Pax7 reporter mouse models: a pocket guide for satellite cell research

Submitted: 11 December 2023
Accepted: 13 December 2023
Published: 18 December 2023
Abstract Views: 1031
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Since their discovery, satellite cells have showcased their need as primary contributors to skeletal muscle maintenance and repair. Satellite cells lay dormant, but when needed, activate, differentiate, fuse to fibres and self-renew, that has bestowed satellite cells with the title of muscle stem cells. The satellite cell specific transcription factor Pax7 has enabled researchers to develop animal models against the Pax7 locus in order to isolate and characterise satellite cell-mediated events. This review focuses specifically on describing Pax7 reporter mouse models. Here we describe how each model was generated and the key findings obtained. The strengths and limitations of each model are also discussed. The aim is to provide new and current satellite cell enthusiasts with a basic understanding of the available Pax7 reporter mice and hopefully guide selection of the most appropriate Pax7 model to answer a specific research question.

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Janssen I, Heymsfield SB, Wang ZM, Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J Appl Physiol (1985). 2000;89(1):81-8. PubMed PMID: 10904038. DOI: https://doi.org/10.1152/jappl.2000.89.1.81
Zammit PS, Relaix F, Nagata Y, Ruiz AP, Collins CA, Partridge TA, et al. Pax7 and myogenic progression in skeletal muscle satellite cells. Journal of cell science. 2006;119(Pt 9):1824-32. Epub 2006/04/13. PubMed PMID: 16608873. DOI: https://doi.org/10.1242/jcs.02908
Le Grand F, Rudnicki MA. Skeletal muscle satellite cells and adult myogenesis. Curr Opin Cell Biol. 2007;19(6):628-33. Epub 20071108. PubMed PMID: 17996437; PubMed Central PMCID: PMC2215059. DOI: https://doi.org/10.1016/j.ceb.2007.09.012
Tajbakhsh S. Skeletal muscle stem cells in developmental versus regenerative myogenesis. J Intern Med. 2009;266(4):372-89. PubMed PMID: 19765181. DOI: https://doi.org/10.1111/j.1365-2796.2009.02158.x
Mauro A. Satellite cell of skeletal muscle fibers. The Journal of biophysical and biochemical cytology. 1961;9:493-5. Epub 1961/02/01. PubMed PMID: 13768451; PubMed Central PMCID: Pmc2225012. DOI: https://doi.org/10.1083/jcb.9.2.493
Zammit PS, Partridge TA, Yablonka-Reuveni Z. The skeletal muscle satellite cell: the stem cell that came in from the cold. J Histochem Cytochem. 2006;54:1177-91. DOI: https://doi.org/10.1369/jhc.6R6995.2006
Collins CA, Olsen I, Zammit PS, Heslop L, Petrie A, Partridge TA, et al. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell. 2005;122(2):289-301. PubMed PMID: 16051152. DOI: https://doi.org/10.1016/j.cell.2005.05.010
Zammit PS. All muscle satellite cells are equal, but are some more equal than others? Journal of cell science. 2008;121(Pt 18):2975-82. PubMed PMID: 18768931. DOI: https://doi.org/10.1242/jcs.019661
Zammit PS. Function of the myogenic regulatory factors Myf5, MyoD, Myogenin and MRF4 in skeletal muscle, satellite cells and regenerative myogenesis. Seminars in cell & developmental biology. 2017;72:19-32. Epub 20171115. PubMed PMID: 29127046. DOI: https://doi.org/10.1016/j.semcdb.2017.11.011
Relaix F, Bencze M, Borok MJ, Der Vartanian A, Gattazzo F, Mademtzoglou D, et al. Perspectives on skeletal muscle stem cells. Nature Communications. 2021;12(1):692. DOI: https://doi.org/10.1038/s41467-020-20760-6
Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA. Pax7 is required for the specification of myogenic satellite cells. Cell. 2000;102(6):777-86. PubMed PMID: 11030621. DOI: https://doi.org/10.1016/S0092-8674(00)00066-0
