SOCS3-mediated blockade reveals major contribution of JAK2/STAT5 signaling pathway to lactation and proliferation of dairy cow mammary epithelial cells in vitro

Molecules

Volumn 18, Issue 10, 2013, Pages 12987-13002

  Huang, Yu Ling ^a   Zhao, Feng ^a   Luo, Chao Chao ^a   Zhang, Xia ^a   Si, Yu ^a   Sun, Zhe ^a   Zhang, Li ^a   Li, Qing Zhang ^a   Gao, Xue Jun ^a  

^a NORTHEAST AGRICULTURAL UNIVERSITY   (China)

Author keywords

Dairy cow mammary epithelial cells; Lactation; Milk fat synthesis; Milk protein synthesis; SOCS3

Indexed keywords

CASEIN; FATTY ACID; JANUS KINASE 2; STAT5 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING; TARGET OF RAPAMYCIN KINASE;

ANIMAL; ARTICLE; BIOSYNTHESIS; CATTLE; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; EPITHELIUM CELL; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; LACTATION; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; UDDER; BOVINAE;

ANIMALS; CASEINS; CATTLE; CELL PROLIFERATION; CELLS, CULTURED; EPITHELIAL CELLS; FATTY ACIDS; FEMALE; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; JANUS KINASE 2; LACTATION; MAMMARY GLANDS, ANIMAL; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TOR SERINE-THREONINE KINASES;

EID: 84886606236     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules181012987     Document Type: Article

References (49)

