A cellular memory mechanism aids overload hypertrophy in muscle long after an episodic exposure to anabolic steroids

Journal of Physiology

Volumn 591, Issue 24, 2013, Pages 6221-6230

  Egner, Ingrid M ^a   Bruusgaard, Jo C ^a,b   Eftestøl, Einar ^a   Gundersen, Kristian ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b Atlantis Medical College   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

TESTOSTERONE PROPIONATE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL COUNT; CELL FUNCTION; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG EXPOSURE; EX VIVO STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOLECULAR IMAGING; MOTOR PERFORMANCE; MOUSE; MUSCLE CELL; MUSCLE HYPERTROPHY; MUSCLE MASS; MUSCLE STRENGTH; MUSCLE TRAINING; NONHUMAN; PHYSICAL INACTIVITY; PRIORITY JOURNAL; SENESCENCE;

ANIMALS; CELL NUCLEUS; FEMALE; HYPERTROPHY; MICE; MUSCLE FIBERS, SKELETAL; PHYSICAL EXERTION; TESTOSTERONE;

EID: 84890799306     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.264457     Document Type: Article

References (62)

1. Allen DL, Monke SR, Talmadge RJ, Roy RR & Edgerton VR (1995). Plasticity of myonuclear number in hypertrophied and atrophied mammalian skeletal muscle fibers. J Appl Physiol 78, 1969-1976.
2. Aloisi M, Mussini I & Schiaffino S (1973). Activation of muscle nuclei in denervation and hypertrophy. In Basic Research in Myology, pp. 338-345. Excerpta Medica, Amsterdam.
3. Alway SE, Degens H, Krishnamurthy G & Smith CA (2002). Potential role for Id myogenic repressors in apoptosis and attenuation of hypertrophy in muscles of aged rats. Am J Physiol Cell Physiol 283, C66-C76.
4. Amthor H, Macharia R, Navarrete R, Schuelke M, Brown SC, Otto A, Voit T, Muntoni F, Vrbova G, Partridge T, Zammit P, Bunger L & Patel K (2007). Lack of myostatin results in excessive muscle growth but impaired force generation. Proc Natl Acad Sci U S A 104, 1835-1840.
5. Amthor H, Otto A, Vulin A, Rochat A, Dumonceaux J, Garcia L, Mouisel E, Hourde C, Macharia R, Friedrichs M, Relaix F, Zammit PS, Matsakas A, Patel K & Partridge T (2009). Muscle hypertrophy driven by myostatin blockade does not require stem/precursor-cell activity. Proc Natl Acad Sci U S A 106, 7479-7484.
6. Aravamudan B, Mantilla CB, Zhan WZ & Sieck GC (2006). Denervation effects on myonuclear domain size of rat diaphragm fibers. J Appl Physiol 100, 1617-1622.
7. Balice-Gordon RJ & Lichtman JW (1994). Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372, 519-524.
8. Barton-Davis ER, Shoturma DI & Sweeney HL (1999). Contribution of satellite cells to IGF-I induced hypertrophy of skeletal muscle. Acta Physiol Scand 167, 301-305.
9. Bhasin S, Storer TW, Berman N, Callegari C, Clevenger B, Phillips J, Bunnell TJ, Tricker R, Shirazi A & Casaburi R (1996). The effects of supraphysiologic doses of testosterone on muscle size and strength in normal men. N Eng J Med 335, 1-7.
10. Blaauw B, Canato M, Agatea L, Toniolo L, Mammucari C, Masiero E, Abraham R, Sandri M, Schiaffino S & Reggiani C (2009). Inducible activation of Akt increases skeletal muscle mass and force without satellite cell activation. FASEB J 23, 3896-3905.
11. Bruusgaard JC, Brack AS, Hughes SM & Gundersen K (2005). Muscle hypertrophy induced by the Ski protein: cyto-architecture and ultrastructure. Acta Physiol Scand 185, 141-149.
12. Bruusgaard JC, Egner IM, Larsen TK, Dupre-Aucouturier S, Desplanches D & Gundersen K (2012). No change in myonuclear number during muscle unloading and reloading. J App Physiol 113, 290-296.
13. Bruusgaard JC & Gundersen K (2008). In vivo time-lapse microscopy reveals no loss of murine myonuclei during weeks of muscle atrophy. J Clin Invest 118, 1450-1457.
14. Bruusgaard JC, Johansen IB, Egner IM, Rana ZA & Gundersen K (2010). Myonuclei acquired by overload exercise precede hypertrophy and are not lost on detraining. Proc Natl Acad Sci U S A 107, 15111-15116.
15. Bruusgaard JC, Liestol K, Ekmark M, Kollstad K & Gundersen K (2003). Number and spatial distribution of nuclei in the muscle fibres of normal mice studied in vivo. J Physiol 551, 467-478.
