Systems biology of skeletal muscle: Fiber type as an organizing principle

Wiley Interdisciplinary Reviews: Systems Biology and Medicine

Volumn 4, Issue 5, 2012, Pages 457-473

  Greising, Sarah M ^a   Gransee, Heather M ^a   Mantilla, Carlos B ^a,b   Sieck, Gary C ^a,b  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; MYOSIN;

CALCIUM TRANSPORT; EMBRYO DEVELOPMENT; EXCITATION CONTRACTION COUPLING; FAST MUSCLE; FAST MUSCLE FIBER; GENE EXPRESSION; HUMAN; MOTOR UNIT; MUSCLE FIBRIL; MUSCLE INNERVATION; MYOFILAMENT; NEUROMUSCULAR SYNAPSE; NEUROMUSCULAR TRANSMISSION; NONHUMAN; PERINATAL PERIOD; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REVIEW; RNA TRANSCRIPTION; SARCOMERE; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE; SLOW MUSCLE; SLOW MUSCLE FIBER; SYSTEMS BIOLOGY; TRANSVERSE TUBULAR SYSTEM;

ANIMALS; CALCIUM; HUMANS; MUSCLE CONTRACTION; MUSCLE PROTEINS; MUSCLE, SKELETAL; SARCOPLASMIC RETICULUM; SYSTEMS BIOLOGY;

EID: 84865155318     PISSN: 19395094     EISSN: 1939005X     Source Type: Journal    
DOI: 10.1002/wsbm.1184     Document Type: Review

References (71)

