Fluoxetine inhibits matrix metalloprotease activation and prevents disruption of blood-spinal cord barrier after spinal cord injury

Brain

Volumn 135, Issue 8, 2012, Pages 2375-2389

  Lee, Jee Y ^a   Kim, Hwang S ^a   Choi, Hye Y ^a   Oh, Tae H ^a   Yune, Tae Y ^a  

^a Kyung Hee University Hospital   (South Korea)

Author keywords

blood brain barrier; fluoxetine; matrix metalloprotease; spinal cord injury; tight junction

Indexed keywords

FLUOXETINE; GELATINASE A; GELATINASE B; GROALPHA PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MACROPHAGE ELASTASE; MATRIX METALLOPROTEINASE; MESSENGER RNA; MIP1ALPHA PROTEIN; OCCLUDIN; PROTEIN ZO1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD BRAIN BARRIER; BLOOD CEREBROSPINAL FLUID BARRIER; BLOOD SPINAL CORD BARRIER; BLOOD VESSEL; CELL DEATH; CELL INFILTRATION; CONTROLLED STUDY; CONTUSION; CONVALESCENCE; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INHIBITION; FLUORIMETRIC ENZYME ACTIVITY ASSAY; FLUOROMETRY; GENE EXPRESSION; IMMUNOFLUORESCENCE; LOCOMOTION; MACROPHAGE; MALE; MOUSE; NEUROPROTECTION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OXYGEN GLUCOSE DEPRIVATION; PRIORITY JOURNAL; REOXYGENATION; SPINAL CORD INJURY; TIGHT JUNCTION; ZYMOGRAPHY;

EID: 84864650244     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aws171     Document Type: Article

References (85)

1. Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006; 7: 41-53.
2. Abdel Salam OM. Fluoxetine and sertraline stimulate gastric acid secretion via a vagal pathway in anaesthetised rats. Pharmacol Res 2004; 50: 309-16.
3. Agrawal S, Anderson P, Durbeej M, van RN, Ivars F, Opdenakker G, et al. Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J Exp Med 2006; 203: 1007-19.
4. Anjaneyulu M, Chopra K. Possible involvement of cholinergic and opioid receptor mechanisms in fluoxetine mediated antinociception response in streptozotocin-induced diabetic mice. Eur J Pharmacol 2006; 538: 80-4.
5. Asahi M, Wang X, Mori T, Sumii T, Jung JC, Moskowitz MA, et al. 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: 7724-32.
6. Asensio VC, Campbell IL. Chemokines in the CNS: plurifunctional mediators in diverse states. Trends Neurosci 1999; 22: 504-12.
7. Basso DM, Fisher LC, Anderson AJ, Jakeman LB, McTigue DM, Popovich PG. Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 2006; 23: 635-59.
8. Bauer AT, Burgers HF, Rabie T, Marti HH. Matrix metalloproteinase-9 mediates hypoxia-induced vascular leakage in the brain via tight junction rearrangement. J Cereb Blood Flow Metab 2010; 30: 837-48.
9. Beattie MS, Farooqui AA, Bresnahan JC. Review of current evidence for apoptosis after spinal cord injury. J Neurotrauma 2000; 17: 915-25.
10. Begovic A, Zulic I, Becic F. Testing of analgesic effect of fluoxetine. Bosn J Basic Med Sci 2004; 4: 79-81.
11. Benton RL, Maddie MA, Minnillo DR, Hagg T, Whittemore SR. Griffonia simplicifolia isolectin B4 identifies a specific subpopulation of angiogenic blood vessels following contusive spinal cord injury in the adult mouse. J Comp Neurol 2008; 507: 1031-52.
12. Bianchi M, Rossoni G, Sacerdote P, Panerai AE, Berti F. Effects of chlomipramine and fluoxetine on subcutaneous carrageenin-induced inflammation in the rat. Inflamm Res 1995; 44: 466-9.
13. Carlson SL, Parrish ME, Springer JE, Doty K, Dossett L. Acute inflammatory response in spinal cord following impact injury. Exp Neurol 1998; 151: 77-88.
14. Chang DI, Hosomi N, Lucero J, Heo JH, Abumiya T, Mazar AP, et al. Activation systems for latent matrix metalloproteinase-2 are upregulated immediately after focal cerebral ischemia. J Cereb Blood Flow Metab 2003; 23: 1408-19.
15. Chen X, Lan X, Roche I, Liu R, Geiger JD. Caffeine protects against MPTP-induced blood-brain barrier dysfunction in mouse striatum. J Neurochem 2008; 107: 1147-57.
16. Choi DC, Lee JY, Moon YJ, Kim SW, Oh TH, Yune TY. Acupuncture-mediated inhibition of inflammation facilitates significant functional recovery after spinal cord injury. Neurobiol Dis 2010; 39: 272-82.
17. Chung ES, Chung YC, Bok E, Baik HH, Park ES, Park JY, et al. Fluoxetine prevents LPS-induced degeneration of nigral dopaminergic neurons by inhibiting microglia-mediated oxidative stress. Brain Res 2010; 1363: 143-50.
18. Chung YC, Kim SR, Park JY, Chung ES, Park KW, Won SY, et al. Fluoxetine prevents MPTP-induced loss of dopaminergic neurons by inhibiting microglial activation. Neuropharmacology 2011; 60: 963-74.
19. Dam M, Tonin P, De BA, Pizzolato G, Casson S, Ermani M, et al. Effects of fluoxetine and maprotiline on functional recovery in poststroke hemiplegic patients undergoing rehabilitation therapy. Stroke 1996; 27: 1211-4.
20. Diamond M, Kelly JP, Connor TJ. Antidepressants suppress production of the Th1 cytokine interferon-gamma, independent of monoamine transporter blockade. Eur Neuropsychopharmacol 2006; 16: 481-90.
21. Fazzino F, Urbina M, Cedeno N, Lima L. Fluoxetine treatment to rats modifies serotonin transporter and cAMP in lymphocytes, CD4 + and CD8 + subpopulations and interleukins 2 and 4. Int Immunopharmacol 2009; 9: 463-7.
22. Feng S, Cen J, Huang Y, Shen H, Yao L, Wang Y, et al. Matrix metalloproteinase-2 and 9 secreted by leukemic cells increase the permeability of blood-brain barrier by disrupting tight junction proteins. PLoS One 2011; 6: e20599.
