Essential role of the synaptic vesicle protein synapsin II in formalin-induced hyperalgesia and glutamate release in the spinal cord

Pain

Volumn 115, Issue 1-2, 2005, Pages 171-181

  Schmidtko, Achim ^a   Del Turco, Domenico ^b   Coste, Ovidiu ^a   Ehnert, Corina ^a   Niederberger, Ellen ^a   Ruth, Peter ^c   Deller, Thomas ^b   Geisslinger, Gerd ^a   Tegeder, Irmgard ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c Pharmazeutisches Institut   (Germany)

Author keywords

Microdialysis; Pain; Spinal cord; Synaptic vesicle protein

Indexed keywords

FORMALDEHYDE; GLUTAMIC ACID; NERVE PROTEIN; PROTEIN C FOS; SYNAPSIN 2; UNCLASSIFIED DRUG; ZYMOSAN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; HINDLIMB; HYPERALGESIA; HYPOALGESIA; IMMUNOCOMPETENT CELL; KNOCKOUT MOUSE; MALE; MICRODIALYSIS; MOTOR COORDINATION; MOUSE; NERVE CELL PLASTICITY; NERVE ENDING; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NOCICEPTIVE STIMULATION; NONHUMAN; PAW EDEMA; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL CORD DORSAL HORN; STRAIN DIFFERENCE; TOUCH; WILD TYPE;

EID: 17044373147     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2005.02.027     Document Type: Article

References (55)

