The effect of short-term hyperglycemia on the innate immune system

American Journal of the Medical Sciences

Volumn 351, Issue 2, 2016, Pages 201-211

  Jafar, Nagham ^a   Edriss, Hawa ^a   Nugent, Kenneth ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

Author keywords

Complement; Host defenses; Hyperglycemia; Neutrophils; Vascular endothelium

Indexed keywords

CYTOKINE; GLUCOSE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; PROTEIN KINASE C; SUPEROXIDE; TOLL LIKE RECEPTOR;

APOPTOSIS; CELL MIGRATION; CELL PHAGOCYTOSIS; CELLULAR IMMUNITY; CLINICAL TRIAL (TOPIC); COMPLEMENT SYSTEM; CRITICALLY ILL PATIENT; CYTOKINE PRODUCTION; ENDOTHELIUM; ENZYME ACTIVATION; EXTRACELLULAR TRAP; GLUCOSE BLOOD LEVEL; GLYCEMIC CONTROL; HOSPITAL INFECTION; HOSPITAL PATIENT; HOST RESISTANCE; HUMAN; HYPERGLYCEMIA; INFLAMMATION; INNATE IMMUNITY; INTRACELLULAR SIGNALING; NEUTROPHIL; NONHUMAN; OPSONIZATION; PHAGOCYTOSIS; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SHORT COURSE THERAPY; SURGICAL INFECTION; SYSTEMATIC REVIEW; VASODILATATION; COMPLICATION; CROSS INFECTION; DIABETES COMPLICATIONS; IMMUNOLOGY;

CROSS INFECTION; DIABETES COMPLICATIONS; HUMANS; HYPERGLYCEMIA; IMMUNITY, INNATE;

EID: 84960862038     PISSN: 00029629     EISSN: 15382990     Source Type: Journal    
DOI: 10.1016/j.amjms.2015.11.011     Document Type: Review

References (88)

