Comparative analysis of the neurovascular injury and functional outcomes in experimental stroke models in diabetic Goto-Kakizaki rats

Brain Research

Volumn 1541, Issue , 2013, Pages 106-114

  Li, Weiguo ^a,b   Qu, Zhi ^b   Prakash, Roshini ^c   Chung, Connie ^b   Ma, Handong ^a,b   Hoda, Md Nasrul ^b   Fagan, Susan C ^a,c   Ergul, Adviye ^a,b,c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

Diabetes; Edema; Hemorrhagic transformation; Infarct; Ischemic stroke; Middle cerebral artery occlusion

Indexed keywords

INSULIN; METFORMIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BLOOD VESSEL INJURY; BRAIN BLOOD FLOW; BRAIN HEMORRHAGE; BRAIN INFARCTION SIZE; CEREBROVASCULAR ACCIDENT; COMPARATIVE STUDY; CONTROLLED STUDY; DIABETES MELLITUS; DRUG EFFECT; EDEMA; FUNCTIONAL STATUS; GLYCEMIC CONTROL; GOTO KAKIZAKI RAT; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; WISTAR RAT;

RATTUS;

2,3,5-TRIPHENYLTETRAZOLIUM CHLORIDE; ADENOSINE MONOPHOSPHATE; AMP; AMP-ACTIVATED PROTEIN KINASE; AMPK; ANALYSIS OF VARIANCE; ANOVA; BBB; BLOOD-BRAIN BARRIER; DIABETES; ECA; EDEMA; EXTERNAL CAROTID ARTERY; GK; GOTO-KAKIZAKI; HEMORRHAGIC TRANSFORMATION; HT; I/R; INFARCT; ISCHEMIA/REPERFUSION; ISCHEMIC STROKE; MCAO; MET; METFORMIN; MIDDLE CEREBRAL ARTERY OCCLUSION; NBG; NORMAL BLOOD GLUCOSE; PE; POLYETHYLENE; SEM; STAIR; STANDARD ERROR OF THE MEAN; STROKE THERAPY ACADEMIA INDUSTRY ROUNDTABLE COMMITTEE; TISSUE PLASMINOGEN ACTIVATOR; TPA; TTC;

ANIMALS; BRAIN EDEMA; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; INTRACRANIAL HEMORRHAGES; MALE; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; REPERFUSION INJURY; STROKE;

EID: 84888015715     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.10.021     Document Type: Article

References (48)

