Matrix Metalloproteinase Inhibition Alters Functional and Structural Correlates of Deafferentation-Induced Sprouting in the Dentate Gyrus

Journal of Neuroscience

Volumn 23, Issue 32, 2003, Pages 10182-10189

  Reeves, Thomas M ^a   Prins, Mayumi L ^b   Zhu, JiePei ^a   Povlishock, John T ^a   Phillips, Linda L ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Collateral sprouting; Deafferentation; Extracellular matrix; Matrix metalloproteinase; Synaptic plasticity; Synaptogenesis

Indexed keywords

FN 439; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE INHIBITOR; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; DEAFFERENTATION; DENDRITE; DENSITY; DENTATE GYRUS; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; ENTORHINAL CORTEX; ENZYME ACTIVITY; GRANULE CELL; HISTOPATHOLOGY; IN VIVO STUDY; LONG TERM POTENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SPROUTING; SYNAPTOGENESIS; TEMPORAL LOBE;

EID: 0344824684     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-32-10182.2003     Document Type: Article

References (67)

1. Amaral DG, Witter MP (1995) The hippocampal formation. In: The rat nervous system, Ed 2 (Paxinos G, ed), pp 443-494. New York: Academic.
2. Amet LE, Lauri SE, Hienola A, Croll SD, Lu Y, Levorse JM, Prabhakaran B, Taira T, Rauvala H, Vogt TF (2001) Enhanced hippocampal long-term potentiation in mice lacking heparin-binding growth-associated molecule. Mol Cell Neurosci 17:1014-1024.
3. Anan H, Matsumoto A, Hamachi T, Yoshimine Y, Morita Y, Maeda K (1996) Effects of a combination of an antibacterial agent (ofloxacin) and a collagenase inhibitor (FN-439) on the healing of rat periapical lesions. J Endod 22:668-673.
4. Bukalo O, Schachner M, Dityatev A (2001) Modification of extracellular matrix by enzymatic removal of chondroitin sulfate and by lack of tenascin-R differentially affects several forms of synaptic plasticity in the hippocampus. Neuroscience 104:359-369.
5. Buki A, Okonkwo DO, Povlishock JT (1999) Postinjury cyclosporin A administration limits damage and disconnection in traumatic brain injury. J Neurotrauma 16:511-521.
6. Burdette LJ, Gilbert ME (1995) Stimulus parameters affecting paired-pulse depression of dentate granule cell field potentials. I. Stimulus intensity. Brain Res 680:53-62.
7. Canning KJ, Leung LS (1997) Lateral entorhinal, perirhinal, and amygdala-entorhinal transition projections to hippocampal CA1 and dentate gyrus in the rat: a current source density study. Hippocampus 7:643-655.
8. Chang HP, Ma YL, Wan FJ, Tsai LY, Lindberg FP, Lee EH (2001) Functional blocking of integrin-associated protein impairs memory retention and decreases glutamate release from the hippocampus. Neuroscience 102:289-296.
9. Choi BH (1994) Role of the basement membrane in neurogenesis and repair of injury in the central nervous system. Microsc Res Tech 28:193-203.
10. Cotman CW, Nieto-Sampedro M, Harris EW (1981) Synapse replacement in the nervous system of adult vertebrates. Physiol Rev 61:684-784.
11. Davies SJA, Goucher DA, Doller C, Silver J (1999) Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci 19:5810-5822.
12. Davis L, Vinsant SL, Steward O (1988) Ultrastructural characterization of the synapses of the crossed temporodentate pathway in rats. J Comp Neurol 267:190-202.
13. Deller T, Frotscher M (1997) Lesion-induced plasticity of central neurons: sprouting of single fibres in the rat hippocampus after unilateral entorhinal cortex lesion. Prog Neurobiol 53:687-727.
14. Deller T, Nitsch R, Frotscher M (1996) Layer-specific sprouting of commissural fibers to the rat fascia dentata after unilateral entorhinal cortex lesion: a Phaseolus vulgaris leucoagglutinin tracing study. Neuroscience 71:651-660.
15. Deller T, Haas CA, Naumann T, Joester A, Faissner A, Frotscher M (1997) Upregulation of astrocyte-derived tenascin-C correlates with neurite outgrowth in the rat dentate, gyrus after unilateral entorhinal cortex lesion. Neuroscience 81:829-846.
16. Desmond NL, Levy WB (1983) Synaptic correlates of associative potentiation/depression: an ultrastructural study in the hippocampus. Brain Res 265:21-30.
17. DiScenna PG, Teyler TJ (1994) Development of inhibitory and excitatory synaptic transmission in the rat dentate gyrus. Hippocampus 4:569-576.
18. Erb DE, Povlishock JT (1991) Neuroplasticity following traumatic brain injury: a study of GABAergic terminal loss and recovery in the cat dorsal lateral vestibular nucleus. Exp Brain Res 83:253-267.
