Rapid assembly of functional presynaptic boutons triggered by adhesive contacts

Journal of Neuroscience

Volumn 29, Issue 40, 2009, Pages 12449-12466

  Lucido, Anna Lisa ^a,b   Sanchez, Fernando Suarez ^b   Thostrup, Peter ^b   Kwiatkowski, Adam V ^c   Leal Ortiz, Sergio ^c   Gopalakrishnan, Gopakumar ^a,b   Liazoghli, Dalinda ^a,b   Belkaid, Wiam ^a,b   Lennox, R Bruce ^b   Grutter, Peter ^b   Garner, Craig C ^c   Colman, David R ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLY DEXTRO LYSINE; POLYPEPTIDE; PROTEOHEPARAN SULFATE;

ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRICITY; NERVE CONDUCTION; NERVE FIBER; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SYNAPSE VESICLE;

ANIMALS; AXONS; CELL ADHESION; CELLS, CULTURED; HIPPOCAMPUS; MEMBRANE PROTEINS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, CONFOCAL; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC VESICLES;

EID: 70349883839     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1381-09.2009     Document Type: Article

References (94)

1. Ahmari SE, Buchanan J, Smith SJ (2000) Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3:445-451. (Pubitemid 30495625)
2. Bandtlow CE, Zimmermann DR (2000) Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol Rev 80:1267-1290.
3. Banker G, Goslin K (1998) Culturing nerve cells, Ed 2. Cambridge, MA: MIT.
4. Benson DL, Tanaka H (1998) N-Cadherin redistribution during synaptogenesis in hippocampal neurons. J Neurosci 18:6892-6904.
5. Biederer T, Sara Y, Mozhayeva M, Atasoy D, Liu X, Kavalali ET, Südhof TC (2002) SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297:1525-1531. (Pubitemid 34970994)
6. Bogdanik L, Framery B, Frölich A, Franco B, Mornet D, Bockaert J, Sigrist SJ, Grau Y, Parmentier ML (2008) Muscle dystroglycan organizes the postsynapse and regulates presynaptic neurotransmitter release at the Drosophila neuromuscular junction. PLoS One 3:e2084.
7. Burry RW (1980) Formation of apparent presynaptic elements in response to poly-basic compounds. Brain Res 184:85-98.
8. Burry RW (1982) Development of apparent presynaptic elements formed in response to polylysine coated surfaces. Brain Res 247:1-16.
9. Burry RW (1983) Postnatal rat neurons form apparent presynaptic elements on polylysine-coated beads in vivo. Brain Res 278:236-239.
10. Burry RW (1985) Protein synthesis requirement for the formation of synaptic elements. Brain Res 344:109-119. (Pubitemid 15245109)
11. Cardin AD, Weintraub HJ (1989) Molecular modeling of protein- glycosaminoglycan interactions. Arteriosclerosis 9:21-32.
12. Chang HC, Samaniego F, Nair BC, Buonaguro L, Ensoli B (1997) HIV-1 Tat protein exits from cells via a leaderless secretory pathway and binds to extracellular matrix-associated heparan sulfate proteoglycans through its basic region. AIDS 11:1421-1431. (Pubitemid 27421173)
13. Changeux JP, Danchin A (1976) Selective stabilization of developing synapses as a mechanism for the specification of neuronal networks. Nature 264:705-712.
14. Chih B, Engelman H, Scheiffele P (2005) Control of excitatory and inhibitory synapse formation by neuroligins. Science 307:1324-1328. (Pubitemid 40299984)
15. Christopherson KS, Ullian EM, Stokes CC, Mullowney CE, Hell JW, Agah A, Lawler J, Mosher DF, Bornstein P, Barres BA (2005) Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120:421-433. (Pubitemid 40222435)
16. Cingolani LA, Goda Y (2008) Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat Rev Neurosci 9:344-356.
17. Colicos MA, Collins BE, Sailor MJ, Goda Y (2001) Remodeling of synaptic actin induced by photoconductive stimulation. Cell 107:605-616.
