Characterization and ontogeny of synapse-associated proteins in the developing facial and hypoglossal motor nuclei of the Brazilian opossum

Journal of Comparative Neurology

Volumn 368, Issue 2, 1996, Pages 270-284

  Swanson, Jack J ^a   Kuehl Kovarik, M Cathleen ^a   Wilson, Michael C ^b   Elmquist, Joel K ^c   Jacobson, Carol D ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

monodelphis; SNAP 25; synaptogenesis; synaptophysin; synaptotagmin

Indexed keywords

BRAIN PROTEIN; MEMBRANE PROTEIN; NEUROMODULIN; PHOSPHOPROTEIN; SYNAPTOPHYSIN; SYNAPTOTAGMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; FACIAL NERVE NUCLEUS; FEMALE; HYPOGLOSSAL NUCLEUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MOTONEURON NUCLEUS; NONHUMAN; ONTOGENY; OPOSSUM; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SYNAPTOGENESIS;

ANIMALS; FACIAL NERVE; HYPOGLOSSAL NERVE; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; MOTOR NEURONS; NERVE TISSUE PROTEINS; OPOSSUMS; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25;

EID: 0030006058     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960429)368:2<270::AID-CNE7>3.0.CO;2-0     Document Type: Article

References (61)

1. Altman, J., and S.A. Bayer (1982) Development of the cranial nerve ganglia and related nuclei in the rat. Adv. Anat. Embryol. Cell Biol. 74.
2. Altman, J., and S.A. Bayer (1995a) Neurogenesis and neuronal migration. In G. Paxinos (ed): The Rat Nervous System. San Diego: Academic Press, pp. 1041-1078.
3. Altman, J., and S.A. Bayer (1995b) Principles of neurogenesis, neuronal migration, and neural circuit formation. In G. Paxinos (ed): The Rat Nervous System. San Diego: Academic Press, pp. 1079-1098.
4. Altman, J., and S.A. Bayer (1995c) Atlas of Prenatal Rat Brain Development. Ann Arbor MI: CRC Press.
5. Ashwell, K.W., and C.R.R. Watson (1983) The development of facial motoneurons in the mouse - Neuronal death and the innervation of facial muscles. J. Embryol. Exp.Morphol. 77:117-141.
6. Bark, I.C. (1993) Structure of the chicken gene for SNAP-25 reveals duplicate exons encoding distinct isoforms of the protein. J. Mol. Biol. 233:67-76.
7. Bark, I.C., and M.C. Wilson (1994) Regulated vesicular fusion in neurons: Snapping together the details. Proc. Natl. Acad. Sci. USA 91:4621-4624.
8. Binder, L.I., A. Frankfurter, and L.I. Rebhun (1986) Differential localization of MAP-2 and Tau in mammalian neurons in situ. Ann. NY Acad. Sci. 466:145-166.
9. Broadie, K., H.J. Bellen, A. DiAntonio, J.T. Littleton, and T.L. Schwarz (1994) Absence of synaptotagmin disrupts excitation-secretion coupling during synaptic transmission. Proc. Natl. Acad. Sci. USA 91:10727-10731.
10. Brose, N., A.G. Petrenko, T.C. Südhof, and R. Jahn (1992) Synaptotagmin: A calcium sensor on the synaptic vesicle surface. Science 256:1021-1025.
11. Caceres. A., G.A. Banker, and L. Binder (1986) Immunocytochemical localization of tubnlin and microtubule-associated protein 2 during the development of hippocampal neurons in culture. J. Neurosci. 6:714-722.
12. Catsicas, S., D. Larhammar, A. Blomqvist, P.P. Sanna, R.J. Milner, and M.C. Wilson (1991) Expression of a conserved cell-type-specinc protein in nerve terminals coincides with synaptogenesis. Proc. Natl. Acad. Sci. USA 88:785-789.
13. Dani, J.W., D.M. Armstrong, and L.I. Benowitz (1991) Mapping the development of the rat brain bv GAP-43 immunohistochemistry. Neuroscience 40:277-287.
14. DeBello, W.M., H. Betz, and G.J. Augustine (1993) Synaptotagmin and neurotransmitter release. Cell 74:947-950.
15. Elmquist, J.K., C.A. Fox, L.R. Ross, and C.D. Jacobson (1992) Galanin-like immunoreaetivity in the adult and developing opossum brain. Dev. Brain Res. 67:161-179.
16. Elmquist, J.K., A. Kao, M.C. Kuehl-Kovarik, and C.D. Jacobson (1993) Developmental profile of galanin binding sites in the mammalian brain. Mol. Cell Neurosci. 4:354-365.
17. Elmquist, J.K., J.J. Swanson, D.S. Sakaguchi, L.R. Ross, and C.D. Jacobson (1994) Developmental distribution of GFAP and vimentin in the Brazilian opossum brain. J. Comp. Neurol. 344:283-296.
