Prolactin and transforming growth factor-β signaling exert opposing effects on mammary gland morphogenesis, involution, and the Akt-forkhead pathway

Molecular Endocrinology

Volumn 18, Issue 5, 2004, Pages 1171-1184

  Bailey, Jason P ^a   Nieport, Kathryn M ^a   Herbst, Matthew P ^a   Srivastava, Sunil ^a   Serra, Rosa A ^a,c   Horseman, Nelson D ^a,b  

^a UNIVERSITY OF CINCINNATI   (United States)

^b University of Alabama Birmingham ^*  (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; PROLACTIN; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; TRANSCRIPTION FACTOR FKHR; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST EPITHELIUM; CELL SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; GENE OVEREXPRESSION; MALE; MAMMARY GLAND; MORPHOGENESIS; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REACTION TIME; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; APOPTOSIS; CELLS, CULTURED; EPITHELIAL CELLS; FEMALE; MAMMARY GLANDS, ANIMAL; MICE; MICE, TRANSGENIC; MORPHOGENESIS; PROLACTIN; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA; MUS MUSCULUS;

EID: 2342579573     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2003-0345     Document Type: Article

References (53)

1. Horseman ND 1999 Prolactin and mammary gland development. J Mammary Gland Biol Neoplasia 4:79-88
2. Strange R, Li F, Saurer S, Burkhardt A, Friis RR 1992 Apoptotic cell death and tissue remodelling during mouse mammary gland involution. Development 115: 49-58
3. Wilde CJ, Knight CH, Flint DJ 1999 Control of milk secretion and apoptosis during mammary involution. J Mammary Gland Biol Neoplasia 4:129-136
4. Talhouk RS, Chin JR, Unemori EN, Werb Z, Bissell MJ 1991 Proteinases of the mammary gland: developmental regulation in vivo and vectorial secretion in culture. Development 112:439-449
5. Faure E, Heisterkamp N, Groffen J, Kaartinen V 2000 Differential expression of TGF-β isoforms during postlactational mammary gland involution. Cell Tissue Res 300: 89-95
6. Metcalfe AD, Gilmore A, Klinowska T, Oliver J, Valentijn AJ, Brown R, Ross A, MacGregor G, Hickman JA, Streull CH 1999 Developmental regulation of Bcl-2 family protein expression in the involuting mammary gland. J Cell Sci 112:1771-1783
7. Baik MG, Lee MJ, Choi YJ 1998 Gene expression during involution of mammary gland. Int J Mol Med 2:39-44 (Review)
8. Hennighausen L, Robinson GW, Wagner KU, Liu W 1997 Prolactin signaling in mammary gland development. J Biol Chem 272:7567-7569
9. Schorr K, Li M, Krajewski S, Reed JC, Furth PA 1999 Bcl-2 gene family and related proteins in mammary gland involution and breast cancer. J Mammary Gland Biol Neoplasia 4:153-164
10. Krumenacker JS, Narang VS, Buckley DJ, Buckley AR 2001 Prolactin signaling to pim-1 expression: a role for phosphatidylinositol 3-kinase. J Neuroimmunol 113: 249-259
11. Al-Sakkaf KA, Mooney LM, Dobson PR, Brown BL 2000 Possible role for protein kinase B in the anti-apoptotic effect of prolactin in rat Nb2 lymphoma cells. J Endocrinol 167:85-92
12. Tessier C, Prigent-Tessier A, Ferguson-Gottschall S, Gu Y, Gibori G 2001 PRL antiapoptotic effect in the rat decidua involves the PI3K/protein kinase B-mediated inhibition of caspase-3 activity. Endocrinology 142: 4086-4094
13. Shin I, Bakin AV, Rodeck U, Brunet A, Arteaga CL 2001 Transforming growth factor β enhances epithelial cell survival via Akt-dependent regulation of FKHRL1. Mol Biol Cell 12:3328-3339
14. Yu L, Hebert MC, Zhang YE 2002 TGF-β receptor-activated p38 MAP kinase mediates Smad-independent TGF-β responses. EMBO J 21:3749-3759
15. Roberts AB, Sporn MB 1988 Transforming growth factor β. Adv Cancer Res 51:107-145
