Retrograde BMP signaling controls synaptic growth at the nmj by regulating trio expression in motor neurons

Neuron

Volumn 66, Issue 4, 2010, Pages 536-549

  Ball, Robin W ^a   Warren Paquin, Maude ^a   Tsurudome, Kazuya ^a   Liao, Edward H ^a   Elazzouzi, Fatima ^a   Cavanagh, Chelsea ^a   An, Beum Soo ^a   Wang, Tian Tian ^a   White, John H ^a   Haghighi, A Pejmun ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Cellbio; Devbio; Signaling

Indexed keywords

BONE MORPHOGENETIC PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE LOCUS; HOMEOSTASIS; MOTONEURON; NERVE CELL DIFFERENTIATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TRANSCRIPTION REGULATION; TRANSGENE;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL LINE; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MOTOR NEURONS; NEUROMUSCULAR JUNCTION; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 77953260849     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2010.04.011     Document Type: Article

References (77)

1. Aberle H., Haghighi A.P., Fetter R.D., McCabe B.D., Magalhães T.R., Goodman C.S. wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 2002, 33:545-558.
2. Albin S.D., Davis G.W. Coordinating structural and functional synapse development: postsynaptic p21-activated kinase independently specifies glutamate receptor abundance and postsynaptic morphology. J. Neurosci. 2004, 24:6871-6879.
3. Awasaki T., Saito M., Sone M., Suzuki E., Sakai R., Ito K., Hama C. The Drosophila trio plays an essential role in patterning of axons by regulating their directional extension. Neuron 2000, 26:119-131.
4. Bateman J., Van Vactor D. The Trio family of guanine-nucleotide-exchange factors: regulators of axon guidance. J. Cell Sci. 2001, 114:1973-1980.
5. Bateman J., Shu H., Van Vactor D. The guanine nucleotide exchange factor trio mediates axonal development in the Drosophila embryo. Neuron 2000, 26:93-106.
6. Birch-Machin I., Gao S., Huen D., McGirr R., White R.A., Russell S. Genomic analysis of heat-shock factor targets in Drosophila. Genome Biol. 2005, 6:R63.
7. Bishop A.L., Hall A. Rho GTPases and their effector proteins. Biochem. J. 2000, 348:241-255.
8. Bos J.L., Rehmann H., Wittinghofer A. GEFs and GAPs: critical elements in the control of small G proteins. Cell 2007, 129:865-877.
9. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
10. Briançon-Marjollet A., Ghogha A., Nawabi H., Triki I., Auziol C., Fromont S., Piché C., Enslen H., Chebli K., Cloutier J.F., et al. Trio mediates netrin-1-induced Rac1 activation in axon outgrowth and guidance. Mol. Cell. Biol. 2008, 28:2314-2323.
11. Bryan B., Kumar V., Stafford L.J., Cai Y., Wu G., Liu M. GEFT, a Rho family guanine nucleotide exchange factor, regulates neurite outgrowth and dendritic spine formation. J. Biol. Chem. 2004, 279:45824-45832.
12. Budnik V., Koh Y.H., Guan B., Hartmann B., Hough C., Woods D., Gorczyca M. Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron 1996, 17:627-640.
13. Cingolani L.A., Goda Y. Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat. Rev. Neurosci. 2008, 9:344-356.
14. Davis G.W. Homeostatic control of neural activity: from phenomenology to molecular design. Annu. Rev. Neurosci. 2006, 29:307-323.
15. de Curtis I. Functions of Rac GTPases during neuronal development. Dev. Neurosci. 2008, 30:47-58.
16. Dickson B.J. Rho GTPases in growth cone guidance. Curr. Opin. Neurobiol. 2001, 11:103-110.
17. Eden S., Rohatgi R., Podtelejnikov A.V., Mann M., Kirschner M.W. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 2002, 418:790-793.
