Aberrant expression of myosin isoforms in skeletal muscles from mice lacking the rev-erbAα orphan receptor gene

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 288, Issue 2 57-2, 2005, Pages

  Pircher, P ^a,d   Chomez, P ^b,e   Yu, F ^a   Vennstrom B ^b   Larsson, L ^a,c  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^d EXELIXIS INC   (United States)

^e GSK   (Belgium)

Author keywords

Fast and slow twitch muscle; Orphan nuclear receptors; Thyroid hormone

Indexed keywords

CELL NUCLEUS RECEPTOR; MYOSIN HEAVY CHAIN; PROTEIN REV ERBAALPHA; STEROID RECEPTOR; THYROID HORMONE RECEPTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EXTENSOR DIGITORUM LONGUS MUSCLE; FAST MUSCLE; KNOCKOUT GENE; MOUSE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SKELETAL MUSCLE; SLOW MUSCLE; SOLEUS MUSCLE; TISSUE DISTRIBUTION; WILD TYPE;

ANIMALS; DNA-BINDING PROTEINS; GENE EXPRESSION; MICE; MICE, KNOCKOUT; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE, SKELETAL; MYOSINS; PROTEIN ISOFORMS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; THYROID HORMONE RECEPTORS ALPHA;

EID: 12344276511     PISSN: 03636119     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpregu.00690.2003     Document Type: Article

References (54)