Gnocchi VF, White RB, Ono Y, Ellis JA, Zammit PS. Further characterisation of the molecular signature of quiescent and activated mouse muscle satellite cells. PLoS One. 2009;4(4):e5205. Epub 20090416. PubMed PMID: 19370151; PubMed Central PMCID: PMC2666265. DOI: https://doi.org/10.1371/journal.pone.0005205
Ortuste Quiroga HP, Goto K, Zammit PS. Isolation, Cryosection and Immunostaining of Skeletal Muscle. Methods in molecular biology (Clifton, NJ). 2016;1460:85-100. PubMed PMID: 27492168. DOI: https://doi.org/10.1007/978-1-4939-3810-0_8
Kuang S, Rudnicki MA. The emerging biology of satellite cells and their therapeutic potential. Trends Mol Med. 2008;14(2):82-91. Epub 20080122. PubMed PMID: 18218339. DOI: https://doi.org/10.1016/j.molmed.2007.12.004
Lepper C, Conway SJ, Fan CM. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature. 2009;460(7255):627-31. PubMed PMID: 19554048; PubMed Central PMCID: PMC2767162. DOI: https://doi.org/10.1038/nature08209
Mitchell KJ, Pannérec A, Cadot B, Parlakian A, Besson V, Gomes ER, et al. Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat Cell Biol. 2010;12(3):257-66. Epub 20100131. PubMed PMID: 20118923. DOI: https://doi.org/10.1038/ncb2025
Murphy MM, Lawson JA, Mathew SJ, Hutcheson DA, Kardon G. Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development (Cambridge, England). 2011;138(17):3625-37. PubMed PMID: 21828091; PubMed Central PMCID: PMC3152921. DOI: https://doi.org/10.1242/dev.064162
Relaix F, Zammit PS. Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development (Cambridge, England). 2012;139(16):2845-56. Epub 2012/07/27. PubMed PMID: 22833472. DOI: https://doi.org/10.1242/dev.069088
van Putten M, Lloyd EM, de Greef JC, Raz V, Willmann R, Grounds MD. Mouse models for muscular dystrophies: an overview. Dis Model Mech. 2020;13(2). Epub 20200221. PubMed PMID: 32224495; PubMed Central PMCID: PMC7044454. DOI: https://doi.org/10.1242/dmm.043562
Allamand V, Campbell KP. Animal models for muscular dystrophy: valuable tools for the development of therapies. Hum Mol Genet. 2000;9(16):2459-67. PubMed PMID: 11005802. DOI: https://doi.org/10.1093/hmg/9.16.2459
Rocheteau P, Gayraud-Morel B, Siegl-Cachedenier I, Blasco MA, Tajbakhsh S. A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division. Cell. 2012;148(1-2):112-25. PubMed PMID: 22265406. DOI: https://doi.org/10.1016/j.cell.2011.11.049
Biressi S, Molinaro M, Cossu G. Cellular heterogeneity during vertebrate skeletal muscle development. Developmental Biology. 2007;308(2):281-93. DOI: https://doi.org/10.1016/j.ydbio.2007.06.006
Rodriguez-Outeiriño L, Hernandez-Torres F, Ramírez-de Acuña F, Matías-Valiente L, Sanchez-Fernandez C, Franco D, et al. Muscle Satellite Cell Heterogeneity: Does Embryonic Origin Matter? Front Cell Dev Biol. 2021;9:750534. Epub 20211015. PubMed PMID: 34722534; PubMed Central PMCID: PMC8554119. DOI: https://doi.org/10.3389/fcell.2021.750534
Sambasivan R, Gayraud-Morel B, Dumas G, Cimper C, Paisant S, Kelly RG, et al. Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates. Dev Cell. 2009;16(6):810-21. PubMed PMID: 19531352. DOI: https://doi.org/10.1016/j.devcel.2009.05.008
Bosnakovski D, Xu Z, Li W, Thet S, Cleaver O, Perlingeiro RC, et al. Prospective isolation of skeletal muscle stem cells with a Pax7 reporter. Stem Cells. 2008;26(12):3194-204. Epub 20080918. PubMed PMID: 18802040; PubMed Central PMCID: PMC4372243. DOI: https://doi.org/10.1634/stemcells.2007-1017
