Activin signaling functions upstream of Gbb to regulate synaptic growth at the Drosophila neuromuscular junction

Developmental Biology

Volumn 342, Issue 2, 2010, Pages 121-133

  Ellis, J E ^a   Parker, L ^a,b   Cho, J ^a   Arora, K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Activin; Baboon; BMP; Dawdle; Drosophila; DSmad2; Futsch; Neuromuscular junction; Synaptic development; TGF

Indexed keywords

ACTIVIN; BONE MORPHOGENETIC PROTEIN; DAWDLE PROTEIN; GLASS BOTTOM BOAT PROTEIN; LIGAND; MICROTUBULE ASSOCIATED PROTEIN 1; MUTANT PROTEIN; PROTEIN; SMAD2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DROSOPHILA; LARVA; MICROTUBULE; NERVE FIBER TRANSPORT; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NEUROMUSCULAR SYNAPSE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYNAPSE; TRANSCRIPTION REGULATION;

PAPIO; VERTEBRATA;

EID: 77952951329     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.03.012     Document Type: Article

References (73)

1. Aberle H., Haghighi A.P., Fetter R.D., McCabe B.D., Magalhaes 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. Alon U. Network motifs: theory and experimental approaches. Nat. Rev. Genet. 2007, 8:450-461.
3. Atwood H.L., Govind C.K., Wu C.F. Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J. Neurobiol. 1993, 24:1008-1024.
4. Bettencourt da Cruz A., Schwarzel M., Schulze S., Niyyati M., Heisenberg M., Kretzschmar D. Disruption of the MAP1B-related protein FUTSCH leads to changes in the neuronal cytoskeleton, axonal transport defects, and progressive neurodegeneration in Drosophila. Mol. Biol. Cell 2005, 16:2433-2442.
5. Brummel T., Abdollah S., Haerry T.E., Shimell M.J., Merriam J., Raftery L., Wrana J.L., O'Connor M.B. The Drosophila activin receptor baboon signals through dSmad2 and controls cell proliferation but not patterning during larval development. Genes Dev. 1999, 13:98-111.
6. Budnik V., Gorczyca M. SSB, an antigen that selectively labels morphologically distinct synaptic boutons at the Drosophila larval neuromuscular junction. J. Neurobiol. 1992, 23:1054-1065.
7. Budnik V., Zhong Y., Wu C.F. Morphological plasticity of motor axons in Drosophila mutants with altered excitability. J. Neurosci. 1990, 10:3754-3768.
8. Collins C.A., DiAntonio A. Synaptic development: insights from Drosophila. Curr. Opin. Neurobiol. 2007, 17:35-42.
9. Das P., Inoue H., Baker J.C., Beppu H., Kawabata M., Harland R.M., Miyazono K., Padgett R.W. Drosophila dSmad2 and Atr-I transmit activin/TGFbeta signals. Genes Cells 1999, 4:123-134.
10. Davis G.W., Bezprozvanny I. Maintaining the stability of neural function: a homeostatic hypothesis. Annu. Rev. Physiol. 2001, 63:847-869.
11. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., Couto A., Marra V., Keleman K., Dickson B.J. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
12. Eaton B.A., Davis G.W. LIM Kinase1 controls synaptic stability downstream of the type II BMP receptor. Neuron 2005, 47:695-708.
13. Eaton B.A., Fetter R.D., Davis G.W. Dynactin is necessary for synapse stabilization. Neuron 2002, 34:729-741.
14. Gesualdi S.C., Haerry T.E. Distinct signaling of Drosophila Activin/TGF-beta family members. Fly (Austin) 2007, 1:212-221.
15. Gibson M.C., Perrimon N. Extrusion and death of DPP/BMP-compromised epithelial cells in the developing Drosophila wing. Science 2005, 307:1785-1789.
16. Gogel S., Wakefield S., Tear G., Klambt C., Gordon-Weeks P.R. The Drosophila microtubule associated protein Futsch is phosphorylated by Shaggy/Zeste-white 3 at an homologous GSK3beta phosphorylation site in MAP1B. Mol. Cell Neurosci. 2006, 33:188-199.
17. 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.
18. Goold R.G., Owen R., Gordon-Weeks P.R. Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J. Cell Sci. 1999, 112(Pt 19):3373-3384.
19. Griffith L.C., Budnik V. Plasticity and second messengers during synapse development. Int. Rev. Neurobiol. 2006, 75:237-265.
20. Gunawardena S., Her L.S., Brusch R.G., Laymon R.A., Niesman I.R., Gordesky-Gold B., Sintasath L., Bonini N.M., Goldstein L.S. Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 2003, 40:25-40.
21. 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.
22. Hummel T., Krukkert K., Roos J., Davis G., Klambt C. Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 2000, 26:357-370.
