Differential subcellular localization of SNAP-25a and SNAP-25b RNA transcripts in spinal motoneurons and plasticity in expression after nerve injury

Molecular Brain Research

Volumn 37, Issue 1-2, 1996, Pages 49-62

  Jacobsson, Gunilla ^a   Piehl, Fredrik ^a   Bark, I Christina ^b   Zhang, Xu ^c   Meister, Björn ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Avulsion; Axotomy; Chicken; GAP 43; Gene; In situ hybridization; Intron; mRNA; Nucleus; Rat; Spinal cord; Synaptic protein; Ventral horn

Indexed keywords

PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; MALE; NERVE FIBER TRANSECTION; NERVE INJURY; NEUROTRANSMITTER RELEASE; NONHUMAN; OLIGONUCLEOTIDE PROBE; PLASTICITY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SPINAL CORD MOTONEURON; SYNAPTOSOME;

ANIMALIA; GALLUS GALLUS;

EID: 0029871438     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/0169-328X(95)00272-T     Document Type: Article

References (60)

1. Aldskogius, H. and Svensson, M., Neuronal and glial cell responses to axon injury. In: Advances in Structural Biology, JAI Press, Vol. 2, 1993, pp. 191-223.
2. Archer, D.R. and McLean W.G., Changes in fast axonally transported proteins in the regenerating rabbit vagus nerve, Neurosci. Lett., 87 (1988) 151-156.
3. Bark, I.C., Structure of the chicken gene for SNAP-25 reveals duplicated exons encoding distinct isoforms of the protein, J. Mol. Biol., 233 (1993) 67-76.
4. Bark, I.C. and Wilson, M.C., Human cDNA clones encoding two different isoforms of the nerve terminal protein SNAP-25, Gene, 139 (1994) 291-292.
5. Bark, I.C. and Wilson, M.C., Regulated vesicular fusion in neurons: snapping together the details, Proc. Natl. Acad. Sci. USA, 91 (1994) 4621-4624.
6. Bark, I.C., Hahn, K.M., Ryabinin, A.E. and Wilson, M.C., Differential expression of SNAP-25 protein isoforms during divergent vesicle fusion events of neural development, Proc. Natl. Acad. Sci. USA, 92 (1995) 1510-1514.
7. Beelman, C.A. and Parker, R., Degradation of mRNA in eukaryotes, Cell 81 (1995) 179-183.
8. Benowitz, L.I. and Routtenberg, A., A membrane phosphoprotein associated with neural development, axonal regeneration, phospholipid metabolism, and synaptic plasticity, Trends Neurosci., 10 (1987) 527-532.
9. Bisby, M.A., Changes in the composition of labeled protein transported in motor axons during their regeneration, J. Neurobiol., 11 (1980) 435-445.
10. Catsicas, S., Larhammar, D., Blomqvist, A., Sanna, P.P., Milner, R.J. and Wilson, M.C., Expression of a conserved cell-type-specific protein in nerve terminals coincides with synaptogenesis, Proc. Natl. Acad. Sci. USA, 88 (1991) 785-789.
11. Clinton, J., Blackman, S.E.-A., Royston, M.C. and Roberts, G.W., Differential synaptic loss in the cortex in Alzheimer's disease: a study using archival material, NeuroReport, 5 (1994) 497-500.
12. Dagerlind, Å., Friberg, K., Bean, A.J. and Hökfelt, T., Sensitive mRNA detection using unfixed tissue: combined radioactive and non-radioactive in situ hybridization histochemistry, Histochemistry, 98 (1992) 39-49.
13. Elliott, D.J., Stutz, F., Lescure, A. and Rosbash, M., mRNA nuclear export, Curr. Opin. Gen. Dev. 4 (1994) 305-309.
14. Erickson, P.A., Feinstein, S.C., Lewis, G.P. and Fisher, S.K., Glial fibrillary acidic protein and its mRNA: ultrastructural detection and determination of changes after CNS injury, J. Struct. Biol., 108 (1992) 148-161.
15. Ferro-Novick, S. and Jahn, R., Vesicle fusion from yeast to man, Nature, 370 (1994) 191-193.
16. Geddes, J.W., Hess, E.J., Hart, R.A., Kesslak, J.P., Cotman, C.W. and Wilson, W.C., Lesions of hippocampal circuitry define synaptosomal-associatcd protein 25 (SNAP-25) as a novel presynaptic marker, Neuroscience, 38 (1990) 515-525.
17. Greengard, P., Valtorta, F., Czernik, A.J. and Benfenati, F., Synaptic vesicle phosphoproteins and regulation of synaptic function, Science, 259 (1993) 780-785.
18. Hamm, J. and Mattaj, I.W., Monomethylated cap structures facilitate RNA export from the nucleus, Cell, 63 (1990) 109-118.
