Cell therapy modulates expression of tax1-binding protein 1 and Synaptotagmin IV in a model of optic nerve lesion

Investigative Ophthalmology and Visual Science

Volumn 53, Issue 8, 2012, Pages 4720-4729

  Mesentier Louro, Louise A ^a,b   Coronel, Juliana ^a,b   Zaverucha do Valle, Camila ^a,b   Mencalha, Andre ^c   Paredes, Bruno D ^a   Abdelhay, Eliana ^c   Mendez Otero, Rosalia ^a,b   Santiago, Marcelo F ^a,b  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b Instituto Nacional de Ciência e Tecnologia Entomologia Molecular   (Brazil)

^c INSTITUTO NACIONAL DE CÂNCER   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PEPTIDES AND PROTEINS; SYNAPTOTAGMIN IV; TAX1 BINDING PROTEIN 1; UNCLASSIFIED DRUG; SIGNAL PEPTIDE; SYNAPTOTAGMIN; TAX1 BINDING PROTEIN 1, RAT; TAX1-BINDING PROTEIN 1, RAT; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BONE MARROW CELL; CELL ISOLATION; CELL THERAPY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; GENE SEQUENCE; IMMUNOHISTOCHEMISTRY; MALE; MONONUCLEAR CELL; MUELLER CELL; NERVE CRUSH; NERVE FIBER; NONHUMAN; OPTIC NERVE LESION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT; RETINA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; DISEASE MODEL; METABOLISM; METHODOLOGY; OPTIC NERVE; OPTIC NERVE INJURY; PHYSIOLOGY; RETINA GANGLION CELL;

ANIMALS; BLOTTING, WESTERN; BONE MARROW CELLS; DISEASE MODELS, ANIMAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NEOPLASM PROTEINS; NERVE CRUSH; OPTIC NERVE; OPTIC NERVE INJURIES; POLYMERASE CHAIN REACTION; RATS; RETINA; RETINAL GANGLION CELLS; SYNAPTOTAGMINS;

EID: 84866443355     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.11-8198     Document Type: Article

References (65)

