Improvement of cold injury-induced mouse brain edema by endothelin ETB antagonists is accompanied by decreases in matrixmetalloproteinase 9 and vascular endothelial growth factor-A

European Journal of Neuroscience

Volumn 42, Issue 6, 2015, Pages 2356-2370

  Michinaga, Shotaro ^a   Seno, Naoki ^a   Fuka, Mayu ^a   Yamamoto, Yui ^a   Minami, Shizuho ^a   Kimura, Akimasa ^a   Hatanaka, Shunichi ^a   Nagase, Marina ^a   Matsuyama, Emi ^a   Yamanaka, Daisuke ^a   Koyama, Yutaka ^a  

^a OSAKA OHTANI UNIVERSITY   (Japan)

Author keywords

Astrocyte; Blood brain barrier; Brain injury; Vascular permeability factors

Indexed keywords

CD31 ANTIGEN; ENDOTHELIN B RECEPTOR ANTAGONIST; GELATINASE B; IRL 2500; MESSENGER RNA; N (2,6 DIMETHYLPIPERIDINOCARBONYL) 4 METHYLLEUCYL DEXTRO (1 METHOXYCARBONYLTRYPTOPHANYL) DEXTRO NORLEUCINE; UNCLASSIFIED DRUG; VASCULOTROPIN A; BIPHENYL DERIVATIVE; DIPEPTIDE; OLIGOPEPTIDE; PIPERIDINE DERIVATIVE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN EDEMA; COLD INJURY INDUCED MOUSE BRAIN EDEMA; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MEMBRANE PERMEABILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BRAIN; COLD INJURY; INJURIES; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; METABOLISM;

ANIMALS; ASTROCYTES; BIPHENYL COMPOUNDS; BRAIN EDEMA; CEREBRUM; COLD INJURY; DIPEPTIDES; ENDOTHELIN B RECEPTOR ANTAGONISTS; INJECTIONS, INTRAVENTRICULAR; MALE; MATRIX METALLOPROTEINASE 9; MICE; OLIGOPEPTIDES; PIPERIDINES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84942163300     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.13020     Document Type: Article

References (55)

