Induction of MAP1B phosphorylation in target-deprived afferent fibers after kainic acid lesion in the adult rat

Journal of Comparative Neurology

Volumn 396, Issue 2, 1998, Pages 193-210

  Soares, Sylvia ^a   Fischer, Itzhak ^b   Ravaille Veron, Michele ^a   Vincent, Jean Didier ^a   Nothias, Fatiha ^a,c  

^a Institut Alfred Fessard   (France)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c CNRS   (France)

Author keywords

Excitotoxicity; Microtubule associated protein; Neurodegeneration; Neuronal plasticity

Indexed keywords

BIOTIN; DEXTRAN; KAINIC ACID; MICROTUBULE ASSOCIATED PROTEIN 5; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; NERVE CELL LESION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RAT; SENSORY NERVE CELL; THALAMUS VENTRAL NUCLEUS;

AFFERENT PATHWAYS; ANIMALS; AXONS; CELL COUNT; FEMALE; FETAL TISSUE TRANSPLANTATION; IMMUNOHISTOCHEMISTRY; KAINIC ACID; MICROTUBULE-ASSOCIATED PROTEINS; NERVE FIBERS; NEURONAL PLASTICITY; NEURONS; PHOSPHORYLATION; RATS; RATS, WISTAR; RNA, MESSENGER; THALAMUS;

EID: 0032578013     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980629)396:2<193::AID-CNE5>3.0.CO;2-W     Document Type: Article

References (58)

