Presynaptic and postsynaptic roles of NO, cGK, and RhoA in long-lasting potentiation and aggregation of synaptic proteins

Neuron

Volumn 45, Issue 3, 2005, Pages 389-403

  Wang, Hong Gang ^a   Lu, Fang Min ^a   Jin, Iksung ^a   Udo, Hiroshi ^a   Kandel, Eric R ^a,b,c,d   De Vente, Jan ^e   Walter, Ulrich ^f   Lohmann, Suzanne M ^f   Hawkins, Robert D ^a,d   Antonova, Irina ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c Kavli Institute for Brain Science   (United States)

^d NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^e MAASTRICHT UNIVERSITY   (Netherlands)

^f UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP DEPENDENT PROTEIN KINASE; NITRIC OXIDE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; ELECTROPHYSIOLOGY; IMMUNOHISTOCHEMISTRY; LONG TERM POTENTIATION; NEWBORN; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ACTINS; ANIMALS; ANIMALS, NEWBORN; CELL ADHESION MOLECULES; CELLS, CULTURED; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; EXCITATORY POSTSYNAPTIC POTENTIALS; GUANYLATE CYCLASE; HIPPOCAMPUS; LONG-TERM POTENTIATION; MICROFILAMENT PROTEINS; NERVE TISSUE PROTEINS; NITRIC OXIDE; PHOSPHOPROTEINS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; SYNAPTIC MEMBRANES; SYNAPTIC TRANSMISSION; SYNAPTOPHYSIN;

EID: 19944432457     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2005.01.011     Document Type: Article

References (80)

