Hormone replacement therapy improves contractile function and myonuclear organization of single muscle fibres from postmenopausal monozygotic female twin pairs

Journal of Physiology

Volumn 591, Issue 9, 2013, Pages 2333-2344

  Qaisar, Rizwan ^a   Renaud, Guillaume ^a   Hedstrom, Yvette ^a   Pöllänen, Eija ^b   Ronkainen, Paula ^b   Kaprio, Jaakko ^d   Alen, Markku ^c   Sipilä, Sarianna ^b   Artemenko, Konstantin ^e   Bergquist, Jonas ^e   Kovanen, Vuokko ^b   Larsson, Lars ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^c OULU UNIVERSITY HOSPITAL   (Finland)

^d NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^e UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; MYOSIN HEAVY CHAIN; MYOSIN HEAVY CHAIN I; MYOSIN HEAVY CHAIN IIA; PROGESTERONE; UNCLASSIFIED DRUG;

ACTIN MYOSIN INTERACTION; ADULT; ARTICLE; CELL NUCLEUS; CELL SIZE; CELL SPECIFICITY; CELLULAR PARAMETERS; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; CYTOPLASMIC VOLUME; FAST MUSCLE; FEMALE; HORMONE SUBSTITUTION; HUMAN; HUMAN CELL; HUMAN TISSUE; MENOPAUSAL SYNDROME; METABOLIC REGULATION; MONOZYGOTIC TWINS; MUSCLE BIOPSY; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE RIGIDITY; MUSCLE STRENGTH; MYONUCLEAR DOMAIN SIZE; POSTMENOPAUSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; SLOW MUSCLE; TREATMENT DURATION;

AGED; AGED, 80 AND OVER; BODY COMPOSITION; CELL NUCLEUS; ESTRADIOL; FEMALE; HORMONE REPLACEMENT THERAPY; HUMANS; MALE; MIDDLE AGED; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; MYOSIN HEAVY CHAINS; POSTMENOPAUSE; PROGESTERONE; PROTEIN ISOFORMS; TWINS, MONOZYGOTIC;

EID: 84876963858     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.250092     Document Type: Article

References (51)

