Brain-derived neurotrophic factor inhibits osmotic swelling of rat retinal glial (Müller) and bipolar cells by activation of basic fibroblast growth factor signaling

Neuroscience

Volumn 295, Issue , 2015, Pages 175-186

  Berk, B A ^a   Vogler, S ^a   Pannicke, T ^a   Kuhrt, H ^a   Garcia, T B ^a,b   Wiedemann, P ^a   Reichenbach, A ^a   Seeger, J ^a   Bringmann, A ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b FEDERAL UNIVERSITY OF PARÁ   (Brazil)

Author keywords

Bipolar cell; Brain derived neurotrophic factor; Cell swelling; Glia; Osmotic stress; Retina

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; RECOMBINANT BASIC FIBROBLAST GROWTH FACTOR; RECOMBINANT BRAIN DERIVED NEUROTROPHIC FACTOR; BARIUM; BRAIN DERIVED NEUROTROPHIC FACTOR; FIBROBLAST GROWTH FACTOR; PROTEIN KINASE C;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SWELLING; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVATION; FEMALE; MALE; MUELLER CELL; NEUROPROTECTION; NONHUMAN; OSMOTIC STRESS; PERIKARYON; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; RETINA BIPOLAR GANGLION CELL; SIGNAL TRANSDUCTION; TRANSACTIVATION; ANALYSIS OF VARIANCE; ANIMAL; CYTOLOGY; DRUG EFFECTS; EDEMA; IN VITRO STUDY; LONG EVANS RAT; MACROGLIA; METABOLISM; NONPARAMETRIC TEST; OSMOTIC PRESSURE; RETINA; TIME;

ANALYSIS OF VARIANCE; ANIMALS; BARIUM; BRAIN-DERIVED NEUROTROPHIC FACTOR; EDEMA; EPENDYMOGLIAL CELLS; FEMALE; FIBROBLAST GROWTH FACTORS; IN VITRO TECHNIQUES; MALE; OSMOTIC PRESSURE; PROTEIN KINASE C; RATS; RATS, LONG-EVANS; RECEPTOR, TRKB; RETINA; RETINAL BIPOLAR CELLS; SIGNAL TRANSDUCTION; STATISTICS, NONPARAMETRIC; TIME FACTORS;

EID: 84926482960     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.03.037     Document Type: Article

References (60)

