Exaggerated Neutrophil-Mediated Reperfusion Injury after Ischemic Stroke in a Rodent Model of Type 2 Diabetes

Microcirculation

Volumn 18, Issue 7, 2011, Pages 552-561

  Ritter, Leslie ^a,b   Davidson, Lisa ^a   Henry, Melissa ^a   Davis Gorman, Grace ^a   Morrison, Helena ^a   Frye, Jennifer B ^a   Cohen, Zoe ^a,b   Chandler, Sierra ^a   Mcdonagh, Paul ^a,b   Funk, Janet L ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Neutrophil; Reperfusion injury; Stroke; Type 2 diabetes; Zucker Diabetic Fatty rat

Indexed keywords

CD11B ANTIGEN; CHEMOATTRACTANT; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA;

ACUTE DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN MICROCIRCULATION; CELL ADHESION; CELL AGGREGATION; CHRONIC DISEASE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE MODEL; ENDOTHELIUM CELL; GENE EXPRESSION; INFLAMMATION; KERATINOCYTE; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE FUNCTION; NEUTROPHIL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; ONCOGENE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; ZUCKER DIABETIC FATTY RAT;

ANIMALS; ANTIGENS, CD11B; CELL ADHESION; CHEMOKINE CXCL1; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; E-SELECTIN; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION; INTERLEUKIN-1BETA; NEUTROPHILS; RATS; RATS, ZUCKER; REPERFUSION INJURY; STROKE;

ANIMALIA; RATTUS; RODENTIA;

EID: 80053483438     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1111/j.1549-8719.2011.00115.x     Document Type: Article

References (51)

