Glucocorticoid alternative effects on proliferating and differentiated mammary epithelium are associated to opposite regulation of cell-cycle inhibitor expression

Journal of Cellular Physiology

Volumn 227, Issue 4, 2012, Pages 1721-1730

  Hoijman, Esteban ^a,b   Rocha Viegas, Luciana ^a,b   Kalko, Susana G ^c   Rubinstein, Natalia ^a,b   Morales Ruiz, Manuel ^c   de Kier Joffé, Elisa Bal ^b   Kordon, Edith C ^a,b   Pecci, Adali ^a,b  

^a INSTITUTO DE FISIOLOGÍA   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CASPASE 3; CRADD PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 2C; DEXAMETHASONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST EPITHELIUM; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; LACTATION; MAMMARY GLAND; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REGULATORY MECHANISM;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P18; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DEXAMETHASONE; DNA-BINDING PROTEINS; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCOCORTICOIDS; LACTATION; MAMMARY GLANDS, ANIMAL; MICE; MICE, INBRED BALB C; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 84855744241     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22896     Document Type: Article

References (59)

1. Altiok S, Groner B. 1998. Regulation of gene expression in mammary epithelial cells by cellular confluence and sequence-specific DNA binding factors. Biochem Soc Symp 63:115-131.
2. Amsterdam A, Tajima K, Sasson R. 2002. Cell-specific regulation of apoptosis by glucocorticoids: Implication to their anti-inflammatory action. Biochem Pharmacol 64:843-850.
3. Atwood CS, Ikeda M, Vonderhaar BK. 1995. Involution of mouse mammary glands in whole organ culture: A model for studying programmed cell death. Biochem Biophys Res Commun 207:860-867.
4. Bagheri-Yarmand R, Vadlamudi RK, Kumar R. 2003. Activating transcription factor 4 overexpression inhibits proliferation and differentiation of mammary epithelium resulting in impaired lactation and accelerated involution. J Biol Chem 278:17421-17429.
5. Ball RK, Friis RR, Schoenenberger CA, Doppler W, Groner B. 1988. Prolactin regulation of beta-casein gene expression and of a cytosolic 120-kd protein in a cloned mouse mammary epithelial cell line. Embo J 7:2089-2095.
6. Berg MN, Dharmarajan AM, Waddell BJ. 2002. Glucocorticoids and progesterone prevent apoptosis in the lactating rat mammary gland. Endocrinology 143:222-227.
7. Brizzi MF, Dentelli P, Rosso A, Calvi C, Gambino R, Cassader M, Salvidio G, Deferrari G, Camussi G, Pegoraro L, Pagano G, Cavallo-Perin P. 2004. RAGE- and TGF-beta receptor-mediated signals converge on STAT5 and p21waf to control cell-cycle progression of mesangial cells: A possible role in the development and progression of diabetic nephropathy. Faseb J 18:1249-1251.
8. Casey TM, Chen H, Plaut K, Chiu JF. 1996. Involution of mouse mammary glands during whole organ culture occurs via apoptosis of epithelial tissue. Cell Biol Int 20:763-767.
9. Casey TM, Plaut K. 2007. The role of glucocorticoids in secretory activation and milk secretion, a historical perspective. J Mammary Gland Biol Neoplasia 12:293-304.
10. 1980. Guide to the care and use of experimental animals Ottawa: Canadian Council of Animal Care.
11. Cella N, Groner B, Hynes NE. 1998. Characterization of Stat5a and Stat5b homodimers and heterodimers and their association with the glucocortiocoid receptor in mammary cells. Mol Cell Biol 18:1783-1792.
12. Chen HJ, Bradley CJ, Meites J. 1976. Stimulation of carcinogen-induced mammary tumor growth in rats by adrenalectomy. Cancer Res 36:1414-1417.
13. Chopin V, Toillon RA, Jouy N, Le Bourhis X. 2004. P21(WAF1/CIP1) is dispensable for G1 arrest, but indispensable for apoptosis induced by sodium butyrate in MCF-7 breast cancer cells. Oncogene 23:21-29.