1. Ken I, Jayshree D, Alison P. Nosocomial infections. Contin Educ Anaesth Crit Care Pain 2005;5:14-7.
2. National Nosocomial Infections Surveillance (NNIS) System report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control 2004;32:470-85.
3. Emine A, Andreas V. Ventilator associated pneumonia and infection control. Ann Clin Microbiol Antimicrob 2006;5:7, http://dx.doi.org/10.1186/1476-0711-5-7.
4. Vergidis P, Patel R. Novel approaches to the diagnosis, prevention, and treatment of med ical device-associated infections. Infect Dis Cl in North Am 2012;26:173-86.
5. Wurtz R, Karajovic M, Dacumos E, et al. Nosocomial infections in a burn intensive care unit. Burns 1995;21:181-4.
6. Giamberardino HI, Cesário EP, Carmes ER, et al. Risk factors for nosocomial infection in trauma patients. Braz J Infect Dis 2007;11:285-9.
7. Dana TG, Rayyan AK. Diabetic complications and dysregulated innate immunity. Front Biosci 2008;13:1227-39.
8. Juliana C, Janine C, Cresio A. Infections in patients with diabetes mellitus: a review of pathogenesis. Indian J Endocrinol Metab 2012;16: 27-36.
9. Krinsley JS. Association between hyperglycemia and increased hospital mortality in a heterogeneous population of critically ill patients. Mayo Clin Proc 2003;78:1471-8.
10. Butler SO, Btaiche IF, Alaniz C. Relationship between hyperglycemia and infection in critically ill patients. Pharmacotherapy 2005;25:963-76.
11. Litman GW, Cannon JP, Dishaw LJ. Reconstructing immune phylog-eny: new perspectives. Nat Rev Immunol 2005;5:866-79.
12. Hoffmann J, Akira S. Innate immunity. Curr Opin Immunol 2013;25:1-3.
13. Janeway CA Jr, Travers P, Walport M, et al. Immunobiology: The Immune System in Health and Disease: Principles of Innate and Adaptive Immunity. 5th ed, New York: Garland Science; 2001.
14. Alba-Loureiro TC, Munhoz CD, Martins JO, et al. Neutrophil function and metabolism in individuals with diabetes mell itus. Braz J Med Biol Res 2007;40:1037-44.
15. Kjersem H, Hilsted J, Madsbad S, et al. Polymorphonuclear leucocyte dysfunction during short term metabolic changes from normo- to hyper-glycemia in type I (i nsul in dependent) diabetic patients. Infection 1988; 16:215-21.
16. Daoud AK, Tayyar MA, Fouda IM, et al. Effect of diabetes mellitus vs in vitro hyperglycemia on selected immune cell functions. J Immunotoxicol 2009;6(1):36-41.
17. Inoue T, Saito H, Matsuda, et al. Growth hormone and insulin-like growth I augment bactericidal capacity of human polymorphonuclear neutrophils. Shock 1998;10(4):278-84.
18. Jin G, Guo Y, Ball C, Houston C. Insulin-like growth factor enhances phagocytosis by human neutrophils in vitro. Regul Pept 1993;49(2):125-31.
19. Stegenga ME, van der Crabben SN, Blumer RM, et al. Hyperglycemia enhances coagulation and reduces neutrophil degranulation, whereas hyperinsulinemia inhibits fibri nolysis duri ng human endotoxemia. Blood 2008;112:82-9.
20. Wierusz-Wysocka B, Wysocki H, Wykretowicz A, et al. The influence of increasing glucose concentrations on selected functions of polymor-phonuclear neutrophils. Acta Diabetol Lat 1988;25:283-8.
21. Nielson CP, Hindson DA. Inhibition of polymorphonuclear leukocyte respiratory burst by elevated glucose concentrations in vitro. Diabetes 1989;38:1031-5.
22. Van Oss CJ, Border JR. Influence of intermittent hyperglycemic glucose levels on the phagocytosis of microorganisms by human granulocytes in vitro. Immunol Commun 1978;7:669-76.
23. Brinkmann V, Zychlinsky A. Neutrophil extracellular traps: is immunity the second function of chromatin? J Cell Biol 2012;198: 773-83.
24. Joshi MB, Lad A, Prasad ASB, et al. High glucose modulates IL-6 mediated immune homeostasis through impeding neutrophil extracellular trap formation. FEBS Lett 2013;587:2241-6.
25. Prince LR, Whyte MK, Sabroe I, et al. The role of TLRs in neutrophil activation. Curr Opin Pharmacol 2011;11:397-403.
26. Dasu MR, Devaraj S, Zhao L, et al. High glucose induces toll-like receptor expression in human monocytes. Diabetes 2008;57:3090-8.
27. Jialal I, Polage C, Devaraj S. Severe hyperglycemia down regulates tolllike receptors on neutrophils: implications for propensity to infections in Diabetes. FASEB J 2013;27(648):11.
28. Xiu F, Stanjcic M, Diao L, Jeschke MG. Stress hyperglycemia, insulin treatment, and innate immune cells. Int J Endocrinol 2014; 2014:1-8.
29. Perner A, Nielsen SE, Rask-Madsen J. High glucose impairs super-oxide production from isolated blood neutrophils. Intensive Care Med 2003;29:642-5.
30. Oldenborg PA, Sundqvist IM, Sehlin J. Different effects of glucose on extracellular and intracellular respiratory burst response in normal human neutrophils activated with the soluble agonist fMet-Leu-Phe. Diabet Med 2000;17:532-7.
31. Metzler KD, Fuchs TA, Nauseef WM, et al. Myeloperoxidase is required for extracellular trap formation: implications for immunity. Blood 2011;117:953-9.