1. Starr, R.; Willson, T.A.; Viney, E.M.; Murray, L.; Rayner, J.R.; Jenkins, B.J.; Gonda, T.J.; Alexander, W.S.; Metcalf, D.; Nicola, N.A. A family of cytokine-inducible inhibitors of signalling. Nature 1997, 387, 917-921.
2. Naka, T.; Narazaki, M.; Hirata, M.; Matsumoto, T.; Minamoto, S.; Aono, A.; Nishimoto, N.; Kajita, T.; Taga, T.; Yoshizaki, K. STAT-induced STAT inhibitor. Nature 1997, 387, 924-929.
3. Endo, T.A.; Masuhara, M.; Yokouchi, M.; Suzuki, R.; Sakamoto, H.; Mitsui, K.; Matsumoto, A.; Tanimura, S.; Ohtsubo, M.; Misawa, H. A new protein containing an SH2 domain that inhibits JAK kinases. Nature 1997, 387, 921-924.
4. Sachithanandan, N.; Fam, B.C.; Fynch, S.; Dzamko, N.; Watt, M.J.; Wormald, S.; Honeyman, J.; Galic, S.; Proietto, J.; Andrikopoulos, S. Liver-pecific suppressor of cytokine signaling-3 deletion in mice enhances hepatic insulin sensitivity and lipogenesis resulting in fatty liver and obesity1. Hepatology 2010, 52, 1632-1642.
5. Trengove, M.C.; Ward, A.C. SOCS proteins in development and disease. Am. J. Clin. Exp. Immunol. 2013, 2, 1-29.
6. Yoshimura, A.; Naka, T.; Kubo, M. SOCS proteins, cytokine signalling and immune regulation. Nat. Rev. Immunol. 2007, 7, 454-465.
7. Tonko-Geymayer, S.; Goupille, O.; Tonko, M.; Soratroi, C.; Yoshimura, A.; Streuli, C.; Ziemiecki, A.; Kofler, R.; Doppler, W. Regulation and function of the cytokine-inducible SH-2 domain proteins, CIS and SOCS3, in mammary epithelial cells. Mol. Endocrinol. 2002, 16, 1680-1695.
8. Hadsell, D.L.; Parlow, A.F.; Torres, D.; George, J.; Olea, W. Enhancement of maternal lactation performance during prolonged lactation in the mouse by mouse GH and long-R3-IGF-I is linked to changes in mammary signaling and gene expression. J. Endocrinol. 2008, 198, 61-70.
9. Barclay, J.L.; Anderson, S.T.; Waters, M.J.; Curlewis, J.D. SOCS3 as a tumor suppressor in breast cancer cells, and its regulation by PRL. Int. J. Cancer 2009, 124, 1756-1766.
10. Anderson, S.T.; Isa, N.N.; Barclay, J.L.; Waters, M.J.; Curlewis, J.D. Maximal expression of suppressors of cytokine signaling in the rat ovary occurs in late pregnancy. Reproduction 2009, 138, 537-544.
11. Robinson, G.W.; Pacher-Zavisin, M.; Zhu, B.M.; Yoshimura, A.; Hennighausen, L. Socs3 modulates the activity of the transcription factor Stat3 in mammary tissue and controls alveolar homeostasis. Dev. Dyn. 2007, 236, 654-661.
12. Dif, F.; Saunier, E.; Demeneix, B.; Kelly, P.A.; Edery, M. Cytokine-inducible SH2-containing protein suppresses PRL signaling by binding the PRL receptor. Endocrinology 2001, 142, 5286-5293.
13. Paukku, K.; Silvennoinen, O. STATs as critical mediators of signal transduction and transcription: Lessons learned from STAT5. Cytokine Growth Factor Rev. 2004, 15, 435-455.
14. Barash, I. Stat5 in the mammary gland: controlling normal development and cancer. J. Cell. Physiol. 2006, 209, 305-313.
15. Dong, B.; Zhao, F.Q. Involvement of the ubiquitous Oct-1 transcription factor in hormonal induction of beta-casein gene expression. Biochem. J. 2007, 401, 57-64.
16. Khatib, H.; Monson, R.; Schutzkus, V.; Kohl, D.; Rosa, G.; Rutledge, J. Mutations in the STAT5A gene are associated with embryonic survival and milk composition in cattle. J. Dairy Sci. 2008, 91, 784-793.
17. He, F.; Sun, D.X; Yu, Y. SNPs detection of STAT5A gene and association with milk production traits in Holstein cattle. Chin. J. Anim. Vet. Sci. 2007, 38, 326-331.
18. Bionaz, M.; Loor, J.J. Gene networks driving bovine mammary protein synthesis during the lactation cycle. Bioinforma. Biol. Insights 2011, 5, 83-98.
