Deregulation of inflammatory response in the diabetic condition is associated with increased ischemic brain injury

Journal of Neuroinflammation

Volumn 11, Issue , 2014, Pages

  Kim, Eunhee ^a,b   Tolhurst, Aaron T ^a   Cho, Sunghee ^a,b  

^a Burke Cornell Medical Research Institute   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Diabetes; Inflammation; Ischemic stroke; Mice; Monocytes macrophages

Indexed keywords

CD36 ANTIGEN; CHEMOKINE RECEPTOR CCR2; GLUCOSE; INSULIN; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; CYTOKINE; GLUCOSE BLOOD LEVEL; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CCR2 GENE; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE ASSOCIATION; DISEASE EXACERBATION; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; IL 6 GENE; IMMUNOCOMPETENT CELL; INFLAMMATION; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; MACROPHAGE; MALE; MCP 1 GENE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OUTCOME ASSESSMENT; WEIGHT GAIN; ANIMAL; BLOOD; BRAIN INJURIES; C57BL MOUSE; CELL CULTURE; COMPLICATION; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC DIET; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PERITONEAL CAVITY; PHYSIOLOGY;

ANIMALS; ANTIGENS, CD36; BLOOD GLUCOSE; BRAIN INJURIES; BRAIN ISCHEMIA; CELLS, CULTURED; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC DIET; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; INSULIN; LIPOPOLYSACCHARIDES; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; PERITONEAL CAVITY;

EID: 84900001473     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-11-83     Document Type: Article

References (52)