23. Hurd D.D., Saxton W.M. Kinesin mutations cause motor neuron disease phenotypes by disrupting fast axonal transport in Drosophila. Genetics 1996, 144:1075-1085.
24. Jin S., Pan L., Liu Z., Wang Q., Xu Z., Zhang Y.Q. Drosophila Tubulin-specific chaperone E functions at neuromuscular synapses and is required for microtubule network formation. Development 2009, 136:1571-1581.
25. Kerjan G., Gleeson J.G. Genetic mechanisms underlying abnormal neuronal migration in classical lissencephaly. Trends Genet. 2007, 23:623-630.
26. Keshishian H., Kim Y.S. Orchestrating development and function: retrograde BMP signaling in the Drosophila nervous system. Trends Neurosci. 2004, 27:143-147.
27. Keshishian H., Chiba A., Chang T.N., Halfon M.S., Harkins E.W., Jarecki J., Wang L., Anderson M., Cash S., Halpern M.E., et al. Cellular mechanisms governing synaptic development in Drosophila melanogaster. J. Neurobiol. 1993, 24:757-787.
28. Koch I., Schwarz H., Beuchle D., Goellner B., Langegger M., Aberle H. Drosophila ankyrin 2 is required for synaptic stability. Neuron 2008, 58:210-222.
29. Kurdyak P., Atwood H.L., Stewart B.A., Wu C.F. Differential physiology and morphology of motor axons to ventral longitudinal muscles in larval Drosophila. J. Comp. Neurol. 1994, 350:463-472.
30. Lahey T., Gorczyca M., Jia X.X., Budnik V. The Drosophila tumor suppressor gene dlg is required for normal synaptic bouton structure. Neuron 1994, 13:823-835.
31. Lecuit T., Brook W.J., Ng M., Calleja M., Sun H., Cohen S.M. Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 1996, 381:387-393.
32. Lo P.C., Frasch M. Sequence and expression of myoglianin, a novel Drosophila gene of the TGF-beta superfamily. Mech. Dev. 1999, 86:171-175.
33. Marques G. Morphogens and synaptogenesis in Drosophila. J. Neurobiol. 2005, 64:417-434.
34. Marques G., Zhang B. Retrograde signaling that regulates synaptic development and function at the Drosophila neuromuscular junction. Int. Rev. Neurobiol. 2006, 75:267-285.
35. Marques 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.
36. Marques G., Haerry T.E., Crotty M.L., Xue M., Zhang B., O'Connor M.B. Retrograde Gbb signaling through the Bmp type 2 receptor wishful thinking regulates systemic FMRFa expression in Drosophila. Development 2003, 130:5457-5470.
37. Mathew D., Ataman B., Chen J., Zhang Y., Cumberledge S., Budnik V. Wingless signaling at synapses is through cleavage and nuclear import of receptor DFrizzled2. Science 2005, 310:1344-1347.
38. McCabe B.D., Marques 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.
39. 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.
40. Nellen D., Burke R., Struhl G., Basler K. Direct and long-range action of a DPP morphogen gradient. Cell 1996, 85:357-368.
41. Nguyen M., Parker L., Arora K. Identification of maverick, a novel member of the TGF-beta superfamily in Drosophila. Mech. Dev. 2000, 95:201-206.
42. Nishimura A.L., Mitne-Neto M., Silva H.C., Richieri-Costa A., Middleton S., Cascio D., Kok F., Oliveira J.R., Gillingwater T., Webb J., Skehel P., Zatz M. A mutation in the vesicle-trafficking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. Am. J. Hum. Genet. 2004, 75:822-831.
43. O'Connor-Giles K.M., Ho L.L., Ganetzky B. Nervous wreck interacts with thickveins and the endocytic machinery to attenuate retrograde BMP signaling during synaptic growth. Neuron 2008, 58:507-518.
44. Packard M., Mathew D., Budnik V. Wnts and TGF beta in synaptogenesis: old friends signalling at new places. Nat. Rev. Neurosci. 2003, 4:113-120.
45. Pack-Chung E., Kurshan P.T., Dickman D.K., Schwarz T.L. A Drosophila kinesin required for synaptic bouton formation and synaptic vesicle transport. Nat. Neurosci. 2007, 10:980-989.
46. Paradis S., Sweeney S.T., Davis G.W. Homeostatic control of presynaptic release is triggered by postsynaptic membrane depolarization. Neuron 2001, 30:737-749.
47. Parker L., Ellis J.E., Nguyen M.Q., Arora K. The divergent TGF-beta ligand Dawdle utilizes an activin pathway to influence axon guidance in Drosophila. Development 2006, 133:4981-4991.
48. Parvari R., Hershkovitz E., Grossman N., Gorodischer R., Loeys B., Zecic A., Mortier G., Gregory S., Sharony R., Kambouris M., Sakati N., Meyer B.F., Al Aqeel A.I., Al Humaidan A.K., Al Zanhrani F., Al Swaid A., Al Othman J., Diaz G.A., Weiner R., Khan K.T., Gordon R., Gelb B.D. Mutation of TBCE causes hypoparathyroidism-retardation-dysmorphism and autosomal recessive Kenny-Caffey syndrome. Nat. Genet. 2002, 32:448-452.