1. T.A. Baird, M.W. Parsons, T. Phanh, K.S. Butcher, P.M. Desmond, B.M. Tress, P.G. Colman, B.R. Chambers, and S.M. Davis Persistent poststroke hyperglycemia is independently associated with infarct expansion and worse clinical outcome Stroke 34 2003 2208 2214
2. A. Bruno, D. Gregori, A. Caropreso, F. Lazzarato, M. Petrinco, and E. Pagano Normal glucose values are associated with a lower risk of mortality in hospitalized patients Diabetes Care 31 2008 2209 2210
3. H.F. Elewa, A. Kozak, A.B. El-Remessy, R.F. Frye, M.H. Johnson, A. Ergul, and S.C. Fagan Early atorvastatin reduces hemorrhage after acute cerebral ischemia in diabetic rats J. Pharmacol. Exp. Ther. 330 2009 532 540
4. M.M. Elgebaly, R. Prakash, W. Li, S. Ogbi, M.H. Johnson, E.M. Mezzetti, S.C. Fagan, and A. Ergul Vascular protection in diabetic stroke: role of matrix metalloprotease-dependent vascular remodeling J. Cereb. Blood Flow Metab 30 2010 1928 1938
5. M.M. Elgebaly, S. Ogbi, W. Li, E.M. Mezzetti, R. Prakash, M.H. Johnson, A. Bruno, S.C. Fagan, and A. Ergul Neurovascular injury in acute hyperglycemia and diabetes: a comparative analysis in experimental stroke Transl. Stroke Res 2 2011 391 398
6. S.R. Ennis, and R.F. Keep Effect of sustained-mild and transient-severe hyperglycemia on ischemia-induced blood-brain barrier opening J. Cereb. Blood Flow Metab 27 2007 1573 1582
7. A. Ergul, M.M. Elgebaly, M.L. Middlemore, W. Li, H. Elewa, J.A. Switzer, C. Hall, A. Kozak, and S.C. Fagan Increased hemorrhagic transformation and altered infarct size and localization after experimental stroke in a rat model type 2 diabetes BMC Neurol 7 2007 33
8. A. Ergul, A. Kelly-Cobbs, M. Abdalla, and S.C. Fagan Cerebrovascular complications of diabetes: focus on stroke Endocr. Metab. Immune Disord. Drug Targets 12 2012 148 158
9. S.C. Fagan, and J.H. Garcia Hemorrhagic transformation in focal cerebral ischemia: influence of time to artery reopening and tissue plasminogen activator Pharmacotherapy 19 1999 139 142
10. X. Fan, J. Qiu, Z. Yu, H. Dai, A.B. Singhal, E.H. Lo, and X. Wang A rat model of studying tissue-type plasminogen activator thrombolysis in ischemic stroke with diabetes Stroke 43 2012 567 570
11. X. Fan, M. Ning, E.H. Lo, and X. Wang Early insulin glycemic control combined with tPA thrombolysis reduces acute brain tissue damages in a focal embolic stroke model of diabetic rats Stroke 44 2013 255 259
12. R.V. Farese, M.L. Standaert, K. Yamada, L.C. Huang, C. Zhang, D.R. Cooper, Z. Wang, Y. Yang, S. Suzuki, and T. Toyota Insulin-induced activation of glycerol-3-phosphate acyltransferase by a chiro-inositol-containing insulin mediator is defective in adipocytes of insulin-resistant, type II diabetic, Goto-Kakizaki rats Proc. Nat. Acad. Sci. U.S.A. 91 1994 11040 11044
13. D.M. Feeney, A. Gonzalez, and W.A. Law Amphetamine, haloperidol, and experience interact to affect rate of recovery after motor cortex injury Science 217 1982 855 857
14. M. Fisher, G. Feuerstein, D.W. Howells, P.D. Hurn, T.A. Kent, S.I. Savitz, and E.H. Lo Update of the stroke therapy academic industry roundtable preclinical recommendations Stroke 40 2009 2244 2250
15. A.R. Folsom, M.L. Rasmussen, L.E. Chambless, G. Howard, L.S. Cooper, M.I. Schmidt, and G. Heiss Prospective associations of fasting insulin, body fat distribution, and diabetes with risk of ischemic stroke. The Atherosclerosis Risk in Communities (ARIC) study investigators Diabetes Care 22 1999 1077 1083
16. R.F. Gillum New considerations in analyzing stroke and heart disease mortality trends: the year 2000 age standard and the international statistical classification of diseases and related health problems, 10th revision Stroke 33 2002 1717 1721
