#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Araucan and Caupolican Integrate Intrinsic and Signalling Inputs for the Acquisition by Muscle Progenitors of the Lateral Transverse Fate


A central issue of myogenesis is the acquisition of identity by individual muscles. In Drosophila, at the time muscle progenitors are singled out, they already express unique combinations of muscle identity genes. This muscle code results from the integration of positional and temporal signalling inputs. Here we identify, by means of loss-of-function and ectopic expression approaches, the Iroquois Complex homeobox genes araucan and caupolican as novel muscle identity genes that confer lateral transverse muscle identity. The acquisition of this fate requires that Araucan/Caupolican repress other muscle identity genes such as slouch and vestigial. In addition, we show that Caupolican-dependent slouch expression depends on the activation state of the Ras/Mitogen Activated Protein Kinase cascade. This provides a comprehensive insight into the way Iroquois genes integrate in muscle progenitors, signalling inputs that modulate gene expression and protein activity.


Vyšlo v časopise: Araucan and Caupolican Integrate Intrinsic and Signalling Inputs for the Acquisition by Muscle Progenitors of the Lateral Transverse Fate. PLoS Genet 7(7): e32767. doi:10.1371/journal.pgen.1002186
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002186

Souhrn

A central issue of myogenesis is the acquisition of identity by individual muscles. In Drosophila, at the time muscle progenitors are singled out, they already express unique combinations of muscle identity genes. This muscle code results from the integration of positional and temporal signalling inputs. Here we identify, by means of loss-of-function and ectopic expression approaches, the Iroquois Complex homeobox genes araucan and caupolican as novel muscle identity genes that confer lateral transverse muscle identity. The acquisition of this fate requires that Araucan/Caupolican repress other muscle identity genes such as slouch and vestigial. In addition, we show that Caupolican-dependent slouch expression depends on the activation state of the Ras/Mitogen Activated Protein Kinase cascade. This provides a comprehensive insight into the way Iroquois genes integrate in muscle progenitors, signalling inputs that modulate gene expression and protein activity.


Zdroje

1. BateM 1993 The mesoderm and its derivatives; Martinez-AriasMBaA Cold Spring Harbor, New York CHS Laboratory Press 1013 1090

2. BayliesMKBateMRuiz GomezM 1998 Myogenesis: a view from Drosophila. Cell 93 921 927

3. CarmenaABateMJimenezF 1995 Lethal of scute, a proneural gene, participates in the specification of muscle progenitors during Drosophila embryogenesis. Genes Dev 9 2373 2383

4. CarmenaAGisselbrechtSHarrisonJJimenezFMichelsonAM 1998 Combinatorial signaling codes for the progressive determination of cell fates in the Drosophila embryonic mesoderm. Genes Dev 12 3910 3922

5. CarmenaAMurugasu-OeiBMenonDJimenezFChiaW 1998 Inscuteable and numb mediate asymmetric muscle progenitor cell divisions during Drosophila myogenesis. Genes Dev 12 304 315

6. Ruiz-GómezMBateM 1997 Segregation of myogenic lineages in Drosophila requires numb. Development 124 4857 4866

7. DuanHSkeathJBNguyenHT 2001 Drosophila Lame duck, a novel member of the Gli superfamily, acts as a key regulator of myogenesis by controlling fusion-competent myoblast development. Development 128 4489 4500

8. FurlongEEAndersenECNullBWhiteKPScottMP 2001 Patterns of gene expression during Drosophila mesoderm development. Science 293 1629 1633

9. Ruiz-GómezMCouttsNSusterMLLandgrafMBateM 2002 myoblasts incompetent encodes a zinc finger transcription factor required to specify fusion-competent myoblasts in Drosophila. Development 129 133 141

10. BayliesMKMichelsonAM 2001 Invertebrate myogenesis: looking back to the future of muscle development. Curr Opin Genet Dev 11 431 439

11. TixierVBatailleLJaglaK 2010 Diversification of muscle types: recent insights from Drosophila. Exp Cell Res 316 3019 3027

12. RushtonEDrysdaleRAbmayrSMMichelsonAMBateM 1995 Mutations in a novel gene, myoblast city, provide evidence in support of the founder cell hypothesis for Drosophila muscle development. Development 121 1979 1988

13. BourgouinCLundgrenSEThomasJB 1992 Apterous is a Drosophila LIM domain gene required for the development of a subset of embryonic muscles. Neuron 9 549 561

14. DuanHZhangCChenJSinkHFreiE 2007 A key role of Pox meso in somatic myogenesis of Drosophila. Development 134 3985 3997

15. JaglaTBellardFLutzYDretzenGBellardM 1998 ladybird determines cell fate decisions during diversification of Drosophila somatic muscles. Development 125 3699 3708

16. CrozatierMVincentA 1999 Requirement for the Drosophila COE transcription factor Collier in formation of an embryonic muscle: transcriptional response to notch signalling. Development 126 1495 1504

