Release of matrix metalloproteinases-2 and 9 by S-nitrosylated caveolin-1 contributes to degradation of extracellular matrix in tPA-treated hypoxic endothelial cells

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Song, Haoming ^a   Cheng, Youjun ^b   Bi, Gang ^a   Zhu, Yihui ^a   Jun, Wei ^a   Ma, Wenlin ^a   Wu, Huimin ^a  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^b Medical University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; FIBRONECTIN; GELATINASE A; GELATINASE B; LAMININ; LAMININ BETA 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; SMALL INTERFERING RNA; TISSUE PLASMINOGEN ACTIVATOR; UNCLASSIFIED DRUG; 1,3-DIHYDROXY-4,4,5,5-TETRAMETHYL-2-(4-CARBOXYPHENYL)TETRAHYDROIMIDAZOLE; BENZOIC ACID DERIVATIVE; CONDITIONED MEDIUM; GLUCOSE; IMIDAZOLE DERIVATIVE; OXYGEN;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN VASCULAR ENDOTHELIAL CELL; CELL HYPOXIA; CELL STIMULATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME RELEASE; EXTRACELLULAR MATRIX; GENE SILENCING; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOUSE; NITROSYLATION; NONHUMAN; OXYGEN GLUCOSE DEPRIVATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CONDITIONED MEDIUM; DEFICIENCY; DRUG EFFECTS; HUMAN; METABOLISM; NITROSATION; PHARMACOLOGY;

ANIMALS; BENZOATES; CAVEOLIN 1; CELL HYPOXIA; CULTURE MEDIA, CONDITIONED; ENDOTHELIAL CELLS; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBRONECTINS; GLUCOSE; HUMANS; IMIDAZOLES; LAMININ; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; NITRIC OXIDE; NITROSATION; OXYGEN; PROTEOLYSIS; TISSUE PLASMINOGEN ACTIVATOR;

EID: 84960540729     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0149269     Document Type: Article

References (51)

1. Wang X., Tsuji K., Lee S. R., Ning M., Furie K. L., Buchan A. M., et al. Mechanisms of hemorrhagic transformation after tissue plasminogen activator reperfusion therapy for ischemic stroke. Stroke; a journal of cerebral circulation. 2004;35:2726-30. PMID: 15459442
2. 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. The Journal of clinical investigation. 2003;112:1533-40. PMID: 14617754
3. Alberts M. J. tPA in acute ischemic stroke: United States experience and issues for the future. Neurology. 1998;51:S53-5.
4. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. The New England journal of medicine. 1995;333:1581-7. PMID: 7477192
5. Leigh R., Jen S. S., Hillis A. E., Krakauer J. W., Barker P. B. Pretreatment blood-brain barrier damage and post-treatment intracranial hemorrhage in patients receiving intravenous tissue-type plasminogen activator. Stroke; ajournal of cerebral circulation. 2014;45:2030-5. doi: 10.1161/STROKEAHA.114. 005249 PMID: 24876245
6. Lansberg M. G., Thijs V. N., Bammer R., Kemp S., Wijman C. A., Marks M. P., et al. Risk factors of symptomatic intracerebral hemorrhage after tPA therapy for acute stroke. Stroke; a journal of cerebral circulation. 2007;38:2275-8. PMID: 17569874
7. Yamashita T., Kamiya T., Deguchi K., Inaba T., Zhang H., Shang J., et al. Dissociation and protection of the neurovascular unit after thrombolysis and reperfusion in ischemic rat brain. Journal of cerebral blood flow and metabolism: official journal of the International Society of Cerebral Blood Flow and Metabolism. 2009;29:715-25.