1. Abbott, N.J., Rönnbäck, L. & Hansson, E. (2006) Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci., 7, 41-53.
2. Argaw, A.T., Gurfein, B.T., Zhang, Y., Zameer, A. & John, G.R. (2009) VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc. Natl. Acad. Sci. USA, 6, 1977-1982.
3. Asahi, M., Wang, X., Mori, T., Sumii, T., Jung, J.C., Moskowitz, M.A., Fini, M.E. & Lo, E.H. (2001) Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J. Neurosci., 21, 7724-7732.
4. Barone, F.C., Ohlstein, E.H., Hunter, A.J., Campbell, C.A., Hadingham, S.H., Parsons, A.A., Yang, Y. & Shohami, E. (2000) Selective antagonism of endothelin-A-receptors improves outcome in both head trauma and focal stroke in rat. J. Cardiovasc. Pharm., 36, S357-S361.
5. Bates, D.O. (2010) Vascular endothelial growth factors and vascular permeability. Cardiovasc. Res., 87, 262-271.
6. Chaturvedi, M. & Kaczmarek, L. (2014) MMP-9 inhibition: a therapeutic strategy in ischemic stroke. Mol. Neurobiol., 49, 563-573.
7. Hayashi, T., Abe, K., Suzuki, H. & Itoyama, Y. (1997) Rapid induction of vascular endothelial growth factor gene expression after transient middle cerebral artery occlusion in rats. Stroke, 28, 2039-2044.
8. B receptors. Eur. J. Neurosci., 9, 895-901.
9. Jiang, S., Xia, R., Jiang, Y., Wang, L. & Gao, F. (2014) Vascular endothelial growth factors enhance the permeability of the mouse blood-brain barrier. PLoS ONE, 2, e86407.
10. Kaundal, R.K., Deshpande, T.A., Gulati, A. & Sharma, S.S. (2012) Targeting endothelin receptors for pharmacotherapy of ischemic stroke: current scenario and future perspectives. Drug Discov. Today, 17, 793-804.
11. Kawai, N., Yamamoto, T., Yamamoto, H., McCarron, R.M. & Spatz, M. (1997) Functional characterization of endothelin receptors on cultured brain capillary endothelial cells of the rat. Neurochem. Int., 4, 597-605.
12. Kawai, N., Kawanishi, M., Okada, M., Matsumoto, Y. & Nagao, S. (2003) Treatment of cold injury-induced brain edema with a nonspecific matrix metalloproteinase inhibitor MMI270 in rats. J. Neurotraum., 7, 649-657.
13. Kimura, R., Nakase, H., Tamaki, R. & Sakaki, T. (2005) Vascular endothelial growth factor antagonist reduces brain edema formation and venous infarction. Stroke, 36, 1259-1263.
14. Koyama, Y. & Michinaga, S. (2012) Regulations of astrocytic functions by endothelins: roles in the pathophysiological responses of damaged brains. J. Pharmacol. Sci., 118, 401-407.
15. B receptor agonist increases expression of matrix metalloproteinase-2 and -9 in rat brain. J. Pharmacol. Sci., 114, 433-443.
16. B receptor agonist increases expressions of GDNF and BDNF in rat brain. Eur. J. Neurosci., 8, 887-894.
17. B receptor agonist stimulates vascular endothelial growth factor-A production and activates vascular endothelial growth factor receptors in rat brain. Neuroscience, 192, 689-698.
18. Koyama, Y., Maebara, Y., Hayashi, M., Nagae, R., Tokuyama, S. & Michinaga, S. (2012) Endothelins reciprocally regulate VEGF-A and angiopoietin-1 production in cultured rat astrocytes: implications on astrocytic proliferation. Glia, 60, 1954-1963.
19. Kumai, Y., Ooboshi, H., Ibayashi, S., Ishikawa, E., Sugimori, H., Kamouchi, M., Kitazono, T., Egashira, K. & Iida, M. (2007) Postischemic gene transfer of soluble Flt-1 protects against brain ischemia with marked attenuation of blood-brain barrier permeability. J. Cerebr. Blood F. Met., 6, 1152-1160.
20. Mackenzie, F. & Ruhrberg, C. (2012) Diverse roles for VEGF-A in the nervous system. Development, 8, 1371-1380.
21. Matsuo, Y., Mihara, S., Ninomiya, M. & Fujimoto, M. (2001) Protective effect of endothelin type A receptor antagonist on brain edema and injury after transient middle cerebral artery occlusion in rats. Stroke, 32, 2143-2148.
22. Matsuura, A., Yamochi, W., Hirata, K., Kawashima, S. & Yokoyama, M. (1998) Stimulatory interaction between vascular endothelial growth factor and endothelin-1 on each gene expression. Hypertension, 1, 89-95.
23. B receptor antagonists in mice. PLoS ONE, 9, e102009.
24. Moldes, O., Sobrino, T., Blanco, M., Agulla, J., Barral, D., Ramos-Cabrer, P. & Castillo, J. (2012) Neuroprotection afforded by antagonists of endothelin-1 receptors in experimental stroke. Neuropharmacology, 63, 279-285.
25. Muir, E.M., Adcock, K.H., Morgenstern, D.A., Clayton, R., von Stillfried, N., Rhodes, K., Ellis, C., Fawcett, J.W. & Rogers, J.H. (2002) Matrix metalloproteases and their inhibitors are produced by overlapping populations of activated astrocytes. Brain Res. Mol. Brain Res., 100, 103-117.
26. Murakami, K., Kondo, T., Yang, G., Chen, S.F., Morita-Fujimura, Y. & Chan, P.H. (1999) Cold injury in mice: a model to study mechanisms of brain edema and neuronal apoptosis. Prog. Neurobiol., 57, 289-299.
27. Nag, S. (1996) Cold-injury of the cerebral cortex: immunolocalization of cellular proteins and blood-brain barrier permeability studies. J. Neuropath. Exp. Neur., 55, 880-888.
28. Nag, S., Eskandarian, M.R., Davis, J. & Eubanks, J.H. (2002) Differential expression of vascular endothelial growth factor-A (VEGF-A) and VEGF-B after brain injury. J. Neuropath. Exp. Neur., 9, 778-788.
