Critical role of calpain in axonal damage-induced retinal ganglion cell death

Journal of Neuroscience Research

Volumn 90, Issue 4, 2012, Pages 802-815

  Ryu, Morin ^a   Yasuda, Masayuki ^a   Shi, Dong ^a,b   Shanab, Ahmed Y ^a   Watanabe, Ryo ^a   Himori, Noriko ^a   Omodaka, Kazuko ^a   Yokoyama, Yu ^a   Takano, Jiro ^c   Saido, Takaomi ^c   Nakazawa, Toru ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b CHINA MEDICAL UNIVERSITY   (China)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Axonal damage; Calpastatin; Glaucoma; Neuroprotection; SNJ1945

Indexed keywords

CALPAIN; CALPASTATIN; FLUOROGOLD; FODRIN; GELATIN SPONGE; SNJ 1945; TUBULIN; UNCLASSIFIED DRUG; VINBLASTINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL LABELING; CELL SURVIVAL; CONTROLLED STUDY; GLAUCOMA; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE CRUSH; NERVE FIBER; NERVE INJURY; NONHUMAN; OPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; RETINA GANGLION CELL; SIGNAL TRANSDUCTION;

AMINO ACIDS; ANIMALS; AXONS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM-BINDING PROTEINS; CALPAIN; CARBAMATES; CARRIER PROTEINS; CELL COUNT; CELL DEATH; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; NEUROFILAMENT PROTEINS; OPTIC NERVE INJURIES; RETINA; RETINAL GANGLION CELLS; STILBAMIDINES; TIME FACTORS; TUBULIN;

EID: 84856717523     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22800     Document Type: Article

References (47)