17. L.B. Goldstein, R. Adams, M.J. Alberts, L.J. Appel, L.M. Brass, C.D. Bushnell, A. Culebras, T.J. DeGraba, P.B. Gorelick, J.R. Guyton, R.G. Hart, G. Howard, M. Kelly-Hayes, J.V. Nixon, and R.L. Sacco Primary prevention of ischemic stroke: a guideline from the American Heart Association/American Stroke Association Stroke Council: cosponsored by the Atherosclerotic Peripheral Vascular Disease Interdisciplinary Working Group; Cardiovascular Nursing Council; Clinical Cardiology Council; Nutrition, Physical Activity, and Metabolism Council; and the Quality of Care and Outcomes Research Interdisciplinary Working Group Circulation 113 2006 e873 e923
18. Y. Goto, M. Kakizaki, and N. Masaki Production of spontaneous diabetic rats by repetition of selective breeding Tohoku J. Exp. Med. 119 1976 85 90
19. Y. Goto, K. Suzuki, T. Ono, M. Sasaki, and T. Toyota Development of diabetes in the non-obese NIDDM rat (GK rat) Adv. Exp. Med. Biol. 246 1988 29 31
20. A.K. Harris, J.R. Hutchinson, K. Sachidanandam, M.H. Johnson, A.M. Dorrance, D.W. Stepp, S.C. Fagan, and A. Ergul Type 2 diabetes causes remodeling of cerebrovasculature via differential regulation of matrix metalloproteinases and collagen synthesis: role of endothelin-1 Diabetes 54 2005 2638 2644
21. M.N. Hoda, W. Li, A. Ahmad, S. Ogbi, M.A. Zemskova, M.H. Johnson, A. Ergul, W.D. Hill, D.C. Hess, and I.Y. Sazonova Sex-independent neuroprotection with minocycline after experimental thromboembolic stroke Exp. Transl. Stroke Med 3 2011 16
22. K.C. Johnston, C.E. Hall, B.M. Kissela, T.P. Bleck, and M.R. Conaway Glucose Regulation in Acute Stroke Patients (GRASP) trial: a randomized pilot trial Stroke 40 2009 3804 3809
23. H. Kamada, F. Yu, C. Nito, and P.H. Chan Influence of hyperglycemia on oxidative stress and matrix metalloproteinase-9 activation after focal cerebral ischemia/reperfusion in rats: relation to blood-brain barrier dysfunction Stroke 38 2007 1044 1049
24. A.I. Kelly-Cobbs, R. Prakash, M. Coucha, R.A. Knight, W. Li, S.N. Ogbi, M. Johnson, and A. Ergul Cerebral myogenic reactivity and blood flow in type 2 diabetic rats: role of peroxynitrite in hypoxia-mediated loss of myogenic tone J. Pharmacol. Exp. Ther. 342 2012 407 415
25. A.I. Kelly-Cobbs, R. Prakash, W. Li, B. Pillai, S. Hafez, M. Coucha, M.H. Johnson, S.N. Ogbi, S.C. Fagan, and A. Ergul Targets of vascular protection in acute ischemic stroke differ in type 2 diabetes Am. J. Physiol. Heart Circ. Physiol 304 2013 H806 H815
26. M. Knoflach, B. Matosevic, M. Rucker, M. Furtner, A. Mair, G. Wille, A. Zangerle, P. Werner, J. Ferrari, C. Schmidauer, L. Seyfang, S. Kiechl, and J. Willeit Functional recovery after ischemic stroke - a matter of age: data from the Austrian Stroke Unit Registry Neurology 78 2012 279 285
27. J.D. Kravetz, and D.G. Federman Implications of new diabetes treatment trials: should current clinical practice be altered? Postgrad. Med 121 2009 67 72
28. P.A. Lapchak Hemorrhagic transformation following ischemic stroke: significance, causes, and relationship to therapy and treatment Curr. Neurol. Neurosci. Rep. 2 2002 38 43
29. J. Li, S.E. Benashski, V.R. Venna, and L.D. McCullough Effects of metformin in experimental stroke Stroke 41 2010 2645 2652
30. D. Lloyd-Jones, R. Adams, M. Carnethon, G. De Simone, T.B. Ferguson, K. Flegal, E. Ford, K. Furie, A. Go, K. Greenlund, N. Haase, S. Hailpern, M. Ho, V. Howard, B. Kissela, S. Kittner, D. Lackland, L. Lisabeth, A. Marelli, M. McDermott, J. Meigs, D. Mozaffarian, G. Nichol, C. O'Donnell, V. Roger, W. Rosamond, R. Sacco, P. Sorlie, R. Stafford, J. Steinberger, T. Thom, S. Wasserthiel-Smoller, N. Wong, J. Wylie-Rosett, and Y. Hong Heart disease and stroke statistics - 2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee Circulation 119 2009 480 486
