Highwire regulates presynaptic BMP signaling essential for synaptic growth

Neuron

Volumn 41, Issue 6, 2004, Pages 891-905

  McCabe, Brian D ^a   Hom, Sabrina ^a   Aberle, Hermann ^a,c   Fetter, Richard D ^a,d   Marques, Guillermo ^b,e   Haerry, Theodore E ^b,f   Wan, Hong ^a,g   O'Connor, Michael B ^b   Goodman, Corey S ^a,g   Haghighi, A Pejmun ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c Max Planck Institutes   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f FLORIDA ATLANTIC UNIVERSITY   (United States)

^g EVOTEC AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; SMAD PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MAD; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE HIGHWIRE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; GENE MUTATION; IMMUNOHISTOCHEMISTRY; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PHENOTYPE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL SIZE; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MICROSCOPY, ELECTRON; MOTOR NEURONS; MUTATION; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; PRESYNAPTIC TERMINALS; PROTEIN BINDING; RECEPTORS, CELL SURFACE; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; SYNAPTIC TRANSMISSION; TRANS-ACTIVATORS;

EID: 12144289951     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(04)00073-X     Document Type: Article

References (70)

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. 33:2002;545-558.
2. Agatep, R., Kirkpatrick, R.D., Parchaliuk, R.A., Woods, R.A., and Gietz, R.D. (1998). Transformation of Saccharomyces cerevisiae by the lithium acetate/single-stranded carrier DNA/polyethylene glycol (LiAc/ss-DNA/PEG) protocol. Technical Tips Online, http://tto.trends.com.
3. Attisano L., Wrana J.L. Signal transduction by the TGF-beta superfamily. Science. 296:2002;1646-1647.
4. Bailey C.H., Kandel E.R. Structural changes accompanying memory storage. Annu. Rev. Physiol. 55:1993;397-426.
5. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 118:1993;401-415.
6. Brummel T.J., Twombly V., Marques G., Wrana J.L., Newfeld S.J., Attisano L., Massague J., O'Connor M.B., Gelbart W.M. Characterization and relationship of Dpp receptors encoded by the saxophone and thick veins genes in Drosophila. Cell. 78:1994;251-261.
7. 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. 13:1999;98-111.
8. Burbea M., Dreier L., Dittman J.S., Grunwald M.E., Kaplan J.M. Ubiquitin and AP180 regulate the abundance of GLR-1 glutamate receptors at postsynaptic elements in C. elegans. Neuron. 35:2002;107-120.
9. Ciechanover A., Orian A., Schwartz A.L. Ubiquitin-mediated proteolysis. biological regulation via destruction Bioessays. 22:2000;442-451.
10. Cline H.T. Dendritic arbor development and synaptogenesis. Curr. Opin. Neurobiol. 11:2001;118-126.
11. de Celis J.F. Expression and function of decapentaplegic and thick veins during the differentiation of the veins in the Drosophila wing. Development. 124:1997;1007-1018.
12. DiAntonio A., Haghighi A.P., Portman S.L., Lee J.D., Amaranto A.M., Goodman C.S. Ubiquitination-dependent mechanisms regulate synaptic growth and function. Nature. 412:2001;449-452.
13. Ehlers M.D. Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat. Neurosci. 6:2003;231-242.
14. Feng X.H., Derynck R. Ligand-independent activation of transforming growth factor (TGF) beta signaling pathways by heteromeric cytoplasmic domains of TGF-beta receptors. J. Biol. Chem. 271:1996;13123-13129.
15. Freemont P.S. RING for destruction? Curr. Biol. 10:2000;R84-R87.
16. Guan K.L., Deschenes R.J., Qiu H., Dixon J.E. Cloning and expression of a yeast protein tyrosine phosphatase. J. Biol. Chem. 266:1991;12964-12970.
17. Guo Q., Xie J., Dang C.V., Liu E.T., Bishop J.M. Identification of a large Myc-binding protein that contains RCC1-like repeats. Proc. Natl. Acad. Sci. USA. 95:1998;9172-9177.
