BDNF and NT4/5 promote survival and neurite outgrowth of pontocerebellar mossy fiber neurons

Journal of Neurobiology

Volumn 40, Issue 2, 1999, Pages 254-269

  Rabacchi, Sylvia A ^a,e   Kruk, Barbara ^a   Hamilton, Jason ^a   Carney, Catrina ^b   Hoffman, John R ^b   Meyer, Sheryl L ^c   Springer, Joe E ^d   Baird, Douglas H ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b BEAVER COLLEGE   (United States)

^c CEPHALON INC   (United States)

^d UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

^e Columbia University ^*  (United States)

Author keywords

Basilar pontine nuclei; Cerebellum; Development; Growth cones; Mossy fibers; Neurotrophins

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; NEUROTROPHIN 3; NEUROTROPHIN 4;

ANIMAL CELL; ARTICLE; IN SITU HYBRIDIZATION; MOSSY FIBER; MOUSE; NERVE CELL CULTURE; NERVE CELL GROWTH; NERVE FIBER GROWTH; NEURITE; NONHUMAN; PONS; PRIORITY JOURNAL; RAT; SYNAPTOGENESIS;

AFFERENT PATHWAYS; ANIMALS; AXONS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL SURVIVAL; IN SITU HYBRIDIZATION; MICE; MICE, INBRED C57BL; NERVE FIBERS; NERVE GROWTH FACTORS; NEURITES; NEURONS; PONS; RATS; RECEPTOR, CILIARY NEUROTROPHIC FACTOR; RECEPTOR, TRKC; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER;

EID: 0032837297     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199908)40:2<254::AID-NEU11>3.0.CO;2-4     Document Type: Article

References (83)