19. Hess, D.T., Slater, T.M., Wilson, M.C. and Skene, J.H.P., The 25 kDa synaptosomal-associated protein SNAP-25 is the major methionine-rich polypeptide in rapid axonal transport and a major substrate for palmitoylation in adult CNS, J. Neurosci., 12 (1992) 4634-4641.
20. Hess, E.J., Jinnah, H.A., Kozak, C.A. and Wilson, M.C., Spontaneous locomotor hyperactivity in a mouse mutant with a deletion including the Snap gene on chromosome 2, J. Neurosci., 12 (1992) 2865-2874.
21. Jacobson, R.D., Viràg, I. and Skene J.P.H., A protein associated with axon growth, GAP-43 is widely distributed and developmentally regulated in rat CNS, J. Neurosci., 6 (1986) 1843-1855.
22. Jacobsson, G., Bean, A.J., Scheller, R.H., Juntti-Berggren, L., Deeney, J.T., Berggren, P.-O. and Meister, B., Identification of synaptic proteins and their isoform mRNAs in compartments of pancreatic endocrine cells, Proc. Natl. Acad. Sci. USA, 91 (1994) 12487-12491.
23. Jacobsson, G., Piehl, F., Zhang, X., Bark, I.C. and Meister, B., SNAP-25 isoform mRNA expression in spinal motoneurons after nerve injury, Soc. Neurosci. Abstr., (1995) 705.14.
24. Kalil, K. and Skene, J.H.P., Elevated synthesis of an axonally transported protein correlates with axon outgrowth in normal and injured pyramidal tracts, J. Neurosci., 6 (1986) 2563-2570.
25. Karns, L.R., Ng, S.C., Freeman, J.A. and Fishman, M.C., Cloning of complementary DNA for GAP-43, a neuronal growth-related protein, Science, 236 (1987) 597-600.
26. Kislauskis, E.H., Li, Z., Singer, R.H. and Taneja, K.L., Isoformspecific 3'-untranslated sequences sort a-cardiac and β-cytoplasmic actin messenger RNAs to different cytoplasmic compartments, J. Cell Biol., 123 (1993) 167-172.
27. Koo, E.H., Sisodia, S.S., Archer, D.R., Martin, L.J., Weidemann, A., Beyreuther, K., Fischer, P., Masters, C.L. and Price, D.L., Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport, Proc. Natl. Acad. Sci. USA, 87 (1990) 1561-1565.
28. Lapchak, P.A., Araujo, D.M. and Hefti, F., BDNF and trkB mRNA expression in the rat hippocampus following entorhinal cortex lesions, NeuroReport, 4 (1993) 191-194.
29. Lapchak, P.A., Araujo, D.M., Beck, K.D., Finch, C.E., Johnson, S.A. and Hefti, F., BDNF and trkB mRNA expression in the hippocampal formation of aging rats, Neurobiol. Aging, 14 (1993) 121-126.
30. Lawrence, J.B. and Singer, R.H., Intracellular localization of messenger RNAs for cytoskeletal proteins. Cell, 45 (1986) 407-415.
31. Legrain, P. and Rosbash, M., Some cis- and trans-acting mutants for splicing target pre-mRNA to the cytoplasm, Cell, 57 (1989) 573-583.
32. 35S-methionine-labeled rapidly transported protein (Superprotein) is identical to SNAP-25, a protein of synaptic terminals, J. Neurosci., 11 (1991) 3412-3421.
33. Lorenz, T. and Willard, M., Subcellular distribution of intra-axonally transported polypeptides in the rabbit visual system, Proc. Natl. Acad. Sci. USA, 75 (1978) 505-509.
34. Lustig, R.H., Hua, P., Wilson, M.C. and Federoff, H.J., Ontogeny, sex dimorphism, and neonatal sex hormone determination of synapse-associated messenger RNAs in rat brain, Mol. Brain Res., 20 (1993) 101-110.
35. Nicholas, A.P., Pieribone, V. and Hökfelt, T., Distribution of mRNAs for alpha-2 adrenergic receptor subtypes in rat brain: an in situ hybridization study, J. Camp. Neurol., 328 (1993) 575-594.
36. Nicolopoulos-Stournaras, S. and Iles, J.F., Motor neuron columns in the lumbar spinal cord of the rat, J. Comp. Neurol., 217 (1983) 75-85.
37. Novick, P., Field, C. and Shekman, R., Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway, Cell, 21 (1980) 205-215.
38. Osen-Sand, A., Catsicas, M., Staple, J.K., Jones, K.A., Ayala, G., Knowles, J., Grenningloh, G. and Catsicas, S., Inhibition of axonal growth by SNAP-25 antisense oligonucleotides in vitro and in vivo, Nature, 364 (1993) 445-448.