16. Bruusgaard JC, Liestol K & Gundersen K (2006). Distribution of myonuclei and microtubules in live muscle fibers of young, middle-aged, and old mice. J Appl Physiol 100, 2024-2030.
17. Cabric M, Appell HJ & Resic A (1987). Effects of electrical stimulation of different frequencies on the myonuclei and fibre size in human muscle. Int J Sports Med 8, 323-326.
18. Cabric M & James NT (1983). Morphometric analyses on the muscles of exercise trained and untrained dogs. Am J Anat 166, 359-368.
19. Carson JA, Yamaguchi M & Alway SE (1995). Hypertrophy and proliferation of skeletal muscle fibers from aged quail. J Appl Physiol 78, 293-299.
20. Cheek DB, Holt AB, Hill DE & Talbert JL (1971). Skeletal muscle cell mass and growth: the concept of the deoxyribonucleic acid unit. Pediat Res 5, 312-328.
21. Conboy IM, Conboy MJ, Smythe GM & Rando TA (2003). Notch-mediated restoration of regenerative potential to aged muscle. Science 302, 1575-1577.
22. Conboy IM & Rando TA (2005). Aging, stem cells and tissue regeneration: lessons from muscle. Cell Cycle 4, 407-410.
23. Dutta C & Hadley EC (1995). The significance of sarcopenia in old age. J Gerontol A Biol Sci Med Sci 50 Spec No, 1-4.
24. Enesco M & Puddy D (1964). Increase in the number of nuclei and weight in skeletal muscle of rats of various ages. Am J Anat 114.
25. Eriksson A, Kadi F, Malm C & Thornell LE (2005). Skeletal muscle morphology in power-lifters with and without anabolic steroids. Histochem Cell Biol 124, 167-175.
26. Giddings CJ & Gonyea WJ (1992). Morphological observations supporting muscle fibre hyperplasia following weight-lifting exercise in cats. Anat Rec 233, 178-195.
27. Goldberg AL (1967). Protein synthesis in tonic and phasic skeletal muscles. Nature 216, 1219-1220.
28. Gundersen K & Bruusgaard JC (2008). Nuclear domains during muscle atrophy: nuclei lost or paradigm lost J Physiol 586, 2675-2681.
29. Hall ZW & Ralston E (1989). Nuclear domains in muscle cells. Cell 59, 771-772.
30. Hughes SM & Schiaffino S (1999). Control of muscle fibre size: a crucial factor in ageing. Acta Physiol Scand 167, 307-312.
31. Jackson J, Mula J, Kirby T, Fry C, Lee J, Ubele M, Campbell K, McCarthy J, Peterson C & Dupont Versteegden E (2012a). Satellite cell depletion does not inhibit adult skeletal muscle regrowth following unloading-induced atrophy. Am J Physiol Cell Physiol 303, C854-C861.
32. Jackson JR, Mula J, Kirby TJ, Fry CS, Lee JD, Ubele MF, Campbell KS, McCarthy JJ, Peterson CA & Dupont-Versteegden EE (2012b). Satellite cell depletion does not inhibit adult skeletal muscle regrowth following unloading-induced atrophy. Am J Physiol Cell Physiol 303, C854-C861.
33. Kadi F (2008). Cellular and molecular mechanisms responsible for the action of testosterone on human skeletal muscle. A basis for illegal performance enhancement. Br J Pharmacol 154, 522-528.
34. Kadi F, Eriksson A, Holmner S, Butler-Browne GS & Thornell LE (1999). Cellular adaptation of the trapezius muscle in strength-trained athletes. Histochem Cell Biol 111, 189-195.
35. Kelly FJ, Lewis SE, Anderson P & Goldspink DF (1984). Pre- and postnatal growth and protein turnover in four muscles of the rat. Muscle Nerve 7, 235-242.
36. Lhrke H, Hesse B & Goerttler K (1984). Spontaneous tumors and lifespan of female NMRI mice of the outbred stock Sut:NMRT during a lifetime study. J Cancer Res Clin Onc 108, 192-196.
37. Lunde I, Anton S, Bruusgaard J, Rana Z, Ellefsen S & Gundersen K (2011). Hypoxia inducible factor 1 links fast-patterned muscle activity and fast muscle phenotype in rats. J Physiol 589, 1443-1454.
38. McCall GE, Allen DL, Linderman JK, Grindeland RE, Roy RR, Mukku VR & Edgerton VR (1998). Maintenance of myonuclear domain size in rat soleus after overload and growth hormone/IGF-I treatment. J Appl Physiol 84, 1407-1412.