1. Aletta, J.M., S.A. Lewis, N.J. Cowan, and L.A. Greene (1988) Nerve growth factor regulates both the phosphorylation, and steady-state levels of microtubule-associated protein 1.2 (MAP1.2). J. Cell Biol. 106:1573-1581.
2. Ben-Ari, Y. and A. Represa (1990) Brief seizure episodes induce long-term potentiation and mossy fibre sprouting in the hippocampus. TINS. 13:312-318.
3. Black, M.M., T. Slaughter, and I. Fischer (1994) Microtubule-associated protein 1b (MAP1b) is concentrated in the distal region of growing axons. J. Neurosc. 14:857-870.
4. Bloom, G.S., F.C. Luca, and R.B. Valle (1985) Microtubule-associated protein 1B: Identification of a major component of neuronal cytoskeleton. Proc, Natl. Acad. Sci. USA 82:5404-5408.
5. Boyne, L.J., K. Martin, S. Hockfield, and I. Fischer (1995) Expression and distribution of phosphorylated MAP1B in growing axons of cultured hippocampal neurons. J. Neurosci. Res. 40:439-450.
6. Brugg, B. and A. Matus (1988) PC12 cells express juvenile microtubule-associated proteins during nerve growth factor-induced neurite outgrowth. J. Cell Biol. 107: 643-650.
7. Brugg, B., D. Reddy, and A. Matus (1993) Attenuation of microtubule-associated protein 1B expression by antisense oligodeoxynucleotides inhibits initiation of neunte outgrowth. Neuroscience 52:489-496.
8. Calvert, R. A., P. L. Woodhams, and B. H. Anderton (1987) Localization of an epitope of a microtubule associated protein 1x in outgrowing axons of the developing rat central nervous system. Neuroscience 23:131-141.
9. Coyle, J.T., M.E. Molliver, and M.J. Kuhar (1978) In situ injection of kainic acid: A new method for selectively lesioning neuronal cell bodies while sparing axons of passage. J. Comp. Neurol. 180:301-324.
10. De Waegh, S.M., V.M. Lee, and S.T. Brady (1992) Local modulation of neurofilament phosphorylation, axonal caliber, and slow axonal transport by myelinating Schwann cells. Cell. 68:451-463.
11. Diaz-Nido, J., E.M. Serrano, and J. Avila (1988) A casein kinase II-related activity is involved in phosphorylation of Microtubule-associated protein MAP1B during neuroblastoma cell differentiation. J. Cell Biol. 106:2057-2065.
12. Diaz-Nido, J., L. Ulloa, C. Sanchez, and J. Avila (1996) The role of the cytoskeleton in the morphological changes occurring during neuronal differentiation. Semin. Cell Dev. Biol. 7:733-739.
13. DiTella, M., F. Feiguin, N. Carri, K. Kosik, and A. Caceres (1996) MAP1b/ Tau functional redundancy during laminin-enhanced axonal growth. J. Cell Sci. 109:467-477.
14. Dusart, I., S. Marty, and M. Peschanski (1991) Glial changes following an excitotoxic lesion in the CNS-II: Astrocytes. Neuroscience 45:541-549.
15. Dusart, I., S. Marty, and M. Peschanski (1992) Demyelination, and remyelination by Schwann cells and oligodendrocytes after kainate-induced neuronal depletion in the central nervous system. Neuroscience 51:137-148.
16. Edelman W., M. Zervas, P. Costello, L. Loback, I. Fischer, A. Hammerback, N. Cowan, P. Davis, B. Wainer, and R. Kucherlapati (1996) Neuronal abnormalities in microtubule-associated protein 1B mutant mice. Proc. Natl. Acad. Sci. USA 93:1270-1275.
17. Fischer, I. and G. Romano-Clarke (1990) Changes in microtubule-associated protein MAP1B phosphorylation during rat brain development. J. Neurochem. 55: 328-333.
18. Gordon-Weeks, P.R. (1996) MAPs in growth cones. In Brain Microtubule Associated Proteins: Modifications in Alzheimer's Disease. Switzerland: Harwood Academic Publishers.
19. Gordon-Weeks, P.R., G.S. Mansfield, C. Alberto, M. Johnstone, and F. Moya (1993) A phosphorylation epitope on MAP1B that is transiently expressed in growing axons in the developing rat nervous system. Eur. J. Neurosci. 5:1302-1311.
20. Hatton, G.I. (1990) Emerging concept of structure-function dynamics in adult brain: The hypothalamoneurohypophysial system. Prog. Neurobiol. 34:437-504.
21. Hirokawa, N. (1994) Microtubule organization and dynamics dependent on microtubule-associated proteins. Curr. Biol. 6:74-81.
22. Keating, H.H. and D.J. Asai (1994) Distribution of phosphorylated microtubule-associated protein 1B during neurite outgrowth in PC12 Cells. Dev. Biol. 162:143-153.
23. Kirkpatrick, L.L. and S.T. Brady (1994) Modulation of the axonal microtubule cytoskeleton by myelinating Schwann cells. J. Neurosci. 14:7400-7450.
24. Letourneau, P.C (1996) The cytoskeleton in nerve growth cone mobility and axonal pathfinding. Perspect. Dev. Neurobiol. 4:111-123.
25. Ludin, B. and A. Matus (1993) The neuronal cytoskeleton and its role in axonal and dendritic plasticity. Hippocampus 3:61-72.
26. Liu, D. and I. Fischer (1996) Two promoters direct neuron-specific expression of the rat microtubule-associated protein 1B gene. J. Neurosci. 16:5026-5036.
27. Ma, D., F. Nothias, L.J. Boyne, and I. Fischer (1997) Differential regulation of MAP1B in rat CNS and PNS during development. J. Neurosci. Res. 49:319-332.
28. Mandell, J.W. and G.A. Banker (1996) Microtubule-associated proteins, phosphorylation gradients, and the establishment of neuronal polarity. Perspect. Dev. Neurobiol. 4:125-135.
29. Marty, S. and M. Peschanski (1994) Fine structural alteration in target-deprived axonal terminals in the rat thalamus. Neuroscience 62:1121-1132.
