Combined suppression of CASP2 and CASP6 protects retinal ganglion cells from apoptosis and promotes axon regeneration through CNTF-mediated JAK/STAT signalling

Brain

Volumn 137, Issue 6, 2014, Pages 1656-1675

  Vigneswara, Vasanthy ^a   Akpan, Nsikan ^b   Berry, Martin ^a   Logan, Ann ^a   Troy, Carol M ^b   Ahmed, Zubair ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b NewYork Presbyterian Hospital   (United States)

Author keywords

apoptosis; axon regeneration; CASP2; CASP6; optic nerve; retinal ganglion cells

Indexed keywords

CASPASE 2; CASPASE 6; CILIARY NEUROTROPHIC FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; JANUS KINASE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY MAB228; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; PENETRATIN; PENETRATIN 1; STAT PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; MUELLER CELL; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; OPTIC NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA CELL; RETINA GANGLION CELL; SIGNAL TRANSDUCTION;

APOPTOSIS; AXON REGENERATION; CASP2; CASP6; OPTIC NERVE; RETINAL GANGLION CELLS;

ANIMALS; APOPTOSIS; AXONS; CASPASE 2; CASPASE 6; CILIARY NEUROTROPHIC FACTOR; CYSTEINE ENDOPEPTIDASES; DISEASE MODELS, ANIMAL; FEMALE; NERVE REGENERATION; OPTIC NERVE; OPTIC NERVE INJURIES; RATS; RATS, SPRAGUE-DAWLEY; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84901452070     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awu037     Document Type: Article

References (86)