1. Barton GM. A calculated response: control of inflammation by the innate immune system. J Clin Invest 2008, 118:413-420. 10.1172/JCI34431, 2214713, 18246191.
2. Hearps AC, Martin GE, Angelovich TA, Cheng WJ, Maisa A, Landay AL, Jaworowski A, Crowe SM. Aging is associated with chronic innate immune activation and dysregulation of monocyte phenotype and function. Aging Cell 2012, 11:867-875. 10.1111/j.1474-9726.2012.00851.x, 22708967.
3. Graves DT, Kayal RA. Diabetic complications and dysregulated innate immunity. Front Biosci 2008, 13:1227-1239. 10.2741/2757, 3130196, 17981625.
4. McColl BW, Rothwell NJ, Allan SM. Systemic inflammatory stimulus potentiates the acute phase and CXC chemokine responses to experimental stroke and exacerbates brain damage via interleukin-1- and neutrophil-dependent mechanisms. J Neurosci 2007, 27:4403-4412. 10.1523/JNEUROSCI.5376-06.2007, 17442825.
5. Kim E, Tolhurst AT, Qin LY, Chen XY, Febbraio M, Cho S. CD36/fatty acid translocase, an inflammatory mediator, is involved in hyperlipidemia-induced exacerbation in ischemic brain injury. J Neurosci 2008, 28:4661-4670. 10.1523/JNEUROSCI.0982-08.2008, 2830708, 18448643.
6. Kernan WN, Inzucchi SE. Type 2 diabetes mellitus and insulin resistance: stroke prevention and management. Curr Treat Options Neurol 2004, 6:443-450. 10.1007/s11940-004-0002-y, 15461922.
7. Almdal T, Scharling H, Jensen JS, Vestergaard H. The independent effect of type 2 diabetes mellitus on ischemic heart disease, stroke, and death: a population-based study of 13,000 men and women with 20 years of follow-up. Arch Intern Med 2004, 164:1422-1426. 10.1001/archinte.164.13.1422, 15249351.
8. Bonow RO, Gheorghiade M. The diabetes epidemic: a national and global crisis. Am J Med 2004, 116(Suppl 5A):2S-10S.
9. Capes SE, Hunt D, Malmberg K, Pathak P, Gerstein HC. Stress hyperglycemia and prognosis of stroke in nondiabetic and diabetic patients: a systematic overview. Stroke 2001, 32:2426-2432. 10.1161/hs1001.096194, 11588337.
10. Mankovsky BN, Ziegler D. Stroke in patients with diabetes mellitus. Diabetes Metab Res Rev 2004, 20:268-287. 10.1002/dmrr.490, 15250030.
11. Sundquist K, Li X. Type 1 diabetes as a risk factor for stroke in men and women aged 15-49: a nationwide study from Sweden. Diabet Med 2006, 23:1261-1267. 10.1111/j.1464-5491.2006.01959.x, 17054606.
12. Smyth S, Heron A. Diabetes and obesity: the twin epidemics. Nat Med 2006, 12:75-80. 10.1038/nm0106-75, 16397575.
13. Kern PA, Ranganathan S, Li C, Wood L, Ranganathan G. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab 2001, 280:E745-E751.
14. Nomura S, Shouzu A, Omoto S, Nishikawa M, Fukuhara S. Significance of chemokines and activated platelets in patients with diabetes. Clin Exp Immunol 2000, 121:437-443. 10.1046/j.1365-2249.2000.01324.x, 1905738, 10971508.
15. Kamei N, Tobe K, Suzuki R, Ohsugi M, Watanabe T, Kubota N, Ohtsuka-Kowatari N, Kumagai K, Sakamoto K, Kobayashi M, Yamauchi T, Ueki K, Oishi Y, Nishimura S, Manabe I, Hashimoto H, Ohnishi Y, Ogata H, Tokuyama K, Tsunoda M, Ide T, Murakami K, Nagai R, Kadowaki T. Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance. J Biol Chem 2006, 281:26602-26614. 10.1074/jbc.M601284200, 16809344.
16. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, Kitazawa R, Kitazawa S, Miyachi H, Maeda S, Egashira K, Kasuga M. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 2006, 116:1494-1505. 10.1172/JCI26498, 1459069, 16691291.
17. Weisberg SP, Hunter D, Huber R, Lemieux J, Slaymaker S, Vaddi K, Charo I, Leibel RL, Ferrante AW. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest 2006, 116:115-124. 10.1172/JCI24335, 1307559, 16341265.
18. Tateya S, Tamori Y, Kawaguchi T, Kanda H, Kasuga M. An increase in the circulating concentration of monocyte chemoattractant protein-1 elicits systemic insulin resistance irrespective of adipose tissue inflammation in mice. Endocrinology 2010, 151:971-979. 10.1210/en.2009-0926, 20056828.
