MyoD, myogenin independent differentiation of primordial myoblasts in mouse somites

M. G. Cusella-De Angelis, G. Lyons, C. Sonnino, L. De Angelis, E. Vivarelli, K. Farmer, W. E. Wright, M. Molinaro, M. Bouché, M. Buckingham, G. Cossu

Research output: Contribution to journalArticle

88 Citations (Scopus)

Abstract

The accumulation of two myogenic regulatory proteins, MyoD and myogenin, was investigated by double-immunocytochemistry and correlated with myosin heavy chain expression in different classes of myoblasts in culture and during early myogenesis in vivo. During in vitro differentiation of fetal myoblasts, MyoD-positive cells were detected first, followed by the appearance of cells positive for both MyoD and myogenin and finally by the appearance of differentiated myocytes and myotubes expressing myosin heavy chain (MHC). A similar pattern of expression was observed in cultures of embryonic and satellite cells. In contrast, most myogenic cells isolated from newly formed somites, expressed MHC in the absence of detectable levels of myogenin or MyoD, In vivo, the appearance of both myogenin and MyoD proteins was only detected at 10.5 d postcoitum (d.p.c.), when terminally differentiated muscle cells could already be identified in the myotome. Parasagittal sections of the caudal myotomes of 10.5-d-old embryos showed that expression of contractile proteins preceded the expression of myogenin or MyoD and, when coexpressed, MHC and myogenin did not co-localize within all the cells of the myotome. In the limb bud, however, many myogenin (or MyoD) positive/MHC negative cells could be observed in the proximal region at day 11. During further embryonic development the expression of these proteins remained constant in all the muscle anlagens examined, decreasing to a low level during the late fetal period. Western and Northern analysis confirmed that the myogenin protein could only be detected after 10.5 d.p.c. while the corresponding message was clearly present at 9.5 d.p.c., strongly suggesting a posttranscriptional regulation of myogenin during this stage of embryonic development. These data show that the first myogenic cells which appear in the mouse myotome, and can be cultured from it, accumulate muscle structural proteins in their cytoplasm without expressing detectable levels of myogenin protein (although the message is clearly accumulated). Neither MyoD message or protein are detectable in these cells, which may represent a distinct myogenic population whose role in development remains to be established.

Original languageEnglish (US)
Pages (from-to)1243-1255
Number of pages13
JournalJournal of Cell Biology
Volume116
Issue number5
StatePublished - Mar 1992

Fingerprint

Myogenin
Somites
Myoblasts
Myosin Heavy Chains
MyoD Protein
Muscle Cells
Embryonic Development
Proteins
Limb Buds
Contractile Proteins
Muscle Development
Muscle Proteins
Skeletal Muscle Fibers
Cytoplasm
Embryonic Structures
Immunohistochemistry

ASJC Scopus subject areas

  • Cell Biology

Cite this

Cusella-De Angelis, M. G., Lyons, G., Sonnino, C., De Angelis, L., Vivarelli, E., Farmer, K., ... Cossu, G. (1992). MyoD, myogenin independent differentiation of primordial myoblasts in mouse somites. Journal of Cell Biology, 116(5), 1243-1255.

MyoD, myogenin independent differentiation of primordial myoblasts in mouse somites. / Cusella-De Angelis, M. G.; Lyons, G.; Sonnino, C.; De Angelis, L.; Vivarelli, E.; Farmer, K.; Wright, W. E.; Molinaro, M.; Bouché, M.; Buckingham, M.; Cossu, G.

In: Journal of Cell Biology, Vol. 116, No. 5, 03.1992, p. 1243-1255.