23. Fulcher YG, Van D Sr. Remote exosites of the catalytic domain of matrix metalloproteinase-12 enhance elastin degradation. Biochemistry 2011; 50: 9488-99.
24. Gainotti G. Origins, controversies and recent developments of the MCI construct. Curr Alzheimer Res 2010; 7: 271-9.
25. Gerzanich V, Woo SK, Vennekens R, Tsymbalyuk O, Ivanova S, Ivanov A, et al. De novo expression of Trpm4 initiates secondary hemorrhage in spinal cord injury. Nat Med 2009; 15: 185-91.
26. Ghirnikar RS, Lee YL, Eng LF. Chemokine antagonist infusion promotes axonal sparing after spinal cord contusion injury in rat. J Neurosci Res 2001; 64: 582-9.
27. Hamada Y, Ikata T, Katoh S, Nakauchi K, Niwa M, Kawai Y, et al. Involvement of an intercellular adhesion molecule 1-dependent pathway in the pathogenesis of secondary changes after spinal cord injury in rats. J Neurochem 1996; 66: 1525-31.
28. Hartung HP, Kieseier BC. The role of matrix metalloproteinases in autoimmune damage to the central and peripheral nervous system. J Neuroimmunol 2000; 107: 140-7.
29. Hawkins BT, Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 2005; 57: 173-85.
30. Heo JH, Lucero J, Abumiya T, Koziol JA, Copeland BR, del Zoppo GJ. Matrix metalloproteinases increase very early during experimental focal cerebral ischemia. J Cereb Blood Flow Metab 1999; 19: 624-33.
31. Higashida T, Kreipke CW, Rafols JA, Peng C, Schafer S, Schafer P, et al. The role of hypoxia-inducible factor-1alpha, aquaporin-4, and matrix metalloproteinase-9 in blood-brain barrier disruption and brain edema after traumatic brain injury. J Neurosurg 2011; 114: 92-101.
32. Horsfield SA, Rosse RB, Tomasino V, Schwartz BL, Mastropaolo J, Deutsch SI. Fluoxetine's effects on cognitive performance in patients with traumatic brain injury. Int J Psychiatry Med 2002; 32: 337-44.
33. Hosokawa T, Nakajima H, Doi Y, Sugino M, Kimura F, Hanafusa T, et al. Increased serum matrix metalloproteinase-9 in neuromyelitis optica: implication of disruption of blood-brain barrier. J Neuroimmunol 2011; 236: 81-6.
34. Hsu JY, McKeon R, Goussev S, Werb Z, Lee JU, Trivedi A, et al. Matrix metalloproteinase-2 facilitates wound healing events that promote functional recovery after spinal cord injury. J Neurosci 2006; 26: 9841-50.
35. Jin YJ, Park I, Hong IK, Byun HJ, Choi J, Kim YM, et al. Fibronectin and vitronectin induce AP-1-mediated matrix metalloproteinase-9 expression through integrin alpha(5)beta(1)/alpha(v)beta(3)-dependent Akt, ERK and JNK signaling pathways in human umbilical vein endothelial cells. Cell Signal 2011; 23: 125-34.
36. Karpus WJ, Ransohoff RM. Chemokine regulation of experimental autoimmune encephalomyelitis: temporal and spatial expression patterns govern disease pathogenesis. J Immunol 1998; 161: 2667-71.
37. Lee JY, Chung H, Yoo YS, Oh YJ, Oh TH, Park S, et al. Inhibition of apoptotic cell death by ghrelin improves functional recovery after spinal cord injury. Endocrinology 2010; 151: 3815-26.
38. Li XQ, Wang HM, Yang CG, Zhang XH, Han DD, Wang HL. Fluoxetine inhibited extracellular matrix of pulmonary artery and inflammation of lungs in monocrotaline-treated rats. Acta Pharmacol Sin 2011; 32: 217-22.
39. Lim CM, Kim SW, Park JY, Kim C, Yoon SH, Lee JK. Fluoxetine affords robust neuroprotection in the postischemic brain via its antiinflammatory effect. J Neurosci Res 2009; 87: 1037-45.
40. Liu W, Hendren J, Qin XJ, Shen J, Liu KJ. Normobaric hyperoxia attenuates early blood-brain barrier disruption by inhibiting MMP-9-mediated occludin degradation in focal cerebral ischemia. J Neurochem 2009; 108: 811-20.
41. Mabon PJ, Weaver LC, Dekaban GA. Inhibition of monocyte/macrophage migration to a spinal cord injury site by an antibody to the integrin alphaD: a potential new anti-inflammatory treatment. Exp Neurol 2000; 166: 52-4.