Beauchamp JR, Heslop L, Yu DS, Tajbakhsh S, Kelly RG, Wernig A, et al. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol. 2000;151(6):1221-34. PubMed PMID: 11121437; PubMed Central PMCID: PMC2190588. DOI: https://doi.org/10.1083/jcb.151.6.1221
Kuang S, Kuroda K, Le Grand F, Rudnicki MA. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell. 2007;129(5):999-1010. PubMed PMID: 17540178; PubMed Central PMCID: PMC2718740. DOI: https://doi.org/10.1016/j.cell.2007.03.044
Incitti T, Magli A, Darabi R, Yuan C, Lin K, Arpke RW, et al. Pluripotent stem cell-derived myogenic progenitors remodel their molecular signature upon in vivo engraftment. Proc Natl Acad Sci U S A. 2019;116(10):4346-51. Epub 20190213. PubMed PMID: 30760602; PubMed Central PMCID: PMC6410870. DOI: https://doi.org/10.1073/pnas.1808303116
Machado L, Esteves de Lima J, Fabre O, Proux C, Legendre R, Szegedi A, et al. In Situ Fixation Redefines Quiescence and Early Activation of Skeletal Muscle Stem Cells. Cell Rep. 2017;21(7):1982-93. PubMed PMID: 29141227. DOI: https://doi.org/10.1016/j.celrep.2017.10.080
Tichy ED, Sidibe DK, Greer CD, Oyster NM, Rompolas P, Rosenthal NA, et al. A robust Pax7EGFP mouse that enables the visualization of dynamic behaviors of muscle stem cells. Skeletal Muscle. 2018;8(1):27. DOI: https://doi.org/10.1186/s13395-018-0169-7
Maesner CC, Almada AE, Wagers AJ. Established cell surface markers efficiently isolate highly overlapping populations of skeletal muscle satellite cells by fluorescence-activated cell sorting. Skelet Muscle. 2016;6:35. Epub 20161108. PubMed PMID: 27826411; PubMed Central PMCID: PMC5100091. DOI: https://doi.org/10.1186/s13395-016-0106-6
Ganassi M, Badodi S, Ortuste Quiroga HP, Zammit PS, Hinits Y, Hughes SM. Myogenin promotes myocyte fusion to balance fibre number and size. Nature Communications. 2018;9(1):4232. DOI: https://doi.org/10.1038/s41467-018-06583-6
Ganassi M, Zammit PS, Hughes SM. Isolation, Culture, and Analysis of Zebrafish Myofibers and Associated Muscle Stem Cells to Explore Adult Skeletal Myogenesis. Methods in molecular biology (Clifton, NJ). 2023;2640:21-43. PubMed PMID: 36995585. DOI: https://doi.org/10.1007/978-1-0716-3036-5_3
Kitajima Y, Ono Y. Visualization of PAX7 protein dynamics in muscle satellite cells in a YFP knock-in-mouse line. Skeletal Muscle. 2018;8(1):26. DOI: https://doi.org/10.1186/s13395-018-0174-x
Mademtzoglou D, Geara P, Mourikis P, Relaix F. Pax7 haploinsufficiency impairs muscle stem cell function in Cre-recombinase mice and underscores the importance of appropriate controls. Stem Cell Res Ther. 2023;14(1):294. Epub 20231013. PubMed PMID: 37833800; PubMed Central PMCID: PMC10576335. DOI: https://doi.org/10.1186/s13287-023-03506-1
Bouabe H, Okkenhaug K. Gene targeting in mice: a review. Methods in molecular biology (Clifton, NJ). 2013;1064:315-36. PubMed PMID: 23996268; PubMed Central PMCID: PMC4524968. DOI: https://doi.org/10.1007/978-1-62703-601-6_23
McLellan MA, Rosenthal NA, Pinto AR. Cre-loxP-Mediated Recombination: General Principles and Experimental Considerations. Curr Protoc Mouse Biol. 2017;7(1):1-12. Epub 20170302. PubMed PMID: 28252198. DOI: https://doi.org/10.1002/cpmo.22
Keller C, Hansen MS, Coffin CM, Capecchi MR. Pax3:Fkhr interferes with embryonic Pax3 and Pax7 function: implications for alveolar rhabdomyosarcoma cell of origin. Genes Dev. 2004;18(21):2608-13. PubMed PMID: 15520281; PubMed Central PMCID: PMC525541. DOI: https://doi.org/10.1101/gad.1243904
Keller C, Arenkiel BR, Coffin CM, El-Bardeesy N, DePinho RA, Capecchi MR. Alveolar rhabdomyosarcomas in conditional Pax3:Fkhr mice: cooperativity of Ink4a/ARF and Trp53 loss of function. Genes Dev. 2004;18(21):2614-26. Epub 20041015. PubMed PMID: 15489287; PubMed Central PMCID: PMC525542. DOI: https://doi.org/10.1101/gad.1244004
