Calpain inhibition attenuates apoptosis of retinal ganglion cells in acute optic neuritis

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 7, 2011, Pages 4935-4941

  Smith, Amena W ^a   Das, Arabinda ^a   Guyton, M Kelly ^a   Ray, Swapan K ^b   Rohrer, Baerbel ^a   Banik, Naren L ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CALPASTATIN; CALPEPTIN; CASPASE 3; CASPASE 8; CYCLOOXYGENASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BAX; PROTEIN BCL 2; TRANSCRIPTION FACTOR POU4F1; CYSTEINE PROTEINASE INHIBITOR; DIPEPTIDE; RNA;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; DNA FRAGMENTATION; IMMUNOHISTOCHEMISTRY; MALE; NICK END LABELING; NONHUMAN; OPTIC NEURITIS; PRIORITY JOURNAL; RAT; RETINA GANGLION CELL; WESTERN BLOTTING; ACUTE DISEASE; ANIMAL; BIOSYNTHESIS; COMPARATIVE STUDY; DISEASE MODEL; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; INTRAPERITONEAL DRUG ADMINISTRATION; LEWIS RAT; METABOLISM; PATHOLOGY; TREATMENT OUTCOME;

ACUTE DISEASE; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CALPAIN; CYSTEINE PROTEINASE INHIBITORS; DIPEPTIDES; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; IN SITU NICK-END LABELING; INJECTIONS, INTRAPERITONEAL; MALE; OPTIC NEURITIS; RATS; RATS, INBRED LEW; RETINAL GANGLION CELLS; RNA; TREATMENT OUTCOME;

EID: 80052366491     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-7027     Document Type: Article

References (58)

