Identification of downstream targets of the bone morphogenetic protein pathway in the Drosophila nervous system

Developmental Dynamics

Volumn 239, Issue 9, 2010, Pages 2413-2425

  Kim, Nam Chul ^a   Marqués, Guillermo ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Expression profiling; Microarray; Motoneuron; Wishful thinking

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CARRIER PROTEIN; MITOCHONDRIAL PROTEIN; NEUROPEPTIDE;

ARTICLE; DEVELOPMENTAL GENE; DROSOPHILA; GENE EXPRESSION PROFILING; INSECT GENETICS; LARVAL DEVELOPMENT; MICROARRAY ANALYSIS; NERVOUS SYSTEM DEVELOPMENT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CENTRAL NERVOUS SYSTEM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICROARRAY ANALYSIS; MOLECULAR SEQUENCE DATA; RECEPTORS, CELL SURFACE; REPRODUCIBILITY OF RESULTS; RNA SPLICING; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

MAMMALIA;

EID: 77956274236     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22368     Document Type: Article

References (72)

1. Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magalhaes TR, Goodman CS. 2002. wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33:545-558.
2. Allan DW, Pierre SE, Miguel-Aliaga I, Thor S. 2003. Specification of neuropeptide cell identity by the integration of retrograde BMP signaling and a combinatorial transcription factor code. Cell 113:73-86.
3. Baines RA. 2004. Synaptic strengthening mediated by bone morphogenetic protein-dependent retrograde signaling in the Drosophila CNS. J Neurosci 24:6904-6911.
4. Berman BP, Nibu Y, Pfeiffer BD, Tomancak P, Celniker SE, Levine M, Rubin GM, Eisen MB. 2002. Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc Natl Acad Sci 99:757-762.
5. Bovolenta P. 2005. Morphogen signaling at the vertebrate growth cone: a few cases or a general strategy? J Neurobiol 64:405-416.
6. Brennecke J, Stark A, Russell RB, Cohen SM. 2005. Principles of microRNA-target recognition. PLoS Biol 3:e85.
7. Cayuso J, Marti E. 2005. Morphogens in motion: growth control of the neural tube. J Neurobiol 64:376-387.
8. Chung H, Sztal T, Pasricha S, Sridhar M, Batterham P, Daborn PJ. 2009. Characterization of Drosophila melanogaster cytochrome P450 genes. Proc Natl Acad Sci 106:5731-5736
9. Colak D, Mori T, Brill MS, Pfeifer A, Falk S, Deng C, Monteiro R, Mummery C, Sommer L, Gotz M. 2008. Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J Neurosci 28:434-446.
10. Daniels RW, Collins CA, Chen K, Gelfand MV, Featherstone DE, DiAntonio A. 2006. A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle. Neuron 49:11-16.
11. David CJ, Manley JL. 2008. The search for alternative splicing regulators: new approaches offer a path to a splicing code. Genes Dev 22:279-285.
12. Davis BN, Hilyard AC, Lagna G, Hata A. 2008. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454:56-61.
13. De Robertis EM, Kuroda H. 2004. Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 20:285-308.
14. Eaton BA, Davis GW. 2005. LIM Kinase1 controls synaptic stability downstream of the type II BMP receptor. Neuron 47:695-708.
15. Fukushima T, Liu R-Y, Byrne JH. 2007. Transforming growth factor-β2 modulates synaptic efficacy and plasticity and induces phosphorylation of CREB in hippocampal neurons. Hippocampus 17:5-9.
16. Gao S, Laughon A. 2007. Flexible interaction of Drosophila Smad complexes with bipartite binding sites. Biochim Biophys Acta 1769:484-496.