1. Ambati J, Chalam KV, Chawla DK, D'Angio CT, Guillet EG, Rose SJ, Vanderlinde RE, Ambati BK. 1997. Elevated gamma-aminobutyric acid, glutamate, and vascular endothelial growth factor levels in the vitreous of patients with proliferative diabetic retinopathy. Arch Ophthalmol 115: 1161-1166.
2. Anderson DR, Drance SM, Schulzer M. 1998. The effectiveness of intraocular pressure reduction in the treatment of normal-tension glaucoma. Collaborative Normal-Tension Glaucoma Study Group. Am J Ophthalmol 126: 498-505.
3. Azuma M, Shearer TR. 2008. The role of calcium-activated protease calpain in experimental retinal pathology. Surv Ophthalmol 53: 150-163.
4. Bizat N, Hermel JM, Boyer F, Jacquard C, Creminon C, Ouary S, Escartin C, Hantraye P, Kajewski S, Brouillet E. 2003a. Calpain is a major cell death effector in selective striatal degeneration induced in vivo by 3-nitropropionate: implications for Huntington's disease. J Neurosci 23: 5020-5030.
5. Bizat N, Hermel JM, Humbert S, Jacquard C, Creminon C, Escartin C, Saudou F, Krajewski S, Hantraye P, Brouillet E. 2003b. In vivo calpain/caspase cross-talk during 3-nitropropionic acid-induced striatal degeneration: implication of a calpain-mediated cleavage of active caspase-3. J Biol Chem 278: 43245-43253.
6. Camins A, Verdaguer E, Folch J, Pallas M. 2006. Involvement of calpain activation in neurodegenerative processes. CNS Drug Rev 12: 135-148.
7. Chatterjee PK, Todorovic Z, Sivarajah A, Mota-Filipe H, Brown PA, Stewart KN, Mazzon E, Cuzzocrea S, Thiemermann C. 2005. Inhibitors of calpain activation (PD150606 and E-64) and renal ischemia-reperfusion injury. Biochem Pharmacol 69: 1121-1131.
8. Chiu K, Lam TT, Ying Li WW, Caprioli J, Kwong Kwong JM. 2005. Calpain and N-methyl-D-aspartate (NMDA)-induced excitotoxicity in rat retinas. Brain Res 1046: 207-215.
9. Coleman M. 2005. Axon degeneration mechanisms: commonality amid diversity. Nat Rev Neurosci 6: 889-898.
10. Deng J, Wu DZ, Gao R. 2000. Detection of glutamate and gamma-aminobutyric acid in vitreous of patients with proliferative diabetic retinopathy. Yan Ke Xue Bao 16: 199-202.
11. Guttmann RP, Sokol S, Baker DL, Simpkins KL, Dong Y, Lynch DR. 2002. Proteolysis of the N-methyl-D-aspartate receptor by calpain in situ. J Pharmacol Exp Ther 302: 1023-1030.
12. Harris F, Biswas S, Singh J, Dennison S, Phoenix DA. 2006. Calpains and their multiple roles in diabetes mellitus. Ann N Y Acad Sci 1084: 452-480.
13. Heijl A, Leske MC, Bengtsson B, Hyman L, Hussein M. 2002. Reduction of intraocular pressure and glaucoma progression: results from the Early Manifest Glaucoma Trial. Arch Ophthalmol 120: 1268-1279.
14. Higuchi M, Tomioka M, Takano J, Shirotani K, Iwata N, Masumoto H, Maki M, Itohara S, Saido TC. 2005. Distinct mechanistic roles of calpain and caspase activation in neurodegeneration as revealed in mice overexpressing their specific inhibitors. J Biol Chem 280: 15229-15237.
15. Huang W, Fileta J, Rawe I, Qu J, Grosskreutz CL. 2010. Calpain activation in experimental glaucoma. Invest Ophthalmol Vis Sci 51: 3049-3054.
16. Huang Y, Wang KK. 2001. The calpain family and human disease. Trends Mol Med 7: 355-362.
17. Iwase A, Suzuki Y, Araie M, Yamamoto T, Abe H, Shirato S, Kuwayama Y, Mishima HK, Shimizu H, Tomita G, Inoue Y, Kitazawa Y. 2004. The prevalence of primary open-angle glaucoma in Japanese: the Tajimi Study. Ophthalmology 111: 1641-1648.
18. Koike T, Yang Y, Suzuki K, Zheng X. 2008. Axon & dendrite degeneration: its mechanisms and protective experimental paradigms. Neurochem Int 52: 751-760.
19. Lam TT, Siew E, Chu R, Tso MO. 1997. Ameliorative effect of MK-801 on retinal ischemia. J Ocul Pharmacol Ther 13: 129-137.
20. Levin LA. 2003. Retinal ganglion cells and neuroprotection for glaucoma. Surv Ophthalmol 48( Suppl 1): S21-S24.
21. Ma H, Tochigi A, Shearer TR, Azuma M. 2009. Calpain inhibitor SNJ-1945 attenuates events prior to angiogenesis in cultured human retinal endothelial cells. J Ocul Pharmacol Ther 25: 409-414.
22. Marzocco S, Di Paola R, Autore G, Mazzon E, Pinto A, Caputi AP, Thiemermann C, Cuzzocrea S. 2004. Calpain inhibitor I reduces intestinal ischemia-reperfusion injury in the rat. Shock 21: 38-44.
23. Matini P, Moroni F, Lombardi G, Faussone-Pellegrini MS. 1997. Ultrastructural and biochemical studies on the neuroprotective effects of excitatory amino acid antagonists in the ischemic rat retina. Exp Neurol 146: 419-434.
24. McKernan DP, Guerin MB, O'Brien CJ, Cotter TG. 2007. A key role for calpains in retinal ganglion cell death. Invest Ophthalmol Vis Sci 48: 5420-5430.
