The developing wing crossvein of Drosophila melanogaster: a fascinating model for signaling and morphogenesis

References

• Blair SS. Wing vein patterning in Drosophila and the analysis of intercellular signaling. Annu Rev Cell Dev Biol. 2007;23(293–319):293–319.
   PubMedGoogle Scholar
• De Celis JF. Pattern formation in the Drosophila wing: the development of the veins. Bioessays. 2003;25(443–451):443–451.
   PubMedGoogle Scholar
• Matamoro-Vidal A, Salazar-Ciudad I, Houle D. Making quantitative morphological variation from basic developmental processes: where are we? the case of the Drosophila wing. Dev Dyn. 2015;244(1058–1073):1058–1073.
   PubMedGoogle Scholar
• Bridges CB. The mutant crossveinless in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1920;6(660–663):660–663.
   PubMedGoogle Scholar
• Waddington CH. The genetic control of wing development in Drosophila. J. Genet. 1940;41(75–139):75–113.
   Google Scholar
• Waddington CH. Genetic assimilation of an acquired character. Evolution. 1953;7(118–126):118–126.
   Google Scholar
• Thompson SR. The effect of temperature on crossvein formation in crossveinless-like strains of drosophila melanogaster. Genetics. 1967;56(13–22):13–22.
   PubMedGoogle Scholar
• Mohler JD. Preliminary genetic analysis of crossveinless-like strains of drosophila melanogaster. Genetics. 1965;51(641–651):641–651.
   PubMedGoogle Scholar
• Mohler JD. The influence of some crossveinless-like genes on the crossveinless phenocopy sensitivity in drosophila melanogaster. Genetics. 1965;51(329–340):329–340.
   PubMedGoogle Scholar
• Milkman RD. The genetic basis of natural variation. VI. selection of a crossveinless strain of Drosophila by phenocopying at high temperature. Genetics. 1965;51:87–96.
   PubMed Web of Science ®Google Scholar
• Mohler JD, Swedberg GS. Wing vein development in crossveinless-like strains of drosophila melanogaster. Genetics. 1964;50(1403–1419):1403–1419.
   PubMedGoogle Scholar
• Milkman RD. The genetic basis of natural variation. V. selection for crossveinless polygenes in new wild strains of Drosophila melanogaster. Genetics. 1964;50:625–632.
   PubMedGoogle Scholar
• Mohler JD. Some interactions of crossveinless-like genes in drosophila melanogaster. Genetics. 1967;57(65–77):65–77.
   PubMedGoogle Scholar
• Marcus JM. The development and evolution of crossveins in insect wings. J Anat. 2001;199(211–216):211–216.
   PubMedGoogle Scholar
• Lindsley DL, Zimm GG. The genome of Drosophila melanogaster. Academic Press; 1992.
   Google Scholar
• Gui J, Huang Y, Montanari M, et al. Coupling between dynamic 3D tissue architecture and BMP morphogen signaling during Drosophila wing morphogenesis. Proc Natl Acad Sci U S A. 2019;116(4352–4361). DOI:10.1073/pnas.1815427116.
   Google Scholar
• Montanari MP, Tran NV, Shimmi O. Regulation of spatial distribution of BMP ligands for pattern formation. Dev Dyn. 2022;251(198–212):178–192.
   PubMedGoogle Scholar
• Shimmi O, Newfeld SJ. New insights into extracellular and post-translational regulation of TGF-beta family signalling pathways. J Biochem. 2013;154(11–19):11–19.
   PubMedGoogle Scholar
• Yan SJ, Zartman JJ, Zhang M, et al. Bistability coordinates activation of the EGFR and DPP pathways in Drosophila vein differentiation. Mol Syst Biol. 2009;5(278). DOI:10.1038/msb.2009.35.
   Google Scholar
• Martín-Blanco E, Roch F, Noll E, et al. A temporal switch in DER signaling controls the specification and differentiation of veins and interveins in the Drosophila wing. Development. 1999;126(5739–5747). DOI:10.1242/dev.126.24.5739.
   PubMedGoogle Scholar
• Ralston A, Blair SS. Long-range Dpp signaling is regulated to restrict BMP signaling to a crossvein competent zone. Dev Biol. 2005;280(187–200):187–200.
   PubMedGoogle Scholar
• Diaz-Benjumea FJ, Garcia-Bellido A. Behaviour of cells mutant for an EGF receptor homologue of Drosophila in genetic mosaics. Proc Biol Sci. 1990;242:36–44.
   PubMedGoogle Scholar
• de Celis JF, Bray S, Garcia-Bellido A. Notch signalling regulates veinlet expression and establishes boundaries between veins and interveins in the Drosophila wing. Development. 1997;124(1919–1928):1919–1928.
