In glaucoma the upregulated truncated TrkC.T1 receptor isoform in glia causes increased TNF-α production, leading to retinal ganglion cell death

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 12, 2010, Pages 6639-6651

  Bai, Yujing ^a,b   Shi, Zhihua ^b   Zhuo, Yehong ^a   Liu, Jing ^c   Malakhov, Andrey ^c   Ko, Eunhwa ^c   Burgess, Kevin ^c   Schaefer, Henry ^d   Esteban, Pedro F ^d   Tessarollo, Lino ^d   Uri Saragovi, H ^b,e  

^a SUN YAT SEN UNIVERSITY   (China)

^b MCGILL UNIVERSITY   (Canada)

^c TEXAS A AND M UNIVERSITY   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2 MACROGLOBULIN; NEUROTROPHIN RECEPTOR; PROTEIN TYROSINE KINASE INHIBITOR; PROTEIN TYROSINE KINASE RECEPTOR C T1; TUMOR NECROSIS FACTOR ALPHA; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG TARGETING; FEMALE; GLAUCOMA; IMMUNOFLUORESCENCE TEST; INTRAOCULAR HYPERTENSION; MALE; MOUSE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; QUANTITATIVE STUDY; RAT; RETINA GANGLION CELL; TRANSGENIC MOUSE; UPREGULATION; WESTERN BLOTTING; WILD TYPE;

ALPHA-MACROGLOBULINS; ANIMALS; BLOTTING, WESTERN; CELL DEATH; DISEASE MODELS, ANIMAL; ELECTROPORATION; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENETIC VECTORS; GLAUCOMA; IN SITU HYBRIDIZATION; INTRAOCULAR PRESSURE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROGLIA; PROTEIN ISOFORMS; RATS; RATS, WISTAR; RECEPTOR, TRKC; RETINAL GANGLION CELLS; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 79956021337     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-5431     Document Type: Article

References (50)

