An Adverse Role for Matrix Metalloproteinase 12 after Spinal Cord Injury in Mice

Journal of Neuroscience

Volumn 23, Issue 31, 2003, Pages 10107-10115

  Wells, Jennifer E A ^a   Rice, Tiffany K ^a   Nuttall, Robert K ^b   Edwards, Dylan R ^b   Zekki, Hakima ^c   Rivest, Serge ^c   Yong, V Wee ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^c UNIVERSITÉ LAVAL   (Canada)

Author keywords

Metalloproteinase; Microglia; Neuroinflammation; Recovery; Spinal cord injury; Trauma

Indexed keywords

COMPLEMENTARY DNA; MACROPHAGE ELASTASE; RNA;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HINDLIMB; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INFLAMMATION; LOCOMOTION; MICROGLIA; MOUSE; MUSCLE STRENGTH; NEUROPATHOLOGY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD COMPRESSION; SPINAL CORD INJURY;

EID: 0242442568     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-31-10107.2003     Document Type: Article

References (71)

1. Arber S, Caroni P (1995) Thrombospondin-4, an extracellular matrix protein expressed in the developing and adult nervous system promotes neurite outgrowth. J Cell Biol 131:1083-1094.
2. Banda MJ, Werb Z (1981) Mouse macrophage elastase: purification and characterization as a metalloproteinase. Biochem J 193:589.
3. Basso DM, Beattie MS, Bresnahan JC (1995) A sensitive and reliable locomotor rating scale for open-field testing in rats. J Neurotrauma 12:1-21.
4. Batchelor PE, Liberatore GT, Wong JYF, Porritt MJ, Frerichs F, Donnan GA, Howells DW (1999) Activated macrophages and microglia induce dopaminergic sprouting in the injured striatum and express brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor. J Neurosci 19:1708-1716.
5. Blight AR (1983) Cellular morphology of chronic spinal cord injury in the cat: analysis of myelinated axons by line. Neuroscience 10:541-543.
6. Blight AR (1994) Effects of silica on the outcome from experimental spinal cord injury: implication of macrophages in secondary tissue damage. Neuroscience 60:263-273.
7. Bodey B, Bodey BJ, Siegel SE, Kaiser HE (2000a) Matrix metalloproteinase expression in childhood astrocytomas. Anticancer Res 20:3287-3292.
8. Bodey B, Bodey BJ, Siegel SE, Kaiser HE (2000b) Significant differences in the matrix metalloproteinase expression profiles of spontaneous medulloblastomas/primitive neuroectodermal tumors as compared with their xenografted, established tumor cell line derived counterparts. In Vivo 14:675-682.
9. Chamak B, Morandi V, Mallat M (1994) Brain macrophages stimulate neurite growth and regeneration by secreting thrombospondin. J Neurosci Res 38:221-233.
10. Curci JA, Liao S, Huffman MD, Shapiro SD, Thompson RW (1998) Expression and localization of macrophage elastase (matrix metalloproteinase-12) in abdominal aortic aneurysms. J Clin Invest 102:1900-1910.
11. D'Haese A, Wuyts A, Dillen C, Dubois B, Billiau A, Heremans H, Van Damme J, Arnold B, Opdenakker G (2000) In vivo neutrophil recruitment by granulocyte chemotactic protein-2 is assisted by gelatinase B/MMP-9 in the mouse. J Interferon Cytokine Res 20:667-674.
12. Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22:391-397.
13. Dusart I, Schwab ME (1994) Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur J Neurosci 6:712-724.
14. Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2:161-174.
15. Eidelberg E, Straehley D, Erspamer R, Watkins C (1977) Relationship between residual hindlimb-assisted locomotion and surviving axons after incomplete spinal cord injuries. Exp Neurol 56:312-322.
