Treatment of rats with pioglitazone in the reperfusion phase of focal cerebral ischemia: A preclinical stroke trial

Experimental Neurology

Volumn 238, Issue 2, 2012, Pages 243-253

  Culman, Juraj ^a   Nguyen Ngoc, Miriam ^a   Glatz, Torben ^a   Gohlke, Peter ^a   Herdegen, Thomas ^a   Zhao, Yi ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

Focal cerebral ischemia; Neurodegeneration; Neuroprotection; Neuroregeneration; Pioglitazone; Rat; Stroke outcome

Indexed keywords

PIOGLITAZONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BLOOD PRESSURE MEASUREMENT; BRAIN EDEMA; BRAIN INFARCTION; BRAIN ISCHEMIA; CELL INFILTRATION; CELL REGENERATION; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; DISEASE ASSOCIATION; DRUG EFFECT; DRUG EFFICACY; DRUG RESPONSE; ENCEPHALITIS; HEART RATE; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOLECULAR DYNAMICS; MORTALITY; NERVE CELL DEGENERATION; NEUROPROTECTION; NONHUMAN; PRACTICE GUIDELINE; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; SYSTEMIC THERAPY; SYSTOLIC BLOOD PRESSURE;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN INFARCTION; BRAIN ISCHEMIA; CASPASE 9; CEREBRAL CORTEX; CYCLOOXYGENASE 2; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ECTODYSPLASINS; HEART RATE; HYPOGLYCEMIC AGENTS; MALE; NERVOUS SYSTEM DISEASES; POLY(ADP-RIBOSE) POLYMERASES; RATS; RATS, WISTAR; REGIONAL BLOOD FLOW; REPERFUSION INJURY; THIAZOLIDINEDIONES; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84866868516     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.09.003     Document Type: Article

References (48)

