Differentiation of Caco-2 cells requires both transcriptional and post-translational down-regulation of Myc

Differentiation

Volumn 83, Issue 3, 2012, Pages 116-127

  Leoni, Bruno Daniele ^a   Natoli, Manuela ^a   Nardella, Marta ^a   Bucci, Barbara ^c   Zucco, Flavia ^a   D'Agnano, Igea ^a,b   Felsani, Armando ^a,b  

^a CNR   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c FATEBENEFRATELLI HOSPITAL   (Italy)

Author keywords

Caco 2 cells; CDX2; Differentiation; Intestine; MYC

Indexed keywords

APC PROTEIN; BETA CATENIN; MYC PROTEIN; TRANSCRIPTION FACTOR CDX2;

APC GENE; ARTICLE; BETA CATENIN GENE; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL POLARITY; CELL STRAIN CACO 2; CONTROLLED STUDY; DOWN REGULATION; GENE; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IN VITRO STUDY; INTESTINE CELL; INTESTINE EPITHELIUM; ONCOGENE MYC; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; TRANSLATION REGULATION;

ADENOMATOUS POLYPOSIS COLI PROTEIN; BETA CATENIN; CACO-2 CELLS; CELL CYCLE; CELL DIFFERENTIATION; ENTEROCYTES; HOMEODOMAIN PROTEINS; HUMANS; INTESTINES; MUTATION; PROTO-ONCOGENE PROTEINS C-MYC; RNA INTERFERENCE;

EID: 81255179847     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2011.10.005     Document Type: Article

References (58)

