The Nucleocytoplasmic Shuttling of E2F4 Is Involved in the Regulation of Human Intestinal Epithelial Cell Proliferation and Differentiation

Journal of Cellular Physiology

Volumn 199, Issue 2, 2004, Pages 262-273

  Deschênes, Claude ^a   Alvarez, Laetitia ^a   Lizotte, Marie Ève ^a   Vézina, Anne ^a   Rivard, Nathalie ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN P130; RETINOBLASTOMA PROTEIN; SERINE; THREONINE; TRANSCRIPTION FACTOR E2F4;

ARTICLE; CANCER CELL; CELL CYCLE G0 PHASE; CELL DIFFERENTIATION; CELL NUCLEUS; CELL PROLIFERATION; COLON CANCER; CONTROLLED STUDY; CYTOPLASM; FETUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTESTINE CRYPT; INTESTINE EPITHELIUM CELL; INTESTINE VILLUS; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SERUM; STAINING;

CELL CYCLE; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL DIVISION; CELL NUCLEUS; CELLS, CULTURED; CYTOPLASM; DNA-BINDING PROTEINS; E2F TRANSCRIPTION FACTORS; E2F1 TRANSCRIPTION FACTOR; E2F4 TRANSCRIPTION FACTOR; ENZYME INHIBITORS; EPITHELIAL CELLS; FETUS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOBLOTTING; INTESTINES; MITOGEN-ACTIVATED PROTEIN KINASES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN TRANSPORT; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 17144458573     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.10455     Document Type: Article

References (70)

