Rapid muscle-specific gene expression changes after a single bout of eccentric contractions in the mouse

American Journal of Physiology - Cell Physiology

Volumn 286, Issue 2 55-2, 2004, Pages

  Barash, Ilona A ^a   Mathew, Liby ^a   Ryan, Allen F ^a   Chen, Ju ^a   Lieber, Richard L ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Cardiac ankyrin repeat protein; Microarray; Muscle ankyrin repeat protein; Muscle LIM protein

Indexed keywords

ACTIN RELATED PROTEIN 2; CARDIAC ANKYRIN REPEAT PROTEIN; LIM PROTEIN; MUSCLE ANKYRIN REPEAT PROTEIN 1; MUSCLE ANKYRIN REPEAT PROTEIN 2; MUSCLE PROTEIN; MYOSIN BINDING PROTEIN H; UNCLASSIFIED DRUG; XIN PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA MICROARRAY; ECCENTRIC MUSCLE CONTRACTION; EXERCISE; GENE; GENE ACTIVATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; MALE; MOUSE; MUSCLE; MUSCLE CONTRACTION; MUSCLE INJURY; MUSCLE ISOMETRIC CONTRACTION; MUSCLE LENGTH; MUSCLE STRENGTH; MUSCLE STRETCHING; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; TISSUE SPECIFICITY; TORQUE;

ANIMALIA; EUKARYOTA;

EID: 0742323119     PISSN: 03636143     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.00211.2003     Document Type: Article

References (91)