1. Adams GR, Haddad F, and Baldwin KM. The interaction of space flight and thyroid state on somatic and skeletal muscle growth and myosin heavy chain expression on neonatal rodents. J Gravit Physiol 7: P15-18, 2000.
2. Baldwin KM, Caiozzo VJ, and Haddad F. Interactive effects of loading and thyroid states on skeletal isomyosins. Int J Sports Med 18, Suppl 4: S296-S298, 1997.
3. Barany M. ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol Suppl 50: 197-218, 1967.
4. Caiozzo VJ, Baker MJ, and Baldwin KM. Novel transitions in MHC isoforms: separate and combined effects of thyroid hormone and mechanical unloading. J Appl Physiol 85: 2237-2248, 1998.
5. Carnac G, Albagli-Curiel O, Vandromme M, Pinset C, Montarras D, Laudet V, and Bonnieu A. 3,5,3′-Triiodothyronine positively regulates both MyoD1 gene transcription and terminal differentiation in C2 myoblasts. Mol Endocrinol 6: 1185-1194, 1992.
6. Chomez P, Neveu I, Mansen A, Kiesler E, Larsson L, Vennstrom B, and Arenas E. Increased cell death and delayed development in the cerebellum of mice lacking the rev-erbAα orphan receptor. Development 127: 1489-1498, 2000.
7. d'Albis M and Butler-Browne G. The hormonal control of myosin isoform expression in skeletal muscle of mammals: a review. Basic Appl Myol 3: 7-16, 1993.
8. Downes M, Carozzi AJ, and Muscat GE. Constitutive expression of the orphan receptor, Rev-erbA alpha, inhibits muscle differentiation and abrogates the expression of the myoD gene family. Mol Endocrinol 9: 1666-1678, 1995.
9. Edstrom L and Larsson L. Effects of age on contractile and enzyme-histochemical properties of fast- and slow-twitch single motor units in the rat. J Physiol 392: 129-145, 1987.
10. Fitzsimons DP, Herrick RE, and Baldwin KM. Isomyosin distributions in rodent muscles: effects of altered thyroid state. J Appl Physiol 69: 321-327, 1990.
11. Forman BM, Chen J, Blumberg B, Kliewer SA, Henshaw R, Ong ES, and Evans RM. Cross-talk among ROR alpha 1 and the Rev-erb family of orphan nuclear receptors. Mol Endocrinol 8: 1253-1261, 1994.
12. Giulian GG, Moss RL, and Greaser M. Improved methodology for analysis and quantitation of proteins on one- dimensional silver-stained slab gels. Anal Biochem 129: 277-287, 1983.
13. Gullberg H, Rudling M, Salto C, Forrest D, Angelin B, and Vennstrom B. Requirement for thyroid hormone receptor beta in T3 regulation of cholesterol metabolism in mice. Mol Endocrinol 16: 1767-1777, 2002.
14. Haddad F, Arnold C, Zeng M, and Baldwin K. Interaction of thyroid state and denervation on skeletal myosin heavy chain expression. Muscle Nerve 20: 1487-1496, 1997.
15. Hamalainen N and Pette D. Expression of an α-cardiac like myosin heavy chain in diaphragm, chronically stimulated, and denervated fast-twitch muscles of rabbit. J Muscle Res Cell Motil 18: 401-411, 1997.
16. Hamilton MT and Booth FW. Skeletal muscle adaptation to exercise: a century of progress. J Appl Physiol 88: 327-331, 2000.
17. Hughes SM, Cho M, Karsch-Mizrachi I, Travis M, Silberstein L, Leinwand LA, and Blau HM. Three slow myosin heavy chains sequentially expressed in developing mammalian skeletal muscle. Dev Biol 158: 183-199, 1993.
18. Hughes SM, Taylor JM, Tapscott SJ, Gurley CM, Carter WJ, and Peterson CA. Selective accumulation of MyoD and myogenin mRNAs in fast and slow adult skeletal muscle is controlled by innervation and hormones. Development 118: 1137-1147, 1993.
19. Ianuzzo D, Patel P, Chen V, O'Brien P, and Williams C. Thyroidal trophic influence on skeletal muscle myosin. Nature 270: 74-76, 1977.
20. Izumo S, Nadal-Ginard B, and Mahdavi V. All members of the MHC multigene family respond to thyroid hormone in a highly tissue-specific manner. Science 231: 597-600, 1986.
21. Koenig RJ, Lazar MA, Hodin RA, Brent GA, Larsen PR, Chin WW, and Moore DD. Inhibition of thyroid hormone action by a non-hormone binding c-erbA protein generated by alternative mRNA splicing. Nature 337: 659-661, 1989.
22. Ladias JA and Karathanasis SK. Regulation of the apolipoprotein AI gene by ARP-1, a novel member of the steroid receptor superfamily. Science 251: 561-565, 1991.
23. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685, 1970.
24. Larsson L and Edstrom L. Effects of age on enzyme-histochemical fibre spectra and contractile properties of fast- and slow-twitch skeletal muscles in the rat. J Neurol Sci 76: 69-89, 1986.
25. Larsson L, Li X, Teresi A, and Salviati G. Effects of thyroid hormone on fast- and slow-twitch skeletal muscles in young and old rats. J Physiol 481: 149-161, 1994.
26. Larsson L, Muller U, Li X, and Schiaffino S. Thyroid hormone regulation of myosin heavy chain isoform composition in young and old rats, with special reference to IIX myosin. Acta Physiol Scand 153: 109-116, 1995.
27. Lazar MA, Hodin RA, Darling DS, and Chin WW. A novel member of the thyroid/steroid hormone receptor family is encoded by the opposite strand of the rat c-erbAα transcriptional unit. Mol Cell Biol 9: 1128-1136, 1989.
28. Li X, Hughes SM, Salviati G, Teresi A, and Larsson L. Thyroid hormone effects on contractility and myosin composition of soleus muscle and single fibres from young and old rats. J Physiol 494: 555-567, 1996.