1. Adhikary S., Eilers M. Transcriptional regulation and transformation by Myc proteins. Nature Reviews Molecular Cell Biology 2005, 6:635-645.
2. Amati B. Myc degradation: dancing with ubiquitin ligases. Proceedings of the National Acadamy of Sciences USA 2004, 101:8843-8844.
3. Amati B., Alevizopoulos K., Vlach J. Myc and the cell cycle. Frontiers in Bioscience 1998, 3:d250-d268.
4. Amati B., Frank S.R., Donjerkovic D., Taubert S. Function of the c-Myc oncoprotein in chromatin remodeling and transcription. Biochimica et Biophysica Acta 2001, 1471:M135-M145.
5. Amati B., Sanchez-Arevalo Lobo V.J. MYC degradation: deubiquitinating enzymes enter the dance. Nature Cell Biology 2007, 9:729-731.
6. Bagchi B., Kumar M., Mani S. CMV promotor activity during ES cell differentiation: potential insight into embryonic stem cell differentiation. Cell Biology International 2006, 30:505-513.
7. Bettess M.D., Dubois N., Murphy M.J., Dubey C., Roger C., Robine S., Trumpp A. c-Myc is required for the formation of intestinal crypts but dispensable for homeostasis of the adult intestinal epithelium. Molecular and Cellular Biology 2005, 25:7868-7878.
8. Brightwell G., Poirier V., Cole E., Ivins S., Brown K.W. Serum-dependent and cell cycle-dependent expression from a cytomegalovirus-based mammalian expression vector. Gene 1997, 194:115-123.
9. Bucci B., D'Agnano I., Amendola D., Citti A., Raza G.H., Miceli R., De Paula U., Marchese R., Albini S., Felsani A., Brunetti E., Vecchione A. Myc down-regulation sensitizes melanoma cells to radiotherapy by inhibiting MLH1 and MSH2 mismatch repair proteins. Clinical Cancer Research 2005, 11:2756-2767.
10. Chantret I., Barbat A., Dussaulx E., Brattain M.G., Zweibaum A. Epithelial polarity, villin expression, and enterocytic differentiation of cultured human colon carcinoma cells: a survey of twenty cell lines. Cancer Research 1988, 48:1936-1942.
11. Clevers H.C. Wnt/beta-catenin signaling in development and disease. Cell 2006, 127:469-480.
12. Czernichow B., Simon-Assmann P., Kedinger M., Arnold C., Parache M., Marescaux J., Zweibaum A., Haffen K. Sucrase-isomaltase expression and enterocytic ultrastructure of human colorectal tumors. Internatioanl Journal of Cancer 1989, 44:238-244.
13. DeSanta F., Albini S., Mezzaroma E., Baron L., Felsani A., Caruso M. pRb-dependent cyclin D3 protein stabilization is required for myogenic differentiation. Molecular and Cellular Biology 2007, 27:7248-7265.
14. Deschenes C., Vezina A., Beaulieu J.F., Rivard N. Role of p27(Kip1) in human intestinal cell differentiation. Gastroenterology 2001, 120:423-438.
15. Diehl J.A., Cheng M., Roussel M.F., Sherr C.J. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes and Development 1998, 12:3499-3511.
16. Ding Q.M., Ko T.C., Evers B.M. Caco-2 intestinal cell differentiation is associated with G1 arrest and suppression of CDK2 and CDK4. American Journal of Physiology 1998, 275:C1193-C1200.
17. Dominguez-Sola D., Ying C.Y., Grandori C., Ruggiero L., Chen B., Li M., Galloway D.A., Gu W., Gautier J., Dalla-Favera R. Non-transcriptional control of DNA replication by c-Myc. Nature 2007, 448:445-451.
18. Evers B.M., Ko T.C., Li J., Thompson E.A. Cell cycle protein suppression and p21 induction in differentiating Caco-2 cells. American Journal of Physiology 1996, 271:G722-G727.
19. Gartel A.L., Serfas M.S., Gartel M., Goufman E., Wu G.S., el-Deiry W.S., Tyner A.L. p21 (WAF1/CIP1) expression is induced in newly nondividing cells in diverse epithelia and during differentiation of the Caco-2 intestinal cell line. Experimental Cell Research 1996, 227:171-181.
20. Gatti G., Maresca G., Natoli M., Florenzano F., Nicolin A., Felsani A., D'Agnano I. MYC prevents apoptosis and enhances endoreduplication induced by paclitaxel. PLoS One 2009, 4:e5442.
21. Gostissa M., Ranganath S., Bianco J.M., Alt F.W. Chromosomal location targets different MYC family gene members for oncogenic translocations. Proceedings of the National Acadamy of Sciences USA 2009, 106:2265-2270.
22. Gregorieff A., Grosschedl R., Clevers H.C. Hindgut defects and transformation of the gastro-intestinal tract in Tcf4(-/-)/Tcf1(-/-) embryos. The EMBO Journal 2004, 23:1825-1833.
23. Gregory M.A., Qi Y., Hann S.R. Phosphorylation by glycogen synthase kinase-3 controls c-myc proteolysis and subnuclear localization. Journal of Biological Chemistry 2003, 278:51606-51612.
24. Gross I., Duluc I., Benameur T., Calon A., Martin E., Brabletz T., Kedinger M., Domon-Dell C., Freund J.N. The intestine-specific homeobox gene Cdx2 decreases mobility and antagonizes dissemination of colon cancer cells. Oncogene 2008, 27:107-115.
25. Halbleib J.M., Saaf A.M., Brown P.O., Nelson W.J. Transcriptional modulation of genes encoding structural characteristics of differentiating enterocytes during development of a polarized epithelium in vitro. Molecular Biology of the Cell 2007, 18:4261-4278.
26. Hanson K.D., Shichiri M., Follansbee M.R., Sedivy J.M. Effects of c-myc expression on cell cycle progression. Molecular and Cellular Biology 1994, 14:5748-5755.
27. He T.C., Sparks A.B., Rago C., Hermeking H., Zawel L., da Costa L.T., Morin P.J., Vogelstein B., Kinzler K.W. Identification of c-MYC as a target of the APC pathway. Science 1998, 281:1509-1512.
28. Huber O., Korn R., McLaughlin J., Ohsugi M., Herrmann B.G., Kemler R. Nuclear localization of beta-catenin by interaction with transcription factor LEF-1. Mechanisms of Development 1996, 59:3-10.
29. Ilyas M., Tomlinson I.P., Rowan A., Pignatelli M., Bodmer W.F. Beta-catenin mutations in cell lines established from human colorectal cancers. Proceedings of the National Acadamy of Sciences USA 1997, 94:10330-10334.
