MMP-3 secreted from endothelial cells of blood vessels after spinal cord injury activates microglia, leading to oligodendrocyte cell death

Neurobiology of Disease

Volumn 82, Issue , 2015, Pages 141-151

  Lee, Jee Y ^a   Choi, Hae Y ^a   Yune, Tae Y ^a  

^a Kyung Hee University Hospital   (South Korea)

Author keywords

Matrix metalloprotease 3; Microglia; Oligodendrocyte; RhoA; Spinal cord injury

Indexed keywords

GHRELIN; GHRELIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE P38; NERVE GROWTH FACTOR; PRO NERVE GROWTH FACTOR; PROTEIN C JUN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; STROMELYSIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME RELEASE; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROGLIA; MOUSE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SPINAL CORD INJURY; WILD TYPE; ANIMAL; CELL DEATH; CELL LINE; DRUG EFFECTS; METABOLISM; NERVE CELL; PATHOLOGY; PHYSIOLOGY; SECRETION (PROCESS); VASCULAR ENDOTHELIUM;

ANIMALS; CELL DEATH; CELL LINE; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GHRELIN; MATRIX METALLOPROTEINASE 3; MICE; MICROGLIA; NERVE GROWTH FACTORS; NEURONS; OLIGODENDROGLIA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; SPINAL CORD INJURIES;

EID: 84935024049     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2015.06.002     Document Type: Article

References (59)

