Differential expression of synaptoporin and synaptophysin in primary sensory neurons and up-regulation of synaptoporin after peripheral nerve injury

Neuroscience

Volumn 141, Issue 3, 2006, Pages 1233-1245

  Sun, T ^a   Xiao, H S ^a,c   Zhou, P B ^a   Lu, Y J ^a   Bao, L ^b   Zhang, X ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^c NATIONAL ENGINEERING CENTER FOR BIOCHIP AT SHANGHAI   (China)

Author keywords

dorsal root ganglion; dorsal spinal cord; gene expression regulation; nociceptor; sciatic nerve transection; synaptic vesicle protein

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; PROTEIN; SYNAPTOPHYSIN; SYNAPTOPORIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CELL SUBPOPULATION; CONTROLLED STUDY; MALE; NERVE CELL; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSORY NERVE; SPINAL GANGLION; SYNAPSE VESICLE; UPREGULATION;

ANALYSIS OF VARIANCE; ANIMALS; AXOTOMY; BLOTTING, WESTERN; CALCITONIN GENE-RELATED PEPTIDE; CELL COUNT; FUNCTIONAL LATERALITY; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LECTINS; MALE; NEURONS, AFFERENT; PERIPHERAL NERVOUS SYSTEM DISEASES; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SYNAPTOPHYSIN; TIME FACTORS;

EID: 33746459317     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.05.010     Document Type: Article

References (59)