1. Aihara Y, Kurabayashi M, Saito Y, Ohyama Y, Tanaka T, Takeda S, Tomaru K, Sekiguchi K, Arai M, Nakamura T, and Nagai R. Cardiac ankyrin repeat protein is a novel marker of cardiac hypertrophy: role of M-CAT element within the promoter. Hypertension 36: 48-53, 2000.
2. Arber S, Halder G, and Caroni P. Muscle LIM protein, a novel essential regulator of myogenesis, promotes myogenic differentiation. Cell 79: 221-231, 1994.
3. Arber S, Hunter JJ, Ross J Jr, Hongo M, Sansig G, Borg J, Perriard JC, Chien KR and Caroni P. MLP-deficient mice exhibit a disruption of cardiac cytoarchitectural organization, dilated cardiomyopathy, and heart failure. Cell 88: 393-403, 1997.
4. Armstrong RB, Ogilvie RW, and Schwane JA. Eccentric exercise-induced injury to rat skeletal muscle. J Appl Physiol 54: 80-93, 1983.
5. 2-terminal kinase pathway in rat skeletal muscle. J Biol Chem 272: 25636-25640, 1997.
6. Ashton-Miller JA, He Y, Kadhiresan VA, McCubbrey DA, and Faulkner JA. An apparatus to measure in vivo biomechanical behavior of dorsi- and plantarflexors of mouse ankle. J Appl Physiol 72: 1205-1211, 1992.
7. Bakay M, Chen YW, Borup R, Zhao P, Nagaraju K, and Hoffman EP. Sources of variability and effect of experimental approach on expression profiling data interpretation. BMC Bioinformatics 3: 4, 2002.
8. Bakay M, Zhao P, Chen J, and Hoffman EP. A web-accessible complete transcriptome of normal human and DMD muscle. Neuromuscul Disord 12, Suppl 1: S125-S141, 2002.
9. Baldi P and Long AD. A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17: 509-519, 2001.
10. Bang ML, Mudry RE, McElhinny AS, Trombitas K, Geach AJ, Yamasaki R, Sorimachi H, Granzier H, Gregorio CC, and Labeit S. Myopalladin, a novel 145-kilodalton sarcomeric protein with multiple roles in Z-disc and I-band protein assemblies. J Cell Biol 153: 413-427, 2001.
11. Barash IA and Lieber RL. Gene expression changes following eccentric contractions. 2003 Experimental Biology meeting abstracts. FASEB J 17: abstract 4991, 2003.
12. Barash IA, Peters D, Friden J, Lutz GJ, and Lieber RL. Desmin cytoskeletal modifications after a bout of eccentric exercise in the rat. Am J Physiol Regut Integr Comp Physiol 283: R958-R963, 2002.
13. 2-terminal kinase activity in human skeletal muscle. J Appl Physiol 87: 1668-1673, 1999.
14. 2-terminal kinase activity and p38 phosphorylation in rat skeletal muscle. Am J Physiol Cell Physiol 280: C352-C358, 2001.
15. Breen EC, Johnson EC, Wagner H, Tseng HM, Sung LA, and Wagner PD. Angiogenic growth factor mRNA responses in muscle to a single bout of exercise. J Appl Physiol 81: 355-361, 1996.
16. Brooks SV, Opiteck JA, and Faulkner JA. Conditioning of skeletal muscles in adult and old mice for protection from contraction-induced injury. J Gerontol A Biol Sci Med Sci 56: B163-B171, 2001.
17. Brooks SV, Zerba E, and Faulkner JA. Injury to muscle fibres after single stretches of passive and maximally stimulated muscles in mice. J Physiol 488: 459-469, 1995.
18. Burkholder TJ and Lieber RL. Sarcomere number adaptation after retinaculum transection in adult mice. J Exp Biol 201: 309-316, 1998.
19. Campbell WG, Gordon SE, Carlson CJ, Pattison JS, Hamilton MT, and Booth FW. Differential global gene expression in red and white skeletal muscle. Am J Physiol Cell Physiol 280: C763-C768, 2001.
20. Carson JA, Nettleton D, and Reecy JM. Differential gene expression in the rat soleus muscle during early work overload-induced hypertrophy. FASEB J 16: 207-209, 2002.
21. Chen YW, Nader GA, Baar KR, Fedele MJ, Hoffman EP, and Esser KA. Response of rat muscle to acute resistance exercise defined by transcriptional and translational profiling. J Physiol 545: 27-41, 2002.
22. Chen YW, Zhao P, Borup R, and Hoffman EP. Expression profiling in the muscular dystrophies: identification of novel aspects of molecular pathophysiology. J Cell Biol 151: 1321-1336, 2000.
23. Chu W, Burns DK, Swerlick RA, and Presky DH. Identification and characterization of a novel cytokine-inducible nuclear protein from human endothelial cells. J Biol Chem 270: 10236-10245, 1995.
24. Edwards RH, Hill DK, Jones DA, and Merton PA. Fatigue of long duration in human skeletal muscle after exercise. J Physiol 272: 769-778, 1977.
25. Ehler E, Horowits R, Zuppinger C, Price RL, Perriard E, Leu M, Caroni P, Sussman M, Eppenberger HM, and Perriard JC. Alterations at the intercalated disk associated with the absence of muscle LIM protein. J Cell Biol 153: 763-772, 2001.
26. Feasson L, Stockholm D, Freyssenet D, Richard I, Duguez S, Beckmann JS, and Denis C. Molecular adaptations of neuromuscular disease-associated proteins in response to eccentric exercise in human skeletal muscle. J Physiol 543: 297-306, 2002.
