Tumor necrosis factor (TNF) interferes with insulin signaling through the p55 TNF receptor death domain

Biochemical and Biophysical Research Communications

Volumn 329, Issue 1, 2005, Pages 397-405

  Csehi, Susan Beatrice ^a   Mathieu, Sabine ^a   Seifert, Ulrike ^a   Lange, Arne ^a   Zweyer, Margit ^b   Wernig, Anton ^b   Adam, Dieter ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

A SMase; Ceramide; Diabetes; Insulin; IRS 1; N SMase; Sphingomyelinase; Tumor necrosis factor

Indexed keywords

CERAMIDE; PROTEIN P55; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA RECEPTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; INFRARED SPECTROSCOPY; INSULIN SYNTHESIS; MOUSE; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; RECEPTOR BINDING; SIGNAL TRANSDUCTION;

EID: 13844299421     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2005.01.140     Document Type: Article

References (66)

1. M.F. White, and M.G. Myers The molecular basis of insulin action L.J. DeGroot J.L. Jameson Endocrinology vol. 1 2001 W.B. Saunders Philadelphia
2. Y. Zick Insulin resistance: a phosphorylation-based uncoupling of insulin signaling Trends Cell Biol. 11 2001 437 441
3. R. DeFronzo Pathogenesis of type 2 diabetes: metabolic and molecular implications for identifying diabetes genes Diabetes Rev. 5 1997 177 269
4. A.R. Saltiel New perspectives into the molecular pathogenesis and treatment of Type 2 diabetes Cell 104 2001 517 529
5. B.B. Kahn Type 2 diabetes: when insulin secretion fails to compensate for insulin resistance Cell 92 1998 593 596
6. G.S. Hotamisligil, N.S. Shargill, and B.M. Spiegelman Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance Science 259 1993 87 91
7. G.S. Hotamisligil, P. Arner, J.F. Caro, R.L. Atkinson, and B.M. Spiegelman Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance J. Clin. Invest. 95 1995 2409 2415
8. K.T. Uysal, S.M. Wiesbrock, M.W. Marino, and G.S. Hotamisligil Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function Nature 389 1997 610 614
9. K.T. Uysal, S.M. Wiesbrock, and G.S. Hotamisligil Functional analysis of tumor necrosis factor (TNF) receptors in TNF-alpha-mediated insulin resistance in genetic obesity Endocrinology 139 1998 4832 4838
10. C. Qi, and P.H. Pekala Tumor necrosis factor-alpha-induced insulin resistance in adipocytes Proc. Soc. Exp. Biol. Med. 223 2000 128 135
11. H. Kanety, R. Feinstein, M.Z. Papa, R. Hemi, and A. Karasik 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 1995 23780 23784
12. K. Paz, R. Hemi, D. LeRoith, A. Karasik, E. Elhanany, H. Kanety, and Y. Zick Elevated serine/threonine phosphorylation of IRS-1 and IRS-2 inhibits their binding to the juxtamembrane region of the insulin receptor and impairs their ability to undergo insulin-induced tyrosine phosphorylation J. Biol. Chem. 272 1997 29911 29918
13. G.S. Hotamisligil, P. Peraldi, A. Budavari, R. Ellis, M.F. White, and B.M. Spiegelman IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance Science 271 1996 665 668
14. R. Zhande, J.J. Mitchell, J. Wu, and X.J. Sun Molecular mechanism of insulin-induced degradation of insulin receptor substrate 1 Mol. Cell. Biol. 22 2002 1016 1026
15. E.D. Werner, J. Lee, L. Hansen, M. Yuan, and S.E. Shoelson Insulin resistance due to phosphorylation of insulin receptor substrate-1 at serine 302 J. Biol. Chem. 279 2004 35298 35305
16. L.Y. Rui, V. Aguirre, J.K. Kim, G.I. Shulman, A. Lee, A. Corbould, A. Dunaif, and M.F. White Insulin/IGF-1 and TNF-alpha stimulate phosphorylation of IRS-1 at inhibitory Ser(307) via distinct pathways J. Clin. Invest. 107 2001 181 189
