Progesterone attenuates hemorrhagic transformation after delayed tPA treatment in an experimental model of stroke in rats: Involvement of the VEGF-MMP pathway

Journal of Cerebral Blood Flow and Metabolism

Volumn 34, Issue 1, 2014, Pages 72-80

  Won, Soonmi ^a   Lee, Jin Hwan ^b   Wali, Bushra ^a   Stein, Donald G ^a   Sayeed, Iqbal ^a  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

hemorrhage; MMP 9; progesterone; stroke; tPA; VEGF

Indexed keywords

CLAUDIN 5; GELATINASE B; OCCLUDIN; PROGESTERONE; TIGHT JUNCTION PROTEIN; TISSUE PLASMINOGEN ACTIVATOR; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; BRAIN CELL; BRAIN HEMORRHAGE; BRAIN ISCHEMIA; CELL HYPOXIA; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT; REOXYGENATION; REPERFUSION INJURY; SPRAGUE DAWLEY RAT; SWELLING;

EID: 84891830754     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2013.163     Document Type: Article

References (40)

1. Hacke W, Kaste M, Bluhmki E, Brozman M, Dávalos A, Guidetti D et al. Throm-bolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 2008; 359: 1317-1329.
2. Donnan GA, Davis SM, Parsons MW, Ma H, Dewey HM, Howells DW. How to make better use of thrombolytic therapy in acute ischemic stroke. Nat Rev Neurol 2011; 7: 400-409.
3. Wang X, Tsuji K, Lee SR, Ning M, Furie KL, Buchan AM et al. Mechanisms of hemorrhagic transformation after tissue plasminogen activator reperfusion therapy for ischemic stroke. Stroke 2004; 35: 2726-2730.
4. Su EJ, Fredriksson L, Geyer M, Folestad E, Cale J, Andrae J et al. Activation of PDGF-CC by tissue plasminogen activator impairs blood-brain barrier integrity during ischemic stroke. Nat Med 2008; 14: 731-737.
5. Sayeed I, Wali B, Stein DG. Progesterone inhibits ischemic brain injury in a rat model of permanent middle cerebral artery occlusion. Restor Neurol Neurosci 2007; 25: 151-159.
6. Ishrat T, Sayeed I, Atif F, Hua F, Stein DG. Progesterone and allopregnanolone attenuate blood-brain barrier dysfunction following permanent focal ischemia by regulating the expression of matrix metalloproteinases. Exp Neurol 2010; 226: 183-190.
7. Ishrat T, Sayeed I, Atif F, Stein DG. Effects of progesterone administration on infarct volume and functional deficits following permanent focal cerebral ischemia in rats. Brain Res 2009; 1257: 94-101.
8. Gibson CL, Murphy SP. Progesterone enhances functional recovery after middle cerebral artery occlusion in male mice. J Cereb Blood Flow Metab 2004; 24: 805-813.
9. Wright DW, Kellermann AL, Hertzberg VS, Clark PL, Frankel M, Goldstein FC et al. ProTECT: a randomized clinical trial of progesterone for acute traumatic brain injury. Ann Emerg Med 2007; 49: e1-e2.
10. Xiao G, Wei J, Yan W, Wang W, Lu Z. Improved outcomes from the administration of progesterone for patients with acute severe traumatic brain injury: a randomized controlled trial. Crit Care 2008; 12: R61.
11. Mun-Bryce S, Rosenberg GA. Matrix metalloproteinases in cerebrovascular disease. J Cereb Blood Flow Metab 1998; 18: 1163-1172.
12. Wang X, Lee SR, Arai K, Lee SR, Tsuji K, Rebeck GW et al. Lipoprotein receptor-mediated induction of matrix metalloproteinase by tissue plasminogen activator. Nat Med 2003; 9: 1313-1317.
13. Mishiro K, Ishiguro M, Suzuki Y, Tsuruma K, Shimazawa M, Hara H. A broad-spectrum matrix metalloproteinase inhibitor prevents hemorrhagic complications induced by tissue plasminogen activator in mice. Neuroscience 2012; 205: 39-48.
14. Castellanos M, Leira R, Serena J, Pumar JM, Lizasoain I, Castillo J et al. Plasma metalloproteinase-9 concentration predicts hemorrhagic transformation in acute ischemic stroke. Stroke 2003; 34: 40-46.
15. Stein DG, Wright DW, Kellermann AL. Does progesterone have neuroprotective properties? Ann Emerg Med 2008; 51: 164-172.
16. Zhu H, Fan X, Yu Z, Liu J, Murata Y, Lu J et al. Annexin A2 combined with low-dose tPA improves thrombolytic therapy in a rat model of focal embolic stroke. J Cereb Blood Flow Metab 2010; 30: 1137-1146.
17. Qin Z, Karabiyikoglu M, Hua Y, Silbergleit R, He Y, Keep RF et al. Hyperbaric oxygen-induced attenuation of hemorrhagic transformation after experimental focal transient cerebral ischemia. Stroke 2007; 38: 1362-1367.
18. Godfrey KR, Tanswell P, Bates RA, Chappell MJ, Madden FN. Nonlinear pharma-cokinetics of tissue-type plasminogen activator in three animal species: a comparison of mathematical models. Biopharm Drug Dispos 1998; 19: 131-140.
