Skip to main content
Log in

Pax7 distribution in human skeletal muscle biopsies and myogenic tissue cultures

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Demonstration of the importance of the paired box transcription factor Pax7 for the murine myosatellite cell population, with persistent expression in mature skeletal muscle, prompted us to investigate the distribution of Pax7 protein in biopsy samples of normal and pathological human skeletal limb muscle. Immunostaining for M-cadherin, an adhesion molecule present at the interface between myofibre and satellite cell, and the characteristic position adjacent to the muscle fibre and beneath the fibre’s basement membrane were used to identify satellite cells. Anti-Pax7 reactivity was found in the majority of satellite cells but a small population was Pax7 negative. Neither could we identify Pax7-positive nuclei in freshly regenerating myotubes or in presumed myoblasts in these biopsies. Similarly, in myogenic cell cultures derived from the explantation of human foetal muscle Pax7 expression was low or undetectable at the proliferative myoblast stage but it became prominent in an increasing proportion of mononucleate cells after the induction of differentiation. This expression was, however, restricted to mononucleate cells; it did not persist into the differentiation stage of newly formed multinucleate myotubes. Despite this, in the biopsy samples, we occasionally found Pax7-positive nuclei in muscle fibres that seemed to be undergoing degenerative changes. Most of these were found to be the nuclei of cells engaged in focal regenerative processes, but Pax7 re-expression by myonuclei “in distress” cannot be ruled out entirely.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2a–l
Fig. 3a–c
Fig. 4
Fig. 5a–i
Fig. 6

Similar content being viewed by others

References

  • Beauchamp JR, Morgan JE, Pagel, Partridge TA (1999) Dynamics of myoblast transplantation reveal a discrete minority of precursors with stem cell-like properties as the myogenic source. J Cell Biol 144:1113–1122

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp JR, Heslop L, Yu DS, Tajbakhsh S, Kelly RG, Wernig A, Buckingham ME, Partridge TA, Zammit P (2000) Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 151:1221–1234

    Article  CAS  PubMed  Google Scholar 

  • 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 202:59–68

    Article  PubMed  Google Scholar 

  • Conboy IM, Rando TA (2002) The regulation of notch signalling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 3:397–409

    CAS  PubMed  Google Scholar 

  • Donalies M, Cramer M, Ringwald M, Starzinski-Powitz A (1991) Expression of M-cadherin, a member of the cadherin multigene family, correlates with differentiation in skeletal muscle cells. Proc Natl Acad Sci U S A 88:8024–8028

    CAS  PubMed  Google Scholar 

  • Epstein JA, Shapiro DN, Cheng J, Lam PYP, Mass RL (1996) Pax3 modulates expression of the c-met receptor during limb muscle development. Proc Natl Acad Sci U S A 93:4212–4218

    Article  Google Scholar 

  • Ericson J, Morton S, Kawakami A, Roelink H, Jessel TM (1996) Two critical periods of sonic hedgehog signaling required for the specification of motor neuron identity. Cell 87:661–673

    CAS  PubMed  Google Scholar 

  • Heslop L, Beauchamp JR, Tajbakhsh S, Buckingham ME, Partridge TA, Zammit PS (2001) Transplanted primary neonatal myoblasts can give rise to functional satellite cells as identified using the Myf5nlacZl+ mouse. Gene Ther 8:778–783

    Article  CAS  PubMed  Google Scholar 

  • Holst BD, Gommer RS, Wood IC, Edelman GM, Jones FS (1994) Binding and activation of the promoter for the neural cell adhesion molecule by Pax-8. J Biol Chem 269:2224–2225

    Google Scholar 

  • Irintchev A, Zeschnigk M, Starzinski-Powitz A, Wernig A (1994) Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev Dyn 199:326–337

    CAS  PubMed  Google Scholar 

  • LaBarge MA, Blau HM (2002) Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell 111:589–601

    CAS  PubMed  Google Scholar 

  • Lagord C, Soulet L, Bonavaud S, Bassaglia Y, Rey C, Barlovatz-Meimon G, Gautron J, Martelly I (1998) Differential myogenicity of satellite cells isolated from extensor digitorum longus (EDL) and soleus rat muscles revealed in vitro. Cell Tissue Res 291:455–468

    Article  CAS  PubMed  Google Scholar 

  • Mansouri A, Hallonet M, Gruss P (1996) Pax genes and their role in cell differentiation and development. Curr Opin Cell Biol 8:851–857

    CAS  PubMed  Google Scholar 

  • Molnar G, Ho ML, Schroedl NA (1996) Evidence for multiple satellite cell populations and a non-myogenic cell type that is regulated differently in regenerating and growing skeletal muscle. Tissue Cell 28:547–556

    CAS  PubMed  Google Scholar 

  • Rantanen J, Hurme T, Lukka R, Heino J, Kalimo H (1995) Satellite cell proliferation and the expression of myogenin and desmin in regenerating skeletal muscle: evidence for two different populations of satellite cells. Lab Invest 72:341–347

    CAS  PubMed  Google Scholar 

  • Rodger J, Ziman MR, Papadimitriou JM, Kay PH (1999) Pax7 is expressed in the capsules surrounding adult mouse neuromuscular spindles. Biochem Cell Biol 77:153–156

    Article  CAS  PubMed  Google Scholar 

  • Rosenblatt JD, Cullen MJ, Irintchev A, Wernig A (1999) M-cadherin is a reliable molecular marker of satellite cells in mouse skeletal muscle. Eur J Physiol 437:R145 (abstract)

    Google Scholar 

  • Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki ME (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102:777–786

    CAS  PubMed  Google Scholar 

  • Watkins SC, Cullen MJ (1988) A quantitative study of myonuclear and satellite cell nuclear size in Duchenne’s muscular dystrophy, polymyositis and normal human skeletal muscle. Anat Rec 222:6–11

    CAS  PubMed  Google Scholar 

  • Weis J (1994) Fos, Jun, Myo D1 and myogenin proteins are increased in skeletal muscle fibre nuclei after denervation. Acta Neuropathol 87:63–70

    Google Scholar 

  • Zammit PS, Heslop L, Hudon V, Rosenblatt JD, Tajbakhsh S, Buckingham ME, Beauchamp JR, Partridge TA (2002) Kinetics of myoblast proliferation show that resident satellite cells are competent to fully regenerate skeletal muscle fibres. Exp Cell Res 281:39–49

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgement

Foetal tissue was provided by the MRC tissue bank in compliance with the government approved recommendations of the Polkinghorne Report (1989) and with permission from the Research Ethics Committee of the Hammersmith, Queen Charlotte’s, Chelsea and Acton Hospitals, London. We wish to thank Prof. Atsushi Kawakami for the development of the anti-Pax7 hybridoma and for his friendly advice. Mrs. Karin Kappes-Horn provided invaluable organisational help again. Prof. Kawakami’s Pax7 hybridoma was obtained from the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by The University of Iowa, Department of Biological Sciences, Iowa City, IA 52242.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jens Reimann.

Additional information

Dr. F. Reimann was supported by a grant from the Deutsche Forschungsgemeinschaft (Re 1547/1–1). Further support came from the Muscular Dystrophy Association (Prof. Partridge)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reimann, J., Brimah, K., Schröder, R. et al. Pax7 distribution in human skeletal muscle biopsies and myogenic tissue cultures. Cell Tissue Res 315, 233–242 (2004). https://doi.org/10.1007/s00441-003-0833-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-003-0833-y

Keywords

Navigation