17. Gao S, Steffen J, Laughon A. 2005. Dpp-responsive silencers are bound by a trimeric Mad-Medea complex. J Biol Chem 280:36158-36164.
18. Genevieve D, Proulle V, Isidor B, Bellais S, Serre V, Djouadi F, Picard C, Vignon-Savoye C, Bader-Meunier B, Blanche S, de Vernejoul MC, Legeai-Mallet L, Fischer AM, Le Merrer M, Dreyfus M, Gaussem P, Munnich A, Cormier-Daire V. 2008. Thromboxane synthase mutations in an increased bone density disorder (Ghosal syndrome). Nat Genet 40:284-286.
19. Gerber B, Stocker RF. 2006. The Drosophila larva as a model for studying chemosensation and chemosensory learning: a review. Chem Senses 32:65-89.
20. Goold CP, Davis GW. 2007. The BMP ligand Gbb gates the expression of synaptic homeostasis independent of synaptic growth control. Neuron 56:109-123.
21. Grienenberger A, Merabet S, Manak J, Iltis I, Fabre A, Berenger H, Scott MP, Pradel J, Graba Y. 2003. Tgfbeta signaling acts on a Hox response element to confer specificity and diversity to Hox protein function. Development 130:5445-5455.
22. Halfon MS, Carmena A, Gisselbrecht S, Sackerson CM, Jimenez F, Baylies MK, Michelson AM. 2000. Ras pathway specificity is determined by the integration of multiple signal-activated and tissue-restricted transcription factors. Cell 103:63-74.
23. Harradine KA, Akhurst RJ. 2006. Mutations of TGFbeta signaling molecules in human disease. Ann Med 38:403-414.
24. Harrison SD, Solomon N, Rubin GM. 1995. A genetic analysis of the 63E-64A genomic region of Drosophila melanogaster: identification of mutations in a replication factor C Subunit. genetics 139:1701-1709.
25. Haussmann IU, White K, Soller M. 2008. Erect wing regulates synaptic growth in Drosophila by integration of multiple signaling pathways. Genome Biol 9:R73.
26. Herzog E, Takamori S, Jahn R, Brose N, Wojcik SM. 2006. Synaptic and vesicular co-localization of the glutamate transporters VGLUT1 and VGLUT2 in the mouse hippocampus. J Neurochem 99:1011-1018.
27. Hidalgo A, Learte AR, McQuilton P, Pennack J, Zhu B. 2006. Neurotrophic and gliatrophic contexts in Drosophila. Brain Behav Evol 68:173-180.
28. Hijazi A, Masson W, Auge B, Waltzer L, Haenlin M, Roch F. 2009. boudin is required for septate junction organisation in Drosophila and codes for a diffusible protein of the Ly6 superfamily. Development 136:2199-2209.
29. Hodge LK, Klassen MP, Han B-X, Yiu G, Hurrell J, Howell A, Rousseau G, Lemaigre F, Tessier-Lavigne M, Wang F. 2007. Retrograde BMP signaling regulates trigeminal sensory neuron identities and the formation of precise face maps. Neuron 55:572.
30. Kanadia RN, Cepko CL. 2010. Alternative splicing produces high levels of noncoding isoforms of bHLH transcription factors during development. Genes Dev 24:229-234.
31. Kim J, Johnson K, Chen HJ, Carroll S, Laughon A. 1997. Drosophila Mad binds to DNA and directly mediates activation of vestigial by Decapentaplegic. Nature 388:304-308.
32. Knirr S, Frasch M. 2001. Molecular integration of inductive and mesoderm-intrinsic inputs governs even-skipped enhancer activity in a subset of pericardial and dorsal muscle progenitors. Dev Biol 238:13-26.
33. Lee HH, Frasch M. 2005. Nuclear integration of positive Dpp signals, antagonistic Wg inputs and mesodermal competence factors during Drosophila visceral mesoderm induction. Development 132:1429-1442.