1. Agudo M, Perez-Marin MC, Lonngren U, Sobrado P, Conesa A, Canovas I, et al. Time course profiling of the retinal transcriptome after optic nerve transection and optic nerve crush. Mol Vis 2008; 14: 1050-63.
2. Ahmed Z, Dent RG, Leadbeater WE, Smith C, Berry M, Logan A. Matrix metalloproteases: degradation of the inhibitory environment of the transected optic nerve and the scar by regenerating axons. Mol Cell Neurosci 2005; 28: 64-78.
3. Ahmed Z, Suggate EL, Brown ER, Dent RG, Armstrong SJ, Barrett LB, et al. Schwann cell-derived factor-induced modulation of the NgR/p75NTR/EGFR axis disinhibits axon growth through CNS myelin in vivo and in vitro. Brain 2006; 129 (Pt 6): 1517-33.
4. Ahmed Z, Aslam M, Lorber B, Suggate EL, Berry M, Logan A. Optic nerve and vitreal inflammation are both RGC neuroprotective but only the latter is RGC axogenic. Neurobiol Dis 2010; 37: 441-54.
5. Ahmed Z, Kalinski H, Berry M, Almasieh M, Ashush H, Slager N, et al. Ocular neuroprotection by siRNA targeting caspase-2. Cell Death Dis 2011; 2: e173.
6. Akpan N, Serrano-Saiz E, Zacharia BE, Otten ML, Ducruet AF, Snipas SJ, et al. Intranasal delivery of caspase-9 inhibitor reduces caspase-6-dependent axon/neuron loss and improves neurological function after stroke. J Neurosci 2011; 31: 8894-904.
7. Anisman H. Cascading effects of stressors and inflammatory immune system activation: implications for major depressive disorder. J Psychiatry Neurosci 2009; 34: 4-20.
8. Berger AB, Sexton KB, Bogyo M. Commonly used caspase inhibitors designed based on substrate specificity profiles lack selectivity. Cell Res 2006; 16: 961-3.
9. Berkelaar M, Clarke DB, Wang YC, Bray GM, Aguayo AJ. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J Neurosci 1994; 14: 4368-74.
10. Berry M, Carlile J, Hunter A. 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 1996; 25: 147-70.
11. Berry M, Carlile J, Hunter A, Tsang W, Rosenstiel P, Sievers J. Optic nerve regeneration after intravitreal peripheral nerve implants: trajectories of axons regrowing through the optic chiasm into the optic tracts. J Neurocytol 1999; 28: 721-41.
12. Bokoch GM. Caspase-mediated activation of PAK2 during apoptosis: proteolytic kinase activation as a general mechanism of apoptotic signal transduction? Cell Death Differ 1998; 5: 637-45.
13. Casciola-Rosen LA, Miller DK, Anhalt GJ, Rosen A. Specific cleavage of the 70-kDa protein component of the U1 small nuclear ribonucleoprotein is a characteristic biochemical feature of apoptotic cell death. J Biol Chem 1994; 269: 30757-60.
14. Chaudhary P, Ahmed F, Quebada P, Sharma SC. Caspase inhibitors block the retinal ganglion cell death following optic nerve transection. Brain Res Mol Brain Res 1999; 67: 36-45.
15. Chauvier D, Ankri S, Charriaut-Marlangue C, Casimir R, Jacotot E. Broad-spectrum caspase inhibitors: from myth to reality? Cell Death Differ 2007; 14: 387-91.
16. Cheung ZH, Chan YM, Siu FK, Yip HK, Wu W, Leung MC, et al. Regulation of caspase activation in axotomized retinal ganglion cells. Mol Cell Neurosci 2004; 25: 383-93.
17. Davidson TJ, Harel S, Arboleda VA, Prunell GF, Shelanski ML, Greene LA, et al. Highly efficient small interfering RNA delivery to primary mammalian neurons induces MicroRNA-like effects before mRNA degradation. J Neurosci 2004; 24: 10040-6.
18. DeChiara TM, Vejsada R, Poueymirou WT, Acheson A, Suri C, Conover JC, et al. Mice lacking the CNTF receptor, unlike mice lacking CNTF, exhibit profound motor neuron deficits at birth. Cell 1995; 83: 313-22.
19. Denault JB, Salvesen GS. Expression, purification, and characterization of caspases. Curr Protoc Protein Sci 2003; Chapter 21: Unit 21 13.
20. Douglas MR, Morrison KC, Jacques SJ, Leadbeater WE, Gonzalez AM, Berry M, et al. Off-target effects of epidermal growth factor receptor antagonists mediate retinal ganglion cell disinhibited axon growth. Brain 2009; 132 (Pt 11): 3102-21.
21. Dyer MA, Cepko CL. Control of Muller glial cell proliferation and activation following retinal injury. Nat Neurosci 2000; 3: 873-80.