1. Williams KC, Ulvestad E, Hickey WF. Immunology of multiple sclerosis. Clin Neurosci. 1994;2:229-245.
2. Arnold AC. Evolving management of optic neuritis and multiple sclerosis. Am J Ophthalmol. 2005;139:1101-1108.
3. Compston A, Sadovnick AD. Epidemiology and genetics of multiple sclerosis. Curr Opin Neurol Neurosurg. 1992;5:175-181.
4. Bitsch A, Schuchardt J, Bunkowski S, Kuhlmann T, Bruck W. Acute axonal injury in multiple sclerosis. Correlation with demyelination and inflammation. Brain. 2000;123:1174-1183.
5. Gartner S. Optic neuropathy in multiple sclerosis. Optic neuritis. AMA Arch Ophthalmol. 1953;50:718-726.
6. Hickman SJ, Toosy AT, Jones SJ, et al. A serial MRI study following optic nerve mean area in acute optic neuritis. Brain. 2004;127: 2498-2505.
7. Hickman SJ, Brex PA, Brierley CM, et al. Detection of optic nerve atrophy following a single episode of unilateral optic neuritis by MRI using a fat-saturated short-echo fast FLAIR sequence. Neuroradiology. 2001;43:123-128.
8. Inglese M, Ghezzi A, Bianchi S, et al. Irreversible disability and tissue loss in multiple sclerosis: a conventional and magnetization transfer magnetic resonance imaging study of the optic nerves. Arch Neurol. 2002;59:250-255.
9. Srinivasan VJ, Ko TH, Wojtkowski M, et al. Noninvasive volumetric imaging and morphometry of the rodent retina with high-speed, ultrahigh-resolution optical coherence tomography. Invest Ophthalmol Vis Sci. 2006;47:5522-5528.
10. Ruggeri M, Wehbe H, Jiao S, et al. In vivo three-dimensional high-resolution imaging of rodent retina with spectral-domain optical coherence tomography. Invest Ophthalmol Vis Sci. 2007;48: 1808-1814.
11. Sergott RC, Frohman E, Glanzman R, Al-Sabbagh A. The role of optical coherence tomography in multiple sclerosis: expert panel consensus. J Neurol Sci. 2007;263:3-14.
12. Shields DC, Tyor WR, Deibler GE, Banik NL. Increased calpain expression in experimental demyelinating optic neuritis: an immunocytochemical study. Brain Res. 1998;784:299-304.
13. Guyton MK, Sribnick EA, Ray SK, Banik NL. A role for calpain in optic neuritis. Ann NY Acad Sci. 2005;1053:48-54.
14. Shields DC, Schaecher KE, Saido TC, Banik NL. A putative mechanism of demyelination in multiple sclerosis by a proteolytic enzyme, calpain. Proc Natl Acad Sci USA. 1999;96:11486-11491.
15. Wu HY, Tomizawa K, Matsui H. Calpain-calcineurin signaling in the pathogenesis of calcium-dependent disorder. Acta Med Okayama. 2007;61:123-137.
16. Tamada Y, Fukiage C, Mizutani K, et al. Calpain inhibitor, SJA6017, reduces the rate of formation of selenite cataract in rats. Curr Eye Res. 2001;22:280-285.
17. Kupina NC, Nath R, Bernath EE, et al. The novel calpain inhibitor SJA6017 improves functional outcome after delayed administration in a mouse model of diffuse brain injury. J Neurotrauma. 2001;18:1229-1240.
18. Sharma AK, Rohrer B. Sustained elevation of intracellular cGMP causes oxidative stress triggering calpain-mediated apoptosis in photoreceptor degeneration. Curr Eye Res. 2007;32:259-269.
19. Das A, Sribnick EA, Wingrave JM, et al. Calpain activation in apoptosis of ventral spinal cord 4.1 (VSC4.1) motoneurons exposed to glutamate: calpain inhibition provides functional neuroprotection. J Neurosci Res. 2005;81:551-562.
20. Das A, Garner DP, Del Re AM, et al. Calpeptin provides functional neuroprotection to rat retinal ganglion cells following Ca2+ influx. Brain Res. 2006;1084:146-157.
21. McKernan DP, Guerin MB, O'Brien CJ, Cotter TG. A key role for calpains in retinal ganglion cell death. Invest Ophthalmol Vis Sci. 2007;48:5420-5430.
22. Cuzzocrea S, McDonald MC, Mazzon E, et al. Calpain inhibitor I reduces the development of acute and chronic inflammation. Am J Pathol. 2000;157:2065-2079.
23. Schaecher K, Goust JM, Banik NL. The effects of calpain inhibition on IkB alpha degradation after activation of PBMCs: identification of the calpain cleavage sites. Neurochem Res. 2004;29:1443-1451.
24. Guyton MK, Das A, Samantaray S, et al. Calpeptin attenuated inflammation, cell death, and axonal damage in animal model of multiple sclerosis. J Neurosci Res. 2010;88:2398-2408.
25. Nadal-Nicolas FM, Jimenez-Lopez M, Sobrado-Calvo P, et al. Brn3a as a marker of retinal ganglion cells: qualitative and quantitative time course studies in naive and optic nerve-injured retinas. Invest Ophthalmol Vis Sci. 2009;50:3860-3868.
26. Sánchez-Migallón MC, Nadal-Nicolás FM, Jiménez-López M, Sobrado-Calvo P, Vidal-Sanz M, Agudo-Barriuso M. Brain derived neurotrophic factor maintains Brn3a expression in axotomized rat retinal ganglion cells. Exp Eye Res. 2011;92:260-267.
27. Helfer B, Boswell BC, Finlay D, et al. Caspase-8 promotes cell motility and calpain activity under nonapoptotic conditions. Cancer Res. 2006;66:4273-4278.
28. Frisch SM. Caspase-8: fly or die. Cancer Res. 2008;68:4491-4493.
29. Vaisid T, Barnoy S, Kosower NS. Calpain activates caspase-8 in neuron-like differentiated PC12 cells via the amyloid-beta-peptide and CD95 pathways. Int J Biochem Cell Biol. 2009;41:2450-2458.
30. Lawen A. Apoptosis: an introduction. Bioessays. 2003;25:888-896.