16. Fehlings MG, Tator CH (1992) The effect of direct current field polarity on recovery after acute experimental spinal cord injury. Brain Res 579:32-42.
17. Frolichsthal-Schoeller P, Vescovi AL, Krekoski CA, Murphy G, Edwards DR, Forsyth P (1999) Expression and modulation of matrix metalloproteinase-2 and tissue inhibitors of metalloproteinases in human embryonic CNS stem cells. NeuroReport 10:345-351.
18. Giulian D, Corpuz M (1993) Microglial secretion products and their impact on the nervous system. Adv Neurol 59:315-320.
19. Giulian D, Robertson C (1990) Inhibition of mononuclear phagocytes reduces ischemic injury in the spinal cord. Ann Neurol 27:33-42.
20. Giulian D, Vaca K (1993) Inflammatory glia mediate delayed neuronal damage after ischemia in the central nervous system. Stroke 24:184-190.
21. Giulian D, Corpuz M, Chapman S, Mansouri M, Robertson C (1993) Reactive mononuclear phagocytes release neurotoxins after ischemic and traumatic injury to the central nervous system. J Neurosci Res 36:681-693.
22. Guth L, Zhang Z, DiProspero NA, Joubin K, Fitch MT (1994) Spinal cord injury in the rat: treatment with bacterial lipopolysaccharide and indomethacin enhances cellular repair and locomotor function. Exp Neurol 126:76-87.
23. Hartung HP, Kieseier BC (2000) The role of matrix metalloproteinases in autoimmune damage to the central and peripheral nervous system. J Neuroimmunol 107:140-147.
24. Hautamaki RD, Kobayashi DK, Senior SD, Shapiro SD (1997) Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 277:2002-2004.
25. Herx LM, Yong VW (2001) Interleukin-1 beta is required for the early evolution of reactive astrogliosis following CNS lesion. J Neuropathol Exp Neurol 60:961-971.
26. Herx LM, Rivest S, Yong VW (2000) Central nervous system initiated inflammation and neurotrophism in trauma: IL-1β is required for the production of ciliary neurotrophic factor. J Immunol 165:2232-2239.
27. Horton MR, Shapiro SD, Bao C, Lowenstein CJ, Noble PW (1999) Induction and regulation of macrophage metalloelastase by hyaluronan fragments in mouse macrophages. J Immunol 162:4171-4176.
28. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S (1998) Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 57:1-9.
29. Johnston JB, Zhang K, Silva C, Shalinsky DR, Conant K, Ni W, Corbett D, Yong VW, Power C (2001) HIV-1 Tat neurotoxicity is prevented by matrix metalloproteinase inhibitors. Ann Neurol 49:230-241.
30. Jonakait GM, Luskin MB, Wei R, Tian XF, Ni L (1996) Conditioned medium from activated microglia promotes cholinergic differentiation in the basal forebrain in vitro. Dev Biol 177:85-95.
31. Kim WK, Ko KH (1998) Potentiation of N-methyl-D-aspartate-mediated neurotoxicity by immunostimulated murine microglia. J Neurosci Res 54:17-26.
32. Knauper V, Murphy G, Tschesche H (1996) Activation of human neutrophil procollagenase by stromelysin 2. Eur J Biochem 235:187-191.
33. Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312-318.
34. Lanone S, Zheng T, Liu W, Lee CG, Ma B, Chen Q, Homer RJ, Wang J, Rabach LA, Rabach ME, Shipley JM, Shapiro SD, Senior RM, Elias JA (2002) Overlapping and enzyme-specific contributions of matrix metalloproteinases-9 and -12 in IL-13-induced inflammation and remodeling. J Clin Invest 110:463-474.
35. Leong SK, Ling EA (1992) Amoeboid and ramified microglia: their interrelationship and response to brain injury. Glia 6:39-47.
