Matrix metalloproteinase-2 and -9 in the cerebellum of teleost fish: Functional implications for adult neurogenesis

Molecular and Cellular Neuroscience

Volumn 68, Issue , 2015, Pages 9-23

  Sîrbulescu, Ruxandra F ^a   Ilieş, Iulian ^a   Zupanc, Günther K H ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Adult neurogenesis; Cell migration; Cerebellum; Knifefish; Matrix metalloproteinase; Stem progenitor cell

Indexed keywords

GELATINASE A; GELATINASE B; MATRIX METALLOPROTEINASE; CYCLINE; GELATINASE; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; TRANSCRIPTION FACTOR SOX; VIMENTIN;

AMINO ACID SEQUENCE; ARTICLE; CELL MIGRATION; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; ENZYME ACTIVITY; FISH; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; TELEOST; ZYMOGRAPHY; ADULT STEM CELL; ANIMAL; CELL FRACTIONATION; CELL MOTION; CHEMICAL STRUCTURE; CYTOLOGY; ENZYMOLOGY; METABOLISM; PHYSIOLOGY;

APTERONOTUS LEPTORHYNCHUS; TELEOSTEI;

ADULT STEM CELLS; ANIMALS; CELL MOVEMENT; CEREBELLUM; FISHES; GELATINASES; GLIAL FIBRILLARY ACIDIC PROTEIN; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MODELS, MOLECULAR; NEUROGENESIS; PROLIFERATING CELL NUCLEAR ANTIGEN; RNA, MESSENGER; SOXB1 TRANSCRIPTION FACTORS; SUBCELLULAR FRACTIONS; VIMENTIN;

EID: 84925967691     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2015.03.015     Document Type: Article

References (71)

