The Reck tumor suppressor protein alleviates tissue damage and promotes functional recovery after transient cerebral ischemia in mice

Journal of Neurochemistry

Volumn 115, Issue 2, 2010, Pages 385-398

  Wang, Huan ^a   Imamura, Yukio ^a   Ishibashi, Ryota ^b   Chandana, Ediriweera P S ^a   Yamamoto, Mako ^a   Noda, Makoto ^a  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Cerebral ischemia; Hippocampus; Laminin; Long term potentiation; Neural precursor cells; Reck

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; KI 67 ANTIGEN; LAMININ; MATRIX METALLOPROTEINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2C; NESTIN; NEUROFILAMENT PROTEIN; REVERSION INDUCING CYSTEINE RICH PROTEIN WITH KAZAL MOTIF; TISSUE INHIBITOR OF METALLOPROTEINASE; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN REGION; CELL DEATH; CONTROLLED STUDY; CONVALESCENCE; ENZYME REGULATION; HIPPOCAMPUS; IMMUNOREACTIVITY; MALE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RECEPTOR UPREGULATION; SUBVENTRICULAR ZONE; TISSUE INJURY; UPREGULATION;

ANIMALS; ANTIGENS, CD31; BIOPHYSICS; CELL COUNT; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; HIPPOCAMPUS; IN SITU NICK-END LABELING; ISCHEMIC ATTACK, TRANSIENT; KI-67 ANTIGEN; LAMINS; LONG-TERM POTENTIATION; MALE; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PATCH-CLAMP TECHNIQUES; RECEPTORS, N-METHYL-D-ASPARTATE; RECOVERY OF FUNCTION; RNA, MESSENGER; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

MUS;

EID: 78651324369     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06933.x     Document Type: Article

References (67)

