Acta Neuropathologica

, Volume 134, Issue 6, pp 869–888 | Cite as

Muscle satellite cells are functionally impaired in myasthenia gravis: consequences on muscle regeneration

  • Mohamed Attia
  • Marie Maurer
  • Marieke Robinet
  • Fabien Le Grand
  • Elie Fadel
  • Rozen Le Panse
  • Gillian Butler-Browne
  • Sonia Berrih-AkninEmail author
Original Paper


Myasthenia gravis (MG) is a neuromuscular disease caused in most cases by anti-acetyl-choline receptor (AChR) autoantibodies that impair neuromuscular signal transmission and affect skeletal muscle homeostasis. Myogenesis is carried out by muscle stem cells called satellite cells (SCs). However, myogenesis in MG had never been explored. The aim of this study was to characterise the functional properties of myasthenic SCs as well as their abilities in muscle regeneration. SCs were isolated from muscle biopsies of MG patients and age-matched controls. We first showed that the number of Pax7+ SCs was increased in muscle sections from MG and its experimental autoimmune myasthenia gravis (EAMG) mouse model. Myoblasts isolated from MG muscles proliferate and differentiate more actively than myoblasts from control muscles. MyoD and MyoG were expressed at a higher level in MG myoblasts as well as in MG muscle biopsies compared to controls. We found that treatment of control myoblasts with MG sera or monoclonal anti-AChR antibodies increased the differentiation and MyoG mRNA expression compared to control sera. To investigate the functional ability of SCs from MG muscle to regenerate, we induced muscle regeneration using acute cardiotoxin injury in the EAMG mouse model. We observed a delay in maturation evidenced by a decrease in fibre size and MyoG mRNA expression as well as an increase in fibre number and embryonic myosin heavy-chain mRNA expression. These findings demonstrate for the first time the altered function of SCs from MG compared to control muscles. These alterations could be due to the anti-AChR antibodies via the modulation of myogenic markers resulting in muscle regeneration impairment. In conclusion, the autoimmune attack in MG appears to have unsuspected pathogenic effects on SCs and muscle regeneration, with potential consequences on myogenic signalling pathways, and subsequently on clinical outcome, especially in the case of muscle stress.


MG patients AChR antibodies Myogenic factors Experimental autoimmune myasthenia gravis (EAMG) 



We thank our colleagues Jacky BISMUTH, Frédérique TRUFFAULT, Nadine DRAGIN-MAMAVI, Floriane LACOUR, Elija SCHIRWIS, Jean-Thomas VILQUIN, and all Myology Research Centre members for their valuable discussions and help. We thank all members of the SPF animal facility (CEF, Université Pierre et Marie Curie) for their valuable advice and help. We also thank our collaborator Socrates TZARTOS for his kind gift of anti-AChR monoclonal antibodies. This study was funded by a Grant from European consortium called Fight-MG (Grant Number 242210).

Compliance with ethical standards

Research involving human participants

All procedures performed in studies involving human participants were in accordance with the ethical standards of the French research committee “Comité de Protection des Personnes (CPP, Ile-de-France VI)” (authorization number 2010-A00250-39) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. All participants gave informed written consent. The experiments involving mice were performed following the principles of the French council on animal care (authorisation number: 02637).

Conflict of interest

The authors declare having no conflict of interest.

Supplementary material

401_2017_1754_MOESM1_ESM.pdf (1.9 mb)
Supplementary material 1 (PDF 1954 kb)


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Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Mohamed Attia
    • 1
    • 2
    • 3
  • Marie Maurer
    • 1
    • 2
    • 3
  • Marieke Robinet
    • 1
    • 2
    • 3
  • Fabien Le Grand
    • 1
    • 2
    • 3
  • Elie Fadel
    • 4
  • Rozen Le Panse
    • 1
    • 2
    • 3
  • Gillian Butler-Browne
    • 1
    • 2
    • 3
  • Sonia Berrih-Aknin
    • 1
    • 2
    • 3
    Email author
  1. 1.Sorbonne Universités, UPMC Université Paris 6ParisFrance
  2. 2.INSERM U974, Centre de Recherche en Myologie (CRM), GH Pitié-SalpêtrièreParis 13France
  3. 3.AIM, Institut de Myologie GH Pitié-SalpêtrièreParisFrance
  4. 4.INSERM U999, Centre Chirurgical Marie LannelongueLe Plessis-RobinsonFrance

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