A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type

Genes and Development

Volumn 12, Issue 16, 1998, Pages 2499-2509

  Chin, Eva R ^a   Olson, Eric N ^a   Richardson, James A ^a   Yang, Quan ^a   Humphries, Caroline ^a   Shelton, John M ^a   Wu, Hai ^a   Zhu, Weiguang ^a   Bassel Duby, Rhonda ^a   Williams, R Sanders ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Cyclosporin A; Exercise; MEF2; Myoglobin; Myosin; NFAT

Indexed keywords

CALCINEURIN; CYCLOSPORIN A; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRAIN 3T3; CONTROLLED STUDY; FAST MUSCLE FIBER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SLOW MUSCLE FIBER; TRANSACTIVATION;

ANIMALIA; MAMMALIA;

EID: 0032529188     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.16.2499     Document Type: Article

References (59)

1. Aramburu, J., F. Garcia-Cozar, A. Raghavan, H. Okamura, A. Rao, and G.G. Hogan. 1998. Selective inhibition of NFAT activation by a peptide spanning the calcineurin targeting site of NFAT. Mol. Cell. 1: 627-637.
2. Bassel-Duby, R., C.M. Grohe, M.E. Jessen, W.J. Parsons, J.A. Richardson, R. Chao, J. Grayson, W.S. Ring, and R.S. Williams. 1993. Sequence elements required for transcriptional activity of the human myoglobin promoter in intact myocardium. Circ. Res. 73: 360-366.
3. Black, B.L. and E.N. Olson. 1998. Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu. Rev. Cell Dev. Biol. 14: 167-196.
4. Booth, F.W. and K.M. Baldwin. 1996. Muscle plasticity: Energy demand and supply processes. In The handbook of physiology: Integration of motor, circulatory, respiratory and metabolic control during exercise (ed. L.B. Rowell and J.T. Shepard), pp. 1075-1123. American Physiology Society, Bethesda, MD.
5. Brooke, M.H. and K.K. Kaiser. 1970. Muscle fiber types: How many and what kind? Arch. Neurol. 23: 369-379.
6. Caiozzo, V.J., M.J. Baker, R.E. Herrick, M. Tao, and K.M. Baldwin. 1994. Effect of spaceflight on skeletal muscle: Mechanical properties and myosin isoform content of a slow antigravity muscle. J. Appl. Physiol. 76: 1764-1773.
7. Cameron, A.M., J.P. Steiner, A.J. Roskams, S.M. Ali, G.V. Ronnett, and S.H. Snyder. 1995. Calcineurin associated with the inositol 1,4,5-trisphosphate receptor-FKBP12 complex modulates Ca2+ flux. Cell 83: 463-472.
8. Chin, E.R. and D.G. Allen. 1996. Changes in intracellular free Ca2+ concentration during constant 10 Hz stimulation of mouse single skeletal muscle fibres. Physiologist 39: A-75.
9. Clipstone, N.A. and G.R. Crabtree. 1992. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357: 695-697.
10. Devlin, B.H., F.C. Wefald, W.E. Kraus, T.S. Bernard, and R.S. Williams. 1989. Identification of a muscle-specific enhancer within the 5′ flanking region of the human myoglobin gene. J. Biol. Chem. 264: 13896-13900.
11. DiMario, J.X., S.E. Fernyak, and F.E. Stockdale. 1993. Myoblasts transferred to the limbs of embryos are committed to specific fibre fates. Nature 362: 165-167.
12. Dolmetsch, R.E., R.S. Lewis, C.C. Goodnow, and J.I. Healy. 1997. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 386: 855-858.
13. Garry, D.J., R.S. Bassel-Duby, J.A. Richardson, J. Grayson, P.D. Neufer, and R.S. Williams. 1996. Postnatal development and plasticity of specialized muscle fiber characteristics in the hindlimb. Dev. Genet. 19: 146-156.
14. Grayson, J., R. Bassel-Duby, and R.S. Williams. 1998. Transcriptional synergism in muscle-specific gene regulation: Physical and functional interactions between MEF-2 and Sp1. J. Cell. Biochem. (in press).
15. Grayson, J., R.S. Williams, Y.T. Yu, and R. Bassel-Duby. 1995. Synergistic interactions between heterologous upstream activation elements and specific TATA sequences in a muscle-specific promoter. Mol. Cell. Biol. 15: 1870-1878.
16. Hennig, R. and T. Lomo. 1985. Firing patterns of motor units in normal rats. Nature 314: 164-166.
17. Hoey, T., Y.L. Sun, K. Williamson, and X. Xu. 1995. Isolation of two new members of the NF-AT gene family and functional characterization of the NF-AT proteins. Immunity 2: 461-472.
18. Holloszy, J.O. and E.F. Coyle. 1984. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J. Appl. Physiol. 56: 831-838.