1. Bickler P. E., Fahlman C. S. and Taylor D. M. (2003) Oxygen sensitivity of NMDA receptors: Relationship to NR2 subunit composition and hypoxia tolerance of neonatal neurons. Neuroscience 118, 25-35.
2. Bliss T. V. and Collingridge G. L. (1993) A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361, 31-39.
3. Calabresi P., Marfia G. A., Centonze D. et al. (1999) Sodium influx plays a major role in the membrane depolarization induced by oxygen and glucose deprivation in rat striatal spiny neurons. Stroke 30, 171-179.
4. Calabresi P., Centonze D. and Bernardi G. (2000) Cellular factors controlling neuronal vulnerability in the brain: A lesson from the striatum. Neurology 55, 1249-1255.
5. Calabresi P., Centonze D., Pisani A. et al. (2003) Synaptic plasticity in the ischaemic brain. Lancet Neurol. 2, 622-629.
6. Centonze D., Marfia G. A., Pisani A. et al. (2001) Ionic mechanisms underlying differential vulnerability to ischemia in striatal neurons. Prog. Neurobiol. 63, 687-696.
7. Chang H. P., Ma Y. L., Wan F. J. et al. (2001) Functional blocking of integrin-associated protein impairs memory retention and decreases glutamate release from the hippocampus. Neuroscience 102, 289-296.
8. Chen Z. L. and Strickland S. (1997) Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 91, 917-925.
9. Crepel V., Hammond C., Krnjevic K. et al. (1993) Anoxia-induced LTP of isolated NMDA receptor-mediated synaptic responses. J. Neurophysiol. 69, 1774-1778.
10. Dirnagl U., Simon R. P. and Hallenbeck J. M. (2003) Ischemic tolerance and endogenous neuroprotection. Trends Neurosci. 26, 248-254.
11. Ellison J. A., Barone F. C. and Feuerstein G. Z. (1999) Matrix remodeling after stroke. De novo expression of matrix proteins and integrin receptors. Ann. N Y Acad. Sci. 890, 204-222.
12. Ernst C. and Christie B. R. (2005) Nestin-expressing cells and their relationship to mitotically active cells in the subventricular zones of the adult rat. Eur. J. Neurosci. 22, 3059-3066.
13. Ethell I. M. and Ethell D. W. (2007) Matrix metalloproteinases in brain development and remodeling: Synaptic functions and targets. J. Neurosci. Res. 85, 2813-2823.
14. Felling R. J., Snyder M. J., Romanko M. J. et al. (2006) Neural stem/ progenitor cells participate in the regenerative response to perinatal hypoxia/ischemia. J. Neurosci. 26, 4359-4369.
15. Feng Y., Rhodes P. G. and Bhatt A. J. (2010) Hypoxic preconditioning provides neuroprotection and increases vascular endothelial growth factor A, preserves the phosphorylation of Akt-Ser-473 and diminishes the increase in caspase-3 activity in neonatal rat hypoxic- ischemic model. Brain Res. 1325, 1-9.
16. Fujimoto M., Takagi Y. and Aoki T. et al. (2008) Tissue inhibitor of metalloproteinases protect blood-brain barrier disruption in focal cerebral ischemia. J. Cereb. Blood Flow Metab. 28, 1674-1685.
17. Gidday J. M. (2006) Cerebral preconditioning and ischaemic tolerance. Nat. Rev. Neurosci. 7, 437-448.
18. Gillardon F., Kiprianova I. and Sandkuhler J. et al. (1999) Inhibition of caspases prevents cell death of hippocampal CA1 neurons, but not impairment of hippocampal long-term potentiation following global ischemia. Neuroscience 93, 1219-1222.
19. Gu Z., Kaul M., Yan B. et al. (2002) S-nitrosylation of matrix metalloproteinases: Signaling pathway to neuronal cell death. Science 297, 1186-1190.
20. Hammond C., Crepel V. and Gozlan H. et al. (1994) Anoxic LTP sheds light on the multiple facets of NMDA receptors. Trends Neurosci. 17, 497-503.
21. Hatta M., Matsuzaki T. and Morioka Y. et al. (2009) Density- and serum- dependent regulation of the Reck tumor suppressor in mouse embryo fibroblasts. Cell. Signal. 21, 1885-1893.
22. Hrabetova S., Serrano P., Blace N. et al. (2000) Distinct NMDA receptor subpopulations contribute to long-term potentiation and long-term depression induction. J. Neurosci. 20, RC81.
23. Ihara M., Tomimoto H. and Kinoshita M. et al. (2001) Chronic cerebral hypoperfusion induces MMP-2 but not MMP-9 expression in the microglia and vascular endothelium of white matter. J. Cereb. Blood Flow Metab. 21, 828-834.
