The novel synaptogenic protein farp1 links postsynaptic cytoskeletal dynamics and transsynaptic organization

Journal of Cell Biology

Volumn 199, Issue 6, 2012, Pages 985-1001

  Cheadle, Lucas ^a   Biederer, Thomas ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; EZRIN; F ACTIN; MOESIN; PLECKSTRIN DOMAIN PROTEIN 1; RAC1 PROTEIN; RADIXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MATURATION; CONTROLLED STUDY; CYTOSKELETON; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; PROTEOMICS; RAT; SYNAPTIC MEMBRANE;

ACTINS; ANIMALS; CELL ADHESION MOLECULES; CYTOSKELETAL PROTEINS; CYTOSKELETON; DENDRITIC SPINES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HIPPOCAMPUS; HUMANS; IMMUNOGLOBULINS; MICE; MICE, KNOCKOUT; NEUROGENESIS; NEURONS; NEUROPEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEOMICS; RAC GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; SYNAPSES;

MUS;

EID: 84872016076     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201205041     Document Type: Article

References (66)

1. Amor, D.J., L. Voullaire, K. Bentley, R. Savarirayan, and K.H. Choo. 2005. Mosaic monosomy of a neocentric ring chromosome maps brachyphalangy and growth hormone deficiency to 13q31.1-13q32.3. Am. J. Med. Genet. A. 133A:151-157. http://dx.doi.o g/10.1002/ajmg.a.30527
2. Biederer, T. 2006. Bioinformatic characterization of the SynCAM family of immunoglobulin-like domain-containing adhesion molecules. Genomics. 87:139-150. http://dx.doi.org/10.1016/j.ygeno.2005.08.017
3. Biederer, T., and P. Scheiffele. 2007. Mixed-culture assays for analyzing neuronal synapse formation. Nat. Protoc. 2:670-676. http://dx.doi.org/10 .1038/nprot.2007.92
4. Biederer, T., Y. Sara, M. Mozhayeva, D. Atasoy, X. Liu, E.T. Kavalali, and T.C. Südhof. 2002. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science. 297:1525-1531. http://dx.doi.org/10.1126/ science.1072356
5. Bonhoeffer, T., and R. Yuste. 2002. Spine motility. Phenomenology, mechanisms, and function. Neuron. 35:1019-1027. http://dx.doi.org/10.1016/ S0896-6273(02)00906-6
6. Burkel, B.M., G. von Dassow, and W.M. Bement. 2007. Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin. Cell Motil. Cytoskeleton. 64:822-832. http://dx.doi.org/10.1002/ cm.20226
7. Chklovskii, D.B., B.W. Mel, and K. Svoboda. 2004. Cortical rewiring and information storage. Nature. 431:782-788. http://dx.doi.org/10.1038/ nature03012
8. Cho, K.O., C.A. Hunt, and M.B. Kennedy. 1992. The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron. 9:929-942. http://dx.doi.org/10 .1016/0896-6273(92)90245-9
9. Dávalos, A., C. Ferńndez-Hernando, G. Sowa, B. Derakhshan, M.I. Lin, J.Y. Lee, H. Zhao, R. Luo, C. Colangelo, and W.C. Sessa. 2010. Quantitative proteomics of caveolin-1-regulated proteins: characterization of polymerase i and transcript release factor/CAVIN-1 IN endothelial cells. Mol. Cell. Proteomics. 9:2109-2124. http://dx.doi.org/10.1074/mcp.M110.001289
10. El-Husseini, A.E., E. Schnell, D.M. Chetkovich, R.A. Nicoll, and D.S. Bredt. 2000. PSD-95 involvement in maturation of excitatory synapses. Science. 290:1364-1368.