30. Klein P.S., Melton D.A. A molecular mechanism for the effect of lithium on development. Proceedings of the National Acadamy of Sciences USA 1996, 93:8455-8459.
31. Liao D.J., Dickson R.B. c-Myc in breast cancer. Endocrine-Related Cancer 2000, 7:143-164.
32. Mariadason J.M., Arango D., Corner G.A., Aranes M.J., Hotchkiss K.A., Yang W., Augenlicht L.H. A gene expression profile that defines colon cell maturation in vitro. Cancer Research 2002, 62:4791-4804.
33. Mariadason J.M., Bordonaro M., Aslam F., Shi L., Kuraguchi M., Velcich A., Augenlicht L.H. Down-regulation of beta-catenin TCF signaling is linked to colonic epithelial cell differentiation. Cancer Research 2001, 61:3465-3471.
34. Mariadason J.M., Nicholas C., L'Italien K.E., Zhuang M., Smartt H.J., Heerdt B.G., Yang W., Corner G.A., Wilson A.J., Klampfer L., Arango D., Augenlicht L.H. Gene expression profiling of intestinal epithelial cell maturation along the crypt-villus axis. Gastroenterology 2005, 128:1081-1088.
35. Muncan V., Sansom O.J., Tertoolen L., Phesse T.J., Begthel H., Sancho E., Cole A.M., Gregorieff A., de Alboran I.M., Clevers H.C., Clarke A.R. Rapid loss of intestinal crypts upon conditional deletion of the Wnt/Tcf-4 target gene c-Myc. Molecular and Cellular Biology 2006, 26:8418-8426.
36. Natoli M., Leoni B.D., D'Agnano I., D'Onofrio M., Brandi R., Arisi I., Zucco F., Felsani A. Cell growing density affects the structural and functional properties of Caco-2 differentiated monolayer. Journal of Cellular Physiology 2011, 226:1531-1543.
37. Nesbit C.E., Tersak J.M., Prochownik E.V. MYC oncogenes and human neoplastic disease. Oncogene 1999, 18:3004-3016.
38. Orsulic S., Huber O., Aberle H., Arnold S., Kemler R. E-cadherin binding prevents beta-catenin nuclear localization and beta-catenin/LEF-1-mediated transactivation. Journal of Cell Science 1999, 112(Pt 8):1237-1245.
39. Pageot L.P., Perreault N., Basora N., Francoeur C., Magny P., Beaulieu J.F. Human cell models to study small intestinal functions: recapitulation of the crypt-villus axis. Microscopy Research Technique 2000, 49:394-406.
40. Pandrea I.V., Carriere V., Barbat A., Cambier D., Dussaulx E., Lesuffleur T., Rousset M., Zweibaum A. Postmitotic differentiation of colon carcinoma caco-2 cells does not prevent reentry in the cell cycle and tumorigenicity. Experimental and Molecular Pathology 2000, 69:37-45.
41. Penn L.J., Brooks M.W., Laufer E.M., Land H. Negative autoregulation of c-myc transcription. The EMBO Journal 1990, 9:1113-1121.
42. Perlmutter D.H., Punsal P.I. Distinct and additive effects of elastase and endotoxin on expression of alpha 1 proteinase inhibitor in mononuclear phagocytes. Journal of Biological Chemistry 1988, 263:16499-16503.
43. Pinto D., Clevers H.C. Wnt control of stem cells and differentiation in the intestinal epithelium. Experimental Cell Research 2005, 306:357-363.
44. Pinto D., Gregorieff A., Begthel H., Clevers H.C. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes and Development 2003, 17:1709-1713.
45. Ryan K.M., Birnie G.D. Myc oncogenes: the enigmatic family. Biochemical Journal 1996, 314(Pt 3):713-721.
46. Saaf A.M., Halbleib J.M., Chen X., Yuen S.T., Leung S.Y., Nelson W.J., Brown P.O. Parallels between global transcriptional programs of polarizing Caco-2 intestinal epithelial cells in vitro and gene expression programs in normal colon and colon cancer. Molecular Biology of the Cell 2007, 18:4245-4260.
47. Saksela K. Myc genes and their deregulation in lung cancer. Journal of Cellular Biochemistry 1990, 42:153-180.
48. Sambuy Y., de Angelis I., Ranaldi G., Scarino M.L., Stammati A., Zucco F. The Caco-2 cell line as a model of the intestinal barrier: influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell Biology and Toxicology 2005, 21:1-26.
49. Sansom O.J., Meniel V.S., Muncan V., Phesse T.J., Wilkins J.A., Reed K.R., Vass J.K., Athineos D., Clevers H.C., Clarke A.R. Myc deletion rescues Apc deficiency in the small intestine. Nature 2007, 446:676-679.
50. Schroeder A., Mueller O., Stocker S., Salowsky R., Leiber M., Gassmann M., Lightfoot S., Menzel W., Granzow M., Ragg T. The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Molecular Biology 2006, 7:3.
51. Sears R., Nuckolls F., Haura E., Taya Y., Tamai K., Nevins J.R. Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability. Genes and Development 2000, 14:2501-2514.
52. Shah P., Jogani V., Bagchi T., Misra A. Role of Caco-2 cell monolayers in prediction of intestinal drug absorption. Biotechnology Progress 2006, 22:186-198.
53. Shtutman M., Zhurinsky J., Simcha I., Albanese C., D'Amico M., Pestell R., Ben-Ze'ev A. The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proceedings of the National Acadamy of Sciences USA 1999, 96:5522-5527.
54. Stambolic V., Ruel L., Woodgett J.R. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Current Biology 1996, 6:1664-1668.
55. Tetsu O., McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999, 398:422-426.
56. van de Wetering M., Sancho E., Verweij C., de L.W., Oving I., Hurlstone A., van der Horn K., Batlle E., Coudreuse D., Haramis A.P., Tjon-Pon-Fong M., Moerer P., van den Born M., Soete G., Pals S., Eilers M., Medema R., Clevers H.C. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 2002, 111:241-250.
57. van Noort M., Clevers H.C. TCF transcription factors, mediators of Wnt-signaling in development and cancer. Develpomental Biology 2002, 244:1-8.
58. Vervoorts J., Luscher-Firzlaff J., Luscher B. The ins and outs of MYC regulation by posttranslational mechanisms. Journal of Biological Chemistry 2006, 281:34725-34729.