   PubMedGoogle Scholar
• de Celis JF. Expression and function of decapentaplegic and thick veins during the differentiation of the veins in the Drosophila wing. Development. 1997;124(1007–1018):1007–1018.
   PubMedGoogle Scholar
• Conley CA, Silburn R, Singer MA, et al. 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. 2000;127(3947–3959). DOI:10.1242/dev.127.18.3947.
   PubMedGoogle Scholar
• Matsuda S, Shimmi O. Directional transport and active retention of Dpp/BMP create wing vein patterns in Drosophila. Dev Biol. 2012;366:153–162.
   PubMedGoogle Scholar
• Shimmi O, Ralston A, Blair SS, et al. 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. 2005;282:70–83.
   PubMed Web of Science ®Google Scholar
• Ray RP, Wharton KA. Context-dependent relationships between the BMPs gbb and dpp during development of the Drosophila wing imaginal disk. Development. 2001;128(3913–3925):3913–3925.
   PubMedGoogle Scholar
• Padgett RW, Wozney JM, Gelbart WM. Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc Natl Acad Sci U S A. 1993;90(2905–2909):2905–2909.
   PubMedGoogle Scholar
• Shimmi O, Newfeld SJ. New insights into extracellular and post-translational regulation of TGF-β family signalling pathways. J Biochem. 2013;154(11–19):11–19.
   PubMedGoogle Scholar
• Christoforou CP, Greer CE, Challoner BR, et al. The detached locus encodes Drosophila dystrophin, which acts with other components of the dystrophin associated protein complex to influence intercellular signalling in developing wing veins. Dev Biol. 2008;313:519–532.
   PubMed Web of Science ®Google Scholar
• Gui J, Huang Y, Shimmi O. Scribbled optimizes BMP signaling through its receptor internalization to the Rab5 endosome and promote robust epithelial morphogenesis. PLoS Genet. 2016;12(e1006424):1006424.
   Google Scholar
• Matsuda S, Blanco J, Shimmi O. A feed-forward loop coupling extracellular BMP transport and morphogenesis in Drosophila wing. PLoS Genet. 2013;9(e1003403):1003403.
   Google Scholar
• St Johnston RD, Hoffmann FM, Blackman RK, et al. Molecular organization of the decapentaplegic gene in Drosophila melanogaster. Genes Dev. 1990;4(1114–1127):1114–1127.
   PubMedGoogle Scholar
• Segal D, Gelbart WM. Shortvein, a new component of the decapentaplegic gene complex in Drosophila melanogaster. Genetics. 1985;109:119–143.
   PubMed Web of Science ®Google Scholar
• Khalsa O, Yoon JW, Torres-Schumann S, et al. TGF-beta/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.
   PubMed Web of Science ®Google Scholar
• Francois V, Solloway M, O’Neill JW, et al. Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene. Genes Dev. 1994;8(2602–2616):2602–2616.
   PubMedGoogle Scholar
• Holley SA, Jackson PD, Sasai Y, et al. A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature. 1995;376(249–253). DOI:10.1038/376249a0.
   PubMedGoogle Scholar
• Yu K, Sturtevant MA, Biehs B, et al. The Drosophila decapentaplegic and short gastrulation genes function antagonistically during adult wing vein development. Development. 1996;122(4033–4044). DOI:10.1242/dev.122.12.4033.
   Google Scholar
• Yu K, Srinivasan S, Shimmi O, et al. Processing of the Drosophila sog protein creates a novel BMP inhibitory activity. Development. 2000;127(2143–2154). DOI:10.1242/dev.127.10.2143.
   Google Scholar
• Ross JJ, Shimmi O, Vilmos P, et al. Twisted gastrulation is a conserved extracellular BMP antagonist. Nature. 2001;410(479–483). DOI:10.1038/35068578.
   Google Scholar
• Vilmos P, Sousa-Neves R, Lukacsovich T, et al. Marsh, crossveinless defines a new family of twisted-gastrulation-like modulators of bone morphogenetic protein signalling. EMBO Rep. 2005;6:262–267.
   PubMed Web of Science ®Google Scholar
• Shimmi O, Umulis D, Othmer H, et al. Facilitated transport of a Dpp/Scw heterodimer by Sog/Tsg leads to robust patterning of the Drosophila blastoderm embryo. Cell. 2005;120(873–886):873–886.
   PubMedGoogle Scholar
• Umulis DM, Shimmi O, O’Connor MB, et al. Organism-scale modeling of early Drosophila patterning via bone morphogenetic proteins. Dev Cell. 2010;18(260–274):260–274.
   PubMedGoogle Scholar
• Shimmi O, O’Connor MB. Physical properties of Tld, Sog, Tsg and Dpp protein interactions are predicted to help create a sharp boundary in Bmp signals during dorsoventral patterning of the Drosophila embryo. Development. 2003;130:4673–4682.