18. Haerry T.E., Khalsa O., O'Connor M.B., Wharton K.A. Synergistic signaling by two BMP ligands through the SAX and TKV receptors controls wing growth and patterning in Drosophila. Development. 125:1998;3977-3987.
19. 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. 39:2003;255-267.
20. Hegde A.N., DiAntonio A. Ubiquitin and the synapse. Nat. Rev. Neurosci. 3:2002;854-861.
21. Henderson K.D., Isaac D.D., Andrew D.J. Cell fate specification in the Drosophila salivary gland. the integration of homeotic gene function with the DPP signaling cascade Dev. Biol. 205:1999;10-21.
22. Holley S.A., Neul J.L., Attisano L., Wrana J.L., Sasai Y., O'Connor M.B., De Robertis E.M., Ferguson E.L. The Xenopus dorsalizing factor noggin ventralizes Drosophila embryos by preventing DPP from activating its receptor. Cell. 86:1996;607-617.
23. 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. 85:1996;489-500.
24. Hu H., Marton T.F., Goodman C.S. Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting active Rac and enhancing RhoA signaling. Neuron. 32:2001;39-51.
25. Huang Y., Baker R.T., Fischer-Vize J.A. Control of cell fate by a deubiquitinating enzyme encoded by the fat facets gene. Science. 270:1995;1828-1831.
26. James P. Yeast two-hybrid vectors and strains. Methods Mol. Biol. 177:2001;41-84.
27. Jazwinska A., Rushlow C., Roth S. The role of brinker in mediating the graded response to Dpp in early Drosophila embryos. Development. 126:1999;3323-3334.
28. Knott G.W., Quairiaux C., Genoud C., Welker E. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron. 34:2002;265-273.
29. Letsou A., Arora K., Wrana J.L., Simin K., Twombly V., Jamal J., Staehling-Hampton K., Hoffmann F.M., Gelbart W.M., Massague J.et al. Drosophila Dpp signaling is mediated by the punt gene product. a dual ligand-binding type II receptor of the TGF beta receptor family Cell. 80:1995;899-908.
30. Lorick K.L., Jensen J.P., Fang S., Ong A.M., Hatakeyama S., Weissman A.M. RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc. Natl. Acad. Sci. USA. 96:1999;11364-11369.
31. 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. 8:1994;1787-1802.
32. Marqués G., Bao H., Haerry T.E., Shimell M.J., Duchek P., Zhang B., O'Connor M.B. The Drosophila BMP type II recptor Wishful Thinking regulates neuromuscular synapse morphology and function. Neuron. 33:2002;529-543.
33. Marqués 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. 130:2003;5457-5470.
34. Massague J. TGF-beta signal transduction. Annu. Rev. Biochem. 67:1998;753-791.
35. 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. 39:2003;241-254.
36. Mel B.W. Have we been hebbing down the wrong path? Neuron. 34:2002;175-177.
37. Myat A., Henry P., McCabe V., Flintoft L., Rotin D., Tear G. Drosophila Nedd4, a ubiquitin ligase, is recruited by Commissureless to control cell surface levels of the roundabout receptor. Neuron. 35:2002;447-459.
38. Nellen D., Affolter M., Basler K. Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic. Cell. 78:1994;225-237.
39. 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. 32:2001;415-424.
40. Pickart C.M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70:2001;503-533.
41. Raftery L.A., Sutherland D.J. TGF-beta family signal transduction in Drosophila development. from Mad to Smads Dev. Biol. 210:1999;251-268.
42. Raftery L.A., Twombly V., Wharton K., Gelbart W.M. Genetic screens to identify elements of the decapentaplegic signaling pathway in Drosophila. Genetics. 139:1995;241-254.
43. 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. 55:2003;134-150.
44. Ruberte E., Marty T., Nellen D., Affolter M., Basler K. An absolute requirement for both the type II and type I receptors, punt and thick veins, for dpp signaling in vivo. Cell. 80:1995;889-897.
