Dynamic Control of Excitatory Synapse Development by a Rac1 GEF/GAP Regulatory Complex

Developmental Cell

Volumn 29, Issue 6, 2014, Pages 701-715

  Um, Kyongmi ^a   Niu, Sanyong ^a   Duman, Joseph G ^a   Cheng, Jinxuan X ^a   Tu, Yen Kuei ^a   Schwechter, Brandon ^a   Liu, Feng ^a   Hiles, Laura ^a   Narayanan, Anjana S ^a   Ash, Ryan T ^a   Mulherkar, Shalaka ^a   Alpadi, Kannan ^a   Smirnakis, Stelios M ^a   Tolias, Kimberley F ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREAKPOINT CLUSTER REGION PROTEIN; EPHRIN RECEPTOR B1; EPHRIN RECEPTOR B2; GUANINE NUCLEOTIDE EXCHANGE FACTOR; RAC1 PROTEIN; TIAM1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; ENZYME INHIBITION; EXCITATORY POSTSYNAPTIC POTENTIAL; GENE DISRUPTION; INTERNALIZATION; MOLECULAR DYNAMICS; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SPINE DEVELOPMENT; SPINE DISEASE; SYNAPTOGENESIS;

ANIMALS; BLOTTING, WESTERN; DENDRITIC SPINES; ELECTROPHYSIOLOGY; ENDOCYTOSIS; GTPASE-ACTIVATING PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; IMMUNOENZYME TECHNIQUES; IMMUNOPRECIPITATION; MICE; MICE, KNOCKOUT; NEURITES; PROTO-ONCOGENE PROTEINS C-BCR; RAC1 GTP-BINDING PROTEIN; RECEPTORS, EPH FAMILY; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84904704517     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.05.011     Document Type: Article

References (53)