19. Fillmore HL, VanMeter TE, Broaddus WC (2001) Membrane-type matrix metalloproteinases (MT-MMPs): expression and function during glioma invasion. J Neuro-oncol 53:187-202.
20. Forster E, Naumann T, Deller T, Straube A, Nitsch R, Frotscher M (1997) Cholinergic sprouting in the rat fascia dentata after entorhinal lesions is not linked to early changes in neurotrophin messenger RNA expression. Neuroscience 80:731-739.
21. Frotscher M (1988) Neuronal elements in the hippocampus and their synaptic connections. Adv Anat Embryol 111:2-17.
22. Fujimura M, Gasche Y, Morita-Fujimura Y, Massengale J, Kawase M, Chan PH (1999) Early appearance of activated matrix metalloproteinase-9 and blood-brain barrier disruption in mice after focal cerebral ischemia and reperfusion. Brain Res 842:92-100.
23. Gage FH, Olejniczak P, Armstrong DM (1988) Astrocytes are important for sprouting in the septohippocampal circuit. Exp Neurol 102:2-13.
24. Haas CA, Deller T, Frotscher M (1997) Basal expression, subcellular distribution, and upregulation of the protooncogene c-JUN in the rat dentate gyrus after unilateral entorhinal cortex lesion. Neuroscience 81:33-45.
25. Haas CA, Rauch U, Thon N, Merten T, Deller T (1999) Entorhinal cortex lesion in adult rats induces the expression of the neuronal chondroitin sulfate proteoglycan neurocan in reactive astrocytes. J Neurosci 19:9953-9963.
26. Johnston D, Wu SM-S (1995) Foundations of cellular neurophysiology. Cambridge, MA: MIT.
27. Kigasawa K, Murata H, Morita Y, Odake S, Suda E, Shimizu I, Morikawa T, Nagai Y (1995) Inhibition of corneal ulceration by tetrapeptidyl hydroxamic acid. Jpn J Opthalmol 39:35-42.
28. Komai S, Matsuyama T, Matsumoto K, Kato K, Kobayashi M, Imamura K, Yoshida S, Ugawa S, Shiosaka S (2000) Neuropsin regulates an early phase of schaffer-collateral long-term potentiation in the murine hippocampus. Eur J Neurosci 12:1479-1486.
29. Lander AD (1993) Proteoglycans in the nervous system. Curr Opin Neurobiol 3:716-723.
30. Lauri SE, Kaukinen S, Kinnunen T, Yilnen A, Imai S, Kaila K, Taira T, Rauvala H (1999) Regulatory role and molecular interactions of a cell-surface heparan sulfate proteoglycan (N-syndecan) in hippocampal long-term potentiation. J Neurosci 19:1226-1235.
31. Lee M-Y, Hofmann H-D, Kirsch M (1997) Differential regulation of CNTF and CNTF receptor alpha expression in astrocytes and neurons of the fascia dentata following entorhinal cortex lesion. J Neurosci 17:1137-1146.
32. Leung LS, Fu X-W (1994) Factors affecting paired-pulse facilitation in hippocampal CA1 neruons in vitro. Brain Res 650:75-84.
33. Leung LS, Roth L, Canning KJ (1995) Entorhinal inputs to hippocampal CA1 and dentate gyrus in the rat: a current-source-density study. J Neurophysiol 73:2392-2403.
34. Loesche J, Steward O (1977) Behavioral correlates of denervation and reinnervation of the hippocampal formation of the rat: recovery of alternation performance following unilateral entorhinal cortex lesions. Brain Res Bull 2:31-39.
35. Lomo T (1971) Potentiation of monosynaptic EPSPs in the perforant path dentate granule cell synapse. Exp Brain Res 12:46-63.
36. Lukes A, Mun-Bryce S, Lukes M, Rosenberg GA (1999) Extracellular matrix degradation by metalloproteinases and central nervous system diseases. Mol Neurobiol 19:267-284.
37. Matthews DA, Cotman CW, Lynch G (1976a) An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. I. Magnitude and time course of degeneration. Brain Res 115:1-21.
38. Matthews DA, Cotman CW, Lynch G (1976b) An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. II. Reappearance of morphologically normal synaptic contacts. Brain Res 115:23-41.
39. Monard D (1988) Cell-derived proteases and protease inhibitors as regulators of neurite outgrowth. Trends Neurosci 11:541-544.
40. Odake S, Morita Y, Morikawa T, Yoshida N, Hori H, Nagai Y (1994) Inhibition of metalloproteinases by peptidyl hydroxiamic acids. Biochem Biophys Res Commun 199:1442-1446.
41. Phillips LL, Belardo ET (1994) Increase of c-fos and ras oncoproteins in the denervated neuropil of the rat dentate gyrus. Neuroscience 58:503-514.
42. Phillips LL, Reeves TM (2001) Interactive pathology following traumatic brain injury modifies hippocampal plasticity. Restor Neurol Neurosci 19:213-235.
43. Phillips LL, Steward O (1990) Increases in mRNA for cytoskeletal proteins in the denervated neuropil of the dentate gyrus: an in situ hybridization study using riboprobes for beta-actin and beta-tubulin. Mol Brain Res 8:249-257.