1. 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 20years of follow-up. Arch Intern Med 164: 1422-1426, 2004.
2. Andersen KK, Olsen TS. One-month to 10-year survival in the copenhagen stroke study: interactions between stroke severity and other prognostic indicators. J Stroke Cerebrovasc Dis 20: 117-123, 2011.
3. Boyle JP, Honeycutt AA, Narayan KM, Hoerger TJ, Geiss LS, Chen H, Thompson TJ. Projection of diabetes burden through 2050: impact of changing demography and disease prevalence in the U.S. Diabetes Care 24: 1936-1940, 2001.
4. Cohen Z, Gonzales RF, Davis-Gorman GF, Copeland JG, McDonagh PF. Thrombin activity and platelet microparticle formation are increased in type 2 diabetic platelets: a potential correlation with caspase activation. Thromb Res 107: 217-221, 2002.
5. Dandona P, Aljada A, Bandyopadhyay A. Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol 25: 4-7, 2004.
6. Dandona P, Aljada A, Chaudhuri A, Mohanty P, Garg R. Metabolic syndrome: a comprehensive perspective based on interactions between obesity, diabetes, and inflammation. Circulation 111: 1448-1454, 2005.
7. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11: 98-107, 2011.
8. El-Benna J, Dang PM, Gougerot-Pocidalo MA. Priming of the neutrophil NADPH oxidase activation: role of p47phox phosphorylation and NOX2 mobilization to the plasma membrane. Semin Immunopathol 30: 279-289, 2008.
9. Ergul A, Li W, Elgebaly MM, Bruno A, Fagan SC. Hyperglycemia, diabetes and stroke: focus on the cerebrovasculature. Vascul Pharmacol 51: 44-49, 2009.
10. Ferreira L, Teixeira-de-Lemos E, Pinto F, Parada B, Mega C, Vala H, Pinto R, Garrido P, Sereno J, Fernandes R, Santos P, Velada I, Melo A, Nunes S, Teixeira F, Reis F. Effects of sitagliptin treatment on dysmetabolism, inflammation, and oxidative stress in an animal model of type 2 diabetes (ZDF rat). Mediators Inflamm 2010: 592760, 2010.
11. Funk JL, Frye JB, Oyarzo JN, Chen G, Lantz RC, Jolad SD, Solyom AM, Timmermann BN. Efficacy and mechanism of action of turmeric supplements in the treatment of experimental arthritis. Arthritis Rheum 54: 3452-3464, 2006.
12. Funk JL, Migliati E, Chen G, Wei H, Wilson J, Downey KJ, Mullarky PJ, Coull BM, McDonagh PF, Ritter LS. Parathyroid hormone-related protein induction in focal stroke: a neuroprotective vascular peptide. Am J Physiol Regul Integr Comp Physiol 284: R1021-R1030, 2003.
13. Gao X, Picchi A, Zhang C. Upregulation of TNF-alpha and receptors contribute to endothelial dysfunction in Zucker Diabetic Rats. Am J Biomed Sci 2: 1-12, 2010.
14. Griffen SC, Wang J, German MS. A genetic defect in beta-cell gene expression segregates independently from the fa locus in the ZDF rat. Diabetes 50: 63-68, 2001.
15. Guilherme A, Virbasius JV, Puri V, Czech MP. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol 9: 367-377, 2008.
16. Hokama JY, Ritter LS, Davis-Gorman G, Cimetta AD, Copeland JG, McDonagh PF. Diabetes enhances leukocyte accumulation in the coronary microcirculation early in reperfusion following ischemia. J Diabetes Complications 14: 96-107, 2000.
17. Hurn PD, Subramanian S, Parker SM, Afentoulis ME, Kaler LJ, Vandenbark AA, Offner H. T- and B-cell-deficient mice with experimental stroke have reduced lesion size and inflammation. J Cereb Blood Flow Metab 27: 1798-1805, 2007.
18. Iadecola C, Zhang F, Xu S, Casey R, Ross ME. Inducible nitric oxide synthase gene expression in brain following cerebral ischemia. J Cereb Blood Flow Metab 15: 378-384, 1995.
19. Janghorbani M, Hu FB, Willett WC, Li TY, Manson JE, Logroscino G, Rexrode KM. Prospective study of type 1 and type 2 diabetes and risk of stroke subtypes: the Nurses' Health Study. Diabetes Care 30: 1730-1735, 2007.
20. Johns DG, Ao Z, Eybye M, Olzinski A, Costell M, Gruver S, Smith SA, Douglas SA, Macphee CH. Rosiglitazone protects against ischemia/reperfusion-induced leukocyte adhesion in the zucker diabetic fatty rat. J Pharmacol Exp Ther 315: 1020-1027, 2005.
21. La Bonte LR, Davis-Gorman G, Stahl GL, McDonagh PF. Complement inhibition reduces injury in the type 2 diabetic heart following ischemia and reperfusion. Am J Physiol Heart Circ Physiol 294: H1282-H1290, 2008.
22. La Bonte LR, Dokken B, Davis-Gorman G, Stahl GL, McDonagh PF. The mannose-binding lectin pathway is a significant contributor to reperfusion injury in the type 2 diabetic heart. Diab Vasc Dis Res 6: 172-180, 2009.
23. Leonard BL, Watson RN, Loomes KM, Phillips AR, Cooper GJ. Insulin resistance in the Zucker diabetic fatty rat: a metabolic characterisation of obese and lean phenotypes. Acta Diabetol 42: 162-170, 2005.
24. Lesniewski LA, Donato AJ, Behnke BJ, Woodman CR, Laughlin MH, Ray CA, Delp MD. Decreased NO signaling leads to enhanced vasoconstrictor responsiveness in skeletal muscle arterioles of the ZDF rat prior to overt diabetes and hypertension. Am J Physiol Heart Circ Physiol 294: H1840-H1850, 2008.
25. Lin B, Ginsberg MD, Busto R, Li L. Hyperglycemia triggers massive neutrophil deposition in brain following transient ischemia in rats. Neurosci Lett 278: 1-4, 2000.
26. Mastej K, Adamiec R. Neutrophil surface expression of CD11b and CD62L in diabetic microangiopathy. Acta Diabetol 45: 183-190, 2008.
27. Mathis D, Shoelson SE. Immunometabolism: an emerging frontier. Nat Rev Immunol 11: 81, 2011.
