Functions of p21 and p27 in the regenerating epithelial linings of the mouse small and large intestine

Cancer Biology and Therapy

Volumn 7, Issue 6, 2008, Pages 873-879

  Zheng, Yu ^a   Bie, Wenjun ^a   Yang, Ruyan ^a   Perekatt, Ansu O ^a   Poole, Aleksandra J ^a   Tyner, Angela L ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Cip; Colon; Cyclin D2; Cyclin D3; Duodenum; Kip; p21; p27; p57

Indexed keywords

CYCLIN D2; CYCLIN D3; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE INHIBITOR; PROTEIN P21; PROTEIN P27; CCND2 PROTEIN, MOUSE; CELL CYCLE PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLINE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL REGENERATION; CELL RENEWAL; COLON CARCINOMA; CONTROLLED STUDY; DOWN REGULATION; EMBRYO DEVELOPMENT; FEMALE; GENE MUTATION; GENOTYPE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INTESTINE EPITHELIUM; MALE; MOUSE; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SMALL INTESTINE; ANIMAL; EPITHELIUM; GENETICS; LARGE INTESTINE; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; REGENERATION; TRANSGENIC MOUSE;

ANIMALS; CELL CYCLE PROTEINS; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLINS; EPITHELIUM; INTESTINE, LARGE; INTESTINE, SMALL; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; REGENERATION; TUMOR SUPPRESSOR PROTEINS;

EID: 56149124254     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.7.6.5868     Document Type: Article

References (61)

