JAK/STAT signaling is required for hinge growth and patterning in the Drosophila wing disc

Developmental Biology

Volumn 382, Issue 2, 2013, Pages 413-426

  Ayala Camargo, Aidee ^a   Anderson, Abigail M ^a   Amoyel, Marc ^a   Rodrigues, Aloma B ^a   Flaherty, Maria Sol ^a   Bach, Erika A ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ara; Gap domain; Hinge; Hth; Msh; Nub; Stat92E; Upd; Wg

Indexed keywords

JANUS KINASE; NUBBIN; STAT PROTEIN; STAT92E PROTEIN; TEASHIRT; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; WNT1 PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FATE; CONTROLLED STUDY; DROSOPHILA; EMBRYO PATTERN FORMATION; IMAGINAL DISC; INHIBITION KINETICS; LARVAL DEVELOPMENT; LIMB DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; WING HINGE DEVELOPMENT;

ARA;

EID: 84884814827     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.08.016     Document Type: Article

References (55)

1. Arbouzova N.I., Zeidler M.P. JAK/STAT signalling in Drosophila: insights into conserved regulatory and cellular functions. Development (Cambridge, England) 2006, 133:2605-2616.
2. Ayala-Camargo A., Ekas L.A., Flaherty M.S., Baeg G.H., Bach E.A. The JAK/STAT pathway regulates proximo-distal patterning in Drosophila. Dev. Dyn. 2007, 236:2721-2730.
3. Azpiazu N., Morata G. Function and regulation of homothorax in the wing imaginal disc of Drosophila. Development (Cambridge, England) 2000, 127:2685-2693.
4. Bach E.A., Ekas L.A., Ayala-Camargo A., Flaherty M.S., Lee H., Perrimon N., Baeg G.H. GFP reporters detect the activation of the Drosophila JAK/STAT pathway in vivo. Gene Expr. Patterns 2007, 7:323-331.
5. Bach E.A., Vincent S., Zeidler M.P., Perrimon N. A sensitized genetic screen to identify novel regulators and components of the Drosophila janus kinase/signal transducer and activator of transcription pathway. Genetics 2003, 165:1149-1166.
6. Bessa J., Carmona L., Casares F. Zinc-finger paralogues tsh and tio are functionally equivalent during imaginal development in Drosophila and maintain their expression levels through auto- and cross-negative feedback loops. Dev. Dyn. 2009, 238:19-28.
7. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development (Cambridge, England) 1993, 118:401-415.
8. Capdevila J., Guerrero I. Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J. 1994, 13:4459-4468.
9. Casares F., Mann R.S. A dual role for homothorax in inhibiting wing blade development and specifying proximal wing identities in Drosophila. Development (Cambridge, England) 2000, 127:1499-1508.
10. Cavodeassi F., Diez Del Corral R., Campuzano S., Dominguez M. Compartments and organising boundaries in the Drosophila eye: the role of the homeodomain Iroquois proteins. Development (Cambridge, England) 1999, 126:4933-4942.
11. Cavodeassi F., Modolell J., Campuzano S. The Iroquois homeobox genes function as dorsal selectors in the Drosophila head. Development (Cambridge, England) 2000, 127:1921-1929.
12. Cavodeassi F., Rodriguez I., Modolell J. Dpp signalling is a key effector of the wing-body wall subdivision of the Drosophila mesothorax. Development (Cambridge, England) 2002, 129:3815-3823.
13. Cifuentes F.J., Garcia-Bellido A. Proximo-distal specification in the wing disc of Drosophila by the nubbin gene. Proc. Natl. Acad. Sci. USA 1997, 94:11405-11410.
14. Couso J.P., Bate M., Martinez-Arias A. A wingless-dependent polar coordinate system in Drosophila imaginal discs. Science (New York, N.Y) 1993, 259:484-489.
15. del Alamo Rodriguez D., Terriente J., Galindo M.I., Couso J.P., Diaz-Benjumea F.J. Different mechanisms initiate and maintain wingless expression in the Drosophila wing hinge. Development (Cambridge, England) 2002, 129:3995-4004.