1. J. Ahluwalia, L. Urban, S. Bevan, M. Capogna, and I. Nagy Cannabinoid 1 receptors are expressed by nerve growth factor- and glial cell-derived neurotrophic factor-responsive primary sensory neurones Neuroscience 110 2002 747 753
2. K.O. Aley, and J.D. Levine Role of protein kinase A in the maintenance of inflammatory pain J Neurosci 19 1999 2181 2186
3. K.O. Aley, G. McCarter, and J.D. Levine Nitric oxide signaling in pain and nociceptor sensitization in the rat J Neurosci 18 1998 7008 7014
4. M. Ates, M. Hamza, K. Seidel, C.E. Kotalla, C. Ledent, and H. Guhring Intrathecally applied flurbiprofen produces an endocannabinoid-dependent antinociception in the rat formalin test Eur J Neurosci 17 2003 597 604
5. M. Bahler, and P. Greengard Synapsin I bundles F-actin in a phosphorylation-dependent manner Nature 326 1987 704 707
6. 2+/calmodulin- dependent protein kinase II is a binding protein for synapsin I Nature 359 1992 417 420
7. D.L. Bennett, G.J. Michael, N. Ramachandran, J.B. Munson, S. Averill, Q. Yan, S.B. McMahon, and J.V. Priestley A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury J Neurosci 18 1998 3059 3072
8. C.A. Brautigam, Y. Chelliah, and J. Deisenhofer Tetramerization and ATP binding by a protein comprising the A, B, and C domains of rat synapsin I J Biol Chem 279 2004 11948 11956
9. P.E. Ceccaldi, F. Grohovaz, F. Benfenati, E. Chieregatti, P. Greengard, and F. Valtorta Dephosphorylated synapsin I anchors synaptic vesicles to actin cytoskeleton: an analysis by videomicroscopy J Cell Biol 128 1995 905 912
10. P. Chi, P. Greengard, and T.A. Ryan Synapsin dispersion and reclustering during synaptic activity Nat Neurosci 4 2001 1187 1193
11. P. Chi, P. Greengard, and T.A. Ryan Synaptic vesicle mobilization is regulated by distinct synapsin I phosphorylation pathways at different frequencies Neuron 38 2003 69 78
12. M. Costigan, K. Befort, L. Karchewski, R.S. Griffin, D. Da'Urso, A. Allchorne, J. Sitarski, J.W. Mannion, R.E. Pratt, and C.J. Woolf 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
13. R. Dubner, and M.A. Ruda Activity-dependent neuronal plasticity following tissue injury and inflammation Trends Neurosci 15 1992 96 103
14. A. Ferreira, K.S. Kosik, P. Greengard, and H.Q. Han Aberrant neurites and synaptic vesicle protein deficiency in synapsin II-depleted neurons Science 264 1994 977 979
15. A. Ferreira, H.Q. Han, P. Greengard, and K.S. Kosik Suppression of synapsin II inhibits the formation and maintenance of synapses in hippocampal culture Proc Natl Acad Sci USA 92 1995 9225 9229
16. A. Ferreira, L.S. Chin, L. Li, L.M. Lanier, K.S. Kosik, and P. Greengard Distinct roles of synapsin I and synapsin II during euronal development Mol Med 4 1998 22 28
17. G. Geisslinger, U. Muth-Selbach, O. Coste, G. Vetter, A. Schrodter, H.G. Schaible, K. Brune, and I. Tegeder Inhibition of noxious stimulus-induced spinal prostaglandin E2 release by flurbiprofen enantiomers: a microdialysis study J Neurochem 74 2000 2094 2100
18. S. Giovedi, F. Darchen, F. Valtorta, P. Greengard, and F. Benfenati Synapsin is a novel RAB3 effector protein on small synaaptic vesicles II. Functional effects of the Rab3A-synapsin 1 interaction J Biol Chem 2004 20
19. S. Giovedi, P. Vaccaro, F. Valtorta, F. Darchen, P. Greengard, G. Cesareni, and F. Benfenati Synapsin is a novel RAB3 effector protein on small synaptic vesicles 1. Identification and characterization of the synapsin I-Rab3 interactions in vitro and in intact nerve terminals J Biol Chem 2004 20
20. P. Greengard, F. Valtorta, A.J. Czernik, and F. Benfenati Synaptic vesicle phosphoproteins and regulation of synaptic function Science 259 1993 780 785
21. H.Q. Han, R.A. Nichols, M.R. Rubin, M. Bahler, and P. Greengard Induction of formation of presynaptic terminals in neuroblastoma cells by synapsin IIb Nature 349 1991 697 700
22. S. Hilfiker, V.A. Pieribone, A.J. Czernik, H.T. Kao, G.J. Augustine, and P. Greengard Synapsins as regulators of neurotransmitter release Philos Trans R Soc Lond B Biol Sci 354 1999 269 279
23. S. Hilfiker, V.A. Pieribone, C. Nordstedt, P. Greengard, and A.J. Czernik Regulation of synaptotagmin I phosphorylation by multiple protein kinases J Neurochem 73 1999 921 932
24. 2+ J Biol Chem 273 1998 13371 13374
25. 2+ regulation J Biol Chem 273 1998 1425 1429
26. M. Hosaka, R.E. Hammer, and T.C. Sudhof A phospho-switch controls the dynamic association of synapsins with synaptic vesicles Neuron 24 1999 377 387
27. A. Huber, W.L. Neuhuber, N. Klugbauer, P. Ruth, and H.D. Allescher Cysteine-rich protein 2, a novel substrate for cGMP kinase I in enteric neurons and intestinal smooth muscle J Biol Chem 275 2000 5504 5511
28. Y. Humeau, F. Doussau, F. Vitiello, P. Greengard, F. Benfenati, and B. Poulain Synapsin controls both reserve and releasable synaptic vesicle pools during neuronal activity and short-term plasticity in Aplysia J Neurosci 21 2001 4195 4206
29. R.R. Ji, H. Baba, G.J. Brenner, and C.J. Woolf Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity Nat Neurosci 2 1999 1114 1119
30. H.T. Kao, H.J. Song, B. Porton, G.L. Ming, J. Hoh, M. Abraham, A.J. Czernik, V.A. Pieribone, M.M. Poo, and P. Greengard A protein kinase A-dependent molecular switch in synapsins regulates neurite outgrowth Nat Neurosci 5 2002 431 437