1. M. Ackermann, and A. Matus Activity-induced targeting of profilin and stabilization of dendritic spine morphology Nat. Neurosci. 6 2003 1194 1200
2. S.E. Ahmari, J. Buchanan, and S.J. Smith Assembly of presynaptic active zones from cytoplasmic transport packets Nat. Neurosci. 3 2000 445 451
3. I. Antonova, O. Arancio, A.-C. Trillat, H.-G. Wang, L. Zablow, H. Udo, E.R. Kandel, and R.D. Hawkins Rapid increase in clusters of presynaptic proteins at onset of long-lasting potentiation Science 294 2001 1547 1550
4. O. Arancio, E.R. Kandel, and R.D. Hawkins Activity-dependent long-term enhancement of transmitter release by presynaptic 3′, 5′-cyclic cGMP in cultured hippocampal neurons Nature 376 1995 74 80
5. O. Arancio, M. Kiebler, C.J. Lee, V. Lev-Ram, R.Y. Tsien, E.R. Kandel, and R.D. Hawkins Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons Cell 87 1996 1025 1035
6. O. Arancio, I. Antonova, S. Gambaryan, S.M. Lohmann, J.S. Wood, D.S. Lawrence, and R.D. Hawkins Presynaptic role of cGMP-dependent protein kinase during long-lasting potentiation J. Neurosci. 21 2001 143 149
7. H. Bito, T. Furuyashi, H. Isihara, Y. Shibasaki, K. Ohashi, K. Mizuno, M. Maekawa, T. Ishizaki, and S. Narumiya A critical role for a Rho-associated kinase, p160ROCK, in determining axon outgrowth in mammalian CNS neurons Neuron 26 2000 431 441
8. S. Blackshaw, M.J. Eliasson, A. Sawa, C.C. Watkins, D. Krug, A. Gupta, T. Arai, R.J. Ferrante, and S.H. Snyder Species, strain and developmental variations in hippocampal neuronal and endothelial nitric oxide synthase clarify discrepancies in nitric oxide-dependent synaptic plasticity Neuroscience 119 2003 979 990
9. C.L.M. Bon, and J. Garthwaite On the role of nitric oxide in hippocampal long-term potentiation J. Neurosci. 23 2003 1941 1948
10. O. Bozdagi, W. Shan, H. Tanaka, D.L. Benson, and G.W. Huntley Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation Neuron 28 2000 245 259
11. J.E. Brenman, D.S. Chao, S.H. Gee, A.W. McGee, S.E. Craven, D.R. Santillano, Z. Wu, F. Huang, H. Xia, and M.F. Peters Interaction of nitric oxide synthase with the post-synaptic density protein PSD-95 and a-l-syntrophin mediated by PDZ domains Cell 94 1996 757 767
12. A. Burette, U. Zabel, R.J. Weinberg, H.H.H.W. Schmidt, and J.G. Valtschanoff Synaptic localization of nitric oxide synthase-I and soluble guanylyl cyclase in the hippocampus J. Neurosci. 22 2002 8961 8970
13. S. Choi, J. Klingauf, and R.W. Tsien Fusion pore modulation as a presynaptic mechanism contributing to expression of long-term potentiation Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 2003 695 705
14. S. Cohen-Cory The developing synapse: construction and modulation of synaptic structures and circuits Science 298 2002 770 776
15. J. DeVente, J.G.J.M. Bol, L. Hudson, J. Schipper, and H.W.M. Steinbusch Atrial natriuretic factor-responding and cyclic guanosine monophosphate (cGMP)-producing cells in the rat hippocampus: A combined micropharmacological and immunocytochemical approach Brain Res. 446 1988 387 395
16. J.L. Dinerman, T.M. Dawson, M.J. Schell, A. Snowman, and S.H. Snyder Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: Implications for synaptic plasticity Proc. Natl. Acad. Sci. USA 91 1994 4214 4218
17. F. Engert, and T. Bonhoeffer Dendritic spine changes associated with hippocampal long-term synaptic plasticity Nature 399 1999 66 70
18. S. Etienne-Manneville, and A. Hall Rho GTPases in cell biology Nature 420 2002 629 635
19. R. Feil, J. Hartmann, C. Luo, W. Wolfsgruber, K. Schilling, S. Feil, J.J. Barski, M. Meyer, A. Konnerth, C.I. De Zeeuw, and F. Hofmann Impairmaent of LTD and cerebellar learning by Purkinje cell-specific ablation of cGMP-dependent protein kinase I J. Cell Biol. 163 2003 295 302
20. U. Frey, and R.G. Morris Synaptic tagging and long-term potentiation Nature 385 1997 533 536
21. H.V. Friedman, T. Bresler, C.C. Garner, and N.E. Ziv Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment Neuron 27 2000 57 69
22. Y. Fukata, M. Amano, and K. Kaibuchi Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells Trends Pharmacol. Sci. 22 2001 32 39
23. Y. Fukazawa, Y. Saitoh, F. Ozawa, Y. Ohta, K. Mizuno, and K. Inokuchi Hippocampal LTP is accompanied by enhanced F-actin content within the dendrite spine that is essential for late LTP maintenance in vivo Neuron 38 2003 447 460
24. O. Geneste, J.W. Copeland, and R. Treisman LIM kinase and Diaphanous cooperate to regulate serum response factor and actin dynamics J. Cell Biol. 157 2002 831 838
25. R. Grosse, J.W. Copeland, T.P. Newsome, M. Way, and R. Treisman A role for VASP in RhoA-Diaphanous signaling to actin dynamics and SRF activity EMBO J. 22 2003 3050 3061
26. T. Gudi, J.C. Chen, D.E. Casteel, T.M. Seasholtz, G.R. Boss, and R.B. Pilz cGMP-dependent protein kinase inhibits serum-response element-dependent transcription by inhibiting rho activation and functions J. Biol. Chem. 277 2002 37382 37393
