Effect of constitutive inactivation of the myostatin gene on the gain in muscle strength during postnatal growth in two murine models
Amalia Stantzou PhD
Université de Versailles Saint-Quentin, Unité de formation et de recherche des sciences de la santé des sciences, Montigny-le-Bretonneux, France
Search for more papers by this authorVanessa Ueberschlag-Pitiot PhD
Université de Strasbourg, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France
Search for more papers by this authorRemi Thomasson PhD
Université Paris Descartes, Institut de Recherche bio-Médicale et d'Epidémiologie du Sport, Sorbonne Paris Cité, Paris, France
Search for more papers by this authorDenis Furling PhD
Sorbonne Universités CNRS, Centre de Recherche en Myologie, Paris, France
Search for more papers by this authorAnne Bonnieu PhD
INRA, Université Montpellier, Dynamique Musculaire et Métabolisme, Montpellier, France
Search for more papers by this authorHelge Amthor PhD
Université de Versailles Saint-Quentin, Unité de formation et de recherche des sciences de la santé des sciences, Montigny-le-Bretonneux, France
Search for more papers by this authorCorresponding Author
Arnaud Ferry PhD
Sorbonne Universités CNRS, Centre de Recherche en Myologie, Paris, France
Université Paris Descartes, Sorbonne Paris Cité, Paris, France
Correspondence to: A. Ferry; G.H. Pitié-Salpétrière, 47, bld de l'Hôpital, Bâtiment Babinski, Centre de Recherche en myoLogie, 75651 Paris cedex 13, France. e-mail: [email protected]Search for more papers by this authorAmalia Stantzou PhD
Université de Versailles Saint-Quentin, Unité de formation et de recherche des sciences de la santé des sciences, Montigny-le-Bretonneux, France
Search for more papers by this authorVanessa Ueberschlag-Pitiot PhD
Université de Strasbourg, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France
Search for more papers by this authorRemi Thomasson PhD
Université Paris Descartes, Institut de Recherche bio-Médicale et d'Epidémiologie du Sport, Sorbonne Paris Cité, Paris, France
Search for more papers by this authorDenis Furling PhD
Sorbonne Universités CNRS, Centre de Recherche en Myologie, Paris, France
Search for more papers by this authorAnne Bonnieu PhD
INRA, Université Montpellier, Dynamique Musculaire et Métabolisme, Montpellier, France
Search for more papers by this authorHelge Amthor PhD
Université de Versailles Saint-Quentin, Unité de formation et de recherche des sciences de la santé des sciences, Montigny-le-Bretonneux, France
Search for more papers by this authorCorresponding Author
Arnaud Ferry PhD
Sorbonne Universités CNRS, Centre de Recherche en Myologie, Paris, France
Université Paris Descartes, Sorbonne Paris Cité, Paris, France
Correspondence to: A. Ferry; G.H. Pitié-Salpétrière, 47, bld de l'Hôpital, Bâtiment Babinski, Centre de Recherche en myoLogie, 75651 Paris cedex 13, France. e-mail: [email protected]Search for more papers by this authorABSTRACT
Introduction: The effect of constitutive inactivation of the gene encoding myostatin on the gain in muscle performance during postnatal growth has not been well characterized. Methods: We analyzed 2 murine myostatin knockout (KO) models, (i) the Lee model (KOLee) and (ii) the Grobet model (KOGrobet), and measured the contraction of tibialis anterior muscle in situ. Results: Absolute maximal isometric force was increased in 6-month-old KOLee and KOGrobet mice, as compared to wild-type mice. Similarly, absolute maximal power was increased in 6-month-old KOLee mice. In contrast, specific maximal force (relative maximal force per unit of muscle mass was decreased in all 6-month-old male and female KO mice, except in 6-month-old female KOGrobet mice, whereas specific maximal power was reduced only in male KOLee mice. Conclusions: Genetic inactivation of myostatin increases maximal force and power, but in return it reduces muscle quality, particularly in male mice. Muscle Nerve 55: 254–261, 2017
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REFERENCES
- 1McMahon CD, Popovic L, Jeanplong F, Oldham JM, Kirk SP, et al. Sexual dimorphism is associated with decreased expression of processed myostatin in males. Am J Physiol Endocrinol Metab 2003; 284: E377–E381.
- 2McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 1997; 387: 83–90.
- 3Grobet L, Pirottin D, Farnir F, Poncelet D, Royo LJ, Brouwers B, et al. Modulating skeletal muscle mass by postnatal, muscle-specific inactivation of the myostatin gene. Genesis 2003; 35: 227–238.
- 4Mendias CL, Lynch EB, Gumucio JP, Flood MD, Rittman DS, Van Pelt DW, et al. Changes in skeletal muscle and tendon structure and function following genetic inactivation of myostatin in rats. J Physiol 2015; 593: 2037–2052.
- 5Gay S, Jublanc E, Bonnieu A, Bacou F. Myostatin deficiency is associated with an increase in number of total axons and motor axons innervating mouse tibialis anterior muscle. Muscle Nerve 2012; 45: 698704.
- 6Mendias CL, Marcin JE, Calerdon DR, Faulkner JA. Contractile properties of EDL and soleus muscles of myostatin-deficient mice. J Appl Physiol 2006; 101: 898–905.