1. Allan J.A., Docherty A.J.P., Barker P.J., Huskisson N.S., Reynolds J.J., Murphy G. Binding of gelatinases A and B to type-I collagen and other matrix components. Biochem. J. 1995, 309:299-306.
2. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
3. Aoudjit F., Masure S., Opdenakker G., Potworowski E.F., St-Pierre Y. Gelatinase B (MMP-9), but not its inhibitor (TIMP-1), dictates the growth rate of experimental thymic lymphoma. Int. J. Cancer 1999, 82:743-747.
4. Arnold K., Bordoli L., Kopp J., Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 2006, 22:195-201.
5. Ayoub A.E., Cai T.Q., Kaplan R.A., Luo J. Developmental expression of matrix metalloproteinases 2 and 9 and their potential role in the histogenesis of the cerebellar cortex. J. Comp. Neurol. 2005, 481:403-415.
6. Barton K.M., Levine E.M. Expression patterns and cell cycle profiles of PCNA, MCM6, cyclin D1, cyclin A2, cyclin B1, and phosphorylated histone H3 in the developing mouse retina. Dev. Dyn. 2008, 237:672-682.
7. Benkert P., Biasini M., Schwede T. Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics 2011, 27:343-350.
8. Biasini M., Bienert S., Waterhouse A., Arnold K., Studer G., Schmidt T., Kiefer F., Cassarino T.G., Bertoni M., Bordoli L. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 2014, 42:W252-W258.
9. Butler G.S., Butler M.J., Atkinson S.J., Will H., Tamura T., van Westrum S.S., Crabbe T., Clements J., d'Ortho M.-P., Murphy G. The TIMP2 membrane type 1 metalloproteinase "receptor" regulates the concentration and efficient activation of progelatinase A: a kinetic study. J. Biol. Chem. 1998, 273:871-880.
10. Butler G.S., Apte S.S., Willenbrock F., Murphy G. Human tissue inhibitor of metalloproteinases 3 interacts with both the N-and C-terminal domains of gelatinases A and B: regulation by polyanions. J. Biol. Chem. 1999, 274:10846-10851.
11. Cha H., Kopetzki E., Huber R., Lanzendörfer M., Brandstetter H. Structural basis of the adaptive molecular recognition by MMP9. J. Mol. Biol. 2002, 320:1065-1079.
12. Cuadrado E., Rosell A., Borrell-Pages M., Garcia-Bonilla L., Hernandez-Guillamon M., Ortega-Aznar A., Montaner J. Matrix metalloproteinase-13 is activated and is found in the nucleus of neural cells after cerebral ischemia. J. Cereb. Blood Flow Metab. 2009, 29:398-410.
13. Daniel C., Duffield J., Brunner T., Steinmann-Niggli K., Lods N., Marti H.P. Matrix metalloproteinase inhibitors cause cell cycle arrest and apoptosis in glomerular mesangial cells. J. Pharmacol. Exp. Ther. 2001, 297:57-68.
14. Ekström P., Johnsson C.-M., Ohlin L.-M. Ventricular proliferation zones in the brain of an adult teleost fish and their relation to neuromeres and migration (secondary matrix) zones. J. Comp. Neurol. 2001, 436:92-110.
15. Elkins P.A., Ho Y.S., Smith W.W., Janson C.A., D'Alessio K.J., McQueney M.S., Cummings M.D., Romanic A.M. Structure of the C-terminally truncated human ProMMP9, a gelatin-binding matrix metalloproteinase. Acta Crystallogr. D Biol. Crystallogr. 2002, 58:1182-1192.
16. Frederiks W.M., Mook O.R.F. Metabolic mapping of proteinase activity with emphasis on in situ zymography of gelatinases: review and protocols. J. Histochem. Cytochem. 2004, 52:711-722.
17. Fujita S. Quantitative analysis of cell proliferation and differentiation in the cortex of the postnatal mouse cerebellum. J. Cell Biol. 1967, 32:277-287.
18. Gama Salgado J.A., Zupanc G.K.H. Echo response to chirping in the weakly electric brown ghost knifefish (Apteronotus leptorhynchus): role of frequency and amplitude modulations. Can. J. Zool. 2011, 89:498-508.
19. Gohlke U., Gomis-Rüth F.-X., Crabbe T., Murphy G., Docherty A.J.P., Bode W. The C-terminal (haemopexin-like) domain structure of human gelatinase A (MMP-2): structural implications for its function. FEBS Lett. 1996, 378:126-130.
20. Goldberg G.I., Strongin A., Collier I.E., Genrich L.T., Marmer B.L. Interaction of 92-kDa type IV collagenase with the tissue inhibitor of metalloproteinases prevents dimerization, complex formation with interstitial collagenase, and activation of the proenzyme with stromelysin. J. Biol. Chem. 1992, 267:4583-4591.
21. Golubkov V.S., Boyd S., Savinov A.Y., Chekanov A.V., Osterman A.L., Remacle A., Rozanov D.V., Doxsey S.J., Strongin A.Y. Membrane type-1 matrix metalloproteinase (MT1-MMP) exhibits an important intracellular cleavage function and causes chromosome instability. J. Biol. Chem. 2005, 280:25079-25086.
22. Grandel H., Kaslin J., Ganz J., Wenzel I., Brand M. Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev. Biol. 2006, 295:263-277.