1. Acheson A, Conoyar JC, Fandl JP, De Chiari TM, Russel M, Thadani A, Squinto SP, Yancopoulos GD, Lindsay RM. 1995. A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature 374:450-453.
2. Altman J. 1972. Postnatal development of the cerebellar cortex in the rat. III. Maturation of the components of the granule layer. J Comp Neurol 145:465-514.
3. Altman J, Bayer SA. 1978. Prenatal development of the cerebellar system in the rat. II. Cytogenesis and histogenesis of the inferior olive, pontine gray, and the precerebellar reticular nuclei. J Comp Neurol 179:49-76.
4. Altman J, Bayer SA. 1996. Development of the cerebellar system: in relation to its evolution, structure and functions. New York: CRC Press, pp. 106;470-477.
5. Ashwell KWS, Zhang LL. 1992. Ontogeny of afferents to the fetal rat cerebellum. Acta Anat 145:17-23.
6. Baird DH, Baptista CA, Wang LC, Mason CA. 1992a. Specificity of a target-derived stop signal for afferent axonal growth. J Neurobiol 23:579-591.
7. Baird DH, Hatten ME, Mason CA. 1992b. Cerebellar target neurons provide a stop-signal for afferent neurite extension. J Neurosci 12:619-634.
8. Baird DH, Kruk B. 1994. Arrest of axonal growth in vitro by living, sectioned or fixed target neurons. Soc Neurosci Abstr 20:1282.
9. Baird DH, Trenkner E, Mason CA. 1996. Arrest of afferent axon extension by target neurons in vitro is regulated by the NMDA receptor. J Neurosci 16:2642-2648.
10. Baynard MD, Rabacchi SA, Carney C, Hoffman JR, Kruk B, Baird DH. 1997. BDNF regulates cerebellar mossy fiber extension and fasciculation. Soc Neurosci Abstr 23:136.9.
11. Berkemeier LR, Winslow JW, Kaplan DR, Nikolics K, Goeddel DV, Rosenthal A. 1991. Neurotrophin-5: a novel neurotrophic factor that activates trk and trkB. Neuron 7:857-866.
12. Boyne L, Martin K, Hockfield S, Fischer I. 1995. Expression and distribution of phosphorylated MAP1B in growing axons of cultured hippocampal neurons. J Neurosci Res 40:439-450.
13. Brodal P, Bjaalie JG. 1992. Organization of the pontine nuclei. Neurosci Res 13:83-118.
14. Brodal P, Mihailoff G, Border B, Ottersen OP, Storm-Mathisen J. 1988. GABA-containing neurons in the pontine nuclei of the rat, cat and monkey: an immunocytochemical study. Neuroscience 235:27-45.
15. Cabelli RJ, Hohn A, Shatz CJ. 1995. Inhibition of ocular dominance column formation by infusion of NT4/5 or BDNF. Science 267:1662-1665.
16. Carter BD, Zirrgiebel U, Barde Y-A. 1995. Differential regulation of p21 activation in neurons by nerve growth factor and brain-derived growth factor. J Biol Chem 270:21751-21757.
17. Causing CG, Gloster A, Aloyz R, Barmji SX, Chang E, Fawcett J, Kuchel G, Miller FD. 1997. Synaptic innervation density is regulated by neuron derived BDNF. Neuron 18:257-267.
18. Cohen-Cory S, Fraser SE. 1995. Effects of brain-derived neurotrophic factor on optic axons branching and remodelling in vivo. Nature 378:192-196.
19. Cooper MW, Smith SJ. 1992. A real-time analysis of growth cone-target cell interactions during the formation of stable contacts between hippocampal neurons in culture. J Neurobiol 23:814-828.
20. D'Angelo E, Rossi P, Armano S, Taglietti V. 1997. LTP of NMDA receptor-mediated transmission at the mossy fiber-granule cell synapse of rat cerebellum. Soc Neurosci Abstr 23:469.11.
21. Daniels RH, Hall PS, Bokoch GM. 1998. Membrane targeting of p21-activated kinase 1 (PAK1) induces neurite outgrowth from PC12 cells. EMBO J 17:754-764.
22. Davies AM. 1994. The role of neurotrophins in the developing nervous system. J Neurobiol 25:1334-1348.
23. Ernfors P, Bengzon J, Kokaia Z, Persson H, Lindvall O. 1991. Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis. Neuron 7:165-176.
24. Ernfors P, Merlio J-P, Persson H. 1992. Cells expressing mRNA for neurotrophins and their receptors during embryonic rat development. Eur J Neurosci 4:1140-1158.
25. Escandon E, Burton LE, Szonyi E, Nikolics K. 1993. Characterization of neurotrophin receptors by affinity crosslinking. J Neurosci Res 34:601-613.
26. Fandl JP, Tobkes NJ, McDonald NQ, Hendrickson WA, Ryan TE, Nigam S, Acheson A, Cudny H, Panayotatos N. 1994. Characterization and crystallization of recombinant human neurotrophin-4. J Biol Chem 269:755-759.
27. Farinas I, Wilkinson GA, Backus C, Reichardt LF, Patapoutian A. 1998. Characterization of neurotrophin and trk receptor functions in developing sensory ganglia: direct NT-3 activation of trkB neurons in vivo. Neuron 21:335-345.
28. Frank L, Ventimiglia R, Anderson K, Lindsay RM, Rudge JS. 1996. BDNF down-regulates neurotrophin responsiveness, trkB protein and trkB mRNA levels in cultured rat hippocampal neurons. Eur J Neurosci 8:1220-1230.