18. Dalva MB, McClelland AC, Kayser MS (2007) Cell adhesion molecules: signaling functions at the synapse. Nat Rev Neurosci 8:206-220. (Pubitemid 46294663)
19. Dean C, Scholl FG, Choih J, DeMaria S, Berger J, Isacoff E, Scheiffele P (2003) Neurexin mediates the assembly of presynaptic terminals. Nat Neurosci 6:708-716. (Pubitemid 36792885)
20. de Wit J, Verhaagen J (2007) Proteoglycans as modulators of axon guidance cue function. In: Semaphorins: receptor and intracellular signaling mechanisms (Pasterkamp RJ, ed), pp 73-89. Berlin: Springer.
21. Dillon C, Goda Y (2005) The actin cytoskeleton: integrating form and function at the synapse. Annu Rev Neurosci 28:25-55. (Pubitemid 41098898)
22. Dityatev A, Schachner M (2006) The extracellular matrix and synapses. Cell Tissue Res 326:647-654.
23. Dityatev A, Dityateva G, Sytnyk V, Delling M, Toni N, Nikonenko I, Muller D, Schachner M (2004) Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses. J Neurosci 24:9372-9382. (Pubitemid 39426174)
24. Dow KE, Mirski SE, Roder JC, Riopelle RJ (1988) Neuronal proteoglycans: biosynthesis and functional interaction with neurons in vitro. J Neurosci 8:3278-3289.
25. Dudanova I, Tabuchi K, Rohlmann A, Südhof TC, Missler M (2007) Deletion of alpha-neurexins does not cause a major impairment of axonal pathfinding or synapse formation. J Comp Neurol 502:261-274. (Pubitemid 46595398)
26. Ethell IM, Yamaguchi Y (1999) Cell surface heparan sulfate proteoglycan syndecan-2 induces the maturation of dendritic spines in rat hippocampal neurons. J Cell Biol 144:575-586.
27. Ethell IM, Irie F, Kalo MS, Couchman JR, Pasquale EB, Yamaguchi Y (2001) EphB/Syndecan-2 signaling in dendritic spine morphogenesis. Neuron 31:1001-1013. (Pubitemid 32925285)
28. Fannon AM, Colman DR (1996) A model for central synaptic junctional complex formation based on the differential adhesive specificities of the cadherins. Neuron 17:423-434.
29. Fox MA, Sanes JR, Borza D-B, Eswarakumar VP, Fässler R, Hudson BG, John SWM, Ninomiya Y, Pedchenko V, Pfaff SL, Rheault MN, Sado Y, Segal Y, Werle MJ, Umemori H (2007) Distinct target-derived signals organize formation, maturation, and maintenance of motor nerve terminals. Cell 129:179-193. (Pubitemid 46507579)
30. Friedman HV, Bresler T, Garner CC, Ziv NE (2000) Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27:57-69.
31. Fujita E, Kouroku Y, Ozeki S, Tanabe Y, Toyama Y, Maekawa M, Kojima N, Senoo H, Toshimori K, Momoi T (2006) Oligo-astheno-teratozoospermia in mice lacking RA175/TSLC1/SynCAM/IGSF4A, a cell adhesion molecule in the immunoglobulin superfamily. Mol Cell Biol 26:718-726. (Pubitemid 43089781)
32. Gallagher JT, Lyon M, Steward WP (1986) Structure and function of heparan sulfate proteoglycans. Biochem J 236:313-325. (Pubitemid 16036974)
33. Gautam M, Noakes PG, Moscoso L, Rupp F, Scheller RH, Merlie JP, Sanes JR (1996) Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85:525-535. (Pubitemid 26157191)
34. Gerrow K, Romorini S, Nabi SM, Colicos MA, Sala C, El-Husseini A (2006) A preformed complex of postsynaptic proteins is involved in excitatory synapse development. Neuron 49:547-562. (Pubitemid 43221890)
35. Graf ER, Zhang X, Jin SX, Linhoff MW, Craig AM (2004) Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119:1013-1026. (Pubitemid 40037614)
36. Hall AC, Lucas FR, Salinas PC (2000) Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100:525-535.
37. Haydon PG, Zoran MJ (1989) Formation and modulation of chemical connections: evoked acetylcholine release from growth cones and neurites of specific identified neurons. Neuron 2:1483-1490.
