Estrogen receptor-α and -β and aromatase knockout effects on lower limb muscle mass and contractile function in female mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 296, Issue 4, 2009, Pages

  Brown, Marybeth ^a   Ning, Jie ^a   Ferreira, J Andries ^a   Bogener, Jennifer L ^b   Lubahn, Dennis B ^a,b  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

Author keywords

Fiber area; Muscle mass; Myosin protein; Peak tetanic tension

Indexed keywords

AROMATASE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTRADIOL; MUSCLE PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; GASTROCNEMIUS MUSCLE; KNOCKOUT MOUSE; LEG MUSCLE; LOCOMOTION; MOUSE; MUSCLE CONTRACTION; NONHUMAN; PLANTARIS MUSCLE; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE; TIBIALIS ANTERIOR MUSCLE; ANIMAL; BODY WEIGHT; C57BL MOUSE; DRUG EFFECT; GENETICS; HISTOLOGY; LEG; METABOLISM; MOUSE MUTANT; ORGAN SIZE; PHYSIOLOGY; SKELETAL MUSCLE;

ANIMALS; AROMATASE; BODY WEIGHT; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; LOWER EXTREMITY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUSCLE, SKELETAL; ORGAN SIZE;

EID: 65649133633     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.90696.2008     Document Type: Article

References (52)

