Brain-derived neurotrophic factor modulates GAP-43 but not Tα1 expression in injured retinal ganglion cells of adult rats

Journal of Neuroscience Research

Volumn 47, Issue 6, 1997, Pages 561-572

  Fournier, A E ^b   Beer, J ^c   Arregui, C O ^d   Essagian, C ^b   Aguayo, A J ^a   McKerracher, L ^b  

^a MONTREAL GENERAL HOSPITAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

axotomy; BDNF; regeneration; RGCs; tubulin

Indexed keywords

ALPHA TUBULIN; BRAIN DERIVED NEUROTROPHIC FACTOR; IODINE 125; MESSENGER RNA; NEUROMODULIN; NEUROTROPHIN;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DAMAGE; CELL GROWTH; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; NERVE FIBER TRANSECTION; NONHUMAN; OPTIC NERVE LESION; PRIORITY JOURNAL; RAT; RETINA GANGLION CELL;

ANIMALS; AUTORADIOGRAPHY; AXONAL TRANSPORT; BRAIN-DERIVED NEUROTROPHIC FACTOR; FEMALE; GAP-43 PROTEIN; IN SITU HYBRIDIZATION; IODINE RADIOISOTOPES; MEMBRANE GLYCOPROTEINS; NERVE TISSUE PROTEINS; NEUROFILAMENT PROTEINS; OPTIC NERVE; OPTIC NERVE INJURIES; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; REFERENCE VALUES; RETINAL GANGLION CELLS; RNA, MESSENGER; TRANSCRIPTION, GENETIC; TUBULIN;

EID: 0030888165     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19970315)47:6<561::AID-JNR1>3.0.CO;2-B     Document Type: Article

References (56)