32. Oldenborg P, Sehlin J. Hyperglycemia in vitro attenuates insulin-stimulated chemokinesis in normal human neutrophils: role of protein kinase C activation. J Leukocyte Biol 1999;65:635-40.
33. Ferrero-Miliani L, Nielsen OH, Andersen PS, et al. Chronic inflammation: importance of NOD2 and NALP3 in interleukin-1beta generation. Clin Exp Immunol 2007;147:227-35.
34. Kim SH, Park KW, Kim YS, et al. Effects of acute hyperglycemia on endothelium-dependent vasodilation in patients with diabetes mellitus or impaired glucose metabolism. Endothelium 2003;10:65-70.
35. Gomes MB, Affonso FS, Cailleaux S, et al. Glucose levels observed in daily clinical practice induce endothelial dysfunction in the rabbit macro-and microcirculation. Fundam Clin Pharmacol 2004;18:339-46.
36. Santilli F, Cipollone F, Mezzetti A, et al. The role of nitric oxide in the development of diabetic angiopathy. Horm Metab Res 2004;36:319-35.
37. Schiekofer S, Balletshofer B, Andrassy M, et al. Endothelial dysfunction in diabetes mellitus. Semin Thromb Hemost 2000;26:503-11.
38. Bjornstad-Ostensen A, Berg T. The role of nitric oxide, adrenergic activation and kin in-degradat ion in blood pressure homeostasi s following an acute kinin-induced hypotension. Br J Pharmacol 1994;113:1567-73.
39. Chakravarthy U, Hayes RG, Stitt AW, et al. Constitutive nitric oxide synthase expression in retinal vascular endothelial cells is suppressed by high glucose and advanced glycation end products. Diabetes 1998;47:945-52.
40. Beckman JA, Goldfine AB, Gordon MB, et al. Inhibition of protein kinase Cp prevents impaired endothelium-dependent vasodilation caused by hyperglycemia in humans. Circ Res 2002;90:107-11.
41. Ishii H, Jirousek MR, Koya D, et al. Amelioration of vascular dysfunctions in diabetic rats by an oral PKC beta inhibitor. Science 1996;272:728-31.
42. Hempel A, Maasch C, Heintze U, et al. High glucose concentrations increase endothel ial cell permeabi l ity via activation of protei n ki nase C alpha. Circ Res 1997;81:363-71.
43. Liu XJ, Zhang ZD, Ma XC. High glucose enhances LPS-stimulated human PMVEC hyperpermeability via the NO pathway. Exp Ther Med 2013;6(2):361-7.
44. Tesfamariam B, Brown ML, Cohen RA. Elevated glucose impairs endothel ium-dependent relaxation by activati ng protei n ki nase C. J Clin Invest 1991;87:1643-8.
45. Cosentino F, Eto M, De Paolis P, et al. High glucose causes upregulation of cyclooxygenase-2 and alters prostanoid profile in human endothelial cells: role of protein kinase C and reactive oxygen species. Circulation 2003;107:1017-23.
46. Tesfamariam B, Cohen RA. Free radicals mediate endothelial cell dysfunction caused by elevated glucose. Am J Physiol 1992;263:321-6.
47. Steinbert BE, Goldenberg NM, Lee WL. Do viral infections mimic bacterial sepsis? The role of microvascular permeability: a review of mechanisms and methods. Antiviral Res 2012;93:2-15.
48. Tang S, Leung JC, Chan LY, et al. Regulation of complement C3 and C4 synthesis in human peritoneal mesothelial cells by peritoneal dialysis fluid. Clin Exp Immunol 2004;136:85-94.
49. Young GA, Kendall S, Brownjohn AM. Complement activation during CAPD. Nephrol Dial Transplant 1993;8:1372-5.
50. Reddingius RE, Schroder CH, Daha MR, et al. Complement in serum and dialysate in children on continuous ambulatory peritoneal dialysis. Perit Dial Int 1995;15:49-53.
51. Saiepour D, Sehlin J, Oldenborg PA. Hyperglycemia-induced protein kinase C activation inhibits phagocytosis of C3b- and immunoglobul in g-opsonized yeast particles in normal human neutrophils. Exp Diabesity Res 2003;4:125-32.
52. Hostetter MK. Handicaps to host defense. Effects of hyperglycemia on C3 and Candida albicans. Diabetes 1990;39:271-5.
53. Hennessey PJ, Black CT, Andrassy RJ. Nonenzymatic glycosylation of immunoglobulin G impairs complement fixation. J Parenter Enteral Nutr 1991;15:60-4.
54. Hair PS, Echague CG, Rohn RD, et al. Hyperglycemic conditions inhibit C3-mediated immunological control of Staphylococcus aureus. J Transl Med 2012;10:35.
55. Mauriello CT, Hair PS, Rohn RD, et al. Hyperglycemia inhibits complement-mediated immunological control of S. aureus in a rat model of peritonitis. J Diabetes Res 2014;1-11.
56. Belardelli F. Role of interferons and other cytokines in the regulation of the immune response. APMIS 1995;102:161-79.
57. De Rekeneire N, Peila R, Ding J, et al. Diabetes, hyperglycemia, and inflammation in older individuals, the health, aging and body composition study. Diabetes Care 2006;29:1902-8.
58. Ling PR, Smith RJ, Bistrian BR. Hyperglycemia enhances the cytokine production and oxidative responses to a low but not high dose of endotoxin in rats. Crit Care Med 2005;33:1084-9.
59. Morohoshi M, Fujisawa K, Uchimura I, et al. Glucose-dependent interleukin 6 and tumor necrosis factor production by human peripheral blood monocytes in vitro. Diabetes 1996;45:954-9.
60. Morohoshi M, Fujisawa K, Uchimura I, et al. The effect of glucose and advanced glycation end products on IL-6 production by human mono-cytes. Ann N Y Acad Sci 1995;748:562-70.