8. Figueroa B. E., Keep R. F., Betz A. L., Hoff JT. Plasminogen activators potentiate thrombin-induced brain injury. Stroke; ajournal of cerebral circulation. 1998;29:1202-7, discussion 8. PMID: 9626295
9. Abu Fanne R., Nassar T., Yarovoi S., Rayan A., Lamensdorf I., Karakoveski M., et al. Blood-brain barrier permeability and tPA-mediated neurotoxicity. Neuropharmacology. 2010;58:972-80. doi: 10. 1016/j.neuropharm.2009.12.017 PMID: 20060006
10. Won S. J., Tang X. N., Suh S. W., Yenari M. A., Swanson R. A. Hyperglycemia promotes tissue plasminogen activator-induced hemorrhage by Increasing superoxide production. Annals of neurology. 2011;70:583-90. doi: 10.1002/ana.22538 PMID: 22002675
11. Yang Y., Rosenberg G. A. Blood-brain barrier breakdown in acute and chronic cerebrovascular disease. Stroke; a journal of cerebral circulation. 2011;42:3323-8. doi: 10.1161/STROKEAHA.110.608257 PMID: 21940972
12. Davis G. E., Senger D. R. Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circulation research. 2005;97:1093-107. PMID: 16306453
13. Liu J., Jin X., Liu K. J., Liu W. Matrix metalloproteinase-2-mediated occludin degradation and caveolin-1-mediated claudin-5 redistribution contribute to blood-brain barrier damage in early ischemic stroke stage. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2012;32:3044-57.
14. Jin X., Liu J., Yang Y., Liu K. J., Liu W. Spatiotemporal evolution of blood brain barrier damage and tissue infarction within the first 3h after ischemia onset. Neurobiology of disease. 2012;48:309-16. doi: 10.1016/j.nbd.2012.07.007 PMID: 22813865
15. Zhao B. Q., Ikeda Y., Ihara H., Urano T., Fan W., Mikawa S., et al. Essential role of endogenous tissue plasminogen activator through matrix metalloproteinase 9 induction and expression on heparin-produced cerebral hemorrhage after cerebral ischemia in mice. Blood. 2004;103:2610-6. PMID: 14630814
16. Taraboletti G., D'Ascenzo S., Borsotti P., Giavazzi R., Pavan A., Dolo V. Shedding of the matrix metalloproteinases MMP-2, MMP-9, and MT1-MMPas membrane vesicle-associated components by endothelial cells. The American journal of pathology. 2002;160:673-80. PMID: 11839588
17. Taraboletti G., D'Ascenzo S., Giusti I., Marchetti D., Borsotti P., Millimaggi D., et al. Bioavailability of VEGF in tumor-shed vesicles depends on vesicle burst induced by acidic pH. Neoplasia. 2006;8:96-103. PMID: 16611402
18. Alam M., Mohammad A., Rahman S., Todd K., Shuaib A. Hyperthermia up-regulates matrix metalloproteinases and accelerates basement membrane degradation in experimental stroke. Neuroscience letters. 2011;495:135-9. doi: 10.1016/j.neulet.2011.03.056 PMID: 21443925
19. del Zoppo G. J., von Kummer R., Hamann G. F. Ischaemic damage of brain microvessels: inherent risks for thrombolytic treatment in stroke. Journal of neurology, neurosurgery, and psychiatry. 1998;65:1-9. PMID: 9667553
20. Hamann G. F., Okada Y., Fitridge R., del Zoppo G. J. Microvascular basal lamina antigens disappear during cerebral ischemia and reperfusion. Stroke; ajournal of cerebral circulation. 1995;26:2120-6. PMID: 7482660
21. Stamatovic S. M., Keep R. F., Wang M. M., Jankovic I., Andjelkovic A. V. Caveolae-mediated internalization of occludin and claudin-5 during CCL2-induced tight junction remodeling in brain endothelial cells. The Journal of biological chemistry. 2009;284:19053-66. doi: 10.1074/jbc. M109.000521 PMID: 19423710
22. Jin Y., Kim H. P., Cao J., Zhang M., Ifedigbo E., Choi A. M. Caveolin-1 regulates the secretion and cytoprotection of Cyr61 in hyperoxic cell death. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2009;23:341-50.