1. Rubin DC. Intestinal morphogenesis. Curr Opin Gastroenterol 2007; 23:111-4.
2. Radtke F, Clevers H. Self-renewal and cancer of the gut: two sides of a coin. Science 2005; 307:1904-9.
3. 1-phase progression. Genes Dev 1999; 13:1501-12.
4. Zhang H, Hannon G, Beach D. p21-containing cyclin kinases exist in both active and inactive states. Genes and Development 1994; 8:1750-8.
5. Soos TJ, Kiyokawa H, Yan JS, Rubin MS, Giordano A, DeBlasio A, Bottega S, Wong B, Mendelsohn J, Koff A. Formation of p27-CDK complexes during the human mitotic cell cycle. Cell Growth Differ 1996; 7:135-46.
6. Kip1 with cyclin A-Cdk2 and cyclin D2-Cdk4. J Biol Chem 1997; 272:25863-72.
7. LaBaer J, Garrett MD, Stevenson LF, Slingerland JM, Sandhu C, Chou HS, Fattaey A, Harlow E. New functional activities for the p21 family of CDK inhibitors. Genes Dev 1997; 11:847-62.
8. Cheng M, Olivier P, Diehl JA, Fero M, Roussel MF, Roberts JM, Sherr CJ. The p21(Cip1) and p27(Kip1) CDK 'inhibitors' are essential activators of cyclin D-dependent kinases in murine fibroblasts. Embo J 1999; 18:1571-83.
9. Martin A, Odajima J, Hunt SL, Dubus P, Ortega S, Malumbres M, Barbacid M. Cdk2 is dispensable for cell cycle inhibition and tumor suppression mediated by p27(Kip1) and p21(Cip1). Cancer Cell 2005; 7:591-8.
10. Santamaria PG, Pagano M. The pRb-Cdh1-p27 autoamplifying network. Nat Cell Biol 2007; 9:137-8.
11. Besson A, Dowdy SF, Roberts JM. CDK Inhibitors: Cell Cycle Regulators and Beyond. Dev Cell 2008; 14:159-69.
12. Denicourt C, Dowdy SF. Cip/Kip proteins: more than just CDKs inhibitors. Genes Dev 2004; 18:851-5.
13. Gartel AL, Serfas MS, Gartel M, Goufman E, Wu GS, el-Deiry WS, Tyner AL. p21 (WAF1/CIP1) expression is induced in newly nondividing cells in diverse epithelia and during differentiation of the Caco-2 intestinal cell line. Exp Cell Res 1996; 227:171-81.
14. Tian JQ, Quaroni A. Involvement of p21(WAF1/Cip1) and p27(Kip1) in intestinal epithelial cell differentiation. Am J Physiol 1999; 276:1245-58.
15. Frey MR, Clark JA, Leontieva O, Uronis JM, Black AR, Black JD. Protein kinase C signaling mediates a program of cell cycle withdrawal in the intestinal epithelium. J Cell Biol 2000; 151:763-78.
16. van de Wetering M, Sancho E, Verweij C, de Lau W, Oving I, Hurlstone A, van der Horn K, Batlle E, Coudreuse D, Haramis AP, Tjon-Pon-Fong M, Moerer P, van den Born M, Soete G, Pals S, Eilers M, Medema R, Clevers H. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 2002; 111:241-50.
17. Deschenes C, Vezina A, Beaulieu JF, Rivard N. Role of p27(Kip1) in human intestinal cell differentiation. Gastroenterology 2001; 120:423-38.
18. kip1 during the adaptation response to massive intestinal resection. Am J Physiol Gastrointest Liver Physiol 2006; 290:933-41.
19. Walsh S, Murphy M, Silverman M, Odze R, Antonioli D, Goldman H, Loda M. p27 expression in inflammatory bowel disease-associated neoplasia. Further evidence of a unique molecular pathogenesis. Am J Pathol 1999; 155:1511-8.
20. Brugarolas J, Chandrasekaran C, Gordon JI, Beach D, Jacks T, Hannon GJ. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 1995; 377:552-7.
21. Quaroni A, Tian JQ, Seth P, Ap Rhys C. p27(Kip1) is an inducer of intestinal epithelial cell differentiation. Am J Physiol Cell Physiol 2000; 279:1045-57.
22. Stehr W, Mercer TI, Bernal NP, Erwin CR, Warner BW. Opposing roles for p21(waf1/cip1) and p27(kip1) in enterocyte differentiation, proliferation, and migration. Surgery 2005; 138:187-94.
23. Boulanger J, Vezina A, Mongrain S, Boudreau F, Perreault N, Auclair BA, Laine J, Asselin C, Rivard N. Cdk2-dependent phosphorylation of homeobox transcription factor CDX2 regulates its nuclear translocation and proteasome-mediated degradation in human intestinal epithelial cells. J Biol Chem 2005; 280:18095-107.
24. Mayo C, Lloreta J, Real FX, Mayol X. In vitro differentiation of HT-29 M6 mucus-secreting colon cancer cells involves a trychostatin A and p27(KIP1)-inducible transcriptional program of gene expression. J Cell Physiol 2007.
25. Kiyokawa H, Kineman RD, Manova-Todorova KO, Soares VC, Hoffman ES, Ono M, Khanam D, Hayday AC, Frohman LA, Koff A. Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(Kip1). Cell 1996; 85:721-32.
26. Kwon YH, Jovanovic A, Serfas MS, Kiyokawa H, Tyner AL. P21 functions to maintain quiescence of p27-deficient hepatocytes. J Biol Chem 2002; 277:41417-22.
27. Potten CS, Kellett M, Roberts SA, Rew DA, Wilson GD. Measurement of in vivo proliferation in human colorectal mucosa using bromodeoxyuridine. Gut 1992; 33:71-8.
28. Rubin DC, Ong DE, Gordon JI. Cellular differentiation in the emerging fetal rat small intestinal epithelium: mosaic patterns of gene expression. Proc Natl Acad Sci USA 1989; 86:1278-82.
29. Haegebarth A, Bie W, Yang R, Crawford SE, Vasioukhin V, Fuchs E, Tyner AL. Protein tyrosine kinase 6 negatively regulates growth and promotes enterocyte differentiation in the small intestine. Mol Cell Biol 2006; 26:4949-57.