1. Horner PJ, Gage FH. Regenerating the damaged central nervous system. Nature. 2000;407:963-970.
2. Johnson EM Jr, Deckwerth TL. Molecular mechanisms of developmental neuronal death. Annu Rev Neurosci. 1993;16: 31-46.
3. Levkovitch-Verbin H. Experimental glaucoma and optic nerve transection induce simultaneous upregulation of proapoptotic and prosurvival genes. Invest Ophthalmol Vis Sci. 2006;47: 2491-2497.
4. Agudo M, Pérez-Marín MC, Lönngren U, et al. Time course profiling of the retinal transcriptome after optic nerve. Mol Vis. 2008;14:1050-1063.
5. Piri N, Kwong JMK, Song M, Elashoff D, Caprioli J. Gene expression changes in the retina following optic nerve transection. Mol Vis. 2006;12:1660-1673.
6. Wong EV, David S, Jacob MH, Jay DG. Inactivation of myelinassociated glycoprotein enhances optic nerve regeneration. J Neurosci. 2003;23:3112-3117.
7. Fischer D. Counteracting the nogo receptor enhances optic nerve regeneration if retinal ganglion cells are in an active growth state. J Neurosci. 2004;24:1646-1651.
8. Lingor P, Teusch N, Schwarz K, et al. 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. 2007;103:181-189.
9. Lingor P, Tonges L, Pieper N, et al. ROCK inhibition and CNTF interact on intrinsic signalling pathways and differentially regulate survival and regeneration in retinal ganglion cells. Brain. 2008;131:250-263.
10. Park KK, Liu K, Hu Y, et al. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science. 2008;322:963-966.
11. Smith PD, Sun F, Park KK, et al. SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron. 2009;64:617-623.
12. Sun F, Park KK, Belin S, et al. Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature. 2011; 480:372-375.
13. Leon S, Yin Y, Nguyen J, Irwin N, Benowitz LI. Lens injury stimulates axon regeneration in the mature rat optic nerve. J Neurosci. 2000;20:4615-4626.
14. Fischer D, Pavlidis M, Thanos S. Cataractogenic lens injury prevents traumatic ganglion cell death and promotes axonal regeneration both in vivo and in culture. Invest Ophthalmol Vis Sci. 2000;41:3943-3954.
15. Yin Y, Cui Q, Li Y, et al. Macrophage-derived factors stimulate optic nerve regeneration. JNeurosci. 2003;23:2284-2293.
16. Yin Y, Henzl MT, Lorber B, et al. Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells. Nat Neurosci. 2006;9:843-852.
17. Yin Y, Cui Q, Gilbert HY, et al. Oncomodulin links inflammation to optic nerve regeneration. Proc Natl Acad Sci USA. 2009;106:19587-19592.
18. Kurimoto T, Yin Y, Omura K, et al. Long-distance axon regeneration in the mature optic nerve: contributions of oncomodulin, cAMP, and pten gene deletion. J Neurosci. 2010; 30:15654-15663.
19. Fischer D. CNTF, a key factor mediating the beneficial effects of inflammatory reactions in the eye. Brain. 2008;131:e97.
20. Leibinger M, Muller A, Andreadaki A, Hauk TG, Kirsch M, Fischer D. Neuroprotective and axon growth-promoting effects following inflammatory stimulation on mature retinal ganglion cells in mice depend on ciliary neurotrophic factor and leukemia inhibitory factor. J Neurosci. 2009;29:14334-14341.
21. 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;41:233-246.
22. Moore DL, Blackmore MG, Hu Y, et al. KLF family members regulate intrinsic axon regeneration ability. Science. 2009;326: 298-301.
23. Parr AM, Tator CH, Keating A. Bone marrow-derived mesenchymal stromal cells for the repair of central nervous system injury. Bone Marrow Transplant. 2007;40:609-619.
24. Ohtaki H, Ylostalo JH, Foraker JE, et al. Stem/progenitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflammatory/immune responses. Proc Natl Acad Sci USA. 2008;105:14638-14643.
25. de Vasconcelos Dos Santos A, da Costa Reis J, Diaz Paredes B, et al. Therapeutic window for treatment of cortical ischemia with bone marrow-derived cells in rats. Brain Res. 2010;1306: 149-158.
26. Brenneman M, Sharma S, Harting M, et al. Autologous bone marrow mononuclear cells enhance recovery after acute ischemic stroke in young and middle-aged rats. J Cereb Blood Flow Metab. 2010;30:140-149.
27. Johnson TV, Bull ND, Hunt DP, Marina N, Tomarev SI, Martin KR. Neuroprotective effects of intravitreal mesenchymal stem cell transplantation in experimental glaucoma. Invest Ophthalmol Vis Sci. 2010;51:2051-2059.
28. Levkovitch-Verbin H, Sadan O, Vander S, et al. Intravitreal injections of neurotrophic factors secreting mesenchymal stem cells are neuroprotective in rat eyes following optic nerve transection. Invest Ophthalmol Vis Sci. 2010;51:6394-6400.
29. Zaverucha-do-Valle C, Gubert F, Bargas-Rega M, et al. Bone marrow mononuclear cells increase retinal ganglion cell survival and axon regeneration in the adult rat. Cell Transplant. 2011;20:391-406.
30. Barbosa da Fonseca LM, Gutfilen B, Rosado de Castro PH, et al. Migration and homing of bone-marrow mononuclear cells in chronic ischemic stroke after intra-arterial injection. Exp Neurol. 2010;221:122-128.
31. Chopp M, Li Y. Treatment of neural injury with marrow stromal cells. Lancet Neurol. 2002;1:92-100.
32. Liang P, Pardee AB. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science. 1992;257:967-971.
33. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25:402-408.
34. De Valck D, Jin DY, Heyninck K, et al. The zinc finger protein A20 interacts with a novel anti-apoptotic protein which is cleaved by specific caspases. Oncogene. 1999;18:4182-4190.