1. Bar PR, Amelink GJ, Oldenburg B, Blankenstein MA. Prevention of exercise induced muscle membrane damage by oestradiol. Life Sci 42: 2677-2681, 1988. (Pubitemid 18145974)
2. Brown M, Foley AM, Ferreira JA. Ovariectomy, hind limb unweighting, and recovery effects on skeletal muscle in adult rats. Aviat Space Environ Med 76:1012-1018, 2005. (Pubitemid 41619123)
3. Ciocca DR, Roig LM. Estrogen receptors in human nontarget tissues: biological and clinical implications. Endocr Rev 16: 35-62, 1995.
4. Couse JF, Korach KS. Estrogen receptor null mice: what have we learned, and where will they lead us? Endocr Rev 20: 358-417, 1999.
5. Couse JF, Lindzey J, Grandien K, Gustafsson JA, Korach K. Tissue distribution and quantitative analysis of estrogen receptor-α (ERα) and estrogen receptor-β (ERβ) messenger ribonucleic acid in the wild type and ERa-knockout mouse. Endocrinology 138: 4613-4621, 1997. (Pubitemid 27460895)
6. Couse JF, Curtis Hewitt S, Korach KS. Receptor null mice reveal contrasting roles for estrogen receptor alpha and beta in reproductive tissues. J Steroid Biochem Mol Biol 74: 287-296, 2000. (Pubitemid 32126241)
7. Cooke VE, Carlisle RT, Talbot RT, Boswell T, Mitchell MA. Oestrogen receptor alpha (ERα) and beta (ERβ) in chicken skeletal muscle: mediators of myo-protection? Br Poult Sci 44, Suppl: S12-S13, 2003. (Pubitemid 37399873)
8. Curran EM, Berghaus LJ, Vernetti NJ, Saporita AJ, Lubahn DB, Estes DM. Natural killer cells express estrogen receptor-alpha and estrogen receptor-beta and can respond to estrogen via a non-estrogen receptor-alpha mediated pathway. Cell Immunol 214: 12-20, 2001.
9. Dahlberg E. Characterization of the cytosolic estrogen receptor in rat skeletal muscle. Biochim Biophys Acta 16: 65-75, 1982.
10. Das SK, Taylor JA, Korach KS, Paria BC, Dey SK, Lubahn DB. Estrogenic responses in estrogen receptor-alpha deficient mice reveal a distinct estrogen signaling pathway. Proc Natl Acad Sci USA 94: 12786-12791, 1997.
11. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 127: 4277-4291, 2000.
12. Fisher JS, Hasser EM, Brown M. Effects of ovariectomy and hindlimb unloading on skeletal muscle. J Appl Physiol 85: 1316-1321, 1998. (Pubitemid 28465058)
13. Glenmark B, Nilsson M, Gao H, Gustafsson JA, Wright KD, Westerblad H. Difference in skeletal muscle function in male vs. female: role of estrogen receptor-β. Am J Physiol Endocrinol Metab 287: E1125-E1131, 2004. (Pubitemid 39491954)
14. Gruber CJ, Tschugguel W, Schneeberger C, Huber JC. Production and actions of estrogens. N Engl J Med 356: 340-352, 2002.
15. Hall JM, McDonnell DP. The estrogen receptor β-isoform (ERβ) of the human estrogen receptor modulates ERα transcription activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology 140: 5566-5578, 1999.
16. Heine PA, Taylor JA, Lwamoto GA, Lubahn DB, Cook PS. Increased adipose tissue in male and female estrogen receptor-α knockout mice. Proc Natl Acad Sci USA 97: 12729-12734, 2000.
17. Honda SJ, Harada N, Ito S, Takagi Y, Maeda S. Disruption of sexual behavior in male aromatase deficient mice lacking exons 1 and 2 of the cyp 19 gene. Biochem Biophys Res Commun 252: 445-449, 1998. (Pubitemid 28542906)
18. Ihemelandu EC. Comparison of effect of oestrogen on muscle development of male and female mice. Acta Anat (Basel) 110: 311-317, 1981.
19. Kalbe C, Mau M, Wollenhaupt K, Rehfeldt C. Evidence for estrogen receptor alpha and beta expression in skeletal muscle of pigs. Histochem Cell Biol 127: 95-107, 2007. (Pubitemid 46011324)
20. Kahlert S, Grohe C, Karas RH, Lobbert K, Neyses L, Vetter H. Effects of estrogen on skeletal myoblast growth. Biochem Biophys Res Commun 232: 373-378, 1997. (Pubitemid 27216222)
21. Knutsson A, Glenmark B, Bodin K, Jansson E, Enmark E. Estrogen receptor alpha and beta in human skeletal muscle (Abstract). FASEB J 16: A396, 2002.
22. Kobori M, Yamamuro T. Effects of gonadectomy and estrogen administration on rat skeletal muscle. Clin Orthop 243: 306-311, 1989. (Pubitemid 19165400)
23. Koot RW, Amelink CG, Blankenstein MA, Bar PR. Tamoxifen and oestrogen both protect the rat muscle against physiological damage. J Steroid Biochem Mol Biol 40: 689-695, 1991.
24. Korach KS, Emmen JM, Walker VR, Hewitt SC, Yates M, Hall JM, Swope DL, Harrell JC, Couse JF. Update on animal models developed for analyses of estrogen receptor biological activity. J Steroid Biochem Mol Biol 86: 387-391, 2003. (Pubitemid 37412576)
25. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, Sar M, Korach KS, Gustafsson JA, Smithies O. Generation and reproductive phenotypes of mice lacking estrogen receptor β. Proc Natl Acad Sci USA 95: 15677-15682, 1998. (Pubitemid 29018759)
26. Larionov AA, Vasyliev DA, Mason JI, Howie AF, Bersterin LM, Miller WR. Aromatase in skeletal muscle. J Steroid Biochem Mol Biol 84: 485-492, 2003.
