Progesterone and allopregnanolone attenuate blood-brain barrier dysfunction following permanent focal ischemia by regulating the expression of matrix metalloproteinases

Experimental Neurology

Volumn 226, Issue 1, 2010, Pages 183-190

  Ishrat, Tauheed ^a   Sayeed, Iqbal ^a   Atif, Fahim ^a   Hua, Fang ^a   Stein, Donald G ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Allopregnanolone; Blood brain barrier; Cytokines; Inflammatory response; Ischemia; Metalloproteinases; Permanent middle cerebral artery occlusion; Progesterone; Tight junction proteins; Tumor necrosis factor alpha

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; CLAUDIN 5; GELATIN; GELATINASE A; GELATINASE B; INTERLEUKIN 6; MATRIX METALLOPROTEINASE; OCCLUDIN; OCCLUDIN 1; P 0130; PROGESTERONE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CLDN5 PROTEIN, RAT; ELTANOLONE; MEMBRANE PROTEIN; OCLN PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN INFARCTION SIZE; BRAIN INJURY; BRAIN ISCHEMIA; CONTROLLED STUDY; DRUG MECHANISM; ELECTROCOAGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING; ZYMOGRAPHY; ANIMAL; BIOSYNTHESIS; BRAIN EDEMA; CEREBRAL ARTERY DISEASE; DRUG EFFECTS; ENZYMOLOGY; LIGATION; MIDDLE CEREBRAL ARTERY; PATHOLOGY; PERMEABILITY; SPRAGUE DAWLEY RAT; STROKE;

ANIMALS; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; BRAIN EDEMA; BRAIN ISCHEMIA; IMMUNOHISTOCHEMISTRY; INFARCTION, MIDDLE CEREBRAL ARTERY; INTERLEUKIN-6; LIGATION; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES; MEMBRANE PROTEINS; MIDDLE CEREBRAL ARTERY; PERMEABILITY; PREGNANOLONE; PROGESTERONE; RATS; RATS, SPRAGUE-DAWLEY; STROKE; TUMOR NECROSIS FACTOR-ALPHA; CLAUDIN-5; OCCLUDIN;

EID: 77957780905     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.08.023     Document Type: Article

References (69)