19. Li G, Simon MJ, Cancel LM, Shi ZD, Ji X, Tarbell JM et al. Permeability of endothelial and astrocyte cocultures: in vitro blood-brain barrier models for drug delivery studies. Ann Biomed Eng 2010; 38: 2499-2511.
20. Chi OZ, Hunter C, Liu X, Weiss HR. Effects of anti-VEGF antibody on blood-brain barrier disruption in focal cerebral ischemia. Exp Neurol 2007; 204: 283-287.
21. Zhang ZG, Zhang L, Tsang W, Soltanian-Zadeh H, Morris D, Zhang R et al. Correlation of VEGF and angiopoietin expression with disruption of blood-brain barrier and angiogenesis after focal cerebral ischemia. J Cereb Blood Flow Metab 2002; 22: 379-392.
22. Kanazawa M, Igarashi H, Kawamura K, Takahashi T, Kakita A, Takahashi H et al. Inhibition of VEGF signaling pathway attenuates hemorrhage after tPA treatment. J Cereb Blood Flow Metab 2011; 31: 1461-1474.
23. Liu W, Hendren J, Qin XJ, Liu KJ. Normobaric hyperoxia reduces the neurovascular complications associated with delayed tissue plasminogen activator treatment in a rat model of focal cerebral ischemia. Stroke 2009; 40: 2526-2531.
24. Latour LL, Kang DW, Ezzeddine MA, Chalela JA, Warach S. Early blood-brain barrier disruption in human focal brain ischemia. Ann Neurol 2004; 56: 468-477.
25. Aihara N, Tanno H, Hall JJ, Pitts LH, Noble LJ. Immunocytochemical localization of immunoglobulins in the rat brain: relationship to the blood-brain barrier. J Comp Neurol 1994; 342: 481-496.
26. Ballabh P, Braun A, Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis 2004; 16: 1-13.
27. Gaillard PJ, Voorwinden LH, Nielsen JL, Ivanov A, Atsumi R, Engman H et al. Establishment and functional characterization of an in vitro model of the blood-brain barrier, comprising a co-culture of brain capillary endothelial cells and astrocytes. Eur J Pharm Sci 2001; 12: 215-222.
28. Hawkins BT, Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 2005; 57: 173-185.
29. Yang Y, Estrada EY, Thompson JF, Liu W, Rosenberg GA. Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J Cereb Blood Flow Metab 2007; 27: 697-709.
30. Jickling GC, Manolescu BN. Breaking down barriers to identify hemorrhagic transformation in ischemic stroke. Neurology 2012; 79: 1632-1633.
31. Ishiguro M, Mishiro K, Fujiwara Y, Chen H, Izuta H, Tsuruma K et al. Phospho-diesterase-III inhibitor prevents hemorrhagic transformation induced by focal cerebral ischemia in mice treated with tPA. PLoS One 2010; 5: e15178.
32. Casas E, Barron C, Francis SA, McCormack JM, McCarthy KM, Schneeberger EE et al. Cholesterol efflux stimulates metalloproteinase-mediated cleavage of occludin and release of extracellular membrane particles containing its C-terminal fragments. Exp Cell Res 2010; 316: 353-365.
33. Wachtel M, Frei K, Ehler E, Fontana A, Winterhalter K, Gloor SM. Occludin proteolysis and increased permeability in endothelial cells through tyrosine phosphatase inhibition. J Cell Sci 1999; 112: 4347-4356.
34. Boardman KC, Aryal AM, Miller WM, Waters CM. Actin re-distribution in response to hydrogen peroxide in airway epithelial cells. J Cell Physiol 2004; 199: 57-66.
35. Madara JL, Barenberg D, Carlson S. Effects of cytochalasin D on occluding junctions of intestinal absorptive cells: further evidence that the cytoskeleton may influence paracellular permeability and junctional charge selectivity. J Cell Biol 1986; 102: 2125-2136.
36. Yan F, Hu Q, Chen J, Wu C, Gu C, Chen G. Progesterone attenuates early brain injury after subarachnoid hemorrhage in rats. Neurosci Lett 2013; 543: 163-167.
37. van Bruggen N, Thibodeaux H, Palmer JT, Lee WP, Fu L, Cairns B et al. VEGF antagonism reduces edema formation and tissue damage after ischemia/reper-fusion injury in the mouse brain. J Clin Invest 1999; 104: 1613-1620.
38. Hayashi T, Abe K, Suzuki H, Itoyama Y. Rapid induction of vascular endothelial growth factor gene expression after transient middle cerebral artery occlusion in rats. Stroke 1997; 28: 2039-2044.
39. Chi OZ, Hunter C, Liu X, Weiss HR. Effects of VEGF and nitric oxide synthase inhibition on blood-brain barrier disruption in the ischemic and non-ischemic cerebral cortex. Neurol Res 2005; 27: 864-868.
40. Ishrat T, Sayeed I, Atif F, Hua F, Stein DG. Progesterone is neuroprotective against ischemic brain injury through its effects on the phosphoinositide 3-kinase/protein kinase B signaling pathway. Neuroscience 2012; 210: 442-450.