1. Alvarez V.A., Sabatini B.L. Anatomical and physiological plasticity of dendritic spines. Annu. Rev. Neurosci. 2007, 30:79-97.
2. Cho Y.J., Cunnick J.M., Yi S.J., Kaartinen V., Groffen J., Heisterkamp N. Abr and Bcr, two homologous Rac GTPase-activating proteins, control multiple cellular functions of murine macrophages. Mol. Cell. Biol. 2007, 27:899-911.
3. Cowan C.W., Shao Y.R., Sahin M., Shamah S.M., Lin M.Z., Greer P.L., Gao S., Griffith E.C., Brugge J.S., Greenberg M.E. Vav family GEFs link activated Ephs to endocytosis and axon guidance. Neuron 2005, 46:205-217.
4. Cunnick J.M., Schmidhuber S., Chen G., Yu M., Yi S.J., Cho Y.J., Kaartinen V., Minoo P., Warburton D., Groffen J., Heisterkamp N. Bcr and Abr cooperate in negatively regulating acute inflammatory responses. Mol. Cell. Biol. 2009, 29:5742-5750.
5. Deininger K., Eder M., Kramer E.R., Zieglgänsberger W., Dodt H.U., Dornmair K., Colicelli J., Klein R. The Rab5 guanylate exchange factor Rin1 regulates endocytosis of the EphA4 receptor in mature excitatory neurons. Proc. Natl. Acad. Sci. USA 2008, 105:12539-12544.
6. Diekmann D., Brill S., Garrett M.D., Totty N., Hsuan J., Monfries C., Hall C., Lim L., Hall A. Bcr encodes a GTPase-activating protein for p21rac. Nature 1991, 351:400-402.
7. Duman J.G., Tzeng C.P., Tu Y.K., Munjal T., Schwechter B., Ho T.S., Tolias K.F. The adhesion-GPCR BAI1 regulates synaptogenesis by controlling the recruitment of the Par3/Tiam1 polarity complex to synaptic sites. J.Neurosci. 2013, 33:6964-6978.
8. Egea J., Klein R. Bidirectional Eph-ephrin signaling during axon guidance. Trends Cell Biol. 2007, 17:230-238.
9. Ethell I.M., Irie F., Kalo M.S., Couchman J.R., Pasquale E.B., Yamaguchi Y. EphB/syndecan-2 signaling in dendritic spine morphogenesis. Neuron 2001, 31:1001-1013.
10. Feige J.N., Sage D., Wahli W., Desvergne B., Gelman L. PixFRET, an ImageJ plug-in for FRET calculation that can accommodate variations in spectral bleed-throughs. Microsc. Res. Tech. 2005, 68:51-58.
11. Feng G., Mellor R.H., Bernstein M., Keller-Peck C., Nguyen Q.T., Wallace M., Nerbonne J.M., Lichtman J.W., Sanes J.R. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000, 28:41-51.
12. Gao Y., Dickerson J.B., Guo F., Zheng J., Zheng Y. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc. Natl. Acad. Sci. USA 2004, 101:7618-7623.
13. García-Mata R., Wennerberg K., Arthur W.T., Noren N.K., Ellerbroek S.M., Burridge K. Analysis of activated GAPs and GEFs in cell lysates. Methods Enzymol. 2006, 406:425-437.
14. Goryachev A.B., Pokhilko A.V. Computational model explains high activity and rapid cycling of Rho GTPases within protein complexes. PLoS Comput. Biol. 2006, 2:e172.
15. Govek E.E., Newey S.E., Van Aelst L. The role of the Rho GTPases in neuronal development. Genes Dev. 2005, 19:1-49.
16. Heerssen H.M., Pazyra M.F., Segal R.A. Dynein motors transportactivated Trks to promote survival of target-dependent neurons. Nat. Neurosci. 2004, 7:596-604.
17. Henkemeyer M., Itkis O.S., Ngo M., Hickmott P.W., Ethell I.M. Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J.Cell Biol. 2003, 163:1313-1326.
18. Kaartinen V., Gonzalez-Gomez I., Voncken J.W., Haataja L., Faure E., Nagy A., Groffen J., Heisterkamp N. Abnormal function of astroglia lacking Abr and Bcr RacGAPs. Development 2001, 128:4217-4227.
19. Kaartinen V., Nagy A., Gonzalez-Gomez I., Groffen J., Heisterkamp N. Vestibular dysgenesis in mice lacking Abr and Bcr Cdc42/RacGAPs. Dev. Dyn. 2002, 223:517-525.
20. Kayser M.S., McClelland A.C., Hughes E.G., Dalva M.B. Intracellular and trans-synaptic regulation of glutamatergic synaptogenesis by EphB receptors. J.Neurosci. 2006, 26:12152-12164.
21. Kirchhausen T., Macia E., Pelish H.E. Use of dynasore, the small molecule inhibitor of dynamin, in the regulation of endocytosis. Methods Enzymol. 2008, 438:77-93.
22. Klein R. Bidirectional modulation of synaptic functions by Eph/ephrin signaling. Nat. Neurosci. 2009, 12:15-20.
23. Komatsu N., Aoki K., Yamada M., Yukinaga H., Fujita Y., Kamioka Y., Matsuda M. Development of an optimized backbone of FRET biosensors for kinases and GTPases. Mol. Biol. Cell 2011, 22:4647-4656.
24. Lai K.O., Wong A.S., Cheung M.C., Xu P., Liang Z., Lok K.C., Xie H., Palko M.E., Yung W.H., Tessarollo L., et al. TrkB phosphorylation by Cdk5 is required for activity-dependent structural plasticity and spatial memory. Nat. Neurosci. 2012, 15:1506-1515.
25. Luo L., Hensch T.K., Ackerman L., Barbel S., Jan L.Y., Jan Y.N. Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines. Nature 1996, 379:837-840.
26. Marston D.J., Dickinson S., Nobes C.D. Rac-dependent trans-endocytosis of ephrinBs regulates Eph-ephrin contact repulsion. Nat. Cell Biol. 2003, 5:879-888.
