Quantitative retinal protein analysis after optic nerve transection reveals a neuroprotective role for hepatoma- derived growth factor on injured retinal ganglion cells

Investigative Ophthalmology and Visual Science

Volumn 53, Issue 7, 2012, Pages 3973-3989

  Hollander, Adam ^a   D'Onofrio, Philippe M ^a   Magharious, Mark M ^a   Lysko, Meghan D ^a   Koeberle, Paulo D ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALNEXIN; COFILIN 1; COLLAPSIN RESPONSE MEDIATOR PROTEIN; G PROTEIN COUPLED RECEPTOR; HEAT SHOCK PROTEIN; HEPATOMA DERIVED GROWTH FACTOR; HISTONE H2A; INITIATION FACTOR 5A; MITOGEN ACTIVATED PROTEIN KINASE; PEROXIREDOXIN 2; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEOME; RETINA S ANTIGEN; THIOREDOXIN; TRANSALDOLASE; TRANSCRIPTION FACTOR; TRANSKETOLASE; VIMENTIN; EYE PROTEIN; HEPATOMA-DERIVED GROWTH FACTOR; NEUROPROTECTIVE AGENT; SIGNAL PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; FRACTIONATION; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; NERVE CELL DEGENERATION; NERVE CELL LESION; NERVE FIBER TRANSECTION; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTIC NERVE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEOMICS; RAT; RETINA GANGLION CELL; UPREGULATION; WESTERN BLOTTING; ANIMAL; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECT; FEMALE; METABOLISM; OPTIC NERVE INJURY; PATHOLOGY; RETINA DEGENERATION; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; BLOTTING, WESTERN; CELL SURVIVAL; DISEASE MODELS, ANIMAL; EYE PROTEINS; FEMALE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; NEUROPROTECTIVE AGENTS; OPTIC NERVE; OPTIC NERVE INJURIES; RATS; RATS, SPRAGUE-DAWLEY; RETINAL DEGENERATION; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION;

EID: 84868333686     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.11-8350     Document Type: Article

References (83)

1. Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet. 2010;376:124-136.
2. Milea D, Amati-Bonneau P, Reynier P, Bonneau D. Genetically determined optic neuropathies. Curr Opin Neurol. 2010;23: 24-28.
3. Qu J, Wang D, Grosskreutz CL. Mechanisms of retinal ganglion cell injury and defense in glaucoma. Exp Eye Res. 2010;91:48-53.
4. Warner N, Eggenberger E. Traumatic optic neuropathy: a review of the current literature. Curr Opin Ophthalmol. 2010; 21:459-462.
5. 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;14:4368-4374.
6. Quigley HA, Nickells RW, Kerrigan LA, Pease ME, Thibault DJ, Zack DJ. Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Invest Ophthalmol Vis Sci. 1995;36:774-786.
7. Koeberle PD, Ball AK. Effects of GDNF on retinal ganglion cell survival following axotomy. Vision Res. 1998;38:1505-1515.
8. Kermer P, Klocker N, Bahr M. Neuronal death after brain injury. Models, mechanisms, and therapeutic strategies in vivo. Cell Tissue Res. 1999;298:383-395.
9. Bahr M. Live or let die-retinal ganglion cell death and survival during development and in the lesioned adult CNS. Trends Neurosci. 2000;23:483-490.
10. Koeberle PD, Bahr M. Growth and guidance cues for regenerating axons: where have they gone? J Neurobiol. 2004;59:162-180.
11. Villegas-Perez MP, Vidal-Sanz M, Bray GM, Aguayo AJ. Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. J Neurosci. 1988;8:265-280.
12. 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.
13. Peinado-Ramon P, Salvador M, Villegas-Perez MP, Vidal-Sanz M. Effects of axotomy and intraocular administration of NT-4, NT- 3, and brain-derived neurotrophic factor on the survival of adult rat retinal ganglion cells. A quantitative in vivo study. Invest Ophthalmol Vis Sci. 1996;37:489-500.
14. Isenmann S, Wahl C, Krajewski S, Reed JC, B̈ahr M. Upregulation of Bax protein in degenerating retinal ganglion cells precedes apoptotic cell death after optic nerve lesion in the rat. Eur J Neurosci. 1997;9:1763-1772.
15. Kermer P, Ankerhold R, Kl̈ocker N, Krajewski S, Reed JC, B̈ahr M. Caspase-9: involvement in secondary death of axotomized rat retinal ganglion cells in vivo. Brain Res Mol Brain Res. 2000;85:144-150.
16. Kermer P, Kl̈ocker N, Labes M, B̈ahr M. Inhibition of CPP32- like proteases rescues axotomized retinal ganglion cells from secondary cell death in vivo. J Neurosci. 1998;18:4656-4662.