1. Aigner L, Caroni P(1995): Absence of persistent spreading, branching, and adhesion in GAP-43 depleted growth cones. J Cell Biol 128:647-660.
2. Aigner L, Arber S, Kapfhammer JP, Laux T, Schneider C, Botteri F, Brenner H-R, Caroni P (1995): Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 83:269-278.
3. Barbacid M (1994): The Trk family of neurotrophin receptors. J Neurobiol 25:1386-1403.
4. Basi GS, Jacobson RD, Virag I, Schilling J, Skene JH (1987): Primary structure and transcriptional regulation of GAP-43, a protein associated with nerve growth. Cell 49:785-791.
5. Basi GS, Skene JHP (1988): Regulation of GAP-43 gene expression during axonal regeneration in sensory neurons. Soc Neurosci Abstr 14:408.
6. Benowitz LI, Lewis ER (1983): Increased transport of 44,000-to 49,000-dalton acidic proteins during regeneration of the goldfish optic nerve: A two-dimensional gel analysis. J Neurosci 3:2153-2163.
7. Benowitz LI, Schmidt JT (1987): Activity-dependent sharpening of the regenerating retinotectal projection in goldfish: Relationship to the expression of growth-associated proteins. Brain Res 417:118-126.
8. Berkelaar M, Clarke DB, Wang Y-C, Bray GM, and Aguayo AJ (1994): Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J Neurosci 14:4368.
9. Cohen A, Bray GM, Aguayo AJ (1994): Neurotrophin-4/5 (NT-4/5) increases adult rat retinal ganglion cell survival and neurite outgrowth in vitro. J Neurobiol 25:953-959.
10. Cohen-Cory S, Fraser SE (1995): Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378:192-196
11. Connolly SE, Hjelmeland LM, LaVail MM (1992): Immunohistochemical localization of basic fibroblast growth factor in mature and developing retinas of normal and RCS rats. Curr Eye Res 11:1005-1017.
12. Consigli SA, Lyser KM, Joseph-Silverstein J (1993): The temporal and spatial expression of basic fibroblast growth factor during ocular development in the chicken. Invest Ophth Visual Sci 34:559-566.
13. Curtis R, Scherer SS, Somogyi R, Adryan KM, Ip NY, Zhu Y, Lindsay RM, DiStefano PS (1994): Retrograde axonal transport of LIF is increased by peripheral nerve injury: correlation with increased LIF expression in distal nerve. Neuron 12:191-204.
14. Doster SK, Lozano AM, Aguayo AJ, Willard MB (1991): Expression of the growth-associated protein GAP-43 in adult rat retinal ganglion cells following axon injury. Neuron 6:635-647.
15. Federoff HJ, Grabczyk E, Fishman MC (1988): Dual regulation of GAP-43 gene expression by nerve growth factor and glucocorticoids. J Biol Chem 263:19290-19295.
16. Friedman WJ, Olson L, Persson H (1991): Cells that express BDNF mRNA in the developing postnatal brain. Eur J Neurosci 3:688-697.
17. Gloster A, Wu W, Speelman A, Weiss S, Causing C, Pozniak C, Reynolds B, Chang G, Toma JG, Miller FD (1994): The Tα1 α-tubulin promoter specified gene expression as a function of neuronal growth and regeneration in transgenic mice. J Neurosci 14:7319-7330.
18. Heumann R (1994): Neurotrophin signalling. Curr Opin Neurobiol 4:668-679.
19. Hu-Tsai M, Winter J, Emson PC, Woolf CJ (1994): Neurite outgrowth and GAP-43 mRNA expression in cultured adult rat dorsal root ganglion neurons: Effects of NGF or prior peripheral axotomy. J Neurosci Res 39:634-645.
20. Ip NY, Stitt TN, Tapley P, Klein R, Glass DJ, Fandl J, Greene LA, Barbacid M, Yancopoulos GD (1993): Similarities and differences in the way neurotrophins interact with the Trk receptors in neuronal and nonneuronal cells. Neuron 10:137-149.
21. JelsmaTN, Friedman HH, Berkelaar M, Bray GM, Aguayo AJ (1993): Different forms of the neurotrophin receptor trkB mRNA predominate in rat retina and optic nerve. J Neurobiol 24:1207-1214.
22. Johnson JE, Barde YA, Schwab M, Thoenen H (1986): Brain-derived neurotrophic factor supports the survival of cultured rat retinal ganglion cells. J Neurosci 6:3031-3038.
23. Kalil K, Skene JH (1986): Elevated synthesis of an axonally transported protein correlates with axon outgrowth in normal and injured pyramidal tracts. J Neurosci 6:2563-2570.
24. Kittlerova P, Playford DE, Bray GM, Aguayo AJ (1994): NT-3 enhances growth and upregulates GAP-43 in a subset of retinal ganglion cells after axotomy. Soc Neurosci Abstr 20:1098 (Abstract).
25. Li JY, Kling-Petersen A, Dahlstrom A (1992): Influence of spinal cord transection on the presence and axonal transport of CGRP-, chromogranin A-, VIP-, synapsin I-, and synaptophysin-like immunoreactivities in rat motor nerve. J Neurobiol 23:1094-1110.
26. Ma Y, Campenot RB, Miller FD (1992): Concentration-dependent regulation of neuronal gene expression by nerve growth factor. J Cell Biol 117:135-141.
27. Mansour-Robaey S, Clarke DB, Wang Y-C, Bray GM, Aguayo AJ (1994): 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 91:1632-1636.
28. Mearow KM, Kril Y (1995): Anti-NGF treatment blocks the upregulation of NGF receptor mRNA expression associated with collateral sprouting of rat dorsal root ganglion neurons. Neurosci Lett 184:55-58.
