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Characterization of Drosophila Muscle Stem Cell-Like Adult Muscle Precursors

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Part of the book series: Methods in Molecular Biology ((MIMB,volume 1556))

Abstract

Uncovering how muscle stem cells behave in quiescent and activated states is central to understand the basic rules governing normal muscle development and regeneration in pathological conditions. Specification of mesodermal lineages including muscle stemlike adult muscle precursors (AMPs) has been extensively studied in Drosophila providing an attractive framework for investigating muscle stem cell properties. Restricted number of AMP cells, relative ease in following their behavior, and large number of genetic tools available make fruit fly an attractive model system for studying muscle stem cells. In this chapter, we describe the recently developed tools to visualize and target the body wall and imaginal AMPs.

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References

  1. Ruiz Gomez M, Bate M (1997) Segregation of myogenic lineages in Drosophila requires numb. Development 124(23):4857–4866

    Article  CAS  PubMed  Google Scholar 

  2. Figeac N, Daczewska M, Marcelle C, Jagla K (2007) Muscle stem cells and model systems for their investigation. Dev Dyn 236(12):3332–3342. doi:10.1002/dvdy.21345

    Article  PubMed  Google Scholar 

  3. Bate M, Rushton E, Currie DA (1991) Cells with persistent twist expression are the embryonic precursors of adult muscles in Drosophila. Development 113(1):79–89

    Article  CAS  PubMed  Google Scholar 

  4. Liotta D, Han J, Elgar S, Garvey C, Han Z, Taylor MV (2007) The Him gene reveals a balance of inputs controlling muscle differentiation in Drosophila. Curr Biol 17(16):1409–1413. doi:10.1016/j.cub.2007.07.039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Postigo AA, Ward E, Skeath JB, Dean DC (1999) zfh-1, the Drosophila homologue of ZEB, is a transcriptional repressor that regulates somatic myogenesis. Mol Cell Biol 19(10):7255–7263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Figeac N, Jagla T, Aradhya R, Da Ponte JP, Jagla K (2010) Drosophila adult muscle precursors form a network of interconnected cells and are specified by the rhomboid-triggered EGF pathway. Development 137(12):1965–1973. doi:10.1242/dev.049080

    Article  CAS  PubMed  Google Scholar 

  7. Tavi P, Korhonen T, Hanninen SL, Bruton JD, Loof S, Simon A, Westerblad H (2010) Myogenic skeletal muscle satellite cells communicate by tunnelling nanotubes. J Cell Physiol 223(2):376–383. doi:10.1002/jcp.22044

    Article  CAS  PubMed  Google Scholar 

  8. Soler C, Daczewska M, Da Ponte JP, Dastugue B, Jagla K (2004) Coordinated development of muscles and tendons of the Drosophila leg. Development 131(24):6041–6051. doi:10.1242/dev.01527

    Article  CAS  PubMed  Google Scholar 

  9. Fernandes J, Bate M, Vijayraghavan K (1991) Development of the indirect flight muscles of Drosophila. Development 113(1):67–77

    Article  CAS  PubMed  Google Scholar 

  10. Fernandes JJ, Keshishian H (1996) Patterning the dorsal longitudinal flight muscles (DLM) of Drosophila: insights from the ablation of larval scaffolds. Development 122(12):3755–3763

    Article  CAS  PubMed  Google Scholar 

  11. Ranganayakulu G, Zhao B, Dokidis A, Molkentin JD, Olson EN, Schulz RA (1995) A series of mutations in the D-MEF2 transcription factor reveal multiple functions in larval and adult myogenesis in Drosophila. Dev Biol 171(1):169–181. doi:10.1006/dbio.1995.1269

    Article  CAS  PubMed  Google Scholar 

  12. Soler C, Taylor MV (2009) The Him gene inhibits the development of Drosophila flight muscles during metamorphosis. Mech Dev 126(7):595–603. doi:10.1016/j.mod.2009.03.003

    Article  CAS  PubMed  Google Scholar 

  13. Sudarsan V, Anant S, Guptan P, VijayRaghavan K, Skaer H (2001) Myoblast diversification and ectodermal signaling in Drosophila. Dev Cell 1(6):829–839

    Article  CAS  PubMed  Google Scholar 

  14. Maqbool T, Soler C, Jagla T, Daczewska M, Lodha N, Palliyil S, VijayRaghavan K, Jagla K (2006) Shaping leg muscles in Drosophila: role of ladybird, a conserved regulator of appendicular myogenesis. PLoS One 1:e122. doi:10.1371/journal.pone.0000122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Bernard F, Dutriaux A, Silber J, Lalouette A (2006) Notch pathway repression by vestigial is required to promote indirect flight muscle differentiation in Drosophila melanogaster. Dev Biol 295(1):164–177. doi:10.1016/j.ydbio.2006.03.022

