Regulation of BMP activity and range in Drosophila wing development

Current Opinion in Cell Biology

Volumn 24, Issue 2, 2012, Pages 158-165

  Raftery, Laurel A ^a   Umulis, David M ^b  

^a UNIVERSITY OF NEVADA   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; MORPHOGEN; PROTEIN; PROTEIN DALLY; PROTEIN LTL; PROTEIN PENT; UNCLASSIFIED DRUG;

CELL INTERACTION; DROSOPHILA; FORELIMB; INSECT DEVELOPMENT; LIMB DEVELOPMENT; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; TISSUE GROWTH;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL COMMUNICATION; DROSOPHILA; DROSOPHILA PROTEINS; SIGNAL TRANSDUCTION; WING;

EID: 84861819769     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2011.11.004     Document Type: Review

References (69)

1. Araujo H., Fontenele M.R., da Fonseca R.N. Position matters: variability in the spatial pattern of BMP modulators generates functional diversity. Genesis 2011, 49:698-718.
2. Bayat V., Jaiswal M., Bellen H.J. The BMP signaling pathway at the Drosophila neuromuscular junction and its links to neurodegenerative diseases. Curr Opin Neurobiol 2011, 21:182-188.
3. Goldstein J.A., Kelly S.M., LoPresti P.P., Heydemann A., Earley J.U., Ferguson E.L., Wolf M.J., McNally E.M. SMAD signaling drives heart and muscle dysfunction in a Drosophila model of muscular dystrophy. Hum Mol Genet 2011, 20:894-904.
4. Harris R.E., Ashe H.L. Cease and desist: modulating short-range Dpp signalling in the stem-cell niche. EMBO Rep 2011, 12:519-526.
5. Lynch J.A., Roth S. The evolution of dorsal-ventral patterning mechanisms in insects. Genes Dev 2011, 25:107-118.
6. Yeung T.M., Chia L.A., Kosinski C.M., Kuo C.J. Regulation of self-renewal and differentiation by the intestinal stem cell niche. Cell Mol Life Sci 2011, 68:2513-2523.
7. Affolter M., Basler K. The Decapentaplegic morphogen gradient: from pattern formation to growth regulation. Nat Rev Genet 2007, 8:663-674.
8. Umulis D., O'Connor M.B., Blair S.S. The extracellular regulation of bone morphogenetic protein signaling. Development 2009, 136:3715-3728.
9. Sopory S., Kwon S., Wehrli M., Christian J.L. Regulation of Dpp activity by tissue-specific cleavage of an upstream site within the prodomain. Dev Biol 2010, 346:102-112.
10. Wolpert L. Positional information revisited. Development 1989, (Suppl.):3-12.
11. Curtiss J., Halder G., Mlodzik M. Selector and signalling molecules cooperate in organ patterning. Nat Cell Biol 2002, 4:E48-E51.
12. Widmann T.J., Dahmann C. Dpp signaling promotes the cuboidal-to-columnar shape transition of Drosophila wing disc epithelia by regulating Rho1. J Cell Sci 2009, 122:1362-1373.
13. Bangi E., Wharton K. Dpp and Gbb exhibit different effective ranges in the establishment of the BMP activity gradient critical for Drosophila wing patterning. Dev Biol 2006, 295:178-193.
14. Bangi E., Wharton K. Dual function of the Drosophila Alk1/Alk2 ortholog Saxophone shapes the Bmp activity gradient in the wing imaginal disc. Development 2006, 133:3295-3303.
15. Oh H., Irvine K.D. Cooperative regulation of growth by Yorkie and Mad through bantam. Dev Cell 2011, 20:109-122.
16. Crozatier M., Glise B., Vincent A. Connecting Hh, Dpp and EGF signalling in patterning of the Drosophila wing: the pivotal role of collier/knot in the AP organiser. Development 2002, 129:4261-4269.
17. Hamaratoglu F., de Lachapelle A., Pyrowolakis G., Bergmann S., Affolter M. Dpp signaling activity requires Pentagone to scale with tissue size in the growing Drosophila wing imaginal disc. PLoS Biol 2011, 9:e1001182.
18. Wartlick O., Mumcu P., Kicheva A., Bittig T., Seum C., Julicher F., Gonzalez-Gaitan M. Dynamics of Dpp signaling and proliferation control. Science 2011, 331:1154-1159.
19. Tabata T. Genetics of morphogen gradients. Nat Rev Genet 2001, 2:620-630.
20. Kunnapuu J., Bjorkgren I., Shimmi O. The Drosophila DPP signal is produced by cleavage of its proprotein at evolutionary diversified furin-recognition sites. Proc Natl Acad Sci USA 2009, 106:8501-8506.
21. Akiyama T., Kamimura K., Firkus C., Takeo S., Shimmi O., Nakato H. Dally regulates Dpp morphogen gradient formation by stabilizing Dpp on the cell surface. Dev Biol 2008, 313:408-419.
