Synthetic gelatinases inhibitor attenuates electromagnetic pulse-induced blood-brain barrier disruption by inhibiting gelatinases-mediated ZO-1 degradation in rats

Toxicology

Volumn 285, Issue 1-2, 2011, Pages 31-38

  Qiu, Lian Bo ^a   Zhou, Yan ^a   Wang, Qi ^b   Yang, Long long ^a   Liu, Hai Qiang ^a   Xu, Sheng Long ^a   Qi, Yu Hong ^b   Ding, Gui Rong ^a   Guo, Guo Zhen ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Blood brain barrier; Electromagnetic pulse; Gelatinase; Permeability; ZO 1

Indexed keywords

GELATINASE A; GELATINASE B; GELATINASE INHIBITOR; MESSENGER RNA; PROTEIN ZO1; SB 3CT; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CORTEX; BRAIN LEVEL; CONTROLLED STUDY; ELECTROMAGNETIC FIELD; ENZYME ACTIVITY; ENZYME INHIBITION; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RAT; TIGHT JUNCTION; ZYMOGRAPHY;

ANIMALS; BLOOD-BRAIN BARRIER; ELECTROMAGNETIC FIELDS; GELATINASES; HETEROCYCLIC COMPOUNDS, 1-RING; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES; MEMBRANE PROTEINS; PHOSPHOPROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SULFONES; TIME FACTORS; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TISSUE INHIBITOR OF METALLOPROTEINASE-2;

RATTUS;

EID: 79956274389     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2011.03.019     Document Type: Article

References (44)