17. KnirrSAzpiazuNFraschM 1999 The role of the NK-homeobox gene slouch (S59) in somatic muscle patterning. Development 126 4525 4535

18. Ruiz-GómezMRomaniSHartmannCJackleHBateM 1997 Specific muscle identities are regulated by Kruppel during Drosophila embryogenesis. Development 124 3407 3414

19. BateMRushtonEFraschM 1993 A dual requirement for neurogenic genes in Drosophila myogenesis. Dev Suppl 149 161

20. NoseAMahajanVBGoodmanCS 1992 Connectin: a homophilic cell adhesion molecule expressed on a subset of muscles and the motoneurons that innervate them in Drosophila. Cell 70 553 567

21. Gomez-SkarmetaJLModolellJ 2002 Iroquois genes: genomic organization and function in vertebrate neural development. Curr Opin Genet Dev 12 403 408

22. CavodeassiFModolellJCampuzanoS 2000 The Iroquois homeobox genes function as dorsal selectors in the Drosophila head. Development 127 1921 1929

23. Diez del CorralRArocaPJLGm-SCavodeassiFModolellJ 1999 The Iroquois homeodomain proteins are required to specify body wall identity in Drosophila. Genes Dev 13 1754 1761

24. FeijooCGManzanaresMde la Calle-MustienesEGomez-SkarmetaJLAllendeML 2004 The Irx gene family in zebrafish: genomic structure, evolution and initial characterization of irx5b. Dev Genes Evol 214 277 284

25. CavodeassiFDiez Del CorralRCampuzanoSDominguezM 1999 Compartments and organising boundaries in the Drosophila eye: the role of the homeodomain Iroquois proteins. Development 126 4933 4942

26. GlavicAGomez-SkarmetaJLMayorR 2002 The homeoprotein Xiro1 is required for midbrain-hindbrain boundary formation. Development 129 1609 1621

27. Gomez-SkarmetaJde La Calle-MustienesEModolellJ 2001 The Wnt-activated Xiro1 gene encodes a repressor that is essential for neural development and downregulates Bmp4. Development 128 551 560

28. Gomez-SkarmetaJLDiez del CorralRde la Calle-MustienesEFerre-MarcoDModolellJ 1996 Araucan and caupolican, two members of the novel iroquois complex, encode homeoproteins that control proneural and vein-forming genes. Cell 85 95 105

29. LeynsLGomez-SkarmetaJLDambly-ChaudiereC 1996 iroquois: a prepattern gene that controls the formation of bristles on the thorax of Drosophila. Mech Dev 59 63 72

30. Rodriguez-SeguelEAlarconPGomez-SkarmetaJL 2009 The Xenopus Irx genes are essential for neural patterning and define the border between prethalamus and thalamus through mutual antagonism with the anterior repressors Fezf and Arx. Dev Biol 329 258 268

31. MichelsonAMAbmayrSMBateMAriasAMManiatisT 1990 Expression of a MyoD family member prefigures muscle pattern in Drosophila embryos. Genes Dev 4 2086 2097

32. NoseAIsshikiTTakeichiM 1998 Regional specification of muscle progenitors in Drosophila: the role of the msh homeobox gene. Development 125 215 223

33. DuboisLEnriquezJDaburonVCrozetFLebretonG 2007 Collier transcription in a single Drosophila muscle lineage: the combinatorial control of muscle identity. Development 134 4347 4355

34. KnirrSFraschM 2001 Molecular integration of inductive and mesoderm-intrinsic inputs governs even-skipped enhancer activity in a subset of pericardial and dorsal muscle progenitors. Dev Biol 238 13 26

35. PhilippakisAABusserBWGisselbrechtSSHeFSEstradaB 2006 Expression-guided in silico evaluation of candidate cis regulatory codes for Drosophila muscle founder cells. PLoS Comput Biol 2 e53 doi:10.1371/journal.pcbi.0020053

36. HartmannCLandgrafMBateMJackleH 1997 Kruppel target gene knockout participates in the proper innervation of a specific set of Drosophila larval muscles. Embo J 16 5299 5309

37. JunionGBatailleLJaglaTDa PonteJPTapinR 2007 Genome-wide view of cell fate specification: ladybird acts at multiple levels during diversification of muscle and heart precursors. Genes Dev 21 3163 3180

38. BatailleLDelonIDa PonteJPBrownNHJaglaK 2010 Downstream of identity genes: muscle-type-specific regulation of the fusion process. Dev Cell 19 317 328

39. CallejaMHerranzHEstellaCCasalJLawrenceP 2000 Generation of medial and lateral dorsal body domains by the pannier gene of Drosophila. Development 127 3971 3980

40. LetiziaABarrioRCampuzanoS 2007 Antagonistic and cooperative actions of the EGFR and Dpp pathways on the iroquois genes regulate Drosophila mesothorax specification and patterning. Development 134 1337 1346