27. J.E. Haley, G.L. Wilcox, and P.F. Chapman The role of nitric oxide in hippocampal long-term potentiation Neuron 8 1992 211 216
28. R.D. Hawkins NO honey, I don't remember Neuron 16 1996 465 467
29. R.D. Hawkins, H. Son, and O. Arancio Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus Prog. Brain Res. 118 1998 166 172
30. T.C. He, S. Zhuo, L.T. da Costa, J. Yu, K.W. Kinzler, and B. Vogelstein A simplified system for generating recombinant adenoviruses Proc. Natl. Acad. Sci. USA 95 1998 2509 2514
31. S. Hindley, B.H. Juurlink, J.W. Gysberg, P.J. Middlemiss, M.A. Herman, and M.P. Rathbone Nitric oxide donors enhance neutrophin-induced neurite outgrowth through a cGMP-dependent mechanism J. Neurosci. Res. 47 1997 427 439
32. S.H. Kim, and J.E. Lisman A role of actin filament in synaptic transmission and long-term potentiation J. Neurosci. 19 1999 4314 4324
33. P.A. Kingston, F. Zufall, and C.T. Barnstable Rat hippocampal neurons express genes for both rod retinal and olfactory cyclic nucleotide-gated channels: Novel targets for cAMP/cGMP function Proc. Natl. Acad. Sci. USA 93 1996 10440 10445
34. T. Kleppisch, A. Pfeifer, P. Kaltt, P. Rutyh, A. Montkowski, R. Fassler, and F. Hofmann Long-term potentiation in the hippocampal CA1 region of mice lacking cGMP-dependent protein kinases is normal and susceptible to inhibition of nitric oxide synthesis J. Neurosci. 19 1999 48 55
35. T. Kleppisch, W. Wolfsgruber, S. Feil, R. Allmann, C.T. Wotjak, S. Goebbels, K.-A. Nare, F. Hofmann, and R. Feil Hippocampal cGMP-dependent protein kinase I supports an age- and protein synthesis-dependent component of long-term potentiation but is not essential for spatial reference and contextual memory J. Neurosci. 23 2003 6005 6013
36. C.A. Korey, and D.V. Van Vactor From the growth cone surface to the cytoskeleton: one journey, many paths J. Neurobiol. 44 2000 184 193
37. T. Krucker, G.R. Siggins, and S. Halpain Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus Proc. Natl. Acad. Sci. USA 97 2000 6856 6861
38. A.V. Kwiatkowski, F.B. Gertler, and J.J. Loureiro Function and regulation of Ena/VASP proteins Trends Cell Biol. 13 2003 386 392
39. R. Lamprecht, C.R. Farb, and J.E. LeDoux Fear memory formation involves p190 RhoGAP and ROCK proteins through a GRB2-mediated complex Neuron 36 2002 727 738
40. C.A. Leamy, C.L. Ho-Pao, and M. Sur Disruption of retinogeniculate pattern formation by inhibition of soluble guanylyl cyclase J. Neurosci. 21 2001 3871 3880
41. C. Lebrand, E.W. Dent, G.A. Strasser, L.M. Lanier, M. Krause, T.M. Svitkina, G.G. Borisy, and F.B. Gertler Critical role of Ena/Vasp proteins for filopodia formation in neurons and in function downstream of netrin-1 Neuron 42 2004 37 49
42. Y.-F. Lu, and R.D. Hawkins Ryanodine receptors contribute to cGMP-induced late-phase LTP and CREB phosphorylation in the hippocampus J. Neurophysiol. 88 2002 1270 1278
43. Y.-F. Lu, E.R. Kandel, and R.D. Hawkins Nitric oxide signaling contributes to late-phase LTP and CREB phosphorylation in the hippocampus J. Neurosci. 23 1999 10250 10261
44. L. Luo Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity Annu. Rev. Cell Dev. Biol. 18 2002 601 635
45. C. Luscher, R.A. Nicoll, R.C. Malenka, and D. Muller Synaptic plasticity and dynamic modulation of the postsynaptic membrane Nat. Neurosci. 3 2000 545 550
46. M. Maletic-Savatic, R. Malinow, and K. Svoboda Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity Science 283 1999 1923 1927
47. A. Malgaroli, and R.W. Tsien Glutamate-induced long-term potentiation of the frequency of miniature synaptic currents in cultured hippocampal neurons Nature 357 1992 134 139
48. R. Malinow, and R.C. Malenka AMPA receptor trafficking and synaptic plasticity Annu. Rev. Neurosci. 25 2002 103 126
49. T. Markert, A.B. Vaandrager, S. Gambaryan, D. Pohler, C. Hausler, U. Walter, H.R. De Jonge, T. Jarchau, and S.M. Lohmann Endogenous expression of type II cGMP-dependent protein kinase mRNA and protein in rat intestine. Implications for cystic fibrosis transmembrane conductance regulator J. Clin. Invest. 96 1995 822 830
50. J. Matsuoka, G. Guili, M. Poyard, D. Stengel, J. Parma, G. Guellaen, and J. Hanoune Localization of adenylyl and guanylyl cyclase in rat brain by in situ hybridization: Comparison with calmodulin mRNA distribution J. Neurosci. 12 1992 3350 3360
51. M. Matsuzaki, N. Honkura, G.C.R. Ellis-Davies, and H. Kasai Structural basis of long-term potentiation in single dendritic spines Nature 429 2004 761 766
52. K.D. Micheva, J. Buchanan, R.W. Holz, and S.J. Smith Retrograde regulation of synaptic vesicle endocytosis and recycling Nat. Neurosci. 6 2003 925 932