1. Patapoutian A, Reichardt LF. Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol. 2001;11:272-280.
2. Palko ME, Coppola V, Tessarollo L. Evidence for a role of truncated trkC receptor isoforms in mouse development. J Neurosci. 1999; 19:775-782.
3. Valenzuela DM, Maisonpierre PC, Glass DJ, et al. Alternative forms of rat TrkC with different functional capabilities. Neuron. 1993; 10:963-974.
4. Das I, Sparrow JR, Lin MI, Shih E, Mikawa T, Hempstead BL. Trk C signaling is required for retinal progenitor cell proliferation [published erratum appears in J Neurosci. 2000;20:5574]. J Neurosci. 2000;20:2887-2895.
5. Baxter GT, Radeke MJ, Kuo RC, et al. Signal transduction mediated by the truncated trkB receptor isoforms, trkB.T1 and trkB.T2. J Neurosci. 1997;17:2683-2690.
6. Dorsey SG, Renn CL, Carim-Todd L, et al. In vivo restoration of physiological levels of truncated TrkB.T1 receptor rescues neuronal cell death in a trisomic mouse model. Neuron. 2006;51: 21-28.
7. Esteban PF, Yoon HY, Becker J, et al. A kinase-deficient TrkC receptor isoform activates Arf6-Rac1 signaling through the scaffold protein tamalin. J Cell Biol. 2006;173:291-299.
8. Rudzinski M, Wong TP, Saragovi HU. Changes in retinal expression of neurotrophins and neurotrophin receptors induced by ocular hypertension. J Neurobiol. 2004;58:341-354.
9. Quigley HA. New paradigms in the mechanisms and management of glaucoma. Eye. 2005;19:1241-1248.
10. Tezel G, Wax MB. Increased production of tumor necrosis factoralpha by glial cells exposed to simulated ischemia or elevated hydrostatic pressure induces apoptosis in cocultured retinal ganglion cells. J Neurosci. 2000;20:8693-8700.
11. Tezel G, Li LY, Patil RV, Wax MB. TNF-alpha and TNF-alpha receptor-1 in the retina of normal and glaucomatous eyes. Invest Ophthalmol Vis Sci. 2001;42:1787-1794.
12. Tezel G, Wax MB. The immune system and glaucoma. Curr Opin Ophthalmol. 2004;15:80-84.
13. Nakazawa T, Nakazawa C, Matsubara A, et al. 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.
14. Shi Z, Rudzinski M, Meerovitch K, et al. α2-Macroglobulin is a mediator of retinal ganglion cell death in glaucoma. J Biol Chem. 2008;283:29156-29165.
15. Wax MB, Tezel G. Neurobiology of glaucomatous optic neuropathy: diverse cellular events in neurodegeneration and neuroprotection. Mol Neurobiol. 2002;26:45-55.
16. Storck T, Kruth U, Kolhekar R, Sprengel R, Seeburg PH. Rapid construction in yeast of complex targeting vectors for gene manipulation in the mouse. Nucleic Acids Res. 1996;24:4594-4596.
17. Khrebtukova I, Michaud EJ, Foster CM, Stark KL, Garfinkel DJ, Woychik RP. Utilization of microhomologous recombination in yeast to generate targeting constructs for mammalian genes. Mutat Res. 1998;401:11-25.
18. Southon E, Tessarollo L. Manipulating mouse embryonic stem cells. Methods Mol Biol. 2009;530:165-185.
19. Reid SW, Tessarollo L. Isolation, microinjection and transfer of mouse blastocysts. Methods Mol Biol. 2009;530:269-285.
20. Garcia-Valenzuela E, Shareef S, Walsh J, Sharma S. Programmed cell death of retinal ganglion cells during experimental glaucoma. Exp Eye Res. 1995;61:33-44.
21. Laquis S, Chaudhary P, Sharma S. The patterns of retinal ganglion cell death in hypertensive eyes. Brain Res. 1998;784:100-104.
22. Naskar R, Wissing M, Thanos S. Detection of early neuron degeneration and accompanying microglial responses in the retina of a rat model of glaucoma. Invest Ophthalmol Vis Sci. 2002;43:2962-2968.
23. Urcola JH, Hernandez M, Vecino E. Three experimental glaucoma models in rats: comparison of the effects of intraocular pressure elevation on retinal ganglion cell size and death. Exp Eye Res. 2006;83:429-437.
24. Shi Z, Birman E, Saragovi HU. Neurotrophic rationale in glaucoma: a TrkA agonist, but not NGF or a p75 antagonist, protects retinal ganglion cells in vivo. Dev Neurobiol. 2007;67:884-894.
25. Danias J, Kontiola AI, Filippopoulos T, Mittag T. Method for the noninvasive measurement of intraocular pressure in mice. Invest Ophthalmol Vis Sci. 2003;44:1138-1141.
26. Buckingham BP, Inman DM, Lambert W, et al. Progressive ganglion cell degeneration precedes neuronal loss in a mouse model of glaucoma. J Neurosci. 2008;28:2735-2744.
