Metabolic stress response implicated in diabetic retinopathy: The role of calpain, and the therapeutic impact of calpain inhibitor

Neurobiology of Disease

Volumn 48, Issue 3, 2012, Pages 556-567

  Shanab, Ahmed Y ^a   Nakazawa, Toru ^a   Ryu, Morin ^a   Tanaka, Yuji ^a   Himori, Noriko ^a   Taguchi, Keiko ^a   Yasuda, Masayuki ^a   Watanabe, Ryo ^a   Takano, Jiro ^b   Saido, Takaomi ^b   Minegishi, Naoko ^a   Miyata, Toshio ^a   Abe, Toshiaki ^a   Yamamoto, Masayuki ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Calpain; Diabetic retinopathy; Neuroprotection; Oxidative stress; Retinal ganglion cell; Synaptophysin

Indexed keywords

CALPAIN 1; CALPAIN 2; CALPASTATIN; FLUOROGOLD; FODRIN; GLUCOSE; MESSENGER RNA; SNJ 1945; STREPTOZOCIN; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL DENSITY; CELL LOSS; CONTROLLED STUDY; CULTURE MEDIUM; DEGENERATIVE DISEASE; DIABETIC RETINOPATHY; ENZYME ACTIVATION; GENETIC MANIPULATION; HYPERGLYCEMIA; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LIPID DIET; MALE; METABOLIC STRESS; MOUSE; NERVE CELL LESION; NERVE CELL NECROSIS; NERVE FIBER DEGENERATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OPTIC NERVE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN SYNTHESIS INHIBITION; RETINA GANGLION CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CALPAIN; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; DIET, HIGH-FAT; GLYCOPROTEINS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRESS, PHYSIOLOGICAL;

EID: 84865565836     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.07.025     Document Type: Article

References (49)