38. Henkemeyer M, Itkis OS, Ngo M, Hickmott PW, Ethell IM (2003) Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J Cell Biol 163:1313-1326. (Pubitemid 38032092)
39. Hsueh YP, Sheng M (1999) Regulated expression and subcellular localization of syndecan heparan sulfate proteoglycans and the syndecan-binding protein CASK/LIN-2 during rat brain development. J Neurosci 19:7415-7425.
40. Hsueh YP, Yang FC, Kharazia V, Naisbitt S, Cohen AR, Weinberg RJ, Sheng M (1998) Direct interaction of CASK/LIN-2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. J Cell Biol 142:139-151. (Pubitemid 28341146)
41. Jacobson M, Baker RE (1968) Neuronal specification of cutaneous nerves through connections with skin grafts. Science 160:543-545.
42. Jin Y, Garner CC (2008) Molecular mechanisms of presynaptic differentiation. Annu Rev Cell Dev Biol 24:237-262.
43. Johnson KG, Tenney AP, Ghose A, Duckworth AM, Higashi ME, Parfitt K, Marcu O, Heslip TR, Marsh JL, Schwarz TL, Flanagan JG, Van Vactor D (2006) The HSPGs syndecan and dallylike bind the receptor phosphatase LAR and exert distinct effects on synaptic development. Neuron 49:517-531. (Pubitemid 43221888)
44. Jontes JD, Phillips GR (2006) Selective stabilization and synaptic specificity: a new cell-biological model. Trends Neurosci 29:186-191.
45. Jontes JD, Buchanan J, Smith SJ (2000) Growth cone and dendrite dynamics in zebrafish embryos: early events in synaptogenesis imaged in vivo. Nat Neurosci 3:231-237. (Pubitemid 30140784)
46. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
47. Kayser MS, McClelland AC, Hughes EG, Dalva MB (2006) Intracellular and trans-synaptic regulation of glutamatergic synaptogenesis by EphB receptors. J Neurosci 26:12152-12164.
48. Kim E, Sheng M (2004) PDZ domain proteins of synapses. Nat Rev Neurosci 5:771-781.
49. Kim S, Burette A, Chung HS, Kwon SK, Woo J, Lee HW, Kim K, Kim H, Weinberg RJ, Kim E (2006) NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nat Neurosci 9:1294-1301. (Pubitemid 44454271)
50. Kleene R, Schachner M (2004) Glycans and neural cell interactions. Nat Rev Neurosci 5:195-208.
51. Ko J, Kim S, Chung HS, Kim K, Han K, Kim H, Jun H, Kaang BK, Kim E (2006) SALM Synaptic cell adhesion-like molecules regulate the differentiation of excitatory synapses. Neuron 50:233-245.
52. Krueger SR, Kolar A, Fitzsimonds RM (2003) The presynaptic release apparatus is functional in the absence of dendritic contact and highly mobile within isolated axons. Neuron 40:945-957. (Pubitemid 37522052)
53. Kwiatkowski AV, Rubinson DA, Dent EW, Edward van Veen J, Leslie JD, Zhang J, Mebane LM, Philippar U, Pinheiro EM, Burds AA, Bronson RT, Mori S, Fässler R, Gertler FB (2007) Ena/VASP is required for neuritogenesis in the developing cortex. Neuron 56:441-455. (Pubitemid 350030877)
54. Kwiatkowski AV, Garner CC, Nelson WJ, Gertler FB (2009) Cell autonomous defects in cortical development revealed by two-color chimera analysis. Mol Cell Neurosci 41:44-50.
