Involvement of caspase-6 and caspase-8 in neuronal apoptosis and the regenerative failure of injured retinal ganglion cells

Journal of Neuroscience

Volumn 31, Issue 29, 2011, Pages 10494-10505

  Monnier, Philippe P ^b,c   D'Onofrio, Philippe M ^a   Magharious, Mark ^a   Hollander, Adam C ^a   Tassew, Nardos ^b,c   Szydlowska, Kinga ^c   Tymianski, Michael ^c   Koeberle, Paulo D ^a  

^a Department of Surgery   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 6; CASPASE 8;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL REGENERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; FEMALE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; NERVE CELL; NERVE FIBER DEGENERATION; NERVE TRANSECTION; NONHUMAN; OPTIC NERVE; PRIORITY JOURNAL; RAT; RETINA GANGLION CELL; UPREGULATION;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; AXONS; CASPASE 6; CASPASE 8; CELL SURVIVAL; CHOLERA TOXIN; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; ENZYME INHIBITORS; FEMALE; GAP-43 PROTEIN; INJECTIONS, INTRAOCULAR; MALE; MYELIN SHEATH; NERVE REGENERATION; OPTIC NERVE INJURIES; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RETINAL GANGLION CELLS; RETROGRADE DEGENERATION; STILBAMIDINES;

EID: 79960679121     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0148-11.2011     Document Type: Article

References (85)

1. Ahmed Z, Berry M, Logan A (2009) ROCK inhibition promotes adult retinal ganglion cell neurite outgrowth only in the presence of growth promoting factors. Mol Cell Neurosci 42:128-133.
2. Bähr M (2000) Live or let die-retinal ganglion cell death and survival during development and in the lesioned adult CNS. Trends Neurosci 23:483-490.
3. Barron KD, Dentinger MP, Krohel G, Easton SK, Mankes R (1986) Qualitative and quantitative ultrastructural observations on retinal ganglion cell layer of rat after intraorbital optic nerve crush. J Neurocytol 15:345-362.
4. Baumgartner R, Meder G, Briand C, Decock A, D'arcy A, Hassiepen U, Morse R, Renatus M (2009) The crystal structure of caspase-6, a selective effector of axonal degeneration. Biochem J 423:429-439.
5. Berkelaar M, Clarke DB, Wang YC, Bray GM, Aguayo AJ (1994) Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J Neurosci 14:4368-4374.
6. Berry M, Carlile J, Hunter A (1996) Peripheral nerve explants grafted into the vitreous body of the eye promote the regeneration of retinal ganglion cell axons severed in the optic nerve. J Neurocytol 25:147-170.
7. Cao Z, Gao Y, Deng K, Williams G, Doherty P, Walsh FS (2010) Receptors for myelin inhibitors: structures and therapeutic opportunities. Mol Cell Neurosci 43:1-14.
8. Chaudhary P, Ahmed F, Quebada P, Sharma SC (1999) Caspase inhibitors block the retinal ganglion cell death following optic nerve transection. Brain Res Mol Brain Res 67:36-45.
9. Chen C, Chen X, Yin X, Yuan R, Wang B, Ye J (2009) NgR RNA interference, combined with zymosan intravitreal injection, enhances optic nerve regeneration. J Neurochem 110:1628-1634.
10. Chen TJ, Gehler S, Shaw AE, Bamburg JR, Letourneau PC (2006) Cdc42 participates n the regulation of ADF/cofilin and retinal growth cone filopodia by brain-derived neurotrophic factor. J Neurobiol 66:103-114.
11. Cheung N, Mitchell P, Wong TY (2010) Diabetic retinopathy. Lancet 376:124-136.
12. Cheung ZH, Chan YM, Siu FK, Yip HK, Wu W, Leung MC, So KF (2004) Regulation of caspase activation in axotomized retinal ganglion cells. Mol Cell Neurosci 25:383-393.
13. Chu W, Rothfuss J, Chu Y, Zhou D, Mach RH (2009) Synthesis and in vitro evaluation of sulfonamide isatin Michael acceptors as small molecule inhibitors of caspase-6. J Med Chem 52:2188-2191.
