Provision of brain-derived neurotrophic factor via anterograde transport from the eye preserves the physiological responses of axotomized geniculate neurons

Journal of Neuroscience

Volumn 23, Issue 1, 2003, Pages 287-296

  Caleo, Matteo ^a,b   Medini, Paolo ^b   Von Bartheld, Christopher S ^c   Maffei, Lamberto ^a,b  

^a CNR   (Italy)

^b SCUOLA NORMALE SUPERIORE   (Italy)

^c UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

Anterograde transport; BDNF; Functional sparing; Lateral geniculate nucleus; Neuronal death; Retrograde degeneration

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CELL COUNT; CELL FUNCTION; CONTROLLED STUDY; EYE; IN VIVO STUDY; LATENT PERIOD; LATERAL GENICULATE BODY; MICROELECTRODE; NERVE CELL; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NERVE FIBER TRANSECTION; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SIGNAL NOISE RATIO; VISUAL ACUITY; VISUAL CORTEX;

EID: 0037223340     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-01-00287.2003     Document Type: Article

References (60)

1. Agarwala S, Kalil RE (1998) Axotomy-induced neuronal death and reactive astrogliosis in the lateral geniculate nucleus following a lesion of the visual cortex in the rat. J Comp Neurol 392:252-263.
2. Al-Abdulla NA, Portera-Cailliau C, Martin LJ (1998) Occipital cortex ablation in adult rat causes retrograde neuronal death in the lateral geniculate nucleus that resembles apoptosis. Neuroscience 86:191-209.
3. Blesch A, Grill RJ, Tuszynski MH (1998) Neurotrophin gene therapy in CNS models of trauma and degeneration. Prog Brain Res 117:473-484.
4. Butowt R, von Bartheld CS (2001) Sorting of internalized neurotrophins into an endocytic transcytosis pathway via the Golgi system: Ultrastructural analysis in retinal ganglion cells. J Neurosci 21:8915-8930.
5. Caleo M, Menna E, Chierzi S, Cenni MC, Maffei L (2000) Brain-derived neurotrophic factor is an anterograde survival factor in the rat visual system. Curr Biol 10:1155-1161.
6. Caleo M, Cenni MC, Costa M, Menna E, Zentilin L, Giadrossi S, Giacca M, Maffei L (2002) Expression of BCL-2 via adeno-associated virus vectors rescues thalamic neurons after visual cortex lesion in the adult rat. Eur J Neurosci 15:1271-1277.
7. Chen H, Weber AJ (2001) BDNF enhances retinal ganglion cell survival in cats with optic nerve damage. Invest Ophthalmol Vis Sci 42:966-974.
8. Cheng L, Sapieha P, Kittlerova P, Hauswirth WW, Di Polo A (2002) TrkB gene transfer protects retinal ganglion cells from axotomy-induced death in vivo. J Neurosci 22:3977-3986.
9. Clark RS, Kochanek PM, Watkins SC, Chen M, Dixon CE, Seidberg NA, Melick J, Loeffert JE, Nathaniel PD, Jin KL, Graham SH (2000) Caspase-3 mediated neuronal death after traumatic brain injury in rats. J Neurochem 74:740-753.
10. Coggeshall RE, Lekan HA (1996) Methods for determining numbers of cells and synapses: A case for more uniform standards of review. J Comp Neurol 364:6-15.
11. Cooper JD, Salehi A, Delcroix JD, Howe CL, Belichenko PV, Chua-Couzens J, Kilbridge JF, Carlson EJ, Epstein CJ, Mobley WC (2001) Failed retrograde transport of NGF in a mouse model of Down's syndrome: Reversal of cholinergic neurodegenerative phenotypes following NGF infusion. Proc Natl Acad Sci USA 98:10439-10444.
12. Cowey A, Stoerig P, Williams C (1999) Variance in transneuronal retrograde ganglion cell degeneration in monkeys after removal of striate cortex: Effects of size of the cortical lesion. Vision Res 39:3642-3652.
13. Dumas TC, Sapolsky RM (2001) Gene therapy against neurological insults: Sparing neurons versus sparing function. Trends Neurosci 24:695-700.
14. Fagiolini M, Pizzorusso T, Porciatti V, Cenni M, Maffei L (1997) Transplant of Schwann cells allows normal development of the visual cortex of dark-reared rats. Eur J Neurosci 9:102-112.
15. 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.