27. Guillemard V, Ivanisevic L, Garcia AG, et al. An agonistic mAb directed to the TrkC receptor juxtamembrane region defines a trophic hot spot, and interactions with p75 co-receptors. Dev Neurobiol. 2009;70:150-164.
28. Brahimi F, Malakhov A, Lee HB, et al. A peptidomimetic of NT-3 acts as a TrkC antagonist. Peptides. 2009;30:1833-1839.
29. Chen D, Brahimi F, Angell Y, et al. Bivalent peptidomimetic ligands of TrkC are biased agonists and selectively induce neuritogenesis or potentiate neurotrophin-3 trophic signals. ACS Chem Biol. 2009;4:769-781.
30. Lebrun-Julien F, Duplan L, Pernet V, et al. Excitotoxic death of retinal neurons in vivo occurs via a non-cell-autonomous mechanism. J Neurosci. 2009;29:5536-5545.
31. Lebrun-Julien F, Morquette B, Douillette A, Saragovi HU, Di Polo A. Inhibition of p75(nTR) in glia potentiates TrkA-mediated survival of injured retinal ganglion cells. Mol Cell Neurosci. 2009;40:410-420.
32. Thanos S. Specific transcellular carbocyanine-labelling of rat retinal microglia during injury-induced neuronal degeneration. Neurosci Lett. 1991;127:108-112.
33. Scotter EL, Narayan P, Glass M, Dragunow M. High throughput quantification of mutant huntingtin aggregates. J Neurosci Methods. 2008;171:174-179.
34. Soto I, Oglesby E, Buckingham BP, et al. Retinal ganglion cells downregulate gene expression and lose their axons within the optic nerve head in a mouse glaucoma model. J Neurosci. 2008; 28:548-561.
35. Bai Y, Xu J, Brahimi F, Zhuo Y, Sarunic MV, Saragovi HU. An agonistic TrkB mAb causes sustained TrkB activation, delays RGC death, and protects the retinal structure in optic nerve axotomy and in glaucoma. Invest Ophthalmol Vis Sci. 2010;51:4722-4731.
36. Ichaso N, Rodriguez RE, Martin-Zanca D, Gonzalez-Sarmiento R. Genomic characterization of the human trkC gene. Oncogene. 1998;17:1871-1875.
37. Wax MB, Tezel G, Yang J, et al. Induced autoimmunity to heat shock proteins elicits glaucomatous loss of retinal ganglion cell neurons via activated T-cell-derived fas-ligand. J Neurosci. 2008; 28:12085-12096.
38. Meda L, Cassatella MA, Szendrei GI, et al. Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature. 1995; 374:647-650.
39. Cotinet A, Goureau O, Hicks D, Thillaye-Goldenberg B, de Kozak Y. Tumor necrosis factor and nitric oxide production by retinal Muller glial cells from rats exhibiting inherited retinal dystrophy. Glia. 1997;20:59-69.
40. Halpern DL, Grosskreutz CL. Glaucomatous optic neuropathy: mechanisms of disease. Ophthalmol Clin North Am. 2002;15:61-68.
41. Rudzinski M, Saragovi HU. Glaucoma: validated and facile in vivo experimental models of a chronic neurodegenerative disease for drug development. Curr Med Chem. 2005;5:43-49.
42. Dkhissi O, Chanut E, Wasowicz M, et al. Retinal TUNEL-positive cells and high glutamate levels in vitreous humor of mutant quail with a glaucoma-like disorder. Invest Ophthalmol Vis Sci. 1999; 40:990-995.
43. Siu AW, Leung MC, To CH, Siu FK, Ji JZ, So KF. Total retinal nitric oxide production is increased in intraocular pressure-elevated rats. Exp Eye Res. 2002;75:401-406.
44. Vorwerk CK, Naskar R, Schuettauf F, et al. Depression of retinal glutamate transporter function leads to elevated intravitreal glutamate levels and ganglion cell death. Invest Ophthalmol Vis Sci. 2000;41:3615-3621.
45. Lipton SA. Paradigm shift in NMDA receptor antagonist drug development: molecular mechanism of uncompetitive inhibitionby memantine in the treatment of Alzheimer's disease and other neurologic disorders. J Alzheimers Dis. 2004;6:S61-S74.
46. Saragovi HU, Hamel E, Di Polo A. A neurotrophic rationale for the therapy of neurodegenerative disorders. Curr Alzheimer Res. 2009;6:419-423.
47. Guo L, Salt TE, Luong V, et al. Targeting amyloid-beta in glaucoma treatment. Proc Natl Acad Sci U S A. 2007;104:13444-13449.
48. McKinnon SJ. Glaucoma: ocular Alzheimer's disease? Front Biosci.2003;8:S1140-S1156.
49. Huang W, Fileta JB, Dobberfuhl A, et al. Calcineurin cleavage istriggered by elevated intraocular pressure, and calcineurin inhibition blocks retinal ganglion cell death in experimental glaucoma. Proc Natl Acad Sci U S A. 2005;102:12242-12247.
50. Suzuki Y, Iwase A, Araie M, et al. Risk factors for open-angle glaucoma in a Japanese population: the Tajimi Study. Ophthalmology. 2006;113:1613-1617.