22. Haerry T.E. The interaction between two TGF-beta type I receptors plays important roles in ligand binding, SMAD activation, and gradient formation. Mech Dev 2010, 127:358-370.
23. Khalsa O., Yoon J.-W., Terres-Schumann S., Wharton K. TGF-β/BMP superfamily members. Gbb-60A and Dpp cooperate to provide pattern information and establish cell identity in the Drosophila wing. Development 1998, 125:2723-2734.
24. Chen S., Kaneko S., Ma X., Chen X., Ip Y.T., Xu L., Xie T. Lissencephaly-1 controls germline stem cell self-renewal through modulating bone morphogenetic protein signaling and niche adhesion. Proc Natl Acad Sci USA 2010, 107:19939-19944.
25. Wynshaw-Boris A., Gambello M.J. LIS1 and dynein motor function in neuronal migration and development. Genes Dev 2001, 15:639-651.
26. Blair S.S. Wing vein patterning in Drosophila and the analysis of intercellular signaling. Annu Rev Cell Dev Biol 2007, 23:293-319.
27. Peluso C.E., Umulis D., Kim Y.J., O'Connor M.B., Serpe M. Shaping BMP morphogen gradients through enzyme-substrate interactions. Dev Cell 2011, 21:375-383.
28. Wang X., Harris R.E., Bayston L.J., Ashe H.L. Type IV collagens regulate BMP signalling in Drosophila. Nature 2008, 455:72-77.
29. Neto-Silva R.M., Wells B.S., Johnston L.A. Mechanisms of growth and homeostasis in the Drosophila wing. Annu Rev Cell Dev Biol 2009, 25:197-220.
30. Zecca M., Struhl G. A feed-forward circuit linking wingless, fat-dachsous signaling, and the warts-hippo pathway to Drosophila wing growth. PLoS Biol 2010, 8:e1000386.
31. Sander V., Eivers E., Choi R.H., De Robertis E.M. Drosophila Smad2 opposes Mad signaling during wing vein development. PLoS ONE 2010, 5:e10383.
32. Parker J. Morphogens, nutrients, and the basis of organ scaling. Evol Dev 2011, 13:304-314.
33. Kicheva A., Gonzalez-Gaitan M. The Decapentaplegic morphogen gradient: a precise definition. Curr Opin Cell Biol 2008, 20:137-143.
34. Schwank G., Dalessi S., Yang S.F., Yagi R., de Lachapelle A.M., Affolter M., Bergmann S., Basler K. Formation of the long range Dpp morphogen gradient. PLoS Biol 2011, 9:e1001111.
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. Belenkaya T.Y., Han C., Yan D., Opoka R.J., Khodoun M., Liu H., Lin X. Drosophila Dpp morphogen movement is independent of dynamin-mediated endocytosis but regulated by the glypican members of heparan sulfate proteoglycans. Cell 2004, 119:231-244.
37. Rodal A.A., Blunk A.D., Akbergenova Y., Jorquera R.A., Buhl L.K., Littleton J.T. A presynaptic endosomal trafficking pathway controls synaptic growth signaling. J Cell Biol 2011, 193:201-217.
38. Ogiso Y., Tsuneizumi K., Masuda N., Sato M., Tabata T. Robustness of the Dpp morphogen activity gradient depends on negative feedback regulation by the inhibitory Smad, Dad. Dev Growth Differ 2011, 53:668-678.
39. Crickmore M.A., Mann R.S. Hox control of organ size by regulation of morphogen production and mobility. Science 2006, 313:63-68.
40. Niepielko M.G., Hernaiz-Hernandez Y., Yakoby N. BMP signaling dynamics in the follicle cells of multiple Drosophila species. Dev Biol 2011, 354:151-159.
41. Xia L., Jia S., Huang S., Wang H., Zhu Y., Mu Y., Kan L., Zheng W., Wu D., Li X., et al. The Fused/Smurf complex controls the fate of Drosophila germline stem cells by generating a gradient BMP response. Cell 2010, 143:978-990.
42. Yan D., Lin X. Shaping morphogen gradients by proteoglycans. Cold Spring Harb Perspect Biol 2009, 1:a002493.
43. Kuo W.J., Digman M.A., Lander A.D. Heparan sulfate acts as a bone morphogenetic protein coreceptor by facilitating ligand-induced receptor hetero-oligomerization. Mol Biol Cell 2010, 21:4028-4041.
44. Dejima K., Kanai M.I., Akiyama T., Levings D.C., Nakato H. Novel contact-dependent bone morphogenetic protein (BMP) signaling mediated by heparan sulfate proteoglycans. J Biol Chem 2011, 286:17103-17111.
45. Guo Z., Wang Z. The glypican Dally is required in the niche for the maintenance of germline stem cells and short-range BMP signaling in the Drosophila ovary. Development 2009, 136:3627-3635.
46. Hayashi Y., Kobayashi S., Nakato H. Drosophila glypicans regulate the germline stem cell niche. J Cell Biol 2009, 187:473-480.