22. Edgington LE, van Raam BJ, Verdoes M, Wierschem C, Salvesen GS, Bogyo M. An optimized activity-based probe for the study of caspase-6 activation. Chem Biol 2012; 19: 340-52.
23. Escartin C, Brouillet E, Gubellini P, Trioulier Y, Jacquard C, Smadja C, et al. Ciliary neurotrophic factor activates astrocytes, redistributes their glutamate transporters GLAST and GLT-1 to raft microdomains, and improves glutamate handling in vivo. J Neurosci 2006; 26: 5978-89.
24. Escartin C, Pierre K, Colin A, Brouillet E, Delzescaux T, Guillermier M, et al. Activation of astrocytes by CNTF induces metabolic plasticity and increases resistance to metabolic insults. J Neurosci 2007; 27: 7094-104.
25. Garcia-Valenzuela E, Gorczyca W, Darzynkiewicz Z, Sharma SC. Apoptosis in adult retinal ganglion cells after axotomy. J Neurobiol 1994; 25: 431-8.
26. Ho LH, Read SH, Dorstyn L, Lambrusco L, Kumar S. Caspase-2 is required for cell death induced by cytoskeletal disruption. Oncogene 2008; 27: 3393-404.
27. Isenmann S, Wahl C, Krajewski S, Reed JC, Bahr M. Up-regulation of Bax protein in degenerating retinal ganglion cells precedes apoptotic cell death after optic nerve lesion in the rat. Eur J Neurosci 1997; 9: 1763-72.
28. Joos KM, Li C, Sappington RM. Morphometric changes in the rat optic nerve following short-term intermittent elevations in intraocular pressure. Invest Ophthalmol Vis Sci 2010; 51: 6431-40.
29. Kahn MA, Ellison JA, Speight GJ, de Vellis J. CNTF regulation of astrogliosis and the activation of microglia in the developing rat central nervous system. Brain Res 1995; 685: 55-67.
30. Kamiguchi H, Yoshida K, Sagoh M, Sasaki H, Inaba M, Wakamoto H, et al. Release of ciliary neurotrophic factor from cultured astrocytes and its modulation by cytokines. Neurochem Res 1995; 20: 1187-93.
31. 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: 4656-62.
32. Kermer P, Klocker N, Labes M, Thomsen S, Srinivasan A, Bahr M. Activation of caspase-3 in axotomized rat retinal ganglion cells in vivo. FEBS Lett 1999; 453: 361-4.
33. Kermer P, Ankerhold R, Klocker N, Krajewski S, Reed JC, Bahr M. Caspase-9: involvement in secondary death of axotomized rat retinal ganglion cells in vivo. Brain Res Mol Brain Res 2000; 85: 144-50.
34. Kirsch M, Trautmann N, Ernst M, Hofmann HD. Involvement of gp130-associated cytokine signaling in Muller cell activation following optic nerve lesion. Glia 2010; 58: 768-79.
35. Klocker N, Kermer P, Weishaupt JH, Labes M, Ankerhold R, Bahr M. Brain-derived neurotrophic factor-mediated neuroprotection of adult rat retinal ganglion cells in vivo does not exclusively depend on phosphatidyl-inositol-3'- kinase/protein kinase B signaling. J Neurosci 2000; 20: 6962-7.
36. Kurimoto T, Yin Y, Omura K, Gilbert HY, Kim D, Cen LP, et al. Longdistance axon regeneration in the mature optic nerve: contributions of oncomodulin, cAMP, and pten gene deletion. J Neurosci 2010; 30: 15654-63.
37. Kurokawa T, Katai N, Shibuki H, Kuroiwa S, Kurimoto Y, Nakayama C, et al. BDNF diminishes caspase-2 but not c-Jun immunoreactivity of neurons in retinal ganglion cell layer after transient ischemia. Invest Ophthalmol Vis Sci 1999; 40: 3006-11.
38. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 1994; 371: 346-7.
39. Leist M, Single B, Castoldi AF, Kuhnle S, Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 1997; 185: 1481-6.
40. Leon S, Yin Y, Nguyen J, Irwin N, Benowitz LI. Lens injury stimulates axon regeneration in the mature rat optic nerve. J Neurosci 2000; 20: 4615-26.
41. Logan A, Ahmed Z, Baird A, Gonzalez AM, Berry M. Neurotrophic factor synergy is required for neuronal survival and disinhibited axon regeneration after CNS injury. Brain 2006; 129 (Pt 2): 490-502.
42. Lorber B, Berry M, Logan A, Tonge D. Effect of lens lesion on neurite outgrowth of retinal ganglion cells in vitro. Mol Cell Neurosci 2002; 21: 301-11.
43. Lorber B, Berry M, Logan A. Lens injury stimulates adult mouse retinal ganglion cell axon regeneration via both macrophage-and lensderived factors. Eur J Neurosci 2005; 21: 2029-34.