29. Li X and Larsson L. Contractility and myosin isoform compositions of skeletal muscles and muscle cells from rats treated with thyroid hormone for 0, 4 and 8 weeks. J Muscle Res Cell Motil 18: 335-344, 1997.
30. Liu JX, Eriksson PO, Thornell LE, and Pedrosa-Domellof F. Myosin heavy chain composition of muscle spindles in human biceps brachii. J Histochem Cytochem 50: 171-183, 2002.
31. Liu JX, Thornell LE, and Pedrosa-Domellof F. Muscle spindles in the deep muscles of the human neck: a morphological and immunocytochemical study. J Histochem Cytochem 51: 175-186, 2003.
32. Lomo T. Nerve-muscle interactions. In: Clinical Neurophysiology of Disorders of Muscle Neuromuscular Junction, Including Fatigue. Handbook of Clinical Neurophysiology, edited by Stålberg E. Amsterdam: Elsevier, 2003, p. 47-65.
33. Lomo T, Massoulie J, and Vigny M. Stimulation of denervated rat soleus muscle with fast and slow activity patterns induces different expression of acetylcholinesterase molecular forms. J Neurosci 5: 1180-1187, 1985.
34. Lompre AM, Schwartz K, d'Albis A, Lacombe G, Van Thiem N, and Swynghedauw B. Myosin isoenzyme redistribution in chronic heart overload. Nature 282: 105-107, 1979.
35. Mahdavi V, Izumo S, and Nadal-Ginard B. Developmental and hormonal regulation of sarcomeric myosin heavy chain gene family. Circ Res 60: 804-814, 1987.
36. Munroe SH and Lazar MA. Inhibition of c-erbA mRNA splicing by a naturally occurring antisense RNA. J Biol Chem 266: 22083-22086, 1991.
37. Muscat GE, Downes M, and Dowhan DH. Regulation of vertebrate muscle differentiation by thyroid hormone: the role of the myoD gene family. Bioessays 17: 211-218, 1995.
38. Nachlas MM, Tsou KG, De Sousa E, Cheng CS, and Seligman AM. Cytochemical demonstration of succinic dehydrogenase by the use of a new p-nitrophenyl substituted ditetrazole. J Histochem Cytochem 5: 420-436, 1957.
39. Nicol CJ and Bruce DS. Effect of hyperthyroidism on the contractile and histochemical properties of fast and slow twitch skeletal muscle in the rat. Pflügers Arch 390: 73-79, 1981.
40. Nwoye L, Mommaerts WF, Simpson DR, Seraydarian K, and Marusich M. Evidence for a direct action of thyroid hormone in specifying muscle properties. Am J Physiol Regul Integr Comp Physiol 242: R401-R408, 1982.
41. Pedrosa-Domellof F, Gohlsch B, Thornell LE, and Pette D. Electrophoretically defined myosin heavy chain patterns of single human muscle spindles. FEBS Lett 335: 39-242, 1993.
42. Pircher P, Chomez P, Vennström B, and Larsson L. Effects of rev-Erb A α orphan receptor knock-out on myosin isoform expression in skeletal muscle (Abstract). J Aging Physic Act 8: 281, 2000.
43. Pircher P, Chomez P, Vennström B, and Larsson L. Expression of myosin isoforms in skeletal muscles from mice lacking Rev-erbAα orphan receptors (Abstract). Biophys J 76: A52, 1999.
44. Pircher P, Chomez P, Vennström B, Wikström L, and Larsson L. Expression of myosin isoforms in skeletal muscles from mice lacking thyroid hormone or rev-erbα orphan receptors (Abstract). FASEB J 12: 2422, 1998.
45. Rubinstein N, Mabuchi K, Pepe F, Salmons S, Gergely J, and Sreter F. Use of type-specific antimyosins to demonstrate the transformation of individual fibers in chronically stimulated rabbit fast muscles. J Cell Biol 79: 252-261, 1978.
46. Salmons S and Sreter FA. Significance of impulse activity in the transformation of skeletal muscle type. Nature 263: 30-34, 1976.
47. Salto C, Kindblom JM, Johansson C, Wang Z, Gullberg H, Nordstrom K, Mansen A, Ohlsson C, Thoren P, Forrest D, and Vennström B. Ablation of TRα2 and a concomitant overexpression of alpha1 yields a mixed hypo- and hyperthyroid phenotype in mice. Mol Endocrinol 15: 2115-2128, 2001.
48. Schiaffino S, Gorza L, Sartore S, Saggin L, Ausoni S, Vianello M, Gundersen K, and Lomo T. Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J Muscle Res Cell Motil 10: 197-205, 1989.
49. Schiaffino S, Gorza L, Ausoni S, Bottinelli R, Reggiano C, Larsson L, Edström L, Gundersen K, and Lømo T. Muscle fibre types expressing different myosin heavy chain isoforms. Their functional properties and adaptive capacity. In: The Dynamic State of Muscle Fibres, edited by Pette D. Berlin: de Gruyter, 1990, p. 329-341.
50. Schiaffino S and Reggiani C. Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev 76: 371-423, 1996.
51. Schuler MJ, Buhler S, and Pette D. Effects of contractile activity and hypothyroidism on nuclear hormone receptor mRNA isoforms in rat skeletal muscle. Eur J Biochem 264: 982-988, 1999.
52. Whalen RG, Sell SM, Butler-Browne GS, Schwartz K, Bouveret P, and Pinset-Harstom I. Three myosin heavy-chain isozymes appear sequentially in rat muscle development. Nature 292: 805-809, 1981.
53. Yu F, Degens H, Li X, and Larsson L. Gender- and age-related differences in the regulatory influence of thyroid hormone on the contractility and myosin composition of single rat soleus muscle fibres. Pflügers Arch 437: 21-30, 1998.
54. Yu F, Gothe S, Wikstrom L, Forrest D, Vennström B, and Larsson L. Effects of thyroid hormone receptor gene disruption on myosin isoform expression in mouse skeletal muscles. Am J Physiol Regul Integr Comp Physiol 278: R1545-R1554, 2000.