14. Danes CG, Wyszomierski SL, Lu J, Neal CL, Yang W, Yu D. 2008. 14-3-3 zeta down-regulates p53 in mammary epithelial cells and confers luminal filling. Cancer Res 68:1760-1767.
15. Elson A, Wang Y, Daugherty CJ, Morton CC, Zhou F, Campos-Torres J, Leder P. 1996. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc Natl Acad Sci USA 93:13084-13089.
16. Farrelly N, Lee YJ, Oliver J, Dive C, Streuli CH. 1999. Extracellular matrix regulates apoptosis in mammary epithelium through a control on insulin signaling. J Cell Biol 144:1337-1348.
17. Feng Z, Marti A, Jehn B, Altermatt HJ, Chicaiza G, Jaggi R. 1995. Glucocorticoid and progesterone inhibit involution and programmed cell death in the mouse mammary gland. J Cell Biol 131:1095-1103.
18. Fischer A, Stuckas H, Gluth M, Russell TD, Rudolph MC, Beeman NE, Bachmann S, Umemura S, Ohashi Y, Neville MC, Theuring F. 2007. Impaired tight junction sealing and precocious involution in mammary glands of PKN1 transgenic mice. J Cell Sci 120:2272-2283.
19. Gartel AL, Tyner AL. 1999. Transcriptional regulation of the p21((WAF1/CIP1)) gene. Exp Cell Res 246:280-289.
20. Gaubin M, Autiero M, Basmaciogullari S, Metivier D, Mis hal Z, Culerrier R, Oudin A, Guardiola J, Piatier-Tonneau D. 1999. Potent inhibition of CD4/TCR-mediated T cell apoptosis by a CD4-binding glycoprotein secreted from breast tumor and seminal vesicle cells. J Immunol 162:2631-2638.
21. Heitzer MD, DeFranco DB. 2006. Mechanism of action of Hic-5/androgen receptor activator 55, a LIM domain-containing nuclear receptor coactivator. Mol Endocrinol 20:56-64.
22. Helt CE, Staversky RJ, Lee YJ, Bambara RA, Keng PC, O'Reilly MA. 2004. The Cdk and PCNA domains on p21Cip1 both function to inhibit G1/S progression during hyperoxia. Am J Physiol Lung Cell Mol Physiol 286:L506-L513.
23. Herr I, Ucur E, Herzer K, Okouoyo S, Ridder R, Krammer PH, von Knebel Doeberitz M, Debatin KM. 2003. Glucocorticoid cotreatment induces apoptosis resistance toward cancer therapy in carcinomas. Cancer Res 63:3112-3120.
24. Herzog KH, Chong MJ, Kapsetaki M, Morgan JI, McKinnon PJ. 1998. Requirement for Atm in ionizing radiation-induced cell death in the developing central nervous system. Science 280:1089-1091.
25. Hostetter DR, Loeb CR, Chu F, Craik CS. 2007. Hip is a pro-survival substrate of granzyme B. J Biol Chem 282:27865-27874.
26. Hosack DA, Dennis G Jr, Sherman BT, Lane HC, Lempicki RA. 2003. Identifying biological themes within lists of genes with EASE. Genome Biol 4:R70.
27. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31:e15.
28. Ishida T, Matsuura K, Setoguchi M, Higuchi Y, Yamamoto S. 1994. Enhancement of murine serum amyloid A3 mRNA expression by glucocorticoids and its regulation by cytokines. J Leukoc Biol 56:797-806.
29. Jiang W, Zhu Z, Bhatia N, Agarwal R, Thompson HJ. 2002. Mechanisms of energy restriction: Effects of corticosterone on cell growth, cell cycle machinery, and apoptosis. Cancer Res 62:5280-5287.