1. Asai N., Abe T., Saito T., Sato H., Ishiguro S., Nishida K. Temporal and spatial differences in expression of TrkB isoforms in rat retina during constant light exposure. Exp Eye Res 2007, 85:346-355.
2. Baxter G.T., Radeke M.J., Kuo R.C., Makrides V., Hinkle B., Hoang R., Medina-Selby A., Coit D., Valenzuela P., Feinstein S.C. Signal transduction mediated by the truncated trkB receptor isoforms, trkB.T1 and trkB.T2. J Neurosci 1997, 17:2683-2690.
3. Bennett J.L., Zeiler S.R., Jones K.R. Patterned expression of BDNF and NT-3 in the retina and anterior segment of the developing mammalian eye. Invest Ophthalmol Vis Sci 1999, 40:2996-3005.
4. Blum R., Konnerth A. Neurotrophin-mediated rapid signaling in the central nervous system: mechanisms and functions. Physiology 2005, 20:70-78.
5. Bresnick G.H. Diabetic maculopathy. A critical review highlighting diffuse macular edema. Ophthalmology 1983, 90:1301-1317.
6. Bringmann A., Uckermann O., Pannicke T., Iandiev I., Reichenbach A., Wiedemann P. Neuronal versus glial cell swelling in the ischaemic retina. Acta Ophthalmol Scand 2005, 83:528-538.
7. Bringmann A., Iandiev I., Pannicke T., Wurm A., Hollborn M., Wiedemann P., Osborne N.N., Reichenbach A. Cellular signaling and factors involved in Müller cell gliosis: neuroprotective and detrimental effects. Prog Retin Eye Res 2009, 28:423-451.
8. Casaccia-Bonnefil P., Gu C., Chao M.V. Neurotrophins in cell survival/death decisions. Adv Exp Med Biol 1999, 468:275-282.
9. Cazorla M., Jouvenceau A., Rose C., Guilloux J.P., Pilon C., Dranovsky A., Prémont J. Cyclotraxin-B, the first highly potent and selective TrkB inhibitor, has anxiolytic properties in mice. PLoS One 2010, 5:e9777.
10. Cellerino A., Kohler K. Brain-derived neurotrophic factor/neurotrophin-4 receptor TrkB is localized on ganglion cells and dopaminergic amacrine cells in the vertebrate retina. J Comp Neurol 1997, 386:149-160.
11. Chao M.V., Hempstead B.L. P75 and Trk: a two-receptor system. Trends Neurosci 1995, 18:321-326.
12. Di Polo A., Cheng L., Bray G.M., Aguayo A.J. Co-localization of TrkB and brain-derived neurotrophic factor proteins in green/red-sensitive cone outer segments. Invest Ophthalmol Vis Sci 2000, 41:4014-4021.
13. Dmitriev A.V., Govardovskii V.I., Schwahn H.N., Steinberg R.H. Light-induced changes of extracellular ions and volume in the isolated chick retina-pigment epithelium preparation. Vis Neurosci 1999, 16:1157-1167.
14. Dorsey S.G., Renn C.L., Carim-Todd L., Barrick C.A., Bambrick L., Krueger B.K., Ward C.W., Tessarollo L. 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.
15. Dudek F.E., Obenhaus A., Tasker J.G. Osmolality-induced changes in extracellular volume alter epileptiform bursts independent of chemical synapses in the rat: importance of non-synaptic mechanisms in hippocampal epileptogenesis. Neurosci Lett 1990, 120:267-270.
16. Faktorovich E.G., Steinberg R.H., Yasumura D., Matthes M.T., LaVail M.M. Basic fibroblast growth factor and local injury protect photoreceptors from light damage in the rat. J Neurosci 1992, 12:3554-3567.
17. Frisen J., Verge V.M., Fried K., Risling M., Persson H., Trotter J., Hökfelt T., Lindholm D. Characterization of glial TrkB receptors: differential response to injury in the central and peripheral nervous systems. Proc Natl Acad Sci USA 1993, 90:4971-4975.
18. Fujieda H., Sasaki H. Expression of brain-derived neurotrophic factor in cholinergic and dopaminergic amacrine cells in the rat retina and the effects of constant light rearing. Exp Eye Res 2008, 86:335-343.
19. Gabriel R., Lesauter J., Silver R., Garcia-Espana A., Witkovsky P. Diurnal and circadian variation of protein kinase C immunoreactivity in the rat retina. J Comp Neurol 2001, 439:140-150.
20. Garcia T.B., Pannicke T., Vogler S., Berk B.-A., Grosche A., Wiedemann P., Seeger J., Reichenbach A., Herculano A.M., Bringmann A. Nerve growth factor inhibits osmotic swelling of rat retinal glial (Müller) and bipolar cells by inducing glial cytokine release. J Neurochem 2014, 131:303-313.
21. Grishanin R.N., Yang H., Liu X., Donohue-Rolfe K., Nune G.C., Zang K., Xu B., Duncan J.L., Lavail M.M., Copenhagen D.R., Reichardt L.F. Retinal TrkB receptors regulate neural development in the inner, but not outer, retina. Mol Cell Neurosci 2008, 38:431-443.