17. M. Verheij, R. Bose, X.H. Lin, B. Yao, W.D. Jarvis, S. Grant, M.J. Birrer, E. Szabo, L.I. Zon, J.M. Kyriakis, A. Haimovitz-Friedman, Z. Fuks, and R.N. Kolesnick Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis Nature 380 1996 75 79
18. Y.-F. Liu, K. Paz, A. Herschkovitz, A. Alt, T. Tennenbaum, S.R. Sampson, M. Ohba, T. Kuroki, D. LeRoith, and Y. Zick Insulin stimulates PKCzeta-mediated phosphorylation of insulin receptor substrate-1 (IRS-1). A self-attenuated mechanism to negatively regulate the function of IRS proteins J. Biol. Chem. 276 2001 14459 14465
19. L.V. Ravichandran, D.L. Esposito, J. Chen, and M.J. Quon Protein kinase c-zeta phosphorylates insulin receptor substrate-1 and impairs its ability to activate phosphatidylinositol 3-kinase in response to insulin J. Biol. Chem. 276 2001 3543 3549
20. J.A. Engelman, A.H. Berg, R.Y. Lewis, M.P. Lisanti, and P.E. Scherer Tumor necrosis factor alpha-mediated insulin resistance, but not dedifferentiation, is abrogated by MEK1/2 inhibitors in 3T3-L1 adipocytes Mol. Endocrinol. 14 2000 1557 1569
21. M. Fujishiro, Y. Gotoh, H. Katagiri, H. Sakoda, T. Ogihara, M. Anai, Y. Onishi, H. Ono, W. Abe, N. Shojima, Y. Fukushima, M. Kikuchi, Y. Oka, and T. Asano Three mitogen-activated protein kinases inhibit insulin signaling by different mechanisms in 3T3-L1 adipocytes Mol. Endocrinol. 17 2003 487 497
22. Z. Gao, D. Hwang, F. Bataille, M. Lefevre, D. York, M.J. Quon, and J. Ye Serine phosphorylation of insulin receptor substrate 1 by inhibitor kappa B kinase complex J. Biol. Chem. 277 2002 48115 48121
23. M. Yuan, N. Konstantopoulos, J. Lee, L. Hansen, Z.W. Li, M. Karin, and S.E. Shoelson Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkbeta Science 293 2001 1673 1677
24. K. Paz, Y.F. Liu, H. Shorer, R. Hemi, D. LeRoith, M. Quan, H. Kanety, R. Seger, and Y. Zick Phosphorylation of insulin receptor substrate-1 (IRS-1) by protein kinase B positively regulates IRS-1 function J. Biol. Chem. 274 1999 28816 28822
25. A. Sekulic, C.C. Hudson, J.L. Homme, P. Yin, D.M. Otterness, L.M. Karnitz, and R.T. Abraham A direct linkage between the phosphoinositide 3-kinase-AKT signaling pathway and the mammalian target of rapamycin in mitogen-stimulated and transformed cells Cancer Res. 60 2000 3504 3513
26. H. Eldar-Finkelman, and E.G. Krebs Phosphorylation of insulin receptor substrate 1 by glycogen synthase kinase 3 impairs insulin action Proc. Natl. Acad. Sci. USA 94 1997 9660 9664
27. P. Peraldi, G.S. Hotamisligil, W.A. Buurman, M.F. White, and B.M. Spiegelman Tumor necrosis factor (TNF)-alpha inhibits insulin signaling through stimulation of the p55 TNF receptor and activation of sphingomyelinase J. Biol. Chem. 271 1996 13018 13022
28. E. Hajduch, A. Balendran, I.H. Batty, G.J. Litherland, A.S. Blair, C.P. Downes, and H.S. Hundal Ceramide impairs the insulin-dependent membrane recruitment of protein kinase B leading to a loss in downstream signalling in L6 skeletal muscle cells Diabetologia 44 2001 173 183
29. C. Schmitz-Peiffer, D.L. Craig, and T.J. Biden Ceramide generation is sufficient to account for the inhibition of the insulin-stimulated PKB pathway in C2C12 skeletal muscle cells pretreated with palmitate J. Biol. Chem. 274 1999 24202 24210
30. P. Storz, H. Döppler, A. Wernig, K. Pfizenmaier, and G. Müller Cross-talk mechanisms in the development of insulin resistance of skeletal muscle cells-Palmitate rather than tumour necrosis factor inhibits insulin-dependent protein kinase B (PKB)/Akt stimulation and glucose uptake Eur. J. Biochem. 266 1999 17 25
31. R.J. Grigsby, and R.T. Dobrowsky Inhibition of ceramide production reverses TNF-induced insulin resistance Biochem. Biophys. Res. Commun. 287 2001 1121 1124