23. Haas B.J., Papanicolaou A., Yassour M., Grabherr M., Blood P.D., Bowden J., Couger M.B., Eccles D., Li B., Lieber M., MacManes M.D., Ott M., Orvis J., Pochet N., Strozzi F., Weeks N., Westerman R., William T., Dewey C.N., Henschel R., LeDuc R.D., Friedman N., Regev A. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 2013, 8:1494-1512.
24. Hibi M., Shimizu T. Development of the cerebellum and cerebellar neural circuits. Dev. Neurobiol. 2012, 72:282-301.
25. Ilieş I., Sîrbulescu R.F., Zupanc G.K.H. Indeterminate body growth and lack of gonadal decline in the brown ghost knifefish (Apteronotus leptorhynchus), an organism exhibiting negligible brain senescence. Can. J. Zool. 2014, 92:947-953.
26. Kaslin J., Kroehne V., Benato F., Argenton F., Brand M. Development and specification of cerebellar stem and progenitor cells in zebrafish: from embryo to adult. Neural Dev. 2013, 8:9.
27. Kaufmann S.H., Desnoyers S., Ottaviano Y., Davidson N.E., Poirier G.G. Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 1993, 53:3976-3985.
28. Klein T., Bischoff R. Physiology and pathophysiology of matrix metalloproteases. Amino Acids 2011, 41:271-290.
29. Kwan J.A., Schulze C.J., Wang W., Leon H., Sariahmetoglu M., Sung M., Sawicka J., Sims D.E., Sawicki G., Schulz R. Matrix metalloproteinase-2 (MMP-2) is present in the nucleus of cardiac myocytes and is capable of cleaving poly (ADP-ribose) polymerase (PARP) in vitro. FASEB J. 2004, 18:690-692.
30. Luo J. The role of matrix metalloproteinases in the morphogenesis of the cerebellar cortex. Cerebellum 2005, 4:239-245.
31. Mannello F., Medda V. Nuclear localization of matrix metalloproteinases. Prog. Histochem. Cytochem. 2012, 47:27-58.
32. Massova I., Kotra L.P., Fridman R., Mobashery S. Matrix metalloproteinases: structures, evolution, and diversification. FASEB J. 1998, 12:1075-1095.
33. McWilliam H., Li W., Uludag M., Squizzato S., Park Y.M., Buso N., Cowley A.P., Lopez R. Analysis tool web services from the EMBL-EBI. Nucleic Acids Res. 2013, 41:W597-W600.
34. Morgunova E., Tuuttila A., Bergmann U., Isupov M., Lindqvist Y., Schneider G., Tryggvason K. Structure of human pro-matrix metalloproteinase-2: activation mechanism revealed. Science 1999, 284:1667-1670.
35. Morrison C.J., Butler G.S., Bigg H.F., Roberts C.R., Soloway P.D., Overall C.M. Cellular activation of MMP-2 (gelatinase A) by MT2-MMP occurs via a TIMP-2-independent pathway. J. Biol. Chem. 2001, 276:47402-47410.
36. Murphy G., Nguyen Q., Cockett M.I., Atkinson S.J., Allan J.A., Knight C.G., Willenbrock F., Docherty A.J.P. Assessment of the role of the fibronectin-like domain of gelatinase A by analysis of a deletion mutant. J. Biol. Chem. 1994, 269:6632-6636.
37. Nagase H., Visse R., Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res. 2006, 69:562-573.
38. Oberhammer F.A., Hochegger K., Froschl G., Tiefenbacher R., Pavelka M. Chromatin condensation during apoptosis is accompanied by degradation of lamin A+B, without enhanced activation of cdc2 kinase. J. Cell Biol. 1994, 126:827-837.
39. O'Connell J.P., Willenbrock F., Docherty A.J.P., Eaton D., Murphy G. Analysis of the role of the COOH-terminal domain in the activation, proteolytic activity, and tissue inhibitor of metalloproteinase interactions of gelatinase B. J. Biol. Chem. 1994, 269:14967-14973.
40. Olson M.W., Gervasi D.C., Mobashery S., Fridman R. Kinetic analysis of the binding of human matrix metalloproteinase-2 and-9 to tissue inhibitor of metalloproteinase (TIMP)-1 and TIMP-2. J. Biol. Chem. 1997, 272:29975-29983.
41. Overall C.M. Molecular determinants of metalloproteinase substrate specificity. Mol. Biotechnol. 2002, 22:51-86.
42. Overall C.M., King A.E., Sam D.K., Ong A.D., Lau T.T., Wallon U.M., DeClerck Y.A., Atherstone J. Identification of the tissue inhibitor of metalloproteinases-2 (TIMP-2) binding site on the hemopexin carboxyl domain of human gelatinase A by site-directed mutagenesis. J. Biol. Chem. 1999, 274:4421-4429.
43. Patterson M.L., Atkinson S.J., Knäuper V., Murphy G. Specific collagenolysis by gelatinase A, MMP-2, is determined by the hemopexin domain and not the fibronectin-like domain. FEBS Lett. 2001, 503:158-162.
44. 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.
45. Rosenberg G.A. Matrix metalloproteinases and their multiple roles in neurodegenerative diseases. Lancet Neurol. 2009, 8:205-216.
46. Rosenblum G., Van den Steen P.E., Cohen S.R., Grossmann J.G., Frenkel J., Sertchook R., Slack N., Strange R.W., Opdenakker G., Sagi I. Insights into the structure and domain flexibility of full-length pro-matrix metalloproteinase-9/gelatinase B. Structure 2007, 15:1227-1236.
47. Ruh M.F., Dunn R., Ruh T.S. Interrelationships between nuclear structure and ligand-activated intracellular receptors. Crit. Rev. Eukaryot. Gene Expr. 1996, 6:271-283.
