TGF-β family signaling in drosophila

Cold Spring Harbor Perspectives in Biology

Volumn 9, Issue 9, 2017, Pages

  Upadhyay, Ambuj ^a   Moss Taylor, Lindsay ^a   Kim, Myung Jun ^a   Ghosh, Arpan C ^a   O’Connor, Michael B ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL; BODY PATTERNING; CYTOLOGY; DROSOPHILA; EMBRYOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMAGINAL DISC; METABOLISM; MOLECULAR MODEL; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; DROSOPHILA; IMAGINAL DISCS; METABOLIC NETWORKS AND PATHWAYS; MODELS, MOLECULAR; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 85023778873     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a022152     Document Type: Article

References (223)

1. Aberle H, Haghighi AP, Fetter RD, McCabe BD, Magalhães TR, Goodman CS. 2002. Wishful thinking encodes a BMP type II Receptor that regulates synaptic growth in Drosophila. Neuron 33: 545-558
2. Affolter M, Basler K. 2007. The decapentaplegic morphogen gradient: From pattern formation to growth regulation. Nat Rev Genet 8: 663-674
3. Akiyama T, Gibson MC. 2015. Decapentaplegic and growth control in the developing Drosophila wing. Nature 527: 375-378
4. Akiyama T, Kamimura K, Firkus C, Takeo S, Shimmi O, Nakato H. 2008. Dally regulates Dpp morphogen gradient formation by stabilizing Dpp on the cell surface. Dev Biol 313: 408-419
5. Akiyama T, Marques G, Wharton KA. 2012. A large bioactive BMP ligand with distinct signaling properties is produced by alternative proconvertase processing. Sci Signal 5: ra28.
6. Alarcon C, Zaromytidou AI, Xi Q, Gao S, Yu J, Fujisawa S, Barlas A, Miller AN, Manova-Todorova K, Macias MJ, et al. 2009. Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-β pathways. Cell 139: 757-769
7. Amore G, Casares F. 2010. Size matters: The contribution of cell proliferation to the progression of the specification Drosophila eye gene regulatory network. Dev Biol 344: 569-577
8. Andersson O, Korach-Andre M, Reissmann E, Ibáñez CF, Bertolino P. 2008. Growth/differentiation factor 3 signals through ALK7 and regulates accumulation of adipose tissue and diet-induced obesity. Proc Natl Acad Sci 105: 7252-7256
9. Arora K, Nusslein-Volhard C. 1992. Altered mitotic domains reveal fate map changes in Drosophila embryos mutant for zygotic dorsoventral patterning genes. Development 114: 1003-1024
10. Arora K, Levine MS, O’Connor MB. 1994. The screw gene encodes a ubiquitously expressed member of the TGF-β family required for specification of dorsal cell fates in the Drosophila embryo. Genes Dev 8: 2588-2601
11. Awasaki T, Huang Y, O’Connor MB, Lee T. 2011. Glia instruct developmental neuronal remodeling through TGF-β signaling. Nat Neurosci 14: 821-823
12. Ayyaz A, Li H, Jasper H. 2015. Haemocytes control stem cell activity in the Drosophila intestine. Nat Cell Biol 17: 736-748
13. Baena-Lopez LA, Nojima H, Vincent JP. 2012. Integration of morphogen signalling within the growth regulatory network. Curr Opin Cell Biol 24: 166-172
14. Bai H, Kang P, Hernandez AM, Tatar M. 2013. Activin signaling targeted by insulin/dFOXO regulates aging and muscle proteostasis in Drosophila. PLoS Genet 9: e1003941.
15. Baines RA. 2004. Synaptic strengthening mediated by bone morphogenetic protein-dependent retrograde signaling in the Drosophila CNS. J Neurosci 24: 6904-6911
16. Baker NE. 2001. Cell proliferation, survival, and death in the Drosophila eye. Semin Cell Dev Biol 12: 499-507
17. Ball RW, Warren-Paquin M, Tsurudome K, Liao EH, Elazzouzi F, Cavanagh C, An BS, Wang TT, White JH, Haghighi AP. 2010. Retrograde BMP signaling controls synaptic growth at the NMJ by regulating trio expression in motor neurons. Neuron 66: 536-549
18. Ballard SL, Jarolimova J, Wharton KA. 2010. Gbb/BMP signaling is required to maintain energy homeostasis in Drosophila. Dev Biol 337: 375-385
19. Bangi E, Wharton K. 2006. Dual function of the Drosophila Alk1/Alk2 ortholog Saxophone shapes the Bmp activity gradient in the wing imaginal disc. Development 133: 3295-3303
20. Belenkaya TY, Han C, Yan D, Opoka RJ, Khodoun M, Liu H, Lin X. 2004. Drosophila Dpp morphogen movement is independent of dynamin-mediated endocytosis but regulated by the glypican members of heparan sulfate proteoglycans. Cell 119: 231-244
21. Benkel BF, Hickey DA. 1986. Glucose repression of amylase gene expression in Drosophila melanogaster. Genetics 114: 137-144
22. Ben-Zvi D, Pyrowolakis G, Barkai N, Shilo BZ. 2011. Expansion-repression mechanism for scaling the Dpp activation gradient in Drosophila wing imaginal discs. Curr Biol 21: 1391-1396
23. Berke B, Wittnam J, McNeill E, Van Vactor DL, Keshishian H. 2013. Retrograde BMP signaling at the synapse: A permissive signal for synapse maturation and activitydependent plasticity. J Neurosci 33: 17937-17950
