Matrix metalloproteinase-9 controls proliferation of NG2+ progenitor cells immediately after spinal cord injury

Experimental Neurology

Volumn 231, Issue 2, 2011, Pages 236-246

  Liu, Huaqing ^a,b   Shubayev, Veronica I ^a,b  

^a University of California   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA AMYLASE; GELATINASE A; GELATINASE B; GLIAL FIBRILLARY ACIDIC PROTEIN; MATRIX METALLOPROTEINASE INHIBITOR; MYELIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; NEURON GLIAL ANTIGEN 2; PROTEOGLYCAN; SB 3CT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG MECHANISM; DRUG TARGETING; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; ENZYME SPECIFICITY; FEMALE; LOCOMOTION; MACROPHAGE; MICROGLIA; MITOSIS; NEURAL STEM CELL; NEURON GLIAL ANTIGEN 2+ PROGENITOR CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; REMYELINIZATION; SOMATOSENSORY SYSTEM; SPINAL CORD DORSAL HORN; SPINAL CORD HEMISECTION; SPINAL CORD INJURY; TREATMENT DURATION;

ANIMALS; ANTIGENS; CELL PROLIFERATION; FEMALE; HETEROCYCLIC COMPOUNDS, 1-RING; MATRIX METALLOPROTEINASE 9; MOTOR ACTIVITY; NEURAL STEM CELLS; NEUROGLIA; PROTEOGLYCANS; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD; SPINAL CORD INJURIES; SULFONES; THORACIC VERTEBRAE;

EID: 80052542874     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.06.015     Document Type: Article

References (57)