    Article  CAS  PubMed  Google Scholar 

  16. Deng H, Hughes SC, Bell JB, Simmonds AJ (2009) Alternative requirements for Vestigial, Scalloped, and Dmef2 during muscle differentiation in Drosophila melanogaster. Mol Biol Cell 20(1):256–269. doi:10.1091/mbc.E08-03-0288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118(2):401–415

    Article  CAS  PubMed  Google Scholar 

  18. Anant S, Roy S, VijayRaghavan K (1998) Twist and Notch negatively regulate adult muscle differentiation in Drosophila. Development 125(8):1361–1369

    Article  CAS  PubMed  Google Scholar 

  19. Fyrberg C, Becker J, Barthmaier P, Mahaffey J, Fyrberg E (1997) A Drosophila muscle-specific gene related to the mouse quaking locus. Gene 197(1-2):315–323

    Article  CAS  PubMed  Google Scholar 

  20. Ranganayakulu G, Elliott DA, Harvey RP, Olson EN (1998) Divergent roles for NK-2 class homeobox genes in cardiogenesis in flies and mice. Development 125(16):3037–3048

    Article  CAS  PubMed  Google Scholar 

  21. Sellin J, Drechsler M, Nguyen HT, Paululat A (2009) Antagonistic function of Lmd and Zfh1 fine tunes cell fate decisions in the Twi and Tin positive mesoderm of Drosophila melanogaster. Dev Biol 326(2):444–455. doi:10.1016/j.ydbio.2008.10.041

    Article  CAS  PubMed  Google Scholar 

  22. Kim J, Sebring A, Esch JJ, Kraus ME, Vorwerk K, Magee J, Carroll SB (1996) Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene. Nature 382(6587):133–138. doi:10.1038/382133a0

    Article  CAS  PubMed  Google Scholar 

  23. Knirr S, Azpiazu N, Frasch M (1999) The role of the NK-homeobox gene slouch (S59) in somatic muscle patterning. Development 126(20):4525–4535

    Article  CAS  PubMed  Google Scholar 

  24. Duan H, Zhang C, Chen J, Sink H, Frei E, Noll M (2007) A key role of Pox meso in somatic myogenesis of Drosophila. Development 134(22):3985–3997. doi:10.1242/dev.008821

    Article  CAS  PubMed  Google Scholar 

  25. Cripps RM, Olson EN (1998) Twist is required for muscle template splitting during adult Drosophila myogenesis. Dev Biol 203(1):106–115. doi:10.1006/dbio.1998.9040

    Article  CAS  PubMed  Google Scholar 

  26. Soler C, Han J, Taylor MV (2012) The conserved transcription factor Mef2 has multiple roles in adult Drosophila musculature formation. Development 139(7):1270–1275. doi:10.1242/dev.077875

    Article  CAS  PubMed  Google Scholar 

  27. Buckingham M, Bajard L, Chang T, Daubas P, Hadchouel J, Meilhac S, Montarras D, Rocancourt D, Relaix F (2003) The formation of skeletal muscle: from somite to limb. J Anat 202(1):59–68

    Article  PubMed  PubMed Central  Google Scholar 

  28. Lilly B, Zhao B, Ranganayakulu G, Paterson BM, Schulz RA, Olson EN (1995) Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science 267(5198):688–693

    Article  CAS  PubMed  Google Scholar 

  29. Jagla K, Jagla T, Heitzler P, Dretzen G, Bellard F, Bellard M (1997) ladybird, a tandem of homeobox genes that maintain late wingless expression in terminal and dorsal epidermis of the Drosophila embryo. Development 124(1):91–100

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We wish to thank all members of the Jagla lab for stimulating discussions. We are grateful to former Jagla lab members, N. Figeac, for initial characterization of AMP markers and to R. Aradhya for generating M6-GAL4 and M6-gapGFP lines. This work is supported by the ANR grant ID-CELL-SPE to KJ, the “Equipe” FRM grant to K.J., and the AFM-Téléthon grant to G.L.

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Correspondence to Krzysztof Jagla .

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Lavergne, G., Soler, C., Zmojdzian, M., Jagla, K. (2017). Characterization of Drosophila Muscle Stem Cell-Like Adult Muscle Precursors. In: Perdiguero, E., Cornelison, D. (eds) Muscle Stem Cells. Methods in Molecular Biology, vol 1556. Humana, New York, NY. https://doi.org/10.1007/978-1-4939-6771-1_5

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  • DOI: https://doi.org/10.1007/978-1-4939-6771-1_5

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  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-4939-6769-8

  • Online ISBN: 978-1-4939-6771-1

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