Retinal TrkB receptors regulate neural development in the inner, but not outer, retina

Molecular and Cellular Neuroscience

Volumn 38, Issue 3, 2008, Pages 431-443

  Grishanin, Ruslan N ^a   Yang, Haidong ^b   Liu, Xiaorong ^a,b   Donohue Rolfe, Kate ^b   Nune, George C ^b   Zang, Keling ^a   Xu, Baoji ^c   Duncan, Jacque L ^b   LaVail, Matthew M ^a,b   Copenhagen, David R ^a,b   Reichardt, Louis F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c GEORGETOWN UNIVERSITY   (United States)

Author keywords

BDNF; Development; Electroretinograms; Photoreceptors; Retina; TrkB

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; TRANSCRIPTION FACTOR SIX3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ELECTRORETINOGRAM; GENOME ANALYSIS; MOUSE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA BIPOLAR GANGLION CELL; RETINA GANGLION CELL; RETINA NERVE CELL; SYNAPTIC TRANSMISSION;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NERVE NET; RECEPTOR, TRKB; RETINA; ROD CELL OUTER SEGMENT; SIGNAL TRANSDUCTION;

MUS;

EID: 45649085624     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2008.04.004     Document Type: Article

References (90)

1. Alsina B., Vu T., and Cohen-Cory S. Visualizing synapse formation in arborizing optic axons in vivo: dynamics and modulation by BDNF. Nat. Neurosci. 4 (2001) 1093-1101
2. Balkowiec A., and Katz D.M. Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J. Neurosci. 22 (2002) 10399-10407
3. Bayer A.U., Mittag T., Cook P., Brodie S.E., Podos S.M., and Maag K.P. Comparisons of the amplitude size and the reproducibility of three different electrodes to record the corneal flash electroretinogram in rodents. Doc. Ophthalmol. 98 (1999) 233-246
4. Blanks J.C., Adinolfi A.M., and Lolley R.N. Synaptogenesis in the photoreceptor terminal of the mouse retina. J. Comp. Neurol. 156 (1974) 81-93
5. Bok D., Yasumura D., Matthes M.T., Ruiz A., Duncan J.L., Chappelow A.V., Zolutukhin S., Hauswirth W., and LaVail M.M. Effects of adeno-associated virus-vectored ciliary neurotrophic factor on retinal structure and function in mice with a P216 L rds/peripherin mutation. Exp. Eye Res. 74 (2002) 719-735
6. Callahan C.A., and Thomas J.B. Tau-beta-galactosidase, an axon-targeted fusion protein. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 5972-5976
7. Cellerino A., and 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. 386 (1997) 149-160
8. Cellerino A., Pinzon-Duarte G., Carroll P., and Kohler K. Brain-derived neurotrophic factor modulates the development of the dopaminergic network in the rodent retina. J. Neurosci. 18 (1998) 3351-3362
9. Cellerino A., Arango-Gonzalez B.A., and Kohler K. Effects of brain-derived neurotrophic factor on the development of NADPH-diaphorase/nitric oxide synthase-positive amacrine cells in the rodent retina. Eur. J. Neurosci. 11 (1999) 2824-2834
10. Chang M.A., Horner J.W., Conklin B.R., DePinho R.A., Bok D., and Zack D.J. Tetracycline-inducible system for photoreceptor-specific gene expression. Invest. Ophthalmol. Vis. Sci. 41 (2000) 4281-4287
11. Conover J.C., Erickson J.T., Katz D.M., Bianchi L.M., Poueymirou W.T., McClain J., Pan L., Helgren M., Ip N.Y., Boland P., Friedman B., Wiegand S., Vejsada R., Kato A.C., DeChiara T.M., and Yancopoulos G.D. Neuronal deficits, not involving motor neurons, in mice lacking BDNF and/or NT4. Nature 18 (1995) 235-238
12. Di Polo A., Cheng L., Bray G.M., and Aguayo A.J. Colocalization of TrkB and brain-derived neurotrophic factor proteins in green-red-sensitive cone outer segments. Invest. Ophthalmol. Vis. Sci. 41 (2000) 4014-4021
