Physiologic versus diabetogenic effects of interleukin-1: A question of weight

Current Pharmaceutical Design

Volumn 20, Issue 29, 2014, Pages 4733-4740

  Besedovsky, Hugo O ^a   Del Rey, Adriana ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Diabetes; Glucose homeostasis; Il 1; Il 1 receptor antagonist; Inflammasome; Physiologic functions

Indexed keywords

CELL ADHESION MOLECULE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 17; INTERLEUKIN 18; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 33; INTERLEUKIN 8; NITRIC OXIDE; PROSTAGLANDIN SYNTHASE; TUMOR NECROSIS FACTOR ALPHA; GLUCOSE;

ADAPTIVE IMMUNITY; ANTIDIABETIC ACTIVITY; ARTICLE; CELL EXPANSION; CYTOKINE PRODUCTION; DIABETOGENESIS; ENERGY METABOLISM; GENE EXPRESSION; GLUCOSE HOMEOSTASIS; GLUCOSE TRANSPORT; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PLEIOTROPY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; ANIMAL; HOMEOSTASIS; IMMUNOLOGY; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; DIABETES MELLITUS, TYPE 2; GLUCOSE; HOMEOSTASIS; HUMANS; INTERLEUKIN-1;

EID: 84906279681     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612820666140130204401     Document Type: Article

References (82)