30. Haegebarth A, Nunez R, Tyner AL. The Intracellular Tyrosine Kinase Brk Sensitizes Non-Transformed Cells to Inducers of Apoptosis. Cell Cycle 2005; 4:1239-46.
31. Silberg DG, Sullivan J, Kang E, Swain GP, Moffett J, Sund NJ, Sackett SD, Kaestner KH. Cdx2 ectopic expression induces gastric intestinal metaplasia in transgenic mice. Gastroenterology 2002; 122:689-96.
32. kip1 Regulates cdk2 activity in the proliferating zone of the mouse intestinal epithelium: potential role in neoplasia. Gastroenterology 2007; 133:232-43.
33. Wei Y, Yu L, Bowen J, Gorovsky MA, Allis CD. Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 1999; 97:99-109.
34. Gartel AL, Tyner AL. The role of the cyclin-dependent kinase inhibitor p21 in apoptosis. Mol Cancer Ther 2002; 1:639-49.
35. Quaroni A, Isselbacher KJ. Study of intestinal cell differentiation with monoclonal antibodies to intestinal cell surface components. Dev Biol 1985; 111:267-79.
36. Taupin D, Podolsky DK. Trefoil factors: initiators of mucosal healing. Nat Rev Mol Cell Biol 2003; 4:721-32.
37. Ouellette AJ. Paneth cell alpha-defensin synthesis and function. Curr Top Microbiol Immunol 2006; 306:1-25.
38. Vassileva G, Huwyler L, Poirier K, Agellon LB, Toth MJ. The intestinal fatty acid binding protein is not essential for dietary fat absorption in mice. Faseb J 2000; 14:2040-6.
39. Agellon LB, Toth MJ, Thomson AB. Intracellular lipid binding proteins of the small intestine. Mol Cell Biochem 2002; 239:79-82.
40. Malaterre J, Mantamadiotis T, Dworkin S, Lightowler S, Yang Q, Ransome MI, Turnley AM, Nichols NR, Emambokus NR, Frampton J, Ramsay RG. c-Myb is Required for Neural Progenitor Cell Proliferation and Maintenance of the Neural Stem Cell Niche in Adult Brain. Stem Cells 2007.
41. Portela Gomes GM, Stridsberg M, Johansson H, Grimelius L. Co-localization of synaptophysin with different neuroendocrine hormones in the human gastrointestinal tract. Histochem Cell Biol 1999; 111:49-54.
42. Batlle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, Huls G, Meeldijk J, Robertson J, van de Wetering M, Pawson T, Clevers H. Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 2002; 111:251-63.
43. 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. Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol 2005; 7:381-6.
44. Cip1 cooperate to restrict proliferative life span in differentiating ovarian cells. J Biol Chem 2003; 278:17021-7.
45. Matsuoka S, Edwards M, Bai C, Parker S, Zhang P, Baldini A, Harper J, Elledge S. p57, a structurally distinct member of the p21 cdk inhibitor family, is a candidate tumor suppressor gene. Genes & Dev 1995; 9:650-62.
46. Bagui TK, Mohapatra S, Haura E, Pledger WJ. p27(Kip1) and p21(Cip1) Are Not Required for the Formation of Active D Cyclin-cdk4 Complexes. Mol Cell Biol 2003; 23:7285-90.
47. Watanabe K, Petro BJ, Sevandal M, Anshuman S, Jovanovic A, Tyner AL. Histochemical examination of periodontal junctional epithelium in p21/p27 double knockout mice. Eur J Oral Sci 2004; 112:253-8
48. Yang R, Bie W, Haegebarth A, Tyner AL. Differential regulation of D-type cyclins in the mouse intestine. Cell Cycle 2006; 5:180-3.
49. Bryja V, Pachernik J, Faldikova L, Krejci P, Pogue R, Nevriva I, Dvorak P, Hampl A. The role of p27(Kip1) in maintaining the levels of D-type cyclins in vivo. Biochim Biophys Acta 2004; 1691:105-16.
50. McKenzie GJ, Bancroft A, Grencis RK, McKenzie AN. A distinct role for interleukin-13 in Th2-cell-mediated immune responses. Curr Biol 1998; 8:339-42.
51. Walker WA, Wu M, Bloch KJ. Stimulation by immune complexes of mucus release from goblet cells of the rat small intestine. Science 1977; 197:370-2.
52. Cheng T, Rodrigues N, Dombkowski D, Stier S, Scadden DT. Stem cell repopulation efficiency but not pool size is governed by p27(kip1). Nat Med 2000; 6:1235-40.
53. cip1/waf1. Science 2000; 287:1804-8.
54. Kip1 safeguards against inflammatory injury. Nat Med 1998; 4:575-80.
55. Sturm A, Itoh J, Jacobberger JW, Fiocchi C. p53 negatively regulates intestinal immunity by delaying mucosal T cell cycling. J Clin Invest 2002; 109:1481-92.
56. Poole AJ, Heap D, Carroll RE, Tyner AL. Tumor suppressor functions for the Cdk inhibitor p21 in the mouse colon. Oncogene 2004; 23:8128-34.
57. -/- mice. Am J Pathol 2005; 166:1239-46.
58. Yang WC, Mathew J, Velcich A, Edelmann W, Kucherlapati R, Lipkin M, Yang K, Augenlicht LH. 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.
59. Cip1 nullizygosity increases tumor metastasis in irradiated mice. Cancer Res 2003; 63:3021-5.
60. kip1 in intestinal tumorigenesis and chemoprevention in the mouse. Cancer Res 2005; 65:9363-8.
61. kip1 is sufficient for large and small intestinal tumorigenesis in the mouse, which can be augmented by a Western-style high-risk diet. Cancer Res 2003; 63:4990-6.