24. Bertolino P, Holmberg R, Reissmann E, Andersson O, Berggren P-O, Ibáñez CF. 2008. Activin B receptor ALK7 is a negative regulator of pancreatic b-cell function. Proc Natl Acad Sci 105: 7246-7251
25. Bickel D, Shah R, Gesualdi SC, Haerry TE. 2008. Drosophila follistatin exhibits unique structural modifications and interacts with several TGF-β family members. Mech Dev 125: 117-129
26. Bienz M. 1994. Homeotic genes and positional signalling in the Drosophila viscera. Trends Genet 10: 22-26
27. Brazil DP, Church RH, Surae S, Godson C, Martin F. 2015. BMP signalling: Agony and antagony in the family. Trends Cell Biol 25: 249-264
28. Brummel TJ, Twombly V, Marques G, Wrana JL, Newfeld SJ, Attisano L, Massague J, O’Connor MB, Gelbart WM. 1994. Characterization and relationship of Dpp receptors encoded by the saxophone and thick veins genes in Drosophila. Cell 78: 251-261
29. Brummel T, Abdollah S, Haerry TE, Shimell MJ, Merriam J, Raftery L, Wrana JL, O’Connor MB. 1999. The Drosophila Activin receptor Baboon signals through dSmad2 and controls cell proliferation but not patterning during larval development. Genes Dev 13: 98-111
30. Burke R, Basler K. 1996. Dpp receptors are autonomously required for cell proliferation in the entire developing Drosophila wing. Development 122: 2261-2269
31. Campbell G, Tomlinson A. 1999. Transducing the Dpp morphogen gradient in the wing of Drosophila: Regulation of Dpp targets by brinker. Cell 96: 553-562
32. Capdevila J, Guerrero I. 1994. Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J 13: 4459-4468
33. Chen D, McKearin D. 2003. Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr Biol 13: 1786-1791
34. Chen CK, Kuhnlein RP, Eulenberg KG, Vincent S, Affolter M, Schuh R. 1998. The transcription factors Knirps and Knirps related control cell migration and branch morphogenesis during Drosophila tracheal. Development 125: 4959-4968
35. Chen J, Honeyager SM, Schleede J, Avanesov A, Laughon A, Blair SS. 2012. Crossveinless d is a vitellogenin-like lipoprotein that binds BMPs and HSPGs, and is required for normal BMP signaling in the Drosophila wing. Development 139: 2170-2176
36. Chng W-BA, Sleiman MSB, Schüpfer F, Lemaitre B. 2014. Transforming growth factor b/activin signaling functions as a sugar-sensing feedback loop to regulate digestive enzyme expression. Cell Rep 9: 336-348
37. Clark RI, Woodcock KJ, Geissmann F, Trouillet C, Dionne MS. 2011. Multiple TGF-β superfamily signals modulate the adult Drosophila immune response. Curr Biol 21: 1672-1677
38. Conley Ca, Silburn R, Singer MA, Ralston A, Rohwer-Nutter D, Olson DJ, Gelbart W, Blair SS. 2000. Crossveinless 2 contains cysteine-rich domains and is required for high levels of BMP-like activity during the formation of the cross veins in Drosophila. Development 127: 3947-3959
39. Crick F. 1970. Diffusion in embryogenesis. Nature 225: 420-422
40. Curtiss J, Mlodzik M. 2000. Morphogenetic furrow initiation and progression during eye development in Drosophila: The roles of decapentaplegic, hedgehog and eyes absent. Development 127: 1325-1336
41. Dani N, Broadie K. 2012. Glycosylated synaptomatrix regulation of trans-synaptic signaling. Dev Neurobiol 72: 2-21
42. Day SJ, Lawrence PA. 2000. Measuring dimensions: The regulation of size and shape. Development 127: 2977-2987
43. de Celis JF. 1997. Expression and function of decapentaplegic and thickveins during the differentiation of the veins in the Drosophila wing. Development 124: 1007-1018
44. de Celis JF. 2003. Pattern formation in the Drosophila wing: The development of the veins. BioEssays 25: 443-451
45. Dickson BJ. 2001. Rho GTPases in growth cone guidance. Curr Opin Neurobiol 11: 103-110
46. Dobens LL, Raftery LA. 1998. Drosophila oogenesis: A model system to understand TGF-b/Dpp directed cell morphogenesis. Ann NY Acad Sci 857: 245-247
47. Dorfman R, Shilo BZ. 2001. Biphasic activation of the BMP pathway patterns the Drosophila embryonic dorsal region. Development 128: 965-972
48. Dupont S, Mamidi A, Cordenonsi M, Montagner M, Zacchigna L, Adorno M, Martello G, Stinchfield MJ, Soligo S, Morsut L, et al. 2009. FAM/USP9x, a deubiquitinating enzyme essential for TGF-β signaling, controls Smad4 monoubiquitination. Cell 136: 123-135
49. Eaton BA, Davis GW. 2005. LIM kinase1 controls synaptic stability downstream of the type II BMP receptor. Neuron 47: 695-708
50. Eivers E, Fuentealba LC, Sander V, Clemens JC, Hartnett L, De Robertis EM. 2009. Mad is required for wingless signaling in wing development and segment patterning in Drosophila. PLoS ONE 4: e6543-e6543.