30. Katayose D, Wersto R, Cowan KH, Seth P. 1995. Effects of a recombinant adenovirus expressing WAF1/Cip1 on cell growth, cell cycle, and apoptosis. Cell Growth Differ 6:1207-1212.
31. Lawson BR, Baccala R, Song J, Croft M, Kono DH, Theofilopoulos AN. 2004. Deficiency of the cyclin kinase inhibitor p21(WAF-1/CIP-1) promotes apoptosis of activated/memory T cells and inhibits spontaneous systemic autoimmunity. J Exp Med 199:547-557.
32. Li D, Das S, Yamada T, Samuels HH. 2004. The NRIF3 family of transcriptional coregulators induces rapid and profound apoptosis in breast cancer cells. Mol Cell Biol 24:3838-3848.
33. Lund LR, Romer J, Thomasset N, Solberg H, Pyke C, Bissell MJ, Dano K, Werb Z. 1996. Two distinct phases of apoptosis in mammary gland involution: Proteinase-independent and -dependent pathways. Development 122:181-193.
34. Marti A, Ritter PM, Jager R, Lazar H, Baltzer A, Schenkel J, Declercq W, Vandenabeele P, Jaggi R. 2001. Mouse mammary gland involution is associated with cytochrome c release and caspase activation. Mech Dev 104:89-98.
35. Matsuda M, Imaoka T, Vomachka AJ, Gudelsky GA, Hou Z, Mistry M, Bailey JP, Nieport KM, Walther DJ, Bader M, Horseman ND. 2004. Serotonin regulates mammary gland development via an autocrine-paracrine loop. Dev Cell 6:193-203.
36. Merlo GR, Basolo F, Fiore L, Duboc L, Hynes NE. 1995. p53-dependent and p53-independent activation of apoptosis in mammary epithelial cells reveals a survival function of EGF and insulin. J Cell Biol 128:1185-1196.
37. Okahara F, Itoh K, Nakagawara A, Murakami M, Kanaho Y, Maehama T. 2006. Critical role of PICT-1, a tumor suppressor candidate, in phosphatidylinositol 3, 4, 5-trisphosphate signals and tumorigenic transformation. Mol Biol Cell 17:4888-4895.
38. Pang D, Kocherginsky M, Krausz T, Kim SY, Conzen SD. 2006. Dexamethasone decreases xenograft response to Paclitaxel through inhibition of tumor cell apoptosis. Cancer Biol Ther 5:933-940.
39. Polek TC, Talpaz M, Spivak-Kroizman TR. 2006. TRAIL-induced cleavage and inactivation of SPAK sensitizes cells to apoptosis. Biochem Biophys Res Commun 349:1016-1024.
40. Ramalingam A, Hirai A, Thompson EA. 1997. Glucocorticoid inhibition of fibroblast proliferation and regulation of the cyclin kinase inhibitor p21Cip1. Mol Endocrinol 11:577-586.
41. Reichardt HM, Horsch K, Grone HJ, Kolbus A, Beug H, Hynes N, Schutz G. 2001. Mammary gland development and lactation are controlled by different glucocorticoid receptor activities. Eur J Endocrinol 145:519-527.
42. Richert MM, Schwertfeger KL, Ryder JW, Anderson SM. 2000. An atlas of mouse mammary gland development. J Mammary Gland Biol Neoplasia 5:227-241.
43. Rocha-Viegas L, Vicent GP, Baranao JL, Beato M, Pecci A. 2006. Glucocorticoids repress bcl-X expression in lymphoid cells by recruiting STAT5B to the P4 promoter. J Biol Chem 281:33959-33970.
44. Rogatsky I, Hittelman AB, Pearce D, Garabedian MJ. 1999. Distinct glucocorticoid receptor transcriptional regulatory surfaces mediate the cytotoxic and cytostatic effects of glucocorticoids. Mol Cell Biol 19:5036-5049.
45. Rogatsky I, Trowbridge JM, Garabedian MJ. 1997. Glucocorticoid receptor-mediated cell cycle arrest is achieved through distinct cell-specific transcriptional regulatory mechanisms. Mol Cell Biol 17:3181-3193.