1. Ahtiainen M, Pollanen E, Ronkainen PH, Alen M, Puolakka J, Kaprio J, Sipila S & Kovanen V (2012). Age and estrogen- based hormone therapy affect systemic and local IL-6 and IGF-1 pathways in women. Age (Dordr) 34, 1249-1260.
2. Armel TZ & Leinwand LA (2010). Mutations at the same amino acid in myosin that cause either skeletal or cardiac myopathy have distinct molecular phenotypes. J Mol Cell Cardiol 48, 1007-1013.
3. Artemenko KA, Bergstrom Lind S, Elfineh L, Mayrhofer C, Zubarev RA, Bergquist J & Pettersson U (2011). Optimization of immunoaffinity enrichment and detection: toward a comprehensive characterization of the phosphotyrosine proteome of K562 cells by liquid chromatography-mass spectrometry. Analyst 136, 1971-1978.
4. Broome CS, Kayani AC, Palomero J, Dillmann WH, Mestril R, Jackson MJ & McArdle A (2006). Effect of lifelong overexpression of HSP70 in skeletal muscle on age-related oxidative stress and adaptation after nondamaging contractile activity. FASEB J 20, 1549-1551.
5. Cristea A, Qaisar R, Edlund PK, Lindblad J, Bengtsson E & Larsson L (2010). Effects of aging and gender on the spatial organization of nuclei in single human skeletal muscle cells. Aging Cell 9, 685-697.
6. Dieli-Conwright CM, Spektor TM, Rice JC, Sattler FR & Schroeder ET (2009a). Hormone therapy attenuates exercise-induced skeletal muscle damage in postmenopausal women. J Appl Physiol 107, 853-858.
7. Dieli-Conwright CM, Spektor TM, Rice JC, Sattler FR & Schroeder ET (2009b). Influence of hormone replacement therapy on eccentric exercise induced myogenic gene expression in postmenopausal women. J Appl Physiol 107, 1381-1388.
8. Edman KA (1979). The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres. J Physiol 291, 143-159.
9. Enns DL, Iqbal S & Tiidus PM (2008). Oestrogen receptors mediate oestrogen-induced increases in post-exercise rat skeletal muscle satellite cells. Acta Physiol (Oxf) 194, 81-93.
10. Fabiato A & Fabiato F (1979). Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J Physiol (Paris) 75, 463-505.
11. Finni T, Noorkoiv M, Pollanen E, Ronkainen PH, Alen M, Kaprio J, Kovanen V & Sipila S (2011). Muscle function in monozygotic female twin pairs discordant for hormone replacement therapy. Muscle Nerve 44, 769-775.
12. Frontera WR, Hughes VA, Fielding RA, Fiatarone MA, Evans WJ & Roubenoff R (2000). Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol 88, 1321-1326.
13. Frontera WR, Hughes VA, Lutz KJ & Evans WJ (1991). A cross-sectional study of muscle strength and mass in 45- to 78-yr-old men and women. J Appl Physiol 71, 644-650.
14. Frontera WR & Larsson L (1997). Contractile studies of single human skeletal muscle fibers: a comparison of different muscles, permeabilization procedures, and storage techniques. Muscle Nerve 20, 948-952.
15. Greising SM, Baltgalvis KA, Lowe DA & Warren GL (2009). Hormone therapy and skeletal muscle strength: a meta-analysis. J Gerontol A Biol Sci Med Sci 64, 1071-1081.
16. Habets PE, Franco D, Ruijter JM, Sargeant AJ, Pereira JA & Moorman AF (1999). RNA content differs in slow and fast muscle fibers: implications for interpretation of changes in muscle gene expression. J Histochem Cytochem 47, 995-1004.
17. Korhonen MT, Cristea A, Alen M, Hakkinen K, Sipila S, Mero A, Viitasalo JT, Larsson L & Suominen H (2006). Aging, muscle fiber type, and contractile function in sprint-trained athletes. J Appl Physiol 101, 906-917.
18. Larsson L (1978). Morphological and functional characteristics of the ageing skeletal muscle in man. A cross-sectional study. Acta Physiol Scand Suppl 457, 1-36.
19. Larsson L (1982). Physical training effects on muscle morphology in sedentary males at different ages. Med Sci Sports Exerc 14, 203-206.
20. Larsson L, Li X, Yu F & Degens H (1997). Age-related changes in contractile properties and expression of myosin isoforms in single skeletal muscle cells. Muscle Nerve Suppl 5, S74-78.
21. Larsson L & Moss RL (1993). Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles. J Physiol 472, 595-614.
22. Larsson L, Sjodin B & Karlsson J (1978). Histochemical and biochemical changes in human skeletal muscle with age in sedentary males, age 22-65 years. Acta Physiol Scand 103, 31-39.
23. Lemoine S, Granier P, Tiffoche C, Berthon PM, Rannou-Bekono F, Thieulant ML, Carre F & Delamarche P (2002). Effect of endurance training on oestrogen receptor alpha transcripts in rat skeletal muscle. Acta Physiol Scand 174, 283-289.
24. Li M & Larsson L (2010). Force-generating capacity of human myosin isoforms extracted from single muscle fibre segments. J Physiol 588, 5105-5114.
25. Lowe DA, Baltgalvis KA & Greising SM (2010). Mechanisms behind estrogen's beneficial effect on muscle strength in females. Exerc Sport Sci Rev 38, 61-67.
26. Lowe DA, Surek JT, Thomas DD & Thompson LV (2001). Electron paramagnetic resonance reveals age-related myosin structural changes in rat skeletal muscle fibers. Am J Physiol Cell Physiol 280, C540-C547.
