Degradation of STAT5 proteins in 3T3-L1 adipocytes is induced by TNF-α and cycloheximide in a manner independent of STAT5A activation

American Journal of Physiology - Endocrinology and Metabolism

Volumn 292, Issue 2, 2007, Pages

  Floyd, Z Elizabeth ^a,b   Segura, Brant M ^a,c   He, Fang ^a   Stephens, Jacqueline M ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Nuclear factor B; Proteasome; Signal transducer and activator of transcription 5; Tumor necrosis factor

Indexed keywords

CYCLOHEXIMIDE; PROTEASOME; STAT5 PROTEIN; STAT5A PROTEIN; STAT5B PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; 3T3-L1 CELLS; ADIPOCYTES; ANIMALS; CYCLOHEXIMIDE; GROWTH HORMONE; MAP KINASE SIGNALING SYSTEM; MICE; NF-KAPPA B; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN DENATURATION; STAT5 TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33846851777     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00334.2006     Document Type: Article

References (49)

1. Arron JR, Vologodskaia M, Wong BR, Naramura M, Kim N, Gu H, Choi Y. A positive regulatory role for Cbl family proteins in tumor necrosis factor-related activation-induced cytokine (trance) and CD40L-mediated Akt activation. J Biol Chem 276: 30011-30017, 2001.
2. Bouwmeester T, Bauch A, Ruffner H, Angrand PO, Bergamini G, Croughton K, Cruciat C, Eberhard D, Gagneur J, Ghidelli S, Hopf C, Huhse B, Mangano R, Michon AM, Schirle M, Schlegl J, Schwab M, Stein MA, Bauer A, Casari G, Drewes G, Gavin AC, Jackson DB, Joberty G, Neubauer G, Rick J, Kuster B, and Superti-Furga G. A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat Cell Biol 6: 97-105, 2004.
3. Carlson CJ, Koterski S, Sciotti RJ, Poccard GB, Rondinone CM. Enhanced basal activation of mitogen-activated protein kinases in adipocytes from type 2 diabetes: potential role of p38 in the downregulation of GLUT4 expression. Diabetes 52: 634-641, 2003.
4. Chia DJ, Ono M, Woelfle J, Schlesinger-Massart M, Jiang H, Rotwein P. Characterization of distinct Stat5b binding sites that mediate growth hormone-stimulated IGF-I gene transcription. J Biol Chem 281: 3190-3197, 2006.
5. Engelman JA, Berg AH, Lewis RY, Lisanti MP, Scherer PE. Tumor necrosis factor alpha-mediated insulin resistance, but not dedifferentiation, is abrogated by MEK1/2 inhibitors in 3T3-L1 adipocytes. Mol Endocrinol 14: 1557-1569, 2000.
6. Fasshauer M, Klein J, Neumann S, Eszlinger M, Paschke R. Tumor necrosis factor alpha is a negative regulator of resistin gene expression and secretion in 3T3-L1 adipocytes. Biochem Biophys Res Commun 288: 1027-1031, 2001.
7. Fasshauer M, Kralisch S, Klier M, Lossner U, Bluher M, Klein J, Paschke R. Insulin resistance-inducing cytokines differentially regulate SOCS mRNA expression via growth factor- and Jak/Stat-signaling pathways in 3T3-L1 adipocytes. J Endocrinol 181: 129-138, 2004.
8. Feinstein R, Kanety H, Papa MZ, Lunenfeld B, Karasik A. Tumor necrosis factor-alpha suppresses insulin-induced tyrosine phosphorylation of insulin receptor and its substrates. J Biol Chem 268: 26055-26058, 1993.
9. Fischer-Posovszky P, Tornqvist H, Debatin KM, Wabitsch M. Inhibition of death-receptor mediated apoptosis in human adipocytes by the insulin-like growth factor I (IGF-I)/IGF-I receptor autocrine circuit. Endocrinology 145: 1849-1859, 2004.
10. Floyd ZE, Stephens JM. STAT5A promotes adipogenesis in nonprecursor cells and associates with the glucocorticoid receptor during adipocyte differentiation. Diabetes 52: 308-314, 2003.
11. Fujishiro M, Gotoh Y, Katagiri H, Sakoda H, Ogihara T, Anai M, Onishi Y, Ono H, Abe M, Shojima N, Fukushima Y, Kikuchi M, Oka Y, Asano T. Three mitogen-activated protein kinases inhibit insulin signaling by different mechanisms in 3T3-L1 adipocytes. Mol Endocrinol 17: 487-497, 2003.
12. Goh EL, Zhu T, Leong WY, Lobie PE. c-Cbl is a negative regulator of GH-stimulated STAT5-mediated transcription. Endocrinology 143: 3590-3603, 2002.
13. Guo D, Donner DB. Tumor necrosis factor promotes phosphorylation and binding of insulin receptor substrate 1 to phosphatidylinositol 3-kinase in 3T3-L1 adipocytes. J Biol Chem 271: 615-618, 1996.
14. Guo D, Dunbar JD, Yang CH, Pfeffer LM, Donner DB. Induction of Jak/STAT signaling by activation of the type 1 TNF receptor. J Immunol 160: 2742-2750, 1998.
15. He F, Stephens JM. Induction of SOCS-3 is insufficient to confer IRS-1 protein degradation in 3T3-L1 adipocytes. Biochem Biophys Res Commun 344: 95-98, 2006.
16. Henkel T, Machleidt T, Alkalay I, Kronke M, Ben-Neriah Y, Baeuerle PA. Rapid proteolysis of I kappa B-alpha is necessary for activation of transcription factor NF-kappa B. Nature 365: 182-185, 1993.
17. Hernandez R, Teruel T, De Alvaro C, Lorenzo M. Rosiglitazone ameliorates insulin resistance in brown adipocytes of Wistar rats by impairing TNF-alpha induction of p38 and p42/p44 mitogen-activated protein kinases. Diabetologia 47: 1615-1624, 2004.
18. Hotamisligil GS. Molecular mechanisms of insulin resistance and the role of the adipocyte. Int J Obes Relat Metab Disord 24, Suppl 4: S23-S27, 2000.
19. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 271: 665-668, 1996.
20. Kanety H, Feinstein R, Papa MZ, Hemi R, Karasik A. Tumor necrosis factor alpha-induced phosphorylation of insulin receptor substrate-1 (IRS-1). Possible mechanism for suppression of insulin-stimulated tyrosine phosphorylation of IRS-1. J Biol Chem 270: 23780-23784, 1995.
21. Lee DH, Goldberg AL. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol 8: 397-403, 1998.
22. Levy DE, Darnell JE Jr. Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 3: 651-662, 2002.
23. Liu J, DeYoung SM, Hwang JB, O'Leary EE, Saltiel AR. The roles of Cbl-b and c-Cbl in insulin-stimulated glucose transport. J Biol Chem 278: 36754-36762, 2003.
24. Liu X, Robinson GW, Gouilleux F, Groner B, Hennighausen L. Cloning and expression of Stat5 and an additional homologue (Stat5b) involved in prolactin signal transduction in mouse mammary tissue. Proc Natl Acad Sci USA 92: 8831-8835, 1995.
25. Medina EA, Afsari RR, Ravid T, Castillo SS, Erickson KL, Goldkorn T. Tumor necrosis factor- decreases Akt protein levels in 3T3-L1 adipocytes via the caspase-dependent ubiquitination of Akt. Endocrinology 146: 2726-2735, 2005.
26. Meng F, D'Mello SR. NF-kappaB stimulates Akt phosphorylation and gene expression by distinct signaling mechanisms. Biochim Biophys Acta 1630: 35-40, 2003.
27. Meng F, Liu L, Chin PC, D'Mello SR. Akt is a downstream target of NF-kappa B. J Biol Chem 277: 29674-29680, 2002.
28. Miura M, Friedlander RM, Yuan J. Tumor necrosis factor-induced apoptosis is mediated by a CrmA-sensitive cell death pathway. Proc Natl Acad Sci USA 92: 8318-8322, 1995.
29. Molero JC, Jensen TE, Withers PC, Couzens M, Herzog H, Thien CB, Langdon WY, Walder K, Murphy MA, Bowtell DD, James DE, Cooney GJ. c-Cbl-deficient mice have reduced adiposity, higher energy expenditure, and improved peripheral insulin action. J Clin Invest 114: 1326-1333, 2004.
30. Nanbu-Wakao R, Morikawa Y, Matsumura I, Masuho Y, Muramatsu MA, Senba E, Wakao H. Stimulation of 3T3-L1 adipogenesis by signal transducer and activator of transcription 5. Mol Endocrinol 16: 1565-1576, 2002.
31. Raingeaud J, Gupta S, Rogers JS, Dickens M, Han J, Ulevitch RJ, Davis RJ. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J Biol Chem 270: 7420-7426, 1995.