1. Argaw A.T., Gurfein B.T., Zhang Y., Zameer A., John G.R. VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc. Natl Acad. Sci. USA 2009, 106:1977-1982.
2. Asahi M., Wang X., Mori T., Sumii T., Jung J.C., Moskowitz M.A., Fini M.E., Lo E.H. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J. Neurosci. 2001, 21:7724-7732.
3. Ballabh P., Braun A., Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol. Dis. 2004, 16:1-13.
4. Betz A.L., Coester H.C. Effect of steroid therapy on ischaemic brain oedema and blood to brain sodium transport. Acta Neurochir Suppl. (Wien) 1990, 51:256-258.
5. Brinton R.D., Wang J.M. Therapeutic potential of neurogenesis for prevention and recovery from Alzheimer's disease: allopregnanolone as a proof of concept neurogenic agent. Curr. Alzheimer Res. 2006, 3:185-190.
6. Chen J., Chopp M., Li Y. Neuroprotective effects of progesterone after transient middle cerebral artery occlusion in rat. J. Neurol. Sci. 1999, 171:24-30.
7. Cinelli P., Madani R., Tsuzuki N., Vallet P., Arras M., Zhao C.N., Osterwalder T., Rulicke T., Sonderegger P. Neuroserpin, a neuroprotective factor in focal ischemic stroke. Mol. Cell. Neurosci. 2001, 18:443-457.
8. Corpechot C., Young J., Calvel M., Wehrey C., Veltz J.N., Touyer G., Mouren M., Prasad V.V., Banner C., Sjovall J., et al. Neurosteroids: 3 alpha-hydroxy-5 alpha-pregnan-20-one and its precursors in the brain, plasma, and steroidogenic glands of male and female rats. Endocrinology 1993, 133:1003-1009.
9. de Vries H.E., Blom-Roosemalen M.C., van Oosten M., de Boer A.G., van Berkel T.J., Breimer D.D., Kuiper J. The influence of cytokines on the integrity of the blood-brain barrier in vitro. J. Neuroimmunol. 1996, 64:37-43.
10. Dirnagl U., Iadecola C., Moskowitz M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 1999, 22:391-397.
11. Djebaili M., Guo Q., Pettus E.H., Hoffman S.W., Stein D.G. The neurosteroids progesterone and allopregnanolone reduce cell death, gliosis, and functional deficits after traumatic brain injury in rats. J. Neurotrauma 2005, 22:106-118.
12. Frydenlund D.S., Bhardwaj A., Otsuka T., Mylonakou M.N., Yasumura T., Davidson K.G., Zeynalov E., Skare O., Laake P., Haug F.M., Rash J.E., Agre P., Ottersen O.P., Amiry-Moghaddam M. Temporary loss of perivascular aquaporin-4 in neocortex after transient middle cerebral artery occlusion in mice. Proc. Natl Acad. Sci. USA 2006, 103:13532-13536.
13. Gibson C.L., Murphy S.P. Progesterone enhances functional recovery after middle cerebral artery occlusion in male mice. J. Cereb. Blood Flow Metab. 2004, 24:805-813.
14. Gibson C.L., Coomber B., Rathbone J. Is progesterone a candidate neuroprotective factor for treatment following ischemic stroke?. Neuroscientist 2009, 15:324-332.
15. Gidday J.M., Gasche Y.G., Copin J.C., Shah A.R., Perez R.S., Shapiro S.D., Chan P.H., Park T.S. Leukocyte-derived matrix metalloproteinase-9 mediates blood-brain barrier breakdown and is proinflammatory after transient focal cerebral ischemia. Am. J. Physiol. Heart Circ. Physiol. 2005, 289:H558-H568.
16. Gotoh O., Asano T., Koide T., Takakura K. Ischemic brain edema following occlusion of the middle cerebral artery in the rat: I. The time courses of the brain water, sodium and potassium contents and blood-brain barrier permeability to 125I-albumin. Stroke 1985, 16:101-109.
17. Griffin L.D., Gong W., Verot L., Mellon S.H. Niemann-Pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone. Nat. Med. 2004, 10:704-711.
18. Guo Q., Sayeed I., Baronne L.M., Hoffman S.W., Guennoun R., Stein D.G. Progesterone administration modulates AQP4 expression and edema after traumatic brain injury in male rats. Exp. Neurol. 2006, 198:469-478.
19. Hatashita S., Hoff J.T. Role of blood-brain barrier permeability in focal ischemic brain edema. Adv. Neurol. 1990, 52:327-333.
20. Hornig C.R., Busse O., Buettner T., Dorndorf W., Agnoli A., Akengin Z. CT contrast enhancement on brain scans and blood-CSF barrier disturbances in cerebral ischemic infarction. Stroke 1985, 16:268-273.
21. Hua F., Wang J., Sayeed I., Ishrat T., Atif F., Stein D.G. The TRIF-dependent signaling pathway is not required for acute cerebral ischemia/reperfusion injury in mice. Biochem. Biophys. Res. Commun. 2009, 390:678-683.
22. Ishrat T., Sayeed I., Atif F., Stein D.G. Effects of progesterone administration on infarct volume and functional deficits following permanent focal cerebral ischemia in rats. Brain Res. 2009, 1257:94-101.