Lepper C, Fan CM. Inducible lineage tracing of Pax7-descendant cells reveals embryonic origin of adult satellite cells. Genesis. 2010;48(7):424-36. PubMed PMID: 20641127; PubMed Central PMCID: PMC3113517. DOI: https://doi.org/10.1002/dvg.20630
Atit R, Sgaier SK, Mohamed OA, Taketo MM, Dufort D, Joyner AL, et al. Beta-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse. Dev Biol. 2006;296(1):164-76. Epub 20060421. PubMed PMID: 16730693. DOI: https://doi.org/10.1016/j.ydbio.2006.04.449
Marti M, Montserrat N, Pardo C, Mulero L, Miquel-Serra L, Rodrigues AM, et al. M-cadherin-mediated intercellular interactions activate satellite cell division. Journal of cell science. 2013;126(Pt 22):5116-31. Epub 20130917. PubMed PMID: 24046443. DOI: https://doi.org/10.1242/jcs.123562
Blum Jordan M, Añó L, Li Z, Van Mater D, Bennett Brian D, Sachdeva M, et al. Distinct and Overlapping Sarcoma Subtypes Initiated from Muscle Stem and Progenitor Cells. Cell Reports. 2013;5(4):933-40. DOI: https://doi.org/10.1016/j.celrep.2013.10.020
Nakamura E, Nguyen MT, Mackem S. Kinetics of tamoxifen-regulated Cre activity in mice using a cartilage-specific CreER(T) to assay temporal activity windows along the proximodistal limb skeleton. Dev Dyn. 2006;235(9):2603-12. PubMed PMID: 16894608. DOI: https://doi.org/10.1002/dvdy.20892
Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nature Genetics. 1999;21(1):70-1. DOI: https://doi.org/10.1038/5007
Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol. 2001;1:4. Epub 20010327. PubMed PMID: 11299042; PubMed Central PMCID: PMC31338. DOI: https://doi.org/10.1186/1471-213X-1-4
Wu S, Wu Y, Capecchi MR. Motoneurons and oligodendrocytes are sequentially generated from neural stem cells but do not appear to share common lineage-restricted progenitors in vivo. Development (Cambridge, England). 2006;133(4):581-90. Epub 20060111. PubMed PMID: 16407399. DOI: https://doi.org/10.1242/dev.02236
Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis. 2007;45(9):593-605. PubMed PMID: 17868096. DOI: https://doi.org/10.1002/dvg.20335
von Maltzahn J, Jones AE, Parks RJ, Rudnicki MA. Pax7 is critical for the normal function of satellite cells in adult skeletal muscle. Proc Natl Acad Sci U S A. 2013;110(41):16474-9. Epub 20130924. PubMed PMID: 24065826; PubMed Central PMCID: PMC3799311. DOI: https://doi.org/10.1073/pnas.1307680110
Brack AS. Pax7 is back. Skeletal Muscle. 2014;4(1):24. DOI: https://doi.org/10.1186/s13395-014-0024-4
Mizuguchi H, Xu Z, Ishii-Watabe A, Uchida E, Hayakawa T. IRES-dependent second gene expression is significantly lower than cap-dependent first gene expression in a bicistronic vector. Mol Ther. 2000;1(4):376-82. PubMed PMID: 10933956. DOI: https://doi.org/10.1006/mthe.2000.0050
Richter JD, Sonenberg N. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature. 2005;433(7025):477-80. PubMed PMID: 15690031. DOI: https://doi.org/10.1038/nature03205
Ibrahimi A, Vande Velde G, Reumers V, Toelen J, Thiry I, Vandeputte C, et al. Highly efficient multicistronic lentiviral vectors with peptide 2A sequences. Hum Gene Ther. 2009;20(8):845-60. PubMed PMID: 19419274. DOI: https://doi.org/10.1089/hum.2008.188

How to Cite

Ortuste Quiroga, H. P., Fujimaki, S., & Ono, Y. (2023). Pax7 reporter mouse models: a pocket guide for satellite cell research. European Journal of Translational Myology, 33(4). https://doi.org/10.4081/ejtm.2023.12174

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