25. Mizukoshi S, Nakazawa M, Sato K, Ozaki T, Metoki T, Ishiguro S. 2010. Activation of mitochondrial calpain and release of apoptosis-inducing factor from mitochondria in RCS rat retinal degeneration. Exp Eye Res 91: 353-361.
26. Nakazawa T, Tamai M, Mori N. 2002. Brain-derived neurotrophic factor prevents axotomized retinal ganglion cell death through MAPK and PI3K signaling pathways. Invest Ophthalmol Vis Sci 43: 3319-3326.
27. Nakazawa T, Shimura M, Endo S, Takahashi H, Mori N, Tamai M. 2005. N-methyl-D-aspartic acid suppresses Akt activity through protein phosphatase in retinal ganglion cells. Mol Vis 11: 1173-1182.
28. Nakazawa T, Nakazawa C, Matsubara A, Noda K, Hisatomi T, She H, Michaud N, Hafezi-Moghadam A, Miller JW, Benowitz LI. 2006. Tumor necrosis factor-alpha mediates oligodendrocyte death and delayed retinal ganglion cell loss in a mouse model of glaucoma. J Neurosci 26: 12633-12641.
29. Nakazawa T, Hisatomi T, Nakazawa C, Noda K, Maruyama K, She H, Matsubara A, Miyahara S, Nakao S, Yin Y, Benowitz L, Hafezi-Moghadam A, Miller JW. 2007a. Monocyte chemoattractant protein 1 mediates retinal detachment-induced photoreceptor apoptosis. Proc Natl Acad Sci U S A 104: 2425-2430.
30. Nakazawa T, Takahashi H, Nishijima K, Shimura M, Fuse N, Tamai M, Hafezi-Moghadam A, Nishida K. 2007b. Pitavastatin prevents NMDA-induced retinal ganglion cell death by suppressing leukocyte recruitment. J Neurochem 100: 1018-1031.
31. Nakazawa T, Shimura M, Mourin R, Kondo M, Yokokura S, Saido TC, Nishida K, Endo S. 2009. Calpain-mediated degradation of G-substrate plays a critical role in retinal excitotoxicity for amacrine cells. J Neurosci Res 87: 1412-1423.
32. Nath R, Raser KJ, Stafford D, Hajimohammadreza I, Posner A, Allen H, Talanian RV, Yuen P, Gilbertsen RB, Wang KK. 1996. Non-erythroid alpha-spectrin breakdown by calpain and interleukin 1 beta-converting-enzyme-like protease(s) in apoptotic cells: contributory roles of both protease families in neuronal apoptosis. Biochem J 319: 683-690.
33. Paquet-Durand F, Sanges D, McCall J, Silva J, van Veen T, Marigo V, Ekstrom P. 2010. Photoreceptor rescue and toxicity induced by different calpain inhibitors. J Neurochem 115: 930-940.
34. Patrick GN, Zukerberg L, Nikolic M, de la Monte S, Dikkes P, Tsai LH. 1999. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 402: 615-622.
35. Qu J, Wang D, Grosskreutz CL. 2010. Mechanisms of retinal ganglion cell injury and defense in glaucoma. Exp Eye Res 91: 48-53.
36. Quigley HA. 1996. Number of people with glaucoma worldwide. Br J Ophthalmol 80: 389-393.
37. Quigley HA, McKinnon SJ, Zack DJ, Pease ME, Kerrigan-Baumrind LA, Kerrigan DF, Mitchell RS. 2000. Retrograde axonal transport of BDNF in retinal ganglion cells is blocked by acute IOP elevation in rats. Invest Ophthalmol Vis Sci 41: 3460-3466.
38. Resnikoff S, Pascolini D, Etya'ale D, Kocur I, Pararajasegaram R, Pokharel GP, Mariotti SP. 2004. Global data on visual impairment in the year 2002. Bull WHO 82: 844-851.
39. Sheppard A, Wu J, Rutishauser U, Lynch G. 1991. Proteolytic modification of neural cell adhesion molecule (NCAM) by the intracellular proteinase calpain. Biochim Biophys Acta 1076: 156-160.
40. Shimazawa M, Suemori S, Inokuchi Y, Matsunaga N, Nakajima Y, Oka T, Yamamoto T, Hara H. 2010. A novel calpain inhibitor, ((1S)-1-((((1S)-1-benzyl-3-cyclopropylamino-2, 3-di-oxopropyl)amino)carbony l)-3-methylbutyl)carbamic acid 5-methoxy-3-oxapentyl ester (SNJ-1945), reduces murine retinal cell death in vitro and in vivo. J Pharmacol Exp Ther 332: 380-387.
41. Shirasaki Y, Yamaguchi M, Miyashita H. 2006. Retinal penetration of calpain inhibitors in rats after oral administration. J Ocul Pharmacol Ther 22: 417-424.
42. Simpkins KL, Guttmann RP, Dong Y, Chen Z, Sokol S, Neumar RW, Lynch DR. 2003. Selective activation induced cleavage of the NR2B subunit by calpain. J Neurosci 23: 11322-11331.
43. Stys PK. 2005. General mechanisms of axonal damage and its prevention. J Neurol Sci 233: 3-13.
44. Suzuki Y, Iwase A, Araie M, Yamamoto T, Abe H, Shirato S, Kuwayama Y, Mishima HK, Shimizu H, Tomita G, Inoue Y, Kitazawa Y. 2006. Risk factors for open-angle glaucoma in a Japanese population: the Tajimi Study. Ophthalmology 113: 1613-1617.
45. Takano J, Tomioka M, Tsubuki S, Higuchi M, Iwata N, Itohara S, Maki M, Saido TC. 2005. Calpain mediates excitotoxic DNA fragmentation via mitochondrial pathways in adult brains: evidence from calpastatin mutant mice. J Biol Chem 280: 16175-16184.
46. Weinreb RN, Khaw PT. 2004. Primary open-angle glaucoma. Lancet 363: 1711-1720.
47. Wu HY, Tomizawa K, Oda Y, Wei FY, Lu YF, Matsushita M, Li ST, Moriwaki A, Matsui H. 2004. Critical role of calpain-mediated cleavage of calcineurin in excitotoxic neurodegeneration. J Biol Chem 279: 4929-4940.