1. Beattie M.S. Inflammation and apoptosis: linked therapeutic targets in spinal cord injury. Trends Mol. Med. 2004, 10:580-583.
2. Beattie M.S., Farooqui A.A., Bresnahan J.C. Review of current evidence for apoptosis after spinal cord injury. J. Neurotrauma 2000, 17:915-925.
3. Beattie M.S., Harrington A.W., Lee R., Kim J.Y., Boyce S.L., Longo F.M., Bresnahan J.C., Hempstead B.L., Yoon S.O. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 2002, 36:375-386.
4. Beattie M.S., Hermann G.E., Rogers R.C., Bresnahan J.C. Cell death in models of spinal cord injury. Prog. Brain Res. 2002, 137:37-47.
5. Blasi E., Barluzzi R., Bocchini V., Mazzolla R., Bistoni F. Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J. Neuroimmunol. 1990, 27:229-237.
6. Block M.L., Hong J.S. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 2005, 76:77-98.
7. Casha S., Yu W.R., Fehlings M.G. Oligodendroglial apoptosis occurs along degenerating axons and is associated with FAS and p75 expression following spinal cord injury in the rat. Neuroscience 2001, 103:203-218.
8. Casha S., Yu W.R., Fehlings M.G. Oligodendroglial apoptosis occurs along degenerating axons and is associated with FAS and p75 expression following spinal cord injury in the rat. Neuroscience 2001, 103:203-218.
9. Chatzipanteli K., Garcia R., Marcillo A.E., Loor K.E., Kraydieh S., Dietrich W.D. Temporal and segmental distribution of constitutive and inducible nitric oxide synthases after traumatic spinal cord injury: effect of aminoguanidine treatment. J. Neurotrauma 2002, 19:639-651.
10. Choi D.C., Lee J.Y., Moon Y.J., Kim S.W., Oh T.H., Yune T.Y. Acupuncture-mediated inhibition of inflammation facilitates significant functional recovery after spinal cord injury. Neurobiol. Dis. 2010, 39:272-282.
11. Cunningham C. Microglia and neurodegeneration: the role of systemic inflammation. Glia 2013, 61:71-90.
12. Dubreuil C.I., Winton M.J., McKerracher L. Rho activation patterns after spinal cord injury and the role of activated Rho in apoptosis in the central nervous system. J. Cell Biol. 2003, 162:233-243.
13. Gris D., Marsh D.R., Oatway M.A., Chen Y., Hamilton E.F., Dekaban G.A., Weaver L.C. Transient blockade of the CD11d/CD18 integrin reduces secondary damage after spinal cord injury, improving sensory, autonomic, and motor function. J. Neurosci. 2004, 24:4043-4051.
14. Hains B.C., Waxman S.G. Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J. Neurosci. 2006, 26:4308-4317.
15. Jiang H., Li L.J., Wang J., Xie J.X. Ghrelin antagonizes MPTP-induced neurotoxicity to the dopaminergic neurons in mouse substantia nigra. Exp. Neurol. 2008, 212:532-537.
16. Kim Y.S., Kim S.S., Cho J.J., Choi D.H., Hwang O., Shin D.H., Chun H.S., Beal M.F., Joh T.H. Matrix metalloproteinase-3: a novel signaling proteinase from apoptotic neuronal cells that activates microglia. J. Neurosci. 2005, 25:3701-3711.
17. Kim Y.S., Choi D.H., Block M.L., Lorenzl S., Yang L., Kim Y.J., Sugama S., Cho B.P., Hwang O., Browne S.E., Kim S.Y., Hong J.S., Beal M.F., Joh T.H. A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation. FASEB J. 2007, 21:179-187.
18. Koistinaho M., Koistinaho J. Role of p38 and p44/42 mitogen-activated protein kinases in microglia. Glia 2002, 40:175-183.
19. Lee J.Y., Yune T.Y. Ghrelin inhibits oligodendrocyte cell death by attenuating microglial activation. Endocrinol. Metab. (Seoul) 2014, 29:371-378.
20. Lee J., Lim E., Kim Y., Li E., Park S. Ghrelin attenuates kainic acid-induced neuronal cell death in the mouse hippocampus. J. Endocrinol. 2010, 205:263-270.
21. Lee J.Y., Chung H., Yoo Y.S., Oh Y.J., Oh T.H., Park S., Yune T.Y. Inhibition of apoptotic cell death by ghrelin improves functional recovery after spinal cord injury. Endocrinology 2010, 151:3815-3826.
22. Lee J.Y., Choi S.Y., Oh T.H., Yune T.Y. 17beta-Estradiol inhibits apoptotic cell death of oligodendrocytes by inhibiting RhoA-JNK3 activation after spinal cord injury. Endocrinology 2012, 153:3815-3827.