13. Donovan M.J., Lin M.I., Wiegn P., Ringstedt T., Kraemer R., Hahn R., Wang S., Ibanez C.F., Rafii S., and Hempstead B.L. Brain derived neurotrophic factor is an endothelial cell survival factor required for intramyocardial vessel stabilization. Development 127 (2000) 4531-4540
14. Du J.L., and Poo M.M. Rapid BDNF-induced retrograde synaptic modification in a developing retinotectal system. Nature 429 (2004) 878-883
15. Du J., Feng L., Yang F., and Lu B. Activity- and Ca(2+)-dependent modulation of surface expression of brain-derived neurotrophic factor receptors in hippocampal neurons. J. Cell Biol. 150 (2000) 1423-1434
16. Fiumelli H., Kiraly M., Ambrus A., Magistretti P.J., and Martin J.L. Opposite regulation of calbindin and calretinin expression by brain-derived neurotrophic factor in cortical neurons. J. Neurochem. 74 (2000) 1870-1877
17. Furuta Y., Lagutin O., Hogan B.L., and Oliver G.C. Retina- and ventral forebrain-specific Cre recombinase activity in transgenic mice. Genesis 26 (2000) 130-132
18. Hackett S.F., Schoenfeld C.L., Freund J., Gottsch J.D., Bhargave S., and Campochiaro P.A. Neurotrophic factors, cytokines and stress increase expression of basic fibroblast growth factor in retinal pigmented epithelial cells. Exp. Eye Res. 64 (1997) 865-873
19. Hackett S.F., Friedman Z., Freund J., Schoenfeld C., Curtis R., DiStefano P.S., and Campochiaro P.A. A splice variant of trkB and brain-derived neurotrophic factor are co-expressed in retinal pigmented epithelial cells and promote differentiated characteristics. Brain Res. 789 (1998) 201-212
20. Haverkamp S., and Wassle H. Immunocytochemical analysis of the mouse retina. J. Comp. Neurol. 424 (2000) 1-23
21. Haverkamp S., Ghosh K.K., Hirano A.A., and Wassle H. Immunocytochemical description of five bipolar cell types of the mouse retina. J. Comp. Neurol. 455 (2003) 463-476
22. Howard D.R., and Sawyer D.C. Electroretinography of acute hypoxic and increased intraocular pressure status in the dog. Am. J. Vet. Res. 36 (1975) 81-84
23. Hu B., Nikolakopoulou A.M., and Cohen-Cory S. BDNF stabilizes synapses and maintains the structural complexity of optic axons in vivo. Development 132 (2005) 4285-4298
24. Huang E.J., and Reichardt L.F. Neurotrophins: roles in neuronal development and function. Annu. Rev., Neurosci. 24 (2001) 677-736
25. Huang E.J., and Reichardt L.F. Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 72 (2003) 609-642
26. Hyman C., Juhasz M., Jackson C., Wright P., Ip N.Y., and Lindsay R.M. Overlapping and distinct actions of the neurotrophins BDNF, NT-3, and NT-4/5 on cultured dopaminergic and GABAergic neurons of the ventral mesencephalon. J. Neurosci. 14 (1994) 335-347
27. Ip N.Y., Li Y., Yancopoulos G.D., and Lindsay R.M. Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4, but not NGF. J. Neurosci. 13 (1993) 3394-3405
28. Iwabe S., Moreno-Mendoza N.A., Trigo-Tavera F., Crowder C., and Garcia-Sanchez G.A. Retrograde axonal transport obstruction of brain-derived neurotrophic factor (BDNF) and its TrkB receptor in the retina and optic nerve of American Cocker Spaniel dogs with spontaneous glaucoma. Vet. Ophthalmol. 10 Suppl 1 (2007) 12-19
29. Jakobs T.C., Libby R.T., Ben Y., John S.W., and Masland R.H. Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice. J. Cell Biol. 171 (2005) 313-325
30. Jones K.R., Farinas I., Backus C., and Reichardt L.F. Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76 (1994) 989-999
31. Katz D.M. Neuronal growth factors and development of respiratory control. Respir. Physiol. Neurobiol. 135 (2003) 155-165
32. Kermani P., Rafii D., Jin D.K., Whitlock P., Schaffer W., Chiang A., Vincent L., Friedrich M., Shido K., Hackett N.R., Crystal R.G., Rafii S., and Hempstead B.L. Neurotrophins promote revascularization by local recruitment of TrkB+ endothelial cells and systemic mobilization of hematopoietic progenitors. J. Clin. Invest. 115 (2005) 653-663