29. Meiri KF, Burdick D. (1991): Nerve growth factor stimulation of GAP-43 phosphorylation in intact isolated growth cones. J Neurosci 11:3155-3164.
30. Mey J. Thanos S (1993): Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo. Brain Res 602:304-317.
31. Miller FD, Naus CC, Higgins GA, Bloom FE, Milner RJ (1987a): Developmentally regulated rat brain mRNAs: Molecular and anatomical characterization. J Neurosci 7:2433-2444.
32. Miller FD, Naus CC, Durand M, Bloom FE, Milner RJ (1987b): Isotypes of alpha tubulin are differentially regulated during neuronal maturation. J Cell Biol 105:3065-3073.
33. Miller FD, Tetzlaff W, Bisby MA, Fawcett JW, Milner RJ (1989): Rapid induction of the major embryonic alpha-tubulin mRNA, T alpha 1, during nerve regeneration in adult rats. J Neurosci 9:1452-1463.
34. Mohiuddin L, Fernandez K, Tomlinson DR, Fernyhough P (1995): Nerve growth factor and neurotrophin-3 enhance neurite outgrowth and up-rcgulate the levels of messenger RNA for growth-associated protein GAP-43 and Tα1 α-tubulin in cultured adult rat sensory neurones. Neurosci Lett 185:20-23.
35. Nishizawa K (1994): NGF-induced stabilization of GAP-43 mRNA is mediated by both the 3' untranslated region and a segment encoding the carboxy-terminus peptide. Biochem Biophys Res Comm 200:789-796.
36. Okazawa H, Kamei M, Imafuku I, Kanazawa I (1994): Gene regulation of trkB and trkC in the chick retina by light/darkness exposure. Oncogene 9:1813-1818.
37. Patel MN, McNamara JO (1995): Selective enhancement of axonal branching of cultured dentate gyrus neurons by neurotrophic factors. Neuroscience 69:763-770.
38. Perry VH (1981): Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience 6:931-944.
39. Perry GW, Burmeister DW, Grafstein B (1990): Effect of target removal on goldfish optic nerve regeneration: Analysis of fast axonally transported proteins. J Neurosci 10:3439-3448.
40. Ren TA, Tetzlaff W, Ertlmaier A, Zwiers H (1993): Developmental study of the expression of B50/GAP-43 in rat retina. J Neurobiol 24:949-958.
41. Rentrop M, Knapp B, Winter W, Schweizer J (1986): Aminoalkylsilone-treated slides as support for in situ hybridization of keratin cDNAs to frozen tissue sections under varying fixation and pretreatment conditions. Histochem J 18:271-276.
42. Rodriguez-Tebar A, Jeffrey PL, Thoenen H, Barde YA (1989): The survival of chick retinal ganglion cells in response to BDNF depends on their embryonic age. Dev Biol 136:296-303.
43. Rodriguez-Tebar A, de la Rosa EJ, Arribas A (1993): Neurotrophin-3 receptors in the developing chicken retina. Eur J Biochem 211:789-794.
44. Rosenthal A, Goeddel DV, Nguyen T, Lewis M, Shih A, Laramee GR, Nikolics K, Winslow JW (1990): Primary structure and biological activity of a novel human neurotrophic factor. Neuron 4:767-773.
45. Sawai H, Clarke DB, Kittlerova P, Bray GM, Aguayo AJ (1996): Brain Derived Neurotrophic Factor and NT-4/5 stimulate the growth of axonal branches from regenerating retinal ganglion cells. J Neurosci 16:3887-3894.
46. Schaden H, Stuermer CAO, Bahr M (1994): GAP-43 immunoreactivity and axon regeneration in retinal ganglion cells of the rat. J Neurobiol 25:1570-1578.
47. Skene JH (1989): Axonal growth-associated proteins. Annu Rev Neurosci 12:127.
48. Skene JH, Willard M (1981a): Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems. J Cell Biol 89:96-103.
49. Skene JH, Willard M (1981b): Electrophoretic analysis of axonally transported proteins in toad retinal ganglion cells. J Neurochem 37:79-87.
50. Strittmatter SM, Fankhauser C, Huang PL, Mashimo H, Fishman MC (1995): Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell 80:445-452.
51. Thanos S, Bahr M, Barde YA, Vanselow J (1989): Survival and axonal elongation of adult rat retinal ganglion cells: In vitro effects of lesion sciatic nerve and brain derived neurotrophic factor. Eur J Neurosci 1:19-26.
52. Thanos S, von Boxberg Y (1989): Factors influencing regeneration of retinal ganglion cell axons in adult mammals. Met Br Dis 4:67-72.
53. Vaudano E, Campbell G, Anderson PN, Davies AP, Woolhead C, Schreyer DJ, Lieberman AR (1995): The effects of a lesion or a peripheral nerve graft on GAP-43 upregulation in the adult rat brain: An in situ hybridization and immunocytochemical study. J Neurosci 15:3594-3611.
54. Villegas-Perez MP, Vidal-Sanz M, Rasminsky M, Bray GM, Aguayo AJ (1993): Rapid and protracted phases of retinal ganglion cell loss follow axotomy in the optic nerve of adult rats. J Neurobiol 24:23-36.
55. Wu W, Mathew TC, Miller FD (1993): Evidence that the loss of homeostatic signals induces regeneration-associated alterations in neuronal gene expression. Dev Biol 158:456-466.
56. Zanellato A, Comelli MC, Dal Toso R, Carmignoto G (1993): Developing rat retinal ganglion cells express the functional NGF receptor p140trkA. Dev Biol 159:105-113.