51. Eivers E, Demagny H, Choi RH, De Robertis EM. 2011. Phosphorylation of Mad controls competition between wingless and BMP signaling. Sci Signal 4: ra68
52. Eldar A, Dorfman R, Weiss D, Ashe H, Shilo BZ, Barkai N. 2002. Robustness of the BMP morphogen gradient in Drosophila embryonic patterning. Nature 419: 304-308
53. Entchev EV, Schwabedissen A, González-Gaitán M. 2000. Gradient formation of the TGF-β homolog Dpp. Cell 103: 981-991
54. Estella C, Mann RS. 2008. Logic of Wg and Dpp induction of distal and medial fates in the Drosophila leg. Development 135: 627-636
55. Estella C, Voutev R, Mann RS. 2012. A dynamic network of morphogens and transcription factors patterns the fly leg. Curr Top Dev Biol 98: 173-198
56. Estrada B, Casares F, Sánchez-Herrero E. 2003. Development of the genitalia in Drosophila melanogaster. Differentiation 71: 299-310
57. Fan X, Labrador JP, Hing H, Bashaw GJ. 2003. Slit stimulation recruits Dock and Pak to the roundabout receptor and increases Rac activity to regulate axon repulsion at the CNS midline. Neuron 40: 113-127
58. Ferguson EL, Anderson KV. 1992. Decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 71: 451-461
59. Fernandez BG, Arias AM, Jacinto A. 2007. Dpp signalling orchestrates dorsal closure by regulating cell shape changes both in the amnioserosa and in the epidermis. Mech Dev 124: 884-897
60. Firth LC, Bhattacharya A, Baker NE. 2010. Cell cycle arrest by a gradient of Dpp signaling during Drosophila eye development. BMC Dev Biol 10: 28-28
61. Frasch M. 1995. Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature 374: 464-467
62. Fritsch C, Sawala A, Harris R, Maartens A, Sutcliffe C, Ashe HL, Ray RP. 2012. Different requirements for proteolytic processing of bone morphogenetic protein 5/6/7/8 ligands in Drosophila melanogaster. J Biol Chem 287: 5942-5953
63. Fuentes-Medel Y, Ashley J, Barria R, Maloney R, Freeman M, Budnik V. 2012. Integration of a retrograde signal during synapse formation by glia-secreted TGF-β ligand. Curr Biol 22: 1831-1838
64. Fujise M, Takeo S, Kamimura K, Matsuo T, Aigaki T, Izumi S, Nakato H. 2003. Dally regulates Dpp morphogen gradient formation in the Drosophila wing. Development 130: 1515-1522
65. Funakoshi Y, Minami M, Tabata T. 2001. Mtv shapes the activity gradient of the Dpp morphogen through regulation of thickveins. Development 128: 67-74
66. Fuss B, Hoch M. 1998. Drosophila endoderm development requires a novel homeobox gene which is a target of Wingless and Dpp signalling. Mech Dev 79: 83-97
67. Gavin-Smyth J, Wang YC, Butler I, Ferguson EL. 2013. A genetic network conferring canalization to a bistable patterning system in Drosophila. Curr Biol 23: 2296-2302
68. Gesualdi SC, Haerry TE. 2007. Distinct signaling of Drosophila Activin/TGF-β family members. Fly (Austin) 1: 212-221
69. Ghosh AC, O’Connor MB. 2014. Systemic activin signaling independently regulates sugar homeostasis, cellular metabolism, and pH balance in Drosophila melanogaster. Proc Natl Acad Sci 111: 5729-5734
70. Gibbens YY, Warren JT, Gilbert LI, O’Connor MB. 2011. Neuroendocrine regulation of Drosophila metamorphosis requires TGFb/Activin signaling. Development 138: 2693-2703
71. Glise B, Noselli S. 1997. Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev 11: 1738-1747
72. Goold CP, Davis GW. 2007. The BMP ligand Gbb gates the expression of synaptic homeostasis independent of synaptic growth control. Neuron 56: 109-123
73. Gorfinkiel N, Sánchez L, Guerrero I. 1999. Drosophila terminalia as an appendage-like structure. Mech Dev 86: 113-123
74. Goto S, Hayashi S. 1997. Specification of the embryonic limb primordium by graded activity of Decapentaplegic. Development 124: 125-132
75. Guo Z, Driver I, Ohlstein B. 2013. Injury-induced BMP signaling negatively regulates Drosophila midgut homeostasis. J Cell Biol 201: 945-961
76. Hamaratoglu F, de Lachapelle AM, Pyrowolakis G, Bergmann S, Affolter M. 2011. Dpp signaling activity requires Pentagone to scale with tissue size in the growing Drosophila wing imaginal disc. PLoS Biol 9: e1001182-e1001182.