1. Alonso G. NG2 proteoglycan-expressing cells of the adult rat brain: possible involvement in the formation of glial scar astrocytes following stab wound. Glia 2005, 49:318-338.
2. Basso D.M., Beattie M.S., Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 1995, 12:1-21.
3. 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.
4. Busch S.A., Horn K.P., Silver D.J., Silver J. Overcoming macrophage-mediated axonal dieback following CNS injury. J. Neurosci. 2009, 29:9967-9976.
5. Busch S.A., Horn K.P., Cuascut F.X., Hawthorne A.L., Bai L., Miller R.H., Silver J. Adult NG2+ cells are permissive to neurite outgrowth and stabilize sensory axons during macrophage-induced axonal dieback after spinal cord injury. J. Neurosci. 2010, 30:255-265.
6. Busch S.A., Hamilton J.A., Horn K.P., Cuascut F.X., Cutrone R., Lehman N., Deans R.J., Ting A.E., Mays R.W., Silver J. Multipotent adult progenitor cells prevent macrophage-mediated axonal dieback and promote regrowth after spinal cord injury. J. Neurosci. 2011, 31:944-953.
7. Buss A., Pech K., Kakulas B.A., Martin D., Schoenen J., Noth J., Brook G.A. Matrix metalloproteinases and their inhibitors in human traumatic spinal cord injury. BMC Neurol. 2007, 7:17.
8. Chattopadhyay S., Shubayev V.I. MMP-9 controls Schwann cell proliferation and phenotypic remodeling via IGF-1 and ErbB receptor-mediated activation of MEK/ERK pathway. Glia 2009, 57:1316-1325.
9. Dawson M.R., Polito A., Levine J.M., Reynolds R. NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol. Cell. Neurosci. 2003, 24:476-488.
10. De Biase L.M., Nishiyama A., Bergles D.E. Excitability and synaptic communication within the oligodendrocyte lineage. J. Neurosci. 2010, 30:3600-3611.
11. de Castro R.C., Burns C.L., McAdoo D.J., Romanic A.M. Metalloproteinase increases in the injured rat spinal cord. Neuroreport 2000, 11:3551-3554.
12. Duchossoy Y., Horvat J.C., Stettler O. MMP-related gelatinase activity is strongly induced in scar tissue of injured adult spinal cord and forms pathways for ingrowing neurites. Mol. Cell. Neurosci. 2001, 17:945-956.
13. Giger R.J., Hollis E.R., Tuszynski M.H. Guidance molecules in axon regeneration. Cold Spring Harb. Perspect. Biol. 2010, 2:a001867.
14. Gijbels K., Proost P., Masure S., Carton H., Billiau A., Opdenakker G. Gelatinase B is present in the cerebrospinal fluid during experimental autoimmune encephalomyelitis and cleaves myelin basic protein. J. Neurosci. Res. 1993, 36:432-440.
15. Griffiths I.R., McCulloch M.C. Nerve fibres in spinal cord impact injuries. Part 1. Changes in the myelin sheath during the initial 5weeks. J. Neurol. Sci. 1983, 58:335-349.
16. Gu Z., Cui J., 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, 25:6401-6408.
17. Horner P.J., Power A.E., Kempermann G., Kuhn H.G., Palmer T.D., Winkler J., Thal L.J., Gage F.H. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J. Neurosci. 2000, 20:2218-2228.
18. Hsu J.Y., McKeon R., Goussev S., Werb Z., Lee J.U., Trivedi A., Noble-Haeusslein L.J. Matrix metalloproteinase-2 facilitates wound healing events that promote functional recovery after spinal cord injury. J. Neurosci. 2006, 26:9841-9850.
19. Hsu J.Y., Bourguignon L.Y., Adams C.M., Peyrollier K., Zhang H., Fandel T., Cun C.L., Werb Z., Noble-Haeusslein L.J. Matrix metalloproteinase-9 facilitates glial scar formation in the injured spinal cord. J. Neurosci. 2008, 28:13467-13477.
20. Jones L.L., Yamaguchi Y., Stallcup W.B., Tuszynski M.H. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J. Neurosci. 2002, 22:2792-2803.
21. Jones L.L., Sajed D., Tuszynski M.H. Axonal regeneration through regions of chondroitin sulfate proteoglycan deposition after spinal cord injury: a balance of permissiveness and inhibition. J. Neurosci. 2003, 23:9276-9288.
22. Kang S.H., Fukaya M., Yang J.K., Rothstein J.D., Bergles D.E. NG2+ CNS glial progenitors remain committed to the oligodendrocyte lineage in postnatal life and following neurodegeneration. Neuron 2010, 68:668-681.
23. Larsen P.H., Wells J.E., Stallcup W.B., Opdenakker G., Yong V.W. Matrix metalloproteinase-9 facilitates remyelination in part by processing the inhibitory NG2 proteoglycan. J. Neurosci. 2003, 23:11127-11135.
24. Larsen P.H., DaSilva A.G., Conant K., Yong V.W. Myelin formation during development of the CNS is delayed in matrix metalloproteinase-9 and -12 null mice. J. Neurosci. 2006, 26:2207-2214.
25. Lehmann H.C., Kohne A., Bernal F., Jangouk P., Meyer Zu Horste G., Dehmel T., Hartung H.P., Previtali S.C., Kieseier B.C. Matrix metalloproteinase-2 is involved in myelination of dorsal root ganglia neurons. Glia 2009, 57:479-489.
26. Liu H., Kim Y., Chattopadhyay S., Shubayev I., Dolkas J., Shubayev V.I. MMP inhibition enhances the rate of nerve regeneration in vivo by promoting de-differentiation and mitosis of supporting Schwann cells. J. Neuropathol. Exp. Neurol. 2010, 69:386-395.
27. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
28. Lytle J.M., Wrathall J.R. Glial cell loss, proliferation and replacement in the contused murine spinal cord. Eur. J. Neurosci. 2007, 25:1711-1724.
