The role of agrin in synaptic development, plasticity and signaling in the central nervous system

Neurochemistry International

Volumn 61, Issue 6, 2012, Pages 848-853

  Daniels, Mathew P ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Agrin; Brain; Filopodia; Synapse development; Synaptic activity; Synaptic plasticity

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AGRIN; ANTISENSE OLIGONUCLEOTIDE; BRAIN RECEPTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MUSCLE SPECIFIC RECEPTOR TYROSINE KINASE; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; BRAIN NERVE CELL; CARBOXY TERMINAL SEQUENCE; CENTRAL NERVOUS SYSTEM; CONFERENCE PAPER; DENDRITE; EMBRYO DEVELOPMENT; FILOPODIUM; HUMAN; MOTONEURON; NERVE CELL PLASTICITY; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; SYNAPTOGENESIS;

AGRIN; ANIMALS; CENTRAL NERVOUS SYSTEM; MICE; MICE, KNOCKOUT; NEURONAL PLASTICITY; SIGNAL TRANSDUCTION; SYNAPSES;

MUS;

EID: 84868205776     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2012.02.028     Document Type: Conference Paper

References (66)

1. M. Annies, G. Bittcher, R. Ramseger, J. Loschinger, S. Woll, E. Porten, C. Abraham, M.A. Ruegg, and S. Kroger Clustering transmembrane-agrin induces filopodia-like processes on axons and dendrites Mol. Cell. Neurosci. 31 2006 515 524
2. C.M. Bose, D. Qiu, A. Bergamaschi, B. Gravante, M. Bossi, A. Villa, F. Rupp, and A. Malgaroli Agrin controls synaptic differentiation in hippocampal neurons J. Neurosci. 20 2000 9086 9095
3. R.W. Burgess, Q.T. Nguyen, Y.-J. Son, J.W. Lichtman, and J.R. Sanes Alternatively spliced isoforms of nerve- and muscle-derived agrin: their roles at the neuromuscular junction Neuron 23 1999 33 44
4. R.W. Burgess, W.C. Skarnes, and J.R. Sanes Agrin isoforms with distinct amino termini: differential expression, localization, and function J. Cell Biol. 151 2000 41 52
5. G. Buzsaki Theta oscillations in the hippocampus Neuron 33 2002 325 340
6. T.M. DeChiara, D.C. Bowen, D.M. Valenzuela, M.V. Simmons, W.T. Poueymirou, S. Thomas, E. Kinetz, D.L. Compton, E. Rojas, J.S. Park, C. Smith, P.S. DiStefano, D.J. Glass, S.J. Burden, and G.D. Yancopoulos The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo Cell 85 1996 501 512
7. M. Ferns, W. Hoch, J.T. Campanelli, F. Rupp, Z.W. Hall, and R.H. Scheller RNA splicing regulates agrin-mediated acetylcholine receptor clustering activity on cultured myotubes Neuron 8 1992 1079 1086
8. A. Ferreira Abnormal synapse formation in agrin-depleted hippocampal neurons J. Cell Sci. 112 1999 4729 4738
9. R. Frischknecht, A. Fejtova, M. Viesti, A. Stephan, and P. Sonderegger Activity-induced synaptic capture and exocytosis of the neuronal serine protease neurotrypsin J. Neurosci. 28 2008 1568 1579
10. A. Garcia-Osta, P. Tsokas, G. Pollonini, M.L. Landau, R. Blitzer, and C.M. Alberini MuSK expressed in the brain mediates cholinergic responses, synaptic plasticity, and memory formation J. Neurosci. 26 2006 7919 7932
11. M. Gautam, P.G. Noakes, L. Moscoso, F. Rupp, R.H. Scheller, J.P. Merlie, and J.R. Sanes Defective neuromuscular synaptogenesis in agrin-deficient mutant mice Cell 85 1996 525 535
12. J. Gingras, and M. Ferns Expression and localization of agrin during sympathetic synapse formation in vitro J. Neurobiol. 48 2001 228 242