23. Jiang N., Chopp M., Stein D., Feit H. Progesterone is neuroprotective after transient middle cerebral artery occlusion in male rats. Brain Res. 1996, 735:101-107.
24. Jiang C., Wang J., Li X., Liu C., Chen N., Hao Y. Progesterone exerts neuroprotective effects by inhibiting inflammatory response after stroke. Inflamm. Res. 2009, 58:619-624.
25. Kebir H., Kreymborg K., Ifergan I., Dodelet-Devillers A., Cayrol R., Bernard M., Giuliani F., Arbour N., Becher B., Prat A. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat. Med. 2007, 13:1173-1175.
26. Koistinaho M., Malm T.M., Kettunen M.I., Goldsteins G., Starckx S., Kauppinen R.A., Opdenakker G., Koistinaho J. Minocycline protects against permanent cerebral ischemia in wild type but not in matrix metalloprotease-9-deficient mice. J. Cereb. Blood Flow Metab. 2005, 25:460-467.
27. Kumon Y., Kim S.C., Tompkins P., Stevens A., Sakaki S., Loftus C.M. Neuroprotective effect of postischemic administration of progesterone in spontaneously hypertensive rats with focal cerebral ischemia. J. Neurosurg. 2000, 92:848-852.
28. Lapchak P.A., Chapman D.F., Zivin J.A. Metalloproteinase inhibition reduces thrombolytic (tissue plasminogen activator)-induced hemorrhage after thromboembolic stroke. Stroke 2000, 31:3034-3040.
29. Lee S.R., Guo S.Z., Scannevin R.H., Magliaro B.C., Rhodes K.J., Wang X., Lo E.H. Induction of matrix metalloproteinase, cytokines and chemokines in rat cortical astrocytes exposed to plasminogen activators. Neurosci. Lett. 2007, 417:1-5.
30. Machado L.S., Kozak A., Ergul A., Hess D.C., Borlongan C.V., Fagan S.C. Delayed minocycline inhibits ischemia-activated matrix metalloproteinases 2 and 9 after experimental stroke. BMC Neurosci. 2006, 7:56.
31. Mahesh V.B., Brann D.W., Hendry L.B. Diverse modes of action of progesterone and its metabolites. J. Steroid Biochem. Mol. Biol. 1996, 56:209-219.
32. McColl B.W., Allan S.M., Rothwell N.J. Systemic inflammation and stroke: aetiology, pathology and targets for therapy. Biochem. Soc. Trans. 2007, 35:1163-1165.
33. McColl B.W., Rothwell N.J., Allan S.M. 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.
34. McColl B.W., Rothwell N.J., Allan S.M. Systemic inflammation alters the kinetics of cerebrovascular tight junction disruption after experimental stroke in mice. J. Neurosci. 2008, 28:9451-9462.
35. McColl B.W., Allan S.M., Rothwell N.J. Systemic infection, inflammation and acute ischemic stroke. Neuroscience 2009, 158:1049-1061.
36. Meistrell M.E., Botchkina G.I., Wang H., Di Santo E., Cockroft K.M., Bloom O., Vishnubhakat J.M., Ghezzi P., Tracey K.J. Tumor necrosis factor is a brain damaging cytokine in cerebral ischemia. Shock 1997, 8:341-348.
37. Miranda E., Lomas D.A. Neuroserpin: a serpin to think about. Cell. Mol. Life Sci. 2006, 63:709-722.
38. Monnet F.P., Mahe V., Robel P., Baulieu E.E. Neurosteroids, via sigma receptors, modulate the [3H]norepinephrine release evoked by N-methyl-D-aspartate in the rat hippocampus. Proc. Natl Acad. Sci. USA 1995, 92:3774-3778.
39. Montaner J., Molina C.A., Monasterio J., Abilleira S., Arenillas J.F., Ribo M., Quintana M., Alvarez-Sabin J. Matrix metalloproteinase-9 pretreatment level predicts intracranial hemorrhagic complications after thrombolysis in human stroke. Circulation 2003, 107:598-603.
40. Nilupul Perera M., Ma H.K., Arakawa S., Howells D.W., Markus R., Rowe C.C., Donnan G.A. Inflammation following stroke. J. Clin. Neurosci. 2006, 13:1-8.
41. O'Connor C.A., Cernak I., Vink R. Both estrogen and progesterone attenuate edema formation following diffuse traumatic brain injury in rats. Brain Res. 2005, 1062:171-174.
42. Rosenberg G.A., Mun-Bryce S. Matrix metalloproteinases in neuroinflammation and cerebral ischemia. Ernst Schering Res. Found. Workshop 2004, 1-16.
43. Rosenberg G.A., Yang Y. Vasogenic edema due to tight junction disruption by matrix metalloproteinases in cerebral ischemia. Neurosurg. Focus 2007, 22:E4.
44. Rosenberg G.A., Estrada E.Y., Dencoff J.E. Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 1998, 29:2189-2195.
45. Rupprecht R., Reul J.M., Trapp T., van Steensel B., Wetzel C., Damm K., Zieglgansberger W., Holsboer F. Progesterone receptor-mediated effects of neuroactive steroids. Neuron 1993, 11:523-530.
46. Sayeed I., Stein D.G. Progesterone as a neuroprotective factor in traumatic and ischemic brain injury. Prog. Brain Res. 2009, 175:219-237.