1. Aliaga JC, Deschênes C, Beaulieu JF, Calvo EL, Rivard N. 1999. Requirement of the MAP kinase cascade for cell cycle progression and differentiation of human intestinal cells. Am J Physiol 277:G631-G641.
2. Altiok S, Xu M, Spiegelman BM. 1997. PPARγ induces cell cycle withdrawal: Inhibition of E2F/DP DNA-binding activity via down-regulation of PP2A. Genes Dev 11:1987-1998.
3. Beijersbergen RL, Kerkhoven RM, Zhu L, Carlee L, Voorhoeve PM, Bernards R. 1994. E2F-4, a new member of the E2F gene family, has oncogenic activity and associates with p107 in vivo. Genes Dev 8(22):2680-2690.
4. Bremner R, Cohen BL, Sopta M, Hamel PA, Ingles CJ, Gallie BL, Phillips RA. 1995. Direct transcriptional repression by pRB and its reversal by specific cyclins. Mol Cell Biol 15(6):3256-3265.
5. Cairnie AB, Lamerton LF, Steel GG. 1965. Cell proliferation studies in the intestinal epithelium of the rat. II. Theoretical aspects. Exp Cell Res 39(2):539-553.
6. Chellappan SP, Hiebert S, Mudryj M, Horowitz JM, Nevins JR. 1991. The E2F transcription factor is a cellular target for the RB protein. Cell 65:1053-1061.
7. Chestukhin A, Litovchick L, Rudich K, De Caprio JA. 2002. Nucleocytoplasmic shuttling of p130/RBL2: Novel regulatory mechanism. Mol Cell Biol 22:453-468.
8. Chittenden T, Livingston DM, De Caprio JA. 1993. Cell cycle analysis of E2F in primary T cells reveals novel E2F complexes and biochemically distinct forms of free E2F. Mol Cell Biol 13:3975-3983.
9. Cinti C, Claudio PP, Howard CM, Neri LM, Fu Y, Leoncini L, Tosi GM, Maraldi NM, Giordano A. 2000. Genetic alterations disrupting the nuclear localization of the retinoblastoma-related gene RB2/p130 in human tumor cell lines and primary tumors. Cancer Res 60:383-389.
10. Corbeil HB, Whyte P, Branton PE. 1995. Characterization of transcription factor E2F complexes during muscle and neuronal differentiation. Oncogene 11:909-920.
11. Dagnilo L, Fry CJ, Bartley SM, Farnham P, Gallie BL, Phillips RA. 1997. Expression patterns of the E2F family of transcription factors during murine epithelial development. Cell Growth Differ 8:553-563.
12. Kip1 in human intestinal cell differentiation. Gastroenterology 120:423-438.
13. 1 arrest and suppression of CDK2 and CDK4. Am J Physiol 275:C1193-C1200.
14. Ding Q, Wang Q, Dong Z, Evers BM. 2000. Characterization and regulation of E2F activity during Caco-2 cell differentiation. Am J Physiol 278:C110-C117.
15. Doell RG, Rosen G, Kretchmer N. 1965. Immunochemical studies of intestinal disaccharidases during normal and precocious development. Proc Natl Acad Sci USA 54:1268-1273.
16. Enslen H, Brancho DM, Davis RJ. 2000. Molecular determinants that mediate selective activation of p38 MAP kinase isoforms. Embo J 19:1301-1311.
17. Evers BM, Ko TC, Li J, Thompson EA. 1996. Cell cycle protein suppression and p21 induction in differentiating Caco-2 cells. Am J Physiol 271:G722-G727.
18. Field SJ, Tsai FY, Kuo F, Zubiaga AM, Kaelin WG, Jr., Livingston DM, Orkin SH, Greenberg ME. 1996. E2F-1 functions in mice to promote apoptosis and suppress proliferation. Cell 85(4):549-561.
19. Frey MR, Clark JA, Leontieva O, Uronis JM, Black AR, Black JD. 2000. Protein kinase C signaling mediates a program of cell cycle withdrawal in the intestinal epithelium. J Cell Biol 151:763-778.
20. Furukawa Y, Iwase S, Kikuchi J, Nakamura M, Yamada H, Matsuda M. 1999. Transcriptional repression of the E2F-1 gene by interferon-alpha is mediated through induction of E2F-4/pRB and E2F-4/p130 complexes. Oncogene 18(11):2003-2014.
21. Gill RM, Hamel PA. 2000. Subcellular compartimentalization of E2F family members is required for maintenance of the postmitotic state in terminally differentiated muscle. J Cell Biol 148:1187-1201.
22. Gill RM, Hamel PA, Zhe J, Zacksenhaus E, Gallie BL, Phillips RA. 1994. Characterization of the human RB1 promoter and of elements involved in transcriptional regulation. Cell Growth Differ 5:467-474.
23. Gordon JA. 1991. Use of vanadate as protein-phosphotyrosine phosphatase inhibitor. Methods Enzymol 201:477-482.
