SynCAM 1 participates in axo-dendritic contact assembly and shapes neuronal growth cones

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 16, 2010, Pages 7568-7573

  Stagi, Massimiliano ^a   Fogel, Adam I ^a   Biederer, Thomas ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

CADM; Focal adhesion kinase; Growth cone; Synaptic adhesion; Synaptogenesis

Indexed keywords

ACTIN; BIOLOGICAL MARKER; CELL ADHESION MOLECULE; FOCAL ADHESION KINASE; IMMUNOGLOBULIN; MEMBRANE PROTEIN; NEUREXIN; NEUREXIN 1ALPHA; NEUREXIN 1BETA; NEUROLIGIN 1; NEUROMODULIN; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN SYNCAM 1; SYNAPTOPHYSIN; TALIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DENDRITE; FILOPODIUM; GROWTH CONE; MORPHOGENESIS; MORPHOLOGY; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN LOCALIZATION; RAT; REGULATORY MECHANISM; SYNAPTOGENESIS;

ANIMALS; AXONS; CELL ADHESION MOLECULES, NEURONAL; CELL DIFFERENTIATION; CELL MOVEMENT; DENDRITES; GROWTH CONES; HYDROGEN-ION CONCENTRATION; IMMUNOGLOBULINS; MEMBRANE PROTEINS; MICE; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; NEURONS; PROTEIN BINDING; RATS; TUMOR SUPPRESSOR PROTEINS;

EID: 77952117227     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0911798107     Document Type: Article

References (56)