24. Imamura Y., Matsumoto N., Kondo S. et al. (2003) Possible involvement of Rap1 and Ras in glutamatergic synaptic transmission. Neuroreport 14, 1203-1207.
25. Imamura Y., Ma C. L. and Pabba M. et al. (2008) Sustained saturating level of glycine induces changes in NR2B-containing-NMDA receptor localization in the CA1 region of the hippocampus. J. Neurochem. 105, 2454-2465.
26. Kadotani H., Namura S. and Katsuura G. et al. (1998) Attenuation of focal cerebral infarct in mice lacking NMDA receptor subunit NR2C. Neuroreport 9, 471-475.
27. Kawashima S., Imamura Y. and Chandana E. P. et al. (2008) Localization of the membrane-anchored MMP-regulator RECK at the neuromuscular junctions. J. Neurochem. 104, 376-385.
28. Kimura T., Okada A., Yatabe T. et al. (2010) RECK is up-regulated and involved in chondrocyte cloning in human osteoarthritic cartilage. Am. J. Pathol. 176, 2858-2867.
29. Koizumi S., Shigemoto-Mogami Y. and Nasu-Tada K. et al. (2007) UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 446, 1091-1095.
30. Van Lent P. L., Span P. N. and Sloetjes A. W. et al. (2005) Expression and localisation of the new metalloproteinase inhibitor RECK (reversion inducing cysteine-rich protein with Kazal motifs) in inflamed synovial membranes of patients with rheumatoid arthritis. Ann. Rheum. Dis. 64, 368-374.
31. Li L., Lundkvist A. and Andersson D. et al. (2008) Protective role of reactive astrocytes in brain ischemia. J. Cereb. Blood Flow Metab. 28, 468-481.
32. Lin T. N., He Y. Y. and Wu G. et al. (1993) Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 24, 117-121.
33. Lo E. H., Dalkara T. and Moskowitz M. A. (2003) Mechanisms, challenges and opportunities in stroke. Nat. Rev. Neurosci. 4, 399-415.
34. Loayza-Puch F., Yoshida Y., Matsuzaki T. et al. (2010) Hypoxia and RAS-signaling pathways converge on, and cooperatively downregulate, the RECK tumor-suppressor protein through microRNAs. Oncogene 29, 2638-2648.
35. Lukes A., Mun-Bryce S. and Lukes M. et al. (1999) Extracellular matrix degradation by metalloproteinases and central nervous system diseases. Mol. Neurobiol. 19, 267-284.
36. Mash D. C., Ffrench-Mullen J. and Adi N. et al. (2007) Gene expression in human hippocampus from cocaine abusers identifies genes which regulate extracellular matrix remodeling. PLoS ONE 2, e1187.
37. Meighan S. E., Meighan P. C., Choudhury P. et al. (2006) Effects of extracellular matrix-degrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity. J. Neurochem. 96, 1227-1241.
38. Miki T., Takegami Y., Okawa K. et al. (2007) The reversion-inducing cysteine-rich protein with Kazal motifs (RECK) interacts with membrane type 1 matrix metalloproteinase and CD13/aminopeptidase N and modulates their endocytic pathways. J. Biol. Chem. 282, 12341-12352.
39. Moore S. A., Saito F. and Chen J. et al. (2002) Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 418, 422-425.
40. Morioka Y., Monypenny J., Matsuzaki T. et al. (2009) The membraneanchored metalloproteinase regulator RECK stabilizes focal adhesions and anterior-posterior polarity in fibroblasts. Oncogene 28, 1454-1464.
41. Muraguchi T., Takegami Y. and Ohtsuka T. et al. (2007) RECK modulates Notch signaling during cortical neurogenesis by regulating ADAM10 activity. Nat. Neurosci. 10, 838-845.
42. Nagy V., Bozdagi O., Matynia A. et al. (2006) Matrix metalloproteinase- 9 is required for hippocampal late-phase long-term potentiation and memory. J. Neurosci. 26, 1923-1934.
43. Nakagami Y., Abe K. and Nishiyama N. et al. (2000) Laminin degradation by plasmin regulates long-term potentiation. J. Neurosci. 20, 2003-2010.
44. Nakaji K., Ihara M. and Takahashi C. et al. (2006) Matrix metalloproteinase- 2 plays a critical role in the pathogenesis of white matter lesions after chronic cerebral hypoperfusion in rodents. Stroke 37, 2816-2823.
45. Nakatomi H., Kuriu T. and Okabe S. et al. (2002) Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110, 429-441.