27. Lowe DA, Warren GL, Snow LM, Thompson LV & Thomas DD (2004). Muscle activity and aging affect myosin structural distribution and force generation in rat fibers. J Appl Physiol 96, 498-506.
28. McArdle A, Vasilaki A & Jackson M (2002). Exercise and skeletal muscle ageing: cellular and molecular mechanisms. Ageing Res Rev 1, 79-93.
29. McDonald KS & Fitts RH (1995). Effect of hindlimb unloading on rat soleus fiber force, stiffness, and calcium sensitivity. J Appl Physiol 79, 1796-1802.
30. 2+ activation in cardiac muscle. Biophys J 92, 4379-4390.
31. Medler S (2002). Comparative trends in shortening velocity and force production in skeletal muscles. Am J Physiol Regul Integr Comp Physiol 283, R368-R378.
32. Meeuwsen IB, Samson MM & Verhaar HJ (2000). Evaluation of the applicability of HRT as a preservative of muscle strength in women. Maturitas 36, 49-61.
33. Meredith C, Herrmann R, Parry C, Liyanage K, Dye DE, Durling HJ, Duff RM, Beckman K, de Visser M, van der Graaff MM, Hedera P, Fink JK, Petty EM, Lamont P, Fabian V, Bridges L, Voit T, Mastaglia FL & Laing NG (2004). Mutations in the slow skeletal muscle fiber myosin heavy chain gene (MYH7) cause Laing early-onset distal myopathy (MPD1). Am J Hum Genet 75, 703-708.
34. Moran AL, Nelson SA, Landisch RM, Warren GL & Lowe DA (2007). Estradiol replacement reverses ovariectomy-induced muscle contractile and myosin dysfunction in mature female mice. J Appl Physiol 102, 1387-1393.
35. Moss RL (1979). Sarcomere length-tension relations of frog skinned muscle fibres during calcium activation at short lengths. J Physiol 292, 177-192.
36. Onambele-Pearson GL (2009). HRT affects skeletal muscle contractile characteristics: a definitive answer J Appl Physiol 107, 4-5.
37. Persky AM, Green PS, Stubley L, Howell CO, Zaulyanov L, Brazeau GA & Simpkins JW (2000). Protective effect of estrogens against oxidative damage to heart and skeletal muscle in vivo and in vitro. Proc Soc Exp Biol Med 223, 59-66.
38. Phillips SK, Rook KM, Siddle NC, Bruce SA & Woledge RC (1993). Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy. Clin Sci (Lond) 84, 95-98.
39. Pöllänen E, Ronkainen PH, Suominen H, Takala T, Koskinen S, Puolakka J, Sipilä S, Kovanen V (2007). Muscular transcriptome in postmenopausal women with or without hormone replacement. Rejuvenation Res 10, 485-500.
40. Qaisar R, Renaud G, Morine K, Barton ER, Sweeney HL & Larsson L (2012). Is functional hypertrophy and specific force coupled with the addition of myonuclei at the single muscle fiber level FASEB J 26, 1077-1085.
41. Regnier M, Martin H, Barsotti RJ, Rivera AJ, Martyn DA & Clemmens E (2004). Cross-bridge versus thin filament contributions to the level and rate of force development in cardiac muscle. Biophys J 87, 1815-1824.
42. Ronkainen PH, Kovanen V, Alen M, Pollanen E, Palonen EM, Ankarberg-Lindgren C, Hamalainen E, Turpeinen U, Kujala UM, Puolakka J, Kaprio J & Sipila S (2009). Postmenopausal hormone replacement therapy modifies skeletal muscle composition and function: a study with monozygotic twin pairs. J Appl Physiol 107, 25-33.
43. Ronkainen PH, Pollanen E, Alen M, Pitkanen R, Puolakka J, Kujala UM, Kaprio J, Sipila S & Kovanen V (2010). Global gene expression profiles in skeletal muscle of monozygotic female twins discordant for hormone replacement therapy. Aging Cell 9, 1098-1110.
44. Ryall JG, Schertzer JD & Lynch GS (2008). Cellular and molecular mechanisms underlying age-related skeletal muscle wasting and weakness. Biogerontology 9, 213-228.
45. Saartok T (1984). Steroid receptors in two types of rabbit skeletal muscle. Int J Sports Med 5, 130-136.
46. Sipila S, Taaffe DR, Cheng S, Puolakka J, Toivanen J & Suominen H (2001). Effects of hormone replacement therapy and high-impact physical exercise on skeletal muscle in post-menopausal women: a randomized placebo-controlled study. Clin Sci (Lond) 101, 147-157.
47. Skelton DA, Phillips SK, Bruce SA, Naylor CH & Woledge RC (1999). Hormone replacement therapy increases isometric muscle strength of adductor pollicis in post-menopausal women. Clin Sci (Lond) 96, 357-364.
48. Tajsharghi H, Darin N, Rekabdar E, Kyllerman M, Wahlstrom J, Martinsson T & Oldfors A (2005). Mutations and sequence variation in the human myosin heavy chain IIa gene (MYH2). Eur J Hum Genet 13, 617-622.
49. Tomonaga M (1977). Histochemical and ultrastructural changes in senile human skeletal muscle. J Am Geriatr Soc 25, 125-131.
50. Widrick JJ, Maddalozzo GF, Lewis D, Valentine BA, Garner DP, Stelzer JE, Shoepe TC & Snow CM (2003). Morphological and functional characteristics of skeletal muscle fibers from hormone-replaced and nonreplaced postmenopausal women. J Gerontol A Biol Sci Med Sci 58, 3-10.
51. Yu F, Hedstrom M, Cristea A, Dalen N & Larsson L (2007). Effects of ageing and gender on contractile properties in human skeletal muscle and single fibres. Acta Physiol (Oxf) 190, 229-241.