19. Hughes, S.M., K. Koishi, M. Rudnicki, and A.M. Maggs. 1997. MyoD protein is differentially accumulated in fast and slow skeletal muscle fibres and required for normal fibre type balance in rodents. Mech. Dev. 61: 151-163.
20. Ianuzzo, C.D., N. Hamilton, and B. Li. 1991. Competitive control of myosin expression: hypertrophy vs. Hyperthyroidism. J. Appl. Physiol. 70: 2328-2830.
21. Izumo, S. and V. Mahdavi. 1988. Thyroid hormone receptor alpha isoforms generated by alternative splicing differentially activate myosin HC gene transcription. Nature 334: 539-542.
22. Kong, X., J. Manchester, S. Salmons, and J.C. Lawrence. 1994. Glucose transporters in single skeletal muscle fibers. J. Biol. Chem. 269: 12963-12967.
23. Lam, E., M.M. Martin, A.P. Timerman, C. Sabers, S. Fleischer, T. Lukas, R.T. Abraham, S.J. O'Keefe, E.A. O'Neill, and G.J. Wiederrecht. 1995. A novel FK506 binding protein can mediate the immunosuppressive effects of FK506 and is associated with the cardiac ryanodine receptor. J. Biol. Chem. 270: 26511-26522.
24. Levitt, L.K., J.V. O'Mahoney, K.J. Brennan, J.E. Joya, L. Zhu, R. Wade, and E. Hardeman. 1995. The human troponin I slow promoter directs slow fiber-specific expression in transgenic mice. DNA Cell Biol. 14: 599-607.
25. Li, L., J. Zhou, G. James, R. Heller-Harrison, M.P. Czech, and E.N. Olson. 1992. FGF inactivates myogenic helix-loop-helix proteins through phosphorylation of a conserved protein kinase C site in their DNA-binding domains. Cell 71: 1181-1194.
26. Liu, J., J.D. Farmer, Jr., W.S. Lane, J. Friedman, I. Weissman, and S.L. Schreiber. 1991. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66: 807-815.
27. Manalan, A.S. and C.B. Klee. 1983. Activation of calcineurin by limited proteolysis. Proc. Natl. Acad. Sci. 80: 4291-4295.
28. Massie, B.M., M. Conway, B. Rajagopalan, R. Yonge, S. Frostick, J. Ledingham, P. Sleight, and G. Radda. 1988. Skeletal muscle metabolism during exercise under ischemic condition in congestive heart failure: evidence for abnormalities unrelated to blood flow. Circulation 78: 320-326.
29. Mercier, J.G., J.F. Hokanson, and G.A. Brooks. 1995. Effects of cyclosporine A on skeletal muscle mitochondrial respiration and endurance time in rats. Am. J. Resp. Crit. Care Med. 151: 1532-1536.
30. Michel, J.B., G.A. Ordway, J.A. Richardson, and R.S. Williams. 1994. Biphasic induction of immediate early genes accompanies activity-dependent angiogenesis and myofiber remodeling of rabbit skeletal muscle. J. Clin. Invest. 94: 277-285.
31. Molkentin, J.D., J. Lu, C.L. Antos, B. Markham, J. Richardson, J. Robbins, S.R. Grant, and E.N. Olson. 1998. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93: 1-20.
32. Molkentin, J.D. and E.N. Olson. 1996. Combinatorial control of muscle development by basic helix-loop-helix and MADS-box transcription factors. Proc. Natl. Acad. Sci. 93: 9366-9373.
33. Nakayama, M., J. Stauffer, J. Cheng, S. Banerjee-Basu, E. Wawrousek, and A. Buonanno. 1996. Common core sequences are found in skeletal muscle slow-and fast-fiber-type-specific regulatory elements. Mol. Cell. Biol. 16: 2408-2417.
34. Neufer, P.D., G.A. Ordway, G.A. Hand, J.M. Shelton, J.A. Richardson, I.J. Benjamin, and R.S. Williams. 1996. Continuous contractile activity induces fiber type specific expression of HSP70 in skeletal muscle. Am. J. Physiol. 271: C1828-C1837.
35. Northrop, J.P., S.N. Ho, L. Chen, D.J. Thomas, L.A. Timmerman, G.P. Nolan, A. Admon, and G.R. Crabtree. 1994. NF-AT components define a family of transcription factors targeted in T-cell activation. Nature 369: 497-502.
36. O'Keefe, S.J., J. Tamura, R.L. Kincaid, M.J. Tocci, and E.A. O'Neill. 1992. FK-506-and CsA-sensitive activation of the interleukin-2 promoter by calcineurin. Nature 357: 692-694.
37. Olson, E.N., M. Perry, and R.A. Schulz. 1995. Regulation of muscle differentiation by the MEF2 family of MADS box transcription factors. Dev. Biol. 172: 2-14.
38. Ontell, M.P., M.M. Sopper, G. Lyons, M. Buckingham, and M. Ontell. 1993. Modulation of contractile protein gene expression in fetal murine crural muscles:emergence of muscle diversity. Dev. Dynm. 198: 203-213.