1. Abu-El-Asrar A.M., Dralands L., Missotten L., Al-Jadaan I.A., Geboes K. Expression of apoptosis markers in the retinas of human subjects with diabetes. Invest. Ophthalmol. Vis. Sci. 2004, 45:2760-2766.
2. Camins A., Verdaguer E., Folch J., Pallas M. Involvement of calpain activation in neurodegenerative processes. CNS Drug Rev. 2006, 12:135-148.
3. Chihara E., Matsuoka T., Ogura Y., Matsumura M. Retinal nerve-fiber layer defect as an early manifestation of diabetic-retinopathy. Ophthalmology 1993, 100:1147-1151.
4. Costa V.P., de Faria J.M.L., Russ H. Retinal nerve fibre layer loss in patients with type 1 diabetes mellitus without retinopathy. Br. J. Ophthalmol. 2002, 86:725-728.
5. Cuerrier D., Moldoveanu T., Inoue J., Davies P.L., Campbell R.L. Calpain inhibition by alpha-ketoamide and cyclic hemiacetal inhibitors revealed by X-ray crystallography. Biochemistry 2006, 45:7446-7452.
6. Fong D.S., Aiello L., Gardner T.W., King G.L., Blankenship G., Cavallerano J.D., Ferris F.L., Klein R. Retinopathy in diabetes. Diabetes Care 2004, 27(Suppl. 1):S84-S87. American Diabetes A.
7. Frishman L.J., Shen F.F., Du L., Robson J.G., Harwerth R.S., Smith E.L., Carter-Dawson L., Crawford M.L. The scotopic electroretinogram of macaque after retinal ganglion cell loss from experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 1996, 37:125-141.
8. Goll D.E., Thompson V.F., Li H., Wei W., Cong J. The calpain system. Physiol. Rev. 2003, 83:731-801.
9. Hancock H.A., Kraft T.W. Oscillatory potential analysis and ERGs of normal and diabetic rats. Invest. Ophthalmol. Vis. Sci. 2004, 45:1002-1008.
10. Hanna R.A., Garcia-Diaz B.E., Davies P.L. Calpastatin simultaneously binds four calpains with different kinetic constants. FEBS Lett. 2007, 581:2894-2898.
11. Hanna R.A., Campbell R.L., Davies P.L. Calcium-bound structure of calpain and its mechanism of inhibition by calpastatin. Nature 2008, 456:409-412.
12. Hinokio Y., Suzuki S., Hirai M., Chiba M., Hirai A., Toyota T. Oxidative DNA damage in diabetes mellitus: its association with diabetic complications. Diabetologia 1999, 42:995-998.
13. Hu F.B. Globalization of diabetes: the role of diet, lifestyle, and genes. Diabetes Care 2011, 34:1249-1257.
14. Huang Y., Wang K.K. The calpain family and human disease. Trends Mol. Med. 2001, 7:355-362.
15. Itoh K., Chiba T., Takahashi S., Ishii T., Igarashi K., Katoh Y., Oyake T., Hayashi N., Satoh K., Hatayama I., Yamamoto M., Nabeshima Y. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 1997, 236:313-322.
16. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J.D., Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999, 13:76-86.
17. Kampfl A., Posmantur R., Nixon R., Grynspan F., Zhao X., Liu S.J., Newcomb J.K., Clifton G.L., Hayes R.L. mu-Calpain activation and calpain-mediated cytoskeletal proteolysis following traumatic brain injury. J. Neurochem. 1996, 67:1575-1583.
18. Kerrigan-Baumrind L.A., Quigley H.A., Pease M.E., Kerrigan D.F., Mitchell R.S. Number of ganglion cells in glaucoma eyes compared with threshold visual field tests in the same persons. Invest. Ophthalmol. Vis. Sci. 2000, 41:741-748.
19. Kizawa J., Machida S., Kobayashi T., Gotoh Y., Kurosaka D. Changes of oscillatory potentials and photopic negative response in patients with early diabetic retinopathy. Jpn. J. Ophthalmol. 2006, 50:367-373.
20. Knoferle J., Koch J.C., Ostendorf T., Michel U., Planchamp V., Vutova P., Tonges L., Stadelmann C., Bruck W., Bahr M., Lingor P. Mechanisms of acute axonal degeneration in the optic nerve in vivo. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:6064-6069.
21. Kurihara T., Ozawa Y., Nagai N., Shinoda K., Noda K., Imamura Y., Tsubota K., Okano H., Oike Y., Ishida S. Angiotensin II type 1 receptor signaling contributes to synaptophysin degradation and neuronal dysfunction in the diabetic retina. Diabetes 2008, 57:2191-2198.
22. Li Z., Cao B., Zhao B., Yang X., Fan M.Z., Yang J. Decreased expression of calpain and calpastatin mRNA during development is highly correlated with muscle protein accumulation in neonatal pigs. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2009, 152:498-503.
23. Ma H., Tochigi A., Shearer T.R., Azuma M. Calpain inhibitor SNJ-1945 attenuates events prior to angiogenesis in cultured human retinal endothelial cells. J. Ocul. Pharmacol. Ther. 2009, 25:409-414.
24. Mu J., Woods J., Zhou Y.P., Roy R.S., Li Z., Zycband E., Feng Y., Zhu L., Li C., Howard A.D., Moller D.E., Thornberry N.A., Zhang B.B. Chronic inhibition of dipeptidyl peptidase-4 with a sitagliptin analog preserves pancreatic beta-cell mass and function in a rodent model of type 2 diabetes. Diabetes 2006, 55:1695-1704.
25. Mullarkey C.J., Edelstein D., Brownlee M. Free radical generation by early glycation products: a mechanism for accelerated atherogenesis in diabetes. Biochem. Biophys. Res. Commun. 1990, 173:932-939.