77. Hamaratoglu F, Affolter M, Pyrowolakis G. 2014. Dpp/BMP signaling in flies: From molecules to biology. Semin Cell Dev Biol 32: 128-136
78. Harmansa S, Hamaratoglu F, Affolter M, Caussinus E. 2015. Dpp spreading is required for medial but not for lateral wing disc growth. Nature 527: 317-322
79. Hevia CF, de Celis JF. 2013. Activation and function of TGFb signalling during Drosophila wing development and its interactions with the BMP pathway. Dev Biol 377: 138-153
80. Hickey DA, Benkel B. 1982. Regulation of amylase activity in Drosophila melanogaster: Effects of dietary carbohydrate. Biochem Genet 20: 1117-1129
81. Horsfield J, Penton A, Secombe J, Hoffman FM, Richardson H. 1998. DDecapentaplegic is required for arrest in G1 phase during Drosophila eye development. Development 125: 5069-5078
82. Huang J, Tian L, Peng C, Abdou M, Wen D, Wang Y, Li S, Wang J. 2011. DPP-mediated TGF signaling regulates juvenile hormone biosynthesis by activating the expression of juvenile hormone acid methyltransferase. Development 138: 2283-2291
83. Humphreys GB, Jud MC, Monroe KM, Kimball SS, Higley M, Shipley D, Vrablik MC, Bates KL, Letsou A. 2013. Mummy, a UDP-N-acetylglucosamine pyrophosphorylase, modulates DPP signaling in the embryonic epidermis of Drosophila. Dev Biol 381: 434-445
84. Igaki T, Kanda H, Yamamoto-Goto Y, Kanuka H, Kuranaga E, Aigaki T, Miura M. 2002. Eiger, a TNF superfamily ligand that triggers the Drosophila JNK pathway. EMBO J 21: 3009-3018
85. Inoue H, Imamura T, Ishidou Y, Takase M, Udagawa Y, Oka Y, Tsuneizumi K, Tabata T, Miyazono K, Kawabata M. 1998. Interplay of signal mediators of decapentaplegic (Dpp): Molecular characterization of mothers against dpp, Medea, and daughters against dpp. Mol Biol Cell 9: 2145-2156
86. James RE, Broihier HT. 2011. Crimpy inhibits the BMP homolog Gbb in motoneurons to enable proper growth control at the Drosophila neuromuscular junction. Development 138: 3273-3286
87. Jaźwińska A, Kirov N, Wieschaus E, Roth S, Rushlow C. 1999. The Drosophila gene brinker reveals a novel mechanism of Dpp target gene regulation. Cell 96: 563-573
88. Jensen PA, Zheng X, Lee T, O’Connor MB. 2009. The Drosophila Activin-like ligand Dawdle signals preferentially through one isoform of the Type-I receptor Baboon. Mech Dev 126: 950-957
89. Johnson AN, Bergman CM, Kreitman M, Newfeld SJ. 2003. Embryonic enhancers in the dpp disk region regulate a second round of Dpp signaling from the dorsal ectoderm to the mesoderm that represses Zfh-1 expression in a subset of pericardial cells. Dev Biol 262: 137-151
90. Johnson AN, Burnett LA, Sellin J, Paululat A, Newfeld SJ. 2007. Defective decapentaplegic signaling results in heart overgrowth and reduced cardiac output in Drosophila. Genetics 176: 1609-1624
91. Kai T, Spradling A. 2003. An empty Drosophila stem cell niche reactivates the proliferation of ectopic cells. Proc Natl Acad Sci 100: 4633-4638
92. Kamiya Y, Miyazono K, Miyazawa K. 2008. Specificity of the inhibitory effects of Dad on TGF-β family type I receptors, Thickveins, Saxophone, and Baboon in Drosophila. FEBS Lett 582: 2496-2500
93. Keisman EL, Baker BS. 2001. The Drosophila sex determination hierarchy modulates wingless and decapentaplegic signaling to deploy dachshund sex-specifically in the genital imaginal disc. Development 128: 1643-1656
94. Khalsa O, Yoon JW, Torres-Schumann S, Wharton KA. 1998. TGF-b/BMP superfamily members, Gbb-60A and Dpp, cooperate to provide pattern information and establish cell identity in the Drosophila wing. Development 125: 2723-2734
95. Kicheva A, González-Gaitán M. 2008. The Decapentaplegic morphogen gradient: A precise definition. Curr Opin Cell Biol 20: 137-143
96. Kim NC, Marques G. 2012. The Ly6 neurotoxin-like molecule target ofwit regulates spontaneous neurotransmitter release at the developing neuromuscular junction in Drosophila. Dev Neurobiol 72: 1541-1558
97. Kim MJ, O’Connor MB. 2014. Anterograde activin signaling regulates postsynaptic membrane potential and GluRIIA/ B abundance at the Drosophila neuromuscular junction. PLoS ONE 9: e107443.
98. 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
99. Kretzschmar M, Doody J, Massagué J. 1997. Opposing BMP and EGF signalling pathways converge on the TGF-β family mediator Smad1. Nature 389: 618-622
100. Kunnapuu J, Bjorkgren I, Shimmi O. 2009. The Drosophila DPP signal is produced by cleavage of its proprotein at evolutionary diversified furin-recognition sites. ProcNatl Acad Sci 106: 8501-8506
101. Kunnapuu J, Tauscher PM, Tiusanen N, Nguyen M, Loytynoja A, Arora K, Shimmi O. 2014. Cleavage of the Drosophila screw prodomain is critical for a dynamic BMP morphogen gradient in embryogenesis. Dev Biol 389: 149-159
102. Kuo WJ, Digman MA, Lander AD. 2010. Heparan sulfate acts as a bone morphogenetic protein coreceptor by facilitating ligand-induced receptor hetero-oligomerization. Mol Biol Cell 21: 4028-4041
103. Lecuit T, Cohen SM. 1997. Proximal-distal axis formation in the Drosophila leg. Nature 388: 139-145
104. Lecuit T, Brook W, Ng M, Calleja M, Sun H, Cohen S. 1996. Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 381: 387-393
105. Lengil T, Gancz D, Gilboa L. 2015. Activin signaling balances proliferation and differentiation of ovarian niche precursors and enables adjustment of niche numbers. Development 142: 883-892