46. Romorini L, Coso OA, Pecci A. 2009. Bcl-XL mediates epidermal growth factor dependent cell survival in HC11 mammary epithelial cells. Biochim Biophys Acta 1793:496-505.
47. Schere-Levy C, Buggiano V, Quaglino A, Gattelli A, Cirio MC, Piazzon I, Vanzulli S, Kordon EC. 2003. Leukemia inhibitory factor induces apoptosis of the mammary epithelial cells and participates in mouse mammary gland involution. Exp Cell Res 282:35-47.
48. Schreiber M, Muller WJ, Singh G, Graham FL. 1999. Comparison of the effectiveness of adenovirus vectors expressing cyclin kinase inhibitors p16INK4A, p18INK4C, p19INK4D, p21(WAF1/CIP1) and p27KIP1 in inducing cell cycle arrest, apoptosis and inhibition of tumorigenicity. Oncogene 18:1663-1676.
49. Sengupta S, Wasylyk B. 2004. Physiological and pathological consequences of the interactions of the p53 tumor suppressor with the glucocorticoid, androgen, and estrogen receptors. Ann NY Acad Sci 1024:54-71.
50. Shibata MA, Yoshidome K, Shibata E, Jorcyk CL, Green JE. 2001. Suppression of mammary carcinoma growth in vitro and in vivo by inducible expression of the Cdk inhibitor p21. Cancer Gene Ther 8:23-35.
51. Urtreger AJ, Puricelli LV, Rivelli L, Vidal A, del C M, Sacerdote de Lustig E, Bal de Kier Joffé E. 1997. Modulation of fibronectin expression and proteolytic activity associated with the invasive and metastatic phenotype in 2 new murine mammary tumor cell lines. Int J Oncol 11:489-496.
52. Vicent GP, Monteserin MC, Veleiro AS, Burton G, Lantos CP, Galigniana MD. 1997. 21-Hydroxy-6, 19-oxidoprogesterone: A novel synthetic steroid with specific antiglucocorticoid properties in the rat. Mol Pharmacol 52:749-753.
53. Viegas LR, Vicent GP, Baranao JL, Beato M, Pecci A. 2004. Steroid hormones induce bcl-X gene expression through direct activation of distal promoter P4. J Biol Chem 279:9831-9839.
54. Wang Q, Maniati M, Jabado O, Pavlaki M, Troy CM, Greene LA, Stefanis L. 2006. RAIDD is required for apoptosis of PC12 cells and sympathetic neurons induced by trophic factor withdrawal. Cell Death Differ 13:75-83.
55. Watson CJ, Khaled WT. 2008. Mammary development in the embryo and adult: A journey of morphogenesis and commitment. Development 135:995-1003.
56. Wintermantel TM, Bock D, Fleig V, Greiner EF, Schutz G. 2005. The epithelial glucocorticoid receptor is required for the normal timing of cell proliferation during mammary lobuloalveolar development but is dispensable for milk production. Mol Endocrinol 19:340-349.
57. Wu W, Chaudhuri S, Brickley DR, Pang D, Karrison T, Conzen SD. 2004. Microarray analysis reveals glucocorticoid-regulated survival genes that are associated with inhibition of apoptosis in breast epithelial cells. Cancer Res 64:1757-1764.
58. Yang M, Cao X, Yu MC, Gu JF, Shen ZH, Ding M, Yu De B Zheng S, Liu X. 2008. Potent antitumor efficacy of ST13 for colorectal cancer mediated by oncolytic adenovirus via mitochondrial apoptotic cell death. Hum Gene Ther 19:343-353.
59. Yi Y, Shepard A, Kittrell F, Mulac-Jericevic B, Medina D, Said TK. 2004. p19ARF determines the balance between normal cell proliferation rate and apoptosis during mammary gland development. Mol Biol Cell 15:2302-2311.