Research output: Contribution to journalArticle

Cusella-De Angelis, MG, Lyons, G, Sonnino, C, De Angelis, L, Vivarelli, E, Farmer, K, Wright, WE, Molinaro, M, Bouché, M, Buckingham, M & Cossu, G 1992, 'MyoD, myogenin independent differentiation of primordial myoblasts in mouse somites', Journal of Cell Biology, vol. 116, no. 5, pp. 1243-1255.
Cusella-De Angelis MG, Lyons G, Sonnino C, De Angelis L, Vivarelli E, Farmer K et al. MyoD, myogenin independent differentiation of primordial myoblasts in mouse somites. Journal of Cell Biology. 1992 Mar;116(5):1243-1255.
Cusella-De Angelis, M. G. ; Lyons, G. ; Sonnino, C. ; De Angelis, L. ; Vivarelli, E. ; Farmer, K. ; Wright, W. E. ; Molinaro, M. ; Bouché, M. ; Buckingham, M. ; Cossu, G. / MyoD, myogenin independent differentiation of primordial myoblasts in mouse somites. In: Journal of Cell Biology. 1992 ; Vol. 116, No. 5. pp. 1243-1255.
@article{328fba333d91423fa17b89e1d9196416,
title = "MyoD, myogenin independent differentiation of primordial myoblasts in mouse somites",
abstract = "The accumulation of two myogenic regulatory proteins, MyoD and myogenin, was investigated by double-immunocytochemistry and correlated with myosin heavy chain expression in different classes of myoblasts in culture and during early myogenesis in vivo. During in vitro differentiation of fetal myoblasts, MyoD-positive cells were detected first, followed by the appearance of cells positive for both MyoD and myogenin and finally by the appearance of differentiated myocytes and myotubes expressing myosin heavy chain (MHC). A similar pattern of expression was observed in cultures of embryonic and satellite cells. In contrast, most myogenic cells isolated from newly formed somites, expressed MHC in the absence of detectable levels of myogenin or MyoD, In vivo, the appearance of both myogenin and MyoD proteins was only detected at 10.5 d postcoitum (d.p.c.), when terminally differentiated muscle cells could already be identified in the myotome. Parasagittal sections of the caudal myotomes of 10.5-d-old embryos showed that expression of contractile proteins preceded the expression of myogenin or MyoD and, when coexpressed, MHC and myogenin did not co-localize within all the cells of the myotome. In the limb bud, however, many myogenin (or MyoD) positive/MHC negative cells could be observed in the proximal region at day 11. During further embryonic development the expression of these proteins remained constant in all the muscle anlagens examined, decreasing to a low level during the late fetal period. Western and Northern analysis confirmed that the myogenin protein could only be detected after 10.5 d.p.c. while the corresponding message was clearly present at 9.5 d.p.c., strongly suggesting a posttranscriptional regulation of myogenin during this stage of embryonic development. These data show that the first myogenic cells which appear in the mouse myotome, and can be cultured from it, accumulate muscle structural proteins in their cytoplasm without expressing detectable levels of myogenin protein (although the message is clearly accumulated). Neither MyoD message or protein are detectable in these cells, which may represent a distinct myogenic population whose role in development remains to be established.",
author = "{Cusella-De Angelis}, {M. G.} and G. Lyons and C. Sonnino and {De Angelis}, L. and E. Vivarelli and K. Farmer and Wright, {W. E.} and M. Molinaro and M. Bouch{\'e} and M. Buckingham and G. Cossu",
year = "1992",
month = "3",
language = "English (US)",
volume = "116",
pages = "1243--1255",
journal = "Journal of Cell Biology",
issn = "0021-9525",
publisher = "Rockefeller University Press",
number = "5",

}

TY - JOUR

T1 - MyoD, myogenin independent differentiation of primordial myoblasts in mouse somites

AU - Cusella-De Angelis, M. G.

AU - Lyons, G.

AU - Sonnino, C.

AU - De Angelis, L.

AU - Vivarelli, E.

AU - Farmer, K.

AU - Wright, W. E.

AU - Molinaro, M.

AU - Bouché, M.

AU - Buckingham, M.

AU - Cossu, G.