44. Lorber B, Berry M, Logan A. Different factors promote axonal regeneration of adult rat retinal ganglion cells after lens injury and intravitreal peripheral nerve grafting. J Neurosci Res 2008; 86: 894-903.
45. Lorber B, Berry M, Douglas MR, Nakazawa T, Logan A. Activated retinal glia promote neurite outgrowth of retinal ganglion cells via apolipoprotein E. J Neurosci Res 2009; 87: 2645-52.
46. Lorber B, Guidi A, Fawcett JW, Martin KR. Activated retinal glia mediated axon regeneration in experimental glaucoma. Neurobiol Dis 2012; 45: 243-52.
47. MacLaren RE. Development and role of retinal glia in regeneration of ganglion cells following retinal injury. Br J Ophthalmol 1996; 80: 458-64.
48. Mansour-Robaey S, Clarke DB, Wang YC, Bray GM, Aguayo AJ. Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomized retinal ganglion cells. Proc Natl Acad Sci USA 1994; 91: 1632-6.
49. McStay GP, Salvesen GS, Green DR. Overlapping cleavage motif selectivity of caspases: implications for analysis of apoptotic pathways. Cell Death Differ 2008; 15: 322-31.
50. Mey J, Thanos S. Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo. Brain Res 1993; 602: 304-17.
51. Mintzer R, Ramaswamy S, Shah K, Hannoush RN, Pozniak CD, Cohen F, et al. A whole cell assay to measure caspase-6 activity by detecting cleavage of lamin A/C. PLoS One 2012; 7: e30376.
52. Monnier PP, D'Onofrio PM, Magharious M, Hollander AC, Tassew N, Szydlowska K, et al. Involvement of caspase-6 and caspase-8 in neuronal apoptosis and the regenerative failure of injured retinal ganglion cells. J Neurosci 2011; 31: 10494-505.
53. Mouser PE, Head E, Ho Ha K, Rohn TT. Caspase-mediated cleavage of glial fibrillary acidic protein within degenerating astrocytes of the Alzheimer's disease brain. Am J Pathol 2006; 168: 936-46.
54. Muller A, Hauk TG, Fischer D. Astrocyte-derived CNTF switches mature RGCs to a regenerative state following inflammatory stimulation. Brain 2007; 130 (Pt 12): 3308-20.
55. Muller A, Hauk TG, Leibinger M, Marienfeld R, Fischer D. Exogenous CNTF stimulates axon regeneration of retinal ganglion cells partially via endogenous CNTF. Mol Cell Neurosci 2009; 41: 233-46.
56. Niizuma K, Endo H, Nito C, Myer DJ, Kim GS, Chan PH. The PIDDosome mediates delayed death of hippocampal CA1 neurons after transient global cerebral ischemia in rats. Proc Natl Acad Sci USA 2008; 105: 16368-73.
57. Nikolaev A, McLaughlin T, O'Leary DD, Tessier-Lavigne M. APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 2009; 457: 981-9.
58. Orth K, Chinnaiyan AM, Garg M, Froelich CJ, Dixit VM. The CED-3/ICElike protease Mch2 is activated during apoptosis and cleaves the death substrate lamin A. J Biol Chem 1996; 271: 16443-6.
59. Park KK, Liu K, Hu Y, Smith PD, Wang C, Cai B, et al. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008; 322: 963-6.
60. Peinado-Ramon P, Salvador M, Villegas-Perez MP, Vidal-Sanz M. Effects of axotomy and intraocular administration of NT-4, NT-3, and brainderived neurotrophic factor on the survival of adult rat retinal ganglion cells. A quantitative in vivo study. Invest Ophthalmol Vis Sci 1996; 37: 489-500.
61. Pernet V, Di Polo A. Synergistic action of brain-derived neurotrophic factor and lens injury promotes retinal ganglion cell survival, but leads to optic nerve dystrophy in vivo. Brain 2006; 129 (Pt 4): 1014-26.
62. Pernet V, Joly S, Dalkara D, Jordi N, Schwarz O, Christ F, et al. Longdistance axonal regeneration induced by CNTF gene transfer is impaired by axonal misguidance in the injured adult optic nerve. Neurobiol Dis 2013; 51: 202-13.
63. Pop C, Salvesen GS. Human caspases: activation, specificity, and regulation. J Biol Chem 2009; 284: 21777-81.
64. Porter AG, Ng P, Janicke RU. Death substrates come alive. Bioessays 1997; 19: 501-7.
65. Rabacchi SA, Bonfanti L, Liu XH, Maffei L. Apoptotic cell death induced by optic nerve lesion in the neonatal rat. J Neurosci 1994; 14: 5292-301.