55. Lauri SE, Kaukinen S, Kinnunen T, Ylinen A, Imai S, Kaila K, Taira T, Rauvala H (1999) Regulatory role and molecular interactions of a cell-surface heparan sulfate proteoglycan (N-syndecan) in hippocampal long-term potentiation. J Neurosci 19:1226-1235. (Pubitemid 29088905)
56. Leal-Ortiz S, Waites CL, Terry-Lorenzo R, Zamorano P, Gundelfinger ED, Garner CC (2008) Piccolo modulation of Synapsin1a dynamics regulates synaptic vesicle exocytosis. J Cell Biol 181:831-846. (Pubitemid 351786987)
57. Ledda F, Paratcha G, Sandoval-Guzmán T, Ibáñez CF (2007) GDNF and GFRα1 promote formation of neuronal synapses by ligand-induced cell adhesion. Nat Neurosci 10:293-300. (Pubitemid 46310474)
58. Li Q, Lau A, Morris TJ, Guo L, Fordyce CB, Stanley EF (2004) A syntaxin 1, Gαo, and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J Neurosci 24:4070-4081. (Pubitemid 38544233)
59. Matsumoto Y, Irie F, Inatani M, Tessier-Lavigne M, Yamaguchi Y (2007) Netrin-1/DCC signaling in commissural axon guidance requires cell-autonomous expression of heparan sulfate. J Neurosci 27:4342-4350. (Pubitemid 46640711)
60. Mislick KA, Baldeschwieler JD (1996) Evidence for a role of proteoglycans in cation-mediated gene transfer. Proc Natl Acad Sci U S A 93:12349-12354. (Pubitemid 26367146)
61. 2+ channels to synaptic vesicle exocytosis. Nature 423:939-948.
62. Nakase I, Tadokoro A, Kawabata N, Takeuchi T, Katoh H, Hiramoto K, Negishi M, Nomizu M, Sugiura Y, Futaki S (2007) Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin reorganization and macropinocytosis. Biochemistry 46:492-501. (Pubitemid 46105438)
63. Noakes PG, Gautam M, Mudd J, Sanes JR, Merlie JP (1995) Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin [beta]2. Nature 374:258-262.
64. Okabe S (2007) Molecular anatomy of the postsynaptic density. Mol Cell Neurosci 34:503-518.
65. Okabe S, Miwa A, Okado H (2001) Spine formation and correlated assembly of presynaptic and postsynaptic molecules. J Neurosci 21:6105-6114. (Pubitemid 32743148)
66. Peng HB, Markey DR, Muhlach WL, Pollack ED (1987) Development of presynaptic specializations induced by basic polypeptide-coated latex beads in spinal cord cultures. Synapse 1:10-19.
67. Phillips GR, Huang JK, Wang Y, Tanaka H, Shapiro L, Zhang W, Shan WS, Arndt K, Frank M, Gordon RE, Gawinowicz MA, Zhao Y, Colman DR (2001) The presynaptic particle web: ultrastructure, composition, dissolution and reconstitution. Neuron 32:63-77. (Pubitemid 32995890)
68. Rauvala H, Peng HB (1997) HB-GAM(Heparin-binding growth-associated molecule) and heparin-type glycans in the development and plasticity of neuron-target contacts. Prog Neurobiol 52:127-144. (Pubitemid 27242703)
69. Ryan TA, Reuter H, Wendland B, Schweizer FE, Tsien RW, Smith SJ (1993) The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron 11:713-724. (Pubitemid 23321779)
70. Sankaranarayanan S, Atluri PP, Ryan TA (2003) Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat Neurosci 6:127-135. (Pubitemid 36182781)
71. Sara Y, Biederer T, Atasoy D, Chubykin A, Mozhayeva MG, Südhof TC, Kavalali ET (2005) Selective capability of synCAM and neuroligin for functional synapse assembly. J Neurosci 25:260-270. (Pubitemid 40110789)
72. Sato S, Omori Y, Katoh K, Kondo M, Kanagawa M, Miyata K, Funabiki K, Koyasu T, Kajimura N, Miyoshi T, Sawai H, Kobayashi K, Tani A, Toda T, Usukura J, Tano Y, Fujikado T, Furukawa T (2008) Pikachurin, a dystroglycan ligand, is essential for photoreceptor ribbon synapse formation. Nat Neurosci 11:923-931.
73. Schacher S, Rayport SG, Ambron RT (1985) Giant Aplysia neuron R2 reliably forms strong chemical connections in vitro. J Neurosci 5:2851-2856. (Pubitemid 16225483)
74. Scheiffele P, Fan J, Choih J, Fetter R, Serafini T (2000) Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101:657-669.