18. Fan X., Labrador J.P., Hing H., Bashaw G.J. Slit stimulation recruits Dock and Pak to the roundabout receptor and increases Rac activity to regulate axon repulsion at the CNS midline. Neuron 2003, 40:113-127.
19. Fanto M., Weber U., Strutt D.I., Mlodzik M. Nuclear signaling by Rac and Rho GTPases is required in the establishment of epithelial planar polarity in the Drosophila eye. Curr. Biol. 2000, 10:979-988.
20. Fitzsimonds R.M., Poo M.M. Retrograde signaling in the development and modification of synapses. Physiol. Rev. 1998, 78:143-170.
21. Frank C.A., Pielage J., Davis G.W. A presynaptic homeostatic signaling system composed of the Eph receptor, ephexin, Cdc42, and CaV2.1 calcium channels. Neuron 2009, 61:556-569.
22. Fu W.Y., Chen Y., Sahin M., Zhao X.S., Shi L., Bikoff J.B., Lai K.O., Yung W.H., Fu A.K., Greenberg M.E., Ip N.Y. Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism. Nat. Neurosci. 2007, 10:67-76.
23. Galindo M.I., Bishop S.A., Greig S., Couso J.P. Leg patterning driven by proximal-distal interactions and EGFR signaling. Science 2002, 297:256-259.
24. Goold C.P., Davis G.W. The BMP ligand Gbb gates the expression of synaptic homeostasis independent of synaptic growth control. Neuron 2007, 56:109-123.
25. Haghighi A.P., McCabe B.D., Fetter R.D., Palmer J.E., Hom S., Goodman C.S. Retrograde control of synaptic transmission by postsynaptic CaMKII at the Drosophila neuromuscular junction. Neuron 2003, 39:255-267.
26. Hakeda-Suzuki S., Ng J., Tzu J., Dietzl G., Sun Y., Harms M., Nardine T., Luo L., Dickson B.J. Rac function and regulation during Drosophila development. Nature 2002, 416:438-442.
27. Hoodless P.A., Haerry T., Abdollah S., Stapleton M., O'Connor M.B., Attisano L., Wrana J.L. MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell 1996, 85:489-500.
28. Hu H., Li M., Labrador J.P., McEwen J., Lai E.C., Goodman C.S., Bashaw G.J. Cross GTPase-activating protein (CrossGAP)/Vilse links the Roundabout receptor to Rac to regulate midline repulsion. Proc. Natl. Acad. Sci. USA 2005, 102:4613-4618.
29. Innocenti M., Zucconi A., Disanza A., Frittoli E., Areces L.B., Steffen A., Stradal T.E., Di Fiore P.P., Carlier M.F., Scita G. Abi1 is essential for the formation and activation of a WAVE2 signalling complex. Nat. Cell Biol. 2004, 6:319-327.
30. Inoue H., Imamura T., Ishidou Y., Takase M., Udagawa Y., Oka Y., Tsuneizumi K., Tabata T., Miyazono K., Kawabata M. Interplay of signal mediators of decapentaplegic (Dpp): molecular characterization of mothers against dpp, Medea, and daughters against dpp. Mol. Biol. Cell 1998, 9:2145-2156.
31. Joneson T., McDonough M., Bar-Sagi D., Van Aelst L. RAC regulation of actin polymerization and proliferation by a pathway distinct from Jun kinase. Science 1996, 274:1374-1376.
32. Keshishian H., Kim Y.S. Orchestrating development and function: retrograde BMP signaling in the Drosophila nervous system. Trends Neurosci. 2004, 27:143-147.
33. Kuromi H., Kidokoro Y. Exocytosis and endocytosis of synaptic vesicles and functional roles of vesicle pools: lessons from the Drosophila neuromuscular junction. Neuroscientist 2005, 11:138-147.
34. Kusanagi K., Inoue H., Ishidou Y., Mishima H.K., Kawabata M., Miyazono K. Characterization of a bone morphogenetic protein-responsive Smad-binding element. Mol. Biol. Cell 2000, 11:555-565.
35. Lai K.O., Ip N.Y. Synapse development and plasticity: roles of ephrin/Eph receptor signaling. Curr. Opin. Neurobiol. 2009, 19:275-283.
36. Lin D.M., Goodman C.S. Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron 1994, 13:507-523.
37. Luo L. Rho GTPases in neuronal morphogenesis. Nat. Rev. Neurosci. 2000, 1:173-180.