29. Nag, S., Manias, J.L. & Stewart, D.J. (2009) Pathology and new players in the pathogenesis of brain edema. Acta Neuropathol., 118, 197-217.
30. Oury, T.D., Piantadosi, C.A. & Crapo, J.D. (1993) Cold-induced brain edema in mice. Involvement of extracellular superoxide dismutase and nitric oxide. J. Biol. Chem., 268, 15394-15398.
31. Pekny, M. & Nilsson, M. (2005) Astrocyte activation and reactive gliosis. Glia, 50, 427-434.
32. Peters, C.M., Rogers, S.D., Pomonis, J.D., Egnaczyk, G.F., Keyser, C.P., Schmidt, J.A., Ghilardi, J.R., Maggio, J.E. & Mantyh, P.W. (2003) Endothelin receptor expression in the normal and injured spinal cord: potential involvement in injury-induced ischemia and gliosis. Exp. Neurol., 180, 1-13.
33. Planas, A.M., Solé, S. & Justicia, C. (2001) Expression and activation of matrix metalloproteinase-2 and -9 in rat brain after transient focal cerebral ischemia. Neurobiol. Dis., 8, 834-846.
34. Rogers, S.D., Peters, C.M., Pomonis, J.D., Hagiwara, H., Ghilardi, J.R. & Mantyh, P.W. (2003) Endothelin B receptors are expressed by astrocytes and regulate astrocyte hypertrophy in the normal and injured CNS. Glia, 41, 180-190.
35. Rosenberg, G.A. & Navratil, M. (1997) Metalloproteinase inhibition blocks edema in intracerebral hemorrhage in the rat. Neurology, 4, 921-926.
36. Rosenberg, G.A., Estrada, E.Y. & Dencoff, J.E. (1998) Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke, 29, 2189-2195.
37. Rosenberg, G.A., Cunningham, L.A., Wallace, J., Alexander, S., Estrada, E.Y., Grossetete, M., Razhagi, A., Miller, K. & Gearing, A. (2001) Immunohistochemistry of matrix metalloproteinases in reperfusion injury to rat brain: activation of MMP9 linked to stromelysin-1 and microglia in cell cultures. Brain Res., 893, 104-112.
38. Schinelli, S. (2006) Pharmacology and physiopathology of the brain endothelin system: an overview. Curr. Med. Chem., 13, 627-638.
39. Seo, J.H., Guo, S., Lok, J., Navaratna, D., Whalen, M.J., Kim, K.W. & Lo, E.H. (2012) Neurovascular matrix metalloproteinases and the blood-brain barrier. Curr. Pharm. Design, 25, 3645-3648.
40. Simard, J.M., Kent, T.A., Chen, M., Tarasov, K.V. & Gerzanich, V. (2007) Brain oedema in focal ischaemia: molecular pathophysiology and theoretical implications. Lancet Neurol., 6, 258-268.
41. Sköld, M.K., von Gertten, C., Sandberg-Nordqvist, A.C., Mathiesen, T. & Holmin, S. (2005) VEGF and VEGF receptor expression after experimental brain contusion in rat. J. Neurotraum., 22, 353-367.
42. Sofroniew, M.V. (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci., 32, 638-647.
43. Sood, R.R., Taheri, S., Candelario-Jalil, E., Estrada, E.Y. & Rosenberg, G.A. (2008) Early beneficial effect of matrix metalloproteinase inhibition on blood-brain barrier permeability as measured by magnetic resonance imaging countered by impaired long-term recovery after stroke in rat brain. J. Cerebr. Blood F. Met., 28, 431-438.
44. Unterberg, A.W., Stover, J., Kress, B. & Kiening, K.L. (2004) Edema and brain trauma. Neuroscience, 4, 1021-1029.
45. Van Bruggen, N., Thibodeaux, H., Palmer, J.T., Lee, W.P., Fu, L., Cairns, B., Tumas, D., Gerlai, R., Williams, S.P., van Lookeren Campagne, M. & Ferrara, N. (1999) VEGF antagonism reduces edema formation and tissue damage after ischemia/reperfusion injury in the mouse brain. J. Clin. Invest., 104, 1613-1620.
46. Van Lint, P. & Libert, C. (2007) Chemokine and cytokine processing by matrix metalloproteinases and its effect on leukocyte migration and inflammation. J. Leukocyte Biol., 82, 1375-1381.
47. Vandenbroucke, R.E. & Libert, C. (2014) Is there new hope for therapeutic matrix metalloproteinase inhibition? Nat. Rev. Drug Discov., 13, 904-927.
48. Walcott, B.P., Kahle, K.T. & Simard, J.M. (2012) Novel treatment targets for cerebral edema. Neurotherapeutics, 9, 65-72.
49. Wang, J. & Tsirka, S.E. (2005) Neuroprotection by inhibition of matrix metalloproteinases in a mouse model of intracerebral haemorrhage. Brain, 128, 1622-1633.
50. Wang, X., Jung, J., Asahi, M., Chwang, W., Russo, L., Moskowitz, M.A., Dixon, C.E., Fini, M.E. & Lo, E.H. (2000) Effects of matrix metalloproteinase-9 gene knock-out on morphological and motor outcomes after traumatic brain injury. J. Neurosci., 20, 7037-7042.
51. Wilhelmsson, U., Li, L., Pekna, M., Berthold, C.H., Blom, S., Eliasson, C., Renner, O., Bushong, E., Ellisman, M., Morgan, T.E. & Pekny, M. (2004) Absence of glial fibrillary acidic protein and vimentin prevents hypertrophy of astrocytic processes and improves post-traumatic regeneration. J. Neurosci., 24, 5016-5021.
52. Wolburg, H., Noell, S., Mack, A., Wolburg-Buchholz, K. & Fallier-Becker, P. (2009) Brain endothelial cells and the glio-vascular complex. Cell Tissue Res., 335, 75-96.
53. Yamaguchi, M., Jadhav, V., Obenaus, A., Colohan, A. & Zhang, J.H. (2007) Matrix metalloproteinase inhibition attenuates brain edema in an in vivo model of surgically-induced brain injury. Neurosurgery, 5, 1067-1075.
54. Yang, Y. & Rosenberg, G.A. (2011) Blood-brain barrier breakdown in acute and chronic cerebrovascular disease. Stroke, 42, 3323-3328.
55. Yong, V.W., Power, C., Forsyth, P. & Edwards, D.R. (2001) Metalloproteinases in biology and pathology of the nervous system. Nat. Rev. Neurosci., 7, 502-511.