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PMID: 10393700 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Exposure of human islets to cytokines can result in disproportionately elevated proinsulin release.

The Journal of clinical investigation ·Vol. 104 ·No. 1 ·1999-07-00 ·Pages 67-72

Hostens K, Pavlovic D, Zambre Y, Ling Z, Van Schravendijk C, Eizirik DL, Pipeleers DG

Abstract

Infiltration of immunocytes into pancreatic islets precedes loss of beta cells in type 1 diabetes. It is conceivable that local release of cytokines affects the function of beta cells before their apoptosis. This study examines whether the elevated proinsulin levels that have been described in prediabetes can result from exposure of beta cells to cytokines. Human beta-cell preparations were cultured for 48 or 72 hours with or without IL-1beta, TNF-alpha, or IFN-gamma, alone or in combination. None of these conditions were cytotoxic, nor did they reduce insulin biosynthetic activity. Single cytokines did not alter medium or cellular content in insulin or proinsulin. Cytokine combinations, in particular IL-1beta plus IFN-gamma, disproportionately elevated medium proinsulin levels. This effect expresses an altered functional state of the beta cells characterized by preserved proinsulin synthesis, a slower hormone conversion, and an increased ratio of cellular proinsulin over insulin content. The delay in proinsulin conversion can be attributed to lower expression of PC1 and PC2 convertases. It is concluded that disproportionately elevated proinsulin levels in pre-type 1 diabetic patients might result from exposure of their beta cells to cytokines released from infiltrating immunocytes. This hormonal alteration expresses an altered functional state of the beta cells that can occur independently of beta-cell death.

