Isolation, Culture, and Analysis of Zebrafish Myofibers and Associated Muscle Stem Cells to Explore Adult Skeletal Myogenesis.


Journal

Methods in molecular biology (Clifton, N.J.)
ISSN: 1940-6029
Titre abrégé: Methods Mol Biol
Pays: United States
ID NLM: 9214969

Informations de publication

Date de publication:
2023
Historique:
medline: 3 4 2023
entrez: 30 3 2023
pubmed: 31 3 2023
Statut: ppublish

Résumé

Adult skeletal musculature experiences continuous physical stress, and hence requires maintenance and repair to ensure its continued efficient functioning. The population of resident muscle stem cells (MuSCs), termed satellite cells, resides beneath the basal lamina of adult myofibers, contributing to both muscle hypertrophy and regeneration. Upon exposure to activating stimuli, MuSCs proliferate to generate new myoblasts that differentiate and fuse to regenerate or grow myofibers. Moreover, many teleost fish undergo continuous growth throughout life, requiring continual nuclear recruitment from MuSCs to initiate and grow new fibers, a process that contrasts with the determinate growth observed in most amniotes. In this chapter, we describe a method for the isolation, culture, and immunolabeling of adult zebrafish myofibers that permits examination of both myofiber characteristics ex vivo and the MuSC myogenic program in vitro. Morphometric analysis of isolated myofibers is suitable to assess differences among slow and fast muscles or to investigate cellular features such as sarcomeres and neuromuscular junctions. Immunostaining for Pax7, a canonical stemness marker, identifies MuSCs on isolated myofibers for study. Furthermore, the plating of viable myofibers allows MuSC activation and expansion and downstream analysis of their proliferative and differentiative dynamics, thus providing a suitable, parallel alternative to amniote models for the study of vertebrate myogenesis.

Identifiants

pubmed: 36995585
doi: 10.1007/978-1-0716-3036-5_3
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

21-43

Subventions

Organisme : Medical Research Council
ID : G1001029
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N021231/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/P023215/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/S002472/1
Pays : United Kingdom

Informations de copyright

© 2023. Springer Science+Business Media, LLC, part of Springer Nature.

