The Panniculus Carnosus Muscle: A Novel Model of Striated Muscle Regeneration That Exhibits Sex Differences in the Mdx Mouse

Overview

Journal Sci Rep

Specialty Science

Date 2019 Nov 6

PMID 31685850

Citations 11

Authors

Ola A Bahri

Neia Naldaiz-Gastesi

Donna C Kennedy

Antony M Wheatley

Ander Izeta

Karl J A McCullagh

Affiliations

Soon will be listed here.

Abstract

The dermal striated muscle panniculus carnosus (PC), prevalent in lower mammals with remnants in humans, is highly regenerative, and whose function is purported to be linked to defence and shivering thermogenesis. Given the heterogeneity of responses of different muscles to disease, we set out to characterize the PC in wild-type and muscular dystrophic mdx mice. The mouse PC contained mainly fast-twitch type IIB myofibers showing body wide distribution. The PC exemplified heterogeneity in myofiber sizes and a prevalence of central nucleated fibres (CNFs), hallmarks of regeneration, in wild-type and mdx muscles, which increased with age. PC myofibers were hypertrophic in mdx compared to wild-type mice. Sexual dimorphism was apparent with a two-fold increase in CNFs in PC from male versus female mdx mice. To evaluate myogenic potential, PC muscle progenitors were isolated from 8-week old wild-type and mdx mice, grown and differentiated for 7-days. Myogenic profiling of PC-derived myocytes suggested that male mdx satellite cells (SCs) were more myogenic than female counterparts, independent of SC density in PC muscles. Muscle regenerative differences in the PC were associated with alterations in expression of calcium handling regulatory proteins. These studies highlight unique aspects of the PC muscle and its potential as a model to study mechanisms of striated muscle regeneration in health and disease.

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References

Garcia-Parra P, Cavaliere F, Maroto M, Bilbao L, Obieta I, de Munain A . Modeling neural differentiation on micropatterned substrates coated with neural matrix components. Front Cell Neurosci. 2012; 6:10. PMC: 3303083. DOI: 10.3389/fncel.2012.00010. View

Kornegay J, Childers M, Bogan D, Bogan J, Nghiem P, Wang J . The paradox of muscle hypertrophy in muscular dystrophy. Phys Med Rehabil Clin N Am. 2012; 23(1):149-72, xii. PMC: 5951392. DOI: 10.1016/j.pmr.2011.11.014. View

Kunert-Keil C, Gredes T, Lucke S, Botzenhart U, Dominiak M, Gedrange T . Differential expression of genes involved in the calcium homeostasis in masticatory muscles of MDX mice. J Physiol Pharmacol. 2014; 65(2):317-24. View

Millay D, Goonasekera S, Sargent M, Maillet M, Aronow B, Molkentin J . Calcium influx is sufficient to induce muscular dystrophy through a TRPC-dependent mechanism. Proc Natl Acad Sci U S A. 2009; 106(45):19023-8. PMC: 2776441. DOI: 10.1073/pnas.0906591106. View

Moens P, Baatsen P, Marechal G . Increased susceptibility of EDL muscles from mdx mice to damage induced by contractions with stretch. J Muscle Res Cell Motil. 1993; 14(4):446-51. DOI: 10.1007/BF00121296. View

Naldaiz-Gastesi N, Bahri O, de Munain A, McCullagh K, Izeta A . The panniculus carnosus muscle: an evolutionary enigma at the intersection of distinct research fields. J Anat. 2018; . PMC: 6081499. DOI: 10.1111/joa.12840. View

Gehrig S, Koopman R, Naim T, Tjoakarfa C, Lynch G . Making fast-twitch dystrophic muscles bigger protects them from contraction injury and attenuates the dystrophic pathology. Am J Pathol. 2009; 176(1):29-33. PMC: 2797866. DOI: 10.2353/ajpath.2010.090760. View

McLoon L, Wirtschafter J . Continuous myonuclear addition to single extraocular myofibers in uninjured adult rabbits. Muscle Nerve. 2002; 25(3):348-58. DOI: 10.1002/mus.10056. View

Cros D, Harnden P, Pellissier J, Serratrice G . Muscle hypertrophy in Duchenne muscular dystrophy. A pathological and morphometric study. J Neurol. 1989; 236(1):43-7. DOI: 10.1007/BF00314217. View

10.

Laschke M, Menger M . The dorsal skinfold chamber: A versatile tool for preclinical research in tissue engineering and regenerative medicine. Eur Cell Mater. 2016; 32:202-15. DOI: 10.22203/eCM.v032a13. View

11.

Yin H, Price F, Rudnicki M . Satellite cells and the muscle stem cell niche. Physiol Rev. 2013; 93(1):23-67. PMC: 4073943. DOI: 10.1152/physrev.00043.2011. View

12.

Gehrig S, van der Poel C, Sayer T, Schertzer J, Henstridge D, Church J . Hsp72 preserves muscle function and slows progression of severe muscular dystrophy. Nature. 2012; 484(7394):394-8. DOI: 10.1038/nature10980. View

13.

Garcia-Parra P, Naldaiz-Gastesi N, Maroto M, Padin J, Goicoechea M, Aiastui A . Murine muscle engineered from dermal precursors: an in vitro model for skeletal muscle generation, degeneration, and fatty infiltration. Tissue Eng Part C Methods. 2013; 20(1):28-41. PMC: 3870606. DOI: 10.1089/ten.TEC.2013.0146. View

14.

DiMario J, Uzman A, Strohman R . Fiber regeneration is not persistent in dystrophic (MDX) mouse skeletal muscle. Dev Biol. 1991; 148(1):314-21. DOI: 10.1016/0012-1606(91)90340-9. View

15.

Stuelsatz P, Shearer A, Li Y, Muir L, Ieronimakis N, Shen Q . Extraocular muscle satellite cells are high performance myo-engines retaining efficient regenerative capacity in dystrophin deficiency. Dev Biol. 2014; 397(1):31-44. PMC: 4309674. DOI: 10.1016/j.ydbio.2014.08.035. View

16.

Porter J, Merriam A, Khanna S, Andrade F, Richmonds C, Leahy P . Constitutive properties, not molecular adaptations, mediate extraocular muscle sparing in dystrophic mdx mice. FASEB J. 2003; 17(8):893-5. DOI: 10.1096/fj.02-0810fje. View

17.

Briguet A, Courdier-Fruh I, Foster M, Meier T, Magyar J . Histological parameters for the quantitative assessment of muscular dystrophy in the mdx-mouse. Neuromuscul Disord. 2004; 14(10):675-82. DOI: 10.1016/j.nmd.2004.06.008. View

18.

Renault V, Forestier C, DiDonna S, Decary S, Hentati F, Saillant G . Skeletal muscle regeneration and the mitotic clock. Exp Gerontol. 2000; 35(6-7):711-9. DOI: 10.1016/s0531-5565(00)00151-0. View

19.

Pavlath G, Thaloor D, Rando T, Cheong M, English A, Zheng B . Heterogeneity among muscle precursor cells in adult skeletal muscles with differing regenerative capacities. Dev Dyn. 1998; 212(4):495-508. DOI: 10.1002/(SICI)1097-0177(199808)212:4<495::AID-AJA3>3.0.CO;2-C. View

20.

Keefe A, Lawson J, Flygare S, Fox Z, Colasanto M, Mathew S . Muscle stem cells contribute to myofibres in sedentary adult mice. Nat Commun. 2015; 6:7087. PMC: 4435732. DOI: 10.1038/ncomms8087. View