19. Bakan, I.; Laplante, M. Connecting mTORC1 signaling to SREBP-1 activation. Curr. Opin. Lipidol. 2012, 23, 226-234.
20. Yamamoto, T.; Watanabe, K.; Inoue, N.; Nakagawa, Y.; Ishigaki, N.; Matsuzaka, T.; Takeuchi, Y.; Kobayashi, K.; Yatoh, S.; Takahashi, A. Protein kinase Cbeta mediates hepatic induction of sterol-regulatory element binding protein-1c by insulin. J. Lipid Res. 2010, 51, 1859-1870.
21. Ueki, K.; Kadowaki, T.; Kahn, C.R. Role of suppressors of cytokine signaling SOCS-1 and SOCS-3 in hepatic steatosis and the metabolic syndrome. Hepatol. Res. 2005, 33, 185-192.
22. Orellana, R.A.; Jeyapalan, A.; Escobar, J.; Frank, J.W.; Nguyen, H.V.; Suryawan, A.; Davis, T.A. Amino acids augment muscle protein synthesis in neonatal pigs during acute endotoxemia by stimulating mTOR-dependent translation initiation. Am. J. Physiol.-Endocrinol. Metab. 2007, 293, E1416-E1425.
23. Correa-Fiz, F.; Reyes-Palomares, A.; Fajardo, I.; Melgarejo, E.; Gutierrez, A.; GarcIa-Ranea, J.A.; Medina, M.A.; Sanchez-Jimenez, F. Regulatory cross-talk of mouse liver polyamine and methionine metabolic pathways: A systemic approach to its physiopathological consequences. Amino Acids 2011, 42, 577-595.
24. Honda, M.; Takehana, K.; Sakai, A.; Tagata, Y.; Shirasaki, T.; Nishitani, S.; Muramatsu, T.; Yamashita, T.; Nakamoto, Y.; Mizukoshi, E. Malnutrition impairs interferon signaling through mTOR and FoxO pathways in patients with chronic hepatitis C. Gastroenterology 2011, 141, 128-140.
25. Lu, L.M.; Gao, X.J.; Li, Q.Z.; Huang, J.G.; Liu, R.; Li, H.M. Comparative phosphoproteomics analysis of the effects of L-methionine on dairy cow mammary epithelial cells. Can. J. Anim. Sci. 2012, 92, 433-442.
26. Peltola, K.J.; Paukku, K.; Aho, T.L.; Ruuska, M.; Silvennoinen, O.; Koskinen, P.J. Pim-1 kinase inhibits STAT5-dependent transcription via its interactions with SOCS1 and SOCS3. Blood 2004, 103, 3744-3750.
27. Helman, D.; Sandowski, Y.; Cohen, Y.; Matsumoto, A.; Yoshimura, A.; Merchav, S.; Gertler, A. Cytokine-inducible SH2 protein (CIS3) and JAK2 binding protein (JAB) abolish prolactin receptor-mediated STAT5 signaling. FEBS Lett. 1998, 441, 287-291.
28. Tam, S.P.; Lau, P.; Djiane, J.; Hilton, D.J.; Waters, M.J. Tissue-specific induction of SOCS gene expression by PRL. Endocrinology 2001, 142, 5015-5026.
29. White, G.E.; Cotterill, A.; Addley, M.R.; Soilleux, E.J.; Greaves, D.R. Suppressor of cytokine signalling protein SOCS3 expression is increased at sites of acute and chronic inflammation. J. Mol. Histol. 2011, 42, 137-151.
30. Jiang, S.Z.; Ren, Z.R.; Xie, F.; Yan, J.B.; Huang, S.Z.; Zeng, Y.T. Bovine prolactin elevates hTF expression directed by a tissue-specific goat β-casein promoter through prolactin receptor-mediated STAT5a activation. Biotechnol. Lett. 2012, 34, 1991-1999.
31. He, X.; Chu, M.X.; Qiao, L.; He, J.N.; Wang, P.Q.; Feng, T.; Di, R.; Cao, G.L.; Fang, L.; An, Y.F. Polymorphisms of STAT5A gene and their association with milk production traits in Holstein cows. Mol. Biol. Rep. 2012, 39, 2901-2907.
32. Chen, C.-C.; Boxer, R.B.; Stairs, D.B.; Portocarrero, C.P.; Horton, R.H.; Alvarez, J.V.; Birnbaum, M.J.; Chodosh, L.A. Akt is required for Stat5 activation and mammary differentiation. Breast Cancer Res. 2010, 12, R72.
33. Cui, Y.; Riedlinger, G.; Miyoshi, K.; Tang, W.; Li, C.; Deng, C.-X.; Robinson, G.W.; Hennighausen, L. Inactivation of Stat5 in mouse mammary epithelium during pregnancy reveals distinct functions in cell proliferation, survival, and differentiation. Mol. Cell. Biol. 2004, 24, 8037-8047.
34. Lee, K.-H.; Moon, K.-J.; Kim, H.S.; Yoo, B.C.; Park, S.; Lee, H.; Kwon, S.; Lee, E.S.; Yoon, S. Increased cytoplasmic levels of CIS, SOCS1, SOCS2, or SOCS3 are required for nuclear translocation. FEBS Lett. 2008, 582, 2319-2324.