16. Dichtel-Danjoy M.L., Caldeira J., Casares F. SoxF is part of a novel negative-feedback loop in the wingless pathway that controls proliferation in the Drosophila wing disc. Development (Cambridge, England) 2009, 136:761-769.
17. Diez del Corral R., Aroca P., JL G.m.-S., Cavodeassi F., Modolell J. The Iroquois homeodomain proteins are required to specify body wall identity in Drosophila. Genes Dev. 1999, 13:1754-1761.
18. Ekas L.A., Baeg G.H., Flaherty M.S., Ayala-Camargo A., Bach E.A. JAK/STAT signaling promotes regional specification by negatively regulating wingless expression in Drosophila. Development (Cambridge, England) 2006, 133:4721-4729.
19. Ekas L.A., Cardozo T.J., Flaherty M.S., McMillan E.A., Gonsalves F.C., Bach E.A. Characterization of a dominant-active STAT that promotes tumorigenesis in Drosophila. Dev. Biol. 2010, 344:621-636.
20. Fasano L., Roder L., Core N., Alexandre E., Vola C., Jacq B., Kerridge S. The gene teashirt is required for the development of Drosophila embryonic trunk segments and encodes a protein with widely spaced zinc finger motifs. Cell 1991, 64:63-79.
21. Flaherty M.S., Salis P., Evans C.J., Ekas L.A., Marouf A., Zavadil J., Banerjee U., Bach E.A. Chinmo is a functional effector of the JAK/STAT pathway that regulates eye development, tumor formation and stem cell self-renewal in Drosophila. Dev. Cell 2010, 18:556-568.
22. Flaherty M.S., Zavadil J., Ekas L.A., Bach E.A. Genome-wide expression profiling in the Drosophila eye reveals unexpected repression of notch signaling by the JAK/STAT pathway. Dev. Dyn. 2009, 238:2235-2253.
23. Gomez-Skarmeta J.L., Diez del Corral R., de la Calle-Mustienes E., Ferre-Marco D., Modolell J. Araucan and caupolican, two members of the novel iroquois complex, encode homeoproteins that control proneural and vein-forming genes. Cell 1996, 85:95-105.
24. Hombria J.C., Brown S., Hader S., Zeidler M.P. Characterisation of Upd2, a Drosophila JAK/STAT pathway ligand. Dev. Biol. 2005, 288:420-433.
25. Ito K., Awano W., Suzuki K., Hiromi Y., Yamamoto D. The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development (Cambridge, England) 1997, 124:761-771.
26. Johnston L.A., Sanders A.L. Wingless promotes cell survival but constrains growth during Drosophila wing development. Nat. Cell Biol. 2003, 5:827-833.
27. Klein T. Wing disc development in the fly: the early stages. Curr. Opinion Genet. Dev. 2001, 11:470-475.
28. Liu X., Grammont M., Irvine K.D. Roles for scalloped and vestigial in regulating cell affinity and interactions between the wing blade and the wing hinge. Dev. Biol. 2000, 228:287-303.
29. Lovegrove B., Simoes S., Rivas M.L., Sotillos S., Johnson K., Knust E., Jacinto A., Hombria J.C. Coordinated control of cell adhesion, polarity, and cytoskeleton underlies Hox-induced organogenesis in Drosophila. Curr. Biol. 2006, 16:2206-2216.
30. McNeill H., Yang C.H., Brodsky M., Ungos J., Simon M.A. Mirror encodes a novel PBX-class homeoprotein that functions in the definition of the dorsal-ventral border in the Drosophila eye. Genes Dev. 1997, 11:1073-1082.
31. Morata G., Ripoll P. Minutes: mutants of Drosophila autonomously affecting cell division rate. Dev. Biol. 1975, 42:211-221.
32. Mukherjee T., Hombria J.C., Zeidler M.P. Opposing roles for Drosophila JAK/STAT signalling during cellular proliferation. Oncogene 2005, 24:2503-2511.
33. Neumann C.J., Cohen S.M. Distinct mitogenic and cell fate specification functions of wingless in different regions of the wing. Development (Cambridge, England) 1996, 122:1781-1789.
34. Neumann C.J., Cohen S.M. Boundary formation in Drosophila wing: notch activity attenuated by the POU protein Nubbin. Science (New York, N.Y) 1998, 281:409-413.
35. Ng M., Diaz-Benjumea F.J., Cohen S.M. Nubbin encodes a POU-domain protein required for proximal-distal patterning in the Drosophila wing. Development (Cambridge, England) 1995, 121:589-599.