- 7Schirwis E, Agbulut O, Vadrot N, Mouisel E, Hourde C, Bonnieu A, et al. The beneficial effect of myostatin deficiency on maximal muscle force and power is attenuated with age. Exp Gerontol 2013; 48: 183–190.
- 8Amthor H, Macharia R, Navarrete R, Schuelke M, Brown SC, Otto A, et al. Lack of myostatin results in excessive muscle growth but impaired force generation. Proc Natl Acad Sci U A 2007; 104: 1835–1840.
- 9Gentry BA, Ferreira JA, Phillips CL, Brown M. Hindlimb skeletal muscle function in myostatin-deficient mice. Muscle Nerve 2011; 43: 49–57.
- 10Ploquin C, Chabi B, Fouret G, Vernus B, Feillet-Coudray C, Coudray C, et al. Lack of myostatin alters intermyofibrillar mitochondria activity, unbalances redox status, and impairs tolerance to chronic repetitive contractions in muscle. Am J Physiol Endocrinol Metab 2012; 302: E1000–E1008.
- 11Matsakas A, Macharia R, Otto A, Elashry MI, Mouisel E, Romanello V, et al. Exercise training attenuates the hypermuscular phenotype and restores skeletal muscle function in the myostatin null mouse. Exp Physiol 2012; 97: 125–140.
- 12Pinter O, Beda Z, Csaba Z, Gerendai I. Differences in the onset of puberty in selected inbred mouse strains. Endocr Abstr 2007; 14: 617.
- 13Ferry A, Parlakian A, Joanne P, Fraysse B, Mgrditchian T, Roy P, et al. Mechanical overloading increases maximal force and reduces fragility in hind limb skeletal muscle from Mdx mouse. Am J Pathol 2015; 185: 2012–2224.
- 14Hourde C, Joanne P, Noirez P, Agbulut O, Butler-Browne G, Ferry A. Protective effect of female gender-related factors on muscle force-generating capacity and fragility in the dystrophic mdx mouse. Muscle Nerve 2013; 48: 68–75.
- 15White RB, Bierinx AS, Gnocchi VF, Zammit PS. Dynamics of muscle fibre growth during postnatal mouse development. BMC Dev Biol 2010; 10: 21.
- 16Mendias CL, Kayupov E, Bradley JR, Brooks SV, Claflin DR. Decreased specific force and power production of muscle fibers from myostatin-deficient mice are associated with a suppression of protein degradation. J Appl Physiol 2011; 111: 185–191.
- 17Qaisar R, Renaud G, Morine K, Barton ER, Sweeney HL, Larsson L. Is functional hypertrophy and specific force coupled with the addition of myonuclei at the single muscle fiber level? FASEB J 2012; 26: 1077–1085.
- 18Bodnar D, Geyer N, Ruzsnavszky O, Olah T, Hegyi B, Sztretye M, et al. Hypermuscular mice with mutation in the myostatin gene display altered calcium signalling. J Physiol 2014; 592(Pt 6): 1353–1365.
- 19Mouisel E, Relizani K, Mille-Hamard L, Denis R, Hourdé C, Agbulut O, et al. Myostatin is a key mediator between energy metabolism and endurance capacity of skeletal muscle. Am J Physiol Regul Integr Comp Physiol 2014; 307: R444–R454.
- 20James RS, Altringham JD, Goldspink DF. The mechanical properties of fast and slow skeletal muscles of the mouse in relation to their locomotory function. J Exp Biol 1995; 198(Pt 2): 491–502.
- 21Chambon C, Duteil D, Vignaud A, Ferry A, Messaddeq N, Malivindi R, et al. Myocytic androgen receptor controls the strength but not the mass of limb muscles. Proc Natl Acad Sci U S A 2010; 107: 14327–14332.
- 22Greising SM, Carey RS, Blackford JE, Dalton LE, Kosir AM, Lowe DA. Estradiol treatment, physical activity, and muscle function in ovarian-senescent mice. Exp Gerontol 2011; 46: 685–693.
- 23Hourde C, Jagerschmidt C, Clement-Lacroix P, Vignaud A, Ammann P, Butler-Browne GS, et al. Androgen replacement therapy improves function in male rat muscles independently of hypertrophy and activation of the Akt/mTOR pathway. Acta Physiol 2009; 195: 471–482.
- 24Braga M, Bhasin S, Jasuja R, Pervin S, Singh R. Testosterone inhibits transforming growth factor-beta signaling during myogenic differentiation and proliferation of mouse satellite cells: potential role of follistatin in mediating testosterone action. Mol Cell Endocrinol 2013; 350: 39–52.
- 25Dubois V, Laurent M, Boonen S, Vanderschueren D, Claessens F. Androgens and skeletal muscle: cellular and molecular action mechanisms underlying the anabolic actions. Cell Mol Life Sci 2013; 69: 1651–1667.
- 26Mendler L, Baka Z, Kovacs-Simon A, Dux L. Androgens negatively regulate myostatin expression in an androgen-dependent skeletal muscle. Biochem Biophys Res Commun 2007; 361: 237–242.