14. Cowling V, Downward J (2002) Caspase-6 is the direct activator of caspase-8 in the cytochrome c-induced apoptosis pathway: absolute requirement for removal of caspase-6 prodomain. Cell Death Differ 9:1046-1056.
15. Cui Q, Cho KS, So KF, Yip HK (2004) Synergistic effect of Nogoneutralizing antibody IN-1 and ciliary neurotrophic factor on axonal regeneration in adult rodent visual systems. J Neurotrauma 21:617-625.
16. DeBellard ME, Tang S, Mukhopadhyay G, Shen YJ, Filbin MT (1996) Myelin-associated glycoprotein inhibits axonal regeneration from a variety of neurons via interaction with a sialoglycoprotein. Mol Cell Neurosci 7:89-101.
17. Degterev A, Boyce M, Yuan J (2003) A decade of caspases. Oncogene 22:8543-8567.
18. Ehrenschwender M, Siegmund D, Wicovsky A, Kracht M, Dittrich-Breiholz O, Spindler V, Waschke J, Kalthoff H, Trauzold A, Wajant H (2010) Mutant PIK3CA licenses TRAIL and CD95L to induce non-apoptotic caspase-8-mediated ROCK activation. Cell Death Differ 17:1435-1447.
19. Finn JT, Weil M, Archer F, Siman R, Srinivasan A, Raff MC (2000) Evidence that Wallerian degeneration and localized axon degeneration induced by local neurotrophin deprivation do not involve caspases. J Neurosci 20:1333-1341.
20. Fischer D, He Z, Benowitz LI (2004) Counteracting the Nogo receptor enhances optic nerve regeneration if retinal ganglion cells are in an active growth state. J Neurosci 24:1646-1651.
21. Fischer U, Stroh C, Schulze-Osthoff K (2006) Unique and overlapping substrate specificities of caspase-8 and caspase-10. Oncogene 25:152-159.
22. Fournier AE, Gould GC, Liu BP, Strittmatter SM (2002) Truncated soluble Nogo receptor binds Nogo-66 and blocks inhibition of axon growth by myelin. J Neurosci 22:8876-8883.
23. Fournier AE, Takizawa BT, Strittmatter SM (2003) Rho kinase inhibition enhances axonal regeneration in the injured CNS. J Neurosci 23:1416-1423.
24. Graham RK, Deng Y, Slow EJ, Haigh B, Bissada N, Lu G, Pearson J, Shehadeh J, Bertram L, Murphy Z, Warby SC, Doty CN, Roy S, Wellington CL, Leavitt BR, Raymond LA, Nicholson DW, Hayden MR (2006) Cleavage at the caspase-6 site is required for neuronal dysfunction and degeneration due to mutant huntingtin. Cell 125:1179-1191.
25. Guo H, Albrecht S, Bourdeau M, Petzke T, Bergeron C, LeBlanc AC (2004) Active caspase-6 and caspase-6-cleaved tau in neuropil threads, neuritic plaques, and neurofibrillary tangles of Alzheimer's disease. Am J Pathol 165:523-531.
26. Hartmann A, Troadec JD, Hunot S, Kikly K, Faucheux BA, Mouatt-Prigent A, Ruberg M, Agid Y, Hirsch EC (2001) Caspase-8 is an effector in apoptotic death of dopaminergic neurons in Parkinson's disease, but pathway inhibition results in neuronal necrosis. J Neurosci 21:2247-2255.
27. Ho CC, Rideout HJ, Ribe E, Troy CM, Dauer WT (2009) The Parkinson disease protein leucine-rich repeat kinase 2 transduces death signals via Fas-associated protein with death domain and caspase-8 in a cellular model of neurodegeneration. J Neurosci 29:1011-1016.
28. Horner PJ, Gage FH (2000) Regenerating the damaged central nervous system. Nature 407:963-970.
29. Inoue S, Browne G, Melino G, Cohen GM (2009) Ordering of caspases in cells undergoing apoptosis by the intrinsic pathway. Cell Death Differ 16:1053-1061.