1. Dinarello CA. Historical insights into cytokines. Eur J Immunol 2007; 37 Suppl 1: S34-S45.
2. Besedovsky HO, Del Rey A, Sorkin E, et al. Lymphoid cells produce an immunoregulatory glucocorticoid increasing factor (GIF) acting through the pituitary gland. Clin Exp Immunol 1985; 59: 622-628.
3. Besedovsky H, Del Rey A. Neuroendocrine and metabolic responses induced by interleukin-1. J Neurosci Res 1987; 18: 172-178.
4. Banchereau J, Pascual V, O'Garra A. From IL-2 to IL-37: the expanding spectrum of anti-inflammatory cytokines. Nat Immunol 2012; 13: 925-931.
5. Sims JE, Smith DE. The IL-1 family: regulators of immunity. Nat Rev Immunol 2010; 10: 89-102.
6. Matsushima K, Yodoi J, Tagaya Y, et al. Down-regulation of interleukin 1 (IL 1) receptor expression by IL 1 and fate of internalized 125I-labeled IL 1 beta in a human large granular lymphocyte cell line. J Immunol 1986; 137: 3183-3188.
7. Ye K, Koch KC, Clark BD, et al. Interleukin-1 down-regulates gene and surface expression of interleukin-1 receptor type I by destabilizing its mRNA whereas interleukin-2 increases its expression. Immunology 1992; 75: 427-434.
8. Vega C, Pellerin L, Dantzer R, et al. Long-term modulation of glucose utilization by IL-1 alpha and TNF-alpha in astrocytes: Na+ pump activity as a potential target via distinct signaling mechanisms. Glia 2002; 39: 10-18.
9. Yu N, Maciejewski-Lenoir D, Bloom FE, et al. Tumor necrosis factor-alpha and interleukin-1 alpha enhance glucose utilization by astrocytes: involvement of phospholipase A2. Mol Pharmacol 1995; 48: 550-558.
10. Del Rey A, Besedovsky H. Interleukin 1 affects glucose homeostasis. Am J Physiol 1987; 253: R794-R798.
11. Besedovsky H, Del Rey A, Sorkin E, et al. Immunoregulatory feedback between interleukin-1 and glucocorticoid hormones. Science 1986; 233: 652-654.
12. Dinarello CA. Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood 2011; 117: 3720-3732.
13. Dinarello CA, Ikejima T, Warner SJ, et al. Interleukin 1 induces interleukin 1. I. Induction of circulating interleukin 1 in rabbits in vivo and in human mononuclear cells in vitro. J Immunol 1987; 139: 1902-1910.
14. Granowitz EV, Vannier E, Poutsiaka DD, et al. Effect of interleukin-1 (IL-1) blockade on cytokine synthesis: II. IL-1 receptor antagonist inhibits lipopolysaccharide-induced cytokine synthesis by human monocytes. Blood 1992; 79: 2364-2369.
15. Besedovsky HO, Del Rey A. Central and peripheral cytokines mediate immune-brain connectivity. Neurochem Res 2011; 36: 1-6.
16. Pitossi F, Del Rey A, Kabiersch A, et al. Induction of cytokine transcripts in the central nervous system and pituitary following peripheral administration of endotoxin to mice. J Neurosci Res 1997; 48: 287-298.
17. Warner SJ, Auger KR, Libby P. Human interleukin 1 induces interleukin 1 gene expression in human vascular smooth muscle cells. J Exp Med 1987; 165: 1316-1331.
18. Del Rey A, Roggero E, Randolf A, et al. IL-1 resets glucose homeostasis at central levels. Proc Natl Acad Sci USA 2006; 103: 16039-16044.
19. O'Neill LA. The interleukin-1 receptor/Toll-like receptor superfamily: 10 years of progress. Immunol Rev 2008; 226: 10-18.
20. Shieh JH, Gordon M, Jakubowski A, et al. Interleukin-1 modulation of cytokine receptors on human neutrophils: in vitro and in vivo studies. Blood 1993; 81: 1745-1754.
21. Ben-Sasson SZ, Hu-Li J, Quiel J, et al. IL-1 acts directly on CD4 T cells to enhance their antigen-driven expansion and differentiation. Proc Natl Acad Sci USA 2009; 106: 7119-7124.
22. Cooper MA, Fehniger TA, Ponnappan A, et al. Interleukin-1beta costimulates interferon-gamma production by human natural killer cells. Eur J Immunol 2001; 31: 792-801.
23. Curtsinger JM, Mescher MF. Inflammatory cytokines as a third signal for T cell activation. Curr Opin Immunol 2010; 22: 333-340.
24. Huber M, Beuscher HU, Rohwer P, et al. Costimulation via TCR and IL-1 receptor reveals a novel IL-1alpha-mediated autocrine pathway of Th2 cell proliferation. J Immunol 1998; 160: 4242-4247.
25. Pape KA, Khoruts A, Mondino A, et al. Inflammatory cytokines enhance the in vivo clonal expansion and differentiation of antigen-activated CD4+ T cells. J Immunol 1997; 159: 591-598.
26. al-Ramadi BK, Welte T, Fernandez-Cabezudo MJ, et al. The Src-protein tyrosine kinase Lck is required for IL-1-mediated costimulatory signaling in Th2 cells. J Immunol 2001; 167: 6827-6833.
27. Ben-Sasson SZ, Hogg A, Hu-Li J, et al. IL-1 enhances expansion, effector function, tissue localization, and memory response of antigen-specific CD8 T cells. J Exp Med 2013; 210: 491-502.