22. Harada T., Harada C., Nakayama N., Okuyama S., Yoshida K., Kohsaka S., Matsuda H., Wada K. Modification of glial-neuronal cell interactions prevents photoreceptor apoptosis during light-induced retinal degeneration. Neuron 2000, 26:533-541.
23. Harada T., Harada C., Kohsaka S., Wada E., Yoshida K., Ohno S., Mamada H., Tanaka K., Parada L.F., Wada K. Microglia-Müller glia cell interactions control neurotrophic factor production during light-induced retinal degeneration. J Neurosci 2002, 22:9228-9236.
24. Harada C., Guo X., Namekata K., Kimura A., Nakamura K., Tanaka K., Parada L.F., Harada T. Glia- and neuron-specific functions of TrkB signalling during retinal degeneration and regeneration. Nat Commun 2011, 2:189.
25. Hauck S.M., Kinkl N., Deeg C.A., Swiatek-de Lange M., Schöffmann S., Ueffing M. GDNF family ligands trigger indirect neuroprotective signaling in retinal glial cells. Mol Cell Biol 2006, 26:2746-2757.
26. Hirsch S., Labes M., Bähr M. Changes in BDNF and neurotrophin receptor expression in degenerating and regenerating rat retinal ganglion cells. Restor Neurol Neurosci 2000, 17:125-134.
27. Kaur C., Sivakumar V., Yong Z., Lu J., Foulds W.S., Ling E.A. Blood-retinal barrier disruption and ultrastructural changes in the hypoxic retina in adult rats: the beneficial effect of melatonin administration. J Pathol 2007, 212:429-439.
28. Klein R., Nanduri V., Jing S.A., Lamballe F., Tapley P., Bryant S., Cordon-Cardo C., Jones K.R., Reichardt L.F., Barbacid M. The TrkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3. Cell 1991, 66:395-403.
29. Krügel K., Wurm A., Linnertz R., Pannicke T., Wiedemann P., Reichenbach A., Bringmann A. Erythropoietin inhibits osmotic swelling of retinal glial cells by Janus kinase and extracellular signal-regulated kinases1/2-mediated release of vascular endothelial growth factor. Neuroscience 2010, 165:1147-1158.
30. Kumar B., Gupta S.K., Srinivasan B.P., Nag T.C., Srivastava S., Saxena R., Jha K.A. Hesperetin rescues retinal oxidative stress, neuroinflammation and apoptosis in diabetic rats. Microvasc Res 2013, 87:65-74.
31. LaVail M.M., Unoki K., Yasumura D., Matthes M.T., Yancopoulos G.D., Steinberg R.H. Multiple growth factors, cytokines, and neurotrophins rescue photoreceptors from the damaging effects of constant light. Proc Natl Acad Sci USA 1992, 89:11249-11253.
32. Mansour-Robaey S., Clarke D.B., Wang Y.C., Bray G.M., Aguayo A.J. 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, 91:1632-1636.
33. Mohammadi M., Froum S., Hamby J.M., Schroeder M.C., Panek R.L., Lu G.H., Eliseenkova A.V., Green D., Schlessinger J., Hubbard S.R. Crystal structure of an angiogenesis inhibitor bound to the FGF receptor tyrosine kinase domain. EMBO J 1998, 17:5896-5904.
34. Ohira K., Shimizu K., Yamashita A., Hayashi M. Differential expression of the truncated TrkB receptor, T1, in the primary motor and prefrontal cortices of the adult macaque monkey. Neurosci Lett 2005, 385:105-109.
35. Pannicke T., Iandiev I., Uckermann O., Biedermann B., Kutzera F., Wiedemann P., Wolburg H., Reichenbach A., Bringmann A. A potassium channel-linked mechanism of glial cell swelling in the postischemic retina. Mol Cell Neurosci 2004, 26:493-502.
36. Perez M.T., Caminos E. Expression of brain-derived neurotrophic factor and of its functional receptor in neonatal and adult rat retina. Neurosci Lett 1995, 183:96-99.
37. Rickman D.W., Brecha N.C. Expression of the proto-oncogene, trk, receptors in the developing rat retina. Vis Neurosci 1995, 12:215-222.
38. Rohrer B., Korenbrot J.I., LaVail M.M., Reichardt L.F., Xu B. Role of neurotrophin receptor TrkB in the maturation of rod photoreceptors and establishment of synaptic transmission to the inner retina. J Neurosci 1999, 19:8919-8930.
39. Rohrer B., Blanco R., Marc R.E., Lloyd M.B., Bok D., Schneeweis D.M., Reichardt L.F. Functionally intact glutamate-mediated signaling in bipolar cells of the TrkB knockout mouse retina. Vis Neurosci 2004, 21:703-713.
40. Rose C.R., Blum R., Pichler B., Lepier A., Kafitz K.W., Konnerth A. Truncated TrkB-T1 mediates neurotrophin-evoked calcium signalling in glia cells. Nature 2003, 426:74-78.