18. Fadem, B.H., G.L. Trupin, J.L. Vandeberg, E. Maliniak, and V. Hayssen (1982) Care and breeding of the grey short-tailed opossum (Monodelphis domestica). Lab. Animal Sci. 32:405-409.
19. Ferreira, A., J. Busciglio, and A. Caceres (1987) An immunocytochemical analysis of the ontogeny of the microtubule-associated proteins MAP-2 and Tau in the nervous system of the rat. Dev. Brain Res. 34:9-31.
20. Fletcher, T.L., P. Cameron, P. DeCamilli, and G. Banker (1991) The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. J. Neurosci. 11:1617-1626.
21. Fox, C.A., M. Jeyapalan, L.R. Ross, and C.D. Jacobson (1991a) Ontogeny of cholecystokinin-like immunoreactivity in the Brazilian opossum brain. Dev. Brain Res. 64:1-18.
22. Fox, C.A., L.R. Ross, and C.D. Jacobson (1991b) Ontogeny of cells containing estrogen receptor-like immunoreactivity in the Brazilian opossum brain. Dev. Brain Res. 63:209-219.
23. 2- sensor for transmitter release as a central synapse. Cell 79:717-727.
24. Goslin, K., D.J. Schreyer, J.H.P. Skene, and G. Banker (1988) Development of neuron polarity: GAP-43 distinguishes axonal from dendritic growth cones. Nature 336:672-674.
25. Goslin, K., D.J. Schreyer. J.H.P. Skene, and G. Banker (1990) Changes in the distribution of GAP-43 during the development of neuronal polarity. J. Neurosci. 10:588-602.
26. Greenberg, S.G., and P. Davies (1990) A preparation of Alzheimer paired helical filaments that displays distinct τ proteins by polyacrylamide gel eleetrophoresis. Proc. Natl. Acad. Sci. USA 57:5827-5831.
27. Greenberg, S.G., P. Davies, J.D. Schein, and L.I. Binder (1992) Hydrofluoric acid-treated tau PHF proteins display the same biochemical properties as normal τ. J. Biol. Chem. 267:564-569.
28. Greengard, P., F. Valtorta, A.J. Czernik, and F. Benfenati (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259:780-785.
29. Iqbal, J., J.K. Elmquist, L.R. Ross, M.R. Ackerman, C.D. Jacobson (1995) Postnatal neurogenesis of the hypothalamic paraventricular and supraoptic nuclei in the Brazilian opossum brain. Dev. Brain Res. 83:151-160.
30. Jacobson, C.D. (1984) Fetal mechanisms involved in the morphological sexual differentiation of the brain. In F. Ellendorf, P. Gluckman, and N. Parvizi (eds): Research in Perinatal Medicine (II): Fetal Neuroendocrinology. New York: Perinatology Press, pp. 137-148.
31. Jahn, R., W. Schiebler, C. Ouimet, and P. Greengard (1985) A 38,000-Dalton membrane protein (p38) present in synaptic vesicles. Proc. Natl. Acad. Sci. USA 82:4137-4141.
32. Knaus, P., H. Betz, and H. Rehm (1986) Expression of synaptophysin during postnatal development of the mouse brain. J. Neurochem. 47:1302-1304.
33. Kuehl-Kovarik, M.C., and C.D. Jacobson (1996) Ontogeny of cholecystokinin binding sites in the laboratory rat hindbrain. Brain Behav. Evol. (in press).
34. Kuehl-Kovarik, M.C., L.R. Ross, J.K. Elmquist, and C.D. Jacobson (1993a) Localization of cholecystokinin binding sites in the adult and developing Brazilian opossum brain. J. Comp. Neurol. 336:40-52.
35. Kuehl-Kovarik, M.C., J.J. Swanson, L.R. Ross, and C.D. Jacobson (1993b) The cholecystokinergic system and the developing facial motor nucleus. Soc. Neurosci. Abstr. 19:729.
36. Laemle, L.K., K.B. Repke, R. Hawkes, and F.L. Rice (1991) Synaptogenesis in the rat suprachiasmatic nucleus: A light microscope immunocytochemical study. Brain Res. 544:108-117.
37. Laemmli, U. (1970) Cleavage of structural proteins during the assembly of bacteriophage T4. Nature 227:680-685.
38. Leclerc, N., P.W. Beesley. I. Brown, M. Colonnier. J.W. Gurd, T. Paladino, and R. Hawkes (1989) Synaptophysin expression during Synaptogenesis in the rat cerebellar cortex. J. Comp. Neurol. 280:197-212.
39. Lou, X., and J.L. Bixby (1993) Coordinate and noncoordinate regulation of synaptic protein genes during embryonic development. Dev. Biol. 159: 327-337.
40. Masliah, E., A.M. Fagan, R.D. Terry. R. DeTeresa, M. Mallory, and F.H. Gage (1991) Reactive synaptogenesis assessed by synaptophysin immunoreactivity is associated with GAP-43 in the dentate gyrus of the adult rat. Exp. Neurol. 113:131-142.