61. Otto MN, Schindler R, Lun A, et al. Hyperosmotic stress enhances cytoki ne product ion and decreases phagocytos is in vitro. Crit Care 2008; 12:R107.
62. Krogh-Madsen R, Moller K, Dela F, et al. Effect of hyperglycemia and hyperinsulinemia on the response of IL-6, TNF-alpha, and FFAs to low-dose endotoxemia in humans. Am J Physiol Endocrinol Metab 2004; 286:766-72.
63. Esposito K, Nappo F, Marfella R, et al. Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: role of oxidative stress. Circulation 2002;106:2067-72.
64. Devaraj S, Venugopal SK, Singh U, Jialal I. Hyperglycemia induces monocytic release of interleukin-6 via induction of protein kinase c-{alpha} and - {beta}. Diabetes 2005;54:85-91.
65. Shanmugam N, Reddy MA, Guha M, et al. High glucose-induced expression of proinflammatory cytokine and chemokine genes in mono-cytic cells. Diabetes 2003;52:1256-64.
66. Leonidou L, Mouzaki A, Michalaki M, et al. Cytokine production and hospital mortality in patients with sepsis-induced stress hyperglycemia. J Infect 2007;55:340-6.
67. Haneda M, Koya D, Isono M, Kikkawa R. Overview of glucose signaling in mesangial cells in diabetic nephropathy. J Am Soc Nephrol 2003; 14:1374-82.
68. Xi G, Shen X, Wai C, et al. Hyperglycemia stimulates p62/PKC interaction, which mediates NF-kB activation, increased Nox4 expression, and inflammatory cytokine activation in vascular smooth muscle. FASEB J 2015;29:1-11.
69. Mudaliar H, Pollock C, Jin Ma, et al. The role of TLR2 and 4-mediated inflammatory pathways in endothelial cells exposed to high glucose. PLOS One 2014;9(10):3108844.
70. Siddle K. Signalling by insulin and IGJ receptors: supporting acts and new players. J Mol Endocrinol 2011;47:R1-10.
71. Kosiborod M, Rathore SS, Inzucchi SE, et al. Admission glucose and mortal ity in elderly patients hospital ized with acute myocardial infarction. Circulation 2005;11:3078-86.
72. Inzucchi SE, Siegel MD. Glucose control in the ICU-how tight is too tight? N Engl J Med 2009;360(13):1346-9.
73. van den Berghe G, Wouters P, Weekers F, et al. Intensive insulin therapy in critically ill patients. N Engl J Med 2001;345(19):1359-67.
74. Van den Berghe G, Wilmer A, Hermans G, et al. Intensive therapy in the medical ICU. N Engl J Med 2006;354(2):449-61.
75. Finfer S, Chittock DR, Su SY, et al. The NICE-SUGAR Study Investigators. Intensive versus conventional glucose control in critically ill patients. N Engl J Med 2009;360(13):1283-97.
76. Arabi YM, Dabbagh OC, Tamim HM, et al. Intensive versus conventional insulin therapy: a randomized controlled trial in medical and surgical critically ill patients. Crit Care Med 2008;36(12):3190-7.
77. Kalfon P, Giraudeau B, Ichai C, et al. Tight computerized versus conventional glucose control in the ICU: a randomized controlled trial. Intensive Care Med 2014;40(2):171-81.
78. Brunkhorst FM, Engel C, Gloos F, et al. German Competence Network Sepsis (SepNet). Intensive insulin therapy and pentastarch resuscitation in severe sepsis. N Engl J Med 2008;358(2):125-39.
79. Qoi YC, Dagi TF, Maltenfort M, et al. Tight glycemic control reduces infection and improves outcmoe in neurosurgical and neurological patients. Neurosurgery 2012;71(3):692-702.
80. Murad MH, Coburn JA, Coto-Yglesias F, et al. Glycemic control in con-critically ill hospitalized patients: a systematic review and metaanalysis. J Clin Endocrinol Metab 2012;97(1):49-58.
81. Sathya B, Davis R, Taveira T, et al. Intensity of peri-operative glycemic control and postoperative outcomes in patients with diabetes: a meta-analysis. Diabetes Res Clin Pract 2013;102(1):8-15.
82. Boreland L, Scott-Hudson M, Hetherington K, et al. The effectiveness of tight glycemic control on decreasing surgical site infections and readmission rates in adult patients with diabetes undergoing cardiac surgery: a systematic review. Heart Lung 2015;44(5):430-40.
83. Hemmila MR, Taddonio MA, Arbabi S, et al. Intensive insulin therapy is associated with reduced infectious complications in burn patients. Surgery 2008;144(4):629-37.
84. Grey NJ, Pedrizet GA. Reduction of nosocomial infections in the surgical intensive-care unit by strict glycemic control. Endocr Pract 2004;10(suppl 2): S46-52.
85. Umpierrez GE, Isaacs SD, Bazargan H, et al. Hyperglycemia: an independent marker of in-hospital mortality in patients with undiagnosed diabetes. J Clin Endocrinol Metabol 2002;87: 978-82.
86. McAlister FA, Majumdar SR, Blitz S, et al. The relation between hyperglycemia and outcomes in 2,471 patients admitted to the hospital with community-acquired pneumonia. Diabetes Care 2005;28: 810-5.
87. Capes SE, Hunt D, Malmberg K, et al. Stress hyperglycaemia and increased risk of death after myocardial infarction in patients with and without diabetes: a systematic overview. Lancet 2000;355:773-8.
88. Minakata K, Sakata R. Perioperative control of blood glucose level in cardiac surgery. Gen Thorac Cardiovasc Surg 2013;61(2):61-6.