106. Li MO, Wan YY, Sanjabi S, Robertson AKL, Flavell RA. 2006. Transforming growth factor-b regulation of immune responses. Annu Rev Immunol 24: 99-146
107. Li L, Shen JJ, Bournat JC, Huang L, Chattopadhyay A, Li Z, Shaw C, Graham BH, Brown CW. 2009. Activin signaling: Effects on body composition and mitochondrial energy metabolism. Endocrinology 150: 3521-3529
108. Li H, Qi Y, Jasper H. 2013a. Dpp signaling determines regional stem cell identity in the regenerating adult Drosophila gastrointestinal tract. Cell Rep 4: 10-18
109. Li Z, Zhang Y, Han L, Shi L, Lin X. 2013b. Trachea-derived dpp controls adult midgut homeostasis in Drosophila. Dev Cell 24: 133-143
110. Lin H. 2002. The stem-cell niche theory: Lessons from flies. Nat Rev Genet 3: 931-940
111. Lo PC, Frasch M. 1999. Sequence and expression of myoglianin, a novel Drosophila gene of the TGF-β superfamily. Mech Dev 86: 171-175
112. Lynch JA, El-Sherif E, Brown SJ. 2012. Comparisons of the embryonic development of Drosophila, Nasonia, and Tribolium. Wiley Interdiscip Rev Dev Biol 1: 16-39
113. Marmion RA, Jevtic M, Springhorn A, Pyrowolakis G, Yakoby N. 2013. The Drosophila BMPRII, wishful thinking, is required for eggshell patterning. Dev Biol 375: 45-53
114. Marques G, Musacchio M, Shimell MJ, Wunnenberg-Stapleton K, Cho KW, O’Connor MB. 1997. Production of a Dpp activity gradient in the early Drosophila embryo through the opposing actions of the SOG and TLD proteins. Cell 91: 417-426
115. Marques 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
116. Martin FA, Perez-Garijo A, Moreno E, Morata G. 2004. The brinker gradient controls wing growth in Drosophila. Development 131: 4921-4930
117. Martin-Castellanos C, Edgar BA. 2002. Acharacterization of the effects of Dpp signaling on cell growth and proliferation in the Drosophila wing. Development 129: 1003-1013
118. Matsuda S, Shimmi O. 2012. Directional transport and active retention of Dpp/BMP create wing vein patterns in Drosophila. Dev Biol 366: 153-162
119. Mattila J, Havula E, Suominen E, Teesalu M, Surakka I, Hynynen R, Kilpinen H, Vaananen J, Hovatta I, Kakela R, et al. 2015. Mondo-Mlx mediates organismal sugar sensing through the Gli-similar transcription factor Sugarbabe. Cell Rep 13: 350-364
120. 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
121. 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
122. Micchelli CA, Perrimon N. 2006. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439: 475-479
123. Milan M, Campuzano S, Garcia-Bellido A. 1996. Cell cycling and patterned cell proliferation in the wing primordium of Drosophila. Proc Natl Acad Sci 93: 640-645
124. Miles WO, Jaffray E, Campbell SG, Takeda S, Bayston LJ, Basu SP, Li M, Raftery LA, Ashe MP, Hay RT, et al. 2008. Medea SUMOylation restricts the signaling range of the Dpp morphogen in the Drosophila embryo. Genes Dev 22: 2578-2590
125. Minami M, Kinoshita N, Kamoshida Y, Tanimoto H, Tabata T. 1999. brinker is a target of Dpp in Drosophila that negatively regulates Dpp-dependent genes. Nature 398: 242-246
126. Mizutani CM, Nie Q, Wan FY, Zhang YT, Vilmos P, Sousa-Neves R, Bier E, Marsh JL, Lander AD. 2005. Formation of the BMP activity gradient in the Drosophila embryo. Dev Cell 8: 915-924
127. Moreno E, Yan M, Basler K. 2002. Evolution of TNF signaling mechanisms: JNK-dependent apoptosis triggered by Eiger, the Drosophila homolog of the TNF superfamily. Curr Biol 12: 1263-1268
128. Musselman LP, Fink JL, Narzinski K, Ramachandran PV, Hathiramani SS, Cagan RL, Baranski TJ. 2011. A highsugar diet produces obesity and insulin resistance inwildtype Drosophila. Dis Model Mech 4: 842-849
129. Myat MM, Lightfoot H, Wang P, Andrew DJ. 2005. A molecular link between FGF and Dpp signaling in branchspecific migration of the Drosophila trachea. Dev Biol 281: 38-52
130. Na J, Musselman LP, Pendse J, Baranski TJ, Bodmer R, Ocorr K, Cagan R. 2013. A Drosophila model of high sugar dietinduced cardiomyopathy. PLoS Genet 9: e1003175.
131. Nahm M, Kim S, Paik SK, Lee M, Lee S, Lee ZH, Kim J, Lee D, Bae YC. 2010a. dCIP4 (Drosophila Cdc42-interacting protein 4) restrains synaptic growth by inhibiting the secretion of the retrograde Glass bottom boat signal. J Neurosci 30: 8138-8150
132. Nahm M, Long AA, Paik SK, Kim S, Bae YC, Broadie K, Lee S. 2010b. The Cdc42-selective GAP rich regulates postsynaptic development and retrograde BMP transsynaptic signaling. J Cell Biol 191: 661-675
133. Nakagoshi H, Hoshi M, Nabeshima Y, Matsuzaki F. 1998. A novel homeobox gene mediates the Dpp signal to establish functional specificity within target cells. Genes Dev 12: 2724-2734
134. Nellen D, Burke R, Struhl G, Basler K. 1996. Direct and longrange action of a Dpp morphogen gradient. Cell 85: 357-368
135. Ng J. 2008. TGFb signals regulate axonal development through distinct Smad-independent mechanisms. Development 135: 4025-4035
136. Nguyen M, Park S, Marques G, Arora K. 1998. Interpretation of a BMP activity gradient in Drosophila embryos depends on synergistic signaling by two type I receptors, SAX and TKV. Cell 95: 495-506
137. Norman M, Vuilleumier R, Springhorn A, Gawlik J, Pyrowolakis G. 2016. Pentagone internalises glypicans to finetune multiple signalling pathways. eLife 5: e13301.