19. Greenwalt DE, Scheck SH, Rhinehart-Jones T. Heart CD36 expression is increased in murine models of diabetes and in mice fed a high fat diet. J Clin Invest 1995, 96:1382-1388. 10.1172/JCI118173, 185760, 7544802.
20. Griffin E, Re A, Hamel N, Fu C, Bush H, McCaffrey T, Asch AS. A link between diabetes and atherosclerosis: Glucose regulates expression of CD36 at the level of translation. Nat Med 2001, 7:840-846. 10.1038/89969, 11433350.
21. Handberg A, Levin K, Hojlund K, Beck-Nielsen H. Identification of the oxidized low-density lipoprotein scavenger receptor CD36 in plasma: a novel marker of insulin resistance. Circulation 2006, 114:1169-1176. 10.1161/CIRCULATIONAHA.106.626135, 16952981.
22. Sampson MJ, Davies IR, Braschi S, Ivory K, Hughes DA. Increased expression of a scavenger receptor (CD36) in monocytes from subjects with Type 2 diabetes. Atherosclerosis 2003, 167:129-134. 10.1016/S0021-9150(02)00421-5, 12618277.
23. Cho S, Szeto HH, Kim E, Kim H, Tolhurst AT, Pinto JT. A novel cell-permeable antioxidant peptide, SS31, attenuates ischemic brain injury by down-regulating CD36. J Biol Chem 2007, 282:4634-4642. 10.1074/jbc.M609388200, 17178711.
24. Ding AH, Nathan CF, Stuehr DJ. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol 1988, 141:2407-2412.
25. Tsunawaki S, Nathan CF. Enzymatic basis of macrophage activation. Kinetic analysis of superoxide production in lysates of resident and activated mouse peritoneal macrophages and granulocytes. J Biol Chem 1984, 259:4305-4312.
26. Bao Y, Kim E, Bhosle S, Mehta H, Cho S. A role for spleen monocytes in post-ischemic brain inflammation and injury. J Neuroinflammation 2010, 7:92. 10.1186/1742-2094-7-92, 3016273, 21159187.
27. Swirski FK, Libby P, Aikawa E, Alcaide P, Luscinskas FW, Weissleder R, Pittet MJ. Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest 2007, 117:195-205. 10.1172/JCI29950, 1716211, 17200719.
28. Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, Figueiredo JL, Kohler RH, Chudnovskiy A, Waterman P, Aikawa E, Mempel TR, Libby P, Weissleder R, Pittet MJ. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 2009, 325:612-616. 10.1126/science.1175202, 2803111, 19644120.
29. Kim E, Febbraio M, Bao Y, Tolhurst AT, Epstein JM, Cho S. CD36 in the periphery and brain synergizes in stroke injury in hyperlipidemia. Ann Neurol 2012, 71:753-764. 10.1002/ana.23569, 3383818, 22718544.
30. Lin TN, He YY, Wu G, Khan M, Hsu CY. Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 1993, 24:117-121. 10.1161/01.STR.24.1.117, 8418534.
31. Bates SH, Stearns WH, Dundon TA, Schubert M, Tso AW, Wang Y, Banks AS, Lavery HJ, Haq AK, Maratos-Flier E, Neel BG, Schwartz MW, Myers MG. STAT3 signalling is required for leptin regulation of energy balance but not reproduction. Nature 2003, 421:856-859. 10.1038/nature01388, 12594516.
32. Kondo T, Kahn CR. Altered insulin signaling in retinal tissue in diabetic states. J Biol Chem 2004, 279:37997-38006. 10.1074/jbc.M401339200, 15201286.
33. Orland MJ, Permutt MA. Quantitative analysis of pancreatic proinsulin mRNA in genetically diabetic (db/db) mice. Diabetes 1987, 36:341-347. 10.2337/diab.36.3.341, 3542656.
34. Folbergrova J, Memezawa H, Smith ML, Siesjo BK. Focal and perifocal changes in tissue energy state during middle cerebral artery occlusion in normo- and hyperglycemic rats. J Cereb Blood Flow Metab 1992, 12:25-33. 10.1038/jcbfm.1992.4, 1727140.
35. Hoxworth JM, Xu K, Zhou Y, Lust WD, LaManna JC. Cerebral metabolic profile, selective neuron loss, and survival of acute and chronic hyperglycemic rats following cardiac arrest and resuscitation. Brain Res 1999, 821:467-479. 10.1016/S0006-8993(98)01332-8, 10064834.
36. Siesjo BK. Mechanisms of ischemic brain damage. Crit Care Med 1988, 16:954-963. 10.1097/00003246-198810000-00006, 3048896.