16. Fukuda Y, Sumitomo I, Sugitani M, Iwama K (1979) Receptive-field properties of cells in the dorsal part of the albino rat's lateral geniculate nucleus. Jpn J Physiol 29:283-307.
17. Gundersen HJ, Jensen B (1987) The efficiency of systematic sampling and its prediction. J Microsc 147:229-263.
18. Hale PT, Sefton AJ, Dreher B (1979) A correlation of receptive field properties with conduction velocity of cells in the rat's retino-geniculo-cortical pathway. Exp Brain Res 35:425-442.
19. Hammond EN, Tetzlaff W, Mestres P, Giehl KM (1999) BDNF, but not NT-3, promotes long-term survival of axotomized adult rat corticospinal neurons in vivo. NeuroReport 10:2671-2675.
20. Hanover JL, Huang ZJ, Tonegawa S, Stryker MP (1999) Brain-derived neurotrophic factor overexpression induces precocious critical period in mouse visual cortex. J Neurosci 19:RC40(1-5).
21. Hefti F (1986) Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. J Neurosci 6:2155-2162.
22. Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF, Maffei L, Tonegawa S (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98:739-755.
23. Kafitz KW, Rose CR, Thoenen H, Konnerth A (1999) Neurotrophin-evoked rapid excitation through TrkB receptors. Nature 401:918-921.
24. Kaplan DR, Miller FD (2000) Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 10:381-391.
25. Klocker N, Cellerino A, Bahr M (1998) Free radical scavenging and inhibition of nitric oxide synthase potentiates the neurotrophic effects of brain-derived neurotrophic factor on axotomized retinal ganglion cells in vivo. J Neurosci 18:1038-1046.
26. Knusel B, Gao H, Okazaki T, Yoshida T, Mori N, Hefti F, Kaplan DR (1997) Ligand-induced down-regulation of Trk messenger RNA, protein and tyrosine phosphorylation in rat cortical neurons. Neuroscience 78:851-862.
27. Kordower JH, Isacson O, Leventhal L, Emerich DF (2000) Cellular delivery oftrophic factors for the treatment of Huntington's disease: Is neuroprotection possible? Prog Brain Res 127:414-430.
28. Lennie P, Perry VH (1981) Spatial contrast sensitivity of cells in the lateral geniculate nucleus of the rat. J Physiol (Lond) 315:69-79.
29. Lewin GR, Barde YA (1996) Physiology of the neurotrophins. Annu Rev Neurosci 19:289-317.
30. Lodovichi C, Berardi N, Pizzorusso T, Maffei L (2000) Effects of neurotrophins on cortical plasticity: Same or different? J Neurosci 20:2155-2165.
31. Mansour-Robaey S, Clarke DB, Wang YC, 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 USA 91:1632-1636.
32. Marrocco RT, McClurkin JSV, Alkire MT (1996) The influence of the visual cortex on the spatiotemporal response properties of lateral geniculate nucleus cells. Brain Res 737:110-118.
33. Martin LJ, Kaiser A, Yu JW, Natale JE, Al-Abdulla NA (2001) Injury-induced apoptosis of neurons in adult brain is mediated by p53-dependent and p53-independent pathways and requires Bax. J Comp Neurol 433:299-311.
34. McLaughlin J, Roozendaal B, Dumas T, Gupta A, Ajilore O, Hsieh J, Ho D, Lawrence M, McGaugh JL, Sapolsky R (2000) Sparing of neuronal function postseizure with gene therapy. Proc Natl Acad Sci USA 97:12804-12809.
35. Meyer-Franke A, Wilkinson GA, Kruttgen A, Hu M, Munro E, Hanson Jr MG, Reichardt LF, Barres BA (1998) Depolarization and cAMP elevation rapidly recruit TrkB to the plasma membrane of CNS neurons. Neuron 21:681-693.
36. Molotchnikoff S, Tremblay F, Lepore F (1984) The role of the visual cortex in response properties of lateral geniculate cells in rats. Exp Brain Res 53:223-232.
37. Montero VM, Brugge JF, Beitel RE (1968) Relation of the visual field to the lateral geniculate body of the albino rat. J Neurophysiol 31:221-236.
38. Morse JK, Wiegand SJ, Anderson K, You Y, Cai N, Carnahan J, Miller J, DiStefano PS, Altar CA, Lindsay RM, Alderson RF (1993) Brain-derived neurotrophic factor (BDNF) prevents the degeneration of medial septal cholinergic neurons following fimbria transection. J Neurosci 13:4146-4156.