34. Lee MK, Pardoux C, Hall MC, Lee PS, Warburton D, Qing J, Smith SM, Derynck R. 2007. TGF-beta activates Erk MAP kinase signalling through direct phosphorylation of ShcA. Embo J 26:3957-3967.
35. Levine AJ, Brivanlou AH. 2007. Proposal of a model of mammalian neural induction. Dev Biol 308:247-256.
36. Leyssen M, Hassan BA. 2007. A fruitfly's guide to keeping the brain wired. EMBO Rep 8:46-50.
37. Lin MC, Park J, Kirov N, Rushlow C. 2006. Threshold response of C15 to the Dpp gradient in Drosophila is established by the cumulative effect of Smad and Zen activators and negative cues. Development 133:4805-4813.
38. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
39. Luan H, Lemon WC, Peabody NC, Pohl JB, Zelensky PK, Wang D, Nitabach MN, Holmes TC, White BH. 2006. Functional dissection of a neuronal network required for cuticle tanning and wing expansion in Drosophila. J Neurosci 26:573-584.
40. Markstein M, Markstein P, Markstein V, Levine MS. 2002. Genome-wide analysis of clustered Dorsal binding sites identifies putative target genes in the Drosophila embryo. Proc Natl Acad Sci USA 99:763-768.
41. Marqués G, Zhang B. 2006. Retrograde signaling that regulates synaptic development and function at the Drosophila neuromuscular junction. Int Rev Neurobiol 75:267-285.
42. Marqués G, Bao H, Haerry TE, Shimell MJ, Duchek P, Zhang B, O'Connor MB. 2002. The Drosophila BMP type II receptor Wishful Thinking regulates neuromuscular synapse morphology and function. Neuron 33:529-543.
43. Marqués G, Haerry T, Crotty LM, Xue M, Zhang B, O'Connor MB. 2003. Retrograde Gbb signaling through the BMP type II receptor Wishful Thinking regulates systemic FMRFa expression in Drosophila. Development 130:5457-5470.
44. McCabe BD, Marques G, Haghighi AP, Fetter RD, Crotty ML, Haerry TE, Goodman CS, O'Connor MB. 2003. The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron 39:241-254.
45. McCabe BD, Hom S, Aberle H, Fetter RD, Marques G, Haerry TE, Wan H, O'Connor MB, Goodman CS, Haghighi AP. 2004. Highwire regulates presynaptic BMP signaling essential for synaptic growth. Neuron 41:891-905.
46. Miguel-Aliaga I, Allan DW, Thor S. 2004. Independent roles of the dachshund and eyes absent genes in BMP signaling, axon pathfinding and neuronal specification. Development 131:5837-5848.
47. Miguel-Aliaga I, Thor S, Gould AP. 2008. Postmitotic specification of Drosophila insulinergic neurons from pioneer neurons. PLoS Biology 6:e58.
48. Miwa JM, Ibanez-Tallon I, Crabtree GW, Sanchez R, Sali A, Role LW, Heintz N. 1999. lynx1, an endogenous toxin-like modulator of nicotinic acetylcholine receptors in the mammalian CNS. Neuron 23:105-114.
49. Miwa JM, Stevens TR, King SL, Caldarone BJ, Ibanez-Tallon I, Xiao C, Fitzsimonds RM, Pavlides C, Lester HA, Picciotto MR, Heintz N. 2006. The prototoxin lynx1 acts on nicotinic acetylcholine receptors to balance neuronal activity and survival in vivo. Neuron 51:587-600.
50. Muller B, Hartmann B, Pyrowolakis G, Affolter M, Basler K. 2003. Conversion of an extracellular Dpp/BMP morphogen gradient into an inverse transcriptional gradient. Cell 113:221-233.
51. Penalva LO, Sanchez L. 2003. RNA binding protein sex-lethal (Sxl) and control of Drosophila sex determination and dosage compensation. Microbiol Mol Biol Rev 67:343-359.
52. Pyrowolakis G, Hartmann B, Muller B, Basler K, Affolter M. 2004. A simple molecular complex mediates widespread BMP-induced repression during Drosophila development. Dev Cell 7:229-240.
