A Feed-Forward Loop Coupling Extracellular BMP Transport and Morphogenesis in Wing
A variety of extracellular factors regulate morphogenesis during development. However, coordination between extracellular signaling and dynamic morphogenesis is largely unexplored. We address the fundamental question by studying posterior crossvein (PCV) development in Drosophila as a model, in which long-range BMP transport from the longitudinal veins plays a critical role during the pupal stages. Here, we show that RhoGAP Crossveinless-C (Cv-C) is induced at the PCV primordial cells by BMP signaling and mediates PCV morphogenesis cell-autonomously by inactivating members of the Rho-type small GTPases. Intriguingly, we find that Cv-C is also required non-cell-autonomously for BMP transport into the PCV region, while a long-range BMP transport is guided toward ectopic wing vein regions by loss of the Rho-type small GTPases. We present evidence that low level of ß-integrin accumulation at the basal side of PCV epithelial cells regulated by Cv-C provides an optimal extracellular environment for guiding BMP transport. These data suggest that BMP transport and PCV morphogenesis are tightly coupled. Our study reveals a feed-forward mechanism that coordinates the spatial distribution of extracellular instructive cues and morphogenesis. The coupling mechanism may be widely utilized to achieve precise morphogenesis during development and homeostasis.
Vyšlo v časopise:
A Feed-Forward Loop Coupling Extracellular BMP Transport and Morphogenesis in Wing. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003403
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003403
Souhrn
A variety of extracellular factors regulate morphogenesis during development. However, coordination between extracellular signaling and dynamic morphogenesis is largely unexplored. We address the fundamental question by studying posterior crossvein (PCV) development in Drosophila as a model, in which long-range BMP transport from the longitudinal veins plays a critical role during the pupal stages. Here, we show that RhoGAP Crossveinless-C (Cv-C) is induced at the PCV primordial cells by BMP signaling and mediates PCV morphogenesis cell-autonomously by inactivating members of the Rho-type small GTPases. Intriguingly, we find that Cv-C is also required non-cell-autonomously for BMP transport into the PCV region, while a long-range BMP transport is guided toward ectopic wing vein regions by loss of the Rho-type small GTPases. We present evidence that low level of ß-integrin accumulation at the basal side of PCV epithelial cells regulated by Cv-C provides an optimal extracellular environment for guiding BMP transport. These data suggest that BMP transport and PCV morphogenesis are tightly coupled. Our study reveals a feed-forward mechanism that coordinates the spatial distribution of extracellular instructive cues and morphogenesis. The coupling mechanism may be widely utilized to achieve precise morphogenesis during development and homeostasis.
Zdroje
1. AffolterM, BaslerK (2007) The Decapentaplegic morphogen gradient: from pattern formation to growth regulation. Nat Rev Genet 8: 663–674.
2. WuMY, HillCS (2009) Tgf-beta superfamily signaling in embryonic development and homeostasis. Dev Cell 16: 329–343.
3. ParkerL, StathakisDG, AroraK (2004) Regulation of BMP and activin signaling in Drosophila. Prog Mol Subcell Biol 34: 73–101.
4. JaffeAB, HallA (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21: 247–269.
5. SchwartzMA, ShattilSJ (2000) Signaling networks linking integrins and rho family GTPases. Trends Biochem Sci 25: 388–391.
6. RossmanKL, DerCJ, SondekJ (2005) GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol 6: 167–180.
7. MoonSY, ZhengY (2003) Rho GTPase-activating proteins in cell regulation. Trends Cell Biol 13: 13–22.
8. CorderoJB, LarsonDE, CraigCR, HaysR, CaganR (2007) Dynamic decapentaplegic signaling regulates patterning and adhesion in the Drosophila pupal retina. Development 134: 1861–1871.
9. WidmannTJ, DahmannC (2009) Dpp signaling promotes the cuboidal-to-columnar shape transition of Drosophila wing disc epithelia by regulating Rho1. J Cell Sci 122: 1362–1373.
10. RalstonA, BlairSS (2005) Long-range Dpp signaling is regulated to restrict BMP signaling to a crossvein competent zone. Dev Biol 280: 187–200.
11. ShimmiO, RalstonA, BlairSS, O'ConnorMB (2005) 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.
12. SerpeM, RalstonA, BlairSS, O'ConnorMB (2005) Matching catalytic activity to developmental function: tolloid-related processes Sog in order to help specify the posterior crossvein in the Drosophila wing. Development 132: 2645–2656.
13. MatsudaS, ShimmiO (2012) Directional transport and active retention of Dpp/BMP create wing vein patterns in Drosophila. Dev Biol 366: 153–162.
14. ShimmiO, UmulisD, OthmerH, O'ConnorMB (2005) Facilitated transport of a Dpp/Scw heterodimer by Sog/Tsg leads to robust patterning of the Drosophila blastoderm embryo. Cell 120: 873–886.
15. WangYC, FergusonEL (2005) Spatial bistability of Dpp-receptor interactions during Drosophila dorsal-ventral patterning. Nature 434: 229–234.
16. O'ConnorMB, UmulisD, OthmerHG, BlairSS (2006) Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 133: 183–193.
17. HoganBL, KolodziejPA (2002) Organogenesis: molecular mechanisms of tubulogenesis. Nat Rev Genet 3: 513–523.
18. SternC (1934) On the Occurrence of Translocations and Autosomal Non-Disjunction in Drosophila melanogaster. Proc Natl Acad Sci U S A 20: 36–39.