PY - 1992/3

Y1 - 1992/3

N2 - The accumulation of two myogenic regulatory proteins, MyoD and myogenin, was investigated by double-immunocytochemistry and correlated with myosin heavy chain expression in different classes of myoblasts in culture and during early myogenesis in vivo. During in vitro differentiation of fetal myoblasts, MyoD-positive cells were detected first, followed by the appearance of cells positive for both MyoD and myogenin and finally by the appearance of differentiated myocytes and myotubes expressing myosin heavy chain (MHC). A similar pattern of expression was observed in cultures of embryonic and satellite cells. In contrast, most myogenic cells isolated from newly formed somites, expressed MHC in the absence of detectable levels of myogenin or MyoD, In vivo, the appearance of both myogenin and MyoD proteins was only detected at 10.5 d postcoitum (d.p.c.), when terminally differentiated muscle cells could already be identified in the myotome. Parasagittal sections of the caudal myotomes of 10.5-d-old embryos showed that expression of contractile proteins preceded the expression of myogenin or MyoD and, when coexpressed, MHC and myogenin did not co-localize within all the cells of the myotome. In the limb bud, however, many myogenin (or MyoD) positive/MHC negative cells could be observed in the proximal region at day 11. During further embryonic development the expression of these proteins remained constant in all the muscle anlagens examined, decreasing to a low level during the late fetal period. Western and Northern analysis confirmed that the myogenin protein could only be detected after 10.5 d.p.c. while the corresponding message was clearly present at 9.5 d.p.c., strongly suggesting a posttranscriptional regulation of myogenin during this stage of embryonic development. These data show that the first myogenic cells which appear in the mouse myotome, and can be cultured from it, accumulate muscle structural proteins in their cytoplasm without expressing detectable levels of myogenin protein (although the message is clearly accumulated). Neither MyoD message or protein are detectable in these cells, which may represent a distinct myogenic population whose role in development remains to be established.

AB - The accumulation of two myogenic regulatory proteins, MyoD and myogenin, was investigated by double-immunocytochemistry and correlated with myosin heavy chain expression in different classes of myoblasts in culture and during early myogenesis in vivo. During in vitro differentiation of fetal myoblasts, MyoD-positive cells were detected first, followed by the appearance of cells positive for both MyoD and myogenin and finally by the appearance of differentiated myocytes and myotubes expressing myosin heavy chain (MHC). A similar pattern of expression was observed in cultures of embryonic and satellite cells. In contrast, most myogenic cells isolated from newly formed somites, expressed MHC in the absence of detectable levels of myogenin or MyoD, In vivo, the appearance of both myogenin and MyoD proteins was only detected at 10.5 d postcoitum (d.p.c.), when terminally differentiated muscle cells could already be identified in the myotome. Parasagittal sections of the caudal myotomes of 10.5-d-old embryos showed that expression of contractile proteins preceded the expression of myogenin or MyoD and, when coexpressed, MHC and myogenin did not co-localize within all the cells of the myotome. In the limb bud, however, many myogenin (or MyoD) positive/MHC negative cells could be observed in the proximal region at day 11. During further embryonic development the expression of these proteins remained constant in all the muscle anlagens examined, decreasing to a low level during the late fetal period. Western and Northern analysis confirmed that the myogenin protein could only be detected after 10.5 d.p.c. while the corresponding message was clearly present at 9.5 d.p.c., strongly suggesting a posttranscriptional regulation of myogenin during this stage of embryonic development. These data show that the first myogenic cells which appear in the mouse myotome, and can be cultured from it, accumulate muscle structural proteins in their cytoplasm without expressing detectable levels of myogenin protein (although the message is clearly accumulated). Neither MyoD message or protein are detectable in these cells, which may represent a distinct myogenic population whose role in development remains to be established.

UR - http://www.scopus.com/inward/record.url?scp=0026579129&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0026579129&partnerID=8YFLogxK

M3 - Article

C2 - 1310995

AN - SCOPUS:0026579129

VL - 116

SP - 1243

EP - 1255

JO - Journal of Cell Biology

JF - Journal of Cell Biology

SN - 0021-9525

IS - 5

ER -