Références

Schiaffino S, Reggiani C (2011) Fiber types in mammalian skeletal muscles. Physiol Rev 91:1447–1531
pubmed: 22013216 doi: 10.1152/physrev.00031.2010
Talbot J, Maves L (2016) Skeletal muscle fiber type: using insights from muscle developmental biology to dissect targets for susceptibility and resistance to muscle disease. Wiley Interdiscip Rev Dev Biol 5:518–534
pubmed: 27199166 pmcid: 5180455 doi: 10.1002/wdev.230
Blagden CS, Currie PD, Ingham PW et al (1997) Notochord induction of zebrafish slow muscle mediated by Sonic hedgehog. Genes Dev 11:2163–2175
pubmed: 9303533 pmcid: 275397 doi: 10.1101/gad.11.17.2163
Hromowyk KJ, Talbot JC, Martin BL et al (2020) Cell fusion is differentially regulated in zebrafish post-embryonic slow and fast muscle. Dev Biol 462:85–100
pubmed: 32165147 pmcid: 7225055 doi: 10.1016/j.ydbio.2020.03.005
van Raamsdonk W, Pool CW, te Kronnie G (1978) Differentiation of muscle fibre types in the teleost Brachydanio rerio. Anat Embryol (Berl) 153:137–155
pubmed: 677468 doi: 10.1007/BF00343370
Pipalia TG, Koth J, Roy SD et al (2016) Cellular dynamics of regeneration reveals role of two distinct Pax7 stem cell populations in larval zebrafish muscle repair. Dis Model Mech 9:671–684
pubmed: 27149989 pmcid: 4920144
Rowlerson A, Scapolo PA, Mascarello F et al (1985) Comparative study of myosins present in the lateral muscle of some fish: species variations in myosin isoforms and their distribution in red, pink and white muscle. J Muscle Res Cell Motil 6:601–640
pubmed: 3905858 doi: 10.1007/BF00711917
Johnston IA, Bower NI, Macqueen DJ (2011) Growth and the regulation of myotomal muscle mass in teleost fish. J Exp Biol 214:1617–1628
pubmed: 21525308 doi: 10.1242/jeb.038620
Katz B (1961) The termination of the afferent nerve fibre in the muscle spindle of the frog. Philos Trans R Soc Lond Ser B Biol Sci 243:221–240
Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495
pubmed: 13768451 pmcid: 2225012 doi: 10.1083/jcb.9.2.493
Purohit G, Dhawan J (2019) Adult muscle stem cells: exploring the links between systemic and cellular metabolism. Front Cell Dev Biol 7:312
pubmed: 31921837 pmcid: 6915107 doi: 10.3389/fcell.2019.00312
Relaix F, Zammit PS (2012) Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development 139:2845–2856
pubmed: 22833472 doi: 10.1242/dev.069088
Collins CA, Olsen I, Zammit PS et al (2005) Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122:289–301
pubmed: 16051152 doi: 10.1016/j.cell.2005.05.010
Halevy O, Piestun Y, Allouh MZ et al (2004) Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev Dyn 231:489–502
pubmed: 15390217 doi: 10.1002/dvdy.20151
Zammit PS, Golding JP, Nagata Y et al (2004) Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 166:347–357
pubmed: 15277541 pmcid: 2172269 doi: 10.1083/jcb.200312007
Buckingham M, Relaix F (2015) PAX3 and PAX7 as upstream regulators of myogenesis. Semin Cell Dev Biol 44:115–125
pubmed: 26424495 doi: 10.1016/j.semcdb.2015.09.017
Ganassi M, Badodi S, Ortuste Quiroga HP et al (2018) Myogenin promotes myocyte fusion to balance fibre number and size. Nat Commun 9:4232
pubmed: 30315160 pmcid: 6185967 doi: 10.1038/s41467-018-06583-6
Hammond CL, Hinits Y, Osborn DP et al (2007) Signals and myogenic regulatory factors restrict pax3 and pax7 expression to dermomyotome-like tissue in zebrafish. Dev Biol 302:504–521
pubmed: 17094960 doi: 10.1016/j.ydbio.2006.10.009
Hinits Y, Osborn DP, Hughes SM (2009) Differential requirements for myogenic regulatory factors distinguish medial and lateral somitic, cranial and fin muscle fibre populations. Development 136:403–414
pubmed: 19141670 pmcid: 2687589 doi: 10.1242/dev.028019
Hinits Y, Williams VC, Sweetman D et al (2011) Defective cranial skeletal development, larval lethality and haploinsufficiency in Myod mutant zebrafish. Dev Biol 358:102–112
pubmed: 21798255 pmcid: 3360969 doi: 10.1016/j.ydbio.2011.07.015