11. Elia, L.P., M. Yamamoto, K. Zang, and L.F. Reichardt. 2006. p120 catenin regulates dendritic spine and synapse development through Rho-family GTPases and cadherins. Neuron. 51:43-56. http://dx.doi.org/10.1016/ j.neuron.2006.05.018
12. Ferguson, S.M., A. Raimondi, S. Paradise, H. Shen, K. Mesaki, A. Ferguson, O. Destaing, G. Ko, J. Takasaki, O. Cremona, et al. 2009. Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev. Cell. 17:811-822. (published erratum appears in Dev. Cell. 2010. 18:332) http://dx.doi.org/10 .1016/j.devcel.2009.11.005
13. Fiala, J.C., M. Feinberg, V. Popov, and K.M. Harris. 1998. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J. Neurosci. 18:8900-8911.
14. Fischer, M., S. Kaech, D. Knutti, and A. Matus. 1998. Rapid actin-based plasticity in dendritic spines. Neuron. 20:847-854. http://dx.doi.org/ 10.1016/S0896-6273(00)80467-5
15. Fogel, A.I., M.R. Akins, A.J. Krupp, M. Stagi, V. Stein, and T. Biederer. 2007. SynCAMs organize synapses through heterophilic adhesion.J. Neurosci. 27:12516-12530. http://dx.doi.org/10.1523/JNEUROSCI .2739-07.2007
16. Fogel, A.I., M. Stagi, K. Perez de Arce, and T. Biederer. 2011. Lateral assembly of the immunoglobulin protein SynCAM 1 controls its adhesive function and instructs synapse formation. EMBO J. 30:4728-4738. http://dx.doi .org/10.1038/emboj.2011.336
17. Frost, N.A., J.M. Kerr, H.E. Lu, and T.A. Blanpied. 2010. A network of networks: cytoskeletal control of compartmentalized function within dendritic spines. Curr. Opin. Neurobiol. 20:578-587. http://dx.doi.org/10 .1016/j.conb.2010.06.009
18. Futai, K., M.J. Kim, T. Hashikawa, P. Scheiffele, M. Sheng, and Y. Hayashi. 2007. Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin. Nat. Neurosci. 10:186-195. http://dx.doi.org/10.1038/nn1837
19. García-Mata, R., K. Wennerberg, W.T. Arthur, N.K. Noren, S.M. Ellerbroek, and K. Burridge. 2006. Analysis of activated GAPs and GEFs in cell lysates. Methods Enzymol. 406:425-437. http://dx.doi.org/10.1016/ S0076-6879(06)06031-9
20. Govek, E.E., S.E. Newey, and L. Van Aelst. 2005. The role of the Rho GTPases in neuronal development. Genes Dev. 19:1-49. http://dx.doi .org/10.1101/gad.1256405
21. Groves, J.T., and J. Kuriyan. 2010. Molecular mechanisms in signal transduction at the membrane. Nat. Struct. Mol. Biol. 17:659-665. http://dx.doi .org/10.1038/nsmb.1844
22. Hart, M.J., A. Eva, D. Zangrilli, S.A. Aaronson, T. Evans, R.A. Cerione, and Y. Zheng. 1994. Cellular transformation and guanine nucleotide exchange activity are catalyzed by a common domain on the dbl oncogene product. J. Biol. Chem. 269:62-6.