48. Salisbury J.P., Sîrbulescu R.F., Moran B., Auclair J.R., Zupanc G.K.H., Agar J.N. The central nervous system transcriptome of the weakly electric brown ghost knifefish (Apteronotus leptorhynchus): de novo assembly, annotation, and proteomics validation. BMC Genomics 2015, 16:166.
49. Sans-Fons M.G., Sole S., Sanfeliu C., Planas A.M. Matrix metalloproteinase-9 and cell division in neuroblastoma cells and bone marrow macrophages. Am. J. Pathol. 2010, 177:2870-2885.
50. Sievers F., Wilm A., Dineen D., Gibson T.J., Karplus K., Li W., Lopez R., McWilliam H., Remmert M., Söding J. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 2011, 7:539.
51. Sîrbulescu R.F., Ilieş I., Vitalo A.G., Trull K., Zhu J., Traniello I.M., Zupanc G.K.H. Adult stem cells in the knifefish cerebellum. Dev. Neurobiol. 2015, 75:39-65.
52. Si-Tayeb K., Monvoisin A., Mazzocco C., Lepreux S., Decossas M., Cubel G., Taras D., Blanc J.F., Robinson D.R., Rosenbaum J. Matrix metalloproteinase 3 is present in the cell nucleus and is involved in apoptosis. Am. J. Pathol. 2006, 169:1390-1401.
53. Sternlicht M.D., Werb Z. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 2001, 17:463-516.
54. Teles M.C., Sîrbulescu R.F., Wellbrock U.M., Oliveira R.F., Zupanc G.K.H. Adult neurogenesis in the brain of the Mozambique tilapia, Oreochromis mossambicus. J. Comp. Physiol. A. 2012, 198:427-449.
55. Traniello I.M., Sîrbulescu R.F., Ilieş I., Zupanc G.K.H. Age-related changes in stem cell dynamics, neurogenesis, apoptosis, and gliosis in the adult brain: a novel teleost fish model of negligible senescence. Dev. Neurobiol. 2014, 74:514-530.
56. Vaillant C., Didier-Bazes M., Hutter A., Belin M.F., Thomasset N. Spatiotemporal expression patterns of metalloproteinases and their inhibitors in the postnatal developing rat cerebellum. J. Neurosci. 1999, 19:4994-5004.
57. Vaillant C., Meissirel C., Mutin M., Belin M.F., Lund L.R., Thomasset N. MMP-9 deficiency affects axonal outgrowth, migration, and apoptosis in the developing cerebellum. Mol. Cell. Neurosci. 2003, 24:395-408.
58. Van Wart H.E., Birkedal-Hansen H. The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:5578-5582.
59. Verslegers M., Van Hove I., Buyens T., Dekeyster E., Knevels E., Moons L. Identification of MMP-2 as a novel enhancer of cerebellar granule cell proliferation. Mol. Cell. Neurosci. 2013, 57:63-72.
60. Verslegers M., Van Hove I., Dekeyster E., Gantois I., Hu T.T., D'Hooge R., Arckens L., Moons L. MMP-2 mediates Purkinje cell morphogenesis and spine development in the mouse cerebellum. Brain Struct. Funct. 2014, (in press). 10.1007/s00429-014-0747-3.
61. Visse R., Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 2003, 92:827-839.
62. Ward R.V., Atkinson S.J., Reynolds J.J., Murphy G. Cell surface-mediated activation of progelatinase A: demonstration of the involvement of the C-terminal domain of progelatinase A in cell surface binding and activation of progelatinase A by primary fibroblasts. Biochem. J. 1994, 304:263-269.
63. Yang Y., Candelario-Jalil E., Thompson J.F., Cuadrado E., Estrada E.Y., Rosell A., Montaner J., Rosenberg G.A. Increased intranuclear matrix metalloproteinase activity in neurons interferes with oxidative DNA repair in focal cerebral ischemia. J. Neurochem. 2010, 112:134-149.
64. Yong V.W. Metalloproteinases: mediators of pathology and regeneration in the CNS. Nat. Rev. Neurosci. 2005, 6:931-944.
65. Yong V.W., Power C., Forsyth P., Edwards D.R. Metalloproteinases in biology and pathology of the nervous system. Nat. Rev. Neurosci. 2001, 2:502-511.
66. Zhao W.Q., Li H., Yamashita K., Guo X.K., Hoshino T., Yoshida S., Shinya T., Hayakawa T. Cell cycle-associated accumulation of tissue inhibitor of metalloproteinases-1 (TIMP-1) in the nuclei of human gingival fibroblasts. J. Cell Sci. 1998, 111:1147-1153.
67. Zupanc G.K.H., Clint S.C. Potential role of radial glia in adult neurogenesis of teleost fish. Glia 2003, 43:77-86.
68. Zupanc G.K.H., Horschke I. Proliferation zones in the brain of adult gymnotiform fish: a quantitative mapping study. J. Comp. Neurol. 1995, 353:213-233.
69. Zupanc G.K.H., Horschke I., Ott R., Rascher G.B. Postembryonic development of the cerebellum in gymnotiform fish. J. Comp. Neurol. 1996, 370:443-464.
70. Zupanc G.K.H., Hinsch K., Gage F.H. Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain. J. Comp. Neurol. 2005, 488:290-319.
71. Zupanc G.K.H., Sîrbulescu R.F., Ilieş I. Radial glia in the cerebellum of adult teleost fish: implications for the guidance of migrating new neurons. Neuroscience 2012, 210:416-430.