Journal of Muscle Research & Cell Motility

, Volume 22, Issue 6, pp 535–544

The muscle-specific enolase is an early marker of human myogenesis

  • Françoise Fougerousse
  • Frédérique Edom-Vovard
  • Tatyana Merkulova
  • Marie-Odile Ott
  • Muriel Durand
  • Gillian Butler-Browne
  • Angélica Keller
Article

DOI: 10.1023/A:1015008208007

Cite this article as:
Fougerousse, F., Edom-Vovard, F., Merkulova, T. et al. J Muscle Res Cell Motil (2001) 22: 535. doi:10.1023/A:1015008208007

Abstract

In higher vertebrates, the glycolytic enzyme enolase (2-phospho-D-glycerate hydrolase; EC 4.2.1.11) is active as a dimer formed from three different subunits, α, β and γ, encoded by separate genes. The expression of these genes is developmentally regulated in a tissue-specific manner. A shift occurs during development, from the unique embryonic isoform αα, towards specific isoforms in two tissues with high energy demands: αβ and γγ in the nervous system, αβ and ββ in striated muscles. The αα remains widely distributed in adult tissues. Here we report the results of the first extensive study of β enolase expression during human development. Indeed, the β subunit is specifically expressed at early stages of human myogenesis. Immunocytochemical analyses demonstrated that it is first detected in the heart of 3-week-old embryos and in the myotomal compartment of somites from 4-week-old embryos. At this stage, the muscle-specific sarcomeric protein titin is expressed in this structure, which will give rise to all body skeletal muscles, but embryonic myosin heavy chain is not yet present. Analyses at the protein level show that, during human ontogenesis, myogenesis is accompanied by an increase in β enolase expression and by a decrease in the expression of the two other α and γ subunits. Furthermore, β enolase subunit is expressed in proliferating myoblasts from both embryonic and post-natal muscles. In addition, clonal analysis of primary cell cultures, obtained from the leg muscle of a 7-week-old human embryo, revealed that the β subunit is present in the dividing myoblasts of all four types, according to the classification of Edom-Vovard et al. [(1999) J Cell Sci 112: 191–199], but not in cells of the non-myogenic lineage. Myoblast fusion is accompanied by a large increase in β enolase expression. Our results demonstrate that this muscle-specific isoform of a glycolytic enzyme (β enolase) is among the earliest markers of myogenic differentiation in humans.

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Françoise Fougerousse
    • 1
  • Frédérique Edom-Vovard
    • 2
  • Tatyana Merkulova
    • 3
  • Marie-Odile Ott
    • 4
  • Muriel Durand
    • 1
  • Gillian Butler-Browne
    • 5
  • Angélica Keller
    • 6
    • 7
  1. 1.GénéthonCNRS URA 1923EvryFrance
  2. 2.Institut d'EmbryologieCNRS et Collèe de FranceNogent sur MarneFrance
  3. 3.Institut des Vaisseaux et du SangHopital LariboisièreParisFrance
  4. 4.CHU Cochin Port-RoyalINSERM U 257ParisFrance
  5. 5.Faculté de Médecine Pitié-SalpétrièreCNRS URA 2115, Université Paris VIParisFrance
  6. 6.Laboratoire CRRET – CNRS UPRESA 7053Faculté des Sciences et Technologie Université Paris XIICréteil CedexFrance
  7. 7.Institut d'EmbryologieCNRS et Collèe de FranceNogent sur MarneFrance