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PMID: 11593036 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Suppressor of cytokine signaling 3 (SOCS-3) protects beta -cells against interleukin-1beta - and interferon-gamma -mediated toxicity.

Karlsen AE, Rønn SG, Lindberg K, Johannesen J, Galsgaard ED, Pociot F, Nielsen JH, Mandrup-Poulsen T, Nerup J, Billestrup N

Abstract

Suppressor of cytokine signaling 3 (SOCS-3) is a negative feedback regulator of IFN-gamma signaling, shown up-regulated in mouse bone marrow cells by the proinflammatory cytokines interleukin-1beta (IL-1beta), tumor necrosis factor-alpha (TNF-alpha), and IFN-gamma. IL-1beta and IFN-gamma alone, or potentiated by TNF-alpha, are cytotoxic to the insulin producing pancreatic beta-cells and beta-cell lines in vitro and suggested to contribute to the specific beta-cell destruction in Type-1 diabetes mellitus (T1DM). Using a doxycycline-inducible SOCS-3 expression system in the rat beta-cell line INS-1, we demonstrate that the toxic effect of both IL-1beta or IFN-gamma at concentrations that reduced the viability by 50% over 3 days, was fully preventable when SOCS-3 expression was turned on in the cells. At cytokine concentrations or combinations more toxic to the cells, SOCS-3 overexpression yielded a partial protection. Whereas SOCS-3-mediated inhibition of IFN-gamma signaling is described in other cell systems, SOCS-3 mediated inhibition of IL-1beta signaling has not previously been described. In addition we show that SOCS-3 prevention of IL-1beta-induced toxicity is accompanied by inhibited transcription of the inducible nitric oxide synthase (iNOS) by 80%, resulting in 60% decreased formation of the toxic nitric oxide (NO). Analysis of isolated native rat islets exposed to IL-1beta revealed a naturally occurring but delayed up-regulated SOCS-3 transcription. Influencing SOCS-3 expression thus represents an approach for affecting cytokine-induced signal transduction at a proximal step in the signal cascade, potentially useful in future therapies aimed at reducing the destructive potential of beta-cell cytotoxic cytokines in T1DM, as well as other cytokine-dependent diseases.

MeSH Terms
Animals Apoptosis Cell Line Cell Survival Cells, Cultured DNA-Binding Proteins/metabolism Gene Expression Humans Interferon-gamma/pharmacology Interleukin-1/pharmacology Islets of Langerhans/cytology,drug effects Nitric Oxide/biosynthesis Nitric Oxide Synthase/genetics Nitric Oxide Synthase Type II Promoter Regions, Genetic Proteins/genetics,physiology RNA, Messenger Rats Rats, Inbred WF Repressor Proteins STAT1 Transcription Factor Signal Transduction/physiology Suppressor of Cytokine Signaling 3 Protein Suppressor of Cytokine Signaling Proteins Trans-Activators/metabolism Transcription Factors
Chemicals
DNA-Binding Proteins Interleukin-1 Proteins RNA, Messenger Repressor Proteins SOCS3 protein, human STAT1 Transcription Factor STAT1 protein, human Socs3 protein, mouse Socs3 protein, rat Suppressor of Cytokine Signaling 3 Protein Suppressor of Cytokine Signaling Proteins Trans-Activators Transcription Factors Nitric Oxide Interferon-gamma NOS2 protein, human Nitric Oxide Synthase Nitric Oxide Synthase Type II Nos2 protein, rat
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Karlsen A E
Steno Diabetes Center, Niels Steensensvej 2, 2820 Gentofte, Denmark. [email protected]
Rønn S G
Lindberg K
Johannesen J
Galsgaard E D
Pociot F
Nielsen J H
Mandrup-Poulsen T
Nerup J
Billestrup N
References (46)
46 references, click to expand
  1. Effects of sodium butyrate on proliferation-dependent insulin gene expression and insulin release in glucose-sensitive RIN-5AH cells.
    J Biol Chem. 1991 Apr 25;266(12):7542-8 PMID: 1708388
  2. A20 inhibits cytokine-induced apoptosis and nuclear factor kappaB-dependent gene activation in islets.
    J Exp Med. 1999 Oct 18;190(8):1135-46 PMID: 10523611
  3. A critical assessment of the use of microculture tetrazolium assays to measure cell growth and function.
    Growth Regul. 1995 Jun;5(2):69-84 PMID: 7627094
  4. Cytokines and the endocrine system. I. The immunoendocrine network.
    Eur J Endocrinol. 1995 Dec;133(6):660-71 PMID: 8548049
  5. Interleukin-1 beta-induced nitric oxide production from isolated rat islets is modulated by D-glucose and 3-isobutyl-1-methyl xanthine.