13. J. Gingras, S. Rassadi, E. Cooper, and M. Ferns Agrin plays an organizing role in the formation of sympathetic synapses J. Cell Biol. 158 2002 1109 1118
14. D.J. Glass, D.C. Bowen, T.N. Stitt, C. Radziejewski, J. Bruno, T.E. Ryan, D.R. Gies, S. Shah, K. Mattsson, S.J. Burden, P.S. DiStefano, D.M. Valenzuela, T.M. DeChiara, and G.D. Yancopoulos Agrin acts via a MuSK receptor complex Cell 85 1996 513 523
15. D.J. Glass, T.M. DeChiara, T.N. Stitt, P.S. DiStefano, D.M. Valenzuela, and G.D. Yancopoulos The receptor tyrosine kinase MuSK is required for neuromuscular junction formation and is a functional receptor for agrin Cold Spring Harb. Symp. Quant. Biol. 61 1996 435 444
16. E.W. Godfrey Comparison of agrin-like proteins from the extracellular matrix of chicken kidney and muscle with neural agrin, a synapse organizing protein Exp. Cell Res. 195 1991 99 109
17. E.W. Godfrey, R.M. Nitkin, B.G. Wallace, L.L. Rubin, and U.J. McMahan Components of Torpedo electric organ and muscle that cause aggregation of acetylcholine receptors on cultured muscle cells J. Cell Biol. 99 1984 615 627
18. A. Hall Rho GTPases and the actin cytoskeleton Science 279 1998 509 514
19. A. Hall Rho GTPases and the control of cell behaviour Biochem. Soc. Trans. 33 2005 891 895
20. L.G. Hilgenberg, C.L. Hoover, and M.A. Smith Evidence of an agrin receptor in cortical neurons J. Neurosci. 19 1999 7384 7393
21. L.G. Hilgenberg, K.D. Ho, D. Lee, D.K. O'Dowd, and M.A. Smith Agrin regulates neuronal responses to excitatory neurotransmitters in vitro and in vivo Mol. Cell. Neurosci. 19 2002 97 110
22. L.G.W. Hilgenberg, H. Su, H. Gu, D.K. O'Dowd, and M.A. Smith Alpha3Na+/K+-ATPase is a neuronal receptor for agrin Cell 125 2006 359 369
23. W. Hoch, M. Ferns, J.T. Campanelli, Z.W. Hall, and R.H. Scheller Developmental regulation of highly active alternatively spliced forms of agrin Neuron 11 1993 479 490
24. C.L. Hoover, L.G. Hilgenberg, and M.A. Smith The COOH-terminal domain of agrin signals via a synaptic receptor in central nervous system neurons J. Cell Biol. 161 2003 923 932
25. Y.-P. Hsueh, and M. Sheng Regulated expression and subcellular localization of syndecan heparan sulfate proteoglycans and the syndecan-binding protein CASK/LIN-2 during rat brain development J. Neurosci. 19 1999 7415 7425
26. E.P. Huang, and C.F. Stevens The matter of mind: molecular control of memory Essays Biochem. 33 1998 165 178
27. R.R. Ji, C.M. Bose, C. Lesuisse, D. Qiu, J.C. Huang, Q. Zhang, and F. Rupp Specific agrin isoforms induce cAMP response element binding protein phosphorylation in hippocampal neurons J. Neurosci. 18 1998 9695 9702
28. E.R. Kandel The molecular biology of memory storage: a dialogue between genes and synapses Science 294 2001 1030 1038
29. L. Karasewski, and A. Ferreira MAPK signal transduction pathway mediates agrin effects on neurite elongation in cultured hippocampal neurons J. Neurobiol. 55 2003 14 24
30. L. Kaczmarek Molecular biology of vertebrate learning: is c-fos a new beginning? J. Neurosci. Res. 34 1993 377 381
31. M.K. Kim, S.L. Cotman, W. Halfter, and G.J. Cole The heparan sulfate proteoglycan agrin modulates neurite outgrowth mediated by FGF-2 J. Neurobiol. 55 2003 261 277