47. Fujise M., Takeo S., Kamimura K., Matsuo T., Aigaki T., Izumi S., Nakato H. Dally regulates Dpp morphogen gradient formation in the Drosophila wing. Development 2003, 130:1515-1522.
48. You J., Belenkaya T., Lin X. Sulfated is a negative feedback regulator of wingless in Drosophila. Dev Dyn 2011, 240:640-648.
49. Weiss A., Charbonnier E., Ellertsdottir E., Tsirigos A., Wolf C., Schuh R., Pyrowolakis G., Affolter M. A conserved activation element in BMP signaling during Drosophila development. Nat Struct Mol Biol 2010, 17:69-76.
50. Kamiya Y., Miyazono K., Miyazawa K. Specificity of the inhibitory effects of Dad on TGF-beta family type I receptors, Thickveins, Saxophone, and Baboon in Drosophila. FEBS Lett 2008, 582:2496-2500.
51. Ben-Zvi D., Pyrowolakis G., Barkai N., Shilo B.Z. Expansion-repression mechanism for scaling the Dpp activation gradient in Drosophila wing imaginal discs. Curr Biol 2011, 21:1391-1396.
52. Vuilleumier R., Springhorn A., Patterson L., Koidl S., Hammerschmidt M., Affolter M., Pyrowolakis G. Control of Dpp morphogen signalling by a secreted feedback regulator. Nat Cell Biol 2010, 12:611-617.
53. Szuperak M., Salah S., Meyer E.J., Nagarajan U., Ikmi A., Gibson M.C. Feedback regulation of Drosophila BMP signaling by the novel extracellular protein larval translucida. Development 2011, 138:715-724.
54. Serpe M., Umulis D., Ralston A., Chen J., Olson D.J., Avanesov A., Othmer H., O'Connor M.B., Blair S.S. The BMP-binding protein Crossveinless 2 is a short-range, concentration-dependent, biphasic modulator of BMP signaling in Drosophila. Dev Cell 2008, 14:940-953.
55. Umulis D.M., Shimmi O., O'Connor M.B., Othmer H.G. Organism-scale modeling of early Drosophila patterning via bone morphogenetic proteins. Dev Cell 2010, 18:260-274.
56. Umulis D.M. Analysis of dynamic morphogen scale invariance. J R Soc Interface 2009, 6:1179-1191.
57. Aegerter-Wilmsen T., Aegerter C.M., Hafen E., Basler K. Model for the regulation of size in the wing imaginal disc of Drosophila. Mech Dev 2007, 124:318-326.
58. Hufnagel L., Teleman A.A., Rouault H., Cohen S.M., Shraiman B.I. On the mechanism of wing size determination in fly development. Proc Natl Acad Sci USA 2007, 104:3835-3840.
59. Rogulja D., Irvine K.D. Regulation of cell proliferation by a morphogen gradient. Cell 2005, 123:449-461.
60. Schwank G., Tauriello G., Yagi R., Kranz E., Koumoutsakos P., Basler K. Antagonistic growth regulation by Dpp and Fat drives uniform cell proliferation. Dev Cell 2011, 20:123-130.
61. Clarke D.C., Liu X. Decoding the quantitative nature of TGF-beta/Smad signaling. Trends Cell Biol 2008, 18:430-442.
62. Lembong J., Yakoby N., Shvartsman S.Y. Pattern formation by dynamically interacting network motifs. Proc Natl Acad Sci USA 2009, 106:3213-3218.
63. Eivers E., Fuentealba L.C., Sander V., Clemens J.C., Hartnett L., De Robertis E.M. Mad is required for wingless signaling in wing development and segment patterning in Drosophila. PLoS ONE 2009, 4:e6543.
64. Kaneko S., Chen X., Lu P., Yao X., Wright T.G., Rajurkar M., Kariya K., Mao J., Ip Y.T., Xu L. Smad inhibition by the Ste20 kinase Misshapen. Proc Natl Acad Sci USA 2011, 108:11127-11132.
65. Dworkin I., Anderson J.A., Idaghdour Y., Parker E.K., Stone E.A., Gibson G. The effects of weak genetic perturbations on the transcriptome of the wing imaginal disc and its association with wing shape in Drosophila melanogaster. Genetics 2011, 187:1171-1184.
66. Lander A.D., Lo W.C., Nie Q., Wan F.Y. The measure of success: constraints, objectives, and tradeoffs in morphogen-mediated patterning. Cold Spring Harb Perspect Biol 2009, 1:a002022.
67. Maroni G., Stamey S.C. Use of blue food to select synchronous, late third-instar larvae. Dros Inf Serv 1983, 59:142-143.
68. Cao J., Pellock B., White K., Raftery L.A. A commercial phospho-Smad antibody that detects endogenous BMP signaling in Drosophila tissues. Dros Inf Serv 2006, 89:131-135.
69. Crickmore M.A., Mann R.S. Hox control of morphogen mobility and organ development through regulation of glypican expression. Development 2007, 134:327-334.