17. Kikuchi M, Tenneti L, Lipton SA. Role of p38 mitogen-activated protein kinase in axotomy-induced apoptosis of rat retinal ganglion cells. J Neurosci. 2000;20:5037-5044.
18. Kuehn MH, Fingert JH, Kwon YH. Retinal ganglion cell death in glaucoma: mechanisms and neuroprotective strategies. Ophthalmol Clin North Am. 2005;18:383-395, vi.
19. Seki M, Lipton SA. Targeting excitotoxic/free radical signaling pathways for therapeutic intervention in glaucoma. Prog Brain Res. 2008;173:495-510.
20. 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.
21. Koeberle PD, Gauldie J, Ball AK. Effects of adenoviral-mediated gene transfer of interleukin-10, interleukin-4, and transforming growth factor-beta on the survival of axotomized retinal ganglion cells. Neuroscience. 2004;125:903-920.
22. Koeberle PD, Wang Y, Schlichter LC. Kv1.1 and Kv1.3 channels contribute to the degeneration of retinal ganglion cells after optic nerve transection in vivo. Cell Death Differ. 2010;17:134-144.
23. Kipnis J, Yoles E, Schori H, Hauben E, Shaked I, Schwartz M. Neuronal survival after CNS insult is determined by a genetically encoded autoimmune response. J Neurosci. 2001;21:4564-4571.
24. Schori H, Yoles E, Schwartz M. T-cell-based immunity counteracts the potential toxicity of glutamate in the central nervous system. J Neuroimmunol. 2001;119:199-204.
25. Schori H, Yoles E, Wheeler LA, Raveh T, Kimchi A, Schwartz M. Immune-related mechanisms participating in resistance and susceptibility to glutamate toxicity. Eur J Neurosci. 2002;16: 557-564.
26. Koeberle PD, Schlichter LC. Targeting K(V) channels rescues retinal ganglion cells in vivo directly and by reducing inflammation. Channels (Austin). 2010;4:337-346.
27. Koeberle PD, Tura A, Tassew NG, Schlichter LC, Monnier PP. The repulsive guidance molecule, RGMa, promotes retinal ganglion cell survival in vitro and in vivo. Neuroscience. 2010; 169:495-504.
28. Tsang TY, Tang WY, Tsang WP, Co NN, Kong SK, Kwok TT. Mechanistic study on growth suppression and apoptosis induction by targeting hepatoma-derived growth factor in human hepatocellular carcinoma HepG2 cells. Cell Physiol Biochem. 2009;24:253-262.
29. Magharious MM, D'Onofrio PM, Koeberle PD. Methods for experimental manipulations after optic nerve transection in the mammalian CNS. J Vis Exp. 2011;(51):2261.
30. Magharious MM, D'Onofrio PM, Koeberle PD. Optic nerve transection: a model of adult neuron apoptosis in the central nervous system. J Vis Exp. 2011;(51):22-41.
31. Arcaro A, Wymann MP. Wortmannin is a potent phosphatidylinositol 3-kinase inhibitor: the role of phosphatidylinositol 3,4,5-trisphosphate in neutrophil responses. Biochem J. 1993; 296:297-301.
32. Powis G, Bonjouklian R, Berggren MM, et al. Wortmannin, a potent and selective inhibitor of phosphatidylinositol-3-kinase. Cancer Res. 1994;54:2419-2423.
33. Alessi DR, Cuenda A, Cohen P, Dudley DT, Saltiel AR. PD 098059 is a specific inhibitor of the activation of mitogenactivated protein kinase kinase in vitro and in vivo. J Biol Chem. 1995;270:27489-27494.
34. Koeberle PD, Bahr M. The upregulation of GLAST-1 is an indirect antiapoptotic mechanism of GDNF and neurturin in the adult CNS. Cell Death Differ. 2008;15:471-483.
35. Magharious M, D'Onofrio PM, Hollander A, Zhu P, Chen J, Koeberle PD. Quantitative iTRAQ analysis of retinal ganglion cell degeneration after optic nerve crush. J Proteome Res. 2011;10:3344-3362.
36. Tang WH, Shilov IV, Seymour SL. Nonlinear fitting method for determining local false discovery rates from decoy database searches. J Proteome Res. 2008;7:3661-3667.
37. Norris EH, Giasson BI, Lee VM. Alpha-synuclein: normal function and role in neurodegenerative diseases. Curr Top Dev Biol. 2004;60:17-54.
38. Keppler D, Sordat B, Sierra F. T-kininogen present in the liver of old rats is biologically active and readily forms complexes with endogenous cysteine proteinases. Mech Ageing Dev. 1997;98:151-165.