1. Adams H.P., del Zoppo G., Alberts M.J., Bhatt D.L., Brass L., Furlan A., Grubb R.L., Higashida R.T., Jauch E.C., Kidwell C., Lyden P.D., Morgenstern L.B., Qureshi A.I., Rosenwasser R.H., Scott P.A., Wijdicks E.F. Guidelines for the early management of adults with ischemic stroke. Stroke 2007, 38:1655-1711.
2. Allahtavakoli M., Moloudi R., Arababadi M.K., Shamsizadeh A., Javanmardi K. Delayed post ischemic treatment with Rosiglitazone attenuates infarct volume, neurological deficits and neutrophilia after embolic stroke in rat. Brain Res. 2009, 1271:121-127.
3. Auriel E., Bornstein N.M. Neuroprotection in acute ischemic stroke-current status. J. Cell. Mol. Med. 2010, 14:2200-2202.
4. Bederson J.B., Pitts L.H., Tsuji M., Nishimura M.C., Davis R.L., Bartkowski H. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 1986, 17:472-476.
5. Boysen G., Christensen H. Early stroke: A dynamic process. Stroke 2001, 32:2423-2425.
6. Brdon J., Kaiser S., Hagemann F., Zhao Y., Culman J., Gohlke P. Comparison between early and delayed systemic treatment with candesartan of rats after ischaemic stroke. J. Hypertens. 2007, 25:187-196.
7. Buchanan T.A., Meehan W.P., Jeng Y.Y., Yang D., Chan T.M., Nadler J.L., Scott S., Rude R.K., Hsueh W.A. Blood pressure lowering by pioglitazone. Evidence for a direct vascular effect. J. Clin. Invest. 1995, 96:354-360.
8. Colca J.R., McDonald W.G., Waldon D.J., Leone J.W., Lull J.M., Bannow C.A., Lund E.T., Mathews W.R. Identification of a novel mitochondrial protein ("mitoNEET") cross-linked specifically by a thiazolidinedione photoprobe. Am. J. Physiol. Endocrinol. Metab. 2004, 286:E252-E260.
9. Collino M., Patel N.S., Thiemermann C. PPARs as new therapeutic targets for the treatment of cerebral ischemia/reperfusion injury. Ther. Adv. Cardiovasc. Dis. 2008, 2:179-197.
10. Culman J., Zhao Y., Gohlke P., Herdegen T. PPAR-gamma: therapeutic target for ischemic stroke. Trends Pharmacol. Sci. 2007, 28:244-249.
11. Dello Russo C., Gavrilyuk V., Weinberg G., Almeida A., Bolanos J.P., Palmer J., Pelligrino D., Galea E., Feinstein D.L. Peroxisome proliferator-activated receptor gamma thiazolidinedione agonists increase glucose metabolism in astrocytes. J. Biol. Chem. 2003, 278:5828-5836.
12. Dirnagl U. Bench to bedside: the quest for quality in experimental stroke research. J. Cereb. Blood Flow Metab. 2006, 26:1465-1478.
13. Dirnagl U., Iadecola C., Moskowitz M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 1999, 22:391-397.
14. Dormandy J.A., Charbonnel B., Eckland D.J., Erdmann E., Massi-Benedetti M., Moules I.K., Skene A.M., Tan M.H., Lefèbvre P.J., Murray G.D., Standl E., Wilcox R.G., Wilhelmsen L., Betteridge J., Birkeland K., Golay A., Heine R.J., Korányi L., Laakso M., Mokán M., Norkus A., Pirags V., Podar T., Scheen A., Scherbaum W., Schernthaner G., Schmitz O., Skrha J., Smith U., Taton J. Secondary prevention of macrovascular events in patients with type 2 diabetes in the PROactive Study (PROspective pioglitAzone Clinical Trial In macroVascular Events): a randomised controlled trial. Lancet 2005, 366:1279-1289.
15. Ehrenreich H., Weissenborn K., Prange H., Schneider D., Weimar C., Wartenberg K., Schellinger P.D., Bohn M., Becker H., Wegrzyn M., Jähnig P., Herrmann M., Knauth M., Bähr M., Heide W., Wagner A., Schwab S., Reichmann H., Schwendemann G., Dengler R., Kastrup A., Bartels C. Recombinant human erythropoietin in the treatment of acute ischemic stroke. Stroke 2009, 40:e647-e656.
16. Fuenzalida K., Quintanilla R., Ramos P., Piderit D., Fuentealba R.A., Martinez G., Inestrosa N.C., Bronfman M. Peroxisome proliferator-activated receptor gamma up-regulates the Bcl-2 anti-apoptotic protein in neurons and induces mitochondrial stabilization and protection against oxidative stress and apoptosis. J. Biol. Chem. 2007, 282:37006-37015.
17. Gamboa J., Blankenship D.A., Niemi J.P., Landreth G.E., Karl M., Hilow E., Sundararajan S. Extension of the neuroprotective time window for thiazolidinediones in ischemic stroke is dependent on time of reperfusion. Neuroscience 2010, 170:846-857.
18. Garcia J.H., Wagner S., Liu K.F., Hu X.J. Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats. Statistical validation. Stroke 1995, 26:627-634. (discussion 635).
19. Ginsberg M.D. Neuroprotection for ischemic stroke: past, present and future. Neuropharmacology 2008, 55:363-389.
20. Gonzales N.R., Shah J., Sangha N., Sosa L., Martinez R., Shen L., Kasam M., Morales M.M., Hossain M.M., Barreto A.D., Savitz S.I., Lopez G., Misra V., Wu T.C., El Khoury R., Sarraj A., Sahota P., Hicks W., Acosta I., Sline M.R., Rahbar M.H., Zhao X., Aronowski J., Grotta J.C. Design of a prospective, dose-escalation study evaluating the Safety of Pioglitazone for Hematoma Resolution in Intracerebral Hemorrhage (SHRINC). Int. J. Stroke 2012, (2012 Feb 20 [Epub ahead of print]). 10.1111/j.1747-4949.2011.00761.x.
21. Guo J., Walss-Bass C., Ludueña R.F. The beta isotypes of tubulin in neuronal differentiation. Cytoskeleton (Hoboken) 2010, 67:431-441.
22. Heneka M.T., Landreth G.E. PPARs in the brain. Biochim. Biophys. Acta 2007, 1771:1031-1045.
23. Hunter A.J., Mackay K.B., Rogers D.C. To what extent have functional studies of ischaemia in animals been useful in the assessment of potential neuroprotective agents?. Trends Pharmacol. Sci. 1998, 19:59-66.