26. Muroya S., Neath K.E., Nakajima I., Oe M., Shibata M., Ojima K., Chikuni K. Differences in mRNA expression of calpains, calpastatin isoforms and calpain/calpastatin ratios among bovine skeletal muscles. Anim. Sci. J. 2012, 83:252-259.
27. Nakazawa T., Nakazawa C., Matsubara A., Noda K., Hisatomi T., She H., Michaud N., Hafezi-Moghadam A., Miller J.W., Benowitz L.I. Tumor necrosis factor-alpha mediates oligodendrocyte death and delayed retinal ganglion cell loss in a mouse model of glaucoma. J. Neurosci. 2006, 26:12633-12641.
28. Nakazawa T., Takahashi H., Nishijima K., Shimura M., Fuse N., Tamai M., Hafezi-Moghadam A., Nishida K. Pitavastatin prevents NMDA-induced retinal ganglion cell death by suppressing leukocyte recruitment. J. Neurochem. 2007, 100:1018-1031.
29. Nakazawa T., Takeda M., Lewis G.P., Cho K.S., Jiao J., Wilhelmsson U., Fisher S.K., Pekny M., Chen D.F., Miller J.W. Attenuated glial reactions and photoreceptor degeneration after retinal detachment in mice deficient in glial fibrillary acidic protein and vimentin. Invest. Ophthalmol. Vis. Sci. 2007, 48:2760-2768.
30. 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 J.W. Monocyte chemoattractant protein 1 mediates retinal detachment-induced photoreceptor apoptosis. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:2425-2430.
31. Nakazawa T., Shimura M., Ryu M., Nishida K., Pages G., Pouyssegur J., Endo S. ERK1 plays a critical protective role against N-methyl-d-aspartate-induced retinal injury. J. Neurosci. Res. 2008, 86:136-144.
32. Nakazawa T., Shimura M., Mourin R., Kondo M., Yokokura S., Saido T.C., Nishida K., Endo S. Calpain-mediated degradation of G-substrate plays a critical role in retinal excitotoxicity for amacrine cells. J. Neurosci. Res. 2009, 87:1412-1423.
33. Nath R., Raser K.J., Stafford D., Hajimohammadreza I., Posner A., Allen H., Talanian R.V., Yuen P., Gilbertsen R.B., Wang K.K. 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. 1996, 319(Pt 3):683-690.
34. Oka T., Walkup R.D., Tamada Y., Nakajima E., Tochigi A., Shearer T.R., Azuma M. Amelioration of retinal degeneration and proteolysis in acute ocular hypertensive rats by 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. Neuroscience 2006, 141:2139-2145.
35. Pan H.Z., Zhang H., Chang D., Li H., Sui H. The change of oxidative stress products in diabetes mellitus and diabetic retinopathy. Br. J. Ophthalmol. 2008, 92:548-551.
36. Park H.R., Park M., Choi J., Park K.Y., Chung H.Y., Lee J. A high-fat diet impairs neurogenesis: involvement of lipid peroxidation and brain-derived neurotrophic factor. Neurosci. Lett. 2010, 482:235-239.
37. Perrin B.J., Huttenlocher A. Calpain. Int. J. Biochem. Cell Biol. 2002, 34:722-725.
38. Ray S.K., Fidan M., Nowak M.W., Wilford G.G., Hogan E.L., Banik N.L. Oxidative stress and Ca2+ influx upregulate calpain and induce apoptosis in PC12 cells. Brain Res. 2000, 852:326-334.
39. Resnikoff S., Pascolini D., Etya'ale D., Kocur I., Pararajasegaram R., Pokharel G.P., Mariotti S.P. Global data on visual impairment in the year 2002. Bull. World Health Organ. 2004, 82:844-851.
40. Ryu M., Yasuda M., Shi D., Shanab A.Y., Watanabe R., Himori N., Omodaka K., Yokoyama Y., Takano J., Saido T., Nakazawa T. Critical role of calpain in axonal damage-induced retinal ganglion cell death. J. Neurosci. Res. 2011.
41. Sano T., Umeda F., Hashimoto T., Nawata H., Utsumi H. Oxidative stress measurement by in vivo electron spin resonance spectroscopy in rats with streptozotocin-induced diabetes. Diabetologia 1998, 41:1355-1360.
42. Shaw J.E., Sicree R.A., Zimmet P.Z. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res. Clin. Pract. 2010, 87:4-14.
43. Shirasaki Y., Miyashita H., Yamaguchi M., Inoue J., Nakamura M. Exploration of orally available calpain inhibitors: peptidyl alpha-ketoamides containing an amphiphile at P3 site. Bioorg. Med. Chem. 2005, 13:4473-4484.
44. Shirasaki Y., Yamaguchi M., Miyashita H. Retinal penetration of calpain inhibitors in rats after oral administration. J. Ocul. Pharmacol. Ther. 2006, 22:417-424.
45. Srinivasan K., Viswanad B., Asrat L., Kaul C.L., Ramarao P. Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening. Pharmacol. Res. 2005, 52:313-320.
46. Stys P.K., Jiang Q. Calpain-dependent neurofilament breakdown in anoxic and ischemic rat central axons. Neurosci. Lett. 2002, 328:150-154.
47. Suzuki K., Hata S., Kawabata Y., Sorimachi H. Structure, activation, and biology of calpain. Diabetes 2004, 53(Suppl. 1):S12-S18.
48. Takano J., Tomioka M., Tsubuki S., Higuchi M., Iwata N., Itohara S., Maki M., Saido T.C. Calpain mediates excitotoxic DNA fragmentation via mitochondrial pathways in adult brains: evidence from calpastatin mutant mice. J. Biol. Chem. 2005, 280:16175-16184.
49. Wakabayashi T., Kosaka J., Mochii M., Miki Y., Mori T., Takamori Y., Yamada H. C38, equivalent to BM88, is developmentally expressed in maturing retinal neurons and enhances neuronal maturation. J. Neurochem. 2010, 112:1235-1248.