47. Sayeed I., Guo Q., Hoffman S.W., Stein D.G. Allopregnanolone, a progesterone metabolite, is more effective than progesterone in reducing cortical infarct volume after transient middle cerebral artery occlusion. Ann. Emerg. Med. 2006, 47:381-389.
48. Sayeed I., Wali B., Stein D.G. Progesterone inhibits ischemic brain injury in a rat model of permanent middle cerebral artery occlusion. Restor. Neurol. Neurosci. 2007, 25:151-159.
49. Sayeed I., Parvez S., Wali B., Siemen D., Stein D.G. Direct inhibition of the mitochondrial permeability transition pore: a possible mechanism for better neuroprotective effects of allopregnanolone over progesterone. Brain Res. 2009, 1263:165-173.
50. Schumacher M., Weill-Engerer S., Liere P., Robert F., Franklin R.J., Garcia-Segura L.M., Lambert J.J., Mayo W., Melcangi R.C., Parducz A., Suter U., Carelli C., Baulieu E.E., Akwa Y. Steroid hormones and neurosteroids in normal and pathological aging of the nervous system. Prog. Neurobiol. 2003, 71:3-29.
51. Stein D.G. Progesterone exerts neuroprotective effects after brain injury. Brain Res. Rev. 2008, 57:386-397.
52. Stein D.G., Wright, D.W., 2010. Progesterone in the clinical treatment of acute traumatic brain injury. Expert Opin Investig Drugs 19, 847-857.
53. Suidan G.L., McDole J.R., Chen Y., Pirko I., Johnson A.J. Induction of blood brain barrier tight junction protein alterations by CD8 T cells. PLoS ONE 2008, 3:e3037.
54. Sumii T., Lo E.H. Involvement of matrix metalloproteinase in thrombolysis-associated hemorrhagic transformation after embolic focal ischemia in rats. Stroke 2002, 33:831-836.
55. Svedin P., Hagberg H., Savman K., Zhu C., Mallard C. Matrix metalloproteinase-9 gene knock-out protects the immature brain after cerebral hypoxia-ischemia. J. Neurosci. 2007, 27:1511-1518.
56. VanLandingham J.W., Cekic M., Cutler S., Hoffman S.W., Stein D.G. Neurosteroids reduce inflammation after TBI through CD55 induction. Neurosci. Lett. 2007, 425:94-98.
57. VanLandingham J.W., Cekic M., Cutler S.M., Hoffman S.W., Washington E.R., Johnson S.J., Miller D., Stein D.G. Progesterone and its metabolite allopregnanolone differentially regulate hemostatic proteins after traumatic brain injury. J. Cereb. Blood Flow Metab. 2008, 28:1786-1794.
58. Wang X. Investigational anti-inflammatory agents for the treatment of ischaemic brain injury. Expert Opin. Investig. Drugs 2005, 14:393-409.
59. Wang Y.F., Tsirka S.E., Strickland S., Stieg P.E., Soriano S.G., Lipton S.A. Tissue plasminogen activator (tPA) increases neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice. Nat. Med. 1998, 4:228-231.
60. Wang J.M., Liu L., Irwin R.W., Chen S., Brinton R.D. Regenerative potential of allopregnanolone. Brain Res. Rev. 2008, 57:398-409.
61. Wright D.W., Bauer M.E., Hoffman S.W., Stein D.G. Serum progesterone levels correlate with decreased cerebral edema after traumatic brain injury in male rats. J. Neurotrauma 2001, 18:901-909.
62. Wright D.W., Kellermann A.L., Hertzberg V.S., Clark P.L., Frankel M., Goldstein F.C., Salomone J.P., Dent L.L., Harris O.A., Ander D.S., Lowery D.W., Patel M.M., Denson D.D., Gordon A.B., Wald M.M., Gupta S., Hoffman S.W., Stein D.G. ProTECT: a randomized clinical trial of progesterone for acute traumatic brain injury. Ann. Emerg. Med. 2007, 49:391-402. 402 e391-392.
63. Yang Y., Estrada E.Y., Thompson J.F., Liu W., Rosenberg G.A. 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.
64. Yepes M., Lawrence D.A. Neuroserpin: a selective inhibitor of tissue-type plasminogen activator in the central nervous system. Thromb. Haemost. 2004, 91:457-464.
65. Yepes M., Sandkvist M., Wong M.K., Coleman T.A., Smith E., Cohan S.L., Lawrence D.A. Neuroserpin reduces cerebral infarct volume and protects neurons from ischemia-induced apoptosis. Blood 2000, 96:569-576.
66. Yepes M., Sandkvist M., Moore E.G., Bugge T.H., Strickland D.K., Lawrence D.A. Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J. Clin. Invest. 2003, 112:1533-1540.
67. Yilmaz G., Granger D.N. Cell adhesion molecules and ischemic stroke. Neurol. Res. 2008, 30:783-793.
68. Zhang Z., Zhang L., Yepes M., Jiang Q., Li Q., Arniego P., Coleman T.A., Lawrence D.A., Chopp M. Adjuvant treatment with neuroserpin increases the therapeutic window for tissue-type plasminogen activator administration in a rat model of embolic stroke. Circulation 2002, 106:740-745.
69. Zlokovic B.V. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008, 57:178-201.