39. Oyler, G.A., Higgins, G.A., Hart, R.A., Battenberg, E., Billingsley, M., Bloom, F.E. and Wilson, W.C., The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations, J. Cell Biol., 109 (1989) 3039-3052.
40. Oyler, G.A., Polli, J.W., Wilson, M.C. and Billingsley, M.L., Developmental expression of the 25-kDa synaptosomal-associated protein (SNAP-25) in rat brain, Proc. Natl. Acad. Sci. USA, 88 (1991) 5247-5251.
41. Pevsner, J., Hsu, S.-C., Braun, J.A.E., Calakos, N., Ting, A.E. and Scheller, R.H., Specificity and regulation of a synaptic vesicle docking complex, Neuron, 13 (1994) 353-361.
42. Piehl, F., Arvidsson, U., Johnson H., Cullheim, S., Dagerlind, Å., Ulfhake, B., Cao, Y., Eide, R., Pettersson, R.F., Terenius, L. and Hökfelt, T., GAP-43, aFGF, CCK and α- and β-CGRP in rat spinal motoneurons subjected to axotomy and/or dorsal root severance, Eur. J. Neurosci., 5 (1993) 1321-1333.
43. Piehl, F., Ru-Rong, J., Cullheim, S., Hökfelt, T., Lindholm, D. and Hughes, R.A., Fibroblast growth factors regulate calcitonin gene-related peptide mRNA expression in rat motoneurons after lesion and in culture, Eur. J. Neurosci., 1 (1995) 1739-1750.
44. Redshaw, J.D. and Bisby, M.A., Fast axonal transport in central nervous system and peripheral nervous system axons following axotomy, J. Neurobiol., 15 (1984) 109-117.
45. Redshaw, J.D. and Bisby, M.A., Proteins of fast axonal transport in the regenerating hypoglossal nerve of the rat. Can. J. Physiol. Pharmacol., 62 (1984) 1387-1393.
46. Redshaw, J.D. and Bisby, M.A., Comparison of the effects of sciatic nerve crush or resection on the proteins of fast axonal transport in rat dorsal root ganglion cells axons, Exp. Neurol., 88 (1985) 437-446.
47. Reh, T.A., Redshaw, J.D. and Bisby, M.A., Axons of the pyramidal tract do not increase their transport of growth-associated proteins after axotomy, Mol. Brain Res., 2 (1987) 1-6.
48. Risinger, C. and Larhammar, D., Multiple loci for synapse protein SNAP-25 in the tetraploid goldfish, Proc. Natl. Acad. Sci. USA, 90 (1993) 10598-10602.
49. Risinger, C., Blomqvist, A.G., Lundell, I., Lambertsson, A., Nässel, D., Pieribone, V.A., Brodin, L., and Larhammar, D., Evolutionary conservation of synaptosome-associated protein 25 kDa (SNAP-25) shown by Drosophila and Torpedo cDNA clones, J. Biol. Chem., 268 (1993) 24408-24414.
50. Roth, D. and Burgoyne, R.D., SNAP-25 is present in a SNARE complex in adrenal chromaffin cells, FEBS Lett., 351 (1994) 207-210.
51. Sachs, A.B., Messenger RNA degradation in eukaryotes, Cell, 74 (1993) 413-421.
52. Sadoul, K., Lang, J., Montecucco, C., Weller, U., Regazzi, R., Catsicas, S., Wollheim, C.B. and Halban, P.A., SNAP-25 is expressed in islets of Langerhans and is involved in insulin release, J. Cell Biol., 128 (1995) 1019-1028.
53. Sanna, P.P., Bloom, F.E. and Wilson, M.C., Dibutyryl-cAMP induces SNAP-25 translocation into the neuntes in PC 12, Dev. Brain Res., 59 (1991) 104-108.
54. Scheller, R.H., Membrane trafficking in the presynaptic nerve terminal, Neuron, 14 (1995) 893-897.
55. Skene, J.H.P. and Willard, M., Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems, J. Cell Biol., 89 (1981) 96-103.
56. Specht, S.C. and Sweadner, K.J., Two different Na, K-ATPases in the optic nerve: cells of origin and axonal transport. Proc. Natl. Acad. Sci. USA, 81 (1984) 1234-1238.
57. Söllner, T. and Rothman, J.E., Neurotransmission: harnessing fusion machinery at the synapse, Trends Neurosci., 17 (1994) 344-348.
58. Swett, J.E., Wikholm, R.P., Blanks, R.H.I., Swett, A.L. and Conley, L.C., Motoneurons of the rat sciatic nerve, Exp. Neurol., 93 (1986) 227-252.
59. Young III, W.S., In situ hybridization histochemistry. In: A. Björklund, T. Hökfelt, F.G. Wouterlood and A.N. van den Pol (Eds.), Handbook of Chemical Neuroanatomy: Analysis of Neuronal Microcircuits and Synaptic Interactions, Elsevier, Amsterdam, 1990, pp. 481-512,
60. Zarrilli, R., Colantuoni, V. and Bruni, C.B., Regulation of insulin-like growth factor-II gene expression in rat liver cells, Eur. J. Biochem., 209 (1992) 445-452.