27. Flick MJ and Konieczny SF. The muscle regulatory and structural protein MLP is a cytoskeletal binding partner of betaI-spectrin. J Cell Sci 113: 1553-1564, 2000.
28. Friden J, Lieber RL, and Thornell LE. Subtle indications of muscle damage following eccentric contractions. Acta Physiol Scand 142: 523-524, 1991.
29. Friden J, Sjostrom M, and Ekblom B. A morphological study of delayed muscle soreness. Experientia 37: 506-507, 1981.
30. Gilbert R, Cohen JA, Pardo S, Basu A, and Fischman DA. Identification of the A-band localization domain of myosin binding proteins C and H (MyBP-C, MyBP-H) in skeletal muscle. J Cell Sci 112: 69-79, 1999.
31. Glass DJ. Signalling pathways that mediate skeletal muscle hypertrophy and atrophy. Nat Cell Biol 5: 87-90, 2003.
32. Golenhofen N, Arbeiter A, Koob R, and Drenckhahn D. Ischemia-induced association of the stress protein alpha B-crystallin with I-band portion of cardiac titin. J Mol Cell Cardiol 34: 309-319, 2002.
33. Gotthardt M, Hammer RE, Hubner N, Monti J, Witt CC, McNabb M, Richardson JA, Granzier H, Labeit S, and Herz J. Conditional expression of mutant M-line titins results in cardiomyopathy with altered sarcomere structure. J Biol Chem 278: 6059-6065, 2003.
34. Granzier H and Labeit S. Cardiac titin: an adjustable multi-functional spring. J Physiol 541: 335-342, 2002.
35. 2 terminus of titin spans the Z-disc: its interaction with a novel 19-kD ligand (T-cap) is required for sarcomeric integrity. J Cell Biol 143: 1013-1027, 1998.
36. Hayashi T, Hirshman MF, Dufresne SD, and Goodyear LJ. Skeletal muscle contractile activity in vitro stimulates mitogen-activated protein kinase signaling. Am J Physiol Cell Physiol 277: C701-C707, 1999.
37. Horowits R, Kempner ES, Bisher ME, and Podolsky RJ. A physiological role for titin and nebulin in skeletal muscle. Nature 323: 160-164, 1986.
38. Ikeda K, Emoto N, Matsuo M, and Yokoyama M. Molecular identification and characterization of a novel nuclear protein whose expression is up-regulated in insulin-resistant animals. J Biol Chem 278: 3514-3520, 2003.
39. Ishiguro N, Baba T, Ishida T, Takeuchi K, Osaki M, Araki N, Okada E, Takahashi S, Saito M, Watanabe M, Nakada C, Tsukamoto Y, Sato K, Ito K, Fukayama M, Mori S, Ito H, and Moriyama M. Carp, a cardiac ankyrin-repeated protein, and its new homologue, Arpp, are differentially expressed in heart, skeletal muscle, and rhabdomyosarcomas. Am J Pathol 160: 1767-1778, 2002.
40. Jeyaseelan R, Poizat C, Baker RK, Abdishoo S, Isterabadi LB, Lyons GE, and Kedes L. A novel cardiac-restricted target for doxorubicin. CARP, a nuclear modulator of gene expression in cardiac progenitor cells and cardiomyocytes. J Biol Chem 272: 22800-22808, 1997.
41. Jones DA, Newham DJ, and Torgan C. Mechanical influences on long-lasting human muscle fatigue and delayed-onset pain. J Physiol 412: 415-427, 1989.
42. Jones DA and Rutherford OM. Human muscle strength training: the effects of three different regimens and the nature of the resultant changes. J Physiol 391: 1-11, 1987.
43. Kemp TJ, Sadusky TJ, Saltisi F, Carey N, Moss J, Yang SY, Sassoon DA, Goldspink G, and Coulton GR. Identification of Ankrd2, a novel skeletal muscle gene coding for a stretch-responsive ankyrin-repeat protein. Genomics 66: 229-241, 2000.
44. Knoll R, Hoshijima M, Hoffman HM, Person V, Lorenzen-Schmidt I, Bang ML, Hayashi T, Shiga N, Yasukawa H, Schaper W, McKenna W, Yokoyama M, Schork NJ, Omens JH, McCulloch AD, Kimura A, Gregorio CC, Poller W, Schaper J, Schultheiss HP, and Chien KR. The cardiac mechanical stretch sensor machinery involves a Z disc complex that is defective in a subset of human dilated cardiomyopathy. Cell 111: 943-955, 2002.
45. Koh TJ and Brooks SV. Lengthening contractions are not required to induce protection from contraction-induced muscle injury. Am J Physiol Regul Integr Comp Physiol 281: R155-R161, 2001.
46. Kong Y, Flick MJ, Kudla AJ, and Konieczny SF. Muscle LIM protein promotes myogenesis by enhancing the activity of MyoD. Mol Cell Biol 17: 4750-4760, 1997.
47. Krook A, Widegren U, Jiang XJ, Henriksson J, Wallberg-Henriksson H, Alessi D, and Zierath JR. Effects of exercise on mitogen- and stress-activated kinase signal transduction in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 279: R1716-R1721, 2000.
48. Kuo H, Chen J, Ruiz-Lozano P, Zou Y, Nemer M, and Chien KR. Control of segmental expression of the cardiac-restricted ankyrin repeat protein gene by distinct regulatory pathways in murine cardiogenesis. Development 126: 4223-4234, 1999.
49. Labeit S and Kolmerer B. Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science 270: 293-296, 1995.
50. Lapointe BM, Frenette J, and Cote CH. Lengthening contraction-induced inflammation is linked to secondary damage but devoid of neutrophil invasion. J Appl Physiol 92: 1995-2004, 2002.