MeSH Terms
Adolescent Adult Apoptosis Biomarkers Cells, Cultured Culture Media, Conditioned/chemistry Cytokines/pharmacology,toxicity Diabetes Mellitus, Type 1/immunology,prevention & control Drug Synergism Humans Hyperinsulinism/chemically induced Insulin/metabolism Insulin Secretion Interferon-gamma/pharmacology,toxicity Interleukin-1/pharmacology,toxicity Islets of Langerhans/cytology,drug effects,immunology,metabolism Middle Aged Prediabetic State/diagnosis,physiopathology Pro-Opiomelanocortin/metabolism Proinsulin/biosynthesis,genetics,metabolism Proprotein Convertase 2 Reverse Transcriptase Polymerase Chain Reaction Secretory Rate/drug effects Subtilisins/metabolism Tumor Necrosis Factor-alpha/pharmacology,toxicity
Chemicals
Biomarkers Culture Media, Conditioned Cytokines Insulin Interleukin-1 Tumor Necrosis Factor-alpha Pro-Opiomelanocortin Interferon-gamma Proinsulin Subtilisins Proprotein Convertase 2
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Hostens K
Diabetes Research Center, Vrije Universiteit Brussel, B-1090 Brussels, Belgium.
Pavlovic D
Zambre Y
Ling Z
Van Schravendijk C
Eizirik D L
Pipeleers D G
References (29)
29 references, click to expand
  1. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids.
    Anal Biochem. 1982 Oct;126(1):131-8 PMID: 7181105
  2. Implantation of standardized beta-cell grafts in a liver segment of IDDM patients: graft and recipients characteristics in two cases of insulin-independence under maintenance immunosuppression for prior kidney graft.
    Diabetologia. 1998 Apr;41(4):452-9 PMID: 9562350
  3. Interplay of nutrients and hormones in the regulation of insulin release.
    Endocrinology. 1985 Sep;117(3):824-33 PMID: 2862021
  4. Immunoreactive alpha-interferon in insulin-secreting beta cells in type 1 diabetes mellitus.
    Lancet. 1987 Dec 19;2(8573):1423-7 PMID: 2891993
  5. Increased proinsulin levels as an early indicator of B-cell dysfunction in non-diabetic twins of type 1 (insulin-dependent) diabetic patients.
    Diabetologia. 1988 Mar;31(3):182-4 PMID: 3286344
  6. Elevated proinsulin in healthy siblings of IDDM patients independent of HLA identity.
    Diabetes. 1989 Oct;38(10):1271-4 PMID: 2792577
  7. Inhibition of insulin secretion by interleukin-1 beta and tumour necrosis factor-alpha via an L-arginine-dependent nitric oxide generating mechanism.
    FEBS Lett. 1990 Dec 10;276(1-2):42-4 PMID: 2265709
  8. Cytokine gene expression in the islets of the diabetic Biobreeding/Worcester rat.
    J Immunol. 1991 May 1;146(9):2990-4 PMID: 2016534
  9. Insulitis in type 1 (insulin-dependent) diabetes mellitus in man--macrophages, lymphocytes, and interferon-gamma containing cells.
    J Pathol. 1991 Oct;165(2):97-103 PMID: 1744803
  10. Differences in glucose recognition by individual rat pancreatic B cells are associated with intercellular differences in glucose-induced biosynthetic activity.
    J Clin Invest. 1992 Jan;89(1):117-25 PMID: 1729264
  11. A rapid and sensitive radioimmunoassay for the measurement of proinsulin in human serum.
    Diabetes. 1992 Sep;41(9):1084-90 PMID: 1499862
  12. Elevated proinsulin levels related to islet cell antibodies in first-degree relatives of IDDM patients.
    Diabetes Care. 1992 May;15(5):632-7 PMID: 1516482
  13. What beta-cell defect could lead to hyperproinsulinemia in NIDDM? Some clues from recent advances made in understanding the proinsulin-processing mechanism.
    Diabetes. 1994 Apr;43(4):511-7 PMID: 8138054
  14. Cytokines suppress human islet function irrespective of their effects on nitric oxide generation.
    J Clin Invest. 1994 May;93(5):1968-74 PMID: 7514190
  15. Disproportionately elevated proinsulin levels precede the onset of insulin-dependent diabetes mellitus in siblings with low first phase insulin responses. The Childhood Diabetes in Finland Study Group.
    J Clin Endocrinol Metab. 1994 Dec;79(6):1570-5 PMID: 7989457
  16. Increased secretory demand rather than a defect in the proinsulin conversion mechanism causes hyperproinsulinemia in a glucose-infusion rat model of non-insulin-dependent diabetes mellitus.
    J Clin Invest. 1995 Mar;95(3):1032-9 PMID: 7883951
  17. Interferon expression in the pancreases of patients with type I diabetes.
    Diabetes. 1995 Jun;44(6):658-64 PMID: 7540571
  18. Hyperproinsulinemia in the diabetic Psammomys obesus is a result of increased secretory demand on the beta-cell.
    Endocrinology. 1995 Oct;136(10):4218-23 PMID: 7664638
  19. Hyperproinsulinemia is associated with increased beta cell demand after hemipancreatectomy in humans.
    J Clin Invest. 1996 Jan 15;97(2):455-60 PMID: 8567967
  20. Cytokine gene expression in pancreatic islet-infiltrating leukocytes of BB rats: expression of Th1 cytokines correlates with beta-cell destructive insulitis and IDDM.
    Diabetes. 1996 Jun;45(6):749-54 PMID: 8635648
  21. Elevated serum levels of macrophage-derived cytokines precede and accompany the onset of IDDM.
    Diabetologia. 1996 Jan;39(1):60-9 PMID: 8720604
  22. The role of interleukin-1 in the pathogenesis of IDDM.
    Diabetologia. 1996 Sep;39(9):1005-29 PMID: 8877284
  23. Increased susceptibility of islets from diabetes-prone Psammomys obesus to the deleterious effects of chronic glucose exposure.
    Endocrinology. 1996 Dec;137(12):5610-5 PMID: 8940391
  24. Prolonged exposure of human beta cells to elevated glucose levels results in sustained cellular activation leading to a loss of glucose regulation.
    J Clin Invest. 1996 Dec 15;98(12):2805-12 PMID: 8981928
  25. Possible role of macrophage-derived soluble mediators in the pathogenesis of encephalomyocarditis virus-induced diabetes in mice.
    J Virol. 1997 May;71(5):4024-31 PMID: 9094680
  26. Cytokines induce deoxyribonucleic acid strand breaks and apoptosis in human pancreatic islet cells.
    Endocrinology. 1997 Jun;138(6):2610-4 PMID: 9165055
  27. Intercellular differences in interleukin 1beta-induced suppression of insulin synthesis and stimulation of noninsulin protein synthesis by rat pancreatic beta-cells.
    Endocrinology. 1998 Apr;139(4):1540-5 PMID: 9528932
  28. Effect of glucose on production and release of proinsulin conversion products by cultured human islets.
    J Clin Endocrinol Metab. 1998 Apr;83(4):1234-8 PMID: 9543147
  29. In situ characterization of autoimmune phenomena and expression of HLA molecules in the pancreas in diabetic insulitis.
    N Engl J Med. 1985 Aug 8;313(6):353-60 PMID: 3159965
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
1999-07-00
Pages
67-72
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC408405
Subset
IM
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