32. S.C. Souza, M.T. Yamamoto, M.D. Franciosa, P. Lien, and A.S. Greenberg BRL 49653 blocks the lipolytic actions of tumor necrosis factor-alpha: a potential new insulin-sensitizing mechanism for thiazolidinediones Diabetes 47 1998 691 695
33. J.K. Westwick, A.E. Bielawska, G. Dbaibo, Y.A. Hannun, and D.A. Brenner Ceramide activates the stress-activated protein kinases J. Biol. Chem. 270 1995 22689 22692
34. G. Müller, M. Ayoub, P. Storz, J. Rennecke, D. Fabbro, and K. Pfizenmaier PKC zeta is a molecular switch in signal transduction of TNF-alpha, bifunctionally regulated by ceramide and arachidonic acid EMBO J. 14 1995 1961 1969
35. M. Krönke, S. Schütze, K. Wiegmann, and T. Machleidt Sphingomyelinases and TNF-induced apoptosis Cell Physiol. Biochem. 6 1996 337 344
36. T. Machleidt, B. Krämer, D. Adam, B. Neumann, S. Schütze, K. Wiegmann, and M. Krönke Function of the p55 tumor necrosis factor receptor death domain mediated by phosphatidylcholine-specific phospholipase C J. Exp. Med. 184 1996 725 733
37. R.N. Kolesnick, and M. Krönke Regulation of ceramide production and apoptosis Annu. Rev. Physiol. 60 1998 643 665
38. K. Wiegmann, S. Schütze, T. Machleidt, D. Witte, and M. Krönke Functional dichotomy of neutral and acidic sphingomyelinases in tumor necrosis factor signaling Cell 78 1994 1005 1015
39. L.A. Tartaglia, T.M. Ayres, G.H.W. Wong, and D.V. Goeddel A novel domain within the 55 kDa TNF receptor signals cell death Cell 74 1993 845 853
40. D. Wallach, E.E. Varfolomeev, N.L. Malinin, Y.V. Goltsev, A.V. Kovalenko, and M.P. Boldin Tumor necrosis factor receptor and Fas signaling mechanisms Annu. Rev. Immunol. 17 1999 331 367
41. E. Boone, V. Vandevoorde, G. DeWilde, and G. Haegeman Activation of p42/p44 mitogen-activated protein kinases (MAPK) and p38 MAPK by tumor necrosis factor (TNF) is mediated through the death domain of the 55-kDa TNF receptor FEBS Lett. 441 1998 275 280
42. S. Lüschen, D. Adam, S. Ussat, D. Kreder, W. Schneider-Brachert, M. Krönke, and S. Adam-Klages Activation of ERK1/2 and cPLA(2) by the p55 TNF receptor occurs independently of FAN Biochem. Biophys. Res. Commun. 274 2000 506 512
43. D. Adam, K. Wiegmann, S. Adam-Klages, A. Ruff, and M. Krönke A novel cytoplasmic domain of the p55 tumor necrosis factor receptor initiates the neutral sphingomyelinase pathway J. Biol. Chem. 271 1996 14617 14622
44. S. Adam-Klages, D. Adam, K. Wiegmann, S. Struve, W. Kolanus, J. Schneider-Mergener, and M. Krönke FAN, a novel WD-repeat protein, couples the p55 TNF-receptor to neutral sphingomyelinase Cell 86 1996 937 947
45. T. Plitz, U. Huffstadt, R. Endres, E. Schaller, T.W. Mak, H. Wagner, and K. Pfeffer The resistance against Listeria monocytogenes and the formation of germinal centers depend on a functional death domain of the 55 kDa tumor necrosis factor receptor Eur. J. Immunol. 29 1999 581 591
46. M. Schuermann An expression vector system for stable expression of oncogenes Nucleic Acids Res. 18 1990 4945 4946
47. A. Irintchev, M. Langer, M. Zweyer, R. Theisen, and A. Wernig Functional improvement of damaged adult mouse muscle by implantation of primary myoblasts J. Physiol. 500 1997 775 785
48. A. Wernig, M. Zweyer, and A. Irintchev Function of skeletal muscle tissue formed after myoblast transplantation into irradiated mouse muscles J. Physiol. 522 2000 333 345
49. R. Schwandner, K. Wiegmann, K. Bernardo, D. Kreder, and M. Krönke TNF receptor death domain-associated proteins TRADD and FADD signal activation of acid sphingomyelinase J. Biol. Chem. 273 1998 5916 5922