35. Ulrich M, Seeber S, Becker CM, Enz R. Tax1-binding protein 1 is expressed in the retina and interacts with the GABA(C) receptor rho1 subunit. Biochem J. 2007;401:429-436.
36. Vician L, Lim IK, Ferguson G, Tocco G, Baudry M, Herschman HR. Synaptotagmin IV is an immediate early gene induced by depolarization in PC12 cells and in brain. Proc Natl Acad Sci USA. 1995;92:2164-2168.
37. Wang CT, Grishanin R, Earles CA, et al. Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science. 2001;294:1111-1115.
38. Zhang Q, Pangrsic T, Kreft M, et al. Fusion-related release of glutamate from astrocytes. J Biol Chem. 2004;279:12724-12733.
39. Saraswati S, Adolfsen B, Littleton JT. Characterization of the role of the Synaptotagmin family as calcium sensors in facilitation and asynchronous neurotransmitter release. Proc Natl Acad Sci USA. 2007;104:14122-14127.
40. Lutsch G, Stahl J, Kargel HJ, Noll F, Bielka H. Immunoelectron microscopic studies on the location of ribosomal proteins on the surface of the 40S ribosomal subunit from rat liver. Eur J Cell Biol. 1990;51:140-150.
41. Kocher O, Krieger M. Role of the adaptor protein PDZK1 in controlling the HDL receptor SR-BI. Curr Opin Lipidol. 2009; 20:236-241.
42. Jin DY, Jeang KT. HTLV-I Tax self-association in optimal transactivation function. Nucleic Acids Res. 1997;25:379-387.
43. Chin KT, Chun AC, Ching YP, Jeang KT, Jin DY. Human T-cell leukemia virus oncoprotein tax represses nuclear receptordependent transcription by targeting coactivator TAX1BP1. Cancer Res. 2007;67:1072-1081.
44. Shembade N, Harhaj NS, Parvatiyar K, et al. The E3 ligase Itch negatively regulates inflammatory signaling pathways by controlling the function of the ubiquitin-editing enzyme A20. Nat Immunol. 2008;9:254-262.
45. Tezel G, Wax MB. Increased production of tumor necrosis factor-alpha by glial cells exposed to simulated ischemia or elevated hydrostatic pressure induces apoptosis in cocultured retinal ganglion cells. J Neurosci. 2000;20:8693-8700.
46. Yuan L, Neufeld AH. Tumor necrosis factor-alpha: a potentially neurodestructive cytokine produced by glia in the human glaucomatous optic nerve head. Glia. 2000;32:42-50.
47. Fontaine V, Mohand-Said S, Hanoteau N, Fuchs C, Pfizenmaier K, Eisel U. Neurodegenerative and neuroprotective effects of tumor necrosis factor (TNF) in retinal ischemia: opposite roles of TNF receptor 1 and TNF receptor 2. J Neurosci. 2002;22: RC216.
48. Tezel G, Yang X, Yang J, Wax MB. Role of tumor necrosis factor receptor-1 in the death of retinal ganglion cells following optic nerve crush injury in mice. Brain Res. 2004;996:202-212.
49. Sudhof TC, Rizo J. Synaptotagmins: C2-domain proteins that regulate membrane traffic. Neuron. 1996;17:379-388.
50. Tocco G, Bi X, Vician L, Lim IK, Herschman H, Baudry M. Two synaptotagmin genes, Syt1 and Syt4, are differentially regulated in adult brain and during postnatal development following kainic acid-induced seizures. Brain Res Mol Brain Res. 1996; 40:229-239.
51. Ibata K, Fukuda M, Hamada T, Kabayama H, Mikoshiba K. Synaptotagmin IV is present at the Golgi and distal parts of neurites. J Neurochem. 2000;74:518-526.
52. Ferguson GD, Thomas DM, Elferink LA, Herschman HR. Synthesis degradation, and subcellular localization of synaptotagmin IV, a neuronal immediate early gene product. J Neurochem. 1999;72:1821-1831.
53. Littleton JT, Serano TL, Rubin GM, Ganetzky B, Chapman ER. Synaptic function modulated by changes in the ratio of synaptotagmin I and IV. Nature. 1999;400:757-760.
54. Wang Z, Chapman ER. Rat and Drosophila synaptotagmin 4 have opposite effects during SNARE-catalyzed membrane fusion. J Biol Chem. 2010;285:30759-30766.
55. Zhang Z, Bhalla A, Dean C, Chapman ER, Jackson MB. Synaptotagmin IV: a multifunctional regulator of peptidergic nerve terminals. Nat Neurosci. 2009;12:163-171.
56. Dean C, Liu H, Dunning FM, Chang PY, Jackson MB, Chapman ER. Synaptotagmin-IV modulates synaptic function and longterm potentiation by regulating BDNF release. Nat Neurosci. 2009;12:767-776.
57. Hamilton NB, Attwell D. Do astrocytes really exocytose neurotransmitters? Nat Rev Neurosci. 2010;11:227-238.
58. Berntson AK, Morgans CW. Distribution of the presynaptic calcium sensors, synaptotagmin I/II and synaptotagmin III, in the goldfish and rodent retinas. J Vis. 2003;3:274-280.
59. Bezzi P, Domercq M, Brambilla L, et al. CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat Neurosci. 2001;4:702-710.
60. Doble A. The role of excitotoxicity in neurodegenerative disease: implications for therapy. Pharmacol Ther. 1999;81: 163-221.
61. Dahlmann-Noor A, Vijay S, Jayaram H, Limb A, Khaw PT. Current approaches and future prospects for stem cell rescue and regeneration of the retina and optic nerve. Can J Ophthalmol. 2010;45:333-341.
62. Rehen SK, Varella MH, Freitas FG, Moraes MO, Linden R. Contrasting effects of protein synthesis inhibition and of cyclic AMP on apoptosis in the developing retina. Development. 1996;122:1439-1448.
63. Nishiura H, Shibuya Y, Yamamoto T. S19 ribosomal protein cross-linked dimer causes monocyte-predominant infiltration by means of molecular mimicry to complement C5a. Lab Invest. 1998;78:1615-1623.
64. Horino K, Nishiura H, Ohsako T, et al. A monocyte chemotactic factor, S19 ribosomal protein dimer, in phagocytic clearance of apoptotic cells. Lab Invest. 1998;78:603-617.
65. Soulet F, Al Saati T, Roga S, Amalric F, Bouche G. Fibroblast growth factor-2 interacts with free ribosomal protein S19. Biochem Biophys Res Commun. 2001;289:591-596.