36. Pai C.Y., Kuo T.S., Jaw T.J., Kurant E., Chen C.T., Bessarab D.A., Salzberg A., Sun Y.H. The Homothorax homeoprotein activates the nuclear localization of another homeoprotein, extradenticle, and suppresses eye development in Drosophila. Genes Dev. 1998, 12:435-446.
37. Perea D., Terriente J., Diaz-Benjumea F.J. Temporal and spatial windows delimit activation of the outer ring of wingless in the Drosophila wing. Dev. Biol. 2009, 328:445-455.
38. Rieckhof G.E., Casares F., Ryoo H.D., Abu-Shaar M., Mann R.S. Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein. Cell 1997, 91:171-183.
39. Rodrigues A.B., Zoranovic T., Ayala-Camargo A., Grewal S., Reyes-Robles T., Krasny M., Wu D.C., Johnston L.A., Bach E.A. Activated STAT regulates growth and induces competitive interactions independently of Myc, Yorkie, Wingless and ribosome biogenesis. Development (Cambridge, England) 2012, 139:4051-4061.
40. St Pierre S.E., Galindo M.I., Couso J.P., Thor S. Control of Drosophila imaginal disc development by rotund and roughened eye: differentially expressed transcripts of the same gene encoding functionally distinct zinc finger proteins. Development (Cambridge, England) 2002, 129:1273-1281.
41. Sun Y.H., Tsai C.J., Green M.M., Chao J.L., Yu C.T., Jaw T.J., Yeh J.Y., Bolshakov V.N. White as a reporter gene to detect transcriptional silencers specifying position-specific gene expression during Drosophila melanogaster eye development. Genetics 1995, 141:1075-1086.
42. Terriente J., Perea D., Suzanne M., Diaz-Benjumea F.J. The Drosophila gene zfh2 is required to establish proximal-distal domains in the wing disc. Dev. Biol. 2008, 320:102-112.
43. Tsai Y.C., Y J.G., C P.H., Posakony J.W., Barolo S., Kim J., Henry Sun Y. Upd/Jak/STAT signaling represses wg transcription to allow initiation of morphogenetic furrow in Drosophila eye development. Dev. Biol. 2007, 306:760-771.
44. Tsai Y.C., Sun Y.H. Long-range effect of upd, a ligand for Jak/STAT pathway, on cell cycle in Drosophila eye development. Genesis 2004, 39:141-153.
45. van de Wetering M., Cavallo R., Dooijes D., van Beest M., van Es J., Loureiro J., Ypma A., Hursh D., Jones T., Bejsovec A., Peifer M., Mortin M., Clevers H. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 1997, 88:789-799.
46. Villa-Cuesta E., Modolell J. Mutual repression between msh and Iro-C is an essential component of the boundary between body wall and wing in Drosophila. Development (Cambridge, England) 2005, 132:4087-4096.
47. Wang S.H., Simcox A., Campbell G. Dual role for Drosophila epidermal growth factor receptor signaling in early wing disc development. Genes Dev. 2000, 14:2271-2276.
48. Whitworth A.J., Russell S. Temporally dynamic response to Wingless directs the sequential elaboration of the proximodistal axis of the Drosophila wing. Dev. Biol. 2003, 254:277-288.
49. Wu J., Cohen S.M. Repression of Teashirt marks the initiation of wing development. Development (Cambridge, England) 2002, 129:2411-2418.
50. Xu T., Rubin G.M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development (Cambridge, England) 1993, 117:1223-1237.
51. Zecca M., Struhl G. Control of growth and patterning of the Drosophila wing imaginal disc by EGFR-mediated signaling. Development (Cambridge, England) 2002, 129:1369-1376.
52. Zecca M., Struhl G. Subdivision of the Drosophila wing imaginal disc by EGFR-mediated signaling. Development (Cambridge, England) 2002, 129:1357-1368.
53. Zecca M., Struhl G. Recruitment of cells into the Drosophila wing primordium by a feed-forward circuit of vestigial autoregulation. Development (Cambridge, England) 2007, 134:3001-3010.
54. 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.
55. Zirin J.D., Mann R.S. Nubbin and Teashirt mark barriers to clonal growth along the proximal-distal axis of the Drosophila wing. Dev. Biol. 2007, 304:745-758.