33. Klein R., Smeyne R.J., Wurst W., Long L.K., Auerbach B.A., Joyner A.L., and Barbacid M. Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death. Cell 75 (1993) 113-122
34. Koide T., Takahashi J.B., Hoshimaru M., Kojima M., Otsuka T., Asahi M., and Kikuchi H. Localization of trkB and low-affinity nerve growth factor receptor mRNA in the developing rat retina. Neurosci. Lett. 185 (1995) 183-186
35. Kothe A.C., and Lovasik J.V. A parametric evaluation of retinal vascular perfusion pressure and visual neural function in man. Electroencephalogr. Clin. Neurophysiol. 75 (1990) 185-199
36. Kramer E.R., Aron L., Ramakers G.M.J., Seitz S., Zhuang X., Beyer K., Smidt M.P., and Klein R. Absence of Ret signaling in mice causes progressive and late degeneration of the nigrostriatal system. PLoS Biol. 5 (2007) e39
37. Krizaj D., Demarco S.J., Johnson J., Strehler E.E., and Copenhagen D.R. Cell-specific expression of plasma membrane calcium ATPase isoforms in retinal neurons. J. Comp. Neurol. 451 (2002) 1-21
38. Ladewig T., Fellner S., Zrenner E., Kohler K., and Guenther E. BDNF regulates NMDA receptor activity in developing retinal ganglion cells. Neuroreport 15 (2004) 2495-2499
39. Landi S., Cenni M.C., Maffei L., and Berardi N. Environmental enrichment effects on development of retinal ganglion cell dendritic stratification require retinal BDNF. PLoS ONE 2 (2007) e346
40. Landi S., Sale A., Berardi N., Viegi A., Maffei L., and Cenni M.C. Retinal functional development is sensitive to environmental enrichment: a role for BDNF. FASEB J. 21 (2007) 130-139
41. LaVail M.M., Gorrin G.M., Repaci M.A., Thomas L.A., and Ginsberg H.M. Genetic regulation of light damage to photoreceptors. Invest. Ophthalmol. Vis. Sci. 28 (1987) 1043-1048
42. Liu X., Grishanin R.N., Tolwani R.J., Renteria R.C., Xu B., Reichardt L.F., and Copenhagen D.R. Brain-derived neurotrophic factor and TrkB modulate visual experience-dependent refinement of neuronal pathways in retina. J. Neurosci. 27 (2007) 7256-7267
43. Lom B., and Cohen-Cory S. Brain-derived neurotrophic factor differentially regulates retinal ganglion cell dendritic and axonal arborization in vivo. J. Neurosci. 19 (1999) 9928-9938
44. Lom B., Cogen J., Sanchez A.L., Vu T., and Cohen-Cory S. Local and target-derived brain-derived neurotrophic factor exert opposing effects on the dendritic arborization of retinal ganglion cells in vivo. J. Neurosci. 22 (2002) 7639-7649
45. Luikart B.W., Nef S., Shipman T., and Parada L.F. In vivo role of truncated trkb receptors during sensory ganglion neurogenesis. Neuroscience 117 (2003) 847-858
46. Luikart B.W., Nef S., Virmani T., Lush M.E., Liu Y., Kavalali E.T., and Parada L.F. TrkB has a cell-autonomous role in the establishment of hippocampal Schaffer collateral synapses. J. Neurosci. 25 (2005) 3774-3786
47. Lykke-Andersen J. mRNA quality control: marking the message for life or death. Curr. Biol. 11 (2001) R88-R91
48. Mandolesi G., Menna E., Harauzov A., von Bartheld C.S., Caleo M., and Maffei L. A role for retinal brain-derived neurotrophic factor in ocular dominance plasticity. Curr. Biol. 15 (2005) 2119-2124
49. Melamed E., Frucht Y., Vidauri J., Uzzan A., and Rosenthal J. Effect of postnatal light deprivation on the ontogenesis of dopamine neurons in rat retina. Brain Res. 391 (1986) 280-284
50. Meyer-Franke A., Wilkinson G.A., Kruttgen A., Hu M., Munro E., Hanson Jr. M.G., Reichardt L.F., and Barres B.A. Depolarization and cAMP elevation rapidly recruit TrkB to the plasma membrane of CNS neurons. Neuron 21 (1998) 681-693
51. Morgan W.W., and Kamp C.W. Postnatal development of the light response of the dopaminergic neurons in the rat retina. J. Neurochem. 39 (1982) 283-285