23. Lee J.Y., Kim H.S., Choi H.Y., Oh T.H., Yune T.Y. Fluoxetine inhibits matrix metalloprotease activation and prevents disruption of blood-spinal cord barrier after spinal cord injury. Brain 2012, 135:2375-2389.
24. Lee S., Kim Y., Li E., Park S. Ghrelin protects spinal cord motoneurons against chronic glutamate excitotoxicity by inhibiting microglial activation. Korean J. Physiol. Pharmacol. 2012, 16:43-48.
25. Lee J.Y., Choi H.Y., Ahn H.J., Ju B.G., Yune T.Y. Matrix metalloproteinase-3 promotes early blood-spinal cord barrier disruption and hemorrhage and impairs long-term neurological recovery after spinal cord injury. Am. J. Pathol. 2014, 184:2985-3000.
26. Lee J.Y., Choi H.Y., Na W.H., Ju B.G., Yune T.Y. Ghrelin inhibits BSCB disruption/hemorrhage by attenuating MMP-9 and SUR1/TrpM4 expression and activation after spinal cord injury. Biochim. Biophys. Acta 2014, 1842:2403-2412.
27. Lim E., Lee S., Li E., Kim Y., Park S. Ghrelin protects spinal cord motoneurons against chronic glutamate-induced excitotoxicity via ERK1/2 and phosphatidylinositol-3-kinase/Akt/glycogen synthase kinase-3beta pathways. Exp. Neurol. 2011, 230:114-122.
28. Lu W.H., Wang C.Y., Chen P.S., Wang J.W., Chuang D.M., Yang C.S., Tzeng S.F. Valproic acid attenuates microgliosis in injured spinal cord and purinergic P2X4 receptor expression in activated microglia. J. Neurosci. Res. 2013, 91:694-705.
29. Maeda A., Sobel R.A. Matrix metalloproteinases in the normal human central nervous system, microglial nodules, and multiple sclerosis lesions. J. Neuropathol. Exp. Neurol. 1996, 55:300-309.
30. Miao Y., Xia Q., Hou Z., Zheng Y., Pan H., Zhu S. Ghrelin protects cortical neuron against focal ischemia/reperfusion in rats. Biochem. Biophys. Res. Commun. 2007, 359:795-800.
31. Moon M., Kim H.G., Hwang L., Seo J.H., Kim S., Hwang S., Kim S., Lee D., Chung H., Oh M.S., Lee K.T., Park S. Neuroprotective effect of ghrelin in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson's disease by blocking microglial activation. Neurotox. Res. 2009, 15:332-347.
32. Moon M., Choi J.G., Nam D.W., Hong H.S., Choi Y.J., Oh M.S., Mook-Jung I. Ghrelin ameliorates cognitive dysfunction and neurodegeneration in intrahippocampal amyloid-beta1-42 oligomer-injected mice. J. Alzheimers Dis. 2011, 23:147-159.
33. Moon Y.J., Lee J.Y., Oh M.S., Pak Y.K., Park K.S., Oh T.H., Yune T.Y. Inhibition of inflammation and oxidative stress by Angelica dahuricae radix extract decreases apoptotic cell death and improves functional recovery after spinal cord injury. J. Neurosci. Res. 2012, 90:243-256.
34. onso de L.M., Egido J.A. Estrogens as neuroprotectants against ischemic stroke. Cerebrovasc. Dis. 2006, 21(Suppl. 2):48-53.
35. Popovich P.G., Wei P., Stokes B.T. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J. Comp. Neurol. 1997, 377:443-464.
36. Popovich P.G., Guan Z., McGaughy V., Fisher L., Hickey W.F., Basso D.M. The neuropathological and behavioral consequences of intraspinal microglial/macrophage activation. J. Neuropathol. Exp. Neurol. 2002, 61:623-633.
37. Qin L., Liu Y., Cooper C., Liu B., Wilson B., Hong J.S. Microglia enhance beta-amyloid peptide-induced toxicity in cortical and mesencephalic neurons by producing reactive oxygen species. J. Neurochem. 2002, 83:973-983.
38. Reitz C., van Rooij F.J., Soares H.D., de Maat M.P., Hofman A., Witteman J.C., Breteler M.M. Matrix metalloproteinase 3 haplotypes and plasma amyloid beta levels: the Rotterdam Study. Neurobiol. Aging 2010, 31:715-718.
39. Ryu J., Pyo H., Jou I., Joe E. Thrombin induces NO release from cultured rat microglia via protein kinase C, mitogen-activated protein kinase, and NF-kappa B. J. Biol. Chem. 2000, 275:29955-29959.
40. Shigemoto-Mogami Y., Koizumi S., Tsuda M., Ohsawa K., Kohsaka S., Inoue K. Mechanisms underlying extracellular ATP-evoked interleukin-6 release in mouse microglial cell line, MG-5. J. Neurochem. 2001, 78:1339-1349.
41. Springer J.E., Azbill R.D., Knapp P.E. Activation of the caspase-3 apoptotic cascade in traumatic spinal cord injury. Nat. Med. 1999, 5:943-946.