1. Cooper MW, Smith SJ (1992) A real-time analysis of growth cone-target cell interactions during the formation of stable contacts between hippocampal neurons in culture. J Neurobiol 23:814-828.
2. Ziv NE, Smith SJ (1996) Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17:91-102.
3. Fiala JC, Feinberg M, Popov V, Harris KM (1998) Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci 18:8900-8911. (Pubitemid 28491754)
4. Rees RP, Bunge MB, Bunge RP (1976) Morphological changes in the neuritic growth cone and target neuron during synaptic junction development in culture. J Cell Biol 68:240-263.
5. Ahmari SE, Smith SJ (2002) Knowing a nascent synapse when you see it. Neuron 34:333-336. (Pubitemid 34465491)
6. Jin Y, Garner CC (2008) Molecular mechanisms of presynaptic differentiation. Annu Rev Cell Dev Biol 24:237-262.
7. Lowery LA, Van Vactor D (2009) The trip of the tip: Understanding the growth cone machinery. Nat Rev Mol Cell Biol 10:332-343.
8. Pak CW, Flynn KC, Bamburg JR (2008) Actin-binding proteins take the reins in growth cones. Nat Rev Neurosci 9:136-147.
9. Maness PF, Schachner M (2007) Neural recognition molecules of the immunoglobulin superfamily: Signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10:19-26.
10. Suter DM, Errante LD, Belotserkovsky V, Forscher P (1998) The Ig superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. J Cell Biol 141:227-240. (Pubitemid 28182654)
11. Dalva MB, McClelland AC, Kayser MS (2007) Cell adhesion molecules: Signalling functions at the synapse. Nat Rev Neurosci 8:206-220. (Pubitemid 46294663)
12. Biederer T, Stagi M (2008) Signaling by synaptogenic molecules. Curr Opin Neurobiol 18:261-269.
13. Arikkath J, Reichardt LF (2008) Cadherins and catenins at synapses: Roles in synaptogenesis and synaptic plasticity. Trends Neurosci 31:487-494.
14. Biederer T, et al. (2002) SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297:1525-1531. (Pubitemid 34970994)
15. Shingai T, et al. (2003) Implications of nectin-like molecule-2/IGSF4/ RA175/SgIGSF/TSLC1/SynCAM1 in cell-cell adhesion and transmembrane protein localization in epithelial cells. J Biol Chem 278:35421-35427. (Pubitemid 37102311)
16. Thomas LA, Akins MR, Biederer T (2008) Expression and adhesion profiles of SynCAM molecules indicate distinct neuronal functions. J Comp Neurol 510:47-67.
17. Fogel AI, et al. (2007) SynCAMs organize synapses through heterophilic adhesion. J Neurosci 27:12516-12530.
18. Kang Y, Zhang X, Dobie F, Wu H, Craig AM (2008) Induction of GABAergic postsynaptic differentiation by alpha-neurexins. J Biol Chem 283:2323-2334.
19. Song JY, Ichtchenko K, Südhof TC, Brose N (1999) Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc Natl Acad Sci USA 96:1100-1105. (Pubitemid 29072190)
20. Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454-1468.
21. Fujita E, et al. (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)
22. Nozumi M, et al. (2009) Identification of functional marker proteins in the mammalian growth cone. Proc Natl Acad Sci USA 106:17211-17216.
23. Miesenböck G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192-195. (Pubitemid 28325974)
24. Meyer MP, Smith SJ (2006) Evidence from in vivo imaging that synaptogenesis guides the growth and branching of axonal arbors by two distinct mechanisms. J Neurosci 26:3604-3614.
25. Ahmari SE, Buchanan J, Smith SJ (2000) Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3:445-451. (Pubitemid 30495625)
26. Anderson TR, Shah PA, Benson DL (2004) Maturation of glutamatergic and GABAergic synapse composition in hippocampal neurons. Neuropharmacology 47:694-705.
27. Sholl DA (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87:387-406.
28. Biederer T (2006) Bioinformatic characterization of the SynCAM family of immunoglobulin-like domain-containing adhesion molecules. Genomics 87:139-150.
29. Hoy J, Constable J, Vicini S, Fu Z, Washbourne P (2009) SynCAM1 recruits NMDA receptors via protein 4.1B. Mol Cell Neurosci vol42:466-483.
30. Diakowski W, Grzybek M, Sikorski AF (2006) Protein 4.1, a component of the erythrocyte membrane skeleton and its related homologue proteins forming the protein 4.1/FERM superfamily. Folia Histochem Cytobiol 44:231-248. (Pubitemid 44696964)
31. Chishti AH, et al. (1998) The FERM domain: A unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem Sci 23:281-282.
32. Burgaya F, Menegon A, Menegoz M, Valtorta F, Girault JA (1995) Focal adhesion kinase in rat central nervous system. Eur J Neurosci 7:1810-1821.
33. Chan KT, Cortesio CL, Huttenlocher A (2009) FAK alters invadopodia and focal adhesion composition and dynamics to regulate breast cancer invasion. J Cell Biol 185:357-370.
34. Robles E, Gomez TM (2006) Focal adhesion kinase signaling at sites of integrin-mediated adhesion controls axon pathfinding. Nat Neurosci 9:1274-1283. (Pubitemid 44454269)
35. Mitra SK, Hanson DA, Schlaepfer DD (2005) Focal adhesion kinase: In command and control of cell motility. Nat Rev Mol Cell Biol 6:56-68.
36. Parsons JT, Martin KH, Slack JK, Taylor JM, Weed SA (2000) Focal adhesion kinase: A regulator of focal adhesion dynamics and cell movement. Oncogene 19:5606-5613.
37. Richardson A, Parsons T (1996) A mechanism for regulation of the adhesion-associated proteintyrosine kinase pp125FAK. Nature 380:538-540. (Pubitemid 26110644)
38. SchallerMD, Borgman CA, Parsons JT (1993) Autonomous expression of a noncatalytic domain of the focal adhesion-associated protein tyrosine kinase pp125FAK. Mol Cell Biol 13:785-791.
39. Benson DL, Tanaka H (1998) N-cadherin redistribution during synaptogenesis in hippocampal neurons. J Neurosci 18:6892-6904.
40. Jontes JD, Emond MR, Smith SJ (2004) In vivo trafficking and targeting of N-cadherin to nascent presynaptic terminals. J Neurosci 24:9027-9034.
41. Niederkofler V, Baeriswyl T, Ott R, Stoeckli ET (2010) Nectin-like molecules/SynCAMs are required for post-crossing commissural axon guidance. Development 137:427-435.
42. Dean C, et al. (2003) Neurexin mediates the assembly of presynaptic terminals. Nat Neurosci 6:708-716. (Pubitemid 36792885)
43. Nam CI, Chen L (2005) Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proc Natl Acad Sci USA 102:6137-6142.
44. Gerrow K, et al. (2006) A preformed complex of postsynaptic proteins is involved in excitatory synapse development. Neuron 49:547-562. (Pubitemid 43221890)
45. Graf ER, Zhang X, Jin S-X, Linhoff MW, Craig AM (2004) Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119:1013-1026. (Pubitemid 40037614)
46. Gupton SL, Gertler FB (2007) Filopodia: The fingers that do the walking. Sci STKE 2007:re5.
47. Faix J, Rottner K (2006) The making of filopodia. Curr Opin Cell Biol 18:18-25.
48. Kayser MS, Nolt MJ, Dalva MB (2008) EphB receptors couple dendritic filopodia motility to synapse formation. Neuron 59:56-69.
49. Sieg DJ, et al. (2000) FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol 2:249-256.
50. Schaller MD, Otey CA, Hildebrand JD, Parsons JT (1995) Focal adhesion kinase and paxillin bind to peptides mimicking beta integrin cytoplasmic domains. J Cell Biol 130:1181-1187.
51. Beggs HE, Baragona SC, Hemperly JJ, Maness PF (1997) NCAM140 interacts with the focal adhesion kinase p125(fak) and the SRC-related tyrosine kinase p59(fyn). J Biol Chem 272:8310-8319.
52. Miao H, Burnett E, Kinch M, Simon E, Wang B (2000) Activation of EphA2 kinase suppresses integrin function and causes focal-adhesion-kinase dephosphorylation. Nat Cell Biol 2:62-69.
53. Dunty JM, et al. (2004) FERM domain interaction promotes FAK signaling. Mol Cell Biol 24:5353-5368.
54. Rico B, et al. (2004) Control of axonal branching and synapse formation by focal adhesion kinase. Nat Neurosci 7:1059-1069. (Pubitemid 41184446)
55. Phelan P, Gordon-Weeks R (1997) Isolation of Synaptosomes, Growth Cones, and Their Subcellular Components (Oxford University Press, Oxford), pp 1-38.
56. Biederer T, Scheiffele P (2007) Mixed-culture assays for analyzing neuronal synapse formation. Nat Protoc 2:670-676. (Pubitemid 47040028)