28. Matsuo Y, Kihara T, Ikeda M, Ninomiya M, Onodera H, Kogure K. Role of neutrophils in radical production during ischemia and reperfusion of the rat brain: effect of neutrophil depletion on extracellular ascorbyl radical formation. J Cereb Blood Flow Metab 15: 941-947, 1995.
29. 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 27: 4403-4412, 2007.
30. Moro MA, Cardenas A, Hurtado O, Leza JC, Lizasoain I. Role of nitric oxide after brain ischaemia. Cell Calcium 36: 265-275, 2004.
31. Morrison H, McKee D, Ritter L. Systemic neutrophil activation in a mouse model of ischemic stroke and reperfusion. Biol Res Nurs 13: 154-163, 2010.
32. Oltman CL, Richou LL, Davidson EP, Coppey LJ, Lund DD, Yorek MA. Progression of coronary and mesenteric vascular dysfunction in Zucker obese and Zucker diabetic fatty rats. Am J Physiol Heart Circ Physiol 291: H1780-H1787, 2006.
33. van Poelje PD, Potter SC, Chandramouli VC, Landau BR, Dang Q, Erion MD. Inhibition of fructose 1, 6-bisphosphatase reduces excessive endogenous glucose production and attenuates hyperglycemia in Zucker diabetic fatty rats. Diabetes 55: 1747-1754, 2006.
34. Ritter LS, Orozco JA, Coull BM, McDonagh PF, Rosenblum WI. Leukocyte accumulation and hemodynamic changes in the cerebral microcirculation during early reperfusion after stroke. Stroke 31: 1153-1161, 2000.
35. Ritter LS, Stempel KM, Coull BM, McDonagh PF. Leukocyte-platelet aggregates in rat peripheral blood after ischemic stroke and reperfusion. Biol Res Nurs 6: 281-288, 2005.
36. Ritter LS, Wilson DS, Williams SK, Copeland JG, McDonagh PF. Early in reperfusion following myocardial ischemia, leukocyte activation is necessary for venular adhesion but not capillary retention. Microcirculation 2: 315-327, 1995.
37. Rodrigues SF, Granger DN. Role of blood cells in ischaemia-reperfusion induced endothelial barrier failure. Cardiovasc Res 87: 291-299, 2010.
38. Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM, Carnethon MR, Dai S, de Simone G, Ford ES, Fox CS, Fullerton HJ, Gillespie C, Greenlund KJ, Hailpern SM, Heit JA, Ho PM, Howard VJ, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Makuc DM, Marcus GM, Marelli A, Matchar DB, McDermott MM, Meigs JB, Moy CS, Mozaffarian D, Mussolino ME, Nichol G, Paynter NP, Rosamond WD, Sorlie PD, Stafford RS, Turan TN, Turner MB, Wong ND, Wylie-Rosett J, American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics - 2011 update: a report from the American Heart Association. Circulation 123: e18-e209, 2011.
39. Roger VL. Executive summary: heart disease and stroke statistics - 2011 update: a report from the American Heart Association. Circulation 123: 459-463, 2011.
40. Ruehl ML, Orozco JA, Stoker MB, McDonagh PF, Coull BM, Ritter LS. Protective effects of inhibiting both blood and vascular selectins after stroke and reperfusion. Neurol Res 24: 226-232, 2002.
41. Santizo RA, Xu HL, Ye S, Baughman VL, Pelligrino DA. Loss of benefit from estrogen replacement therapy in diabetic ovariectomized female rats subjected to transient forebrain ischemia. Brain Res 956: 86-95, 2002.
42. Schmid-Schonbein GW. The damaging potential of leukocyte activation in the microcirculation. Angiology 44: 45-56, 1993.
43. Suematsu M, Schmid-Schonbein GW, Chavez-Chavez RH, Yee TT, Tamatani T, Miyasaka M, Delano FA, Zweifach BW. In vivo visualization of oxidative changes in microvessels during neutrophil activation. Am J Physiol 264(3 Pt 2): H881-H891, 1993.
44. Suzaki Y, Ozawa Y, Kobori H. Intrarenal oxidative stress and augmented angiotensinogen are precedent to renal injury in Zucker diabetic fatty rats. Int J Biol Sci 3: 40-46, 2007.
45. Szocs Z, Brunmair B, Stadlbauer K, Nowotny P, Bauer L, Luger A, Furnsinn C. Age-dependent development of metabolic derangement and effects of intervention with pioglitazone in Zucker diabetic fatty rats. J Pharmacol Exp Ther 326: 323-329, 2008.
46. Teixeira de Lemos E, Reis F, Baptista S, Pinto R, Sepodes B, Vala H, Rocha-Pereira P, Correia da Silva G, Teixeira N, Silva AS, Carvalho L, Teixeira F, Das UN. Exercise training decreases proinflammatory profile in Zucker diabetic (type 2) fatty rats. Nutrition 25: 330-339, 2009.
47. Terao S, Yilmaz G, Stokes KY, Ishikawa M, Kawase T, Granger DN. Inflammatory and injury responses to ischemic stroke in obese mice. Stroke 39: 943-950, 2008.
48. Tipton A, Downey K, Frank OC, Migliati E, Wilson J, McDonagh P, Funk J, Ritter L. Neutrophil function in aged versus young rats subjected to global cerebral ischemia and reperfusion. FASEB J 17: A1075-A1076, 2003.
49. Xu HL, Vetri F, Lee HK, Ye S, Paisansathan C, Mao L, Tan F, Pelligrino DA. Estrogen replacement therapy in diabetic ovariectomized female rats potentiates postischemic leukocyte adhesion in cerebral venules via a RAGE-related process. Am J Physiol Heart Circ Physiol 297: H2059-H2067, 2009.
50. Yilmaz G, Arumugam TV, Stokes KY, Granger DN. Role of T lymphocytes and interferon-gamma in ischemic stroke. Circulation 113: 2105-2112, 2006.
51. Zhang RL, Chopp M, Zaloga C, Zhang ZG, Jiang N, Gautam SC, Tang WX, Tsang W, Anderson DC, Manning AM. The temporal profiles of ICAM-1 protein and mRNA expression after transient MCA occlusion in the rat. Brain Res 682: 182-188, 1995.