16. Chuang LY, Hung WC, Chang CC, Tsai JH 1994 Characterization of apoptosis induced by transforming growth factor β 1 in human hepatoma cells. Anticancer Res 14:147-152
17. Yanagihara K, Tsumuraya M 1992 Transforming growth factor β 1 induces apoptotic cell death in cultured human gastric carcinoma cells. Cancer Res 52:4042-4045
18. Martikainen P, Kyprianou N, Isaacs JT 1990 Effect of transforming growth factor-β 1 on proliferation and death of rat prostatic cells. Endocrinology 127:2963-2968
19. Rotello RJ, Lieberman RC, Purchio AF, Gerechenson LE 1991 Coordinated regulation of apoptosis and cell proliferation by transforming growth factor β 1 in cultured uterine epithelial cells. Proc Natl Acad Sci USA 88: 3412-3415
20. Kordon EC, McKnight RA, Jhappan C, Hennighausen L, Merlino G, Smith GH 1995 Ectopic TGF β 1 expression in the secretory mammary epithelium induces early senescence of the epithelial stem cell population. Dev Biol 168:47-61
21. Massague J 1998 TGF-β signal transduction. Annu Rev Biochem 68:753-791
22. Nguyen AV, Pollard JW 2000 Transforming growth factor β3 induces cell death during the first stage of mammary gland involution. Development 127:3107-3118
23. Gorska AE, Joseph H, Derynck R, Moses HL, Serra R 1998 Dominant-negative interference of the transforming growth factor β type II receptor in mammary gland epithelium results in alveolar hyperplasia and differentiation in virgin mice. Cell Growth Differ 9:229-238
24. Krumenacker JS, Buckley DJ, Leff MA, McCormack JT, de Jong G, Gout PW, Reed JC, Miyashita T, Magnuson NS, Buckley AR 1998 Prolactin-regulated apoptosis of Nb2 lymphoma cells: pim-1, bcl-2, and bax expression. Endocrine 9:163-170
25. Kirito K, Watanabe T, Sawada K, Endo H, Ozawa K, Komatsu N 2002 Thrombopoietin regulates Bcl-xL gene expression through Stat5 and phosphatidylinositol 3-kinase activation pathways. J Biol Chem 277:8329-8337
26. Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N, Cohen P, Hemmings BA 1996 Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 15: 6541-51
27. Yan S, Krebs S, Leister KJ, Wenner CE 2000 Perturbation of EGF-activated MEK1 and PKB signal pathways by TGF-β1 correlates with perturbation of EGF-induced cyclin D1 and DNA synthesis by TGF-β1 in C3H 10T1/2 cells. J Cell Physiol 185:107-116
28. Chen RH, Chang MC, Su YH, Tsai YT, Kuo ML 1999 Interleukin-6 inhibits transforming growth factor-β-induced apoptosis through the phosphatidylinositol 3-kinase/Akt and signal transducers and activators of transcription 3 pathways. J Biol Chem 274:23013-23019
29. al-Sakkaf KA, Dobson PR, Brown BL 1997 Prolactin induced tyrosine phosphorylation of p59fyn may mediate phosphatidylinositol 3-kinase activation in Nb2 cells. J Mol Endocrinol 19:347-350
30. Berlanga JJ, Gualillo O, Buteau H, Applanat M, Kelly PA, Edery M 1997 Prolactin activates tyrosyl phosphorylation of insulin receptor substrate 1 and phosphatidylinositol-3-OH kinase. J Biol Chem 272:2050-2052
31. Hunter S, Burton EA, Wu SC, Anderson SM 1999 Fyn associates with Cbl and phosphorylates tyrosine 731 in Cbl, a binding site for phosphatidylinositol 3-kinase. J Biol Chem 274:2097-2106
32. Bellacosa A, Chan TO, Ahmed NN, Datta K, Malstrom S, Stokoe D, McCormick F, Feng J, Tsichlis P 1998 Akt activation by growth factors is a multiple-step process: the role of the PH domain. Oncogene 17:313-325
33. Alessi DR, Cohen P 1998 Mechanism of activation and function of protein kinase B. Curr Opin Genet Dev 8:55-62
34. Datta SR, Brunet A, Greenberg ME 1999 Cellular survival: a play in three Akts. Genes Dev 13:2905-2927