23. Puddu A., Salani B., Cordera R., Viviani G. L., Maggi D. Caveolin-1 is essential forglimepiride-induced insulin secretion in the pancreatic betaTC-6 cell line. Biochemical and biophysical research communications. 2008;375:235-7. doi: 10.1016/j.bbrc.2008.08.003 PMID: 18703018
24. Henkhaus R. S., Roy U. K., Cavallo-Medved D., Sloane B. F., Gerner E. W., Ignatenko N. A. Caveolin-1-mediated expression and secretion of kallikrein 6 in colon cancer cells. Neoplasia. 2008;10:140-8. PMID: 18283336
25. Tahir S. A., Yang G., Goltsov A. A., Watanabe M., Tabata K., Addai J., et al. Tumor cell-secreted caveolin-1 has proangiogenic activities in prostate cancer. Cancer research. 2008;68:731-9. doi: 10.1158/0008-5472. CAN-07-2668 PMID: 18245473
26. Wu D., Terrian D. M. Regulation of caveolin-1 expression and secretion by a protein kinase cepsilon signaling pathway in human prostate cancer cells. The Journal of biological chemistry. 2002;277:40449-55. PMID: 12185081
27. Tahir S. A., Yang G., Ebara S., Timme T. L, Satoh T., Li L, et al. Secreted caveolin-1 stimulates cell survival/clonal growth and contributes to metastasis in androgen-insensitive prostate cancer. Cancer research. 2001;61:3882-5. PMID: 11358800
28. Han F., Zhu H. G. Caveolin-1 regulating the invasion and expression of matrix metalloproteinase (MMPs) in pancreatic carcinoma cells. The Journal of surgical research. 2010;159:443-50. doi: 10. 1016/j.jss.2009.03.079 PMID: 20031158
29. Inoue T., Pecen P., Maddala R., Skiba N. P., Pattabiraman P. P., Epstein D. L., et al. Characterization of cytoskeleton-enriched protein fraction of the trabecular meshwork and ciliary muscle cells. Investigative ophthalmology & visual science. 2010;51:6461-71.
30. Liu W., Furuichi T., Miyake M., Rosenberg G. A., Liu K. J. Differential expression of tissue inhibitor of metalloproteinases-3 in cultured astrocytes and neurons regulates the activation of matrix metalloproteinase-2. J Neurosci Res. 2007;85:829-36. PMID: 17279554
31. Montagnani M., Chen H., Barr V. A., Quon M. J. Insulin-stimulated activation of eNOS is independent of Ca2+but requires phosphorylation by Aktat Ser (1179). The Journal of biological chemistry. 2001;276:30392-8. PMID: 11402048
32. Mukhopadhyay S., Lee J., Sehgal P. B. Depletion of the ATPase NSF from Golgi membranes with hypo-S-nitrosylation of vasorelevant proteins in endothelial cells exposed to monocrotaline pyrrole. American journal of physiology. Heart and circulatory physiology. 2008;295:H1943-55. doi: 10.1152/ajpheart.00642.2008 PMID: 18775848
33. Wang X., Lee S. R., Arai K., Tsuji K., Rebeck G. W., Lo E. H. Lipoprotein receptor-mediated induction of matrix metalloproteinase by tissue plasminogen activator. Nature medicine. 2003;9:1313-7. PMID: 12960961
34. Suzuki Y., Nagai N., Yamakawa K., Kawakami J., Lijnen H. R., Umemura K. Tissue-type plasminogen activator (t-PA) induces stromelysin-1 (MMP-3) in endothelial cells through activation of lipoprotein receptor-related protein. Blood. 2009;114:3352-8. doi: 10.1182/blood-2009-02-203919 PMID: 19608750
35. Roux P. P., Blenis J. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiology and molecular biology reviews: MMBR. 2004;68:320-44. PMID: 15187187
36. Meloche S., Pouyssegur J. The ERK1/2 mitogen-activated protein kinase pathway as a master regulator of the G1- to S-phase transition. Oncogene. 2007;26:3227-39. PMID: 17496918
37. Chaudhry K., Rogers R., Guo M., Lai Q., Goel G., Liebelt B., et al. Matrix metalloproteinase-9 (MMP-9) expression and extracellular signal-regulated kinase 1 and 2 (ERK1/2) activation in exercise-reduced neuronal apoptosis afterstroke. Neuroscience letters. 2010;474:109-14. doi: 10.1016/j.neulet.2010. 03.020 PMID: 20298757
38. Maddahi A., Chen Q., Edvinsson L. Enhanced cerebrovascular expression of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 via the MEK/ERK pathway during cerebral ischemia in the rat. BMC neuroscience. 2009;10:56. doi: 10.1186/1471-2202-10-56 PMID: 19497125
39. Adya R., Tan B. K., Punn A., Chen J., Randeva H. S. Visfatin induces human endothelial VEGF and MMP-2/9 production via MAPK and PI3K/Akt signalling pathways: novel insights into visfatin-induced angiogenesis. Cardiovascular research. 2008;78:356-65. PMID: 18093986
40. Polavarapu R., Gongora M. C., Yi H., Ranganthan S., Lawrence D. A., Strickland D., et al. Tissue-type plasminogen activator-mediated shedding of astrocytic low-density lipoprotein receptor-related protein increases the permeability of the neurovascular unit. Blood. 2007;109:3270-8. PMID: 17170123
41. Intengan H. D., Schiffrin E. L. Vascular remodeling in hypertension: roles of apoptosis, inflammation, and fibrosis. Hypertension. 2001;38:581-7. PMID: 11566935
42. Schubert W., Frank P. G., Woodman S. E., Hyogo H., Cohen D. E., Chow C. W., et al. Microvascular hyperpermeability in caveolin-1 (-/-) knock-out mice. Treatment with a specific nitric-oxide synthase inhibitor, L-NAME, restores normal microvascular permeability in Cav-1 null mice. The Journal of biological chemistry. 2002;277:40091-8. PMID: 12167625
43. Gu Y., Zheng G., Xu M., Li Y., Chen X., Zhu W., et al. Caveolin-1 regulates nitric oxide-mediated matrix metalloproteinases activity and blood-brain barrier permeability in focal cerebral ischemia and reperfusion injury. Journal of neurochemistry. 2012;120:147-56. doi: 10.1111/j.1471-4159.2011.07542.x PMID: 22007835
44. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEBJ. 1992;6:3051-64. PMID: 1381691
45. Navarro-Gonzalvez J. A., Garcia-Benayas C, Arenas J. Semiautomated measurement of nitrate in biological fluids. Clin Chem. 1998;44:679-81. PMID: 9510886
46. Chi O. Z., Chang Q., Wang G., Weiss H. R. Effects of nitric oxide on blood-brain barrier disruption caused by intracarotid injection of hyperosmolar mannitol in rats. Anesth Analg. 1997;84:370-5. PMID: 9024031
47. Correa F., Gauberti M., Parcq J., Macrez R., Hommet Y., Obiang P., et al. Tissue plasminogen activator prevents white matter damage following stroke. The Journal of experimental medicine. 2011;208:1229-42. doi: 10.1084/jem.20101880 PMID: 21576385
48. Mantuano E., Lam M. S., Gonias S. L. LRP1 assembles unique co-receptor systems to initiate cell signaling in response to tissue-type plasminogen activator and myelin-associated glycoprotein. The Journal of biological chemistry. 2013;288:34009-18. doi: 10.1074/jbc. M113.509133 PMID: 24129569
49. Parcq J., Bertrand T., Montagne A., Baron A. F., Macrez R., Billard J. M., et al. Unveiling an exceptional zymogen: the single-chain form of tPA is a selective activator of NMDA receptor-dependent signaling and neurotoxicity. Cell death and differentiation. 2012;19:1983-91. doi: 10.1038/cdd.2012.86 PMID: 22743997
50. Xu P., Derynck R. Direct activation of TACE-mediated ectodomain shedding by p38 MAP kinase regulates EGF receptor-dependent cell proliferation. Molecular cell. 2010;37:551-66. doi: 10.1016/j. molcel.2010.01.034 PMID: 20188673
51. Swendeman S., Mendelson K., Weskamp G., Horiuchi K., Deutsch U., Scherle P., et al. VEGF-Astimulates ADAM17-dependent shedding of VEGFR2 and crosstalk between VEGFR2 and ERK signaling. Circulation research. 2008;103:916-8. doi: 10.1161/CIRCRESAHA.108.184416 PMID: 18818406