32. N. Kim, A.L. Stiegler, T.O. Cameron, P.T. Hallock, A.M. Gomez, J.H. Huang, S.R. Hubbard, M.L. Dustin, and S.J. Burden Lrp4 is a receptor for agrin and forms a complex with MuSK Cell 135 2008 334 342
33. I. Ksiazek, C. Burkhardt, S. Lin, R. Seddik, M. Maj, G. Bezakova, M. Jucker, S. Arber, P. Caroni, J.R. Sanes, B. Bettler, and M.A. Ruegg Synapse loss in cortex of agrin-deficient mice after genetic rescue of perinatal death J. Neurosci. 27 2007 7183 7195
34. T.T. Kummer, T. Misgeld, and J.R. Sanes Assembly of the postsynaptic membrane at the neuromuscular junction: paradigm lost Curr. Opin. Neurobiol. 16 2006 74 82
35. Z. Li, J.L. Massengill, D.K. O'Dowd, and M.A. Smith Agrin gene expression in mouse somatosensory cortical neurons during development in vivo and in cell culture Neuroscience 79 1997 191 201
36. Z. Li, L.G. Hilgenberg, D.K. O'Dowd, and M.A. Smith Formation of functional synaptic connections between cultured cortical neurons from agrin-deficient mice J. Neurobiol. 39 1999 547 557
37. W. Lin, R.W. Burgess, B. Dominguez, S.L. Pfaff, J.R. Sanes, and K.F. Lee Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse Nature 410 2001 1057 1064
38. L. Lin, S. McCroskery, J.M. Ross, Y. Chak, B. Neuhuber, and M.P. Daniels Induction of filopodia-like protrusions by transmembrane agrin: role of agrin glycosaminoglycan chains and Rho-family GTPases Exp. Cell Res. 316 2010 2260 2277
39. E. Ma, R. Morgan, and E.W. Godfrey Distribution of agrin mRNAs in the chick embryo nervous system J. Neurosci. 14 1994 2943 2952
40. S. Mann, and S. Kroger Agrin is synthesized by retinal cells and colocalizes with gephyrin [corrected] Mol. Cell. Neurosci. 8 1996 1 13
41. K. Matsumoto-Miyai, E. Sokolowska, A. Zurlinden, C.E. Gee, D. Luscher, S. Hettwer, J. Wolfel, A.P. Ladner, J. Ster, U. Gerber, T. Rulicke, B. Kunz, and P. Sonderegger Coincident pre- and postsynaptic activation induces dendritic filopodia via neurotrypsin-dependent agrin cleavage Cell 136 2009 1161 1171
42. S. McCroskery, A. Chaudhry, L. Lin, and M.P. Daniels Transmembrane agrin regulates filopodia in rat hippocampal neurons in culture Mol. Cell. Neurosci. 33 2006 15 28
43. S. McCroskery, A. Bailey, L. Lin, and M.P. Daniels Transmembrane agrin regulates dendritic filopodia and synapse formation in mature hippocampal neuron cultures Neuroscience 163 2009 168 179
44. M.M. McKay, and D.K. Morrison Integrating signals from RTKs to ERK/MAPK Oncogene 26 2007 3113 3121
45. U.J. McMahan The agrin hypothesis Cold Spring Harb. Symp. Quant. Biol. 55 1990 407 418
46. F.R. Neumann, G. Bittcher, M. Annies, B. Schumacher, S. Kroger, and M.A. Ruegg An alternative amino-terminus expressed in the central nervous system converts agrin to a type II transmembrane protein Mol. Cell. Neurosci. 17 2001 208 225
47. L.T. O'Connor, J.C. Lauterborn, C.M. Gall, and M.A. Smith Localization and alternative splicing of agrin mRNA in adult rat brain: transcripts encoding isoforms that aggregate acetylcholine receptors are not restricted to cholinergic regions J. Neurosci. 14 1994 1141 1152
48. E. Porten, B. Seliger, V.A. Schneider, S. Woll, D. Stangel, R. Ramseger, and S. Kroger The process-inducing activity of transmembrane agrin requires follistatin-like domains J. Biol. Chem. 285 2010 3114 3125