24. Izawa Y., Takahashi S., Suzuki N. Pioglitazone enhances pyruvate and lactate oxidation in cultured neurons but not in cultured astroglia. Brain Res. 2009, 1305:64-73.
25. Ji S., Kronenberg G., Balkaya M., Färber K., Gertz K., Kettenmann H., Endres M. Acute neuroprotection by pioglitazone after mild brain ischemia without effect on long-term outcome. Exp. Neurol. 2009, 216:321-328.
26. Lee J., Reding M. Effects of thiazolidinediones on stroke recovery: a case-matched controlled study. Neurochem. Res. 2007, 32:635-638.
27. Lin T.N., Cheung W.M., Wu J.S., Chen J.J., Lin H., Chen J.J., Liou J.Y., Shyue S.K., Wu K.K. 15d-prostaglandin J2 protects brain from ischemia-reperfusion injury. Arterioscler. Thromb. Vasc. Biol. 2006, 26:481-487.
28. Liu S., Zhen G., Meloni B.P., Campbell K., Winn H.R. Rodent stroke model guidelines for preclinical stroke trials (1st Edition). J. Exp. Stroke Transl. Med. 2009, 2:2-27.
29. Liu F., Schafer D.P., McCullough L.D. TTC, fluoro-Jade B and NeuN staining confirm evolving phases of infarction induced by middle cerebral artery occlusion. J. Neurosci. Methods 2009, 179:1-8.
30. Maeshiba Y., Kiyota Y., Yamashita K., Yoshimura Y., Motohashi M., Tanayama S. Disposition of the new antidiabetic agent pioglitazone in rats, dogs, and monkeys. Arzneimittelforschung 1997, 47:29-35.
31. Mazzeo A.T., Beat A., Singh A., Bullock M.R. The role of mitochondrial transition pore, and its modulation, in traumatic brain injury and delayed neurodegeneration after TBI. Exp. Neurol. 2009, 218:363-370.
32. Ntaios G., Bath P., Michel P. Blood pressure treatment in acute ischemic stroke: a review of studies and recommendations. Curr. Opin. Neurol. 2010, 23:46-52.
33. Paddock M.L., Wiley S.E., Axelrod H.L., Cohen A.E., Roy M., Abresch E.C., Capraro D., Murphy A.N., Nechushtai R., Dixon J.E., Jennings P.A. MitoNEET is a uniquely folded 2Fe 2S outer mitochondrial membrane protein stabilized by pioglitazone. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:14342-14347.
34. Poulain F.E., Sobel A. The microtubule network and neuronal morphogenesis: Dynamic and coordinated orchestration through multiple players. Mol. Cell. Neurosci. 2010, 43:15-32.
35. Ricote M., Glass C.K. PPARs and molecular mechanisms of transrepression. Biochim. Biophys. Acta 2007, 1771:926-935.
36. Rosenberg G.A. Neurological diseases in relation to the blood-brain barrier. J. Cereb. Blood Flow Metab. 2012, (Jan 18 [Epub ahead of print]). 10.1038/jcbfm.2011.197.
37. Sandset E.C., Bath P.M., Boysen G., Jatuzis D., Kõrv J., Lüders S., Murray G.D., Richter P.S., Roine R.O., Terént A., Thijs V., Berge E., SCAST Study Group The angiotensin-receptor blocker candesartan for treatment of acute stroke (SCAST): a randomised, placebo-controlled, double-blind trial. Lancet 2011, 377:741-750.
38. Schiffrin E.L., Amiri F., Benkirane K., Iglarz M., Diep Q.N. Peroxisome proliferator-activated receptors: vascular and cardiac effects in hypertension. Hypertension 2003, 42:664-668.
39. Schmued L.C., Stowers C.C., Scallet A.C., Xu L. Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res. 2005, 1035:24-31.
40. Shimazu T., Inoue I., Araki N., Asano Y., Sawada M., Furuya D., Nagoya H., Greenberg J.H. A peroxisome proliferator-activated receptor-gamma agonist reduces infarct size in transient but not in permanent ischemia. Stroke 2005, 36:353-359.
41. Tureyen K., Kapadia R., Bowen K.K., Satriotomo I., Liang J., Feinstein D.L., Vemuganti R. Peroxisome proliferator-activated receptor-gamma agonists induce neuroprotection following transient focal ischemia in normotensive, normoglycemic as well as hypertensive and type-2 diabetic rodents. J. Neurochem. 2007, 101:41-56.
42. Victor N.A., Wanderi E.W., Gamboa J., Zhao X., Aronowski J., Deininger K., Lust W.D., Landreth G.E., Sundararajan S. Altered PPARgamma expression and activation after transient focal ischemia in rats. Eur. J. Neurosci. 2006, 24:1653-1663.
43. Wang C.X., Ding X., Noor R., Pegg C., He C., Shuaib A. Rosiglitazone alone or in combination with tissue plasminogen activator improves ischemic brain injury in an embolic model in rats. J. Cereb. Blood Flow Metab. 2009, 29:1683-1694.
44. White A.T., Murphy A.N. Administration of thiazolidinediones for neuroprotection in ischemic stroke: a pre-clinical systematic review. J. Neurochem. 2010, 115:845-853.
45. Zhao Y., Patzer A., Herdegen T., Gohlke P., Culman J. Activation of cerebral peroxisome proliferator-activated receptors gamma promotes neuroprotection by attenuation of neuronal cyclooxygenase-2 overexpression after focal cerebral ischemia in rats. FASEB J. 2006, 20:1162-1175.
46. Zhao X., Ou Z., Grotta J.C., Waxham N., Aronowski J. Peroxisome-proliferator-activated receptor-gamma (PPARgamma) activation protects neurons from NMDA excitotoxicity. Brain Res. 2006, 1073-1074:460-469.
47. Zhao X., Sun G., Zhang J., Strong R., Song W., Gonzales N., Grotta J.C., Aronowski J. Hematoma resolution as a target for intracerebral hemorrhage treatment: role for peroxisome proliferator-activated receptor gamma in microglia/macrophages. Ann. Neurol. 2007, 61:352-362.
48. Zuhayra M., Zhao Y., von Forstner C., Henze E., Gohlke P., Culman J., Lützen U. Activation of cerebral peroxisome proliferator-activated receptors γ (PPARγ) reduces neuronal damage in the substantia nigra after transient focal cerebral ischaemia in the rat. Neuropathol. Appl. Neurobiol. 2011, 37:738-752.