30. Ivins KJ, Thornton PL, Rohn TT, Cotman CW (1999) Neuronal apoptosis induced by beta-amyloid is mediated by caspase-8. Neurobiol Dis 6:440-449.
31. Kermer P, Klöcker N, Labes M, Bähr M (1998) Inhibition of CPP32-like proteases rescues axotomized retinal ganglion cells from secondary cell death in vivo. J Neurosci 18:4656-4662.
32. Kermer P, Klöcker N, Bähr M (1999) Long-term effect of inhibition of ced 3-like caspases on the survival of axotomized retinal ganglion cells in vivo. Exp Neurol 158:202-205.
33. Kermer P, Ankerhold R, Klöcker N, Krajewski S, Reed JC, Bähr M (2000) Caspase-9: involvement in secondary death of axotomized rat retinal ganglion cells in vivo. Brain Res Mol Brain Res 85:144-150.
34. Kim HS, Park CK (2005) Retinal ganglion cell death is delayed by activation of retinal intrinsic cell survival program. Brain Res 1057:17-28.
35. Klaiman G, Petzke TL, Hammond J, Leblanc AC (2008) Targets of caspase-6 activity in human neurons and Alzheimer disease. Mol Cell Proteomics 7:1541-1555.
36. Koeberle PD, Bähr M (2004) Growth and guidance cues for regenerating axons: where have they gone? J Neurobiol 59:162-180.
37. Koeberle PD, Bähr M (2008) The upregulation of GLAST-1 is an indirect antiapoptotic mechanism of GDNF and neurturin in the adult CNS. Cell Death Differ 15:471-483.
38. Koeberle PD, Tura A, Tassew NG, Schlichter LC, Monnier PP (2010) The repulsive guidance molecule, RGMa, promotes retinal ganglion cell survival in vitro and in vivo. Neuroscience 169:495-504.
39. Kuida K, Zheng TS, Na S, Kuan C, Yang D, Karasuyama H, Rakic P, Flavell RA (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384:368-372.
40. LeBlanc A, Liu H, Goodyer C, Bergeron C, Hammond J (1999) Caspase-6 role in apoptosis of human neurons, amyloidogenesis, and Alzheimer's disease. J Biol Chem 274:23426-23436.
41. Leon S, Yin Y, Nguyen J, Irwin N, Benowitz LI (2000) Lens injury stimulates axon regeneration in the mature rat optic nerve. J Neurosci 20:4615-4626.
42. Li M, Shibata A, Li C, Braun PE, McKerracher L, Roder J, Kater SB, David S (1996) Myelin-associated glycoprotein inhibits neurite/axon growth and causes growth cone collapse. J Neurosci Res 46:404-414.
43. Lingor P, Teusch N, Schwarz K, Mueller R, Mack H, Bähr M, Mueller BK (2007) Inhibition of Rho kinase (ROCK) increases neurite outgrowth on chondroitin sulphate proteoglycan in vitro and axonal regeneration in the adult optic nerve in vivo. J Neurochem 103:181-189.
44. Lingor P, Tönges L, Pieper N, Bermel C, Barski E, Planchamp V, Bähr M (2008) ROCK inhibition and CNTF interact on intrinsic signalling pathways and differentially regulate survival and regeneration in retinal ganglion cells. Brain 131:250-263.
45. Lund LM, Machado VM, McQuarrie IG (2002) Increased beta-actin and tubulin polymerization in regrowing axons: relationship to the conditioning lesion effect. Exp Neurol 178:306-312.
46. Matsui T, Ramasamy K, Ingelsson M, Fukumoto H, Conrad C, Frosch MP, Irizarry MC, Yuan J, Hyman BT (2006) Coordinated expression of caspase 8, 3 and 7 mRNA in temporal cortex of Alzheimer disease: relationship to formic acid extractableAβ42 levels. J Neuropathol Exp Neurol 65:508-515.