28. Luqman M, Greenbaum L, Lu D, et al. Differential effect of interleukin 1 on naive and memory CD4+ T cells. Eur J Immunol 1992; 22: 95-100.
29. Sutton C, Brereton C, Keogh B, et al. A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J Exp Med 2006; 203: 1685-1691.
30. Li L, Kim J, Boussiotis VA. IL-1beta-mediated signals preferentially drive conversion of regulatory T cells but not conventional T cells into IL-17-producing cells. J Immunol 2010; 185: 4148-4153.
31. Brinster C, Shevach EM. Costimulatory effects of IL-1 on the expansion/differentiation of CD4+CD25+Foxp3+ and CD4+CD25+Foxp3- T cells. J Leukoc Biol 2008; 84: 480-487.
32. Besedovsky HO, Del Rey A. Interleukin-1 resets glucose homeostasis at central and peripheral levels: relevance for immunoregulation. Neuroimmunomodulation 2010; 17: 139-141.
33. Romanyukha AA, Rudnev SG, Sidorov IA. Energy cost of infection burden: an approach to understanding the dynamics of host-pathogen interactions. J Theor Biol 2006; 241: 1-13.
34. McGuinness OP. Defective glucose homeostasis during infection. Annu Rev Nutr 2005; 25: 9-35.
35. Fox CJ, Hammerman PS, Thompson CB. Fuel feeds function: energy metabolism and the T-cell response. Nat Rev Immunol 2005; 5: 844-852.
36. Fukuzumi M, Shinomiya H, Shimizu Y, et al. Endotoxin-induced enhancement of glucose influx into murine peritoneal macrophages via GLUT1. Infect Immun 1996; 64: 108-112.
37. Garcia-Welsh A, Schneiderman JS, Baly DL. Interleukin-1 stimulates glucose transport in rat adipose cells. Evidence for receptor discrimination between IL-1 beta and IL-1 alpha. FEBS Lett 1990; 269: 421-424.
38. Bird TA, Davies A, Baldwin SA, et al. Interleukin 1 stimulates hexose transport in fibroblasts by increasing the expression of glucose transporters. J Biol Chem 1990; 265: 13578-13583.
39. Shikhman AR, Brinson DC, Lotz MK. Distinct pathways regulate facilitated glucose transport in human articular chondrocytes during anabolic and catabolic responses. Am J Physiol Endocrinol Metab 2004; 286: E980-E985.
40. Gould GW, Cuenda A, Thomson FJ, et al. The activation of distinct mitogen-activated protein kinase cascades is required for the stimulation of 2-deoxyglucose uptake by interleukin-1 and insulin-like growth factor-1 in KB cells. Biochem J 1995; 311 (Pt 3): 735-738.
41. Fischereder M, Schroppel B, Wiese P, et al. Regulation of glucose transporters in human peritoneal mesothelial cells. J Nephrol 2003; 16: 103-109.
42. Riera MF, Galardo MN, Pellizzari EH, et al. Participation of phosphatidyl inositol 3-kinase/protein kinase B and ERK1/2 pathways in interleukin-1beta stimulation of lactate production in Sertoli cells. Reproduction 2007; 133: 763-773.
43. Metzger S, Nusair S, Planer D, et al. Inhibition of hepatic gluconeogenesis and enhanced glucose uptake contribute to the development of hypoglycemia in mice bearing interleukin-1beta-secreting tumor. Endocrinology 2004; 145: 5150-5156.
44. Dasu MR, Devaraj S, Jialal I. High glucose induces IL-1beta expression in human monocytes: mechanistic insights. Am J Physiol Endocrinol Metab 2007; 293: E337-E346.
45. Besedovsky HO, Del Rey A. Immune-neuro-endocrine interactions: facts and hypotheses. Endocr Rev 1996; 17: 64-102.
46. Del Rey A, Besedovsky H. Antidiabetic effects of interleukin 1. Proc Natl Acad Sci USA 1989; 86: 5943-5947.
47. Oguri S, Motegi K, Iwakura Y, et al. Primary role of interleukin-1 alpha and interleukin-1 beta in lipopolysaccharide-induced hypoglycemia in mice. Clin Diagn Lab Immunol 2002; 9: 1307-1312.
48. Shimizu H, Uehara Y, Shimomura Y, et al. Involvement of interleukin-1 in the inhibition of in vivo insulin release: possible role of adrenal glands. J Endocrinol Invest 1991; 14: 401-404.
49. Maitra SR, Wojnar MM, Lang CH. Alterations in tissue glucose uptake during the hyperglycemic and hypoglycemic phases of sepsis. Shock 2000; 13: 379-385.
50. Crown J, Jakubowski A, Kemeny N, et al. A phase I trial of recombinant human interleukin-1 beta alone and in combination with myelosuppressive doses of 5-fluorouracil in patients with gastrointestinal cancer. Blood 1991; 78: 1420-1427.
51. Agwunobi AO, Reid C, Maycock P, et al. Insulin resistance and substrate utilization in human endotoxemia. J Clin Endocrinol Metab 2000; 85: 3770-3778.
52. Bloesch D, Keller U, Spinas GA, et al. Effects of endotoxin on leucine and glucose kinetics in man: contribution of prostaglandin E2 assessed by a cyclooxygenase inhibitor. J Clin Endocrinol Metab 1993; 77: 1156-1163.