46. Namba T., Mochizuki H., Onodera M. et al. (2005) The fate of neural progenitor cells expressing astrocytic and radial glial markers in the postnatal rat dentate gyrus. Eur. J. Neurosci. 22, 1928-1941.
47. Nishimura M., Izumiya Y. and Higuchi A. et al. (2008) Adiponectin prevents cerebral ischemic injury through endothelial nitric oxide synthase dependent mechanisms. Circulation 117, 216-223.
48. Noda M. and Takahashi C. (2007) Recklessness as a hallmark of aggressive cancer. Cancer Sci. 98, 1659-1665.
49. Noda M., Oh J., Takahashi R. et al. (2003) RECK: A novel suppressor of malignancy linking oncogenic signaling to extracellular matrix remodeling. Cancer Metastasis Rev. 22, 167-175.
50. Oh J., Takahashi R., Kondo S. et al. (2001) The membrane-anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell 107, 789-800.
51. Omura A., Matsuzaki T. and Mio K. et al. (2009) RECK Forms Cowbell- shaped Dimers and Inhibits Matrix Metalloproteinase-catalyzed Cleavage of Fibronectin. J. Biol. Chem. 284, 3461-3469.
52. Pforte C., Henrich-Noack P. and Baldauf K. et al. (2005) Increase in proliferation and gliogenesis but decrease of early neurogenesis in the rat forebrain shortly after transient global ischemia. Neuroscience 136, 1133-1146.
53. Reeves T. M., Prins M. L. and Zhu J. et al. (2003) Matrix metalloproteinase inhibition alters functional and structural correlates of deafferentation- induced sprouting in the dentate gyrus. J. Neurosci. 23, 10182-10189.
54. Rosell A., Ortega-Aznar A., Alvarez-Sabin J. et al. (2006) Increased brain expression of matrix metalloproteinase-9 after ischemic and hemorrhagic human stroke. Stroke 37, 1399-1406.
55. Sasahara R. M., Takahashi C. and Noda M. (1999) Involvement of the Sp1 site in ras-mediated downregulation of the RECK metastasis suppressor gene. Biochem. Biophys. Res. Commun. 264, 668-675.
56. Small D. L., Poulter M. O. and Buchan A. M. et al. (1997) Alteration in NMDA receptor subunit mRNA expression in vulnerable and resistant regions of in vitro ischemic rat hippocampal slices. Neurosci. Lett. 232, 87-90.
57. Sternlicht M. D. and Werb Z. (2001) How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 17, 463-516.
58. Stoppini L., Buchs P. A. and Muller D. (1991) A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37, 173-182.
59. Sykova E. and Vargova L. (2008) Extrasynaptic transmission and the diffusion parameters of the extracellular space. Neurochem. Int. 52, 5-13.
60. Takahashi C., Sheng Z., Horan T. P. et al. (1998) Regulation of matrix metalloproteinase-9 and inhibition of tumor invasion by the membrane-anchored glycoprotein RECK. Proc. Natl Acad. Sci. USA 95, 13221-13226.
61. Tsuji K., Aoki T., Tejima E. et al. (2005) Tissue plasminogen activator promotes matrix metalloproteinase-9 upregulation after focal cerebral ischemia. Stroke 36, 1954-1959.
62. Wang Y. F., Tsirka S. E. and Strickland S. et al. (1998) Tissue plasminogen activator (tPA) increases neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice. Nat. Med. 4, 228-231.
63. Wang L., Zhang Z. G., Zhang R. L. et al. (2006) Matrix metalloproteinase 2 (MMP2) and MMP9 secreted by erythropoietin-activated endothelial cells promote neural progenitor cell migration. J. Neurosci. 26, 5996-6003.
64. Whitlock J. R., Heynen A. J. and Shuler M. G. et al. (2006) Learning induces long-term potentiation in the hippocampus. Science 313, 1093-1097.
65. Yang G., Kitagawa K., Matsushita K. et al. (1997) C57BL/6 strain is most susceptible to cerebral ischemia following bilateral common carotid occlusion among seven mouse strains: Selective neuronal death in the murine transient forebrain ischemia. Brain Res. 752, 209-218.
66. Yong V. W., Power C., Forsyth P. et al. (2001) Metalloproteinases in biology and pathology of the nervous system. Nat. Rev. Neurosci. 2, 502-511.
67. Zhao B. Q., Wang S., Kim H. Y. et al. (2006) Role of matrix metalloproteinases in delayed cortical responses after stroke. Nat. Med. 12, 441-445.