30. Marty, S. and M. Peschanski (1995) Effect of target deprivation on the morphology and survival of adult dorsal column nuclei neurons. J. Comp. Neurol. 356:523-536.
31. Marty, S., I. Dusart, and M. Peschanski (1991) Glial changes following an excitotoxic lesion in the CNS-I: Microglia/macrophages. Neuroscience 45:529-539.
32. Marty, S., J.M. Weinitz, and M. Peschanski (1994) Target dependence of adult neurons: Pattern of terminal arborizations. J. Neurosci. 14:5257-5266.
33. Mattson, M.P., M. Murain, and P.B. Guthrie (1990) Localized calcium influx orients axon formation in embryonic hippocampal pyramidal neurons. Dev. Brain Res. 52:201-204.
34. Matus, A. (1991) Microtubule-associated proteins morphogenesis. J. Cell Sci. 15:61-67.
35. Nothias, F. and M. Peschanski (1990) Homotypic fetal transplants into an experimental model of spinal cord neurodegeneration. J. Comp. Neurol. 301:520-534.
36. Nothias, F., B. Onteniente, F. Roudier, and M. Peschanski (1988a) Immunocytochemical study of serotoninergic and noradrenergic innervation of the ventrobasal complex of the rat thalamus. Neurosc. Lett. 95:59-63.
37. Nothias, F., K. Wictorin, O. Isacson, A. Bjorklund, and M. Peschanski (1988b) Morphological alteration of thalamic afferents in the excitotoxically lesioned striatum. Brain Res. 461:349-354.
38. Nothias, F., B. Onteniente, M. Geffard, and M. Peschanski (1990) Dissimilar responses of adult thalamic monoaminergic and somatosensory afferent fibers to implantation of thalamic fetal cells. Neuroscience 37:353-366.
39. Nothias, F., A. Tessler, and M. Murray (1993) Restoration of substance P and calcitonin gene-related peptide in dorsal root ganglia and dorsal horn after neonatal sciatic nerve lesion. J. Comp. Neurol. 334:370-384.
40. Nothias, F., I. Fischer, M. Murray, S. Mirman, and J.-D. Vincent (1996) Expression of a phosphorylated isoform of MAP1B is maintained in adult central nervous system areas that retain capacity for structural plasticity. J. Comp. Neurol. 368:317-334.
41. Nothias, F., P. Vernier, Y.V. Boxberg, S. Mirman, and J.-D. Vincent (1997) Modulation of NCAM polysialylation is associated with morphofunctional modifications in the hypothalamoneurohypophysial system during lactation. Eur. J. Neurosci. 9:1553-1565.
42. Nunez, J. and I. Fischer (1997) Microtubule-associated proteins (MAPs) in the peripheral nervous system during development and regeneration. J. Mol. Neurosci. 8:207-222.
43. Paxinos, G. and C. Watson (1986) The Rat Brain in Stereotaxic Coordinates. London: Academic Press.
44. Peschanski, M. and J.-M. Besson (1987) Structural alteration and possible growth of afferents after kainate lesion in the adult thalamus. J. Comp. Neurol. 258:185-203.
45. Piginio, G., G. Paglini, L. Ulloa, J. Avila, and A. Caceres (1997) Analysis of the expression, distribution and function of cyclin dependent kinase 5 (cdk5) in developing cerebellar macroneurons. J. Cell Sci. 110:257-270.
46. Rajakumar, N., K. Elisevich, and B.A. Flumerfelt (1993) Biotinylated dextran: A versatile anterograde and retrograde neuronal tracer. Brain Res. 607:47-53.
47. Riederer, B.M., R. Cohen, and A. Matus (1986) MAP5: A novel brain microtubule-associated protein under strong developmental regulation. J. Neurocytol. 15:763-775.
48. Rossi, F., T. Borsello, E. Vaudano, and P. Strata (1993) Regressive modifications of climbing fibers following Purkinje cell degeneration in the cerebellar cortex of the adult rat. Neuroscience 53:759-778.
49. Safaei, R. and I. Fischer (1989) Cloning of a cDNA encoding MAP1B in rat brain: Regulation of mRNA levels during development. J. Neurochem. 52:1871-1879.
50. Sato-Yoshitake, R., Y. Shiomura, H. Miyasaka, and N. Hirokawa (1989) Microtubule-associated protein 1B: Molecular structure, localization, and phosphorylation-dependent expression in developing neurons. Neuron 3:229-238.
51. Schoenfeld, T.A. and R.A. Obar (1994) Diverse distribution and function of fibrous microtubule-associated proteins in the nervous system. Int. Rev. Cytol. 151:67-137.
52. Takei, Y., S. Kondu, A. Harada, S. Inomata, T. Noda, and N. Hirokawa (1997) Delayed development of nervous system in mice homozygous for disrupted microtubule-associated protein 1B (MAP1B) gene. J. Cell Biol. 137:1615-1626.
53. Tanaka, E. and J. Sabry (1995) Making the connection: Cytoskeletal rearrangements during growth cone guidances. Cell. 83:171-176.
54. Theodosis, D.T., D.A. Poulain, and J.-D. Vincent (1981) Possible morphological bases for synchronisation of neuronal firing in the rat supraoptic nucleus during lactation. Neuroscience 6:919-929.
55. Tucker, R.P., C.C. Garner, and A. Matus (1989) In situ localization of microtubule-associated protein mRNA in the developing and adult rat brain. Neuron 2:1245-1256.
56. Ulloa, L., V. Dombradi, J. Diaz-Nido, K. Szucs, P. Gergely, P. Friedrich, and J. Avila (1993a) Dephosphorylation of distinct sites on microtubule-associated protein MAP1B by protein phosphatases 1, 2A and 2B. FEBS. 1:85-89.
57. Ulloa, L., J. Avila, and J. Diaz-Nido (1993b) Heterogeneity in the phosphorylation of microtubule-associated protein MAP1B during rat brain development. J. Neurochem. 61:961-972.
58. Viereck, C., R.P. Tucker, and A. Matus (1989) The adult rat olfactory system expresses microtubule-associated proteins. Int. Rev. Cytol. 124:217-273.