35. Alessi DR, James SR, Downes CP, Holmes AB, Gaffney PR, Reese CB, Cohen P 1997 Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Bα. Curr Biol 7:261-269
36. Cross DA, Watt PW, Shaw M, van der Kaay J, Downes CP, Holder JC, Cohen P 1997 Insulin activates protein kinase B, inhibits glycogen synthase kinase-3 and activates glycogen synthase by rapamycin-insensitive pathways in skeletal muscle and adipose tissue. FEBS Lett 406:211-215
37. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME 1997 Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91:231-241
38. del Peso L, Gonzalez-Garcia M, Page C, Herrera R, Nunez G 1997 Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278: 687-689
39. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME 1999 Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868
40. Schwertfeger KL, Richert MM, Anderson SM 2001 Mammary gland involution is delayed by activated Akt in transgenic mice. Mol Endocrinol 15:867-881
41. Fujio Y, Guo K, Mano T, Mitsuuchi Y, Testa JR, Walsh K 1999 Cell cycle withdrawal promotes myogenic induction of Akt, a positive modulator of myocyte survival. Mol Cell Biol 19:5073-6082
42. Krishnan N, Thellin O, Buckley DJ, Horseman ND, Buckley AR 2003 Prolactin suppresses glucocorticoid-induced thymocyte apoptosis in vivo. Endocrinology 144: 2102-2110
43. Valderrama-Carvajal H, Cocolakis E, Lacerte A, Lee EH, Krystal G, Ali S, Lebrun JJ 2002 Activin/TGF-β induce apoptosis through Smad-dependent expression of the lipid phosphatase SHIP. Nat Cell Biol 4:963-969
44. Petritsch C, Beug H, Balmain A, Oft M 2000 TGF-β inhibits p70 S6 kinase via protein phosphatase 2A to induce G(1) arrest. Genes Dev 14:3093-3101
45. Choi I, Lee MJ, Kim EJ, Kang HS, Pyun KH 1998 Roles of protein phosphatase 2A in IL-6 signal transduction in Hep3B cells. Immunol Lett 61:103-107
46. Salh B, Marotta A, Wagey R, Sayed M, Pelech S 2002 Dysregulation of phosphatidylinositol 3-kinase and downstream effectors in human breast cancer. Int J Cancer 98:148-154
47. Mills GB, Lu Y, Fang X, Wang H, Eder A, Mao M, Swaby R, Cheng KW, Stokoe D, Siminovitz K, Jaffe R, Gray J 2001 The role of genetic abnormalities of PTEN and the phosphatidylinositol 3-kinase pathway in breast and ovarian tumorigenesis, prognosis, and therapy. Semin Oncol 5(Suppl 16):125-141
48. Marti A, Jehn B, Costello E, Keon N, Ke G, Martin F, Jaggi R 1994 Protein kinase A and AP-1 (c-Fos/JunD) are induced during apoptosis of mouse mammary epithelial cells. Oncogene 9:1213-1223
49. Wang L, Zhu Y, Sharma K 1998 Transforming growth factor-β1 stimulates protein kinase A in mesangial cells. J Biol Chem 273:8522-8527
50. Silberstein GB, Flanders KC, Roberts AB, Daniel CW 1992 Regulation of mammary morphogenesis: evidence for extracellular matrix-mediated inhibition of ductal budding by transforming growth factor-β 1. Dev Biol 152: 354-362
51. Gorska AE, Jensen RA, Shyr Y, Aakre ME, Bhowmick NA, Moses HL 2003 Transgenic mice expressing a dominant-negative mutant type II transforming growth factor-β receptor exhibit impaired mammary development and enhanced mammary tumor formation. Am J Pathol 163: 1539-1549
52. Horseman ND, Zhao W, Montecino-Rodriguez E, Tanaka M, Nakashima K, Engle SJ, Smith F, Markoff E, Dorshkind K 1997 Defective mammopoiesis, but normal hematopoiesis, in mice with a targeted disruption of the prolactin gene. EMBO J 16:6926-6935
53. Imagawa W, Pedchenko VK, Helber J, Xing C 2000 Attenuation and loss of hormonal modulation of KGF (FGF-7)/KGF receptor expression and mitogenesis during mammary tumor progression. J Cell Physiol 184: 222-228