammation and the pathogenesis of Barrett's metaplasia. Trends Mol Med 2009; 15:313-22.
79. Vernon SW, Gritz ER, Peterson SK, Amos CI, Perz CA, Baile WF, Lynch PM. Correlates of psychologic distress in colorectal cancer patients undergoing genetic testing for hereditary colon cancer. Health Psychol 1997; 16:73-86.
80. Boursi B, Arber N. Current and future clinical strategies in colon cancer prevention and the emerging role of chemoprevention. Curr Pharm Des 2007; 13:2274-82. (Pubitemid 47317035)