1. Barnard RJ, Edgerton VR, Furukawa T, Peter JB. Histochemical, biochemical, and contractile properties of red, white, and intermediate fibers. Am J Physiol 1971, 220:410-414.
2. Schiaffino S, Reggiani C. Fiber types in mammalian skeletal muscles. Physiol Rev 2011, 91:1447-1531.
3. Geiger PC, Cody MJ, Macken RL, Bayrd ME, Fang YH, Sieck GC. Mechanisms underlying increased force generation by rat diaphragm muscle fibers during development. J Appl Physiol 2001, 90:380-388.
4. Sieck GC, Zhan WZ, Prakash YS, Daood MJ, Watchko JF. SDH and actomyosin ATPase activities of different fiber types in rat diaphragm muscle. J Appl Physiol 1995, 79:1629-1639.
5. Sieck GC, Regnier M. Invited Review: plasticity and energetic demands of contraction in skeletal and cardiac muscle. J Appl Physiol 2001, 90:1158-1164.
6. Watchko JF, Daood MJ, Sieck GC. Myosin heavy chain transitions during development. Functional implications for the respiratory musculature. Comp Biochem Physiol B Biochem Mol Biol 1998, 119:459-470.
7. Geiger PC, Cody MJ, Han YS, Hunter LW, Zhan WZ, Sieck GC. Effects of hypothyroidism on maximum specific force in rat diaphragm muscle fibers. J Appl Physiol 2002, 92:1506-1514.
8. Gosselin LE, Johnson BD, Sieck GC. Age-related changes in diaphragm muscle contractile properties and myosin heavy chain isoforms. Am J Respir Crit Care Med 1994, 150:174-178.
9. Ben Hamida C, Soussi-Yanicostas N, Butler-Browne GS, Bejaoui K, Hentati F, Ben Hamida M. Biochemical and immunocytochemical analysis in chronic proximal spinal muscular atrophy. Muscle Nerve 1994, 17:400-410.
10. Baloh RH, Rakowicz W, Gardner R, Pestronk A. Frequent atrophic groups with mixed-type myofibers is distinctive to motor neuron syndromes. Muscle Nerve 2007, 36:107-110.
11. Sieck GC. Physiological effects of diaphragm muscle denervation and disuse. Clin Chest Med 1994, 15:641-659.
12. Mantilla CB, Sieck GC. Invited review: mechanisms underlying motor unit plasticity in the respiratory system. J Appl Physiol 2003, 94:1230-1241.
13. Fournier M, Sieck GC. Mechanical properties of muscle units in the cat diaphragm. J Neurophysiol 1988, 59:1055-1066.
14. Enad JG, Fournier M, Sieck GC. Oxidative capacity and capillary density of diaphragm motor units. J Appl Physiol 1989, 67:620-627.
15. Sieck GC, Fournier M, Prakash YS, Blanco CE. Myosin phenotype and SDH enzyme variability among motor unit fibers. J Appl Physiol 1996, 80:2179-2189.
16. Zhan WZ, Miyata H, Prakash YS, Sieck GC. Metabolic and phenotypic adaptations of diaphragm muscle fibers with inactivation. J Appl Physiol 1997, 82:1145-1153.
17. Miyata H, Zhan WZ, Prakash YS, Sieck GC. Myoneural interactions affect diaphragm muscle adaptations to inactivity. J Appl Physiol 1995, 79:1640-1649.
18. Geiger PC, Bailey JP, Zhan WZ, Mantilla CB, Sieck GC. Denervation-induced changes in myosin heavy chain expression in the rat diaphragm muscle. J Appl Physiol 2003, 95:611-619.
19. Hellyer NJ, Mantilla CB, Park EW, Zhan WZ, Sieck GC. Neuregulin-dependent protein synthesis in C2C12 myotubes and rat diaphragm muscle. Am J Physiol Cell Physiol 2006, 291:C1056-C1061.
20. Mantilla CB, Sieck GC. Trophic factor expression in phrenic motor neurons. Respir Physiol Neurobiol 2008, 164:252-262.
21. Loeb JA, Hmadcha A, Fischbach GD, Land SJ, Zakarian VL. Neuregulin expression at neuromuscular synapses is modulated by synaptic activity and neurotrophic factors. J Neurosci 2002, 22:2206-2214.
22. Littlefield RS, Fowler VM. Thin filament length regulation in striated muscle sarcomeres: pointed-end dynamics go beyond a nebulin ruler. Semin Cell Dev Biol 2008, 19:511-519.
23. Millman BM. The filament lattice of striated muscle. Physiol Rev 1998, 78:359-391.
24. Ingalls CP, Warren GL, Armstrong RB. Dissociation of force production from MHC and actin contents in muscles injured by eccentric contractions. J Muscle Res Cell Motil 1998, 19:215-224.
25. Yates LD, Greaser ML. Quantitative determination of myosin and actin in rabbit skeletal muscle. J Mol Biol 1983, 168:123-141.
26. Ryder JW, Lau KS, Kamm KE, Stull JT. Enhanced skeletal muscle contraction with myosin light chain phosphorylation by a calmodulin-sensing kinase. J Biol Chem 2007, 282:20447-20454.
27. Ottenheijm CA, van Hees HW, Heunks LM, Granzier H. Titin-based mechanosensing and signaling: role in diaphragm atrophy during unloading? Am J Physiol Lung Cell Mol Physiol 2010, 300:L161-L166.
28. Bonnemann CG, Laing NG. Myopathies resulting from mutations in sarcomeric proteins. Curr Opin Neurol 2004, 17:529-537.
29. Prado LG, Makarenko I, Andresen C, Kruger M, Opitz CA, Linke WA. Isoform diversity of giant proteins in relation to passive and active contractile properties of rabbit skeletal muscles. J Gen Physiol 2005, 126:461-480.
30. Ottenheijm CA, Granzier H. New insights into the structural roles of nebulin in skeletal muscle. J Biomed Biotechnol 2010, 2010:968139.
31. Rowley KL, Mantilla CB, Ermilov LG, Sieck GC. Synaptic vesicle distribution and release at rat diaphragm neuromuscular junctions. J Neurophysiol 2007, 98:478-487.
32. Mantilla CB, Zhan WZ, Sieck GC. Neurotrophins improve neuromuscular transmission in the adult rat diaphragm. Muscle Nerve 2004, 29:381-386.
33. Mantilla CB, Rowley KL, Fahim MA, Zhan WZ, Sieck GC. Synaptic vesicle cycling at type-identified diaphragm neuromuscular junctions. Muscle Nerve 2004, 30:774-783.
34. Day NC, Wood SJ, Ince PG, Volsen SG, Smith W, Slater CR, Shaw PJ. Differential localization of voltage-dependent calcium channel alpha1 subunits at the human and rat neuromuscular junction. J Neurosci 1997, 17:6226-6235.