41. Rothova A., Suttorp-van Schulten M.S., Frits Treffers W., Kijlstra A. Causes and frequency of blindness in patients with intraocular inflammatory disease. Br J Ophthalmol 1996, 80:332-336.
42. Saito T., Abe T., Wakusawa R., Sato H., Asai H., Tokita-Ishikawa Y., Nishida K. TrkB-T1 receptors on Müller cells play critical role in brain-derived neurotrophic factor-mediated photoreceptor protection against phototoxicity. Curr Eye Res 2009, 34:580-588.
43. Seki M., Nawa H., Fukuchi T., Abe H., Takei N. BDNF is upregulated by postnatal development and visual experience: quantitative and immunohistochemical analyses of BDNF in the rat retina. Invest Ophthalmol Vis Sci 2003, 44:3211-3218.
44. Seki M., Tanaka T., Sakai Y., Fukuchi T., Abe H., Nawa H., Takei N. Müller cells as a source of brain-derived neurotrophic factor in the retina: noradrenaline upregulates brain-derived neurotrophic factor levels in cultured rat Müller cells. Neurochem Res 2005, 30:1163-1170.
45. Shen J., Ghai K., Sompol P., Liu X., Cao X., Iuvone P.M., Ye K. N-acetyl serotonin derivatives as potent neuroprotectants for retinas. Proc Natl Acad Sci USA 2012, 109:3540-3545.
46. Stepinac T.K., Chamot S.R., Rungger-Brändle E., Ferrez P., Munoz J.L., Van Den Bergh H., Riva C.E., Pournaras C.J., Wagnieres G.A. Light-induced retinal vascular damage by Pd-porphyrin luminescent oxygen probes. Invest Ophthalmol Vis Sci 2005, 46:956-966.
47. Suzuki A., Nomura S., Morii E., Fukuda Y., Kosaka J. Localization of mRNAs for trkB isoforms and p75 in rat retinal ganglion cells. J Neurosci Res 1998, 54:27-37.
48. Szél Á., Röhlich P. Two cone types of rat retina detected by anti-visual pigment antibodies. Exp Eye Res 1992, 55:47-52.
49. Tapley P., Lamballe F., Barbacid M. K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors. Oncogene 1992, 7:371-381.
50. Uckermann O., Vargová L., Ulbricht E., Klaus C., Weick M., Rillich K., Wiedemann P., Reichenbach A., Syková E., Bringmann A. Glutamate-evoked alterations of glial and neuronal cell morphology in the guinea-pig retina. J Neurosci 2004, 24:10149-10158.
51. Uckermann O., Wolf A., Kutzera F., Kalisch F., Beck-Sickinger A., Wiedemann P., Reichenbach A., Bringmann A. Glutamate release by neurons evokes a purinergic inhibitory mechanism of osmotic glial cell swelling in the rat retina: activation by neuropeptide Y. J Neurosci Res 2006, 83:538-550.
52. Unoki K., LaVail M.M. Protection of the rat retina from ischemic injury by brain-derived neurotrophic factor, ciliary neurotrophic factor, and basic fibroblast growth factor. Invest Ophthalmol Vis Sci 1994, 35:907-915.
53. Vecino E., García-Crespo D., García M., Martinez-Millán L., Sharma S.C., Carrascal E. Rat retinal ganglion cells co-express brain derived neurotrophic factor (BDNF) and its receptor TrkB. Vision Res 2002, 42:151-157.
54. Vogler S., Grosche A., Pannicke T., Ulbricht E., Wiedemann P., Reichenbach A., Bringmann A. Hypoosmotic and glutamate-induced swelling of bipolar cells in the rat retina: comparison with swelling of Müller glial cells. J Neurochem 2013, 126:372-381.
55. Wahl V., Vogler S., Grosche A., Pannicke T., Ueffing M., Wiedemann P., Reichenbach A., Hauck S.M., Bringmann A. Osteopontin inhibits osmotic swelling of retinal glial (Müller) cells by inducing release of VEGF. Neuroscience 2013, 246:59-72.
56. Wahlin K.J., Campochiaro P.A., Zack D.J., Adler R. Neurotrophic factors cause activation of intracellular signaling pathways in Müller cells and other cells of the inner retina, but not photoreceptors. Invest Ophthalmol Vis Sci 2000, 41:927-936.
57. Wahlin K.J., Adler R., Zack D.J., Campochiaro P.A. Neurotrophic signaling in normal and degenerating rodent retinas. Exp Eye Res 2001, 73:693-701.
58. Wexler E.M., Berkovich O., Nawy S. Role of the low-affinity NGF receptor (p75) in survival of retinal bipolar cells. Vis Neurosci 1998, 15:211-218.
59. Wurm A., Pannicke T., Wiedemann P., Reichenbach A., Bringmann A. Glial cell-derived glutamate mediates autocrine cell volume regulation in the retina: activation by VEGF. J Neurochem 2008, 104:386-399.
60. Yacoubian T.A., Lo D.C. Truncated and full-length TrkB receptors regulate distinct modes of dendritic growth. Nat Neurosci 2000, 3:342-349.