39. Mufson EJ, Kroin JS, Sendera TJ, Sobreviela T (1999) Distribution and retrograde transport of trophic factors in the central nervous system: Functional implications for the treatment of neurodegenerative diseases. Prog Neurobiol 57:451-484.
40. Murphy PC, Sillito AM (1987) Corticofugal feedback influences the generation of length tuning in the visual pathway. Nature 329:727-729.
41. Patapoutian A, Reichardt LF (2001) Trk receptors: Mediators of neurotrophin action. Curr Opin Neurobiol 11:272-280.
42. Perry VH, Cowey A (1979) The effects of unilateral cortical and tectal lesions on retinal ganglion cells in rats. Exp Brain Res 35:85-95.
43. Pizzorusso T, Fagiolini M, Porciatti V, Maffei L (1997) Temporal aspects of contrast visual evoked potentials in the pigmented rat: Effect of dark rearing. Vision Res 37:389-395.
44. Porciatti V, Pizzorusso T, Maffei L (1999) The visual physiology of the wild type mouse determined with pattern VEPs. Vision Res 39:3071-3081.
45. Porciatti V, Bonanni P, Fiorentini A, Guerrini R (2000) Lack of cortical contrast gain control in human photosensitive epilepsy. Nat Neurosci 3:259-263.
46. Reese BE, Jeffery G (1983) Crossed and uncrossed visual topography in dorsal lateral geniculate nucleus of the pigmented rat. J Neurophysiol 49:877-885.
47. Riddle DR, Lo DC, Katz LC (1995) NT-4 mediated rescue of lateral geniculate neurons from effects of monocular deprivation. Nature 378:189-191.
48. Rivadulla C, Martinez LM, Varela C, Cudeiro J (2002) Completing the corticofugal loop: A visual role for the corticogeniculate type 1 metabotropic glutamate receptor. J Neurosci 22:2956-2962.
49. Sefton AJ, Dreher B (1995) Visual system. In: The Rat Nervous System (Paxinos G, ed), pp 833-898. New York: Academic.
50. Shen S, Wiemelt AP, McMorris FA, Barres BA (1999) Retinal ganglion cells lose trophic responsiveness after axotomy. Neuron 23:285-295.
51. Sommerfeld MT, Schweigreiter R, Barde YA, Hoppe E (2000) Down-regulation of the neurotrophin receptor TrkB following ligand binding. Evidence for an involvement of the proteasome and differential regulation of TrkA and TrkB. J Biol Chem 275:8982-8990.
52. Spalding KL, Tan MM, Hendry IA, Harvey AR (2002) Anterograde transport and trophic actions of BDNF and NT-4/5 in the developing rat visual system. Mol Cell Neurosci 19:485-500.
53. Tuszynski MH, Roberts J, Senut MC, U HS, Gage FH (1996) Gene therapy in the adult primate brain: Intraparenchymal grafts of cells genetically modified to produce nerve growth factor prevent cholinergic neuronal degeneration. Gene Ther 3:305-314.
54. Vejsada R, Sagot Y, Kato AC (1994) BDNF-mediated rescue of axotomized motor neurones decreases with increasing dose. NeuroReport 5:1889-1892.
55. von Bartheld CS (2001) Tracing with radiolabeled neurotrophins. Methods Mol Biol 169:195-216.
56. von Bartheld CS, Byers MR, Williams R, Bothwell M (1996) Anterograde transport of neurotrophins and axodendritic transfer in the developing visual system. Nature 379:830-833.
57. von Bartheld CS, Wang X, Butowt R (2001) Anterograde axonal transport, transcytosis, and recycling of neurotrophic factors: The concept of trophic currencies in neural networks. Mol Neurobiol 24:1-28.
58. West MJ (1999) Stereological methods for estimating the total number of neurons and synapses: Issues of precision and bias. Trends Neurosci 22:51-61.
59. Williams LR, Varon S, Peterson GM, Wictorin K, Fischer W, Bjorklund A, Gage FH (1986) Continuous infusion of nerve growth factor prevents basal forebrain neuronal death after fimbria fornix transection. Proc Natl Acad Sci USA 83:9231-9235.
60. Zuccato C, Ciammola A, Rigamonti D, Leavitt BR, Goffredo D, Conti L, MacDonald ME, Friedlander RM, Silani V, Hayden MR, Timmusk T, Sipione S, Cattaneo E (2001) Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 293:493-498.