32. Reid TR, Torti FM, Ringold GM. Evidence for two mechanisms by which tumor necrosis factor kills cells. J Biol Chem 264: 4583-4589, 1989.
33. Richter HE, Albrektsen T, Billestrup N. The role of signal transducer and activator of transcription 5 in the inhibitory effects of GH on adipocyte differentiation. J Mol Endocrinol 30: 139-150, 2003.
34. Rizk NM, Stammsen D, Preibisch G, Eckel J. Leptin and tumor necrosis factor-alpha induce the tyrosine phosphorylation of signal transducer and activator of transcription proteins in the hypothalamus of normal rats in vivo. Endocrinology 142: 3027-3032, 2001.
35. Ruan H, Hacohen N, Golub TR, Van Parijs L, Lodish HF. Tumor necrosis factor-alpha suppresses adipocyte-specific genes and activates expression of preadipocyte genes in 3T3-L1 adipocytes: nuclear factor-kappaB activation by TNF-alpha is obligatory. Diabetes 51: 1319-1336, 2002.
36. Ruan H, Lodish HF. Insulin resistance in adipose tissue: direct and indirect effects of tumor necrosis factor-alpha. Cytokine Growth Factor Rev 14: 447-455, 2003.
37. Ryden M, Dicker A, van Harmelen V, Hauner H, Brunnberg M, Perbeck L, Lonnqvist F, Arner P. Mapping of early signaling events in tumor necrosis factor-alpha-mediated lipolysis in human fat cells. J Biol Chem 277: 1085-1091, 2002.
38. Shang CA, Waters MJ. Constitutively active signal transducer and activator of transcription 5 can replace the requirement for growth hormone in adipogenesis of 3T3-F442A preadipocytes. Mol Endocrinol 17: 2494-2508, 2003.
39. Stephens JM, Lee J, Pilch PF. Tumor necrosis factor-alpha-induced insulin resistance in 3T3-L1 adipocytes is accompanied by a loss of insulin receptor substrate-1 and GLUT4 expression without a loss of insulin receptor-mediated signal transduction. J Biol Chem 272: 971-976, 1997.
40. Stewart WC, Baugh JE Jr, Floyd ZE, and Stephens JM. STAT 5 activators can replace the requirement of FBS in the adipogenesis of 3T3-L1 cells. Biochem Biophys Res Commun 324: 355-359, 2004.
41. Summers SA, Whiteman EL, Birnbaum MJ. Insulin signaling in the adipocyte. Int J Obes Relat Metab Disord 24, Suppl 4: S67-S70, 2000.
42. Valladares A, Alvarez AM, Ventura JJ, Roncero C, Benito M, Porras A. p38 mitogen-activated protein kinase mediates tumor necrosis factor-alpha-induced apoptosis in rat fetal brown adipocytes. Endocrinology 141: 4383-4395, 2000.
43. Valladares A, Roncero C, Benito M, Porras A. TNF-alpha inhibits UCP-1 expression in brown adipocytes via ERKs. Opposite effect of p38 MAPK. FEBS Lett 493: 6-11, 2001.
44. Wang D, Moriggl R, Stravopodis D, Carpino N, Marine JC, Teglund S, Feng J, Ihle JN. A small amphipathic alpha-helical region is required for transcriptional activities and proteasome-dependent turnover of the tyrosine-phosphorylated Stat5. EMBO J 19: 392-399, 2000.
45. Wang Y, Jiang H. Identification of a distal STAT5-binding DNA region that may mediate growth hormone regulation of insulin-like growth factor-I gene expression. J Biol Chem 280: 10955-10963, 2005.
46. Warne JP. Tumour necrosis factor alpha: a key regulator of adipose tissue mass. J Endocrinol 177: 351-355, 2003.
47. Winston BW, Remigio LK, Riches DW. Preferential involvement of MEK1 in the tumor necrosis factor-alpha-induced activation of p42mapk/erk2 in mouse macrophages. J Biol Chem 270: 27391-27394, 1995.
48. Wormald S, Hilton DJ. Inhibitors of cytokine signal transduction. J Biol Chem 279: 821-824, 2004.
49. Xu J, Yeh CH, Chen S, He L, Sensi SL, Canzoniero LM, Choi DW, Hsu CY. Involvement of de novo ceramide biosynthesis in tumor necrosis factor-alpha/cycloheximide-induced cerebral endothelial cell death. J Biol Chem 273: 16521-16526, 1998.