41. Matthew, W.D., L. Tsavaler, and L.F. Reichardt (1981) Identification of a synaptic vesicle-specific membrane protein with a wide distribution in neuronal and neurosecretory tissue. J. Cell Biol. 91:257-269.
42. Moore, R.Y., and M.E. Bernstein (1989) Synaptogenesis in the rat suprachiasmatic nucleus demonstrated by electron microscopy and synapsin I immunoreactivity. J. Neurosci. 9:2151-2162.
43. Navone, F., R. Jahn, G.D. Gioia, H. Stukenbrok, P. Greengard, and P. DeCamilli (1986) Protein p38: An integral membrane protein specific for small vesicles of neurons and neuroendocrine cells. J. Cell Biol. 103:2511-2527.
44. Nelson, P.T., L. Marton, and C.B. Saper (1993) Alz-50 immunohistochemistry in the normal sheep striatum: A light and electron microscope study. Brain Res. 600:285-297.
45. O'Connor, V., G.J. Augustine, and H. Betz (1994) Synaptic vesicle exocytosis: Molecules and models. Cell 76:785-787.
46. Oyler, G.A., J.W. Poffi, M.C. Wilson, and M.L. Billingsley (1991) Developmental expression of the 25 kDa synaptosomal-associated protein (SNAP-25) in rat brain. Proc. Natl. Acad. Sci. USA 88:5247-5251.
47. Paxinos, G., I. Tork, L.H. Tecott, and KL. Valentino (1991) Atlas of the Developmental Rat Brain. San Diego: Academic Press.
48. Paxinos, G., K.W.S. Ashwell, and I. Tork (1994) Atlas of the Developmental Rat Brain, Second Edition. San Diego: Academic Press.
49. Perin, M.S., V.A. Fried, G.A. Mignery, R. Jahn, and T.C. Südhof (1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 345:260-263.
50. Pope, W., S.A. Enam, N. Bawa, B.E. Miller, H.A. Ghanbari, and W.L. Klein (1993) Phosphorylated tau epitope of Alzheimer's disease is coupled to axon development in the avian central nervous system. Exp. Neurol. 120:106-113.
51. Pope, W.B., M.P. Lambert, B. Leypold, R. Seupaul, L. Sletten, G. Krafft, and W.L. Klein (1994) Microtubule-associated protein tau is hyperphosphorylated during mitosis in the human neuroblastoma cell line SH-SY5Y. Exp. Neurol. 126:185-194.
52. Sakaguchi, D.S., J.F. Moeller, C.R. Coffman, N. Gallenson, and W.A. Harris (1989) Growth cone interactions with a glial cell line from embryonic Xenopus retina. Dev. Biol. 134:158-174.
53. Schwanzel-Fukuda, M., B.H. Fadem, M.S. Garcia, and D.W. Paff (1988) Immunocytochemical localization of luteinizing hormone-releasing hormone (LHRH) in the nervus terminalis of the adult and early neonatal grey short-tailed opossum (Monodelphis domestica). J. Comp. Neurol. 276:44-60.
54. Senba, E., M. Tohyama, Y. Shiotani, Y. Kawasaki, T. Kubo, T. Matsunaga, P.C. Emson, and H.W. Steinbusch (1985) Peptidergic and aminergic innervation of the facial nucleus of the rat with special reference to ontogenetic development. J. Comp. Neurol. 238:429-439.
55. Südhof, T.C., and R. Jahn (1991) Proteins of synaptic vesicles involved in exocytosis and membrane recycling. Neuron 6:665-677.
56. Swanson, J.J., J. Iqbal, J.K. Elmquist, and C.D. Jacobson (1994) Neurogenesis and synaptogenesis of the developing septum and amygdala in the Brazilian opossum brain. Soc. Neurosci. Abstr. 20:1486.
57. Swanson, J.J., J. Iqbal, and C.D. Jacobson (1995) Migration of facial motoneurons in the developing Brazilian opossum brain. Soc. Neurosci. Abstr. 21:1039.
58. Tribollet, E., M. Goumaz, M. Raggenbass, M. Dubois-Dauphin, and J.J. Dreifuss (1991) Early appearance and transient expression of vasopressin receptors in the brain of the rat fetus and infant. An autoradiographical and electrophysiological study. Dev. Brain Res. 58:13-24.
59. Voigt, T., D.D. Lima, and M. Beckmann (1993) Synaptophysin immunoreactivity reveals inside-out pattern of early synaptogenesis in ferret cerebral cortex. J. Comp. Neurol. 330:48-64.
60. Walch-Solimena, C., K. Takei, K.L. Marek, K. Midyett, T.C. Südhof, P.D. Camilli, and R. Jahn (1993) Synaptotagmin: A membrane constituent of neuropeptide-containing large dense-core vesicles. J. Neurosci. 13:3895-3903.
61. Yokosuka, M., and S. Hayashi (1992) Transient expression of estrogen-receptor-like immunoreactivity (ER-LI) in the facial motor nucleus of the neonatal rat. Neurosci. Res. 15:90-95.