Osborn DPS, Li K, Cutty SJ et al (2020) Fgf-driven Tbx protein activities directly induce myf5 and myod to initiate zebrafish myogenesis. Development 147:dev184689
pubmed: 32345657 pmcid: 7197714 doi: 10.1242/dev.184689
Alexander MS, Kawahara G, Kho AT et al (2011) Isolation and transcriptome analysis of adult zebrafish cells enriched for skeletal muscle progenitors. Muscle Nerve 43:741–750
pubmed: 21337346 pmcid: 3075361 doi: 10.1002/mus.21972
Froehlich JM, Seiliez I, Gabillard JC et al (2014) Preparation of primary myogenic precursor cell/myoblast cultures from basal vertebrate lineages. J Vis Exp 86:51354
Moyle LA, Zammit PS (2014) Isolation, culture and immunostaining of skeletal muscle fibres to study myogenic progression in satellite cells. Methods Mol Biol 1210:63–78
pubmed: 25173161 doi: 10.1007/978-1-4939-1435-7_6
Rosenblatt JD, Lunt AI, Parry DJ et al (1995) Culturing satellite cells from living single muscle fiber explants. In Vitro Cell Dev Biol Anim 31:773–779
pubmed: 8564066 doi: 10.1007/BF02634119
Bischoff R (1975) Regeneration of single skeletal muscle fibers in vitro. Anat Rec 182:215–235
pubmed: 168794 doi: 10.1002/ar.1091820207
Cardasis CA, Cooper GW (1975a) An analysis of nuclear numbers in individual muscle fibers during differentiation and growth: a satellite cell-muscle fiber growth unit. J Exp Zool 191:347–358
pubmed: 1127400 doi: 10.1002/jez.1401910305
Cardasis CA, Cooper GW (1975b) A method for the chemical isolation of individual muscle fibers and its application to a study of the effect of denervation on the number of nuclei per muscle fiber. J Exp Zool 191:333–346
pubmed: 1092803 doi: 10.1002/jez.1401910304
Baruffaldi F, Montarras D, Basile V et al (2017) Dynamic phosphorylation of the myocyte enhancer factor 2Calpha1 splice variant promotes skeletal muscle regeneration and hypertrophy. Stem Cells 35:725–738
pubmed: 27612437 doi: 10.1002/stem.2495
Beauchamp JR, Heslop L, Yu DS et al (2000) Expression of CD34 and myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151:1221–1234
pubmed: 11121437 pmcid: 2190588 doi: 10.1083/jcb.151.6.1221
Bischoff R (1986) Proliferation of muscle satellite cells on intact myofibers in culture. Dev Biol 115:129–139
pubmed: 3516758 doi: 10.1016/0012-1606(86)90234-4
Brack AS, Bildsoe H, Hughes SM (2005) Evidence that satellite cell decrement contributes to preferential decline in nuclear number from large fibres during murine age-related muscle atrophy. J Cell Sci 118:4813–4821
pubmed: 16219688 doi: 10.1242/jcs.02602
Kuang S, Kuroda K, Le Grand F et al (2007) Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129:999–1010
pubmed: 17540178 pmcid: 2718740 doi: 10.1016/j.cell.2007.03.044
Lukjanenko L, Karaz S, Stuelsatz P et al (2019) Aging disrupts muscle stem cell function by impairing matricellular WISP1 secretion from fibro-adipogenic progenitors. Cell Stem Cell 24:433–446 e437
pubmed: 30686765 pmcid: 6408230 doi: 10.1016/j.stem.2018.12.014
Yablonka-Reuveni Z, Rivera AJ (1994) Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev Biol 164:588–603
pubmed: 7913900 pmcid: 4128087 doi: 10.1006/dbio.1994.1226
Zammit PS, Relaix F, Nagata Y et al (2006) Pax7 and myogenic progression in skeletal muscle satellite cells. J Cell Sci 119:1824–1832
pubmed: 16608873 doi: 10.1242/jcs.02908
Davies MLF, Johnston IA, van de Wal JW (1995) Muscle fibers in rostral and caudal myotomes of the Atlantic Cod (Gadus morhua L.) have different mechanical properties. Physiol Zool 68:673–697
doi: 10.1086/physzool.68.4.30166351
Johnston I, Altringham J (1988) Muscle contraction in polar fishes: experiments with demembranated muscle fibres. Comp Biochem Physiol 90B:547–555
Johnston IA, Abercromby M, Vieira VL et al (2004) Rapid evolution of muscle fibre number in post-glacial populations of Arctic charr Salvelinus alpinus. J Exp Biol 207:4343–4360
pubmed: 15557021 doi: 10.1242/jeb.01292
Anderson JE, Wozniak AC et al (2012) Single muscle-fiber isolation and culture for cellular, molecular, pharmacological, and evolutionary studies. Methods Mol Biol 798:85–102