35. Ermilov LG, Mantilla CB, Rowley KL, Sieck GC. Safety factor for neuromuscular transmission at type-identified diaphragm fibers. Muscle Nerve 2007, 35:800-803.
36. Johnson BD, Sieck GC. Differential susceptibility of diaphragm muscle fibers to neuromuscular transmission failure. J Appl Physiol 1993, 75:341-348.
37. Geiger PC, Cody MJ, Sieck GC. Force-calcium relationship depends on myosin heavy chain and troponin isoforms in rat diaphragm muscle fibers. J Appl Physiol 1999, 87:1894-1900.
38. Macdonald WA, Stephenson DG. Effect of ADP on slow-twitch muscle fibres of the rat: implications for muscle fatigue. J Physiol 2006, 573:187-198.
39. Quiroz-Rothe E, Rivero JL. Coordinated expression of myosin heavy chains, metabolic enzymes, and morphological features of porcine skeletal muscle fiber types. Microsc Res Tech 2004, 65:43-61.
40. Gordon AM, Homsher E, Regnier M. Regulation of contraction in striated muscle. Physiol Rev 2000, 80:853-924.
41. Sieck GC, Prakash YS. Cross-bridge kinetics in respiratory muscles. Eur Respir J 1997, 10:2147-2158.
42. Huxley AF. Muscle structure and theories of contraction. Prog Biophys Biophys Chem 1957, 7:255-318.
43. Geiger PC, Cody MJ, Macken RL, Sieck GC. Maximum specific force depends on myosin heavy chain content in rat diaphragm muscle fibers. J Appl Physiol 2000, 89:695-703.
44. Geiger PC, Cody MJ, Macken RL, Bayrd ME, Sieck GC. Effect of unilateral denervation on maximum specific force in rat diaphragm muscle fibers. J Appl Physiol 2001, 90:1196-1204.
45. Brenner B. The necessity of using two parameters to describe isotonic shortening velocity of muscle tissues: the effect of various interventions upon initial shortening velocity (vi) and curvature (b). Basic Res Cardiol 1986, 81:54-69.
46. Brenner B, Eisenberg E. Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution. Proc Natl Acad Sci USA 1986, 83:3542-3546.
47. Guth K, Wojciechowski R. Perfusion cuvette for the simultaneous measurement of mechanical, optical and energetic parameters of skinned muscle fibres. Pflugers Arch 1986, 407:552-557.
48. Sieck GC, Zhan WZ, Han YS, Prakash YS. Effect of denervation on ATP consumption rate of diaphragm muscle fibers. J Appl Physiol 2007, 103:858-866.
49. Fenn WO. A quantitative comparison between the energy liberated and the work performed by the isolated sartorius muscle of the frog. J Physiol 1923, 58:175-203.
50. Sieck GC, Han YS, Prakash YS, Jones KA. Cross-bridge cycling kinetics, actomyosin ATPase activity and myosin heavy chain isoforms in skeletal and smooth respiratory muscles. Comp Biochem Physiol B Biochem Mol Biol 1998, 119:435-450.
51. Sieck GC, Prakash YS, Han YS, Fang YH, Geiger PC, Zhan WZ. Changes in actomyosin ATP consumption rate in rat diaphragm muscle fibers during postnatal development. J Appl Physiol 2003, 94:1896-1902.
52. Han YS, Geiger PC, Cody MJ, Macken RL, Sieck GC. ATP consumption rate per cross bridge depends on myosin heavy chain isoform. J Appl Physiol 2003, 94:2188-2196.
53. Kjaer M. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 2004, 84:649-698.
54. Tidball JG. Desmin at myotendinous junctions. Exp Cell Res 1992, 199:206-212.
55. Tidball JG. Force transmission across muscle cell membranes. J Biomech 1991, 24 (Suppl 1):43-52.
56. Grounds MD, Sorokin L, White J. Strength at the extracellular matrix-muscle interface. Scand J Med Sci Sports 2005, 15:381-391.
57. Ervasti JM. Costameres: the Achilles' heel of Herculean muscle. J Biol Chem 2003, 278:13591-13594.
58. Aravamudan B, Mantilla CB, Zhan WZ, Sieck GC. Denervation effects on myonuclear domain size of rat diaphragm fibers. J Appl Physiol 2006, 100:1617-1622.
59. Verheul AJ, Mantilla CB, Zhan WZ, Bernal M, Dekhuijzen PN, Sieck GC. Influence of corticosteroids on myonuclear domain size in the rat diaphragm muscle. J Appl Physiol 2004, 97:1715-1722.
60. Mantilla CB, Sill RV, Aravamudan B, Zhan WZ, Sieck GC. Developmental effects on myonuclear domain size of rat diaphragm fibers. J Appl Physiol 2008, 104:787-794.
61. Geiger PC, Bailey JP, Mantilla CB, Zhan WZ, Sieck GC. Mechanisms underlying myosin heavy chain expression during development of the rat diaphragm muscle. J Appl Physiol 2006, 101:1546-1555.
62. Williams AH, Liu N, van Rooij E, Olson EN. MicroRNA control of muscle development and disease. Curr Opin Cell Biol 2009, 21:461-469.
63. MacQuarrie K, Yao Z, Young J, Cao Y, Tapscott S. miR-206 integrates multiple components of differentiation pathways to control the transition from growth to differentiation in rhabdomyosarcoma cells. Skeletal Muscle 2012, 2:7.
64. van Lunteren E, Leahy P. Gene expression microarrays and respiratory muscles. Respir Physiol Neurobiol 2007, 156:103-115.
65. Sandri M. Signaling in muscle atrophy and hypertrophy. Physiology 2008, 23:160-170.
66. Argadine HM, Hellyer NJ, Mantilla CB, Zhan WZ, Sieck GC. The effect of denervation on protein synthesis and degradation in adult rat diaphragm muscle. J Appl Physiol 2009, 107:438-444.
67. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, et al. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 2001, 294:1704-1708.
68. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 2001, 98:14440-14445.
69. Argadine HM, Mantilla CB, Zhan WZ, Sieck GC. Intracellular signaling pathways regulating net protein balance following diaphragm muscle denervation. Am J Physiol Cell Physiol 2011, 300:C318-C327.
70. Goodman CA, Mabrey DM, Frey JW, Miu MH, Schmidt EK, Pierre P, Hornberger TA. Novel insights into the regulation of skeletal muscle protein synthesis as revealed by a new nonradioactive in vivo technique. FASEB J 2011, 25:1028-1039.
71. Gransee HM, Mantilla CB, Sieck GC. Respiratory muscle plasticity. Compr Physiol 2012, 2:1441-1462.