42. McTigue DM, Tani M, Krivacic K, Chernosky A, Kelner GS, Maciejewski D, et al. Selective chemokine mRNA accumulation in the rat spinal cord after contusion injury. J Neurosci Res 1998; 53: 368-76.
43. Miyazaki K, Ohta Y, Nagai M, Morimoto N, Kurata T, Takehisa Y, et al. Disruption of neurovascular unit prior to motor neuron degeneration in amyotrophic lateral sclerosis. J Neurosci Res 2011; 89: 718-28.
44. Mun-Bryce S, Rosenberg GA. Gelatinase B modulates selective opening of the blood-brain barrier during inflammation. Am J Physiol 1998a; 274: R1203-11.
45. Mun-Bryce S, Rosenberg GA. Matrix metalloproteinases in cerebrovascular disease. J Cereb Blood Flow Metab 1998b; 18: 1163-72.
46. Noble LJ, Donovan F, Igarashi T, Goussev S, Werb Z. Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events. J Neurosci 2002; 22: 7526-35.
47. Noble LJ, Wrathall JR. Distribution and time course of protein extravasation in the rat spinal cord after contusive injury. Brain Res 1989; 482: 57-66.
48. Okada S, Nakamura M, Mikami Y, Shimazaki T, Mihara M, Ohsugi Y, et al. Blockade of interleukin-6 receptor suppresses reactive astrogliosis and ameliorates functional recovery in experimental spinal cord injury. J Neurosci Res 2004; 76: 265-76.
49. Ousman SS, David S. MIP-1alpha, MCP1, GM-CSF, and TNF-alpha control the immune cell response that mediates rapid phagocytosis of myelin from the adult mouse spinal cord. J Neurosci 2001; 21: 4649-56.
50. Pariente J, Loubinoux I, Carel C, Albucher JF, Leger A, Manelfe C, et al. Fluoxetine modulates motor performance and cerebral activation of patients recovering from stroke. Ann Neurol 2001; 50: 718-29.
51. Pellegrino TC, Bayer BM. Role of central 5-HT(2) receptors in fluoxetine-induced decreases in T lymphocyte activity. Brain Behav Immun 2002; 16: 87-103.
52. Popovich PG, van RN, Hickey WF, Preidis G, McGaughy V. Hematogenous macrophages express CD8 and distribute to regions of lesion cavitation after spinal cord injury. Exp Neurol 2003; 182: 275-87.
53. Rosenberg GA. Matrix metalloproteinases in neuroinflammation. Glia 2002; 39: 279-91.
54. Rosenberg GA, Dencoff JE, McGuire PG, Liotta LA, Stetler-Stevenson WG. Injury-induced 92-kilodalton gelatinase and urokinase expression in rat brain. Lab Invest 1994; 71: 417-22.
55. Rosenberg GA, Estrada EY, Dencoff JE. Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 1998; 29: 2189-95.
56. Rosenberg GA, Estrada EY, Dencoff JE, Stetler-Stevenson WG. Tumor necrosis factor-alpha-induced gelatinase B causes delayed opening of the blood-brain barrier: an expanded therapeutic window. Brain Res 1995; 703: 151-5.
57. Rosenberg GA, Navratil M. Metalloproteinase inhibition blocks edema in intracerebral hemorrhage in the rat. Neurology 1997; 48: 921-6.
58. Roumestan C, Michel A, Bichon F, Portet K, Detoc M, Henriquet C, et al. Anti-inflammatory properties of desipramine and fluoxetine. Respir Res 2007; 8: 35.
59. Saiwai H, Ohkawa Y, Yamada H, Kumamaru H, Harada A, Okano H, et al. The LTB4-BLT1 axis mediates neutrophil infiltration and secondary injury in experimental spinal cord injury. Am J Pathol 2010; 176: 2352-66.
60. Simard JM, Tsymbalyuk O, Ivanov A, Ivanova S, Bhatta S, Geng Z, et al. Endothelial sulfonylurea receptor 1-regulated NC Ca-ATP channels mediate progressive hemorrhagic necrosis following spinal cord injury. J Clin Invest 2007; 117: 2105-13.
61. Simard JM, Woo SK, Norenberg MD, Tosun C, Chen Z, Ivanova S, et al. Brief suppression of Abcc8 prevents autodestruction of spinal cord after trauma. Sci Transl Med 2010; 2: 28ra29.
62. Sixt M, Engelhardt B, Pausch F, Hallmann R, Wendler O, Sorokin LM. Endothelial cell laminin isoforms, laminins 8 and 10, play decisive roles in T cell recruitment across the blood-brain barrier in experimental autoimmune encephalomyelitis. J Cell Biol 2001; 153: 933-46.
63. Sounvoravong S, Nakashima MN, Wada M, Nakashima K. Modification of antiallodynic and antinociceptive effects of morphine by peripheral and central action of fluoxetine in a neuropathic mice model. Acta Biol Hung 2007; 58: 369-79.