    Eur J Endocrinol. 1996 Feb;134(2):251-9 PMID: 8630528
  6. mRNA profiling of rat islet tumors reveals nkx 6.1 as a beta-cell-specific homeodomain transcription factor.
    J Biol Chem. 1996 Aug 2;271(31):18749-58 PMID: 8702531
  7. The harmony of the spheres: inducible nitric oxide synthase and related genes in pancreatic beta cells.
    Diabetologia. 1996 Aug;39(8):875-90 PMID: 8858209
  8. The role of interleukin-1 in the pathogenesis of IDDM.
    Diabetologia. 1996 Sep;39(9):1005-29 PMID: 8877284
  9. Modulation of glucose responsiveness of insulinoma beta-cells by graded overexpression of glucokinase.
    Proc Natl Acad Sci U S A. 1997 Apr 29;94(9):4372-7 PMID: 9113996
  10. Cytokines induce deoxyribonucleic acid strand breaks and apoptosis in human pancreatic islet cells.
    Endocrinology. 1997 Jun;138(6):2610-4 PMID: 9165055
  11. A family of cytokine-inducible inhibitors of signalling.
    Nature. 1997 Jun 26;387(6636):917-21 PMID: 9202125
  12. Interferon-gamma-induced interferon regulatory factor-1 (IRF-1) expression in rodent and human islet cells precedes nitric oxide production.
    Endocrinology. 1997 Jul;138(7):2747-53 PMID: 9202213
  13. Insulin-like growth factor I reverses interleukin-1beta inhibition of insulin secretion, induction of nitric oxide synthase and cytokine-mediated apoptosis in rat islets of Langerhans.
    FEBS Lett. 1997 Nov 10;417(2):235-8 PMID: 9395303
  14. Continuous monitoring of ATP levels in living insulin secreting cells expressing cytosolic firefly luciferase.
    FEBS Lett. 1998 Feb 6;422(3):328-32 PMID: 9498809
  15. Interleukin-1, interleukin-1 receptors and interleukin-1 receptor antagonist.
    Int Rev Immunol. 1998;16(5-6):457-99 PMID: 9646173
  16. An update on cytokines in the pathogenesis of insulin-dependent diabetes mellitus.
    Diabetes Metab Rev. 1998 Jun;14(2):129-51 PMID: 9679667
  17. Characterization of the inhibitory effect of growth hormone on primary preadipocyte differentiation.
    Mol Endocrinol. 1998 Aug;12(8):1140-9 PMID: 9717840
  18. Ciliary neurotrophic factor potentiates the beta-cell inhibitory effect of IL-1beta in rat pancreatic islets associated with increased nitric oxide synthesis and increased expression of inducible nitric oxide synthase.
    Diabetes. 1998 Oct;47(10):1602-8 PMID: 9753298
  19. Mechanism of inhibition of growth hormone receptor signaling by suppressor of cytokine signaling proteins.
    Mol Endocrinol. 1999 Nov;13(11):1832-43 PMID: 10551777
  20. Beta-cell maturation leads to in vitro sensitivity to cytotoxins.
    Diabetes. 1999 Dec;48(12):2324-32 PMID: 10580420
  21. Inhibitors keep cytokines in check.
    Curr Biol. 1999 Dec 2;9(23):R899-902 PMID: 10607559
  22. Interferon-gamma induces interleukin-1 converting enzyme expression in pancreatic islets by an interferon regulatory factor-1-dependent mechanism.
    J Clin Endocrinol Metab. 2000 Feb;85(2):830-6 PMID: 10690898
  23. Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model.
    Science. 2000 Apr 14;288(5464):335-9 PMID: 10764647
  24. SOCS-3 is an insulin-induced negative regulator of insulin signaling.
    J Biol Chem. 2000 May 26;275(21):15985-91 PMID: 10821852
  25. Inhibitory effect of IGF-I on type 2 nitric oxide synthase expression in Ins-1 cells and protection against activation-dependent apoptosis: involvement of phosphatidylinositol 3-kinase.