29. Friedman WJ, Black IB, Kaplan DR. 1998. Distribution of the neurotrophins brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin 4/5 in the post-natal rat brain: an immunohistochemical study. Neuroscience 84: 101-114.
30. Friedman WJ, Olson L, Persson H. 1991. Cells that express brain-derived neurotrophic factor mRNA in the developing post-natal rat brain. Eur J Neurosci 3:688-697.
31. Gall CM, Isakson PJ. 1989. Limbic seizures increase neuronal production of messenger RNA for nerve growth factor. Science 245:758-761.
32. Gallo G, Pollack ED. 1995. Cyclic remodelling of growth cone lamellae and the effect of target tissue. Dev Brain Res 85:140-145.
33. Gao W-Q, Zheng JL, Karihaloo M. 1995. Neurotrophin 4/5 (NT-4/5) and brain-derived neurotrophic factor (BDNF) act at later stages of cerebellar granule cell differentiation. J Neurosci 15:2656-2667.
34. Hamori J, Somogyi J. 1983. Differentiation of cerebellar mossy fiber synapses in the rat: a quantitative electron microscope study. J Comp Neurol 220:365-377.
35. Henderson CE. 1996. The role of neurotrophic factors in neuronal development. Curr Opin Neurobiol 6:64-70.
36. Hofer M, Pagliusi SR, Hohn A, Leibrock J, Barde Y-A. 1990. Regional distribution of brain derived neurotrophic factor mRNA in the adult mouse brain. EMBO J 9:2459-2464.
37. Ip NY, Ibanez CF, Nye SH, McClain J, Jones PF, Gies DR, Belluscio L, Le Beau MM, Espinosa R III, Squinto SP, et al. 1992. Mammalian neurotrophin-4: structure, chromosomal localization, tissue distribution, and receptor specificity. Proc Natl Acad Sci USA 89:3060-3064.
38. Ip NY, Li Y, Yancopoulos GD, Lindsay RM. 1993a. Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4, but not to NGF. J Neurosci 13:3394-3405.
39. Ip NY, Stitt TN, Tapley P, Klein R, Glass DJ, Fandl J, Greene LA, Barbacid M, Yancopoulos GD. 1993b. Similarities and differences in the way neurotrophins interact with the Trk receptors in neuronal and nonneuronal cells. Neuron 10:137-149.
40. Kennedy TE, Tessier-Lavigne M. 1995. Guidance and induction of branch formation in developing axons by target-derived diffusable factors. Curr Opin Neurobiol 5:83-90.
41. Klein R, Smeyne RJ, Wurst W, Long LK, Auerbach BA, Joyner AL, Barbacid M. 1993. Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death. Cell 75:113-122.
42. Korte M, Carrol P, Wolf E, Brem G, Thoenen H, Bonhoeffer T. 1995. Hippocampal long term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci USA 92:8856-8860.
43. Korte M, Staiger V, Griesbeck O, Thoenen H, Bonhoeffer T. 1996. The involvement of brain-derived neurotrophic factor in hippocampal long-term potentiation revealed by gene targeting experiments. J Physiol Paris 90:157-164.
44. Lindholm D, Carrol P, Tzimagiogis G, Thoenen H. 1996. Autocrine-paracrine regulation of hippocampal neuron survival by IGF-1 and the neurotrophins BDNF, NT3 and NT4. Eur J Neurosci 8:1452-1460.
45. Lindholm D, Dechant G, Heisenberg CP, Thoenen H. 1993. Brain-derived neurotrophic factor is a survival factor for cultured rat cerebellar granule neurons and protects them against glutamate-induced neurotoxicity. Eur J Neurosci 5:1455-1464.
46. Lindholm D, Hamner S, Zirrgiebel U. 1997. Neurotrophins and cerebellar development. Persp Dev Neurobiol. The cerebellum: a model for construction of a cortex. 5:83-94.
47. Lo DC. 1995. Neurotrophic factors and synaptic plasticity. Neuron 15:979-981.
48. Lu B, Buck CR, Dreyfus CF, Black IB. 1989. Expression of NGF and NGF receptor mRNA in the developing brain: evidence for local delivery and action of NGF. Exp Neurol 104:191-199.
49. Luo L, Jan LY, Jan Y-N. 1997. Rho family small GTP-binding proteins in growth cone signalling. Curr Opin Neurobiol 7:81-86.
50. Maisonpierre PC, Belluscio L, Friedman B, Alderson RF, Wiegand SJ, Furth ME, Lindsay RM, Yancopoulos GD. 1990. NT3, BDNF and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron 5:501-509.
51. Marsh L, Letourneau PC. 1984. Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B. J Cell Biol 99:2041-2047.
52. Mason CA, Morrison ME, Ward MS, Zhang Q, Baird DH. 1997. Axon-target interactions in the developing cerebellum. Persp Dev Neurobiol. 5:69-82.
53. Merlio JP, Ernfors P, Jaber M, Persson H. 1992. Molecular cloning of rat trkC and distribution of cells expressing messenger RNAs for members of the trk family in the rat central nervous system. Neuroscience 51:3:513-532.
54. Meyer SL, Lang DM, Forbes ME, Knight E Jr, Hirsch JD, Trusko SP, Scott RW. 1994. Production and characterization of recombinant mouse brain-derived neurotrophic factor and rat neurotrophin-3 expressed in insect cells. J Neurochem 62:825-833.
55. Mihailoff GA. 1993. Cerebellar nuclear projections from the basilar pontine nuclei and nucleus reticularis tegmenti pontis as demonstrated with PHA-L tracing in the rat. J Comp Neurol 330:130-146.