38. Luo L. Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. Annu. Rev. Cell Dev. Biol. 2002, 18:601-635.
39. Luo L., Liao Y.J., Jan L.Y., Jan Y.N. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 1994, 8:1787-1802.
40. Ma X.M., Huang J., Wang Y., Eipper B.A., Mains R.E. Kalirin, a multifunctional Rho guanine nucleotide exchange factor, is necessary for maintenance of hippocampal pyramidal neuron dendrites and dendritic spines. J. Neurosci. 2003, 23:10593-10603.
41. Marqués G., Bao H., Haerry T.E., Shimell M.J., Duchek P., Zhang B., O'Connor M.B. The Drosophila BMP type II receptor Wishful Thinking regulates neuromuscular synapse morphology and function. Neuron 2002, 33:529-543.
42. Matus A., Brinkhaus H., Wagner U. Actin dynamics in dendritic spines: a form of regulated plasticity at excitatory synapses. Hippocampus 2000, 10:555-560.
43. McCabe B.D., Marqués G., Haghighi A.P., Fetter R.D., Crotty M.L., Haerry T.E., Goodman C.S., O'Connor M.B. The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron 2003, 39:241-254.
44. McCabe B.D., Hom S., Aberle H., Fetter R.D., Marques G., Haerry T.E., Wan H., O'Connor M.B., Goodman C.S., Haghighi A.P. Highwire regulates presynaptic BMP signaling essential for synaptic growth. Neuron 2004, 41:891-905.
45. Merino C., Penney J., González M., Tsurudome K., Moujahidine M., O'Connor M.B., Verheyen E.M., Haghighi P. Nemo kinase interacts with Mad to coordinate synaptic growth at the Drosophila neuromuscular junction. J. Cell Biol. 2009, 185:713-725.
46. Morales M., Colicos M.A., Goda Y. Actin-dependent regulation of neurotransmitter release at central synapses. Neuron 2000, 27:539-550.
47. Newsome T.P., Schmidt S., Dietzl G., Keleman K., Asling B., Debant A., Dickson B.J. Trio combines with dock to regulate Pak activity during photoreceptor axon pathfinding in Drosophila. Cell 2000, 101:283-294.
48. Ng J., Luo L. Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron 2004, 44:779-793.
49. Ng J., Nardine T., Harms M., Tzu J., Goldstein A., Sun Y., Dietzl G., Dickson B.J., Luo L. Rac GTPases control axon growth, guidance and branching. Nature 2002, 416:442-447.
50. O'Donnell M., Chance R.K., Bashaw G.J. Axon growth and guidance: receptor regulation and signal transduction. Annu. Rev. Neurosci. 2009, 32:383-412.
51. Osterwalder T., Yoon K.S., White B.H., Keshishian H. A conditional tissue-specific transgene expression system using inducible GAL4. Proc. Natl. Acad. Sci. USA 2001, 98:12596-12601.
52. Parnas D., Haghighi A.P., Fetter R.D., Kim S.W., Goodman C.S. Regulation of postsynaptic structure and protein localization by the Rho-type guanine nucleotide exchange factor dPix. Neuron 2001, 32:415-424.
53. Pawson C., Eaton B.A., Davis G.W. Formin-dependent synaptic growth: evidence that Dlar signals via Diaphanous to modulate synaptic actin and dynamic pioneer microtubules. J. Neurosci. 2008, 28:11111-11123.
54. Penzes P., Johnson R.C., Sattler R., Zhang X., Huganir R.L., Kambampati V., Mains R.E., Eipper B.A. The neuronal Rho-GEF Kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis. Neuron 2001, 29:229-242.
55. Qurashi A., Sahin H.B., Carrera P., Gautreau A., Schenck A., Giangrande A. HSPC300 and its role in neuronal connectivity. Neural Dev. 2007, 2:18.
56. Rawson J.M., Lee M., Kennedy E.L., Selleck S.B. Drosophila neuromuscular synapse assembly and function require the TGF-beta type I receptor saxophone and the transcription factor Mad. J. Neurobiol. 2003, 55:134-150.
57. Regehr W.G., Carey M.R., Best A.R. Activity-dependent regulation of synapses by retrograde messengers. Neuron 2009, 63:154-170.