53. P. Montfort, M.D. Munoz, E. Kusenko, and V. Felipo Long-term potentiation in hippocampus involves sequential activation of soluble guanylate cyclase, cGMP-dependent protein kinase, and cGMP-degrading phosphodiesterase J. Neurosci. 22 2002 10116 10122
54. A.Y. Nakayama, M.B. Harms, and L. Luo Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons J. Neurosci. 20 2000 5329 5338
55. I. Nikonenko, P. Jourdain, and D. Muller Presynaptic remodeling contributes to activity-dependent synaptogenesis J. Neurosci. 24 2003 8498 8505
56. I. Ninan, and O. Arancio Presynaptic CamkII is necessary for synaptic plasticity in cultured hippocampal neurons Neuron 42 2004 129 141
57. 2+ channels sets the polarity of nerve growth-cone turning Nature 423 2003 990 995
58. T.J. O'Dell, R.D. Hawkins, E.R. Kandel, and O. Arancio Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger Proc. Natl. Acad. Sci. USA 88 1991 11285 11289
59. V. Petit, and J.-P. Thiery Focal adhesions: structure and dynamics Biol. Cell. 92 2000 477 494
60. G. Pfitzer Invited review: regulation of myosin phosphorylation in smooth muscle J. Appl. Physiol. 91 2001 497 503
61. S. Popov, and M.-M. Poo Diffusional transport of macromolecules in developing nerve processes J. Neurosci. 12 1992 77 85
62. A. Rao, and A.M. Craig Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons Neuron 19 1997 801 812
63. M. Reinhard, T. Jarchau, and U. Walter Actin-based motility: stop and go with Ena/VASP proteins Trends Biochem. Sci. 26 2001 243 249
64. M. Russwurmm, N. Wittau, and D. Koesling Guanylyl cyclase/PSD-95 interaction: targeting of the nitric oxide-sensitive alpha2beta1 guanylyl cyclase to synaptic membranes J. Biol. Chem. 276 2001 44647 44652
65. J.R. Sanes, and J.W. Lichtman Development of the vertebrate neuromuscular junction Annu. Rev. Neurosci. 22 1999 389 442
66. V. Sauzeau, H. LeJeune, C. Cari-Toumaniantz, A. Smolenski, S.M. Lohmann, J. Bertoglio, P. Chardin, P. Pacaud, and G. Loirand Cyclic GMP-dependent protein kinase signaling pathway inhibits Rho A-induced Ca2+ sensitization of contraction in vascular smooth muscle J. Biol. Chem. 275 2000 21722 21729
67. P. Scheiffele Cell-cell signaling during synapse formation in the CNS Annu. Rev. Neurosci. 26 2003 485 508
68. H. Schmidt, M. Werner, P.A. Heppenstall, M. Henning, M.I. Moré, S. Kuhbandner, G.R. Lewin, F. Hofmann, R. Feil, and F.G. Rathjen cGMP-mediated signaling via cGKIα is required for the guidance and connectivity of sensory axons J. Cell Biol. 159 2002 489 498
69. W.C. Sin, K. Hass, E.S. Rothazer, and H.T. Cline Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases Nature 419 2002 475 480
70. A. Smolenski, C. Bachmann, K. Reinhard, P. Honig-Liedl, T. Jarchau, H. Hoschuetzky, and U. Walter Analysis and regulation of vasodilator-stimulated phosphoprotein serine 239 phosphorylation in vitro and in intact cells using a phosphospecific monoclonal antibody J. Biol. Chem. 273 1998 20029 20035
71. A. Smolenski, W. Poller, U. Walter, and S.M. Lohmann Regulation of human endothelial cell focal adhesion sites and migration of cGMP-dependent protein kinase I J. Cell Biol. 275 2000 25723 25732
72. H. Son, Y.-F. Lu, M. Zhuo, O. Arancio, E.R. Kandel, and R.D. Hawkins The specific role of cGMP in hippocampal LTP Learn. Mem. 5 1998 231 245
73. P.K. Stanton, J. Winterer, C.P. Bailey, A. Kyrozis, I. Raginov, G. Laube, R.W. Veh, C.Q. Nguyen, and W. Muller Long-term depression of presynaptic release from the readily releasable vesicle pool induced by NMDA receptor-dependent retrograde nitric oxide J. Neurosci. 23 2003 5936 5944
74. J. Tanaka, M. Markerink-van Ittersum, H.W. Steinbusch, and J. de Vente Nitric oxide-mediated cGMP synthesis in oligodendrocytes in the developing rat brain Glia 19 1997 286 297
75. N. Toni, P.A. Buchs, I. Nikonenko, C.R. Bron, and D. Muller LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite Nature 402 1999 421 425
76. S. Van Wagenen, and V. Rehder Regulation of neuronal growth cone filopodia by nitric oxide J. Neurobiol. 39 1999 168 185
77. A. Verma, D.J. Hrisch, C.E. Glatt, G.V. Ronnett, and S.H. Snyder Carbon monoxide: A putative neural messenger Science 259 1993 381 384
78. B. Wendland, F.E. Schweizer, T.A. Ryan, M. Nakane, F. Murad, R.H. Scheller, and R.W. Tsein Existence of nitric oxide synthase in rat hippocampal pyramidal cells Proc. Natl. Acad. Sci. USA 91 1994 2151 2155
79. S. Zhuang, G.T. Nguyen, Y. Chen, T. Gudi, M. Eigenthaler, T. Jarchau, U. Walter, G.R. Boss, and R.B. Pilz Vasodilator-stimulated phosphoptotein activation of serum-response element-dependent transcription occurs downstream of RhoA and is inhibited by cGMP-dependent protein kinase phosphorylation J. Biol. Chem. 279 2004 10397 10407
80. M. Zhuo, Y. Hu, C. Schultz, E.R. Kandel, and R.D. Hawkins Role of guanylyl cyclase and cGMP-dependent protein kinase in long-term potentiation Nature 368 1994 635 639