31. Gu Q, Wang JD, Xia HH, et al. Activation of the caspase-8/Bid and Bax pathways in aspirin-induced apoptosis in gastric cancer. Carcinogenesis. 2005;26:541-546.
32. Roth W, Stenner-Liewen F, Pawlowski K, Godzik A, Reed JC. Identification and characterization of DEDD2, a death effector domain-containing protein. J Biol Chem. 2002;277:7501-7508.
33. Drescher KM, Whittum-Hudson JA. Herpes simplex virus type 1 alters transcript levels of tumor necrosis factor-alpha and interleukin-6 in retinal glial cells. Invest Ophthalmol Vis Sci. 1996;37: 2302-2312.
34. Roberge FG, Caspi RR, Chan CC, Nussenblatt RB. Inhibition of T lymphocyte proliferation by retinal glial Muller cells: reversal of inhibition by glucocorticoids. J Autoimmun. 1991;4:307-314.
35. Gramlich OW, Joachim SC, Gottschling PF, et al. Ophthalmopathology in rats with MBP-induced experimental autoimmune encephalomyelitis. Graefes Arch Clin Exp Ophthalmol. In press.
36. Koeberle PD, Ball AK. Nitric oxide synthase inhibition delays axonal degeneration and promotes the survival of axotomized retinal ganglion cells. Exp Neurol. 1999;158:366-381.
37. Brambilla R, Bracchi-Ricard V, Hu WH, et al. Inhibition of astroglial nuclear factor kappaB reduces inflammation and improves functional recovery after spinal cord injury. J Exp Med. 2005;202:145-156.
38. Li C, Chen S, Yue P, et al. Proteasome inhibitor PS-341 (bortezomib) induces calpain-dependent IkappaB(alpha) degradation. J Biol Chem. 2010;285:16096-16104.
39. Frohman EM, Dwyer MG, Frohman T, et al. Relationship of optic nerve and brain conventional and non-conventional MRI measures and retinal nerve fiber layer thickness, as assessed by OCT and GDx: a pilot study. J Neurol Sci. 2009;282:96-105.
40. Agudo M, Perez-Marin MC, Sobrado-Calvo P, et al. Immediate upregulation of proteins belonging to different branches of the apoptotic cascade in the retina after optic nerve transection and optic nerve crush. Invest Ophthalmol Vis Sci. 2009;50:424-431.
41. Huang W, Fileta J, Rawe I, Qu J, Grosskreutz CL. Calpain activation in experimental glaucoma. Invest Ophthalmol Vis Sci. 2010;51: 3049-3054.
42. Kermer P, Klocker N, Labes M, Bahr M. Inhibition of CPP32-like proteases rescues axotomized retinal ganglion cells from secondary cell death in vivo. J Neurosci. 1998;18:4656-4662.
43. Salmena L, Lemmers B, Hakem A, et al. Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev. 2003;17:883-895.
44. Kang TB, Ben-Moshe T, Varfolomeev EE, et al. Caspase-8 serves both apoptotic and nonapoptotic roles. J Immunol. 2004;173: 2976-2984.
45. Wood DE, Newcomb EW. Cleavage of Bax enhances its cell death function. Exp Cell Res. 2000;256:375-382.
46. Li P, Nijhawan D, Budihardjo I, et al. Cytochrome c and dATPdependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 1997;91:479-489.
47. Gao XY, Kuang HY, Zou W, Liu XM, Lin HB, Yang Y. The timing of re-institution of good blood glucose control affects apoptosis and expression of Bax and Bcl-2 in the retina of diabetic rats. Mol Biol Rep. 2009;36:1977-1982.
48. Qiu W, Wei R, Zhang C, Leng W, Wang W. A glycine site-specific NMDA receptor antagonist protects retina ganglion cells from ischemic injury by modulating apoptotic cascades. J Cell Physiol. 2010;223:819-826.
49. van Loo G, De Lorenzi R, Schmidt H, et al. Inhibition of transcription factor NF-kappaB in the central nervous system ameliorates autoimmune encephalomyelitis in mice. Nat Immunol. 2006;7: 954-961.
50. Brambilla R, Persaud T, Hu X, et al. Transgenic inhibition of astroglial NF-kappa B improves functional outcome in experimental autoimmune encephalomyelitis by suppressing chronic central nervous system inflammation. J Immunol. 2009;182:2628-2640.
51. Towler HM, Lightman S. Symptomatic intraocular inflammation in multiple sclerosis. Clin Exp Ophthalmol. 2000;28:97-102.
52. Adamus G, Amundson D, Vainiene M, et al. Myelin basic protein specific T-helper cells induce experimental anterior uveitis. J Neurosci Res. 1996;44:513-518.
53. Adamus G, Manczak M, Sugden B, Arendt A, Hargrave PA, Offner H. Epitope recognition and T cell receptors in recurrent autoimmune anterior uveitis in Lewis rats immunized with myelin basic protein. J Neuroimmunol. 2000;108:122-130.
54. Adamus G, Sugden B, Arendt A, Hargrave PA. Importance of cryptic myelin basic protein epitopes in the pathogenicity of acute and recurrent anterior uveitis associated with EAE. J Neuroimmunol. 2001;113:212-219.
55. Zheng X, Li PH, Song SF. Expression of glial fibrillary acidic protein in retina of rats in acute experimental autoimmune encephalomyelitis [in Chinese]. Sichuan Da Xue Xue Bao Yi Xue Ban. 2008;39:719-722.
56. Talman LS, Bisker ER, Sackel DJ, et al. Longitudinal study of vision and retinal nerve fiber layer thickness in multiple sclerosis. Ann Neurol. 2010;67:749-760.
57. Burkholder BM, Osborne B, Loguidice MJ, et al. Macular volume determined by optical coherence tomography as a measure of neuronal loss in multiple sclerosis. Arch Neurol. 2009;66:1366-1372.
58. Salter AR, Conger A, Frohman TC, et al. Retinal architecture predicts pupillary reflex metrics in MS. Mult Scler. 2009;15:479-486.