53. Rahimi RA, Leof EB. 2007. TGF-beta signaling: a tale of two responses. J Cell Biochem 102:593-608.
54. Rawson JM, Lee M, Kennedy EL, Selleck SB. 2003. Drosophila neuromuscular synapse assembly and function require the TGF-beta type I receptor saxophone and the transcription factor Mad. J Neurobiol 55:134-150.
55. Ross S, Hill CS. 2007. How the Smads regulate transcription. Int J Biochem Cell Biol 40:383-408.
56. Roy PJ, Stuart JM, Lund J, Kim SK. 2002. Chromosomal clustering of muscle-expressed genes in Caenorhabditis elegans. Nature 418:975-979.
57. Rushlow C, Colosimo PF, Lin MC, Xu M, Kirov N. 2001. Transcriptional regulation of the Drosophila gene zen by competing Smad and Brinker inputs. Genes Dev 15:340-351.
58. Salinas PC. 2005. Signaling at the vertebrate synapse: new roles for embryonic morphogens? J Neurobiol 64:435-445.
59. Sanchez-Soriano N, Tear G, Whitington P, Prokop A. 2007. Drosophila as a genetic and cellular model for studies on axonal growth. Neural Development 2:9.
60. Schmierer B, Hill CS. 2007. TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol 8:970-982.
61. Steward O, Schuman EM. 2003. Compartmentalized synthesis and degradation of proteins in neurons. Neuron 40:347-359.
62. Sun M, Thomas MJ, Herder R, Bofenkamp ML, Selleck SB, O'Connor MB. 2007. Presynaptic contributions of chordin to hippocampal plasticity and spatial learning. J Neurosci 27:7740.
63. Takahashi H, Liu FC. 2006. Genetic patterning of the mammalian telencephalon by morphogenetic molecules and transcription factors. Birth Defects Res C Embryo Today 78:256-266.
64. Trivedi P, Edwards JW, Wang J, Gadbury GL, Srinivasasainagendra V, Zakharkin SO, Kim K, Mehta T, Brand JP, Patki A, Page GP, Allison DB. 2005. HDBStat!: a platform-independent software suite for statistical analysis of high dimensional biology data. BMC Bioinformatics 6:86.
65. Walsh CM, Carroll SB. 2007. Collaboration between Smads and a Hox protein in target gene repression. Development 134:3585-3592.
66. Wang G-S, Cooper TA. 2007. Splicing in disease: disruption of the splicing code and the decoding machinery. Nat Rev Genet 8:749-761.
67. Wharton SJ, Basu SP, Ashe HL. 2004. Smad affinity can direct distinct readouts of the embryonic extracellular Dpp gradient in Drosophila. Curr Biol 14:1550-1558.
68. Wu MN, Joiner WJ, Dean T, Yue Z, Smith CJ, Chen D, Hoshi T, Sehgal A, Koh K. 2010. SLEEPLESS, a Ly-6/neurotoxin family member, regulates the levels, localization and activity of Shaker. Nat Neurosci 13:69-75.
69. Xu M, Kirov N, Rushlow C. 2005. Peak levels of BMP in the Drosophila embryo control target genes by a feed-forward mechanism. Development 132:1637-1647.
70. Xu X, Yin Z, Hudson JB, Ferguson EL, Frasch M. 1998. Smad proteins act in combination with synergistic and antagonistic regulators to target Dpp responses to the Drosophila mesoderm. Genes Dev 12:2354-2370.
71. Yang M, Nelson D, Funakoshi Y, Padgett RW. 2004. Genome-wide microarray analysis of TGFbeta signaling in the Drosophila brain. BMC Dev Biol 4:14.
72. Yao LC, Blitz IL, Peiffer DA, Phin S, Wang Y, Ogata S, Cho KW, Arora K, Warrior R. 2006. Schnurri transcription factors from Drosophila and vertebrates can mediate Bmp signaling through a phylogenetically conserved mechanism. Development 133:4025-4034.