49. Pennetta G., Hiesinger P.R., Fabian-Fine R., Meinertzhagen I.A., Bellen H.J. Drosophila VAP-33A directs bouton formation at neuromuscular junctions in a dosage-dependent manner. Neuron 2002, 35:291-306.
50. Pereira H.S., MacDonald D.E., Hilliker A.J., Sokolowski M.B. Chaser (Csr), a new gene affecting larval foraging behavior in Drosophila melanogaster. Genetics 1995, 141:263-270.
51. Piperno G., Fuller M.T. Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms. J. Cell Biol. 1985, 101:2085-2094.
52. Prokop A. Organization of the efferent system and structure of neuromuscular junctions in Drosophila. Int. Rev. Neurobiol. 2006, 75:71-90.
53. Ranganayakulu G., Schulz R.A., Olson E.N. Wingless signaling induces nautilus expression in the ventral mesoderm of the Drosophila embryo. Dev. Biol. 1996, 176:143-148.
54. 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.
55. Riederer B.M. Microtubule-associated protein 1B, a growth-associated and phosphorylated scaffold protein. Brain Res. Bull. 2007, 71:541-558.
56. Roos J., Hummel T., Ng N., Klambt C., Davis G.W. Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 2000, 26:371-382.
57. Ruiz-Canada C., Budnik V. Synaptic cytoskeleton at the neuromuscular junction. Int. Rev. Neurobiol. 2006, 75:217-236.
58. Ruiz-Canada C., Ashley J., Moeckel-Cole S., Drier E., Yin J., Budnik V. New synaptic bouton formation is disrupted by misregulation of microtubule stability in aPKC mutants. Neuron 2004, 42:567-580.
59. Salinas S., Carazo-Salas R.E., Proukakis C., Schiavo G., Warner T.T. Spastin and microtubules: functions in health and disease. J. Neurosci. Res. 2007, 85:2778-2782.
60. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3:1101-1108.
61. Schuster C.M., Davis G.W., Fetter R.D., Goodman C.S. Genetic dissection of structural and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron 1996, 17:655-667.
62. Serpe M., O'Connor M.B. The metalloprotease tolloid-related and its TGF-beta-like substrate Dawdle regulate Drosophila motoneuron axon guidance. Development 2006, 133:4969-4979.
63. Sherwood N.T., Sun Q., Xue M., Zhang B., Zinn K. Drosophila spastin regulates synaptic microtubule networks and is required for normal motor function. PLoS Biol. 2004, 2:e429.
64. Sweeney S.T., Davis G.W. Unrestricted synaptic growth in spinster-a late endosomal protein implicated in TGF-beta-mediated synaptic growth regulation. Neuron 2002, 36:403-416.
65. Ting C.Y., Herman T., Yonekura S., Gao S., Wang J., Serpe M., O'Connor M.B., Zipursky S.L., Lee C.H. Tiling of r7 axons in the Drosophila visual system is mediated both by transduction of an activin signal to the nucleus and by mutual repulsion. Neuron 2007, 56:793-806.
66. Trotta N., Orso G., Rossetto M.G., Daga A., Broadie K. The hereditary spastic paraplegia gene, spastin, regulates microtubule stability to modulate synaptic structure and function. Curr. Biol. 2004, 14:1135-1147.
67. Wang X., Shaw W.R., Tsang H.T., Reid E., O'Kane C.J. Drosophila spichthyin inhibits BMP signaling and regulates synaptic growth and axonal microtubules. Nat. Neurosci. 2007, 10:177-185.
68. White B.H., Osterwalder T.P., Yoon K.S., Joiner W.J., Whim M.D., Kaczmarek L.K., Keshishian H. Targeted attenuation of electrical activity in Drosophila using a genetically modified K(+) channel. Neuron 2001, 31:699-711.
69. Zhang Y.Q., Bailey A.M., Matthies H.J., Renden R.B., Smith M.A., Speese S.D., Rubin G.M., Broadie K. Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell 2001, 107:591-603.
70. Zheng X., Wang J., Haerry T.E., Wu A.Y., Martin J., O'Connor M.B., Lee C.H., Lee T. TGF-beta signaling activates steroid hormone receptor expression during neuronal remodeling in the Drosophila brain. Cell 2003, 112:303-315.
71. Zheng X., Zugates C.T., Lu Z., Shi L., Bai J.M., Lee T. Baboon/dSmad2 TGF-beta signaling is required during late larval stage for development of adult-specific neurons. Embo J. 2006, 25:615-627.
72. Zhu C.C., Boone J.Q., Jensen P.A., Hanna S., Podemski L., Locke J., Doe C.Q., O'Connor M.B. Drosophila Activin- and the Activin-like product Dawdle function redundantly to regulate proliferation in the larval brain. Development 2008, 135:513-521.
73. Zito K., Parnas D., Fetter R.D., Isacoff E.Y., Goodman C.S. Watching a synapse grow: noninvasive confocal imaging of synaptic growth in Drosophila. Neuron 1999, 22:719-729.