49. R. Ramseger, R. White, and S. Kroger Transmembrane form agrin-induced process formation requires lipid rafts and the activation of Fyn and MAPK J. Biol. Chem. 284 2009 7697 7705
50. R. Reif, S. Sales, S. Hettwer, B. Dreier, C. Gisler, J. Wölfel, D. Lüscher, A. Zurlinden, A. Stephan, S. Ahmed, A. Baici, B. Ledermann, B. Kunz, and P. Sonderegger Specific cleavage of agrin by neurotrypsin, a synaptic protease linked to mental retardation FASEB J. 21 2007 3468 3478
51. A.J. Ridley Rho family proteins and regulation of the actin cytoskeleton Prog. Mol. Subcell. Biol. 22 1999 1 22
52. M. Rimer Emerging roles for MAP kinases in agrin signaling Commun. Integr. Biol. 4 2011 143 146
53. F. Rupp, D.G. Payan, C. Magill-Solc, D.M. Cowan, and R.H. Scheller Structure and expression of a rat agrin Neuron 6 1991 811 823
54. A.S. Serpinskaya, G. Feng, J.R. Sanes, and A.M. Craig Synapse formation by hippocampal neurons from agrin-deficient mice Dev. Biol. 205 1999 65 78
55. D.M. Stone, and K. Nikolics Tissue- and age-specific expression patterns of alternatively spliced agrin mRNA transcripts in embryonic rat suggest novel developmental roles J. Neurosci. 15 1995 6767 6778
56. A.J. Sytkowski, Z. Vogel, and M.W. Nirenberg Development of acetylcholine receptor clusters on cultured muscle cells Proc. Natl. Acad. Sci. USA 70 1973 270 274
57. H. Takahashi, Y. Sekino, S. Tanaka, T. Mizui, S. Kishi, and T. Shirao Drebrin-dependent actin clustering in dendritic filopodia governs synaptic targeting of postsynaptic density-95 and dendritic spine morphogenesis J. Neurosci. 23 2003 6586 6595
58. Q.-B. Tian, T. Suzuki, T. Yamauchi, H. Sakagami, Y. Yoshimura, S. Miyazawa, K. Nakayama, F. Saitoh, J.-P. Zhang, Y. Lu, H. Kondo, and S. Endo Interaction of LDL receptor-related protein 4 (LRP4) with post synaptic scaffold proteins via its C-terminal PDZ domain-binding motif, and its regulation by Ca2+/calmodulin-dependent protein kinase II Eur. J. Neurosci. 23 2006 2864 2876
59. K.W. Tsim, M.A. Ruegg, G. Escher, S. Kroger, and U.J. McMahan cDNA that encodes active agrin Neuron 8 1992 677 689
60. D.M. Valenzuela, T.N. Stitt, P.S. DiStefano, E. Rojas, K. Mattsson, D.L. Compton, L. Nunez, J.S. Park, J.L. Stark, and D.R. Gies Receptor tyrosine kinase specific for the skeletal muscle lineage: expression in embryonic muscle, at the neuromuscular junction, and after injury Neuron 15 1995 573 584
61. M. Weller, and R. Waltereit Signaling from cAMP/PKA to MAPK and synaptic plasticity Mol. Neurobiol. 27 2003 99 106
62. U. Winzen, G.J. Cole, and W. Halfter Agrin is a chimeric proteoglycan with the attachment sites for heparan sulfate/chondroitin sulfate located in two multiple serine-glycine clusters J. Biol. Chem. 278 2003 30106 30114
63. H. Wu, W.C. Xiong, and L. Mei To build a synapse: signaling pathways in neuromuscular junction assembly Development 137 2010 1017 1033
64. R. Yuste, and T. Bonhoeffer Genesis of dendritic spines: insights from ultrastructural and imaging studies Nat. Rev. Neurosci. 5 2004 24 34
65. B. Zhang, S. Luo, Q. Wang, T. Suzuki, W.C. Xiong, and L. Mei LRP4 serves as a co-receptor of agrin Neuron 60 2008 285 297
66. N.E. Ziv, and S.J. Smith Evidence for a role of dendritic filopodia in synaptogenesis and spine formation Neuron 17 1996 91 102