    Diabetes. 2000 Feb;49(2):209-17 PMID: 10868937
  26. Prolonged exposure of mouse macrophages to IFN-beta suppresses transcription of the inducible nitric oxide synthase gene: altered availability of transcription factor Stat1alpha.
    Eur J Immunol. 2000 Jun;30(6):1551-61 PMID: 10898490
  27. Protection of insulin-producing RINm5F cells against cytokine-mediated toxicity through overexpression of antioxidant enzymes.
    Diabetes. 2000 Jul;49(7):1123-30 PMID: 10909968
  28. SOCS: physiological suppressors of cytokine signaling.
    J Cell Sci. 2000 Aug;113 ( Pt 16):2813-9 PMID: 10910765
  29. Regulation of expression of the rat SOCS-3 gene in hepatocytes by growth hormone, interleukin-6 and glucocorticoids mRNA analysis and promoter characterization.
    Eur J Biochem. 2000 Oct;267(19):5849-57 PMID: 10998044
  30. The effect of burn injury on suppressors of cytokine signalling.
    Shock. 2000 Sep;14(3):392-8; discussion 398-9 PMID: 11028562
  31. Suppressor of cytokine signaling (SOCS)-3 protein interacts with the insulin-like growth factor-I receptor.
    Biochem Biophys Res Commun. 2000 Nov 11;278(1):38-43 PMID: 11071852
  32. Caspase-1 and -3 are sequentially activated in motor neuron death in Cu,Zn superoxide dismutase-mediated familial amyotrophic lateral sclerosis.
    Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13901-6 PMID: 11095709
  33. Janus kinases: components of multiple signaling pathways.
    Oncogene. 2000 Nov 20;19(49):5662-79 PMID: 11114747
  34. Expression of the transcription factor STAT-1 alpha in insulinoma cells protects against cytotoxic effects of multiple cytokines.
    J Biol Chem. 2001 Jan 5;276(1):766-72 PMID: 11024034
  35. Negative cross-talk between interleukin-3 and interleukin-11 is mediated by suppressor of cytokine signalling-3 (SOCS-3).
    Biochem J. 2001 Jan 15;353(Pt 2):223-30 PMID: 11139384
  36. Massive parallel gene expression profiling of RINm5F pancreatic islet beta-cells stimulated with interleukin-1beta.
    APMIS. 2000 Dec;108(12):855-72 PMID: 11252820
  37. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids.
    Anal Biochem. 1982 Oct;126(1):131-8 PMID: 7181105
  38. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays.
    J Immunol Methods. 1983 Dec 16;65(1-2):55-63 PMID: 6606682
  39. Affinity-purified human interleukin I is cytotoxic to isolated islets of Langerhans.
    Diabetologia. 1986 Jan;29(1):63-7 PMID: 3514344
  40. Cytotoxicity of human pI 7 interleukin-1 for pancreatic islets of Langerhans.
    Science. 1986 Jun 20;232(4757):1545-7 PMID: 3086977
  41. Ultrastructural studies of time-course and cellular specificity of interleukin-1 mediated islet cytotoxicity.
    Acta Pathol Microbiol Immunol Scand C. 1987 Apr;95(2):55-63 PMID: 3300162
  42. Regulation by cytokines of the inducible nitric oxide synthase promoter in insulin-producing cells.
    Diabetologia. 1998 Sep;41(9):1101-8 PMID: 9754830
  43. Transfection of human pancreatic islets with an anti-apoptotic gene (bcl-2) protects beta-cells from cytokine-induced destruction.
    Diabetes. 1999 Jun;48(6):1223-9 PMID: 10342808
  44. Interaction of interferon regulatory factor-1 and nuclear factor kappaB during activation of inducible nitric oxide synthase transcription.
    J Mol Biol. 1999 Jun 11;289(3):459-71 PMID: 10356322
  45. Prolonged STAT1 activation is associated with interferon-gamma priming for interleukin-1-induced inducible nitric-oxide synthase expression by islets of Langerhans.
    J Biol Chem. 1999 Oct 8;274(41):29266-73 PMID: 10506184
  46. Effects of sex and pregnancy hormones on growth hormone and prolactin receptor gene expression in insulin-producing cells.
    Endocrinology. 1993 Sep;133(3):1165-72 PMID: 8365359
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2001-10-09
Epub
2001-00-02
Pages
12191-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC59790
Subset
IM
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