45. Schaefer A.M., Hadwiger G.D., Nonet M.L. rpm-1, a conserved neuronal gene that regulates targeting and synaptogenesis in C. elegans. Neuron. 26:2000;345-356.
46. 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. 17:1996;655-667.
47. 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. 139:1995;1347-1358.
48. Simin K., Bates E.A., Horner M.A., Letsou A. Genetic analysis of punt, a type II Dpp receptor that functions throughout the Drosophila melanogaster life cycle. Genetics. 148:1998;801-813.
49. 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. 275:1997;543-547.
50. Speese S.D., Trotta N., Rodesch C.K., Aravamudan B., Broadie K. The ubiquitin proteasome system acutely regulates presynaptic protein turnover and synaptic efficacy. Curr. Biol. 13:2003;899-910.
51. Stepanyants A., Hof P.R., Chklovskii D.B. Geometry and structural plasticity of synaptic connectivity. Neuron. 34:2002;275-288.
52. Sweeney S.T., Davis G.W. Unrestricted synaptic growth in spinster - a late endosomal protein implicated in TGF-beta-mediated synaptic growth regulation. Neuron. 36:2002;403-416.
53. Tanimoto H., Itoh S., ten Dijke P., Tabata T. Hedgehog creates a gradient of DPP activity in Drosophila wing imaginal discs. Mol. Cell. 5:2000;59-71.
54. Tomoyasu Y., Nakamura M., Ueno N. Role of dpp signalling in prepattern formation of the dorsocentral mechanosensory organ in Drosophila melanogaster. Development. 125:1998;4215-4224.
55. Trachtenberg J.T., Chen B.E., Knott G.W., Feng G., Sanes J.R., Welker E., Svoboda K. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature. 420:2002;788-794.
56. Tsuneizumi K., Nakayama T., Kamoshida Y., Kornberg T.B., Christian J.L., Tabata T. Daughters against dpp modulates dpp organizing activity in Drosophila wing development. Nature. 389:1997;627-631.
57. 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. 122:1996;1555-1565.
58. Wan H.I., DiAntonio A., Fetter R.D., Bergstrom K., Strauss R., Goodman C.S. Highwire regulates synaptic growth in Drosophila. Neuron. 26:2000;313-329.
59. Watts R.J., Hoopfer E.D., Luo L. Axon pruning during Drosophila metamorphosis. evidence for local degeneration and requirement of the ubiquitin-proteasome system Neuron. 38:2003;871-885.
60. Wisotzkey R.G., Mehra A., Sutherland D.J., Dobens L.L., Liu X., Dohrmann C., Attisano L., Raftery L.A. Medea is a Drosophila Smad4 homolog that is differentially required to potentiate DPP responses. Development. 125:1998;1433-1445.
61. Wrana J.L., Attisano L. The Smad pathway. Cytokine Growth Factor Rev. 11:2000;5-13.
62. Wrana J.L., Attisano L., Wieser R., Ventura F., Massague J. Mechanism of activation of the TGF-beta receptor. Nature. 370:1994;341-347. a.
63. Wrana J.L., Tran H., Attisano L., Arora K., Childs S.R., Massague J., O'Connor M.B. Two distinct transmembrane serine/threonine kinases from Drosophila melanogaster form an activin receptor complex. Mol. Cell. Biol. 14:1994;944-950. b.
64. Wu Z., Li Q., Fortini M.E., Fischer J.A. Genetic analysis of the role of the drosophila fat facets gene in the ubiquitin pathway. Dev. Genet. 25:1999;312-320.
65. Xie T., Finelli A.L., Padgett R.W. The Drosophila saxophone gene. a serine-threonine kinase receptor of the TGF-beta superfamily Science. 263:1994;1756-1759.
66. Yang H., Scholich K., Poser S., Storm D.R., Patel T.B., Goldowitz D. Developmental expression of PAM (protein associated with MYC) in the rodent brain. Brain Res. Dev. Brain Res. 136:2002;35-42.
67. Yuste R., Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 24:2001;1071-1089.
68. Zhen M., Huang X., Bamber B., Jin Y. Regulation of presynaptic terminal organization by C. elegans RPM-1, a putative guanine nucleotide exchanger with a RING-H2 finger domain. Neuron. 26:2000;331-343.
69. 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. 112:2003;303-315.
70. Zito K., Svoboda K. Activity-dependent synaptogenesis in the adult mammalian cortex. Neuron. 35:2002;1015-1017.