39. Harashima S, Wang Y, Horiuchi T, Seino Y, Inagaki N. Purkinje cell protein 4 positively regulates neurite outgrowth and neurotransmitter release. J Neurosci Res. 2011;89:1519-1530.
40. Liedtke T, Schwamborn JC, Schr̈oer U, Thanos S. Elongation of axons during regeneration involves retinal crystallin beta b2 (crybb2). Mol Cell Proteomics. 2007;6:895-907.
41. Shin OH, Xu J, Rizo J, S̈udhof TC. Differential but convergent functions of Ca2+binding to synaptotagmin-1 C2 domains mediate neurotransmitter release. Proc Natl Acad Sci U S A. 2009;106:16469-16474.
42. Ishizaki H, Miyoshi J, Kamiya H, et al. Role of rab GDP dissociation inhibitor alpha in regulating plasticity of hippocampal neurotransmission. Proc Natl Acad Sci U S A. 2000;97: 11587-11592.
43. D'Adamo P, Menegon A, Lo Nigro C, et al. Mutations in GDI1 are responsible for X-linked non-specific mental retardation. Nat Genet. 1998;19:134-139.
44. Hirsch S, Labes M, Bahr M. Changes in BDNF and neurotrophin receptor expression in degenerating and regenerating rat retinal ganglion cells. Restor Neurol Neurosci. 2000;17:125-134.
45. Lindqvist N, Peinado-Ramónn P, Vidal-Sanz M, Hallb̈öok F. GDNF, R et, GFRalpha1 and 2 in the adult rat retino-tectal system after optic nerve transection. Exp Neurol. 2004;187: 487-499.
46. Klocker N, Cellerino A, Bahr M. Free radical scavenging and inhibition of nitric oxide synthase potentiates the neurotrophic effects of brain-derived neurotrophic factor on axotomized retinal ganglion cells in vivo. J Neurosci. 1998;18:1038-1046.
47. Koeberle PD, Ball AK. Neurturin enhances the survival of axotomized retinal ganglion cells in vivo: combined effects with glial cell line-derived neurotrophic factor and brainderived neurotrophic factor. Neuroscience. 2002;110:555-567.
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 U S A. 1994;91:1632-1636.
49. 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;602:304-317.
50. Nakazawa T, Tamai M, Mori N. Brain-derived neurotrophic factor prevents axotomized retinal ganglion cell death through MAPK and PI3K signaling pathways. Invest Ophthalmol Vis Sci. 2002;43:3319-3326.
51. Park K, Luo JM, Hisheh S, Harvey AR, Cui Q. Cellular mechanisms associated with spontaneous and ciliary neurotrophic factor-cAMP-induced survival and axonal regeneration of adult retinal ganglion cells. J Neurosci. 2004;24:10806-10815.
52. Pernet V, Hauswirth WW, Di Polo A. Extracellular signalregulated kinase 1/2 mediates survival, but not axon regeneration, of adult injured central nervous system neurons in vivo. J Neurochem. 2005;93:72-83.
53. Sapieha PS, Hauswirth WW, Di Polo A. Extracellular signalregulated kinases 1/2 are required for adult retinal ganglion cell axon regeneration induced by fibroblast growth factor-2. J Neurosci Res. 2006;83:985-995.
54. Zhou Y, Pernet V, Hauswirth WW, et al. Activation of the extracellular signal-regulated kinase 1/2 pathway by AAV gene transfer protects retinal ganglion cells in glaucoma. Mol Ther. 2005;12:402-412.
55. Fitzgerald M, Bartlett CA, Harvey AR, Dunlop SA. Early events of secondary degeneration after partial optic nerve transection: an immunohistochemical study. J Neurotrauma. 2010; 27:439-452.
56. Garcia-Valenzuela E, Sharma SC, Pina AL. Multilayered retinal microglial response to optic nerve transection in rats. Mol Vis. 2005;11:225-231.
57. Gafken PR, Lampe PD. Methodologies for characterizing phosphoproteins by mass spectrometry. Cell Commun Adhes. 2006;13:249-262.
58. Tannu NS, Hemby SE. Methods for proteomics in neuroscience. Prog Brain Res. 2006;158:41-82.
59. Agudo M, P érez-Mar ín MC, L̈onngren U, et al. Time course profiling of the retinal transcriptome after optic nerve transection and optic nerve crush. Mol Vis. 2008;14:1050-1063.
60. Selles-Navarro I, Ellezam B, Fajardo R, Latour M, McKerracher L. Retinal ganglion cell and nonneuronal cell responses to a microcrush lesion of adult rat optic nerve. Exp Neurol. 2001; 167:282-289.
61. Schwartz M. Optic nerve crush: protection and regeneration. Brain Res Bull. 2004;62:467-471.
62. Guo Y, Cepurna WO, Dyck JA, Doser TA, Johnson EC, Morrison JC. Retinal cell responses to elevated intraocular pressure: a gene array comparison between the whole retina and retinal ganglion cell layer. Invest Ophthalmol Vis Sci. 2010;51:3003-3018.