37. Nedergaard M, Diemer NH. Focal ischemia of the rat brain, with special reference to the influence of plasma glucose concentration. Acta Neuropathol 1987, 73:131-137. 10.1007/BF00693778, 3604580.
38. Nedergaard M, Jakobsen J, Diemer NH. Autoradiographic determination of cerebral glucose content, blood flow, and glucose utilization in focal ischemia of the rat brain: influence of the plasma glucose concentration. J Cereb Blood Flow Metab 1988, 8:100-108. 10.1038/jcbfm.1988.13, 3339100.
39. Vannucci SJ, Willing LB, Goto S, Alkayed NJ, Brucklacher RM, Wood TL, Towfighi J, Hurn PD, Simpson IA. Experimental stroke in the female diabetic, db/db, mouse. J Cereb Blood Flow Metab 2001, 21:52-60.
40. Alvarez-Rodriguez L, Lopez-Hoyos M, Calvo-Alen J, Aurrecoechea E, Villa I, Martinez-Taboada VM. Phagocyte dysfunction in polymyalgia rheumatica and other age-related, chronic, inflammatory conditions. J Leukoc Biol 2013, 94:1071-1078.
41. Kumari R, Willing LB, Krady JK, Vannucci SJ, Simpson IA. Impaired wound healing after cerebral hypoxia-ischemia in the diabetic mouse. J Cereb Blood Flow Metab 2007, 27:710-718.
42. Ilyas R, Wallis R, Soilleux EJ, Townsend P, Zehnder D, Tan BK, Sim RB, Lehnert H, Randeva HS, Mitchell DA. High glucose disrupts oligosaccharide recognition function via competitive inhibition: a potential mechanism for immune dysregulation in diabetes mellitus. Immunobiology 2011, 216:126-131. 10.1016/j.imbio.2010.06.002, 3088832, 20674073.
43. Kumari R, Willing LB, Patel SD, Krady JK, Zavadoski WJ, Gibbs EM, Vannucci SJ, Simpson IA. The PPAR-gamma agonist, darglitazone, restores acute inflammatory responses to cerebral hypoxia-ischemia in the diabetic ob/ob mouse. J Cereb Blood Flow Metab 2010, 30:352-360. 10.1038/jcbfm.2009.221, 2949120, 19861974.
44. Martins JO, Ferracini M, Anger DB, Martins DO, Ribeiro LF, Sannomiya P, Jancar S. Signaling pathways and mediators in LPS-induced lung inflammation in diabetic rats: role of insulin. Shock 2010, 33:76-82. 10.1097/SHK.0b013e3181a85ec4, 19373130.
45. Martins JO, Zanoni FL, Martins DO, Coimbra R, Krieger JE, Jancar S, Sannomiya P. Insulin regulates cytokines and intercellular adhesion molecule-1 gene expression through nuclear factor-kappaB activation in LPS-induced acute lung injury in rats. Shock 2009, 31:404-409. 10.1097/SHK.0b013e318186275e, 18791499.
46. Cho S, Park EM, Febbraio M, Anrather J, Park L, Racchumi G, Silverstein RL, Iadecola C. The class B scavenger receptor CD36 mediates free radical production and tissue injury in cerebral ischemia. J Neurosci 2005, 25:2504-2512. 10.1523/JNEUROSCI.0035-05.2005, 15758158.
47. Alkhatatbeh MJ, Mhaidat NM, Enjeti AK, Lincz LF, Thorne RF. The putative diabetic plasma marker, soluble CD36, is non-cleaved, non-soluble and entirely associated with microparticles. J Thromb Haemost 2011, 9:844-851. 10.1111/j.1538-7836.2011.04220.x, 21276198.
48. Bruno A, Qualls C. Risk factors for intracerebral and subarachnoid hemorrhage among Hispanics and non-Hispanic whites in a New Mexico community. Neuroepidemiology 2000, 19:227-232. 10.1159/000026252, 10859503.
49. Eugenin EA, D'Aversa TG, Lopez L, Calderon TM, Berman JW. MCP-1 (CCL2) protects human neurons and astrocytes from NMDA or HIV-tat-induced apoptosis. J Neurochem 2003, 85:1299-1311. 10.1046/j.1471-4159.2003.01775.x, 12753088.
50. Madrigal JL, Leza JC, Polak P, Kalinin S, Feinstein DL. Astrocyte-derived MCP-1 mediates neuroprotective effects of noradrenaline. J Neurosci 2009, 29:263-267. 10.1523/JNEUROSCI.4926-08.2009, 19129402.
51. DiPietro LA, Polverini PJ, Rahbe SM, Kovacs EJ. Modulation of JE/MCP-1 expression in dermal wound repair. Am J Pathol 1995, 146:868-875. 1869244, 7717454.
52. Low QE, Drugea IA, Duffner LA, Quinn DG, Cook DN, Rollins BJ, Kovacs EJ, DiPietro LA. Wound healing in MIP-1alpha(-/-) and MCP-1(-/-) mice. Am J Pathol 2001, 159:457-463. 10.1016/S0002-9440(10)61717-8, 1850564, 11485904.