24. Green C, Chatterjee R, McGarridge HHG, Ahmed F, Thomas NSB. 2000. p107 is active in the nucleolus in non-dividing human granulosa lutein cells. J Mol Endocrinol 25:275-286.
25. Gu Y, Rosenblatt J, Morgan DO. 1992. Cell cycle regulation of CDK2 activity by phosphorylation of Thr160 and Tyr15. EMBO J 11:3995-4005.
26. Honkanen RE, Zwiller J, Moore RE, Daily SL, Khatra BS, Dukelow M, Boynton AL. 1990. Characterization of microcystin-LR, a potent inhibitor of type 1 and type 2A protein phosphatases. J Biol Chem 265(32):19401-19404.
27. Houde M, Laprise P, Jean D, Blais M, Asselin C, Rivard N. 2001. Intestinal epithelial cell differentiation involves activation of p38 mitogen-activated protein kinase that regulates the homeobox transcription factor CDX2. J Biol Chem 276(24):21885-21894.
28. Ikeda M, Orimo H, Moriyama H, Nakajima E, Matsubara N, Mibu R, Tanaka N, Shimada T, Kimura A, Shimizu K. 1998. Close correlation between mutations of E2F4 and hMSH3 genes in colorectal cancers with microsatellite instability. Cancer Res 58:594-598.
29. Jiang H, Lin J, Young SM, Goldstein NI, Waxman S, Davila V, Chelappan SP, Fisher PB. 1995. Cell cycle gene expression and E2F transcription factor in human melanoma cells induced to terminally differentiate. Oncogene 11:1179-1189.
30. Johnson DG, Schwarz JK, Cress WD, Nevins JR. 1993. Expression of transcription factor E2F1 induces quiescent cells to enter S phase. Nature 365:349-352.
31. Karam SM. 1999. Lineage commitment and maturation of epithelial cells in the gut. Front Biosci 4:D286-D298.
32. Kiess M, Gill RM, Hamel PA. 1995. Expression and activity of the retinoblastoma protein (pRb)-family proteins, p107 and p130, during L6 myoblast differentiation. Cell Growth Differ 6:1287-1298.
33. Kim SH, Roth KA, Coopersmith CM, Pipas JM, Gordon JI. 1994. Expression of wild-type and mutant Simian virus 40 large tumor antigen in villus-associated enterocytes of trangenic mice. Proc Natl Acad Sci USA 91:6914-6918.
34. Kowalik TF, DeGregori J, Schwarz JK, Nevins JR. 1995. E2F1 overexpression in quiescent fibroblasts leads to induction of cellular DNA synthesis and apoptosis. J Virol 69(4):2491-2500.
35. Krek W, Xu G, Livingston DM. 1995. Cyclin A-kinase regulation of E2F1 DNA binding function underlies suppression of an S phase checkpoint. Cell 83:1149-1158.
36. La Thangue NB. 1994. DP and E2F proteins: Components of a heterotrimeric transcription factor implicated in cell cycle control. Curr Opin Cell Biol 6:443-450.
37. MacCallum DE, Hall PA. 1999. Biochemical characterization of pKi67 with the identification of a mitotic-specific form associated with hyperphosphorylation and altered DNA binding. Exp Cell Res 10:186-198.
38. Mulligan G, Jacks T. 1998. The retinoblastoma gene family: Cousins with overlapping interests. Trends Genet 14:223-229.
39. Paramio JM, Segrelles C, Casanova ML, Jorcano JL. 2000. Opposite functions for E2F1 and E2F4 in human epidermal keratinocyte differentiation. J Biol Chem 275:41219-41226.
40. 1 events and regulation of cell proliferation. Science 246:603-608.
41. Perreault N, Beaulieu JF. 1996. Use of the dissociating enzyme thermolysin to generate viable human intestinal epithelial cell cultures. Exp Cell Res 224:354-364.
42. Perreault N, Beaulieu JF. 1998. Primary cultures of fully differentiated and pure human intestinal epithelial cells. Exp Cell Res 245:34-42.
43. Persengiev SP, Kondova II, Kilpatrick DL. 1999. E2F4 actively promotes the initiation and maintenance of nerve growth factor-induced cell differentiation. Mol Cell Biol 19:6048-6056.
44. Peterson GL. 1977. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83:346-356.
45. Pierce AM, Gimenez-Conti IB, Schneider-Broussard R, Martinez LA, Conti CJ, Johnson DG. 1998. Increased E2F1 activity induces skin tumors in mice heterozygous and nullizygous for p53. Proc Natl Acad Sci USA 95(15):8858-8863.
46. Pierce AM, Schneider-Broussard R, Gimenez-Conti IB, Russell JL, Conti CJ, Johnson DG. 1999. E2F1 has both oncogenic and tumor-suppressive properties in a transgenic model. Mol Cell Biol 19(9):6408-6414.