41. McNeillHYangCHBrodskyMUngosJSimonMA 1997 mirror encodes a novel PBX-class homeoprotein that functions in the definition of the dorsal-ventral border in the Drosophila eye. Genes Dev 11 1073 1082

42. González-PérezE 2009 Función y regulación de las homeoproteínas del complejo génico Iroquois en los discos imaginales de ala y ojo-antena de Drosophila melanogaster Madrid Autónoma de Madrid 146

43. MullerDJaglaTBodartLMJahrlingNDodtHU 2010 Regulation and functions of the lms homeobox gene during development of embryonic lateral transverse muscles and direct flight muscles in Drosophila. PLoS ONE 5 e14323 doi:10.1371/journal.pone.0014323

44. HerranzH 2001 Estudio de la función del gen pannier en el desarrollo embrionario de Drosophila melanogaster Madrid Autónoma de Madrid 79

45. Ruiz-GómezMCouttsNPriceATaylorMVBateM 2000 Drosophila dumbfounded: a myoblast attractant essential for fusion. Cell 102 189 198

46. KimSJParkTLeeKK 1999 Identification of a novel cis-acting positive element responsible for the cell-specific expression of the NK-1 homeobox gene. Biochem Biophys Res Commun 257 538 544

47. BilioniACraigGHillCMcNeillH 2005 Iroquois transcription factors recognize a unique motif to mediate transcriptional repression in vivo. Proc Natl Acad Sci U S A 102 14671 14676

48. MatsumotoKNishiharaSKamimuraMShiraishiTOtoguroT 2004 The prepattern transcription factor Irx2, a target of the FGF8/MAP kinase cascade, is involved in cerebellum formation. Nat Neurosci 7 605 612

49. LeeTFeigLMontellDJ 1996 Two distinct roles for Ras in a developmentally regulated cell migration. Development 122 409 418

50. DengHBellJBSimmondsAJ 2010 Vestigial is required during late-stage muscle differentiation in Drosophila melanogaster embryos. Mol Biol Cell 21 3304 3316

51. BuffECarmenaAGisselbrechtSJimenezFMichelsonAM 1998 Signalling by the Drosophila epidermal growth factor receptor is required for the specification and diversification of embryonic muscle progenitors. Development 125 2075 2086

52. CavodeassiFModolellJGomez-SkarmetaJL 2001 The Iroquois family of genes: from body building to neural patterning. Development 128 2847 2855

53. BaumgardtMMiguel-AliagaIKarlssonDEkmanHThorS 2007 Specification of neuronal identities by feedforward combinatorial coding. PLoS Biol 5 e37 doi:10.1371/journal.pbio.0050037

54. de CelisJFBarrioRKafatosFC 1996 A gene complex acting downstream of dpp in Drosophila wing morphogenesis. Nature 381 421 424

55. RanganayakuluGElliottDAHarveyRPOlsonEN 1998 Divergent roles for NK-2 class homeobox genes in cardiogenesis in flies and mice. Development 125 3037 3048

56. CallejaMMorenoEPelazSMorataG 1996 Visualization of gene expression in living adult Drosophila. Science 274 252 255

57. BrandAHPerrimonN 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118 401 415

58. MartinBSRuiz-GomezMLandgrafMBateM 2001 A distinct set of founders and fusion-competent myoblasts make visceral muscles in the Drosophila embryo. Development 128 3331 3338

59. KosmanDSmallSReinitzJ 1998 Rapid preparation of a panel of polyclonal antibodies to Drosophila segmentation proteins. Dev Genes Evol 208 290 294

60. GoubeaudAKnirrSRenkawitz-PohlRPaululatA 1996 The Drosophila gene alien is expressed in the muscle attachment sites during embryogenesis and encodes a protein highly conserved between plants, Drosophila and vertebrates. Mech Dev 57 59 68

61. MeadowsLAGellDBroadieKGouldAPWhiteRA 1994 The cell adhesion molecule, connectin, and the development of the Drosophila neuromuscular system. J Cell Sci 107 Pt 1 321 328

62. WilliamsJABellJBCarrollSB 1991 Control of Drosophila wing and haltere development by the nuclear vestigial gene product. Genes Dev 5 2481 2495

63. KiehartDPFeghaliR 1986 Cytoplasmic myosin from Drosophila melanogaster. J Cell Biol 103 1517 1525

64. GilchristDANechaevSLeeCGhoshSKCollinsJB 2008 NELF-mediated stalling of Pol II can enhance gene expression by blocking promoter-proximal nucleosome assembly. Genes Dev 22 1921 1933

65. WhartonKAJrCrewsST 1993 CNS midline enhancers of the Drosophila slit and Toll genes. Mech Dev 40 141 154

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2011 Číslo 7
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#