56. Mihailoff GA, McArdle CB, Adams CE. 1981. The cytoarchitecture, cytology, and synaptic organization of the basilar pontine nuclei in the rat. I. Nissl and Golgi studies, J Comp Neurol 195:181-201.
57. Morrison ME, Mason CA. 1998. Granule neuron regulation of Purkinje cell development: striking a balance between neurotrophin and glutamate signaling. J Neurosci 18: 3563-3573.
58. Mulach WL, Pollack E. 1982. Target tissue control of nerve growth rate and periodicity in vitro. Dev Brain Res 4:361-364.
59. Muller Y, Duperray C, Caruso F, Clos J. 1994. Autocrine regulation of proliferation of cerebellar granule neurons by nerve growth factor. J Neurosci Res 38:41-55.
60. Nawa H, Carnahan J, Gall C. 1995. BDNF protein measured by a novel enzyme immunoassay in normal brain and after seizure: partial disagreement with mRNA levels. Eur J Neurosci 7:1527-1535.
61. Oppenheim RW. 1981. Studies in developmental neurobiology. New York: Oxford, p 74-133.
62. Palay SL, Chan Palay V. 1974. Cerebellar cortex: cytology and organization. New York: Springer Verlag, p 143.
63. Patterson SL, Abel T, Deuel TA, Martin KC, Rose JC, Kandel ER. 1996. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16:1137-1145.
64. Purves D. 1986. The trophic theory of neural connections. Trends Neurosci 9:486-489.
65. Rabacchi SA, Meyer SL, Baird DH, Springer JE. 1995. The neurotrophic actions of BDNF in the developing pontine-cerebellar system. Soc Neurosci Abstr 21:421.11.
66. Reichardt LF, Fariñas I. 1997. Neurotrophic factors and their receptors. In: Cowan WM, Jessel TM, Zipursky SL, editors. Molecular and cellular approaches to neural development. New York: Oxford University Press, p 220-263.
67. Riddle DR, Lo DC, Katz LC. 1995. NT-4-mediated rescue of lateral geniculate neurons from effects of monocular deprivation. Nature 378:189-191.
68. Rocamora N, Garcia-Ladona FJ, Palacios JM, Mengod G. 1993. Differential expression of brain-derived neurotrophic factor, neurotrophin 3, and low affinity nerve growth factor receptor during postnatal development of the rat cerebellar system. Mol Brain Res 17:1-8.
69. Schnell L, Schneider R, Kolbeck R, Barde Y-A, Schwab ME. 1994. Neurotrophin 3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367:170-173.
70. Schwartz PM, Borghesani PR, Levy RL, Pomeroy SL, Segal RA. 1997. Abnormal cerebellar development and foliation in BDNF -/-mice reveals a role for neurotrophins in CNS patterning. Neuron 19:269-281.
71. Segal RA, Pomeroy SL, Stiles CD. 1995. Axonal growth and fasciculation linked to differential expression of BDNF and NT3 receptors in developing cerebellar granule cells. J Neurosci 15:4970-4981.
72. Segal RA, Takahashi H, McKay RDG. 1992. Changes in neurotrophin responsiveness during the development of cerebellar granule neurons. Neuron 9:1041-1052.
73. Shatz CJ. 1997. Neurotrophins and visual system plasticity. In: Cowan WM, Jessel TM, Zipursky SL, editors. Molecular and cellular approaches to neural development. New York: Oxford University Press, p 509-524.
74. Shinoda Y, Sugiuchi Y, Futami T, Izawa R. 1992. Axon collaterals of mossy fibers from the pontine nucleus in the cerebellar dentate nucleus. J Neurophysiol 67:547-560.
75. Somasekhar T, Pollack ED. 1992. Morphological response of extending spinal neuritic growth cones to peripheral target tissue. J Comp Neurol 326:314-326.
76. Thoenen H. 1995. Neurotrophins and synaptic plasticity. Science 270:593-598.
77. Timmusk T, Belluardo N, Metsis M, Persson H. 1993. Widespread and developmentally regulated expression of neurotrophin 4 mRNA in rat brain and peripheral tissues. Eur J Neurosci 5:605-613.
78. von Bartheld CS, Byers MR, Williams R, Bothwell M. 1996. Anterograde transport of neurotrophins and dendritic transfer in the developing visual system. Nature 379:830-833.
79. White FA, Silos-Santiago I, Molliver DC, Nishimura M, Phillips H, Barbacid M, Snider WD. 1996. Synchronous onset of NGF and TrkA survival dependence in developing dorsal root ganglia. J Neurosci 16:4662-4672.
80. Widemer HR, Ohsawa F, Knusel B, Hefti F. 1993. Down-regulation of phosphatidyl response to BDNF and NT3 in cultures of cortical neurons. Brain Res 614:325-334.
81. Zafra F, Castren E, Thoenen H, Lindholm D. 1991. Interplay between glutamate and gamma-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in hippocampal neurons. Proc Natl Acad Sci USA 88:10037-10041.
82. Zafra F, Hengerer B, Leibrock J, Thoenen H, Lindholm D. 1990. Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J 9:3545-3550.
83. Zhang L, Schmidt RE, Van Q, Snider WD. 1994. NGF and NT-3 have differing effects on the growth of dorsal root axons in developing mammalian spinal cord. J Neurosci 14:5187-5201.