138. Nusslein-Volhard C, Wieschaus E, Kluding H. 1984. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. I: Zygotic loci on the second chromosome. Wilhelm Roux’s Arch Dev Biol 193: 267-282
139. O’Connor MB, Umulis D, Othmer HG, Blair SS. 2006. Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 133: 183-193
140. O’Connor-Giles KM, Ho LL, Ganetzky B. 2008. Nervous wreck interacts with thickveins and the endocytic machinery to attenuate retrograde BMP signaling during synaptic growth. Neuron 58: 507-518
141. Ogiso Y, Tsuneizumi K, Masuda N, Sato M, Tabata T. 2011. Robustness of the Dpp morphogen activity gradient depends on negative feedback regulation by the inhibitory Smad, Dad. Dev Growth Differ 53: 668-678
142. Oh H, Irvine KD. 2010. Yorkie: The final destination of Hippo signaling. Trends Cell Biol 20: 410-417
143. Oh H, Irvine KD. 2011. Cooperative regulation of growth by Yorkie and Mad through bantam. Dev Cell 20: 109-122
144. Ohlstein B, Spradling A. 2006. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439: 470-474
145. Padgett RW, St Johnston RD, Gelbart WM. 1987. A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-b family. Nature 325: 81-84
146. Padgett RW, Wozney JM, Gelbart WM. 1993. Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc Natl Acad Sci 90: 2905-2909
147. Parker L, Ellis JE, Nguyen MQ, Arora K. 2006. The divergent TGF-β ligand Dawdle utilizes an activin pathway to influence axon guidance in Drosophila. Development 133: 4981-4991
148. Peluso CE, Umulis D, Kim YJ, O’Connor MB, Serpe M. 2011. Shaping BMP morphogen gradients through enzyme-substrate interactions. Dev Cell 21: 375-383
149. Pentek J, Parker L, Wu A, Arora K. 2009. Follistatin preferentially antagonizes activin rather than BMP signaling in Drosophila. Genesis 47: 261-273
150. Pera EM, Ikeda A, Eivers E, De Robertis EM. 2003. Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural induction. Genes Dev 17: 3023-3028
151. Peterson AJ, O’Connor MB. 2013. Activin receptor inhibition by Smad2 regulates Drosophila wing disc patterning through BMP-response elements. Development 140: 649-659
152. Peterson AJ, Jensen PA, Shimell M, Stefancsik R, Wijayatonge R, Herder R, Raftery LA, O’Connor MB. 2012. RSmad competition controls activin receptor output in Drosophila. PLoS ONE 7: e36548.
153. Piccioli ZD, Littleton JT. 2014. Retrograde BMP signaling modulates rapid activity-dependent synaptic growth via presynaptic LIM kinase regulation of cofilin. J Neurosci 34: 4371-4381
154. Quijano JC, Stinchfield MJ, Newfeld SJ. 2011. Wg signaling via Zw3 and mad restricts self-renewal of sensory organ precursor cells in Drosophila. Genetics 189: 809-824
155. Ralston A, Blair SS. 2005. Long-range Dpp signaling is regulated to restrict BMP signaling to a crossvein competent zone. Dev Biol 280: 187-200
156. Ramirez-Weber FA, Kornberg TB. 1999. Cytonemes: Cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell 97: 599-607
157. Rawson JM, Lee M, Kennedy EL, Selleck SB. 2003. Drosophila neuromuscular synapse assembly and function require the TGF-β type I receptor saxophone and the transcription factor Mad. J Neurobiol 55: 134-150
158. Ray RP, Wharton KA. 2001. Context-dependent relationships between the BMPs gbb and dpp during development of the Drosophila wing imaginal disk. Development 128: 3913-3925
159. Rentzsch F, Zhang J, Kramer C, Sebald W, Hammerschmidt M. 2006. Crossveinless 2 is an essential positive feedback regulator of Bmp signaling during zebrafish gastrulation. Development 133: 801-811
160. Restrepo S, Zartman JJ, Basler K. 2014. Coordination of patterning and growth by the morphogen DPP. Curr Biol 24: R245-255
161. Ross JJ, Shimmi O, Vilmos P, Petryk A, Kim H, Gaudenz K, Hermanson S, Ekker SC, O’Connor MB, Marsh JL. 2001. Twisted gastrulation is a conserved extracellular BMP antagonist. Nature 410: 479-483
162. Roy S, Kornberg TB. 2011. Direct delivery mechanisms of morphogen dispersion. Sci Signal 4: pt8.
163. Roy S, Huang H, Liu S, Kornberg TB. 2014. Cytonememediated contact-dependent transport of the Drosophila decapentaplegic signaling protein. Science 343: 1244624.
164. Sampath TK, Rashka KE, Doctor JS, Tucker RF, Hoffmann FM. 1993. Drosophila transforming growth factor b superfamily proteins induce endochondral bone formation in mammals. Proc Natl Acad Sci 90: 6004-6008
165. Sánchez L, Guerrero I. 2001. The development of the Drosophila genital disc. BioEssays 23: 698-707
166. Sánchez L, Gorfinkiel N, Guerrero I. 2001. Sex determination genes control the development of the Drosophila genital disc, modulating the response to Hedgehog, Wingless and Decapentaplegic signals. Development 128: 1033-1043
167. Sander V, Eivers E, Choi RH, De Robertis EM. 2010. Drosophila Smad2 opposes Mad signaling during wing vein development. PLoS ONE 5: e10383
168. Sawala A, Sutcliffe C, Ashe HL. 2012. Multistep molecular mechanism for bone morphogenetic protein extracellular transport in the Drosophila embryo. ProcNatl Acad Sci 109: 11222-11227
169. Schulz C. 2004. A misexpression screen reveals effects of bag-of-marbles and TGF class signaling on the Drosophila male germ-line stem cell lineage. Genetics 167: 707-723
170. Schwank G, Restrepo S, Basler K. 2008. Growth regulation by Dpp: An essential role for Brinker and a non-essential role for graded signaling levels. Development 135: 4003-4013
171. Schwank G, Dalessi S, Yang SF, Yagi R, de Lachapelle AM, Affolter M, Bergmann S, Basler K. 2011. Formation of the long range Dpp morphogen gradient. PLoS Biol 9: e1001111.