29. Manabe S., Gu Z., Lipton S.A. Activation of matrix metalloproteinase-9 via neuronal nitric oxide synthase contributes to NMDA-induced retinal ganglion cell death. Invest. Ophthalmol. Vis. Sci. 2005, 46:4747-4753.
30. McTigue D.M., Wei P., Stokes B.T. Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J. Neurosci. 2001, 21:3392-3400.
31. Moore C.S., Milner R., Nishiyama A., Frausto R.F., Serwanski D.R., Pagarigan R.R., Whitton J.L., Miller R.H., Crocker S.J. Astrocytic tissue inhibitor of metalloproteinase-1 (TIMP-1) promotes oligodendrocyte differentiation and enhances CNS myelination. J. Neurosci. 2011, 31:6247-6254.
32. Nagase H., Visse R., Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res. 2006, 69:562-573.
33. Nakamura M., Zhou X.Z., Lu K.P. Critical role for the EB1 and APC interaction in the regulation of microtubule polymerization. Curr. Biol. 2001, 11:1062-1067.
34. Nishiyama A., Komitova M., Suzuki R., Zhu X. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat. Rev. Neurosci. 2009, 10:9-22.
35. Noble L.J., 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, 22:7526-7535.
36. Oh L.Y., Larsen P.H., Krekoski C.A., Edwards D.R., Donovan F., Werb Z., Yong V.W. Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocytes. J. Neurosci. 1999, 19:8464-8475.
37. Page-McCaw A., Ewald A.J., Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 2007, 8:221-233.
38. Pauly T., Ratliff M., Pietrowski E., Neugebauer R., Schlicksupp A., Kirsch J., Kuhse J. Activity-dependent shedding of the NMDA receptor glycine binding site by matrix metalloproteinase 3: a PUTATIVE mechanism of postsynaptic plasticity. PLoS One 2008, 3:e2681.
39. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
40. Piccard H., Van den Steen P.E., Opdenakker G. Hemopexin domains as multifunctional liganding modules in matrix metalloproteinases and other proteins. J. Leukoc. Biol. 2007, 81:870-892.
41. Proost P., Van Damme J., Opdenakker G. Leukocyte gelatinase B cleavage releases encephalitogens from human myelin basic protein. Biochem. Biophys. Res. Commun. 1993, 192:1175-1181.
42. Rosenberg G.A. Matrix metalloproteinases and their multiple roles in neurodegenerative diseases. Lancet Neurol. 2009, 8:205-216.
43. Rosenberg M.M., Yang F., Giovanni M., Mohn J.L., Temburni M.K., Jacob M.H. Adenomatous polyposis coli plays a key role, in vivo, in coordinating assembly of the neuronal nicotinic postsynaptic complex. Mol. Cell. Neurosci. 2008, 38:138-152.
44. Shubayev V.I., Angert M., Dolkas J., Campana W.M., Palenscar K., Myers R.R. TNFalpha-induced MMP-9 promotes macrophage recruitment into injured peripheral nerve. Mol. Cell. Neurosci. 2006, 31:407-415.
45. Siegenthaler M.M., Tu M.K., Keirstead H.S. The extent of myelin pathology differs following contusion and transection spinal cord injury. J. Neurotrauma 2007, 24:1631-1646.
46. Szklarczyk A., Ewaleifoh O., Beique J.C., Wang Y., Knorr D., Haughey N., Malpica T., Mattson M.P., Huganir R., Conant K. MMP-7 cleaves the NR1 NMDA receptor subunit and modifies NMDA receptor function. FASEB J. 2008, 22:3757-3767.
47. Toma J.S., McPhail L.T., Ramer M.S. Differential RIP antigen (CNPase) expression in peripheral ensheathing glia. Brain Res. 2007, 1137:1-10.
48. Uhm J.H., Dooley N.P., Oh L.Y., Yong V.W. Oligodendrocytes utilize a matrix metalloproteinase, MMP-9, to extend processes along an astrocyte extracellular matrix. Glia 1998, 22:53-63.
49. Weidner N., Ner A., Salimi N., Tuszynski M.H. Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:3513-3518.
50. Wells J.E., Rice T.K., Nuttall R.K., Edwards D.R., Zekki H., Rivest S., Yong V.W. An adverse role for matrix metalloproteinase 12 after spinal cord injury in mice. J. Neurosci. 2003, 23:10107-10115.
51. Yang Z., Suzuki R., Daniels S.B., Brunquell C.B., Sala C.J., Nishiyama A. NG2 glial cells provide a favorable substrate for growing axons. J. Neurosci. 2006, 26:3829-3839.
52. Yang H., Lu P., McKay H.M., Bernot T., Keirstead H., Steward O., Gage F.H., Edgerton V.R., Tuszynski M.H. Endogenous neurogenesis replaces oligodendrocytes and astrocytes after primate spinal cord injury. J. Neurosci. 2006, 26:2157-2166.
53. Yu F., Kamada H., Niizuma K., Endo H., Chan P.H. Induction of mmp-9 expression and endothelial injury by oxidative stress after spinal cord injury. J. Neurotrauma 2008, 25:184-195.
54. Zai L.J., Wrathall J.R. Cell proliferation and replacement following contusive spinal cord injury. Glia 2005, 50:247-257.
55. Zawadzka M., Rivers L.E., Fancy S.P., Zhao C., Tripathi R., Jamen F., Young K., Goncharevich A., Pohl H., Rizzi M., Rowitch D.H., Kessaris N., Suter U., Richardson W.D., Franklin R.J. CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 2010, 6:578-590.
56. Zhang H., Adwanikar H., Werb Z., Noble-Haeusslein L.J. Matrix metalloproteinases and neurotrauma: evolving roles in injury and reparative processes. Neuroscientist 2010, 16:156-170.
57. Zhu X., Bergles D.E., Nishiyama A. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 2008, 135:145-157.