1. Alder J., Kanki H., Valtorta F., Greengard P., and Poo M.M. Overexpression of synaptophysin enhances neurotransmitter secretion at Xenopus neuromuscular synapses. J Neurosci 15 (1995) 511-519
2. Alder J., Xie Z.P., Valtorta F., Greengard P., and Poo M. Antibodies to synaptophysin interfere with transmitter secretion at neuromuscular synapses. Neuron 9 (1992) 759-768
3. Bao L., Wang H.F., Cai H.J., Tong Y.G., Jin S.X., Lu Y.J., Grant G., Hokfelt T., and Zhang X. Peripheral axotomy induces only very limited sprouting of coarse myelinated afferents into inner lamina II of rat spinal cord. Eur J Neurosci 16 (2002) 175-185
4. Becher A., Drenckhahn A., Pahner I., Margittai M., Jahn R., and Ahnert-Hilger G. The synaptophysin-synaptobrevin complex. a hallmark of synaptic vesicle maturation. J Neurosci 19 (1999) 1922-1931
5. Bergmann M., Schuster T., Grabs D., Marqueze-Pouey B., Betz H., Traurig H., Mayerhofer A., and Gratzl M. Synaptophysin and synaptoporin expression in the developing rat olfactory system. Brain Res Dev Brain Res 74 (1993) 235-244
6. Betz H. Homology and analogy in transmembrane channel design. lessons from synaptic membrane proteins. Biochemistry 29 (1990) 3591-3599
7. Brandstatter J.H., Lohrke S., Morgans C.W., and Wassle H. Distributions of two homologous synaptic vesicle proteins, synaptoporin and synaptophysin, in the mammalian retina. J Comp Neurol 370 (1996) 1-10
8. Calakos N., and Scheller R.H. Vesicle-associated membrane protein and synaptophysin are associated on the synaptic vesicle. J Biol Chem 269 (1994) 24534-24537
9. Costigan M., Befort K., Karchewski L., Griffin R.S., D'Urso D., Allchorne A., Sitarski J., Mannion J.W., Pratt R.E., and Woolf C.J. Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci 3 (2002) 16
10. Daly C., Sugimori M., Moreira J.E., Ziff E.B., and Llinas R. Synaptophysin regulates clathrin-independent endocytosis of synaptic vesicles. Proc Natl Acad Sci U S A 97 (2000) 6120-6125
11. Daly C., and Ziff E.B. Ca2+-dependent formation of a dynamin-synaptophysin complex. potential role in synaptic vesicle endocytosis. J Biol Chem 277 (2002) 9010-9015
12. De Biasi S., and Rustioni A. Glutamate and substance P coexist in primary afferent terminals in the superficial laminae of spinal cord. Proc Natl Acad Sci U S A 85 (1988) 7820-7824
13. Edelmann L., Hanson P.I., Chapman E.R., and Jahn R. Synaptobrevin binding to synaptophysin. a potential mechanism for controlling the exocytotic fusion machine. EMBO J 14 (1995) 224-231
14. Fykse E.M., Takei K., Walch-Solimena C., Geppert M., Jahn R., De Camilli P., and Südhof T.C. Relative properties and localizations of synaptic vesicle protein isoforms. the case of the synaptophysins. J Neurosci 13 (1993) 4997-5007
15. Gerst J.E. SNARE regulators. matchmakers and matchbreakers. Biochim Biophys Acta 1641 (2003) 99-110
16. Grabs D., Bergmann M., Schuster T., Fox P.A., Brich M., and Gratz M. Differential expression of synaptophysin and synaptoporin during pre- and postnatal development of the rat hippocampal network. Eur J Neurosci 6 (1994) 1765-1771
17. Hökfelt T., Zhang X., and Wiesenfeld-Hallin Z. Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci 17 (1994) 22-30
18. Horikawa H.P., Kneussel M., El Far O., and Betz H. Interaction of synaptophysin with the AP-1 adaptor protein gamma-adaptin. Mol Cell Neurosci 21 (2002) 454-462
19. Hubner K., Windoffer R., Hutter H., and Leube R.E. Tetraspan vesicle membrane proteins. synthesis, subcellular localization, and functional properties. Int Rev Cytol 214 (2002) 103-159
20. Hunt S.P., and Mantyh P.W. The molecular dynamics of pain control. Nat Rev Neurosci 2 (2001) 83-91
21. Jahn R., Lang T., and Südhof T.C. Membrane fusion. Cell 112 (2003) 519-533
22. Jahn R., Schiebler W., Ouimet C., and Greengard P. A 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc Natl Acad Sci U S A 82 (1985) 4137-4141
23. Johnston P.A., Jahn R., and Südhof T.C. Transmembrane topography and evolutionary conservation of synaptophysin. J Biol Chem 264 (1989) 1268-1273
24. Johnston P.A., and Südhof T.C. The multisubunit structure of synaptophysin. Relationship between disulfide bonding and homo-oligomerization. J Biol Chem 265 (1990) 8869-8873
25. Knaus P., Betz H., and Rehm H. Expression of synaptophysin during postnatal development of the mouse brain. J Neurochem 47 (1986) 1302-1304
26. Knaus P., Marqueze-Pouey B., Scherer H., and Betz H. Synaptoporin, a novel putative channel protein of synaptic vesicles. Neuron 5 (1990) 453-462
27. Leube R.E. Expression of the synaptophysin gene family is not restricted to neuronal and neuroendocrine differentiation in rat and human. Differentiation 56 (1994) 163-171
28. Leube R.E., Kaiser P., Seiter A., Zimbelmann R., Franke W.W., Rehm H., Knaus P., Prior P., Betz H., Reinke H., et al. Synaptophysin. molecular organization and mRNA expression as determined from cloned cDNA. EMBO J 6 (1987) 3261-3268
29. Marqueze-Pouey B., Wisden W., Malosio M.L., and Betz H. Differential expression of synaptophysin and synaptoporin mRNAs in the postnatal rat central nervous system. J Neurosci 11 (1991) 3388-3397
30. McMahon H.T., Bolshakov V.Y., Janz R., Hammer R.E., Siegelbaum S.A., and Südhof T.C. Synaptophysin, a major synaptic vesicle protein, is not essential for neurotransmitter release. Proc Natl Acad Sci U S A 93 (1996) 4760-4764