50. H. Kanety, P. Hemi, M.Z. Papa, and A. Karasik Sphingomyelinase and ceramide suppress insulin-induced tyrosine phosphorylation of the insulin receptor substrate-1 J. Biol. Chem. 271 1996 9895 9897
51. D. Kreder, O. Krut, S. Adam-Klages, K. Wiegmann, G. Scherer, T. Plitz, J.M. Jensen, E. Proksch, J. Steinmann, K. Pfeffer, and M. Krönke Impaired neutral sphingomyelinase activation and cutaneous barrier repair in FAN-deficient mice EMBO J. 18 1999 2472 2479
52. K. Wiegmann, R. Schwandner, O. Krut, W.C. Yeh, T.W. Mak, and M. Krönke Requirement of FADD for tumor necrosis factor-induced activation of acid sphingomyelinase J. Biol. Chem. 274 1999 5267 5270
53. K. Wiegmann, S. Schütze, E. Kampen, A. Himmler, T. Machleidt, and M. Krönke Human 55-kDa receptor for tumor necrosis factor coupled to signal transduction cascades J. Biol. Chem. 267 1992 17997 18001
54. B. Bossenmaier, L. Mosthaf, H. Mischak, A. Ullrich, and H.U. Häring Protein kinase C isoforms beta 1 and beta 2 inhibit the tyrosine kinase activity of the insulin receptor Diabetologia 40 1997 863 866
55. K. De Fea, and R.A. Roth Protein kinase C modulation of insulin receptor substrate-1 tyrosine phosphorylation requires serine 612 Biochemistry 36 1997 12939 12947
56. M. Kellerer, J. Mushack, E. Seffer, H. Mischak, A. Ullrich, and H.U. Häring Protein kinase C isoforms alpha, delta and theta require insulin receptor substrate-1 to inhibit the tyrosine kinase activity of the insulin receptor in human kidney embryonic cells (HEK 293 cells) Diabetologia 41 1998 833 838
57. G.Q. Jiang, Q. Dallas-Yang, F. Liu, D.E. Moller, and B.B. Zhang Salicylic acid reverses phorbol 12-myristate-13-acetate (PMA)- and tumor necrosis factor alpha (TNF alpha)-induced insulin receptor substrate 1 (IRS1) serine 307 phosphorylation and insulin resistance in human embryonic kidney 293 (HEK293) cells J. Biol. Chem. 278 2003 180 186
58. M. Kellerer, J. Mushack, H. Mischak, and H.U. Häring Protein kinase C (PKC) epsilon enhances the inhibitory effect of TNF alpha on insulin signaling in HEK293 cells FEBS Lett. 418 1997 119 122
59. A.R. Saltiel, and C.R. Kahn Insulin signalling and the regulation of glucose and lipid metabolism Nature 414 2001 799 806
60. P. Storz, H. Döppler, A. Wernig, K. Pfizenmaier, and G. Müller TNF inhibits insulin induced STAT5 activation in differentiated mouse muscle cells pmi28 FEBS Lett. 440 1998 41 45
61. H. Shi, I. Tzameli, C. Bjørbaek, and J.S. Flier Suppressor of cytokine signaling 3 is a physiological regulator of adipocyte insulin signaling J. Biol. Chem. 279 2004 34733 34740
62. J. Hirosumi, G. Tuncman, L.F. Chang, C.Z. Görgün, K.T. Uysal, K. Maeda, M. Karin, and G.S. Hotamisligil A central role for JNK in obesity and insulin resistance Nature 420 2002 333 336
63. H. Kaneto, Y. Nakatani, T. Miyatsuka, D. Kawamori, T.A. Matsuoka, M. Matsuhisa, Y. Kajimoto, H. Ichijo, Y. Yamasaki, and M. Hori Possible novel therapy for diabetes with cell-permeable JNK-inhibitory peptide Nat. Med. 10 2004 1128 1132
64. C. de Alvaro, T. Teruel, R. Hernandez, and M. Lorenzo Tumor necrosis factor alpha produces insulin resistance in skeletal muscle by activation of inhibitor kappaB kinase in a p38 MAPK-dependent manner J. Biol. Chem. 279 2004 17070 17078
65. C.D. Carlson, and R.P. Hart Activation of acidic sphingomyelinase and protein kinase C zeta is required for IL-1 induction of LIF mRNA in a Schwann cell line Glia 18 1996 49 58
66. S. Stratford, K.L. Hoehn, F. Liu, and S.A. Summers Regulation of insulin action by ceramide: dual mechanisms linking ceramide accumulation to the inhibition of Akt/protein kinase B J. Biol. Chem. 279 2004 36608 36615