64. Sternlicht MD, Lochter A, Sympson CJ, Huey B, Rougier JP, Gray JW, et al. The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell 1999; 98: 137-46.
65. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001; 17: 463-516.
66. Stirling DP, Yong VW. Dynamics of the inflammatory response after murine spinal cord injury revealed by flow cytometry. J Neurosci Res 2008; 86: 1944-58.
67. Tahanian E, Sanchez LA, Shiao TC, Roy R, Annabi B. Flavonoids targeting of IkappaB phosphorylation abrogates carcinogen-induced MMP9 and COX2 expression in human brain endothelial cells. Drug Des Devel Ther 2011; 5: 299-309.
68. Taoka Y, Okajima K, Uchiba M, Murakami K, Kushimoto S, Johno M, et al. Role of neutrophils in spinal cord injury in the rat. Neuroscience 1997; 79: 1177-82.
69. Tian DS, Liu JL, Xie MJ, Zhan Y, Qu WS, Yu ZY, et al. Tamoxifen attenuates inflammatory-mediated damage and improves functional outcome after spinal cord injury in rats. J Neurochem 2009; 109: 1658-67.
70. Toft-Hansen H, Buist R, Sun XJ, Schellenberg A, Peeling J, Owens T. Metalloproteinases control brain inflammation induced by pertussis toxin in mice overexpressing the chemokine CCL2 in the central nervous system. J Immunol 2006; 177: 7242-9.
71. Utepbergenov DI, Mertsch K, Sporbert A, Tenz K, Paul M, Haseloff RF, et al. Nitric oxide protects blood-brain barrier in vitro from hypoxia/ reoxygenation-mediated injury. FEBS Lett 1998; 424: 197-201.
72. Wasserman JK, Schlichter LC. Minocycline protects the blood-brain barrier and reduces edema following intracerebral hemorrhage in the rat. Exp Neurol 2007; 207: 227-37.
73. Wells JE, Rice TK, Nuttall RK, Edwards DR, Zekki H, Rivest S, et al. An adverse role for matrix metalloproteinase 12 after spinal cord injury in mice. J Neurosci 2003; 23: 10107-15.
74. Werb Z. ECM and cell surface proteolysis: regulating cellular ecology. Cell 1997; 91: 439-42.
75. Wiart L, Petit H, Joseph PA, Mazaux JM, Barat M. Fluoxetine in early poststroke depression: a double-blind placebo-controlled study. Stroke 2000; 31: 1829-32.
76. Wu C, Ivars F, Anderson P, Hallmann R, Vestweber D, Nilsson P, et al. Endothelial basement membrane laminin alpha5 selectively inhibits T lymphocyte extravasation into the brain. Nat Med 2009; 15: 519-27.
77. Xu J, Kim GM, Ahmed SH, Xu J, Yan P, Xu XM, et al. Glucocorticoid receptor-mediated suppression of activator protein-1 activation and matrix metalloproteinase expression after spinal cord injury. J Neurosci 2001; 21: 92-7.
78. 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.
79. Yong C, Arnold PM, Zoubine MN, Citron BA, Watanabe I, Berman NE, et al. Apoptosis in cellular compartments of rat spinal cord after severe contusion injury. J Neurotrauma 1998; 15: 459-72.
80. Yu F, Kamada H, Niizuma K, Endo H, Chan PH. Induction of mmp-9 expression and endothelial injury by oxidative stress after spinal cord injury. J Neurotrauma 2008; 25: 184-95.
81. Yune TY, Lee JY, Cui CM, Kim HC, Oh TH. Neuroprotective effect of Scutellaria baicalensis on spinal cord injury in rats. J Neurochem 2009; 110: 1276-87.
82. Yune TY, Lee JY, Jung GY, Kim SJ, Jiang MH, Kim YC, et al. Minocycline alleviates death of oligodendrocytes by inhibiting pro-nerve growth factor production in microglia after spinal cord injury. J Neurosci 2007; 27: 7751-61.
83. Yune TY, Lee SM, Kim SJ, Park HK, Oh YJ, Kim YC, et al. Manganese superoxide dismutase induced by TNF-beta is regulated transcriptionally by NF-kappaB after spinal cord injury in rats. J Neurotrauma 2004; 21: 1778-94.
84. Zhang H, Trivedi A, Lee JU, Lohela M, Lee SM, Fandel TM, et al. Matrix metalloproteinase-9 and stromal cell-derived factor-1 act synergistically to support migration of blood-borne monocytes into the injured spinal cord. J Neurosci 2011; 31: 15894-903.
85. Zlokovic BV. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008; 57: 178-201.