35. Ehrentraut, S.; Nagel, S.; Scherr, M.E.; Schneider, B.; Quentmeier, H.; Geffers, R.; Kaufmann, M.; Meyer, C.; Prochorec-Sobieszek, M.; Ketterling, R.P. t (8; 9)(p22; p24)/PCM1-JAK2 activates SOCS2 and SOCS3 via STAT5. PLoS One 2013, 8, e53767.
36. Le Provost, F.; Miyoshi, K.; Vilotte, J.-L.; Bierie, B.; Robinson, G.W.; Hennighausen, L. SOCS3 promotes apoptosis of mammary differentiated cells. Biochem. Biophys. Res. Commun. 2005, 338, 1696-1701.
37. Chueh, F.-Y.; Leong, K.-F.; Cronk, R.J.; Venkitachalam, S.; Pabich, S.; Yu, C.-L. Nuclear localization of pyruvate dehydrogenase complex-E2 (PDC-E2), a mitochondrial enzyme, and its role in signal transducer and activator of transcription 5 (STAT5)-dependent gene transcription. Cell Signal. 2011, 23, 1170-1178.
38. Toerien, C.A.; Trout, D.R.; Cant, J.P. Nutritional stimulation of milk protein yield of cows is associated with changes in phosphorylation of mammary eukaryotic initiation factor 2 and ribosomal s6 kinase 1. J. Nutr. 2010, 140, 285-292.
39. Galbaugh, T.; Cerrito, M.G.; Jose, C.C.; Cutler, M.L. EGF-induced activation of Akt results in mTOR-dependent p70S6 kinase phosphorylation and inhibition of HC11 cell lactogenic differentiation. BMC Cell Biol. 2006, 7, 34.
40. Stahl, A.; Joyal, J.-S.; Chen, J.; Sapieha, P.; Juan, A.M.; Hatton, C.J.; Pei, D.T.; Hurst, C.G.; Seaward, M.R.; Krah, N.M. SOCS3 is an endogenous inhibitor of pathologic angiogenesis. Blood 2012, 120, 2925-2929.
41. Boutinaud, M.; Guinard-Flament, J.; Jammes, H. The number and activity of mammary epithelial cells, determining factors for milk production. Reprod. Nutr. Dev. 2004, 44, 499-508.
42. He, B.; You, L.; Uematsu, K.; Zang, K.; Xu, Z.; Lee, A.Y.; Costello, J.F.; McCormick, F.; Jablons, D.M. SOCS-3 is frequently silenced by hypermethylation and suppresses cell growth in human lung cancer. Proc. Natl. Acad. Sci. USA 2003, 100, 14133-14138.
43. Elam, M.B.; Yellaturu, C.; Howell, G.E.; Deng, X.; Cowan, G.S.; Kumar, P.; Park, E.A.; Hiler, M.L.; Wilcox, H.G.; Hughes, T.A. Dysregulation of sterol regulatory element binding protein-1c in livers of morbidly obese women is associated with altered suppressor of cytokine signaling-3 and signal transducer and activator of transcription-1 signaling. Metabolism 2010, 59, 587-598.
44. Ueki, K.; Kondo, T.; Tseng, Y.-H.; Kahn, C.R. Central role of suppressors of cytokine signaling proteins in hepatic steatosis, insulin resistance, and the metabolic syndrome in the mouse. Proc. Natl. Acad. Sci. USA 2004, 101, 10422-10427.
45. Ma, L.; Corl, B.A. Transcriptional regulation of lipid synthesis in bovine mammary epithelial cells by sterol regulatory element binding protein-1. J. Dairy Sci. 2012, 95, 3743-3755.
46. Han, J.M.; Jeong, S.J.; Park, M.C.; Kim, G.; Kwon, N.H.; Kim, H.K.; Ha, S.H.; Ryu, S.H.; Kim, S. Leucyl-tRNA synthetase is an intracellular leucine sensor for the mTORC1-signaling pathway. Cell 2012, 149, 410-424.
47. Prizant, R.L.; Barash, I. Negative effects of the amino acids Lys, His, and Thr on S6K1 phosphorylation in mammary epithelial cells. J. Cell. Biochem. 2008, 105, 1038-1047.
48. Lu, L.M.; Li, Q.Z.; Huang, J.G.; Gao, X.J. Proteomic and functional analyses reveal MAPK1 regulates milk protein synthesis. Molecules 2013, 18, 263-275.
49. Huang, J.G.; Gao, X.J.; Li, Q.Z.; Lu, L.M.; Liu, R.; Luo, C.C.; Wang, J.L.; Qiao, B.; Jin, X. Proteomic analysis of the nuclear phosphorylated proteins in dairy cow mammary epithelial cells treated with estrogen. In Vitro Cell. Dev. Biol.-Anim. 2012, 48, 449-457.