172. Schwank G, Yang SF, Restrepo S, Basler K. 2012. Comment on “Dynamics of dpp signaling and proliferation control.” Science 335: 401.
173. Serpe M, O’Connor MB. 2006. The metalloprotease Tolloidrelated and its TGF-β-like substrate Dawdle regulate Drosophila motoneuron axon guidance. Development 133: 4969-4979
174. Serpe M, Umulis D, Ralston A, Chen J, Olson DJ, Avanesov A, Othmer H, O’Connor MB, Blair SS. 2008. The BMPbinding protein Crossveinless 2 is a short-range, concentration-dependent, biphasic modulator of BMPsignaling in Drosophila. Dev Cell 14: 940-953
175. Shimell MJ, Ferguson EL, Childs SR, O’Connor MB. 1991. The Drosophila dorsal-ventral patterning gene tolloid is related to human bone morphogenetic protein 1. Cell 67: 469-481
176. Shimmi O, Ralston A, Blair SS, O’Connor MB. 2005a. The crossveinless gene encodes a new member of the Twisted gastrulation family of BMP-binding proteins which, with Short gastrulation, promotes BMP signaling in the crossveins of the Drosophila wing. Dev Biol 282: 70-83
177. Shimmi O, Umulis D, Othmer H, O’Connor MB. 2005b. Facilitated transport of a Dpp/Scw heterodimer by Sog/ Tsg leads to robust patterning of the Drosophila blastoderm embryo. Cell 120: 873-886
178. Shivdasani AA, Ingham PW. 2003. Regulation of stem cell maintenance and transit amplifying cell proliferation by TGF-β signaling in Drosophila spermatogenesis. Curr Biol 13: 2065-2072
179. Song X, Wong MD, Kawase E, Xi R, Ding BC, McCarthy JJ, Xie T. 2004. Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development 131: 1353-1364
180. Sopory S, Kwon S, Wehrli M, Christian JL. 2010. Regulation of Dpp activity by tissue-specific cleavage of an upstream site within the prodomain. Dev Biol 346: 102-112
181. Spencer FA, Hoffmann FM, Gelbart WM. 1982. Decapentaplegic: A gene complex affecting morphogenesis in Drosophila melanogaster. Cell 28: 451-461
182. Staehling-Hampton K, Hoffmann FM. 1994. Ectopic decapentaplegic in the Drosophila midgut alters the expression of five homeotic genes, dpp, and wingless, causing specific morphological defects. Dev Biol 164: 502-512
183. Stinchfield MJ, Takaesu NT, Quijano JC, Castillo AM, Tiusanen N, Shimmi O, Enzo E, Dupont S, Piccolo S, Newfeld SJ. 2012. Fat facets deubiquitylation of Medea/ Smad4 modulates interpretation of a Dpp morphogen gradient. Development 139: 2721-2729
184. Sulkowski M, Kim YJ, Serpe M. 2014. Postsynaptic glutamate receptors regulate local BMP signaling at the Dro-sophila neuromuscular junction. Development 141: 436-447
185. Sulkowski MJ, Han TH, Ott C, Wang Q, Verheyen EM, Lippincott-Schwartz J, Serpe M. 2016. A novel, noncanonical BMP pathway modulates synapse maturation at the Drosophila neuromuscular junction. PLoS Genet 12: e1005810.
186. Sweeney ST, Davis GW. 2002. Unrestricted synaptic growth in spinster—A late endosomal protein implicated in TGF-b-mediated synaptic growth regulation. Neuron 36: 403-416
187. Szuts D, Bienz M. 2000. An autoregulatory function of Dfos during Drosophila endoderm induction. Mech Dev 98: 71-76
188. Takaesu NT, Bulanin DS, Johnson AN, Orenic TV, Newfeld SJ. 2008. A combinatorial enhancer recognized by Mad, TCF and Brinker first activates then represses dpp expression in the posterior spiracles of Drosophila. Dev Biol 313: 829-843
189. Teleman AA, Cohen SM. 2000. Dpp gradient formation in the Drosophila wing imaginal disc. Cell 103: 971-980
190. Tian A, Jiang J. 2014. Intestinal epithelium-derived BMP controls stem cell self-renewal in Drosophila adult midgut. eLife 3: e01857.