31. P.D. Lyden, and J.A. Zivin Hemorrhagic transformation after cerebral ischemia: mechanisms and incidence Cerebrovasc. Brain Metab. Rev. 5 1993 1 16
32. S.R. Martini, and T.A. Kent Hyperglycemia in acute ischemic stroke: a vascular perspective J. Cereb. Blood Flow Metab 27 2007 435 451
33. N. Musi, M.F. Hirshman, J. Nygren, M. Svanfeldt, P. Bavenholm, O. Rooyackers, G. Zhou, J.M. Williamson, O. Ljunqvist, S. Efendic, D.E. Moller, A. Thorell, and L.J. Goodyear Metformin increases AMP-activated protein kinase activity in skeletal muscle of subjects with type 2 diabetes Diabetes 51 2002 2074 2081
34. R. Ning, M. Chopp, T. Yan, A. Zacharek, C. Zhang, C. Roberts, X. Cui, M. Lu, and J. Chen Tissue plasminogen activator treatment of stroke in type-1 diabetes rats Neuroscience 222 2012 326 332
35. A.Y. Poppe, S.R. Majumdar, T. Jeerakathil, W. Ghali, A.M. Buchan, and M.D. Hill Admission hyperglycemia predicts a worse outcome in stroke patients treated with intravenous thrombolysis Diabetes Care 32 2009 617 622
36. R. Prakash, M. Johnson, S.C. Fagan, and A. Ergul Cerebral neovascularization and remodeling patterns in two different models of type 2 diabetes PLoS One 8 2013 e56264
37. R. Prakash, W. Li, Z. Qu, M.A. Johnson, S.C. Fagan, and A. Ergul Vascularization pattern after ischemic stroke is different in control versus diabetic rats: relevance to stroke recovery Stroke 2013
38. Z. Qin, M. Karabiyikoglu, Y. Hua, R. Silbergleit, Y. He, R.F. Keep, and G. Xi Hyperbaric oxygen-induced attenuation of hemorrhagic transformation after experimental focal transient cerebral ischemia Stroke 38 2007 1362 1367
39. N.N. Rizk, J.A. Rafols, and J.C. Dunbar Cerebral ischemia-induced apoptosis and necrosis in normal and diabetic rats: effects of insulin and C-peptide Brain Res. 1096 2006 204 212
40. E. Siemkowicz, A.J. Hansen, and A. Gjedde Hyperglycemic ischemia of rat brain: the effect of post-ischemic insulin on metabolic rate Brain Res. 243 1982 386 390
41. M.L. Standaert, M.P. Sajan, A. Miura, Y. Kanoh, H.C. Chen, R.V. Farese Jr., and R.V. Farese Insulin-induced activation of atypical protein kinase C, but not protein kinase B, is maintained in diabetic (ob/ob and Goto-Kakazaki) liver. Contrasting insulin signaling patterns in liver versus muscle define phenotypes of type 2 diabetic and high fat-induced insulin-resistant states J. Biol. Chem 279 2004 24929 24934
42. B. Stegmayr, and K. Asplund Diabetes as a risk factor for stroke. A population perspective Diabetologia 38 1995 1061 1068
43. A.V. Terry Jr., D.A. Gearhart, S. Warner, E.J. Hohnadel, M.L. Middlemore, G. Zhang, M.G. Bartlett, and S.P. Mahadik Protracted effects of chronic oral haloperidol and risperidone on nerve growth factor, cholinergic neurons, and spatial reference learning in rats Neuroscience 150 2007 413 424
44. F.M. Turnbull, C. Abraira, R.J. Anderson, R.P. Byington, J.P. Chalmers, W.C. Duckworth, G.W. Evans, H.C. Gerstein, R.R. Holman, T.E. Moritz, B.C. Neal, T. Ninomiya, A.A. Patel, S.K. Paul, F. Travert, and M. Woodward Intensive glucose control and macrovascular outcomes in type 2 diabetes Diabetologia 52 2009 2288 2298
45. D.S. Warner, T.X. Gionet, M.M. Todd, and A.M. McAllister Insulin-induced normoglycemia improves ischemic outcome in hyperglycemic rats Stroke 23 1992 1775 1780 (discussion 1781)
46. C.T. Wass, and W.L. Lanier Glucose modulation of ischemic brain injury: review and clinical recommendations Mayo Clin. Proc. 71 1996 801 812
47. I.A. Weiss, G. Valiquette, and M.D. Schwarcz Impact of glycemic treatment choices on cardiovascular complications in type 2 diabetes Cardiol. Rev. 17 2009 165 175
48. R.L. Zhang, M. Chopp, Z.G. Zhang, Q. Jiang, and J.R. Ewing A rat model of focal embolic cerebral ischemia Brain Res. 766 1997 83 92