   PubMed Web of Science ®Google Scholar
• Serpe M, Ralston A, Blair SS, et al. Matching catalytic activity to developmental function: tolloid-related processes Sog in order to help specify the posterior crossvein in the Drosophila wing. Development. 2005;132(2645–2656):2645–2656.
   PubMedGoogle Scholar
• Lecuit T, Cohen SM. Dpp receptor levels contribute to shaping the Dpp morphogen gradient in the Drosophila wing imaginal disc. Development. 1998;125(4901–4907):4901–4907.
   PubMedGoogle Scholar
• Serpe M, Umulis D, Ralston A, et al. 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.
   PubMed Web of Science ®Google Scholar
• Chen J, Honeyager SM, Schleede J, et al. Crossveinless d is a vitellogenin-like lipoprotein that binds BMPs and HSPGs, and is required for normal BMP signaling in the Drosophila wing. Development. 2012;139:2170–2176.
   PubMed Web of Science ®Google Scholar
• Michele DE, Campbell KP. Dystrophin-glycoprotein complex: post-translational processing and dystroglycan function. J Biol Chem. 2003;278(15457–15460):15457–15460.
   PubMedGoogle Scholar
• Gilmour D, Rembold M, Leptin M. From morphogen to morphogenesis and back. Nature. 2017;541(311–320):311–320.
   PubMedGoogle Scholar
• Denholm B, Brown S, Ray RP, et al. crossveinless-c is a RhoGAP required for actin reorganisation during morphogenesis. Development. 2005;132(2389–2400). DOI:10.1242/dev.01829.
   PubMedGoogle Scholar
• Araujo H, Negreiros E, Bier E. Integrins modulate sog activity in the Drosophila wing. Development. 2003;130(3851–3864):3851–3864.
   PubMedGoogle Scholar
• Genova JL, Jong S, Camp JT, et al. Functional analysis of Cdc42 in actin filament assembly, epithelial morphogenesis, and cell signaling during Drosophila development. Dev Biol. 2000;221:181–194.
   PubMed Web of Science ®Google Scholar
• Bilder D, Perrimon N. Localization of apical epithelial determinants by the basolateral PDZ protein scribble. Nature. 2000;403(676–680):676–680.
   PubMedGoogle Scholar
• Bilder D. Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. Genes Dev. 2004;18(1909–1925):1909–1925.
   PubMedGoogle Scholar
• Bonello TT, Peifer M. Scribble: a master scaffold in polarity, adhesion, synaptogenesis, and proliferation. J Cell Biol. 2019;218:742–756.
   PubMed Web of Science ®Google Scholar
• Mason ED, Konrad KD, Webb CD, et al. Dorsal midline fate in Drosophila embryos requires twisted gastrulation, a gene encoding a secreted protein related to human connective tissue growth factor. Genes Dev. 1994;8:1489–1501.
   PubMed Web of Science ®Google Scholar
• Bier E, De Robertis EM. EMBRYO DEVELOPMENT. BMP gradients: a paradigm for morphogen-mediated developmental patterning. Science. 2015;348:5838.
   Web of Science ®Google Scholar
• Matsuda S, Yoshiyama N, Künnapuu-Vulli J, et al. Dpp/BMP transport mechanism is required for wing venation in the sawfly athalia rosae. Insect Biochem Mol Biol. 2013;43(466–473):466–473.
   PubMedGoogle Scholar
• Shimmi O, Matsuda S, Hatakeyama M. Insights into the molecular mechanisms underlying diversified wing venation among insects. Proc Biol Sci. 2014;281(20140264).
   PubMedGoogle Scholar
• Huang Y, Hatakeyama M, Shimmi O. Wing vein development in the sawfly athalia rosae is regulated by spatial transcription of Dpp/BMP signaling components. Arthropod Struct Dev. 2018;47(408–415):408–415.
   PubMedGoogle Scholar
• Ichikawa A, Kotaki M, Sahashi R, et al. Targeted overexpression of drosophila transglutaminase-b induced characteristic phenotypes in a manner similar to transglutaminase-A. Biosci Biotechnol Biochem. 2011;75(1402–1404):1402–1404.
   PubMedGoogle Scholar
• Ichikawa A, Yamada A, Sakamoto H, et al. Overexpression of transglutaminase in the drosophila wing imaginal disc induced an extra wing crossvein phenotype. Biosci Biotechnol Biochem. 2010;74(2494–2496):2494–2496.
   PubMedGoogle Scholar
• Toddie-Moore DJ, Montanari MP, Tran NV, et al. Mechano-chemical feedback mediated competition for BMP signalling leads to pattern formation. Dev Biol. 2022;481(43–51). DOI:10.1016/j.ydbio.2021.09.006.
   PubMedGoogle Scholar