Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Cellular and Molecular Biology Letters

Editor-in-Chief: /


IMPACT FACTOR 2016: 1.260
5-year IMPACT FACTOR: 1.506

CiteScore 2016: 1.56

SCImago Journal Rank (SJR) 2016: 0.615
Source Normalized Impact per Paper (SNIP) 2016: 0.470

Online
ISSN
1689-1392
See all formats and pricing
More options …
Volume 16, Issue 2 (Jun 2011)

The expression of myogenic regulatory factors and muscle growth factors in the masticatory muscles of dystrophin-deficient (MDX) mice

Alexander Spassov / Tomasz Gredes / Tomasz Gedrange / Silke Lucke / Dragan Pavlovic / Christiane Kunert-Keil
Published Online: 2011-03-26 | DOI: https://doi.org/10.2478/s11658-011-0003-2

Abstract

The activities of myogenic regulatory factors (MRF) and muscle growth factors increase in muscle that is undergoing regeneration, and may correspond to some specific changes. Little is known about the role of MRFs in masticatory muscles in mdx mice (the model of Duchenne muscular dystrophy) and particularly about their mRNA expression during the process of muscle regeneration. Using Taqman RT-PCR, we examined the mRNA expression of the MRFs myogenin and MyoD1 (myogenic differentiation 1), and of the muscle growth factors myostatin, IGF1 (insulin-like growth factor) and MGF (mechanogrowth factor) in the masseter, temporal and tongue masticatory muscles of mdx mice (n = 6 to 10 per group). The myogenin mRNA expression in the mdx masseter and temporal muscle was found to have increased (P < 0.05), whereas the myostatin mRNA expressions in the mdx masseter (P < 0.005) and tongue (P < 0.05) were found to have diminished compared to those for the controls. The IGF and MGF mRNA amounts in the mdx mice remained unchanged. Inside the mdx animal group, gender-related differences in the mRNA expressions were also found. A higher mRNA expression of myogenin and MyoD1 in the mdx massterer and temporal muscles was found in females in comparison to males, and the level of myostatin was higher in the masseter and tongue muscle (P < 0.001 for all comparisons). Similar gender-related differences were also found within the control groups. This study reveals the intermuscular differences in the mRNA expression pattern of myogenin and myostatin in mdx mice. The existence of these differences implies that dystrophinopathy affects the skeletal muscles differentially. The finding of gender-related differences in the mRNA expression of the examined factors may indicate the importance of hormonal influences on muscle regeneration.

Keywords: Mdx mice; Dystrophy; Masticatory muscles; MyoD1; Myogenin

  • [1] Hoffman, E.P., Brown, R.H., Jr. and Kunkel, L.M. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51 (1987) 919–928. http://dx.doi.org/10.1016/0092-8674(87)90579-4CrossrefGoogle Scholar

  • [2] Eckardt, L. and Harzer, W. Facial structure and functional findings in patients with progressive muscular dystrophy (Duchenne). Am. J. Orthod. Dentofacial. Orthop. 110 (1996) 185–190. http://dx.doi.org/10.1016/S0889-5406(96)70107-5CrossrefGoogle Scholar

  • [3] Botteron, S., Verdebout, C.M., Jeannet, P.Y. and Kiliaridis, S. Orofacial dysfunction in Duchenne muscular dystrophy. Arch. Oral. Biol. 54 (2009) 26–31. http://dx.doi.org/10.1016/j.archoralbio.2008.07.012Web of ScienceCrossrefGoogle Scholar

  • [4] Manzur, A.Y., Kinali, M. and Muntoni, F. Update on the management of Duchenne muscular dystrophy. Arch. Dis. Child. 93 (2008) 986–990. http://dx.doi.org/10.1136/adc.2007.118141CrossrefWeb of ScienceGoogle Scholar

  • [5] Pane, M., Vasta, I., Messina, S., Sorleti, D., Aloysius, A., Sciarra, F., Mangiola, F., Kinali, M., Ricci, E. and Mercuri, E. Feeding problems and weight gain in Duchenne muscular dystrophy. Eur. J. Paediatr. Neurol. 10 (2006) 231–236. http://dx.doi.org/10.1016/j.ejpn.2006.08.008CrossrefGoogle Scholar