19. DenholmB, BrownS, RayRP, Ruiz-GomezM, SkaerH, et al. (2005) crossveinless-c is a RhoGAP required for actin reorganisation during morphogenesis. Development 132: 2389–2400.
20. FristromD, WilcoxM, FristromJ (1993) The distribution of PS integrins, laminin A and F-actin during key stages in Drosophila wing development. Development 117: 509–523.
21. St JohnstonRD, HoffmannFM, BlackmanRK, SegalD, GrimailaR, et al. (1990) Molecular organization of the decapentaplegic gene in Drosophila melanogaster. Genes Dev 4: 1114–1127.
22. BroduV, CasanovaJ (2006) The RhoGAP crossveinless-c links trachealess and EGFR signaling to cell shape remodeling in Drosophila tracheal invagination. Genes Dev 20: 1817–1828.
23. SimoesS, DenholmB, AzevedoD, SotillosS, MartinP, et al. (2006) Compartmentalisation of Rho regulators directs cell invagination during tissue morphogenesis. Development 133: 4257–4267.
24. FehonRG, OrenT, LaJeunesseDR, MelbyTE, McCartneyBM (1997) Isolation of mutations in the Drosophila homologues of the human Neurofibromatosis 2 and yeast CDC42 genes using a simple and efficient reverse-genetic method. Genetics 146: 245–252.
25. LeeT, LuoL (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451–461.
26. SerpeM, UmulisD, RalstonA, ChenJ, OlsonDJ, et al. (2008) The BMP-binding protein Crossveinless 2 is a short-range, concentration-dependent, biphasic modulator of BMP signaling in Drosophila. Dev Cell 14: 940–953.
27. TelemanAA, CohenSM (2000) Dpp gradient formation in the Drosophila wing imaginal disc. Cell 103: 971–980.
28. BaronM, O'LearyV, EvansDA, HicksM, HudsonK (2000) Multiple roles of the Dcdc42 GTPase during wing development in Drosophila melanogaster. Mol Gen Genet 264: 98–104.
29. GenovaJL, JongS, CampJT, FehonRG (2000) Functional analysis of Cdc42 in actin filament assembly, epithelial morphogenesis, and cell signaling during Drosophila development. Dev Biol 221: 181–194.
30. AraujoH, NegreirosE, BierE (2003) Integrins modulate Sog activity in the Drosophila wing. Development 130: 3851–3864.
31. WilcoxM, DiAntonioA, LeptinM (1989) The function of PS integrins in Drosophila wing morphogenesis. Development 107: 891–897.
32. BementWM, MillerAL, von DassowG (2006) Rho GTPase activity zones and transient contractile arrays. Bioessays 28: 983–993.
33. YanJ, LuQ, FangX, AdlerPN (2009) Rho1 has multiple functions in Drosophila wing planar polarity. Dev Biol 333: 186–199.
34. Dominguez-GimenezP, BrownNH, Martin-BermudoMD (2007) Integrin-ECM interactions regulate the changes in cell shape driving the morphogenesis of the Drosophila wing epithelium. J Cell Sci 120: 1061–1071.
35. ChenJ, HoneyagerSM, SchleedeJ, AvanesovA, LaughonA, et al. (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. BuntS, HooleyC, HuN, ScahillC, WeaversH, et al. (2010) Hemocyte-secreted type IV collagen enhances BMP signaling to guide renal tubule morphogenesis in Drosophila. Dev Cell 19: 296–306.
37. WangX, HarrisRE, BaystonLJ, AsheHL (2008) Type IV collagens regulate BMP signalling in Drosophila. Nature 455: 72–77.
38. Pastor-ParejaJC, XuT (2011) Shaping cells and organs in Drosophila by opposing roles of fat body-secreted Collagen IV and perlecan. Dev Cell 21: 245–256.
39. MurrayMA, FesslerLI, PalkaJ (1995) Changing distributions of extracellular matrix components during early wing morphogenesis in Drosophila. Dev Biol 168: 150–165.
40. VuilleumierR, SpringhornA, PattersonL, KoidlS, HammerschmidtM, et al. (2010) Control of Dpp morphogen signalling by a secreted feedback regulator. Nat Cell Biol 12: 611–617.
41. SzuperakM, SalahS, MeyerEJ, NagarajanU, IkmiA, et al. (2011) Feedback regulation of Drosophila BMP signaling by the novel extracellular protein larval translucida. Development 138: 715–724.
42. KesavanG, SandFW, GreinerTU, JohanssonJK, KobberupS, et al. (2009) Cdc42-mediated tubulogenesis controls cell specification. Cell 139: 791–801.
43. LahozA, HallA (2008) DLC1: a significant GAP in the cancer genome. Genes Dev 22: 1724–1730.
44. MassagueJ (2008) TGFbeta in Cancer. Cell 134: 215–230.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2013 Číslo 3
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Fine Characterisation of a Recombination Hotspot at the Locus and Resolution of the Paradoxical Excess of Duplications over Deletions in the General Population
- Molecular Networks of Human Muscle Adaptation to Exercise and Age
- Recurrent Rearrangement during Adaptive Evolution in an Interspecific Yeast Hybrid Suggests a Model for Rapid Introgression
- Genome-Wide Association Study and Gene Expression Analysis Identifies as a Predictor of Response to Etanercept Therapy in Rheumatoid Arthritis