47. Puri PL, Cimino L, Fulco M, Zimmerman C, LaThangue N, Giordano A, Graessmann A, Levrero M. 1998. Regulation of E2F4 mitogenic activity during terminal differentiation by its heterodimerization partners for nuclear translocation. Cancer Res 58:1325-1331.
48. Quaroni A, Isselbacher KJ. 1985. Study of intestinal cell differentiation with monoclonal antibodies to intestinal cell surface components. Dev Biol 111(2):267-279.
49. Rempel RE, Saenz-Robles MT, Storms R, Morham S, Ishida S, Engel A, Jakoi L, Melhem MF, Pipas JM, Smith C, Nevins JR. 2000. Loss of E2F4 activity leads to abnormal development of multiple cellular lineages. Mol Cell 6:293-306.
50. Rhoads JM, Argenzio RA, Chen W, Graves LM, Licato LL, Blikslager AT, Smith J, Gatzy J, Brenner DA. 2000. Glutamine metabolism stimulates intestinal cell MAPKs by a cAMP-inhibitable, Raf-independent mechanism. Gastroenterology 118:90-100.
51. Sardet C, Vidal M, Cobrinik D, Geng Y, Onufryk C, Chen A, Weinberg RA. 1995. E2F-4 and E2F-5, two members of the E2F family, are expressed in the early phases of the cell cycle. Proc Natl Acad Sci USA 92:2403-2407.
52. Shin EK, Shin A, Paulding C, Schaffausen B, Yee AS. 1995. Multiple changes in E2F function occur upon muscle differentiation. Mol Cell Biol 15:2252-2262.
53. Singh P, Wong SH, Hong W. 1994. Overexpression of E2F-1 in rat embryo fibroblasts leads to neoplastic transformation. EMBO J 13(14):3329-3338.
54. Slansky JE, Farnham PJ. 1996. Introduction to the E2F family: Protein structure and gene regulation. Curr Topic Microbiol Imunol 208:1-30.
55. Slansky JE, Li Y, Kaelin WG, Farnham PG. 1993. A protein synthesis-dependent increase in E2F1 mRNA correlates with growth regulation of the dihydrofolate reductase promoter. Mol Cell Biol 13:1610-1618.
56. Stappenbeck TS, Wong MH, Saam JR, Mysorekar IU, Gordon JI. 1998. Notes from some crypt watchers: Regulation of renewal in the mouse intestinal epithelium. Curr Opin Cell Biol 10:702-709.
57. Streeter GL. 1920. Weight, sitting head, head size, foot length, and menstrual age of the human embryo. Contr Embryol 11:143-179.
58. Tian JQ, Quaroni A. 1999. Involvement of p21(WAF1/Cip1) and p27(Kip1) in intestinal epithelial cell differentiation. Am J Physiol 276:C1245-C1258.
59. Vachon PH, Beaulieu JF. 1995. Extracellular heterotrimeric laminin promotes differentiation in human enterocytes. Am J Physiol 268: G857-G867.
60. Verona R, Moberg K, Estes S, Starz M, Vernon JP, Lees JA. 1997. E2F activity is regulated by cell cycle-dependent changes in subcellular localization. Mol Cell Biol 17:7268-7282.
61. Wang Q, Wang X, Hernandez A, Hellmich MR, Gatalica Z, Evers BM. 2002. Regulation of TRAIL expression by the phosphatidylinositol 3-kinase/Akt/GSK-3 pathway in human colon cancer cells. J Biol Chem 277:36602-36610.
62. Weinberg RA. 1996. E2F and cell proliferation: A world turned upside down. Cell 85(4):457-459.
63. Weintraub SJ, Prater CA, Dean DC. 1992. Retinoblastoma protein switches the E2F site from positive to negative element. Nature 358(6383):259-261.
64. 1 to S phase transition. J Biol Chem 272:4483-4492.
65. Xu X, Levine AJ. 1994. p53 and E2F-1 cooperate to mediate apoptosis. Proc Natl Acad Sci USA 91(9):3602-3606.
66. Xu M, Sheppard KA, Peng CY, Yee AS, Piwnica-Worms H. 1994. Cyclin A/cdk2 dinds directly to E2F1 and inhibits the DNA-binding activity of E2F1/DP1 by phosphorylation. Mol Cell Biol 14:8420-8431.
67. Xu G, Livingston DM, Krek W. 1995. Multiple members of the E2F transcription factor family are the products of oncogenes. Proc Natl Acad Sci USA 92(5):1357-1361.
68. Yamasaki L, Jacks T, Bronson R, Goillot E, Harlow E, Dyson NJ. 1996. Tumor induction and tissue atrophy in mice lacking E2F-1. Cell 85(4):537-548.
69. Zacksenhaus E, Jiang Z, Phillips RA, Gallie BL. 1996. Dual mechanisms of repression of E2F1 activity by the retinoblastoma gene product. EMBO J 15(21):5917-5927.
70. 1-S phase progression. Curr Opin Cell Biol 9:773-781.