23. Hoover, K.B., and P.J. Bryant. 2000. The genetics of the protein 4.1 family: organizers of the membrane and cytoskeleton. Curr. Opin. Cell Biol. 12:229-234. http://dx.doi.org/10.1016/S0955-0674(99)00080-0
24. Hotulainen,P., and C.C. Hoogenraad. 2010. Actin in dendritic spines: connecting dynamics to function. J. Cell Biol. 189:619-629. http://dx.doi .org/10.1083/jcb.201003008
25. Itoh, R.E., K. Kurokawa, Y. Ohba, H. Yoshizaki, N. Mochizuki, and M. Matsuda. 2002. Activation of rac and cdc42 video imaged by fluorescent resonance energy transfer-based single-molecule probes in the membrane of living cells. Mol. Cell. Biol. 22:6582-6591. http://dx.doi .org/10.1128/MCB.22.18.6582-6591.2002
26. Jaffe, A.B., and A. Hall. 2005. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21:247-269. http://dx.doi.org/10.1146/annurev .cellbio.21.020604.150721
27. Jones, D.H., and A.I. Matus. 1974. Isolation of synaptic plasma membrane from brain by combined flotation-sedimentation density gradient centrifugation. Biochim. Biophys. Acta. 356:276-287. http://dx.doi.org/10.1016/0005-2736(74)90268-5
28. Kasai, H., M. Matsuzaki, J. Noguchi, N. Yasumatsu, and H. Nakahara. 2003. Structure-stability-function relationships of dendritic spines. Trends Neurosci. 26:360-368. http://dx.doi.org/10.1016/S0166-2236(03)00162-0
29. Kayser, M.S., M.J. Nolt, and M.B. Dalva. 2008. EphB receptors couple dendritic filopodia motility to synapse formation. Neuron. 59:56-69. http://dx.doi .org/10.1016/j.neuron.2008.05.007
30. Klein, R. 2009. Bidirectional modulation of synaptic functions by Eph/ephrin signaling. Nat. Neurosci. 12:15-20. http://dx.doi.org/10.1038/nn.2231
31. Knott, G.W., A. Holtmaat, L. Wilbrecht, E. Welker, and K. Svoboda. 2006. Spine growth precedes synapse formation in the adult neocortex in vivo. Nat. Neurosci. 9:1117-1124. http://dx.doi.org/10.1038/nn1747
32. Koyano, Y., T. Kawamoto, M. Shen, W. Yan, M. Noshiro, K. Fujii, and Y. Kato. 1997. Molecular cloning and characterization of CDEP, a novel human protein containing the ezrin-like domain of the band 4.1 superfamily and the Dbl homology domain of Rho guanine nucleotide exchange factors. Biochem. Biophys. Res. Commun. 241:369-375. http://dx.doi.org/10.1006/bbrc.1997.7826
33. Lindskog, M., L. Li, R.D. Groth, D. Poburko, T.C. Thiagarajan, X. Han, and R.W. Tsien. 2010. Postsynaptic GluA1 enables acute retrograde enhancement of presynaptic function to coordinate adaptation to synaptic inactivity. Proc. Natl. Acad. Sci USA. 107:21806-21811. http://dx.doi .org/10.1073/pnas.1016399107
34. Matus, A., M. Ackermann, G. Pehling, H.R. Byers, and K. Fujiwara. 1982. High actin concentrations in brain dendritic spines and postsynaptic densities. Proc. Natl. Acad. Sci. USA. 79:7590-7594. http://dx.doi.org/ 10.1073/pnas.79.23.7590
35. Missler, M., T.C. S-dhof, and T. Biederer. 2012. Synaptic cell adhesion. Cold Spring Harb. Perspect. Biol. 4:a005694. htt ://dx.doi.org/10.1101/ cshperspect.a005694
36. Moeller, M.L., Y. Shi, L.F. Reichardt, and I.M. Ethell. 2006. EphB receptors regulat dendritic spine morphogenesis through the recruitment/phosphorylation of focal adhesion kinase and RhoA activation. J. Biol. Chem. 281:1587-1598. http://dx.doi.org/10.1074/jbc.M511756200
37. Nakamura, T., K. Aoki, and M. Matsuda. 2005. Monitoring spatio-temporal regulation of Ras and Rho GTPase with GFP-based FRET probes. Methods. 37:146-153. http://dx.doi.org/10.1016/j.ymeth.2005.05.021
38. Nakayama, A.Y., M.B. Harms, and L. Luo. 2000. Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J. Neurosci. 20:5329-5338.