63. Stowell C, Arbogast B, Cioffi G, Burgoyne C, Zhou A. Retinal proteomic changes following unilateral optic nerve transection and early experimental glaucoma in non-human primate eyes. Exp Eye Res. 2011;93:13-28.
64. Quigley HA, Davis EB, Anderson DR. Descending optic nerve degeneration in primates. Invest Ophthalmol Vis Sci. 1977;16: 841-849.
65. Quigley HA, Nickells RW, Kerrigan LA, Pease ME, Thibault DJ, Zack DJ. Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Invest Ophthalmol Vis Sci. 1995;36:774-786.
66. Morrison JC. Elevated intraocular pressure and optic nerve injury models in the rat. J Glaucoma. 2005;14:315-317.
67. Nakamura H, Izumoto Y, Kambe H, et al. Molecular cloning of complementary DNA for a novel human hepatoma-derived growth factor. Its homology with high mobility group-1 protein. J Biol Chem. 1994;269:25143-25149.
68. Izumoto Y, Kuroda T, Harada H, Kishimoto T, Nakamura H. Hepatoma-derived growth factor belongs to a gene family in mice showing significant homology in the amino terminus. Biochem Biophys Res Commun. 1997;238:26-32.
69. El-Tahir HM, Dietz F, Dringen R, et al. Expression of hepatomaderived growth factor family members in the adult central nervous system. BMC Neurosci. 2006;7:6.
70. Zhou Z, Yamamoto Y, Sugai F, et al. Hepatoma-derived growth factor is a neurotrophic factor harbored in the nucleus. J Biol Chem. 2004;279:27320-27326.
71. Nakamura H, Kambe H, Egawa T, et al. Partial purification and characterization of human hepatoma-derived growth factor. Clin Chim Acta. 1989;183:273-284.
72. Oliver JA, Al-Awqati Q. An endothelial growth factor involved in rat renal development. J Clin Invest. 1998;102:1208-1219.
73. Everett AD, Lobe DR, Matsumura ME, Nakamura H, McNamara CA. Hepatoma-derived growth factor stimulates smooth muscle cell growth and is expressed in vascular development. J Clin Invest. 2000;105:567-575.
74. Everett AD, Stoops T, McNamara CA. Nuclear targeting is required for hepatoma-derived growth factor-stimulated mitogenesis in vascular smooth muscle cells. J Biol Chem. 2001; 276:37564-37568.
75. Kishima Y, Yamamoto H, Izumoto Y, et al. Hepatoma-derived growth factor stimulates cell growth after translocation to the nucleus by nuclear localization signals. J Biol Chem. 2002;277: 10315-10322.
76. Matsuyama A, Inoue H, Shibuta K, et al. Hepatoma-derived growth factor is associated with reduced sensitivity to irradiation in esophageal cancer. Cancer Res. 2001;61:5714-5717.
77. Abouzied MM, El-Tahir HM, Prenner L, Ḧaberlein H, Gieselmann V, Franken S. Hepatoma-derived growth factor. Significance of amino acid residues 81-100 in cell surface interaction and proliferative activity. J Biol Chem. 2005;280:10945-10954.
78. Wang CH, Davamani F, Sue SC, et al. Cell surface heparan sulfates mediate internalization of the PWWP/HATH domain of HDGF via macropinocytosis to fine-tune cell signalling processes involved in fibroblast cell migration. Biochem J. 2011;433:127-138.
79. Kolomeyer AM, Sugino IK, Zarbin MA. Characterization of conditioned media collected from cultured adult versus fetal retinal pigment epithelial cells. Invest Ophthalmol Vis Sci. 2011;52:5973-5986.
80. Everett AD, Narron JV, Stoops T, Nakamura H, Tucker A. Hepatoma-derived growth factor is a pulmonary endothelial cell-expressed angiogenic factor. Am J Physiol Lung Cell Mol Physiol. 2004;286:L1194-1201.
81. Mao J, Xu Z, Fang Y, et al. Hepatoma-derived growth factor involved in the carcinogenesis of gastric epithelial cells through promotion of cell proliferation by Erk1/2 activation. Cancer Sci. 2008;99:2120-2127.
82. Eun SY, Woo IS, Jang HS. Identification of cytochrome c oxidase subunit 6A1 as a suppressor of Bax-induced cell death by yeast-based functional screening. Biochem Biophys Res Commun. 2008;373:58-63.
83. Nickells RW, Semaan SJ, Schlamp CL. Involvement of the Bcl2 gene family in the signaling and control of retinal ganglion cell death. Prog Brain Res. 2008;173:423-435.