31. Mitter D., Reisinger C., Hinz B., Hollmann S., Yelamanchili S.V., Treiber-Held S., Ohm T.G., Herrmann A., and Ahnert-Hilger G. The synaptophysin/synaptobrevin interaction critically depends on the cholesterol content. J Neurochem 84 (2003) 35-42
32. Morris J.L., Konig P., Shimizu T., Jobling P., and Gibbins I.L. Most peptide-containing sensory neurons lack proteins for exocytotic release and vesicular transport of glutamate. J Comp Neurol 483 (2005) 1-16
33. Nagy G., Reim K., Matti U., Brose N., Binz T., Rettig J., Neher E., and Sorensen J.B. Regulation of releasable vesicle pool sizes by protein kinase A-dependent phosphorylation of SNAP-25. Neuron 41 (2004) 417-429
34. Ovtscharoff W., Bergmann M., Marqueze-Pouey B., Knaus P., Betz H., Grabs D., Reisert I., and Gratzl M. Ontogeny of synaptophysin and synaptoporin in the central nervous system. differential expression in striatal neurons and their afferents during development. Brain Res Dev Brain Res 72 (1993) 219-225
35. Rehm H., Wiedenmann B., and Betz H. Molecular characterization of synaptophysin, a major calcium-binding protein of the synaptic vesicle membrane. EMBO J 5 (1986) 535-541
36. Reisinger C., Yelamanchili S.V., Hinz B., Mitter D., Becher A., Bigalke H., and Ahnert-Hilger G. The synaptophysin/synaptobrevin complex dissociates independently of neuroexocytosis. J Neurochem 90 (2004) 1-8
37. Ribeiro-de-Silva A. Substantia gelatinosa of spinal cord. In: Paxinos G. (Ed). The rat nervous system (1995), Academic Press, San Diego 47-59
38. Shibaguchi H., Takemura K., Kan S., Kataoka Y., Kaibara M., Saito N., and Taniyama K. Role of synaptophysin in exocytotic release of dopamine from Xenopus oocytes injected with rat brain mRNA. Cell Mol Neurobiol 20 (2000) 401-408
39. Silverman J.D., and Kruger L. Lectin and neuropeptide labeling of separate populations of dorsal root ganglion neurons and associated "nociceptor" thin axons in rat testis and cornea whole-mount preparations. Somatosens Res 5 (1988) 259-267
40. Singec I., Knoth R., Ditter M., Hagemeyer C.E., Rosenbrock H., Frotscher M., and Volk B. Synaptic vesicle protein synaptoporin is differently expressed by subpopulations of mouse hippocampal neurons. J Comp Neurol 452 (2002) 139-153
41. Snider W.D., and McMahon S.B. Tackling pain at the source. new ideas about nociceptors. Neuron 20 (1998) 629-632
42. Sørensen J.B. SNARE complexes prepare for membrane fusion. Trends Neurosci 28 (2005) 453-455
43. Sørensen J.B., Nagy G., Varoqueaux F., Nehring R.B., Brose N., Wilson M.C., and Neher E. Differential control of the releasable vesicle pools by SNAP-25 splice variants and SNAP-23. Cell 114 (2003) 75-86
44. Spiwoks-Becker I., Vollrath L., Seeliger M.W., Jaissle G., Eshkind L.G., and Leube R.E. Synaptic vesicle alterations in rod photoreceptors of synaptophysin-deficient mice. Neuroscience 107 (2001) 127-142
45. Südhof T.C. The synaptic vesicle cycle. Annu Rev Neurosci 27 (2004) 509-547
46. Tarsa L., and Goda Y. Synaptophysin regulates activity-dependent synapse formation in cultured hippocampal neurons. Proc Natl Acad Sci U S A 99 (2002) 1012-1016
47. Thiele C., Hannah M.J., Fahrenholz F., and Huttner W.B. Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat Cell Biol 2 (2000) 42-49
48. Thomas L., Hartung K., Langosch D., Rehm H., Bamberg E., Franke W.W., and Betz H. Identification of synaptophysin as a hexameric channel protein of the synaptic vesicle membrane. Science 242 (1988) 1050-1053
49. Tracey D.J., De Biasi S., Phend K., and Rustioni A. Aspartate-like immunoreactivity in primary afferent neurons. Neuroscience 40 (1991) 673-686
50. Valder C.R., Liu J.J., Song Y.H., and Luo Z.D. Coupling gene chip analyses and rat genetic variances in identifying potential target genes that may contribute to neuropathic allodynia development. J Neurochem 87 (2003) 560-573
51. Valtorta F., Pennuto M., Bonanomi D., and Benfenati F. Synaptophysin. leading actor or walk-on role in synaptic vesicle exocytosis?. Bioessays 26 (2004) 445-453
52. Voigt C., Metzdorf R., and Gahr M. Differential expression pattern and steroid hormone sensitivity of SNAP-25 and synaptoporin mRNA in the telencephalic song control nucleus HVC of the zebra finch. J Comp Neurol 475 (2004) 83-94
53. Wall P.D. Neuropathic pain. Pain 43 (1990) 267-268
54. Wang H., Sun H., Della Penna K., Benz R.J., Xu J., Gerhold D.L., Holder D.J., and Koblan K.S. Chronic neuropathic pain is accompanied by global changes in gene expression and shares pathobiology with neurodegenerative diseases. Neuroscience 114 (2002) 529-546
55. Washbourne P., Schiavo G., and Montecucco C. Vesicle-associated membrane protein-2 (synaptobrevin-2) forms a complex with synaptophysin. Biochem J 305 Pt 3 (1995) 721-724
56. Wiedenmann B., and Franke W.W. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell 41 (1985) 1017-1028
57. Woolf C.J., and Salter M.W. Neuronal plasticity. increasing the gain in pain. Science 288 (2000) 1765-1769
58. Xiao H.S., Huang Q.H., Zhang F.X., Bao L., Lu Y.J., Guo C., Yang L., Huang W.J., Fu G., Xu S.H., Cheng X.P., Yan Q., Zhu Z.D., Zhang X., Chen Z., Han Z.G., and Zhang X. Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain. Proc Natl Acad Sci U S A 99 (2002) 8360-8365
59. Zhang X., and Xiao H.S. Gene array analysis to determine the components of neuropathic pain signaling. Curr Opin Mol Ther 7 (2005) 532-537