27. Lemoine S, Granier P, Tiffoche C, Berthon PM, Thieulant ML, Carre F, Delamarche P. Effect of endurance training on estrogen receptor alpha expression in different rat skeletal muscle type. Acta Physiol Scand 175: 211-217, 2002.
28. Lemoine S, Granier P, Tiffoche C, Rannou-Bekono F, Thieulant ML, Delamarche P. Estrogen receptor alpha mRNA in human skeletal muscles. Med Sci Sports Exerc 35: 439-443, 2003. (Pubitemid 36278769)
29. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 90: 11162-11166, 1993. (Pubitemid 23354389)
30. MacLean HE, Chiu WSM, Notini AJ, Axell AM, Davey RA, McManus JF, Ma C, Plant DR, Lynch GS, Zajac JD. Impaired skeletal muscle development and function in male, but not female, genomic androgen receptor knockout mice. FASEB J 22: 2676-2689, 2008.
31. McClung JM, Davis JM, Wilson MA, Goldsmith EC, Carson JA. Estrogen status and skeletal muscle recovery from disuse atrophy. J Appl Physiol 100: 2012-2023, 2006.
32. McCormick KM, Burn KL, Piccone CM, Gosselin LE, Brazeau GA. Effects of ovariectomy and estrogen on skeletal muscle function in growing rats. J Muscle Res Cell Motil 25: 21-27, 2003.
33. Moran AL, Nelson SA, Landisch RM, Warren GL, Lowe DA. Estradiol replacement reveres ovariectomy-induced muscle contractile and myosin dysfunction in mature female mice. J Appl Physiol 102: 1387-1392, 2007.
34. Moran AL, Warren GL, Lowe DA. Removal of ovarian hormones from mature mice detrimentally affects muscle contractile function and myosin structural distribution. J Appl Physiol 100: 548-559, 2006.
35. Nilsson S, Gustafsson JA. Estrogen receptor action. Crit Rev Eukaryot Gene Exp 12: 237-257, 2002. (Pubitemid 37051498)
36. Pettersson K, Grandien K, Kuiper GG, Gustafsson JA. Mouse estrogen receptor β forms estrogen response element-binding heterodimers with estrogen receptor α. Mol Endocrinol 11: 1486-1496, 1997. (Pubitemid 27366759)
37. Pfaffl MW, Lange IG, Daxenberger A, Meyer HH. Tissue-specific pattern of estrogen receptors (ER): quantification of ERα and ERβ mRNA with real-time RT-PCR. APMIS 109: 345-355, 2001. (Pubitemid 32640882)
38. Phillips BJ, Ansell PJ, Newton LG, Harada N, Honda S, Ganjam VK, Rottinghaus GE, Welshons WV, Lubahn DB. Estrogen receptor-independent catechol estrogen binding activity: protein binding studies in wild type, estrogen receptor-α KO and aromatase KO tissues. Biochemistry 43: 6698-6708, 2004. (Pubitemid 38701762)
39. Phillips SK, Rook KM, Siddle NC, Bruce SA, Woledge RC. Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy. Clin Sci 84: 95-98, 1993.
40. Santollo J, Wiley MD, Eckel LA. Acute activation of ERα decreases food intake, meals size, and body weight in ovariectomized rats. Am J Physiol Regul Integr Comp Physiol 293: R2194-R2201, 2007. (Pubitemid 350224011)
41. Schiaffino S, Reggiani C. Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev 76: 371-1342, 1996. (Pubitemid 26163713)
42. Simpson ER, Misso M, Hewitt KN, Hill RA, Boon WC, Jones ME, Kovacic A, Zhou J, Clyne CD. Estrogen-the good, the bad, and the unexpected. Endocrine Reviews 26: 322-330, 2005.
43. Sitnick M, Foley AM, Brown M, Spangenburg EE. Ovariectomy prevents the recovery of atrophied gastrocnemius muscle mass. J Appl Physiol 100: 286-293, 2006. (Pubitemid 43671120)
44. Suzuki S, Yamamuro T. Long-term effects of estrogen on rat skeletal muscle. Exp Neurol 87: 291-299, 1985. (Pubitemid 15174402)
45. Swope DL, Korach KS. Estrogen receptor biology and lessons from knockout mice. In: Encylopedia of Hormones, edited by J Henry and A Norman. Riverside, CA: University of California Press, 2003, vol.1, pp. 608-614, 2003.
46. Tayler AH, Al-Azzawi F. Immnunolocalization of estrogen receptor beta in human tissues. J Mol Endocrinol 24: 145-155, 2000. (Pubitemid 30117668)
47. Tiidus PM. Influence of estrogen on skeletal muscle damage, inflammation, and repair. Exerc Sport Sci Rev 31: 40-44, 2003.
48. Trenkle A. The anabolic effect of estrogens on nitrogen metabolism of growing and finishing cattle and sheep. Environ Qual Saf Suppl 5: 79-88, 1976.
49. Vidal O, Lindberg M, Savendahl L, Lubahn DB, Ritzen EM, Gustafsson JA, Ohlsson C. Disproportional body growth in female estrogen receptor-alpha- inactivated mice. Biochem Biophys Res Commun 19: 569-571, 1999.
50. Wiik A, Glenmark B, Ekman M, Esbjörnssoon-Liljedahl M, Johansson O, Bodin K, Enmark E, Jansson E. Oestrogen receptor β is expressed in adult human skeletal muscle both at the mRNA and protein level. Acta Physiol Scand 179: 381-387, 2003. (Pubitemid 38021588)
51. Yakar S, Liu JL, Stannard B, Butler A, Accili D, Sauer B, LeRoith D. Normal growth and development in the absence of hepatic insulin-like growth factor. Proc Natl Acad Sci USA 96: 7324-7329, 1999. (Pubitemid 29299660)
52. Zhang L, Li X, Burghardt R, Smith R III, Safe SH. Role of estrogen receptor (ER) in insulin-like growth factor (IGF)-1-induced responses in MCF-7 breast cancer cells. J Mol Endocrinol 35: 433-437, 2005. (Pubitemid 43025570)