52. Mullen R.J., and LaVail M.M. Inherited retinal dystrophy: primary defect in pigment epithelium determined with experimental rat chimeras. Science 192 (1976) 799-801
53. Neal M., Cunningham J., Lever I., Pezet S., and Malcangio M. Mechanism by which brain-derived neurotrophic factor increases dopamine release from the rabbit retina. Invest. Ophthalmol. Vis. Sci. 44 (2003) 791-798
54. Nusinowitz S., Ridder III W.H., and Heckenlively J.R. Electrophysiological testing of the mouse visual system. In: Smith R.S., John S.W.M., Nishina P.M., and Sundberg J.P. (Eds). Systematic Evaluation of the Mouse Eye: Anatomy, Pathology and Biomethods (2002), CRC Press, Boca Raton, FL 320
55. Oliver G., Mailhos A., Wehr R., Copeland N.G., Jenkins N.A., and Gruss P. Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 121 (1995) 4045-4055
56. Olney J.W. Centripetal sequence of appearance of receptor-bipolar synaptic structures in developing mouse retina. Nature 218 (1968) 281-282
57. Pappas I.S., and Parnavelas J.G. Neurotrophins and basic fibroblast growth factor induce the differentiation of calbindin-containing neurons in the cerebral cortex. Exp. Neurol. 144 (1997) 302-314
58. Peachey N.S., Goto Y., al Ubaidi M.R., and Naash M.I. Properties of the mouse cone-mediated electroretinogram during light adaptation. Neurosci. Lett. 162 (1993) 9-11
59. Pease M.E., McKinnon S.J., Quigley H.A., Kerrigan-Baumrind L.A., and Zack D.J. Obstructed axonal transport of BDNF and its receptor TrkB in experimental glaucoma. Invest Ophthalmol. Vis. Sci. 41 (2000) 764-774
60. Perez M.T., and Caminos E. Expression of brain-derived neurotrophic factor and of its functional receptor in neonatal and adult rat retina. Neurosci. Lett. 183 (1995) 96-99
61. Pollock G.S., Robichon R., Boyd K.A., Kerkel K.A., Kramer M., Lyles J., Ambalavanar R., Khan A., Kaplan D.R., Williams R.W., and Frost D.O. TrkB receptor signaling regulates developmental death dynamics, but not final number, of retinal ganglion cells. J. Neurosci. 23 (2003) 10137-10145
62. Pollock G.S., Vernon E., Forbes M.E., Yan Q., Ma Y.T., Hsieh T., Robichon R., Frost D.O., and Johnson J.E. Effects of early visual experience and diurnal rhythms on BDNF mRNA and protein levels in the visual system, hippocampus, and cerebellum. J. Neurosci. 21 (2001) 3923-3931
63. Quigley H.A., McKinnon S.J., Zack D.J., Pease M.E., Kerrigan-Baumrind L.A., Kerrigan D.F., and Mitchell R.S. Retrograde axonal transport of BDNF in retinal ganglion cells is blocked by acute IOP elevation in rats. Invest. Ophthalmol. Vis. Sci. 41 (2000) 3460-3466
64. Quina L.A., Pak W., Lanier J., Banwait P., Gratwick K., Liu Y., Velasquez T., O'Leary D.D., Goulding M., and Turner E.E. Brn3a-expressing retinal ganglion cells project specifically to thalamocortical and collicular visual pathways. J. Neurosci. 25 (2005) 11595-11604
65. Reichardt L.F. Neurotrophin-regulated signalling pathways. Philos. Trans. R. Soc. Lond., B Biol. Sci. 361 (2006) 1545-1564
66. Rico B., Xu B., and Reichardt L.F. TrkB receptor signaling is required for establishment of GABAergic synapses in the cerebellum. Nat. Neurosci. 5 (2002) 225-233
67. Robson J.G., Saszik S.M., Ahmed J., and Frishman L.J. Rod and cone contributions to the a-wave of the electroretinogram of the macaque. J. Physiol 547 (2003) 509-530
68. Rohrer B. Gene dosage effect of the TrkB receptor on rod physiology and biochemistry in juvenile mouse retina. Mol. Vis. 7 (2001) 288-296
69. Rohrer B., Korenbrot J.I., LaVail M.M., Reichardt L.F., and Xu B. Role of neurotrophin receptor TrkB in the maturation of rod photoreceptors and establishment of synaptic transmission to the inner retina. J. Neurosci. 19 (1999) 8919-8930