  • [6] Bulfield, G., Siller, W.G., Wight, P.A. and Moore, K.J. X chromosomelinked muscular dystrophy (mdx) in the mouse. Proc. Natl. Acad. Sci. USA 81 (1984) 1189–1192. http://dx.doi.org/10.1073/pnas.81.4.1189CrossrefGoogle Scholar

  • [7] Pastoret, C. and Sebille, A. Age-related differences in regeneration of dystrophic (mdx) and normal muscle in the mouse. Muscle Nerve 18 (1995) 1147–1154. http://dx.doi.org/10.1002/mus.880181011CrossrefGoogle Scholar

  • [8] Tanabe, Y., Esaki, K. and Nomura, T. Skeletal muscle pathology in X chromosome-linked muscular dystrophy (mdx) mouse. Acta. Neuropathol. 69 (1986) 91–95. http://dx.doi.org/10.1007/BF00687043CrossrefGoogle Scholar

  • [9] McArdle, A., Edwards, R.H. and Jackson, M.J. How does dystrophin deficiency lead to muscle degeneration?—evidence from the mdx mouse. Neuromuscul. Disord. 5 (1995) 445–456. http://dx.doi.org/10.1016/0960-8966(95)00001-4CrossrefGoogle Scholar

  • [10] Buskin, J.N. and Hauschka, S.D. Identification of a myocyte nuclear factor that binds to the muscle-specific enhancer of the mouse muscle creatine kinase gene. Mol. Cell. Biol. 9 (1989) 2627–2640. Google Scholar

  • [11] Rudnicki, M.A. and Jaenisch, R. The MyoD family of transcription factors and skeletal myogenesis. Bioessays 17 (1995) 203–209. http://dx.doi.org/10.1002/bies.950170306CrossrefGoogle Scholar

  • [12] Gayraud-Morel, B., Chretien, F., Flamant, P., Gomes, D., Zammit, P.S. and Tajbakhsh, S. A role for the myogenic determination gene Myf5 in adult regenerative myogenesis. Dev. Biol. 312 (2007) 13–28. http://dx.doi.org/10.1016/j.ydbio.2007.08.059CrossrefWeb of ScienceGoogle Scholar

  • [13] Goldspink, G., Wessner, B., Tschan, H. and Bachl, N. Growth factors, muscle function, and doping. Endocrinol. Metab. Clin. North. Am. 39 (2010) 169–181, xi. http://dx.doi.org/10.1016/j.ecl.2009.11.001CrossrefGoogle Scholar

  • [14] Gredes, T., Spassov, A., Mai, R., Mack, H., Loster, B.W., Mazurkiewicz-Janik, M., Kubein-Meesenburg, D., Fanghanel, J. and Gedrange, T. Changes in insulin like growth factors, myostatin and vascular endothelial growth factor in rat musculus latissimus dorsi by poly-3-hydroxybutyrate implants. J. Physiol. Pharmacol. 60Suppl 3 (2009) 77–81. Google Scholar

  • [15] Enns, D.L. and Tiidus, P.M. Estrogen influences satellite cell activation and proliferation following downhill running in rats. J. Appl. Physiol. 104 (2008) 347–353. http://dx.doi.org/10.1152/japplphysiol.00128.2007Web of ScienceCrossrefGoogle Scholar

  • [16] Tiidus, P.M. Oestrogen and sex influence on muscle damage and inflammation: evidence from animal models. Curr. Opin. Clin. Nutr. Metab. Care 4 (2001) 509–513. http://dx.doi.org/10.1097/00075197-200111000-00008CrossrefGoogle Scholar

  • [17] Tiidus, P.M., Holden, D., Bombardier, E., Zajchowski, S., Enns, D. and Belcastro, A. Estrogen effect on post-exercise skeletal muscle neutrophil infiltration and calpain activity. Can. J. Physiol. Pharmacol. 79 (2001) 400–406. http://dx.doi.org/10.1139/cjpp-79-5-400CrossrefGoogle Scholar

  • [18] Valentine, B.A., Cooper, B.J., de Lahunta, A., O’Quinn, R. and Blue, J.T. Canine X-linked muscular dystrophy. An animal model of Duchenne muscular dystrophy: clinical studies. J. Neurol. Sci. 88 (1988) 69–81. http://dx.doi.org/10.1016/0022-510X(88)90206-7CrossrefGoogle Scholar