53. Soop M, Duxbury H, Agwunobi AO, et al. Euglycemic hyperinsulinemia augments the cytokine and endocrine responses to endotoxin in humans. Am J Physiol Endocrinol Metab 2002; 282: E1276-E1285.
54. Wen H, Gris D, Lei Y, et al. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol 2011; 12: 408-415.
55. Del Rey A, Monge-Arditi G, Klusman I, et al. Metabolic and endocrine effects of interleukin-1 in obese, diabetic Zucker fa/fa rats. Exp Clin Endocrinol Diabetes 1996; 104: 317-326.
56. Garcia MC, Wernstedt I, Berndtsson A, et al. Mature-onset obesity in interleukin-1 receptor I knockout mice. Diabetes 2006; 55: 1205-1213.
57. Hosoi T, Yokoyama S, Matsuo S, et al. Myeloid differentiation factor 88 (MyD88)-deficiency increases risk of diabetes in mice. PLoS One 2010; 5.
58. Matsuki T, Horai R, Sudo K, et al. IL-1 plays an important role in lipid metabolism by regulating insulin levels under physiological conditions. J Exp Med 2003; 198: 877-888.
59. Mandrup-Poulsen T, Pickersgill L, Donath MY. Blockade of interleukin 1 in type 1 diabetes mellitus. Nat Rev Endocrinol 2010; 6: 158-166.
60. Moran A, Bundy B, Becker DJ, et al. Interleukin-1 antagonism in type 1 diabetes of recent onset: two multicentre, randomised, double-blind, placebo-controlled trials. Lancet 2013.
61. Wen H, Ting JP, O'Neill LA. A role for the NLRP3 inflammasome in metabolic diseases--did Warburg miss inflammation? Nat Immunol 2012; 13: 352-357.
62. Akash MS, Shen Q, Rehman K, et al. Interleukin-1 receptor antagonist: a new therapy for type 2 diabetes mellitus. J Pharm Sci 2012; 101: 1647-1658.
63. Dinarello CA, Donath MY, Mandrup-Poulsen T. Role of IL-1beta in type 2 diabetes. Curr Opin Endocrinol Diabetes Obes 2010; 17: 314-321.
64. Ye J, McGuinness OP. Inflammation during obesity is not all bad: evidence from animal and human studies. Am J Physiol Endocrinol Metab 2013; 304: E466-E477.
65. Larsen CM, Faulenbach M, Vaag A, et al. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med 2007; 356: 1517-1526.
66. Jager J, Gremeaux T, Cormont M, et al. Interleukin-1beta-induced insulin resistance in adipocytes through down-regulation of insulin receptor substrate-1 expression. Endocrinology 2007; 148: 241-251.
67. Lagathu C, Yvan-Charvet L, Bastard JP, et al. Long-term treatment with interleukin-1beta induces insulin resistance in murine and human adipocytes. Diabetologia 2006; 49: 2162-2173.
68. Suzawa M, Takada I, Yanagisawa J, et al. Cytokines suppress adipogenesis and PPAR-gamma function through the TAK1/TAB1/NIK cascade. Nat Cell Biol 2003; 5: 224-230.
69. Luheshi GN, Gardner JD, Rushforth DA, et al. Leptin actions on food intake and body temperature are mediated by IL-1. Proc Natl Acad Sci USA 1999; 96: 7047-7052.
70. Mills KH, Dunne A. Immune modulation: IL-1, master mediator or initiator of inflammation. Nat Med 2009; 15: 1363-1364.
71. Li P, Lu M, Nguyen MT, et al. Functional heterogeneity of CD11c-positive adipose tissue macrophages in diet-induced obese mice. J Biol Chem 2010; 285: 15333-15345.
72. Nov O, Shapiro H, Ovadia H, et al. Interleukin-1beta regulates fat-liver crosstalk in obesity by auto-paracrine modulation of adipose tissue inflammation and expandability. PLoS One 2013; 8: e53626.
73. Hotamisligil GS, Erbay E. Nutrient sensing and inflammation in metabolic diseases. Nat Rev Immunol 2008; 8: 923-934.
74. Stienstra R, Tack CJ, Kanneganti TD, et al. The inflammasome puts obesity in the danger zone. Cell Metab 2012; 15: 10-18.
75. Backhed F, Ding H, Wang T, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 2004; 101: 15718-15723.
76. Cani PD, Amar J, Iglesias MA, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007; 56: 1761-1772.
77. Ley RE, Backhed F, Turnbaugh P, et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 2005; 102: 11070-11075.
78. Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006; 444: 1027-1031.
79. Del Rey A, Monge-Arditi G, Besedovsky HO. Central and peripheral mechanisms contribute to the hypoglycemia induced by interleukin-1. Ann N Y Acad Sci 1998; 840: 153-161.
80. Xu H, Barnes GT, Yang Q, et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003; 112: 1821-1830.
81. Schmidt MI, Duncan BB, Vigo A, et al. Leptin and incident type 2 diabetes: risk or protection? Diabetologia 2006; 49: 2086-2096.
82. Besedovsky HO, Del Rey A. Regulating inflammation by glucocorticoids. Nat Immunol 2006; 7: 537.