39. Okamoto, K., T. Nagai, A. Miyawaki, and Y. Hayashi. 2004. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat. Neurosci. 7:1104-1112. http:// dx.doi.org/10.1038/nn1311
40. Penzes, P., A. Beeser, J. Chernoff, M.R. Schiller, B.A. Eipper, R.E. Mains, and R.L. Huganir. 2003. Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron. 37:263-274. http://dx.doi.org/10.1016/ S0896-6273(02)01168-6
41. Penzes, P., M.E. Cahill, K.A. Jones, J.E. VanLeeuwen, and K.M. Woolfrey. 2011. Dendritic spine pathology in neuropsychiatric disorders. Nat. Neurosci. 14:285-293. http://dx.doi.org/10.1038/nn.2741
42. Regalado, M.P., R.T. Terry-Lorenzo, C.L. Waites, C.C. Garner, and R.C. Malenka. 2006. Transsynaptic signaling by postsynaptic synapseassociated protein 97. J. Neurosci. 26:2343-2357. http://dx.doi.org/10 .1523/JNEUROSCI.5247-05.2006
43. Robbins, E.M., A.J. Krupp, K. Perez de Arce, A.K. Ghosh, A.I. Fogel, A. Boucard, T.C. SÖdhof, V. Stein, and T. Biederer. 2010. SynCAM 1 adhesion dynamically regulates synapse number and impacts plasticity and learning. Neuron. 68:894-906. http://dx.doi.org/10.1016/ j.neuron.2010.11.003
44. Shilov I.V., S.L. Seymour, A.A. Patel, A. Loboda, W.H. Tang, S.P. Keating, C.L. Hunter, L.M. Nuwaysir, and D.A. Schaeffer. 2007. The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol. Cell. Proteomics. 6:1638-1655. http://dx.doi .org/10.1074/mcp.T600050-MCP200
45. Shu, X., V. Lev-Ram, T.J. Deerinck, Y. Qi, E.B. Ramko, M.W. Davidson, Y. Jin, M.H. Ellisman, and R.Y. Tsien. 2011. A gene ically encoded tag for correlated light and electron microscopy of intact cells, tissues, an organisms. PLoS Biol. 9:e1001041. http://dx.doi.org/10.1371/journal .pbio.1001041
46. Stagi, M., A.I. Fogel, and T. Biederer. 2010. SynCAM 1 participates in axodendritic contact assembly and shapes neuronal growth cones. Proc. Natl. Acad. Sci. USA. 107:7568-7573. http://dx.doi.org/10.1073/ pnas.0911798107
47. Stoppini, L., P.A. Buchs, and D. Muller. 1991. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods. 37:173-182. http:// dx.doi.org/10.1016/0165-0270(91)90128-M
48. SÖdhof, T.C. 2008. Neuroligins and neurexins link synaptic function to cognitive disease. Nature. 455:903-911. http://dx.doi.org/10.1038/ nature07456
49. Sugita, S., and T.C. SÖdhof. 2000. Specificity of Ca2+-dependent protein interactions mediated by the C2A domains of synaptotagmins. Biochemistry. 39:2940-2949. http://dx.doi.org/10.1021/bi9920984
50. Tada, T., and M. Sheng. 2006. Molecular mechanisms of dendritic spine morphogenesis. Curr. Opin. Neurobiol. 16:95-101. http://dx.doi.org/10.1016/ j.conb.2005.12.001
51. Tagliaferro, P., and M. Morales. 2008. Synapses between corticotropin-releasing factor-containing axon terminals and dopaminergic neurons in the ventral tegmental area are predominantly glutamatergic. J. Comp. Neurol. 506:616-626. http://dx.doi.org/10.1002/cne.21576
52. Tashiro, A., A. Minden, and R. Yuste. 2000. Regulation of dendritic spine morphology by the rho family of small GTPases: antagonistic roles of Rac and Rho. Cereb. Cortex. 10:927-938. http://dx.doi.org/10 .1093/cercor/10.10.927