  • [19] Boland, B., Himpens, B., Denef, J.F. and Gillis, J.M. Site-dependent pathological differences in smooth muscles and skeletal muscles of the adult mdx mouse. Muscle Nerve 18 (1995) 649–657. http://dx.doi.org/10.1002/mus.880180612CrossrefGoogle Scholar

  • [20] Spassov, A., Gredes, T., Gedrange, T., Lucke, S., Pavlovic, D. and Kunert-Keil, C. Histological changes in masticatory muscles of mdx mice. Arch. Oral. Biol. 55 (2010) 318–324. http://dx.doi.org/10.1016/j.archoralbio.2010.02.005CrossrefWeb of ScienceGoogle Scholar

  • [21] Spassov, A., Gredes, T., Gedrange, T., Lucke, S., Morgensternm S., Pavlovic, D. and Kunert-Keil, C. Differential expression of MyHC isoforms in masticatory muscles of mdx mice. Eur. J. Orthod. (2010) DOI: 10.1093/ejo/CJQ1113. CrossrefGoogle Scholar

  • [22] Kunert-Keil, C., Bisping, F., Kruger, J. and Brinkmeier, H. Tissue-specific expression of TRP channel genes in the mouse and its variation in three different mouse strains. BioMed. Central Genomics 7 (2006) 159. Google Scholar

  • [23] Mack, H.B., Mai, R., Lauer, G., Mack, F., Gedrange, T., Franke, R. and Gredes, T. Adaptation of myosin heavy chain mRNA expression after implantation of poly(3)hydroxybutyrate scaffolds in rat m. latissimus dorsi. J. Physiol. Pharmacol. 59Suppl 5 (2008) 95–103. Google Scholar

  • [24] Livak, K.J. and Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001) 402–408. http://dx.doi.org/10.1006/meth.2001.1262CrossrefGoogle Scholar

  • [25] Marotta, M., Sarria, Y., Ruiz-Roig, C., Munell, F. and Roig-Quilis, M. Laser microdissection-based expression analysis of key genes involved in muscle regeneration in mdx mice. Neuromuscul. Disord. 17 (2007) 707–718. http://dx.doi.org/10.1016/j.nmd.2007.05.007CrossrefGoogle Scholar

  • [26] Fuchtbauer, E.M. and Westphal, H. MyoD and myogenin are coexpressed in regenerating skeletal muscle of the mouse. Dev. Dyn. 193 (1992) 34–39. http://dx.doi.org/10.1002/aja.1001930106CrossrefGoogle Scholar

  • [27] Beilharz, M.W., Lareu, R.R., Garrett, K.L., Grounds, M.D. and Fletcher, S. Quantitation of muscle precursor cell activity in skeletal muscle by Northern analysis of MyoD and myogenin expression: Application to dystrophic (mdx) mouse muscle. Mol. Cell. Neurosci. 3 (1992) 326–331. http://dx.doi.org/10.1016/1044-7431(92)90029-2CrossrefGoogle Scholar

  • [28] Jin, Y., Murakami, N., Saito, Y., Goto, Y., Koishi, K. and Nonaka, I. Expression of MyoD and myogenin in dystrophic mice, mdx and dy, during regeneration. Acta Neuropathol. 99 (2000) 619–627. http://dx.doi.org/10.1007/s004010051172CrossrefGoogle Scholar

  • [29] Hasty, P., Bradley, A., Morris, J.H., Edmondson, D.G., Venuti, J.M., Olson, E.N. and Klein, W.H. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364 (1993) 501–506. http://dx.doi.org/10.1038/364501a0CrossrefGoogle Scholar

  • [30] Nabeshima, Y., Hanaoka, K., Hayasaka, M., Esumi, E., Li, S. and Nonaka, I. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364 (1993) 532–535. http://dx.doi.org/10.1038/364532a0CrossrefGoogle Scholar

  • [31] Weintraub, H. The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 75 (1993) 1241–1244. http://dx.doi.org/10.1016/0092-8674(93)90610-3CrossrefGoogle Scholar