47. Mattson MP (2006) Neuronal life-and-death signaling, apoptosis, and eurodegenerative disorders. Antioxid Redox Signal 8:1997-2006.
48. McKerracher L, David S, Jackson DL, Kottis V, Dunn RJ, Braun PE (1994) Identification of myelin-associated glycoprotein as a major myelinderived inhibitor of neurite growth. Neuron 13:805-811.
49. Meyer RL, Miotke JA, Benowitz LI (1994) Injury induced expression of growth-associated protein-43 in adult mouse retinal ganglion cells in vitro. Neuroscience 63:591-602.
50. Milea D, Amati-Bonneau P, Reynier P, Bonneau D (2010) Genetically determined optic neuropathies. Curr Opin Neurol 23:24-28.
51. Misantone LJ, Gershenbaum M, Murray M (1984) Viability of retinal ganglion cells after optic nerve crush in adult rats. J Neurocytol 13:449-465.
52. Miyoshi K, Ohyagi Y, Sakae N, Motomura K, Ma L, Taniwaki T, Furuya H, Tabira T, Kira J (2009) Enhancement of activation of caspases by presenilin 1 gene mutations and its inhibition by secretase inhibitors. J Alzheimers Dis 16:551-564.
53. Monnier PP, Sierra A, Schwab JM, Henke-Fahle S, Mueller BK (2003) The Rho/ROCK pathway mediates neurite growth-inhibitory activity associated with the chondroitin sulfate proteoglycans of the CNS glial scar. Mol Cell Neurosci 22:319-330.
54. Muzio M, Stockwell BR, Stennicke HR, Salvesen GS, Dixit VM (1998) An induced proximity model for caspase-8 activation. J Biol Chem 273:2926-2930.
55. Nash M, Pribiag H, Fournier AE, Jacobson C (2009) Central nervous system regeneration inhibitors and their intracellular substrates. Mol Neurobiol 40:224-235.
56. Nikolaev A, McLaughlin T, O'Leary DD, Tessier-Lavigne M (2009) APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457:981-989.
57. Nishio T (2009) Axonal regeneration and neural network reconstruction in mammalian CNS. J Neurol 256 [Suppl 3]:306-309.
58. Park KJ, Grosso CA, Aubert I, Kaplan DR, Miller FD (2010) P75ntrdependent, myelin-mediated axonal degeneration regulates neural connectivity in the adult brain. Nat Neurosci 13:559-566.
59. Qu J, Wang D, Grosskreutz CL (2010) Mechanisms of retinal ganglion cell injury and defense in glaucoma. Exp Eye Res 91:48-53.
60. Quigley HA, Nickells RW, Kerrigan LA, Pease ME, Thibault DJ, Zack DJ (1995) Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Invest Ophthalmol Vis Sci 36:774-786.
61. Quinn CC, Wadsworth WG (2008) Axon guidance: asymmetric signaling orients polarized outgrowth. Trends Cell Biol 18:597-603.
62. Rohn TT, Head E, Nesse WH, Cotman CW, Cribbs DH (2001) Activation of caspase-8 in the Alzheimer's disease brain. Neurobiol Dis 8:1006-1016.
63. Sautter J, Sabel BA (1993) Recovery of brightness discrimination in adult rats despite progressive loss of retrogradely labelled retinal ganglion cells after controlled optic nerve crush. Eur J Neurosci 5:680-690.
64. Schwab ME (1990) Myelin-associated inhibitors of neurite growth and regeneration in the CNS. Trends Neurosci 13:452-456.
65. Shin EY, Shin KS, Lee CS, Woo KN, Quan SH, Soung NK, Kim YG, Cha CI, Kim SR, Park D, Bokoch GM, Kim EG (2002) Phosphorylation of p85 beta PIX, a Rac/Cdc42-specific guanine nucleotide exchange factor, via the Ras/ERK/PAK2 pathway is required for basic fibroblast growth factorinduced neurite outgrowth. J Biol Chem 277:44417-44430.