31. L. Li, L.S. Chin, O. Shupliakov, L. Brodin, T.S. Sihra, O. Hvalby, V. Jensen, D. Zheng, J.O. McNamara, P. Greengard, and P. Andersen Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice Proc Natl Acad Sci USA 92 1995 9235 9239
32. A.B. Malmberg, and T.L. Yaksh Cyclooxygenase inhibition and the spinal release of prostaglandin E2 and amino acids evoked by paw formalin injection: a microdialysis study in unanesthetized rats J Neurosci 15 1995 2768 2776
33. A.B. Malmberg, E.P. Brandon, R.L. Idzerda, H. Liu, G.S. McKnight, and A.I. Basbaum Diminished inflammation and nociceptive pain with preservation of neuropathic pain in mice with a targeted mutation of the type I regulatory subunit of cAMP-dependent protein kinase J Neurosci 17 1997 7462 7470
34. A.B. Malmberg, C. Chen, S. Tonegawa, and A.I. Basbaum Preserved acute pain and reduced neuropathic pain in mice lacking PKCgamma Science 278 1997 279 283
35. J.W. Mandell, A.J. Czernik, P. De Camilli, P. Greengard, and E. Townes-Anderson Differential expression of synapsins I and II among rat retinal synapses J Neurosci 12 1992 1736 1749
36. S.T. Meller, and G.F. Gebhart Nitric oxide (NO) and nociceptive processing in the spinal cord Pain 52 1993 127 136
37. D.C. Molliver, D.E. Wright, M.L. Leitner, A.S. Parsadanian, K. Doster, D. Wen, Q. Yan, and W.D. Snider IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life Neuron 19 1997 849 861
38. T.C. Petrucci, and J.S. Morrow Synapsin I: an actin-bundling protein under phosphorylation control J Cell Biol 105 1987 1355 1363
39. Y. Qian, D.S. Chao, D.R. Santillano, T.L. Cornwell, A.C. Nairn, P. Greengard, T.M. Lincoln, and D.S. Bredt cGMP-dependent protein kinase in dorsal root ganglion: relationship with nitric oxide synthase and nociceptive neurons J Neurosci 16 1996 3130 3138
40. A.M. Ritter, C.J. Woodbury, K. Albers, B.M. Davis, and H.R. Koerber Maturation of cutaneous sensory neurons from normal and NGF-overexpressing mice J Neurophysiol 83 2000 1722 1732
41. T.W. Rosahl, D. Spillane, M. Missler, J. Herz, D.K. Selig, J.R. Wolff, R.E. Hammer, R.C. Malenka, and T.C. Sudhof Essential functions of synapsins I and II in synaptic vesicle regulation Nature 375 1995 488 493
42. J. Sandkuhler, and X. Liu Induction of long-term potentiation at spinal synapses by noxious stimulation or nerve injury Eur J Neurosci 10 1998 2476 2480
43. H. Schmidt, M. Werner, P.A. Heppenstall, M. Henning, M.I. More, S. Kuhbandner, G.R. Lewin, F. Hofmann, R. Feil, and F.G. Rathjen cGMP-mediated signaling via cGKIalpha is required for the guidance and connectivity of sensory axons J Cell Biol 159 2002 489 498
44. A. Schmidtko, P. Ruth, G. Geisslinger, and I. Tegeder Inhibition of cyclic guanosine 5′-monophosphate-dependent protein kinase I (PKG-I) in lumbar spinal cord reduces formalin-induced hyperalgesia and PKG upregulation Nitric Oxide 8 2003 89 94
45. S.A. Schnell, W.A. Staines, and M.W. Wessendorf Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue J Histochem Cytochem 47 1999 719 730
46. A.J. Silva, T.W. Rosahl, P.F. Chapman, Z. Marowitz, E. Friedman, P.W. Frankland, V. Cestari, D. Cioffi, T.C. Sudhof, and R. Bourtchuladze Impaired learning in mice with abnormal short-lived plasticity Curr Biol 6 1996 1509 1518
47. T. Sugiyama, T. Shinoe, Y. Ito, H. Misawa, T. Tojima, E. Ito, and T. Yoshioka A novel function of synapsin II in neurotransmitter release Brain Res Mol Brain Res 85 2000 133 143
48. I. Tegeder, E. Niederberger, G. Vetter, L. Brautigam, and G. Geisslinger Effects of selective COX-1 and -2 inhibition on formalin-evoked nociceptive behaviour and prostaglandin E(2) release in the spinal cord J Neurochem 79 2001 777 786
49. I. Tegeder, D. Del Turco, A. Schmidtko, M. Sausbier, R. Feil, F. Hofmann, T. Deller, P. Ruth, and G. Geisslinger Reduced inflammatory hyperalgesia with preservation of acute thermal nociception in mice lacking cGMP-dependent protein kinase I Proc Natl Acad Sci USA 101 2004 3253 3257
50. S. Terada, T. Tsujimoto, Y. Takei, T. Takahashi, and N. Hirokawa Impairment of inhibitory synaptic transmission in mice lacking synapsin I J Cell Biol 145 1999 1039 1048
51. A.J. Todd, Z. Puskar, R.C. Spike, C. Hughes, C. Watt, and L. Forrest Projection neurons in lamina I of rat spinal cord with the neurokinin 1 receptor are selectively innervated by substance p-containing afferents and respond to noxious stimulation J Neurosci 22 2002 4103 4113
52. Y. Tu, S.K. Nayak, J. Woodson, and E.M. Ross Phosphorylation-regulated inhibition of the Gz GTPase-activating protein activity of RGS proteins by synapsin I J Biol Chem 278 2003 52273 52281
53. F. Valtorta, F. Benfenati, and P. Greengard Structure and function of the synapsins J Biol Chem 267 1992 7195 7198
54. C.J. Woolf, and M. Costigan Transcriptional and posttranslational plasticity and the generation of inflammatory pain Proc Natl Acad Sci USA 96 1999 7723 7730
55. T.L. Yaksh, X.Y. Hua, I. Kalcheva, N. Nozaki-Taguchi, and M. Marsala The spinal biology in humans and animals of pain states generated by persistent small afferent input Proc Natl Acad Sci USA 96 1999 7680 7686