39. Parsons, W.J., J.A. Richardson, K.H. Graves, R.S. Williams, and R.W. Moreadith. 1993. Gradients of transgene expression directed by the human myoglobin promoter in the developing mouse heart. Proc. Natl. Acad. Sci. 90: 1726-1730.
40. Pette, D. and G. Vrbova. 1992. Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev. Physiol. Biochem. Pharmacol. 120: 115-202.
41. Qin, W., Z. Khuchua, S.C. Klein, and A.W. Strauss. 1997. Elements regulating cardiomyocyte expression of the human sarcomeric mitochondrial creatine kinase gene in transgenic mice. J. Biol. Chem. 272: 25210-25216.
42. Rao, A., C. Luo, and P.G. Hogan. 1997. Transcription factors of the NFAT family: Regulation and function. Annu. Rev. Immunol. 15: 707-747.
43. Sabbah, H.N., F. Hansen-Smith, V.G. Sharov, T. Kono, M. Lesch, P.J. Gengo, R.P. Steffen, T.B. Levine, and S. Goldstein. 1993. Decreased proportion of type I myofibers in skeletal muscle of dogs with chronic heart failure. Circulation 87: 1729-1737.
44. Saltin, B. and P.D. Gollnick. 1983. Skeletal muscle adaptability: Significance for metabolism and performance. In Handbook of physiology: Skeletal muscle (ed. L.D.D. Peachey), pp. 555-632. American Physiological Society, Bethesda, MD.
45. Schiaffino, S. and C. Reggiani. 1996. Molecular diversity of myofibrillar proteins: Gene regulation and functional significance. Physiol. Rev. 76: 371-423.
46. Shield, M.A., H.S. Haugen, C.H. Clegg, and S.D. Hauschka. 1996. E-box sites and a proximal regulatory region of the muscle creatine kinase gene differentially regulate expression in diverse skeletal muscles and cardiac muscle of transgenic mice. Mol. Cell. Biol. 16: 5058-5068.
47. Sreter, F.A., J.R. Lopez, L. Alamo, K. Mabuchi, and J. Gergely. 1987. Changes in intracellular ionized Ca concentration associated with muscle fiber type transformation. Am. J. Physiol. 253: C296-C300.
48. Stockdale, F.E. 1997. Mechanisms of formation of muscle fiber types. Cell Struct. Funct. 22: 37-43.
49. Sullivan, M.J., M.B. Higginbotham, and F.R. Cobb. 1989. Exercise training in patients with chronic heart failure delays ventilatory anaerobic threshold and improves submaximal exercise performance. Circulation 79: 324-329.
50. Tikkanen, H.O., H. Naveri, and M. Harkonen. 1996. Skeletal muscle fiber distribution influences serum high-density lipoprotein cholesterol level. Atherosclerosis 120: 1-5.
51. Timmerman, L.A., N.A. Clipstone, S.N. Ho, J.P. Northrop, and G.R. Crabtree. 1996. Rapid shuttling of NF-AT in discrimination of Ca2+ signals and immunosuppression. Nature 383: 837-840.
52. Vrbova, G. 1963. The effect of motoneurone activity on the speed of contraction of striated muscle. J. Physiol. (London) 169: 513-526.
53. Walsh, M.P., J.L. Busaan, E.D. Fraser, S.Y. Fu, M.D. Pato, and M. Michalak. 1995. Characterization of the recombinant C-terminal domain of dystrophin: Phosphorylation by calmodulin-dependent protein kinase II and dephosphorylation by type 2B protein phosphatase. Biochemistry 34: 5561-5568.
54. Webster, C., L. Silberstein, A.P. Hays, and H.M. Blau. 1988. Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell 52: 503-513.
55. Westerblad, H. and D.G. Allen. 1991. Changes in myoplasmic calcium concentration during fatigue in single mouse muscle fibers. J. Gen. Physiol. 98: 615-635.
56. Williams, R.S. and P.D. Neufer. 1996. Regulation of gene expression in skeletal muscle by contractile activity. In The handbook of physiology: Integration of motor, circulatory, respiratory and metabolic control during exercise (ed. L.B. Rowell and J.T. Shepard), pp. 1124-1150. American Physiology Society, Bethesda, MD.
57. Williams, R.S., S. Salmons, E.A. Newsholme, R.E. Kaufman, and J. Mellor. 1986. Regulation of nuclear and mitochondrial gene expression by contractile activity in skeletal muscle. J. Biol. Chem. 261: 376-380.
58. Yamashita, K. and T. Yoshioka. 1991. Profiles of creatine kinase isoenzyme compositions in single muscle fibres of different types. J. Muscle Res. Cell Motil. 12: 37-44.
59. Yang, Q., R. Bassel-Duby, and R.S. Williams. 1997. Transient expression of a winged-helix protein, MNF-β, during myogenesis. Mol. Cell. Biol. 17: 5236-5243.