36. Lo EH, Wang X, Cuzner ML (2002) Extracellular proteolysis in brain injury and inflammation: role for plasminogen activators and matrix metalloproteinases. J Neurosci Res 69:1-9.
37. Mabon PJ, Weaver LC, Dekaban GA (2000) Inhibition of monocyte/macrophage migration to a spinal cord injury site by an antibody to the integrin αD: a potential new anti-inflammatory treatment. Exp Neurol 166:52-64.
38. McCawley LJ, Matrisian LM (2001) Matrix metalloproteinases: they're not just for matrix anymore. Curr Opin Cell Biol 13:534-540.
39. Mo'rioka T, Kalehua AN, Streit WJ (1991) The microglial reaction in the rat dorsal hippocampus following transient forebrain ischemia. J Cereb Blood Flow Metab 11:966-973.
40. Muller D, Breathnach R, Englemann A, Millon R, Bronner G, Flesch H, Dumont P, EberM, Abecassis J (1991) Expression of collagenase-related metalloproteinase genes in human lung or head and neck tumours. Int J Cancer 48:550-556.
41. Nagata A, Takei K, Nakajima K, Saito H, Kohsaka S (1993) Microglial conditioned medium promotes survival and development of cultured mesencephalic neurons from embryonic rat brain. J Neurosci Res 34:357-363.
42. Nakamura H, Fujii Y, Ohuchi E, Yamamoto E, Okada Y (1998) Activation of the precursor of human stromelysin 2 and its interaction with other matrix metalloproteinases. Eur J Biochem 253:67-75.
43. Nicholson R, Murphy G, Breathnach R (1989) Human and rat malignant-tumor-associated mRNAs encode stromelysin-like metalloproteinases. Biochemistry 28:5195-5203.
44. Noble LJ, Donovan F, Igarashi T, Goussev S, Werb Z (2002) Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events. J Neurosci 22:7526-7535.
45. Nuttall RK, Pennington CJ, Taplin J, Wheal A, Yong VW, Forsyth PA, Edwards DR (2003) Elevated membrane-type matrix metalloproteinases in gliomas revealed by profiling proteases and inhibitors in human cancer cells. Mol Cancer Res 1:333-345.
46. Oh LY, Larsen PH, Krekoski CA, Edwards DR, Donovan F, Werb Z, Yong VW (1999) Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocytes. J Neurosci 19:8464-8475.
47. O'Shea KS, Liu LH, Dixit VM (1991) Thrombospondin and a 140 kD fragment promote adhesion and neurite outgrowth from embryonic central and peripheral neurons and PC12 cells. Neuron 7:231-237.
48. Pagenstecher A, Stalder AK, Campbell IL (1997) RNAse protection assays for the simultaneous and semiquantitative analysis of multiple murine matrix metalloproteinase (MMP) and MMP inhibitor mRNAs. J Immunol Methods 206:1-9.
49. Pittman RN (1985) Release of plasminogen activator and a calcium-dependent metalloproteinase from cultured sympathetic and sensory neurons. Dev Biol 110:91-101.
50. Popovich PG, Guan Z, Wei P, Huitinga I, van Rooijen N, Stokes BT (1999) Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp Neurol 158:351-365.
51. Power C, Henry S, Del Bigio MR, Larsen PH, Corbett D, Imai Y, Yong VW, Peeling J (2003) Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann Neurol 53:731-742.
52. Rabchevsky AG, Streit WJ (1997) Grafting of cultured microglial cells into the lesioned spinal cord of adult rats enhances neurite outgrowth. J Neurosci Res 47:34-48.
53. Rapalino O, Lazarov-Spiegler O, Agranov E, Velan GJ, Yoles E, Fraidakis M, Solomon A, Gepstein R, Katz A, Belkin M, Handani M, Schwartz M (1998) Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats. Nat Med 4:814-821.