pubmed: 22130833 doi: 10.1007/978-1-61779-343-1_6
Zhang H, Anderson JE (2014) Satellite cell activation and populations on single muscle-fiber cultures from adult zebrafish (Danio rerio). J Exp Biol 217:1910–1917
pubmed: 24577448
Ganassi M, Badodi S, Wanders K et al (2020) Myogenin is an essential regulator of adult myofibre growth and muscle stem cell homeostasis. elife 9:e60445
pubmed: 33001028 pmcid: 7599067 doi: 10.7554/eLife.60445
Ganassi M, Muntoni F, Zammit PS (2022) Defining and identifying satellite cellopathies within muscular dystrophies and myopathies. Exp Cell Res 411:112906. https://doi.org/10.1016/j.yexcr.2021.112906
Ganassi M, Zammit PS (2022) Involvement of muscle satellite cell dysfunction in neuromuscular disorders: Expanding the portfolio of satellite cell-opathies. Eur J Transl Myol 32. https://doi.org/10.4081/ejtm.2022.10064
Ganassi M, Zammit PS, Hughes SM (2021) Isolation of myofibres and culture of muscle stem cells from adult zebrafish. Bio Protoc 11:e4149. https://doi.org/10.21769/BioProtoc.4149
Elworthy S, Hargrave M, Knight R et al (2008) Expression of multiple slow myosin heavy chain genes reveals a diversity of zebrafish slow twitch muscle fibres with differing requirements for Hedgehog and Prdm1 activity. Development 135:2115–2126
pubmed: 18480160 doi: 10.1242/dev.015719
Berberoglu MA, Gallagher TL, Morrow ZT et al (2017) Satellite-like cells contribute to pax7-dependent skeletal muscle repair in adult zebrafish. Dev Biol 424:162–180
pubmed: 28279710 pmcid: 5437870 doi: 10.1016/j.ydbio.2017.03.004
Chen Y, Lin G, Slack JM (2006) Control of muscle regeneration in the Xenopus tadpole tail by Pax7. Development 133:2303–2313
pubmed: 16687446 doi: 10.1242/dev.02397
Hollway GE, Bryson-Richardson RJ, Berger S et al (2007) Whole-somite rotation generates muscle progenitor cell compartments in the developing zebrafish embryo. Dev Cell 12:207–219
pubmed: 17276339 doi: 10.1016/j.devcel.2007.01.001
Kawakami A, Kimura-Kawakami M, Nomura T et al (1997) Distributions of PAX6 and PAX7 proteins suggest their involvement in both early and late phases of chick brain development. Mech Dev 66:119–130
pubmed: 9376315 doi: 10.1016/S0925-4773(97)00097-X
Olguin HC, Olwin BB (2004) Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev Biol 275:375–388
pubmed: 15501225 pmcid: 3322464 doi: 10.1016/j.ydbio.2004.08.015
Seale P, Sabourin LA, Girgis-Gabardo A et al (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102:777–786
pubmed: 11030621 doi: 10.1016/S0092-8674(00)00066-0
Seger C, Hargrave M, Wang X et al (2011) Analysis of Pax7 expressing myogenic cells in zebrafish muscle development, injury, and models of disease. Dev Dyn 240:2440–2451
pubmed: 21954137 doi: 10.1002/dvdy.22745
Mahalwar P, Walderich B, Singh AP et al (2014) Local reorganization of xanthophores fine-tunes and colors the striped pattern of zebrafish. Science 345:1362–1364
pubmed: 25214630 doi: 10.1126/science.1254837
Harper C, Lawrence C (2011) The laboratory zebrafish. CRC Press, Boca Raton
Westerfield M (2000) The zebrafish book – a guide for the laboratory use of zebrafish (Danio rerio). University of Oregon Press
Nord H, Burguiere AC, Muck J et al (2014) Differential regulation of myosin heavy chains defines new muscle domains in zebrafish. Mol Biol Cell 25:1384–1395
pubmed: 24523292 pmcid: 3983002 doi: 10.1091/mbc.e13-08-0486
Davis GK, Jaramillo CA, Patel NH (2001) Pax group III genes and the evolution of insect pair-rule patterning. Development 128:3445–3458
pubmed: 11566851 doi: 10.1242/dev.128.18.3445

Auteurs

Massimo Ganassi (M)

Randall Centre for Cell and Molecular Biophysics, King's College London, London, UK. massimo.ganassi@kcl.ac.uk.

Peter S Zammit (PS)

Randall Centre for Cell and Molecular Biophysics, King's College London, London, UK.

Simon M Hughes (SM)

Randall Centre for Cell and Molecular Biophysics, King's College London, London, UK. simon.hughes@kcl.ac.uk.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH