Distinct Molecular Strategies for Hox-Mediated Limb Suppression in : From Cooperativity to Dispensability/Antagonism in TALE Partnership

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The emergence following gene duplication of a large repertoire of Hox paralogue proteins underlies the importance taken by Hox proteins in controlling animal body plans in development and evolution. Sequence divergence of paralogous proteins accounts for functional specialization, promoting axial morphological diversification in bilaterian animals. Yet functionally specialized paralogous Hox proteins also continue performing ancient common functions. In this study, we investigate how highly divergent Hox proteins perform an identical function. This was achieved by comparing in Drosophila the mode of limb suppression by the central (Ultrabithorax and AbdominalA) and posterior class (AbdominalB) Hox proteins. Results highlight that Hox-mediated limb suppression relies on distinct modes of DNA binding and a distinct use of TALE cofactors. Control of common functions by divergent Hox proteins, at least in the case studied, relies on evolving novel molecular properties. Thus, changes in protein sequences not only provide the driving force for functional specialization of Hox paralogue proteins, but also provide means to perform common ancient functions in distinct ways.

Vyšlo v časopise: Distinct Molecular Strategies for Hox-Mediated Limb Suppression in : From Cooperativity to Dispensability/Antagonism in TALE Partnership. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003307
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003307

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Zdroje

1. PearsonJC, LemonsD, McGinnisW (2005) Modulating Hox gene functions during animal body patterning. Nat Rev Genet 6: 893–904.

2. MannRS, LelliKM, JoshiR (2009) Hox specificity unique roles for cofactors and collaborators. Curr Top Dev Biol 88: 63–101.

3. MerabetS, HudryB, SaadaouiM, GrabaY (2009) Classification of sequence signatures: a guide to Hox protein function. Bioessays 31: 500–511.

4. GehringWJ, KloterU, SugaH (2009) Evolution of the Hox gene complex from an evolutionary ground state. Curr Top Dev Biol 88: 35–61.

5. SchubertFR, Nieselt-StruweK, GrussP (1993) The Antennapedia-type homeobox genes have evolved from three precursors separated early in metazoan evolution. Proc Natl Acad Sci Usa 90: 143–147.

6. DubouleD (1994) Guidebook to the Homeobox genes: oxford university press.

7. de RosaR, GrenierJK, AndreevaT, CookCE, AdoutteA, et al. (1999) Hox genes in brachiopods and priapulids and protostome evolution. Nature 399: 772–776.

8. HueberSD, WeillerGF, DjordjevicMA, FrickeyT Improving Hox protein classification across the major model organisms. PLoS ONE 5: e10820 doi:10.1371/journal.pone.0010820.

9. RohsR, JinX, WestSM, JoshiR, HonigB, et al. (2010) Origins of specificity in protein-DNA recognition. Annu Rev Biochem 79: 233–269.

10. CoiffierD, CharrouxB, KerridgeS (2008) Common functions of central and posterior Hox genes for the repression of head in the trunk of Drosophila. Development 135: 291–300.

11. HirthF, LoopT, EggerB, MillerDF, KaufmanTC, et al. (2001) Functional equivalence of Hox gene products in the specification of the tritocerebrum during embryonic brain development of Drosophila. Development 128: 4781–4788.

12. JohnsonFB, ParkerE, KrasnowMA (1995) Extradenticle protein is a selective cofactor for the Drosophila homeotics: Role of the homeodomain and YPWM amino acid motif in the interaction. ProcNatlAcadSciUSA 92: 739–743.

13. LelliKM, NoroB, MannRS (2011) Variable motif utilization in homeotic selector (Hox)-cofactor complex formation controls specificity. Proc Natl Acad Sci U S A 108: 21122–21127.

14. SaadaouiM, MerabetS, Litim-MecheriI, ArbeilleE, SambraniN, et al. (2011) Selection of distinct Hox-Extradenticle interaction modes fine-tunes Hox protein activity. Proc Natl Acad Sci U S A 108: 2276–2281.

15. MerabetS, SaadaouiM, SambraniN, HudryB, PradelJ, et al. (2007) A unique Extradenticle recruitment mode in the Drosophila Hox protein Ultrabithorax. Proc Natl Acad Sci U S A 104: 16946–16951.

16. LaRonde-LeBlancNA, WolbergerC (2003) Structure of HoxA9 and Pbx1 bound to DNA: Hox hexapeptide and DNA recognition anterior to posterior. Genes Dev 17: 2060–2072.

17. VachonG, CohenB, PfeifleC, McGuffinME, BotasJ, et al. (1992) Homeotic genes of the bithorax complex repress limb development in the abdomen of the Drosophila embryo through the target gene Distal-less. Cell 71: 437–450.

18. GalindoMI, Fernandez-GarzaD, PhillipsR, CousoJP (2011) Control of Distal-less expression in the Drosophila appendages by functional 3′ enhancers. Dev Biol 353: 396–410.

19. GebeleinB, CuliJ, RyooHD, ZhangW, MannRS (2002) Specificity of distalless repression and limb primordia development by abdominal hox proteins. Dev Cell 3: 487–498.

20. GebeleinB, McKayDJ, MannRS (2004) Direct integration of Hox and segmentation gene inputs during Drosophila development. Nature 431: 653–659.

21. AgelopoulosM, McKayDJ, MannRS (2012) Developmental regulation of chromatin conformation by Hox proteins in Drosophila. Cell Rep 1: 350–359.

22. CelnikerSE, LewisEB (1987) Transabdominal, a dominant mutant of the Bithorax Complex, produces a sexually dimorphic segmental transformation in Drosophila. Genes Dev 1: 111–123.

23. AzpiazuN, MorataG (1998) Functional and regulatory interactions between Hox and extradenticle genes. Genes Dev 12: 261–273.

24. RivasML, Espinoza-VasquezJM, SambraniN, GreigS, MerabetS, GrabaY, Castelli-Gair HombríaJ (2013) Antagonism versus cooperativity with TALE cofactors at the base of the functional diversification of Hox protein function. PLoS Genet 9: e1003252 doi:10.1371/journal.pgen.1003252.

25. Sánchez-HerreroE, CrosbyMA (1988) The Abdominal-B gene of Drosophila melanogaster: overlapping transcripts exhibit two different spatial distributions. EMBO J 2163–2173.

26. PassnerJM, RyooHD, ShenL, MannRS, AggarwalAK (1999) Structure of a DNA-bound Ultrabithorax-Extradenticle homeodomain complex. Nature 397: 714–719.

27. PiperDE, BatchelorAH, ChangCP, ClearyML, WolbergerC (1999) Structure of a HoxB1-Pbx1 heterodimer bound to DNA: role of the hexapeptide and a fourth homeodomain helix in complex formation. Cell 96: 587–597.

28. JoshiR, PassnerJM, RohsR, JainR, SosinskyA, et al. (2007) Functional specificity of a Hox protein mediated by the recognition of minor groove structure. Cell 131: 530–543.

29. GalantR, WalshCM, CarrollSB (2002) Hox repression of a target gene: extradenticle-independent, additive action through multiple monomer binding sites. Development 129: 3115–3126.

30. MerabetS, KambrisZ, CapovillaM, BerengerH, PradelJ, et al. (2003) The Hexapeptide and Linker Regions of the AbdA Hox Protein Regulate Its Activating and Repressive Functions. Dev Cell 4: 761–768.

31. MerabetS, Litim-MecheriI, KarlssonD, DixitR, SaadaouiM, et al. (2011) Insights into Hox protein function from a large scale combinatorial analysis of protein domains. PLoS Genet 7: e1002302 doi:10.1371/journal.pgen.1002302.

32. ZengW, AndrewDJ, MathiesLD, HornerMA, ScottMP (1993) Ectopic expression and function of the Antp and Scr homeotic genes: The N terminus of the homeodomain is critical to functional specificity. Development 118: 339–352.

33. Furukubo-TokunagaK, FlisterS, GehringWJ (1993) Functional specificity of the antennapedia homeodomain. Proc Natl Acad Sci Usa 90: 6360–6364.