42. Sternlicht M.D., Werb Z. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 2001, 17:463-516.
43. Sternlicht M.D., Lochter A., Sympson C.J., Huey B., Rougier J.P., Gray J.W., Pinkel D., Bissell M.J., Werb Z. The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell 1999, 98:137-146.
44. Stirling D.P., Khodarahmi K., Liu J., McPhail L.T., McBride C.B., Steeves J.D., Ramer M.S., Tetzlaff W. Minocycline treatment reduces delayed oligodendrocyte death, attenuates axonal dieback, and improves functional outcome after spinal cord injury. J. Neurosci. 2004, 24:2182-2190.
45. Taoka Y., Okajima K., Uchiba M., Murakami K., Kushimoto S., Johno M., Naruo M., Okabe H., Takatsuki K. Role of neutrophils in spinal cord injury in the rat. Neuroscience 1997, 79:1177-1182.
46. Tian D.S., Dong Q., Pan D.J., He Y., Yu Z.Y., Xie M.J., Wang W. Attenuation of astrogliosis by suppressing of microglial proliferation with the cell cycle inhibitor olomoucine in rat spinal cord injury model. Brain Res. 2007, 1154:206-214.
47. Trang T., Beggs S., Wan X., Salter M.W. P2X4-receptor-mediated synthesis and release of brain-derived neurotrophic factor in microglia is dependent on calcium and p38-mitogen-activated protein kinase activation. J. Neurosci. 2009, 29:3518-3528.
48. Valluru L., Diao Y., Hachmeister J.E., Liu D. Mn (III) tetrakis (4-benzoic acid) porphyrin protects against neuronal and glial oxidative stress and death after spinal cord injury. CNS Neurol. Disord. Drug Targets 2012, 11:774-790.
49. Walker E.J., Rosenberg G.A. TIMP-3 and MMP-3 contribute to delayed inflammation and hippocampal neuronal death following global ischemia. Exp. Neurol. 2009, 216:122-131.
50. Wang X., Arcuino G., Takano T., Lin J., Peng W.G., Wan P., Li P., Xu Q., Liu Q.S., Goldman S.A., Nedergaard M. P2X7 receptor inhibition improves recovery after spinal cord injury. Nat. Med. 2004, 10:821-827.
51. Warden P., Bamber N.I., Li H., Esposito A., Ahmad K.A., Hsu C.Y., Xu X.M. Delayed glial cell death following Wallerian degeneration in white matter tracts after spinal cord dorsal column cordotomy in adult rats. Exp. Neurol. 2001, 168:213-224.
52. Werb Z. ECM and cell surface proteolysis: regulating cellular ecology. Cell 1997, 91:439-442.
53. Wilms H., Rosenstiel P., Sievers J., Deuschl G., Zecca L., Lucius R. Activation of microglia by human neuromelanin is NF-kappaB dependent and involves p38 mitogen-activated protein kinase: implications for Parkinson's disease. FASEB J. 2003, 17:500-502.
54. Xu J.T., Xin W.J., Wei X.H., Wu C.Y., Ge Y.X., Liu Y.L., Zang Y., Zhang T., Li Y.Y., Liu X.G. p38 activation in uninjured primary afferent neurons and in spinal microglia contributes to the development of neuropathic pain induced by selective motor fiber injury. Exp. Neurol. 2007, 204:355-365.
55. Yu W.R., Fehlings M.G. Fas/FasL-mediated apoptosis and inflammation are key features of acute human spinal cord injury: implications for translational, clinical application. Acta Neuropathol. 2011, 122:747-761.
56. Yune T.Y., Chang M.J., Kim S.J., Lee Y.B., Shin S.W., Rhim H., Kim Y.C., Shin M.L., Oh Y.J., Han C.T., Markelonis G.J., Oh T.H. Increased production of tumor necrosis factor-alpha induces apoptosis after traumatic spinal cord injury in rats. J. Neurotrauma 2003, 20:207-219.
57. Yune T.Y., Lee J.Y., Jung G.Y., Kim S.J., Jiang M.H., Kim Y.C., Oh Y.J., Markelonis G.J., Oh T.H. Minocycline alleviates death of oligodendrocytes by inhibiting pro-nerve growth factor production in microglia after spinal cord injury. J. Neurosci. 2007, 27:7751-7761.
58. Yune T.Y., Lee J.Y., Cui C.M., Kim H.C., Oh T.H. Neuroprotective effect of Scutellaria baicalensis on spinal cord injury in rats. J. Neurochem. 2009, 110:1276-1287.
59. Zhang W., Wang T., Pei Z., Miller D.S., Wu X., Block M.L., Wilson B., Zhang W., Zhou Y., Hong J.S., Zhang J. Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson's disease. FASEB J. 2005, 19:533-542.