27. Mertens A.E., Roovers R.C., Collard J.G. Regulation of Tiam1-Rac signalling. FEBS Lett. 2003, 546:11-16.
28. Miyamoto Y., Yamauchi J., Tanoue A., Wu C., Mobley W.C. TrkB binds and tyrosine-phosphorylates Tiam1, leading to activation of Rac1 and induction of changes in cellular morphology. Proc. Natl. Acad. Sci. USA 2006, 103:10444-10449.
29. Murai K.K., Nguyen L.N., Irie F., Yamaguchi Y., Pasquale E.B. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat. Neurosci. 2003, 6:153-160.
30. Nakayama A.Y., Harms M.B., Luo L. Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J.Neurosci. 2000, 20:5329-5338.
31. Narayanan A.S., Reyes S.B., Um K., McCarty J.H., Tolias K.F. The Rac-GAP Bcr is a novel regulator of the Par complex that controls cell polarity. Mol. Biol. Cell 2013, 24:3857-3868.
32. Newey S.E., Velamoor V., Govek E.E., Van Aelst L. Rho GTPases, dendritic structure, and mental retardation. J.Neurobiol. 2005, 64:58-74.
33. Nikolić M. The Pak1 kinase: an important regulator of neuronal morphology and function in the developing forebrain. Mol. Neurobiol. 2008, 37:187-202.
34. Oh D., Han S., Seo J., Lee J.R., Choi J., Groffen J., Kim K., Cho Y.S., Choi H.S., Shin H., et al. Regulation of synaptic Rac1 activity, long-term potentiation maintenance, and learning and memory by BCR and ABR Rac GTPase-activating proteins. J.Neurosci. 2010, 30:14134-14144.
35. Park A.R., Oh D., Lim S.H., Choi J., Moon J., Yu D.Y., Park S.G., Heisterkamp N., Kim E., Myung P.K., Lee J.R. Regulation of dendritic arborization by BCR Rac1 GTPase-activating protein, a substrate of PTPRT. J.Cell Sci. 2012, 125:4518-4531.
36. Pasquale E.B. Eph receptor signalling casts a wide net on cell behaviour. Nat. Rev. Mol. Cell Biol. 2005, 6:462-475.
37. Penzes P., Jones K.A. Dendritic spine dynamics-a key role for kalirin-7. Trends Neurosci. 2008, 31:419-427.
38. Penzes P., Beeser A., Chernoff J., Schiller M.R., Eipper B.A., Mains R.E., Huganir R.L. Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 2003, 37:263-274.
39. Penzes P., Cahill M.E., Jones K.A., Srivastava D.P. Convergent CaMK and RacGEF signals control dendritic structure and function. Trends Cell Biol. 2008, 18:405-413.
40. Pertz O. Spatio-temporal Rho GTPase signaling - where are we now?. J.Cell Sci. 2010, 123:1841-1850.
41. Pitulescu M.E., Adams R.H. Eph/ephrin molecules-a hub for signaling and endocytosis. Genes Dev. 2010, 24:2480-2492.
42. Ramakers G.J. Rho proteins, mental retardation and the cellular basis of cognition. Trends Neurosci. 2002, 25:191-199.
43. Shieh J.C., Schaar B.T., Srinivasan K., Brodsky F.M., McConnell S.K. Endocytosis regulates cell soma translocation and the distribution of adhesion proteins in migrating neurons. PLoS ONE 2011, 6:e17802.
44. Spiering D., Hodgson L. Dynamics of the Rho-family small GTPases in actin regulation and motility. Cell Adhes. Migr. 2011, 5:170-180.
45. Tolias K.F., Bikoff J.B., Burette A., Paradis S., Harrar D., Tavazoie S., Weinberg R.J., Greenberg M.E. The Rac1-GEF Tiam1 couples the NMDA receptor to the activity-dependent development of dendritic arbors and spines. Neuron 2005, 45:525-538.
46. Tolias K.F., Bikoff J.B., Kane C.G., Tolias C.S., Hu L., Greenberg M.E. The Rac1 guanine nucleotide exchange factor Tiam1 mediates EphB receptor-dependent dendritic spine development. Proc. Natl. Acad. Sci. USA 2007, 104:7265-7270.
47. Tolias K.F., Duman J.G., Um K. Control of synapse development and plasticity by Rho GTPase regulatory proteins. Prog. Neurobiol. 2011, 94:133-148.
48. Voncken J.W., van Schaick H., Kaartinen V., Deemer K., Coates T., Landing B., Pattengale P., Dorseuil O., Bokoch G.M., Groffen J., et al. Increased neutrophil respiratory burst in bcr-null mutants. Cell 1995, 80:719-728.
49. Voncken J.W., Baram T.Z., Gonzales-Gomez I., Van Schaick H., Shih J.C., Chen K., Groffen J., Heisterkamp N. Abnormal stress response and increased fighting behavior in mice lacking the bcr gene product. Int. J. Mol. Med. 1998, 2:577-583.
50. Yoo S., Shin J., Park S. EphA8-ephrinA5 signaling and clathrin-mediated endocytosis is regulated by Tiam-1, a Rac-specific guanine nucleotide exchange factor. Mol. Cells 2010, 29:603-609.
51. Yoo S., Kim Y., Noh H., Lee H., Park E., Park S. Endocytosis of EphA receptors is essential for the proper development of the retinocollicular topographic map. EMBO J. 2011, 30:1593-1607.
52. Zhang H., Macara I.G. The polarity protein PAR-3 and TIAM1 cooperate in dendritic spine morphogenesis. Nat. Cell Biol. 2006, 8:227-237.
53. Zimmer M., Palmer A., Köhler J., Klein R. EphB-ephrinB bi-directional endocytosis terminates adhesion allowing contact mediated repulsion. Nat. Cell Biol. 2003, 5:869-878.