  • [32] Abe, S., Kasahara, N., Amano, M., Yoshii, M., Watanabe, H. and Ide, Y. Histological study of masseter muscle in a mouse muscular dystrophy model (mdx mouse). Bull. Tokyo Dent. Coll. 41 (2000) 119–122. http://dx.doi.org/10.2209/tdcpublication.41.119CrossrefGoogle Scholar

  • [33] McMahon, C.D., Popovic, L., Oldham, J.M., Jeanplong, F., Smith, H.K., Kambadur, R., Sharma, M., Maxwell, L. and Bass, J.J. Myostatin-deficient mice lose more skeletal muscle mass than wild-type controls during hindlimb suspension. Am. J. Physiol. Endocrinol. Metab. 285 (2003) E82–87. Google Scholar

  • [34] Ono, Y., Boldrin, L., Knopp, P., Morgan, J.E. and Zammit, P.S. Muscle satellite cells are a functionally heterogeneous population in both somitederived and branchiomeric muscles. Dev. Biol. 337 (2010) 29–41. http://dx.doi.org/10.1016/j.ydbio.2009.10.005Web of ScienceCrossrefGoogle Scholar

  • [35] Schneider, A.G., Leuthauser, K. and Pette, D. Parathyroid hormone-related protein is rapidly up-regulated in blood vessels of rat skeletal muscle by low-frequency stimulation. Pflugers Arch. 439 (1999) 167–173. http://dx.doi.org/10.1007/s004240051141CrossrefGoogle Scholar

  • [36] Pedraza-Alva, G., Zingg, J.M., Donda, A. and Perez-Martinez, L. Estrogen receptor regulates MyoD gene expression by preventing AP-1-mediated repression. Biochem. Biophys. Res. Commun. 389 (2009) 360–365. http://dx.doi.org/10.1016/j.bbrc.2009.08.153CrossrefWeb of ScienceGoogle Scholar

  • [37] Eason, J.M., Schwartz, G.A., Pavlath, G.K. and English, A.W. Sexually dimorphic expression of myosin heavy chains in the adult mouse masseter. J. Appl. Physiol. 89 (2000) 251–258. Google Scholar

  • [38] McMahon, C.D., Popovic, L., Jeanplong, F., Oldham, J.M., Kirk, S.P., Osepchook, C.C., Wong, K.W., Sharma, M., Kambadur, R. and Bass, J.J. Sexual dimorphism is associated with decreased expression of processed myostatin in males. Am. J. Physiol. Endocrinol. Metab. 284 (2003) E377–381. Google Scholar

  • [39] Gonzalez-Cadavid, N.F. and Bhasin, S. Role of myostatin in metabolism. Curr. Opin. Clin. Nutr. Metab. Care 7 (2004) 451–457. http://dx.doi.org/10.1097/01.mco.0000134365.99523.7fCrossrefGoogle Scholar

  • [40] Gedrange, T., Büttner, C., Schneider, M., Oppitz, R. and Harzer, W. Myosin heavy chain protein and gene expression in the masseter muscle of adult patients with distal or mesial malocclusion. J. Appl. Genet. 46 (2005) 227–236. Google Scholar

About the article

Published Online: 2011-03-26

Published in Print: 2011-06-01


Citation Information: Cellular and Molecular Biology Letters, ISSN (Online) 1689-1392, DOI: https://doi.org/10.2478/s11658-011-0003-2.

Export Citation

© 2011 Versita Warsaw. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

[1]
Alberto Malerba, Jagjeet K Kang, Graham McClorey, Amer F Saleh, Linda Popplewell, Michael J Gait, Matthew JA Wood, and George Dickson
Molecular Therapy - Nucleic Acids, 2012, Volume 1, Page e62
[2]
Alexander Spassov, Tomasz Gredes, Dragan Pavlovic, Tomasz Gedrange, Christian Lehmann, Silke Lucke, and Christiane Kunert-Keil
Archivum Immunologiae et Therapiae Experimentalis, 2012, Volume 60, Number 2, Page 137
[3]
A. Spassov, T. Gredes, C. Lehmann, T. Gedrange, S. Lucke, D. Pavlovic, and C. Kunert-Keil
Journal of Orofacial Orthopedics / Fortschritte der Kieferorthopädie, 2011, Volume 72, Number 6, Page 469

Comments (0)

Please log in or register to comment.
Log in