191. Ting CY, Herman T, Yonekura S, Gao S, Wang J, Serpe M, O’Connor MB, Zipursky SL, Lee CH. 2007. 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 56: 793-806
192. Ting CY, McQueen Philip G, Pandya N, Lin TY, Yang M, Reddy OV, O’Connor Michael B, McAuliffe M, Lee CH. 2014. Photoreceptor-derived activin promotes dendritic termination and restricts the receptive fields of first-order Interneurons in Drosophila. Neuron 81: 830-846
193. Tsuneizumi K, Nakayama T, Kamoshida Y, Kornberg TB, Christian JL, Tabata T. 1997. Daughters against dpp modulates dpp organizing activity in Drosophila wing development. Nature 389: 627-631
194. Umulis DM, Serpe M, O’Connor MB, Othmer HG. 2006. Robust, bistable patterning of the dorsal surface of the Drosophila embryo. Proc Natl Acad Sci 103: 11613-11618
195. Umulis D, O’Connor MB, Blair SS. 2009. The extracellular regulation of bone morphogenetic protein signaling. Development 136: 3715-3728
196. Umulis DM, Shimmi O, O’Connor MB, Othmer HG. 2010. Organism-scale modeling of early Drosophila patterning via bone morphogenetic proteins. Dev Cell 18: 260-274
197. Vincent S, Ruberte E, Grieder NC, Chen CK, Haerry T, Schuh R, Affolter M. 1997. DPP controls tracheal cell migration along the dorsoventral body axis of the Drosophila embryo. Development 124: 2741-2750
198. Vuilleumier R, Springhorn A, Patterson L, Koidl S, Hammerschmidt M, Affolter M, Pyrowolakis G. 2010. Control of Dpp morphogen signalling by a secreted feedback regulator. Nature 12: 611-617
199. Wang YC, Ferguson EL. 2005. Spatial bistability of Dppreceptor interactions during Drosophila dorsal-ventral patterning. Nature 434: 229-234
200. Wang X, Shaw WR, Tsang HT, Reid E, O’Kane CJ. 2007. Drosophila spichthyin inhibits BMP signaling and regulates synaptic growth and axonal microtubules. Nat Neurosci 10: 177-185
201. Wang X, Harris RE, Bayston LJ, Ashe HL. 2008. Type IV collagens regulate BMP signalling in Drosophila. Nature 455: 72-77
202. Wang RN, Green J, Wang Z, Deng Y, Qiao M, Peabody M, Zhang Q, Ye J, Yan Z, Denduluri S, et al. 2014. Bone morphogenetic protein (BMP) signaling in development and human diseases. Genes Dis 1: 87-105
203. Wartlick O, Mumcu P, Julicher F, Gonzalez-Gaitan M. 2011a. Understanding morphogenetic growth control— Lessons from flies. Nat Rev Mol Cell Biol 12: 594-604
204. Wartlick O, Mumcu P, Kicheva A, Bittig T, Seum C, Julicher F, Gonzalez-Gaitan M. 2011b. Dynamics of Dpp signaling and proliferation control. Science 331: 1154-1159
205. Weiss A, Charbonnier E, Ellertsdó ttir E, Tsirigos A, Wolf C, Schuh R, Pyrowolakis G, Affolter M. 2010. A conserved activation element in BMP signaling during Drosophila development. Nat Struct Mol Biol 17: 69-76
206. Wharton KA, Ray RP, Gelbart WM. 1993. An activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo. Development 117: 807-822
207. Wharton KA, Cook JM, Torres-Schumann S, de Castro K, Borod E, Phillips DA. 1999. Genetic analysis of the bone morphogenetic protein-related gene, gbb, identifies multiple requirements during Drosophila development. Genetics 152: 629-640
208. Wieschaus E, Nusslein-Volhard C, Kluding H. 1984. Krüppel, a gene whose activity is required early in the zygotic genome for normal embryonic segmentation. Dev Biol 104: 172-186
209. Winstanley J, Sawala A, Baldock C, Ashe HL. 2015. Synthetic enzyme-substrate tethering obviates the Tolloid-ECM interaction during Drosophila BMP gradient formation. eLife 4: e05508.
210. Wolfman NM, McPherron AC, Pappano WN, Davies MV, Song K, Tomkinson KN, Wright JF, Zhao L, Sebald SM, Greenspan DS, et al. 2003. Activation of latent myostatin by the BMP-1/tolloid family of metalloproteinases. Proc Natl Acad Sci 100: 15842-15846
211. Wu MY, Hill CS. 2009. TGF-β superfamily signaling in embryonic development and homeostasis. Dev Cell 16: 329-343
212. Xie T, Spradling AC. 1998. decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell 94: 251-260
213. Xie T, Spradling A. 2000. A niche maintaining germ line stem cells in the Drosophila ovary. Science 290: 328-330
214. Yakoby N, Bristow CA, Gong D, Schafer X, Lembong J, Zartman JJ, Halfon MS, Schüpbach T, Shvartsman SY. 2008a. A combinatorial code for pattern formation in Drosophila oogenesis. Dev Cell 15: 725-737
215. Yakoby N, Lembong J, Schüpbach T, Shvartsman SY. 2008b. Drosophila eggshell is patterned by sequential action of feedforward and feedback loops. Development 135: 343-351
216. Yamashita YM, Fuller MT, Jones DL. 2005. Signaling in stem cell niches: Lessons from the Drosophila germline. J Cell Sci 118: 665-672
217. Yu XM, Gutman I, Mosca TJ, Iram T, Ö zkan E, Garcia KC, Luo L, Schuldiner O. 2013. Plum, an immunoglobulin superfamily protein, regulates axon pruning by facilitating TGF-β signaling. Neuron 78: 456-468
218. Zahedi B, Shen W, Xu X, Chen X, Mahey M, Harden N. 2008. Leading edge-secreted Dpp cooperates with ACKdependent signaling from the amnioserosa to regulate myosin levels during dorsal closure. Dev Dyn 237: 2936-2946
219. Zamani N, Brown CW. 2011. Emerging roles for the transforming growth factor-b superfamily in regulating adiposity and energy expenditure. Endocr Rev 32: 387-403
220. Zecca M, Basler K, Struhl G. 1995. Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 121: 2265-2278
221. Zheng X, Wang J, Haerry TE, Wu AYH, Martin J, O’Connor MB, Lee C-HJ, Lee T. 2003. TGF-β signaling activates steroid hormone receptor expression during neuronal remodeling in the Drosophila brain. Cell 112: 303-315
222. Zhou S, Lo WC, Suhalim JL, Digman MA, Gratton E, Nie Q, Lander AD. 2012. Free extracellular diffusion creates the Dpp morphogen gradient of the Drosophila wing disc. Curr Biol 22: 668-675
223. Zhu CC, Boone JQ, Jensen PA, Hanna S, Podemski L, Locke J, Doe CQ, O’Connor MB. 2008. Drosophila Activin-b and the activin-like product Dawdle function redundantly to regulate proliferation in the larval brain. Development 135: 513-521