66. Shin EY, Woo KN, Lee CS, Koo SH, Kim YG, Kim WJ, Bae CD, Chang SI, Kim EG (2004) Basic fibroblast growth factor stimulates activation of Rac1 through a p85 betaPIX phosphorylation-dependent pathway. J Biol Chem 279:1994-2004.
67. Shin EY, Shim ES, Lee CS, Kim HK, Kim EG (2009) Phosphorylation of RhoGDI1 by p21-activated kinase 2 mediates basic fibroblast growth factor-stimulated neurite outgrowth in PC12 cells. Biochem Biophys Res Commun 379:384-389.
68. Stevenson JA (1987) Growth of retinal ganglion cell axons following optic nerve crush in adult hamsters. Exp Neurol 97:77-89.
69. Su HX, Cho EY (2003) Sprouting of axon-like processes from axotomized retinal ganglion cells induced by normal and preinjured intravitreal optic nerve grafts. Brain Res 991:150-162.
70. Su Y, Wang F, Zhao SG, Pan SH, Liu P, Teng Y, Cui H (2008) Axonal regeneration after optic nerve crush in Nogo-A/B/C knockout mice. Mol Vis 14:268-273.
71. Su Y, Wang F, Teng Y, Zhao SG, Cui H, Pan SH (2009) Axonal regeneration of optic nerve after crush in Nogo66 receptor knockout mice. Neurosci Lett 460:223-226.
72. Sun F, He Z (2010) Neuronal intrinsic barriers for axon regeneration in the adult CNS. Curr Opin Neurobiol 20:510-518.
73. Szczepanowska J (2009) Involvement of Rac/Cdc42/PAK pathway in cytoskeletal rearrangements. Acta Biochim Pol 56:225-234.
74. Tahirovic S, Hellal F, Neukirchen D, Hindges R, Garvalov BK, Flynn KC, Stradal TE, Chrostek-Grashoff A, Brakebusch C, Bradke F (2010) Rac1 regulates neuronal polarization through the WAVE complex. J Neurosci 30:6930-6943.
75. Thies E, Davenport RW (2003) Independent roles of Rho-GTPases in growth cone and axonal behavior. J Neurobiol 54:358-369.
76. Vaisid T, Barnoy S, Kosower NS (2009) Calpain activates caspase-8 in neuron-like differentiated PC12 cells via the amyloid-beta-peptide and CD95 pathways. Int J Biochem Cell Biol 41:2450-2458.
77. Villegas-Pérez MP, Vidal-Sanz M, Bray GM, Aguayo AJ (1988) Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. J Neurosci 8:265-280.
78. Viswanath V, Wu Y, Boonplueang R, Chen S, Stevenson FF, Yantiri F, Yang L, Beal MF, Andersen JK (2001) Caspase-9 activation results in downstream caspase-8 activation and bid cleavage in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced Parkinson's disease. J Neurosci 21:9519-9528.
79. Wang KC, Kim JA, Sivasankaran R, Segal R, He Z (2002) P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420:74-78.
80. Warner N, Eggenberger E (2010) Traumatic optic neuropathy: a review of the current literature. Curr Opin Ophthalmol 21:459-462.
81. Weishaupt JH, Diem R, Kermer P, Krajewski S, Reed JC, Bähr M (2003) Contribution of caspase-8 to apoptosis of axotomized rat retinal ganglion cells in vivo. Neurobiol Dis 13:124-135.
82. Wong EV, David S, Jacob MH, Jay DG (2003) Inactivation of myelinassociated glycoprotein enhances optic nerve regeneration. J Neurosci 23:3112-3117.
83. Yang C, Kaushal V, Haun RS, Seth R, Shah SV, Kaushal GP (2008) Transcriptional activation of caspase-6 and -7 genes by cisplatin-induced p53 and its functional significance in cisplatin nephrotoxicity. Cell Death Differ 15:530-544.
84. Yew DT, Ping Li W, Liu WK (2004) Fas and activated caspase 8 in normal, Alzheimer and multiple infarct brains. Neurosci Lett 367:113-117.
85. Yi CH, Yuan J (2009) The Jekyll and Hyde functions of caspases. Dev Cell 16:21-34.