39. McCarthy JJ, Mula J, Miyazaki M, Erfani R, Garrison K, Farooqui AB, Srikuea R, Lawson BA, Grimes B, Keller C, Van Zant G, Campbell KS, Esser KA, Dupont-Versteegden EE & Peterson CA (2011). Effective fibre hypertrophy in satellite cell-depleted skeletal muscle. Development 138, 3657-3666.
40. Matthews GD, Huang CL, Sun L & Zaidi M (2011). Translational musculoskeletal science: is sarcopenia the next clinical target after osteoporosis Ann N Y Acad Sci 1237, 95-105.
41. Mendias CL, Kayupov E, Bradley JR, Brooks SV & Claflin DR (2011). Decreased specific force and power production of muscle fibers from myostatin-deficient mice are associated with a suppression of protein degradation. J Appl Physiol 111, 185-191.
42. Metzger T, Gache V, Xu M, Cadot B & Folker E (2012). MAP and kinesin-dependent nuclear positioning is required for skeletal muscle function. Nature 484, 120.
43. Moss FP (1968). The relationship between the dimensions of the fibers and the number of nuclei during normal growth of skeletal muscle in the domestic fowl. Am J Anat 122, 555-564.
44. Pavlath GK, Rich K, Webster SG & Blau HM (1989). Localization of muscle gene products in nuclear domains. Nature 337, 570-573.
45. Puckelwartz M & McNally EM (2011). Emery-Drefuss muscular dystrophy. Handb Clin Neurol 101, 156-166.
46. Qaisar R, Renaud G, Morine K, Barton E, Sweeney HL & Larsson L (2012). Is functional hypertrophy and specific force coupled with the addition of myonuclei at the single muscle fibre level FASEB J 26, 1077-1085.
47. Raffaello A, Milan G, Masiero E, Carnio S, Lee D, Lanfranchi G, Goldberg AL & Sandri M (2010). JunB transcription factor maintains skeletal muscle mass and promotes hypertrophy. J Cell Biol 191, 101-113.
48. Roy RR, Monke SR, Allen DL & Edgerton VR (1999). Modulation of myonuclear number in functionally overloaded and exercised rat plantaris fibers. J Appl Physiol 87, 634-642.
49. Rutherford OM & Jones DA (1986). The role of learning and coordination in strength training. Eur J Appl Physiol Occup Physiol 55, 100-105.
50. Schiaffino S, Bormioli SP & Aloisi M (1976). The fate of newly formed satellite cells during compensatory muscle hypertrophy. Virchows Archiv B, Cell pathology 21, 113-118.
51. Schiaffino S, Dyar KA, Ciciliot S, Blaauw B & Sandri M (2013). Mechanisms regulating skeletal muscle growth and atrophy. FEBS J 280, 4294-4314.
52. Schultz E & Lipton BH (1982). Skeletal muscle satellite cells: changes in proliferation potential as a function of age. Mech Ageing Dev 20, 377-383.
53. Seiden D (1976). Quantitative analysis of muscle cell changes in compensatory hypertrophy and work-induced hypertrophy. Am J Anat 145, 459-465.
54. Smith K, Winegard K, Hicks AL & McCartney N (2003). Two years of resistance training in older men and women: the effects of three years of detraining on the retention of dynamic strength. Can J Appl Physiol 28, 462-474.
55. Staron RS, Leonardi MJ, Karapondo DL, Malicky ES, Falkel JE, Hagerman FC & Hikida RS (1991). Strength and skeletal muscle adaptations in heavy-resistance-trained women after detraining and retraining. J Appl Physiol 70, 631-640.
56. Taaffe DR & Marcus R (1997). Dynamic muscle strength alterations to detraining and retraining in elderly men. Clin Physiol 17, 311-324.
57. Utvik JK, Njå A & Gundersen K (1999). DNA injection into single cells of intact mice. Hum Gene Ther 10.
58. van der Meer SFT, Jaspers R, Jones D & Degens H (2011). Time-course of changes in the myonuclear domain during denervation in young-adult and old rat gastrocnemius muscle. Muscle Nerve 43, 212-222.
59. WADA (2009). World anti-doping code. World Anti-Doping Agency, Montreal, Canada.
60. Wada KI, Takahashi H, Katsuta S & Soya H (2002). No decrease in myonuclear number after long-term denervation in mature mice. Am J Physiol Cell Physiol 283, C484-C488.
61. Wang Y & Rudnicki M (2012). Satellite cells, the engines of muscle repair. Nature Rev Mol Cell Biol 13, 127-133.
62. Winchester PK & Gonyea WJ (1992). A quantitative study of satellite cells and myonuclei in stretched avian slow tonic muscle. Anat Rec 232, 369-377.