53. Thomas, L.A., M.R. Akins, and T. Biederer. 2008. Expression and adhesion profiles of SynCAM molecules indicate distinct neuronal functions. J. Comp. Neurol. 510:47-67. http://dx.doi.org/10.1002/cne.21773
54. Tolias, K.F., J.B. Bikoff, C.G. Kane, C.S. Tolias, L. Hu, and M.E. Greenberg. 2007. The Rac1 guanine nucleotide exchange factor Tiam1 mediates EphB receptor-dependent dendritic spine development. Proc. Natl. Acad. Sci. USA. 104:7265-7270. http://dx.doi.org/10.1073/pnas.0702044104
55. Tracy, T.E., J.J. Yan, and L. Chen. 2011. Acute knockdown of AMPA receptors reveals a trans-synaptic signal for presynaptic maturation. EMBO J. 30:1577-1592. http://dx.doi.org/10.1038/emboj.2011.59
56. Tran, T.S., M.E. Rubio, R.L. Clem, D. Johnson, L. Case, M. Tessier-Lavigne, R.L. Huganir, D.D. Ginty, and A.L. Kolodkin. 2009. Secreted semaphorins control spine distribution and morphogenesis in the postnatal CNS. Nature. 462:1065-1069. http://dx.doi.org/10.1038/nature08628
57. Wittenmayer, N., C. Körber, H. Liu, T. Kremer, F. Varoqueaux, E.R. Chapman, N. Brose, T. Kuner, and T. Dresbach. 2009. Postsynaptic Neuroligin1 regulates presynaptic maturation. Proc. Natl. Acad. Sci. USA. 106:13564-13569. http://dx.doi.org/10.1073/pnas.0905819106
58. Woolfrey, K.M., D.P. Srivastava, H. Photowala, M. Yamashita, M.V. Barbolina, M.E. Cahill, Z. Xie, K.A. Jones, L.A. Quilliam, M. Prakriya, and P. Penzes. 2009. Epac2 induces synapse remodeling and depression and its disease-associated forms alter spines. Nat. Neurosci. 12:1275-1284. http://dx.doi.org/10.1038/nn.2386
59. Xie, Z., H. Photowala, M.E. Cahill, D.P. Srivastava, K.M. Woolfrey, C.Y. Shum, R.L. Huganir, and P. Penzes. 2008. Coordination of synaptic adhesion with dendritic spine remodeling by AF-6 and kalirin-7. J. Neurosci. 28:6079-6091. http://dx.doi.org/10.1523/JNEUROSCI.1170-08.2008
60. Yuste, R. 2011. Dendritic spines and distributed circuits. Neuron. 71:772-781. http://dx.doi.org/10.1016/j.neuron.2011.07.024 Yuste, R., and T. Bonhoeffer. 2004. Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat. Rev. Neurosci. 5:24-34. http:// dx.doi.org/10.1038/nrn1300
61. Yuste, R., and T. Bonhoeffer. 2004. Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat. Rev. Neurosci. 5:24-34. http:// dx.doi.org/10.1038/nrn1300
62. Zhang, W.D., and D.L. Benson. 2001. Stages of synapse development defined by dependence on F-actin. J. Neurosci. 21:5169-5181.
63. Zhang, H., D.J. Webb, H. Asmussen, S. Niu, and A.F. Horwitz. 2005. A GIT1/ PIX/Rac/PAK signaling module regulates spine morphogenesis and synapse formation through MLC. J. Neurosci. 25:3379-3388. http://dx .doi.org/10.1523/JNEUROSCI.3553-04.2005
64. Zhuang, B., Y.S. Su, and S. Sockanathan. 2009. FARP1 promotes the dendritic growth of spinal motor neuron subtypes through transmembrane Semaphorin6A and PlexinA4 signaling. Neuron. 61:359-372. http:// dx.doi.org/10.1016/j.neuron.2008.12.022
65. Zito, K., G. Knott, G.M. Shepherd, S. Shenolikar, and K. Svoboda. 2004.Induction of spine growth and synapse formation by regulation of the spine actin cytoskeleton. Neuron. 44:321-334. http://dx.doi.org/10 .1016/j.neuron.2004.09.022
66. Ziv, N.E., and S.J. Smith. 1996. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron. 17:91-102. http://dx.doi .org/10.1016/S0896-6273(00)80283-4