54. Rogove AD, Tsirka SE (1998) Neurotoxic responses by microglia elicited by excitotoxic injury in the mouse hippocampus. Curr Biol 8:19-25.
55. Rosenberg GA (2002) Matrix metalloproteinases in neuroinflammation. Glia 39:279-291.
56. Rostworowski M, Balasingam V, Chabot S, Owens T, Yong VW (1997) Astrogliosis in the neonatal and adult murine brain post-trauma: elevation of inflammatory cytokines and the lack of requirement for endogenous interferon-γ. J Neurosci 17:3664-3674.
57. Rothwell NJ, Luheshi G, Toulmond S (1996) Cytokines and their receptors in the central nervous system: physiology, pharmacology, and pathology. Pharmacol Ther 69:85-95.
58. Saghizadeh M, Brown DJ, Castellon R, Chwa M, Huang GH, Ljubimova JY, Rosenberg S, Spirin KS, Stoilitenko RB, Adachi W, Kinoshita S, Murphy G, Windsor LJ, Kenney MC, Ljubimov AV (2001) Overexpression of matrix metalloproteinase-10 and matrix metalloproteinase-3 in human diabetic corneas. Am J Pathol 158:723-734.
59. Shapiro SD, Kobayashi DK, Ley TJ (1993) Cloning and characterization of a unique elastolytic metalloproteinase produced by human alveolar macrophages. J Biol Chem 268:23824-23829.
60. Sheffield JB, Krasnolpolsky V, Dehlinger E (1994) Inhibition of retinal growth cone activity by specific metalloproteinase inhibitors in vitro. Dev Dyn 200:79-88.
61. Shipley JM, Wessekschmidt RL, Kobayashi DK, Ley TJ, Shapiro SD (1996) Metalloelastase is required for macrophage-mediated proteolysis and matrix invasion in mice. Proc Natl Acad Sci USA 93:3942-3946.
62. Streit WJ, Semple-Rowland SL, Hurley SD, Miller RC, Popovich PG, Stokes BT (1998) Cytokine mRNA profiles in contused spinal cord and axotomized facial nucleus suggest a beneficial role for inflammation and gliosis. Exp Neurol 152:74-87.
63. Vos CM, Sjulson L, Nath A, McArthur JC, Pardo CA, Rothstein J, Conant K (2000) Cytotoxicity by matrix metalloprotease-1 in organotypic spinal cord and dissociated neuronal cultures. Exp Neurol 163:324-330.
64. Vos CMP, Van Haastert ES, De Groot CJA, Van der Valk P, De Vries HE (2003) Matrix metalloproteinase-12 is expressed in phagocytic macrophages in active multiple sclerosis lesions. J Immunol 138:106-114.
65. Wang X, Jung J, Asahi M, Chwang W, Russo L, Moskowitz MA, Dixon CE, Fini ME, Lo EH (2000) Effects of matrix metalloproteinase-9 gene knock-out on morphological and motor outcomes after traumatic brain injury. J Neurosci 20:7037-7042.
66. Webber CA, Hocking JC, Yong VW, Stange CL, McFarlane S (2002) Metalloproteases and guidance of retinal axons in the developing visual system. J Neurosci 22:8091-8100.
67. Wells JEA, Hudbert RJ, Fehlings MG, Yong VW (2003) Neuroprotection by minocycline facilitates significant recovery from spinal cord injury in mice. Brain 126:1628-1637.
68. Windsor LJ, Grenett H, Birkedal-Hansen B, Bodden MK, Engler JA, Birkedal-Hansen H (1993) Cell type-specific regulation of SL-1 and SL-2 genes: induction of the SL-2 gene but not the SL-1 gene by human keratinocytes in response to cytokines and phorbol esters. J Biol Chem 268:17341-17347.
69. Yong VW, Power C, Forsyth P, Edwards DR (2001) Metalloproteinases in biology and pathology of the nervous system. Nat Rev Neurosci 2:502-511.
70. Yrjanheikki J, Keinanen R, Pellikka M, Hokfelt T, Koistinaho J (1998) Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci USA 95:15769-15774.
71. Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan PH, Koistinaho J (1999) A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci USA 96:13496-13500.