34. Joshi R, Sun L, Mann R Dissecting the functional specificities of two Hox proteins. Genes Dev 24: 1533–1545.

35. CapovillaM, BrandtM, BotasJ (1994) Direct regulation of decapentaplegic by Ultrabithorax and its role in midugt morphogenesis. Cell 76: 461–475.

36. TreismanJ, GönczyP, VashishthaM, HarrisE, DesplanC (1989) A single amino acid can determine the DNA-binding specificity of homeodomain proteins. Cell 59: 553–562.

37. HudryB, RemacleS, DelfiniMC, RezsohazyR, GrabaY, et al. (2012) Hox Proteins Display a Common and Ancestral Ability to Diversify Their Interaction Mode with the PBC Class Cofactors. PLoS Biol 10: e1001351 doi:10.1371/journal.pbio.1001351.

38. RyooHD, MannRS (1999) The control of trunk Hox specificity and activity by Extradenticle. Genes Dev 13: 1704–1716.

39. PeiferM, WieschausE (1990) Mutations in the Drosophila gene extradenticle affect the way specific homeo domain proteins regulate segmental identity. Genes Dev 4: 1209–1223.

40. GrienenbergerA, MerabetS, ManakJ, IltisI, FabreA, et al. (2003) Tgf{beta} signaling acts on a Hox response element to confer specificity and diversity to Hox protein function. Development 130: 5445–5455.

41. HuN, Castelli-GairJ (1999) Study of the posterior spiracles of Drosophila as a model to understand the genetic and cellular mechanisms controlling morphogenesis. Dev Biol 214: 197–210.

42. EstradaB, Sanchez-HerreroE (2001) The Hox gene Abdominal-B antagonizes appendage development in the genital disc of Drosophila. Development 128: 331–339.

43. SlatteryM, RileyT, LiuP, AbeN, Gomez-AlcalaP, et al. (2011) Cofactor binding evokes latent differences in DNA binding specificity between Hox proteins. Cell 147: 1270–1282.

44. CasaresF, MannRS (2000) A dual role for homothorax in inhibiting wing blade development and specifying proximal wing identities in Drosophila. Development 127: 1499–1508.

45. MerabetS, EbnerA, AffolterM (2005) The Drosophila Extradenticle and Homothorax selector proteins control branchless/FGF expression in mesodermal bridge-cells. EMBO Rep 6: 762–768.

46. CasaresF, MannRS (1998) Control of antennal versus leg development in Drosophila [see comments]. Nature 392: 723–726.

47. FerrettiE, LiB, ZewduR, WellsV, HebertJM, et al. (2011) A conserved Pbx-Wnt-p63-Irf6 regulatory module controls face morphogenesis by promoting epithelial apoptosis. Dev Cell 21: 627–641.

48. GehringWJ, QianYQ, BilleterM, Furokubo-TokunagaK, SchierAF, et al. (1994) Homeodomain-DNA recognition. Cell 78: 211–223.

49. TourE, HittingerCT, McGinnisW (2005) Evolutionarily conserved domains required for activation and repression functions of the Drosophila Hox protein Ultrabithorax. Development 132: 5271–5281.

50. Castelli-GairJ, GreigS, MicklemG, AkamM (1994) Dissecting the temporal requirements for homeotic gene function. Development 120: 1983–1995.

51. YoffeKB, ManoukianAS, WilderEL, BrandAH, PerrimonN (1995) Evidence for engrailed-independent wingless autoregulation in Drosophila. DevBiol 170: 636–650.

52. SansonB, WhiteP, VincentJP (1996) Uncoupling cadherin-based adhesion from wingless signalling in Drosophila. Nature 383: 627–630.

53. RubinGM, SpradlingAC (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218: 348–353.

54. BischofJ, MaedaRK, HedigerM, KarchF, BaslerK (2007) An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci U S A 104: 3312–3317.

55. ChanSK, JaffeL, CapovillaM, BotasJ, MannRS (1994) The DNA binding specificity of Ultrabithorax is modulated by cooperative interactions with extradenticle, another homeoprotein. Cell 78: 603–615.