70. Rohrer B., LaVail M.M., Jones K.R., and Reichardt L.F. Neurotrophin receptor TrkB activation is not required for the postnatal survival of retinal ganglion cells in vivo. Exp. Neurol. 172 (2001) 81-91
71. Rohrer B., and Ogilvie J.M. Retarded outer segment development in TrkB knockout mouse retina organ culture. Mol. Vis. 9 (2003) 18-23
72. Rohrer B., Blanco R., Marc R.E., Lloyd M.B., Bok D., Schneeweis D.M., and Reichardt L.F. Functionally intact glutamate-mediated signaling in bipolar cells of the TRKB knockout mouse retina. Vis. Neurosci. 21 (2004) 703-713
73. Seki M., Nawa H., Fukuchi T., Abe H., and 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. 44 (2003) 3211-3218
74. Shelke R.R., Lakshmana M.K., Ramamohan Y., and Raju T.R. Levels of dopamine and noradrenaline in the developing of retina-effect of light deprivation. Int. J. Dev. Neurosci. 15 (1997) 139-143
75. Shieh P.B., Hu S.C., Bobb K., Timmusk T., and Ghosh A. Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 20 (1998) 727-740
76. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21 (1999) 70-71
77. Spira A.W., and Parkinson D. Effects of dark-rearing on the retinal dopaminergic system in the neonatal and postnatal guinea pig. Brain Res. Dev. Brain Res. 62 (1991) 142-145
78. Studer L., Spenger C., Seiler R.W., Altar C.A., Lindsay R.M., and Hyman C. Comparison of the effects of the neurotrophins on the morphological structure of dopaminergic neurons in cultures of rat substantia nigra. Eur. J. Neurosci. 7 (1995) 223-233
79. Suzuki A., Nomura S., Morii E., Fukuda Y., and Kosaka J. Localization of mRNAs for trkB isoforms and p75 in rat retinal ganglion cells. J. Neurosci. Res. 54 (1998) 27-37
80. Tinjust D., Kergoat H., and Lovasik J.V. Neuroretinal function during mild systemic hypoxia. Aviat. Space Environ. Med. 73 (2002) 1189-1194
81. Turner B.A., Sparrow J., Cai B., Monroe J., Mikawa T., and Hempstead B.L. TrkB/BDNF signaling regulates photoreceptor progenitor cell fate decisions. Dev. Biol 299 (2006) 455-465
82. Ugolini G., Cremisi F., and Maffei L. TrkA, TrkB and p75 mRNA expression is developmentally regulated in the rat retina. Brain Res. 704 (1995) 121-124
83. Wachtmeister L. Oscillatory potentials in the retina: what do they reveal. Prog. Retin. Eye Res. 17 (1998) 485-521
84. Wahlin K.J., Campochiaro P.A., Zack D.J., and Adler R. Neurotrophic factors cause activation of intracellular signaling pathways in Muller cells and other cells of the inner retina, but not photoreceptors. Invest. Ophthalmol. Vis. Sci. 41 (2000) 927-936
85. Wahlin K.J., Lim L., Grice E.A., Campochiaro P.A., Zack D.J., and Adler R. A method for analysis of gene expression in isolated mouse photoreceptor and Muller cells. Mol. Vis. 10 (2004) 366-375
86. Widmer H.R., and Hefti F. Stimulation of GABAergic neuron differentiation by NT-4/5 in cultures of rat cerebral cortex. Brain Res. Dev. Brain Res. 80 (1994) 279-284
87. Witkovsky P. Dopamine and retinal function. Doc. Ophthalmol. 108 (2004) 17-40
88. Witkovsky P., Veisenberger E., Haycock J.W., Akopian A., Garcia-Espana A., and Meller E. Activity-dependent phosphorylation of tyrosine hydroxylase in dopaminergic neurons of the rat retina. J. Neurosci. 24 (2004) 4242-4249
89. Witkovsky P., Arango-Gonzalez B., Haycock J.W., and Kohler K. Rat retinal dopaminergic neurons: differential maturation of somatodendritic and axonal compartments. J. Comp. Neurol. 481 (2005) 352-362
90. Xu B., Zang K., Ruff N.L., Zhang Y.A., McConnell S.K., Stryker M.P., and Reichardt L.F. Cortical degeneration in the absence of neurotrophin signaling: dendritic retraction and neuronal loss after removal of the receptor TrkB. Neuron 26 (2000) 233-245