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
Ruiz Gomez M, Bate M (1997) Segregation of myogenic lineages in Drosophila requires numb. Development 124(23):4857–4866
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
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
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
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
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
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
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
Fernandes J, Bate M, Vijayraghavan K (1991) Development of the indirect flight muscles of Drosophila. Development 113(1):67–77
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
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
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
Sudarsan V, Anant S, Guptan P, VijayRaghavan K, Skaer H (2001) Myoblast diversification and ectodermal signaling in Drosophila. Dev Cell 1(6):829–839
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
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
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
Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118(2):401–415
Anant S, Roy S, VijayRaghavan K (1998) Twist and Notch negatively regulate adult muscle differentiation in Drosophila. Development 125(8):1361–1369
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
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
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
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
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
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
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
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
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
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
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
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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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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