66. Ruchaud S, Korfali N, Villa P, Kottke TJ, Dingwall C, Kaufmann SH, et al. Caspase-6 gene disruption reveals a requirement for lamin A cleavage in apoptotic chromatin condensation. EMBO J 2002; 21: 1967-77.
67. Simon DJ, Weimer RM, McLaughlin T, Kallop D, Stanger K, Yang J, et al. A caspase cascade regulating developmental axon degeneration. J Neurosci 2012; 32: 17540-53.
68. Singh M, Savitz SI, Hoque R, Gupta G, Roth S, Rosenbaum PS, et al. Cell-specific caspase expression by different neuronal phenotypes in transient retinal ischemia. J Neurochem 2001; 77: 466-75.
69. Song Q, Lees-Miller SP, Kumar S, Zhang Z, Chan DW, Smith GC, et al. DNA-dependent protein kinase catalytic subunit: a target for an ICElike protease in apoptosis. EMBO J 1996; 15: 3238-46.
70. Sun F, Park KK, Belin S, Wang D, Lu T, Chen G, et al. Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature 2011; 480: 372-5.
71. Takahashi A, Alnemri ES, Lazebnik YA, Fernandes-Alnemri T, Litwack G, Moir RD, et al. Cleavage of lamin A by Mch2 alpha but not CPP32: multiple interleukin 1 beta-converting enzyme-related proteases with distinct substrate recognition properties are active in apoptosis. Proc Natl Acad Sci USA 1996; 93: 8395-400.
72. Tang G, Xu Z, Goldman JE. Synergistic effects of the SAPK/JNK and the proteasome pathway on glial fibrillary acidic protein (GFAP) accumulation in Alexander disease. J Biol Chem 2006; 281: 38634-43.
73. Thanos S, Vidal-Sanz M, Aguayo AJ. The use of rhodamine-B-isothiocyanate (RITC) as an anterograde and retrograde tracer in the adult rat visual system. Brain Res 1987; 406: 317-21.
74. Timmer JC, Salvesen GS. Caspase substrates. Cell Death Differ 2007; 14: 66-72.
75. Troy CM, Stefanis L, Greene LA, Shelanski ML. Nedd2 is required for apoptosis after trophic factor withdrawal, but not superoxide dismutase (SOD1) downregulation, in sympathetic neurons and PC12 cells. J Neurosci 1997; 17: 1911-8.
76. Troy CM, Rabacchi SA, Friedman WJ, Frappier TF, Brown K, Shelanski ML. Caspase-2 mediates neuronal cell death induced by beta-amyloid. J Neurosci 2000; 20: 1386-92.
77. Troy CM, Rabacchi SA, Hohl JB, Angelastro JM, Greene LA, Shelanski ML. Death in the balance: alternative participation of the caspase-2 and-9 pathways in neuronal death induced by nerve growth factor deprivation. J Neurosci 2001; 21: 5007-16.
78. Troy CM, Ribe EM. Caspase-2: vestigial remnant or master regulator? Sci Signal 2008; 1: pe42.
79. Van Eldik LJ, Thompson WL, Ralay Ranaivo H, Behanna HA, Martin Watterson D. Glia proinflammatory cytokine upregulation as a therapeutic target for neurodegenerative diseases: function-based and target-based discovery approaches. Int Rev Neurobiol 2007; 82: 277-96.
80. Vigneswara V, Berry M, Logan A, Ahmed Z. Pharmacological inhibition of caspase-2 protects axotomised retinal ganglion cells from apoptosis in adult rats. PLoS One 2012; 7: e53473.
81. Vigneswara V, Berry M, Logan A, Ahmed Z. Pigment epithelium-derived factor is retinal ganglion cell neuroprotective and axogenic after optic nerve crush injury. Invest Ophthalmol Vis Sci 2013; 54: 2624-33.
82. Villegas-Perez MP, Vidal-Sanz M, Rasminsky M, Bray GM, Aguayo AJ. Rapid and protracted phases of retinal ganglion cell loss follow axotomy in the optic nerve of adult rats. J Neurobiol 1993; 24: 23-36.
83. Vohra BP, Sasaki Y, Miller BR, Chang J, DiAntonio A, Milbrandt J. Amyloid precursor protein cleavage-dependent and-independent axonal degeneration programs share a common nicotinamide mononucleotide adenylyltransferase 1-sensitive pathway. J Neurosci 2010; 30: 13729-38.
84. Weishaupt JH, Diem R, Kermer P, Krajewski S, Reed JC, Bahr M. Contribution of caspase-8 to apoptosis of axotomized rat retinal ganglion cells in vivo. Neurobiol Dis 2003; 13: 124-35.
85. Winter CG, Saotome Y, Levison SW, Hirsh D. A role for ciliary neurotrophic factor as an inducer of reactive gliosis, the glial response to central nervous system injury. Proc Natl Acad Sci USA 1995; 92: 5865-9.
86. Yin Y, Cui Q, Li Y, Irwin N, Fischer D, Harvey AR, et al. Macrophagederived factors stimulate optic nerve regeneration. J Neurosci 2003; 23: 2284-93.