58. Rodal A.A., Motola-Barnes R.N., Littleton J.T. Nervous wreck and Cdc42 cooperate to regulate endocytic actin assembly during synaptic growth. J. Neurosci. 2008, 28:8316-8325.
59. Sanchez-Soriano N., Tear G., Whitington P., Prokop A. Drosophila as a genetic and cellular model for studies on axonal growth. Neural Dev. 2007, 2:9.
60. Schenck A., Qurashi A., Carrera P., Bardoni B., Diebold C., Schejter E., Mandel J.L., Giangrande A. WAVE/SCAR, a multifunctional complex coordinating different aspects of neuronal connectivity. Dev. Biol. 2004, 274:260-270.
61. Schuster C.M., Davis G.W., Fetter R.D., Goodman C.S. Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron 1996, 17:641-654.
62. Sekelsky J.J., Newfeld S.J., Raftery L.A., Chartoff E.H., Gelbart W.M. Genetic characterization and cloning of mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics 1995, 139:1347-1358.
63. Shamah S.M., Lin M.Z., Goldberg J.L., Estrach S., Sahin M., Hu L., Bazalakova M., Neve R.L., Corfas G., Debant A., Greenberg M.E. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 2001, 105:233-244.
64. Sone M., Hoshino M., Suzuki E., Kuroda S., Kaibuchi K., Nakagoshi H., Saigo K., Nabeshima Y., Hama C. Still life, a protein in synaptic terminals of Drosophila homologous to GDP-GTP exchangers. Science 1997, 275:543-547.
65. Sone M., Suzuki E., Hoshino M., Hou D., Kuromi H., Fukata M., Kuroda S., Kaibuchi K., Nabeshima Y., Hama C. Synaptic development is controlled in the periactive zones of Drosophila synapses. Development 2000, 127:4157-4168.
66. Steven R., Kubiseski T.J., Zheng H., Kulkarni S., Mancillas J., Ruiz Morales A., Hogue C.W., Pawson T., Culotti J. UNC-73 activates the Rac GTPase and is required for cell and growth cone migrations in C. elegans. Cell 1998, 92:785-795.
67. Stewart B.A., Atwood H.L., Renger J.J., Wang J., Wu C.F. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J. Comp. Physiol. [A] 1994, 175:179-191.
68. Strutt D.I., Weber U., Mlodzik M. The role of RhoA in tissue polarity and Frizzled signalling. Nature 1997, 387:292-295.
69. Thomas S., Ritter B., Verbich D., Sanson C., Bourbonnière L., McKinney R.A., McPherson P.S. Intersectin regulates dendritic spine development and somatodendritic endocytosis but not synaptic vesicle recycling in hippocampal neurons. J. Biol. Chem. 2009, 284:12410-12419.
70. 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.
71. Twombly V., Blackman R.K., Jin H., Graff J.M., Padgett R.W., Gelbart W.M. The TGF-beta signaling pathway is essential for Drosophila oogenesis. Development 1996, 122:1555-1565.
72. Twombly V., Bangi E., Le V., Malnic B., Singer M.A., Wharton K.A. Functional analysis of saxophone, the Drosophila gene encoding the bmp type I receptor orthologue of human ALK1/ACVRL1 and ACVR1/ALK2. Genetics 2009, 183:563-579.
73. Van Aelst L., Cline H.T. Rho GTPases and activity-dependent dendrite development. Curr. Opin. Neurobiol. 2004, 14:297-304.
74. Watabe-Uchida M., Govek E.E., Van Aelst L. Regulators of Rho GTPases in neuronal development. J. Neurosci. 2006, 26:10633-10635.
75. Wharton K.A., Cook J.M., Torres-Schumann S., de Castro K., Borod E., Phillips D.A. Genetic analysis of the bone morphogenetic protein-related gene, gbb, identifies multiple requirements during Drosophila development. Genetics 1999, 152:629-640.
76. Yang L., Bashaw G.J. Son of sevenless directly links the Robo receptor to rac activation to control axon repulsion at the midline. Neuron 2006, 52:595-607.
77. Zeng Y.A., Rahnama M., Wang S., Sosu-Sedzorme W., Verheyen E.M. Drosophila Nemo antagonizes BMP signaling by phosphorylation of Mad and inhibition of its nuclear accumulation. Development 2007, 134:2061-2071.