1. Abbott N.J., Patabendige A.A., Dolman D.E., Yusof S.R., Begley D.J. Structure and function of the blood-brain barrier. Neurobiol. Dis. 2010, 37:13-25.
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. Brown S., Bernardo M.M., Li Z.H., Kotra L.P., Tanaka Y., Fridman R., Mobashery S. Potent and selective mechanism-based inhibition of gelatinases. J. Am. Chem. Soc. 2000, 122:6799-6800.
5. Daniel C., Duffield J., Brunner T., Steinmann-Niggli K., Lods N., Marti H.P. Matrix metalloproteinase inhibitors cause cell cycle arrest and apoptosis in glomerular messangial cells. J. Pharmacol. Exp. Ther. 2001, 297:57-68.
6. Ding G.R., Qiu L.B., Wang X.W., Li K.C., Zhou Y.C., Zhou Y., Zhang J., Zhou J.X., Li Y.R., Guo G.Z. EMP-induced alterations of tight junction protein expression and disruption of the blood-brain barrier. Toxicol. Lett. 2010, 196:154-160.
7. Ding Z., Hao Q., Hu L., Su J., Liu G. All-solid-state repetitive semiconductor opening switch-based short pulse generator. Rev. Sci. Instrum. 2009, 80:093303. 10.1063/1.3233937.
8. Dobrogowska D.H., Vobrodt A.W. Immunogold localization of tight junctional proteins in normal and osmotically-affected rat blood-brain barrier. J. Mol. Histol. 2004, 35:529-539.
9. Ebnet K., Schulz C.U., Meyer Zu, Brickwedde M.K., Pendl G.G., Vestweber D. Junctional adhesion molecule interacts with the PDZ domain-containing proteins AF-6 and ZO-1. J. Biol. Chem. 2000, 275:27979-27988.
10. Fujimoto M., Takagi Y., Aoki T., Hayase M., Marumo T., Gomi M., Nishimura M., Kataoka H., Hashimoto N., Nozaki K. Tissue inhibitor of metalloproteinases protect blood-brain barrier disruption in focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2008, 28:1674-1685.
11. Furuse M., Itoh M., Hirase T., Nagafuchi A., Yonemura S., Tsukita S. Direct association of occludin with ZO-1 and its possible involvement in the localization of occludin at tight junctions. J. Cell Biol. 1994, 127:1617-1626.
12. Galis Z.S., Sukhova G.K., Libby P. Microscopic localization of active proteases by in situ zymography: detection of matrix metalloproteinase activity in vascular tissue. FASEB J. 1995, 9:974-980.
13. Gasche Y., Soccal P.M., Kanemitsu M., Copin J.C. Matrix metalloproteinases and diseases of the central nervous system with a special emphasis on ischemic brain. Front. Biosci. 2006, 11:1289-1301.
14. Gu Z., Cui J.K., Brown S., Fridman R., Mobashery S., Strongin A.Y., Lipton S.A. A highly specific inhibitor of matrix metalloproteinase-9 rescues laminin from proteolysis and neurons from apoptosis in transient focal cerebral ischemia. J. Neurosci. 2005, 25. 6401-6308.
15. Harkness K.A., Adamson P., Sussman J.D., Davies-Jones G.A., Greenwood J., Woodroofe M.N. Dexamethasone regulation of matrix metalloproteinase expression in CNS vascular endothelium. Brain 2000, 123:698-709.
16. Haskins J., Gu L., Wittchen E.S., Hibbard J., Stevenson B.R. ZO-3, a novel member of the MAGUK protein family found at the tight junction, interacts with ZO-1 and occludin. J. Cell Biol. 1998, 141:199-208.
17. Hawkins B.T., Davis T.P. The blood-brain barrier/neurovascular unit in health and disease. Pharm. Rev. 2005, 57:173-185.
18. Huang W., Eum S.Y., András I.E., Hennig B., Toborek M. PPARα and PPARγ attenuate HIV-induced dysregulation of tight junction proteins by modulations of matrix metalloproteinase and proteasome activities. FASEB J. 2009, 23:1596-1606.
19. Kähäri V.M., Saarialho-Kere U. Matrix metalloproteinases and their inhibitors in tumor growth and invasion. Ann. Med. 1999, 31:34-45.
20. Kapural M., Krizanac-Bengez L., Barnett G., Perl J., Masaryk T., Apollo D., Rasmussen P., Mayberg M.R., Janigro D. Serum S-100β as a possible marker of blood-brain barrier disruption. Brain Res. 2002, 940:102-104.
21. Kieseier B.C., Paul R., Koedel U., Seifert T., Clement J.M., Gearing A.J., Pfister H.W., Hartung H.P. Differential expression of matrix metalloproteinases in bacterial meningitis. Brain 1999, 122:1579-1587.
22. Kim D.H., Lilliehook C., Roides B., Chen Z.X., Chang M., Mobashery S., Goldman S.A. Testosterone-induced matrix metalloproteinase activation is a checkpoint for neuronal addition to the adult songbird brain. J. Neurosci. 2008, 28:208-216.
23. Kniesel U., Wolburg H. Tight junctions of the blood-brain barrier. Cell Mol. Neurobiol. 2000, 20:57-76.
24. Krüger A., J.E., Arlt M., Gerg M., Kopitz C., Bernardo M.M., Chang M., Mobashery S., Fridman R. Antimetastatic activity of a novel mechanism-based gelatinase inhibitor. Cancer Res. 2005, 65:3523-3526.
25. Liuzzi G.M., Mastroianni C.M., Santacroce M.P., Fanelli M., D'Agostino C., Vullo V., Riccio P. Increased activity of matrix metalloproteinases in the cerebrospinal fluid of patients with HIV-associated neurological diseases. J. Neurovirol. 2000, 6:156-163.
26. 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.
27. Morita-Fujimura Y., Fujimura M., Gasche Y., Copin J., Chan P.H. Overexpression of copper and zinc superoxide dismutase in transgenic mice prevents the induction and activation of matrix metalloproteinases after cold injury induced brain trauma. J. Cereb. Blood Flow Metab. 1999, 20:130-138.
28. Mun-Bryce S., Rosenberg G.A. Gelatinase B modulates selective opening of the blood-brain barrier during inflammation. Am. J. Physiol. 1998, 274:R1203-R1211.
29. Oscar K.J., Hawkins T.D. Microwave alteration of the blood-brain barrier system of rats. Brain Res. 1977, 126:281-293.
30. Papadopoulos M.C., Saadoun S., Woodrow C.J., Davies D.C., Costa-Martins P., Moss R.F., Krishna S., Bell B.A. Occludin expression in microvessels of neoplastic and non-neoplastic human brain. Neuropathol. Appl. Neurobiol. 2001, 27:384-395.
31. Qiu L.B., Ding G.R., Li K.C., Wang X.W., Zhou Y., Zhou Y.C., Li Y.R., Guo G.Z. The role of protein kinase C in the opening of blood-brain barrier induced by electromagnetic pulse. Toxicology 2010, 273:29-34.
32. Rooprai H.K., McCormick D. Proteases and their inhibitors in human brain tumor: a review. Anticancer Res. 1997, 17:4151-4162.
33. Rosenberg G.A. Matrix metalloproteinases in neuroinflammation. Glia 2002, 39:279-291.
34. Rosenberg G.A., Estrada E.Y., Mobashery S. Effect of synthetic matrix metalloproteinase inhibitors on lipopolysaccharide-induced blood-brain barrier opening in rodents: differences in response based on strains and solvents. Brain Res. 2007, 1133:186-192.
35. Schirmacher A., Winters S., Fischer S., Goeke J., Galla H.J., Kullnick U., Ringelstein E.B., Stögbauer F. Electromagnetic fields (1.8GHz) increase the permeability to sucrose of the blood-brain barrier in vitro. Bioelectromagnetics 2000, 21:338-345.
36. Shapiro S.D. Matrix metalloproteinase degradation of extracellular matrix: biological consequences. Curr. Opin. Cell Biol. 1998, 10:602-608.
37. Stevenson B.R., Siliciano J.D., Mooseker M.S., Goodenough D.A. Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J. Cell Biol. 1986, 103:755-766.
38. Tanaka Y., Koizumi C., Marumo T., Omura T., Yoshida S. Serum S100B indicates brain edema formation and predicts long-term neurological outcomes in rat transient middle cerebral artery occlusion model. Brain Res. 2007, 1137:140-145.
39. Tanaka Y., Marumo T., Shibuta H., Omura T., Yoshida S. Serum S100B, brain edema, and hematoma formation in a rat model of collagenase-induced hemorrhagic stroke. Brain Res. Bull. 2009, 78:158-163.
40. Williams W.M., Del-Cerro M., Michaelson S.M. Effect of 2450-MHz microwave energy on the blood-brain barrier to hydrophilic molecules. B. Effect on the permeability to HRP. Brain Res. 1984, 319:171-181.
41. 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.
42. Yong V.W., Krekoski C.A., Forsyth P.A., Bell R., Edwards D.R. Matrix metalloproteinases and diseases of the CNS. Trends Neurosci. 1998, 21:75-80.
43. Yong V.W., Power C., Forsyth P., Edwards D.R. Metalloproteinases in biology and pathology of the nervous system. Nat. Rev. Neurosci. 2001, 2:502-511.
44. Zhang J.W., Deb S., Gottschall P.E. Regional and age-related expression of gelatinases in brains of young and old rats after treatment with kainic acid. Neurosci. Lett. 2000, 295:9-12.