44. Phillips LL, Lyeth BG, Hamm RJ, Povlishock JT (1994) Combined fluid percussion brain injury and entorhinal cortical lesion: a model for assessing the interaction between neuroexcitation and deafferentation. J Neurotrauma 11:641-656.
45. Ramirez JJ, Stein DG (1984) Sparing and recovery of spatial alternation performance after entorhinal cortex lesions in rats. Behav Brain Res 13:53-61.
46. Ramirez JJ, McQuilkin M, Carrigan T, MacDonald K, Kelly MS (1996) Progressive enthorhinal cortex lesions accelerate hippocampal sprouting and spare spatial memory in rats. Proc Natl Acad Sci USA 93:15512-15517.
47. Reeves TM, Smith DC (1987) Reinnervation of the dentate gyrus and recovery of alternation behavior following entorhinal cortical lesions. Behav Neurosci 101:179-186.
48. Reeves TM, Steward O (1986) Emergence of the capacity for LTP during reinnervation of the dentate gyrus: evidence that abnormally shaped spines can mediate LTP. Exp Brain Res 65:167-175.
49. Reeves TM, Lyeth BG, Povlishock JT (1995) Long-term potentiation deficits and excitability changes following traumatic brain injury. Exp Brain Res 106:248-256.
50. Reeves TM, Zhu J, Povlishock JT, Phillips LL (1997) The effect of combined fluid percussion and entorhinal cortical lesions on long-term potentiation. Neuroscience 77:431-444.
51. Richardson TL, Turner RW, Miller JJ (1987) Action-potential discharge in hippocampal CA1 pyramidal neurons: current source-density analysis. J Neurophysiol 58:981-996.
52. Steward O (1976) Reinnervation of the dentate gyrus by homologous afferents following entorhinal cortex lesion in adult rats. Science 194:426-428.
53. Steward O (1991) Synapse replacement on cortical neurons following denervation. Cereb Cortex 9:81-132.
54. Steward O (1994) Reorganization of neuronal circuitry following central nervous system trauma: naturally occurring processes and opportunities for therapeutic intervention. In: The neurobiology of central nervous system trauma (Salzman SK, Faden AI, eds), pp 266-287. New York: Oxford UP.
55. Steward O, Vinsant SL (1983) The process of reinnervation in the dentate gyrus of the adult rat: a quantitative electron microscopic analysis of terminal proliferation and reactive synaptogenesis. J Comp Neurol 214:370-386.
56. Steward O, White CW, Cotman CW, Lynch G (1976) Potentiation of excitatory synaptic transmission in the normal and in the reinnervated dentate gyrus of the rat. Exp Brain Res 26:423-441.
57. Uhm JH, Dooley NP, Oh LY, Yong VW (1998) Oligodendrocytes utilize a matrix metalloproteinase, MMP-9, to extend processes along an astrocyte extracellular matrix. Glia 22:53-63.
58. Vaillant C, Didier-Bazes M, Hutter A, Belin M-F, Thomasset N (1999) Spatiotemporal expression patterns of metalloproteinases and their inhibitors in the postnatal developing rat cerebellum. J Neurosci 19:4994-5004.
59. Wang X, Jung J, Asahi M, Chwang W, Russo L, Moskowitz M, Dixon CE, Fini ME, Lo EH (2000) Effects of matrix metalloproteinase-9 gene knockout on morphological and motor outcomes after traumatic brain injury. J Neurosci 20:7037-7042.
60. White G, Levy WB, Steward O (1990) Spatial overlap between populations of synapses determines the extent of their associative interaction during the induction of long-term potentiation and depression. J Neurophysiol 64:1186-1198.
61. Wilson RC (1981) Changes in translation of synaptic excitation to dentategranule cell discharge accompanying long-term potentiation. I. Differences between normal and reinnervated dentate gyrus. J Neurophysiol 46:324-338.
62. Wilson RC, Levy WB, Steward O (1981) Changes in translation of synaptic excitation to dentate granule cell discharge accompanying long-term potentiation. II. An evaluation of mechanisms utilizing dentate gyrus dually innervated by surviving ipsilateral and sprouted crossed temporodentate inputs. J Neurophysiol 46:339-355.
63. Wyss JM (1981) An autoradiographic study of the efferent connections of the entorhinal cortex in the rat. J Comp Neurol 199:495-512.
64. Yaghmai A, Povlishock JT (1992) Traumatically induced reactive change as visualized through the use of monoclonal antibodies targeted to neurofilament subunits. J Neuropathol Exp Neurol 51:158-176.
65. Yong VW, Krekoski CA, Forsyth PA, Bell R, Edwards DR (1998) Matrix metalloproteinases and disease of the CNS. Trends Neurosci 21:75-80.
66. Yuan W, Matthews RT, Sandy JD, Gottschall PE (2002) Association between protease-specific proteolytic cleavage of brevican and synaptic loss in the dentate gyrus of kainate-treated rats. Neuroscience 114:1091-1101.
67. Zucker RS (1989) Short-term synaptic plasticity. Annu Rev Neurosci 12:13-31.