75. Schlüter OM, Xu W, Malenka RC (2006) Alternative N-terminal domains of PSD-95 and SAP97 govern activity-dependent regulation of synaptic AMPA receptor function. Neuron 51:99-111. (Pubitemid 43963332)
76. Shapira M, Zhai RG, Dresbach T, Bresler T, Torres VI, Gundelfinger ED, Ziv NE, Garner CC (2003) Unitary assembly of presynaptic active zones from piccolo-bassoon transport vesicles. Neuron 38:237-252. (Pubitemid 36555650)
77. Shapiro L, Love J, Colman DR (2007) Adhesion molecules in the nervous system: Structural insights into function and diversity. Annu Rev Neurosci 30:451-474. (Pubitemid 47218764)
78. Spector I, Braet F, Shochet NR, Bubb MR (1999) New anti-actin drugs in the study of the organization and function of the actin cytoskeleton. Microsc Res Tech 47:18-37. (Pubitemid 29474832)
79. Sperry RW (1963) Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc Natl Acad Sci U S A 50:703-710.
80. Sugiura M, Dow KE (1994) Activity-dependent regulation of neuronal synthesis and release of neurite-promoting heparan sulfate proteoglycans. Dev Biol 164:102-110. (Pubitemid 24234338)
81. Sur M, Garraghty PE, Roe AW (1988) Experimentally induced visual projections into auditory thalamus and cortex. Science 242:1437-1441. (Pubitemid 19008073)
82. Tsuriel S, Geva R, Zamorano P, Dresbach T, Boeckers T, Gundelfinger ED, Garner CC, Ziv NE (2006) Local sharing as a predominant determinant of synaptic matrix molecular dynamics. PLoS Biol 4:e271.
83. Ullian EM, Sapperstein SK, Christopherson KS, Barres BA (2001) Control of synapse number by glia. Science 291:657-661.
84. Umemori H, Linhoff MW, Ornitz DM, Sanes JR (2004) FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 118:257-270. (Pubitemid 38962580)
85. van der Weyden L, Arends MJ, Chausiaux OE, Ellis PJ, Lange UC, Surani MA, Affara N, Murakami Y, Adams DJ, Bradley A (2006) Loss of TSLC1 causes male infertility due to a defect at the spermatid stage of spermatogenesis. Mol Cell Biol 26:3595-3609.
86. Van Vactor D, Wall DP, Johnson KG (2006) Heparan sulfate proteoglycans and the emergence of neuronal connectivity. Curr Opin Neurobiol 16:40-51. (Pubitemid 43221852)
87. Varoqueaux F, Aramuni G, Rawson RL, Mohrmann R, Missler M, Gottmann K, Zhang W, Südhof TC, Brose N (2006) Neuroligins determine synapse maturation and function. Neuron 51:741-754. (Pubitemid 44374915)
88. Waites CL, Specht CG, Härtel K, Leal-Ortiz S, Genoux D, Li D, Drisdel RC, Jeyifous O, Cheyne JE, Green WN, Montgomery JM, Garner CC (2009) Synaptic SAP97 isoforms regulate AMPA receptor dynamics and access to presynaptic glutamate. J Neurosci 29:4332-4345.
89. Webb SJ, Monk CS, Nelson CA (2001) Mechanisms of postnatal neurobiological development: implications for human development. Dev Neuropsychol 19:147-171. (Pubitemid 32845926)
90. Withers GS, Higgins D, Charette M, Banker G (2000) Bone morphogenetic protein-7 enhances dendritic growth and receptivity to innervation in cultured hippocampal neurons. Eur J Neurosci 12:106-116. (Pubitemid 30068416)
91. Yavin E, Yavin Z (1974) Attachment and culture of dissociated cells from rat embryo cerebral hemispheres on polylysine-coated surface. J Cell Biol 62:540-546.
92. Zhang W, Benson DL (2001) Stages of synapse development defined by dependence on F-actin. J Neurosci 21:5169-5181. (Pubitemid 32622942)
93. Zhang ZW (2006) Postnatal development of the mammalian neocortex: role of activity revisited. Can J Neurol Sci 33:158-169.
94. Zwimpfer TJ, Aguayo AJ, Bray GM (1992) Synapse formation and preferential distribution in the granule cell layer by regenerating retinal ganglion cell axons guided to the cerebellum of adult hamsters. J Neurosci 12:1144-1159.