51. Lazarides E and Balzer DR Jr. Specificity of desmin to avian and mammalian muscle cells. Cell 14: 429-438, 1978.
52. Lieber RL. Muscle fiber length and moment arm coordination during dorsi- and plantarflexion in the mouse hindlimb. Acta Anat (Basel) 159: 84-89, 1997.
53. Lieber RL and Friden J. Muscle damage is not a function of muscle force but active muscle strain. J Appl Physiol 74: 520-526, 1993.
54. Lieber RL, Schmitz MC, Mishra DK, and Friden J. Contractile and cellular remodeling in rabbit skeletal muscle after cyclic eccentric contractions. J Appl Physiol 77: 1926-1934, 1994.
55. Lieber RL, Thornell LE, and Friden J. Muscle cytoskeletal disruption occurs within the first 15 min of cyclic eccentric contraction. J Appl Physiol 80: 278-284, 1996.
56. Loots GG, Ovcharenko I, Pachter L, Dubchak I, and Rubin EM. rVista for comparative sequence-based discovery of functional transcription factor binding sites. Genome Res 12: 832-839, 2002.
57. Martineau LC and Gardiner PF. Insight into skeletal muscle mechanotransduction: MAPK activation is quantitatively related to tension. J Appl Physiol 91: 693-702, 2001.
58. Mayor C, Brudno M, Schwartz JR, Poliakov A, Rubin EM, Frazer KA, Pachter LS, and Dubchak I. VISTA: visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 16: 1046-1047, 2000.
59. McCully KK and Faulkner JA. Injury to skeletal muscle fibers of mice following lengthening contractions. J Appl Physiol 59: 119-126, 1985.
60. Moriyama M, Tsukamoto Y, Fujiwara M, Kondo G, Nakada C, Baba T, Ishiguro N, Miyazaki A, Nakamura K, Hori N, Sato K, Shomori K, Takeuchi K, Satoh H, Mori S, and Ito H. Identification of a novel human ankyrin-repeated protein homologous to CARP. Biochem Biophys Res Commun 285: 715-723, 2001.
61. Newham DJ, Jones DA, and Clarkson PM. Repeated high-force eccentric exercise: effects on muscle pain and damage. J Appl Physiol 63: 1381-1386, 1987.
62. Newham DJ, Mills KR, Quigley BM, and Edwards RH. Pain and fatigue after concentric and eccentric muscle contractions. Clin Sci (Lond) 64: 55-62, 1983.
63. Ngai J, Capetanaki YG, and Lazarides E. Expression of the genes coding for the intermediate filament proteins vimentin and desmin. Ann NY Acad Sci 455: 144-157, 1985.
64. Nicholas G, Thomas M, Langley B, Somers W, Patel K, Kemp CF, Sharma M, and Kambadur R. Titin-cap associates with, and regulates secretion of, Myostatin. J Cell Physiol 193: 120-131, 2002.
65. Omens JH, Usyk TP, Li Z, and McCulloch AD. Muscle LIM protein deficiency leads to alterations in passive ventricular mechanics. Am J Physiol Heart Circ Physiol 282: H680-H687, 2002.
66. Osbaldeston NJ, Lee DM, Cox VM, Hesketh JE, Morrison JF, Blair GE, and Goldspink DF. The temporal and cellular expression of c-fos and c-jun in mechanically stimulated rabbit latissimus dorsi muscle. Biochem J 308: 465-471, 1995.
67. Peters D, Barash IA, Burdi M, Yuan PS, Mathew L, Fridén J, and Lieber RL. Asynchronous functional, cellular, and transcriptional changes after a bout of eccentric exercise in the rat. J Physiol 553: 947-957, 2003.
68. Pizza FX, Koh TJ, McGregor SJ, and Brooks SV. Muscle inflammatory cells after passive stretches, isometric contractions, and lengthening contractions. J Appl Physiol 92: 1873-1878, 2002.
69. Porter JD, Khanna S, Kaminski HJ, Rao JS, Merriam AP, Richmonds CR, Leahy P, Li J, Guo W, and Andrade FH. A chronic inflammatory response dominates the skeletal muscle molecular signature in dystrophin-deficient mdx mice. Hum Mol Genet 11: 263-272, 2002.
70. Proske U and Morgan DL. Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol 537: 333-345, 2001.
71. Ryder JW, Fahlman R, Wallberg-Henriksson H, Alessi DR, Krook A, and Zierath JR. Effect of contraction on mitogen-activated protein kinase signal transduction in skeletal muscle. Involvement of the mitogen- and stress-activated protein kinase 1. J Biol Chem 275: 1457-1462, 2000.
72. Sacco P and Jones DA. The protective effect of damaging eccentric exercise against repeated bouts of exercise in the mouse tibialis anterior muscle. Exp Physiol 77: 757-760, 1992.
73. Sam M, Shah S, Friden J, Milner DJ, Capetanaki Y, and Lieber RL. Desmin knockout muscles generate lower stress and are less vulnerable to injury compared with wild-type muscles. Am J Physiol Cell Physiol 279: C1116-C1122, 2000.
74. Schneider AG, Sultan KR, and Pette D. Muscle LIM protein: expressed in slow muscle and induced in fast muscle by enhanced contractile activity. Am J Physiol Cell Physiol 276: C900-C906, 1999.
75. Schwane JA and Armstrong RB. Effect of training on skeletal muscle injury from downhill running in rats. J Appl Physiol 55: 969-975, 1983.
76. Seiler SH, Fischman DA, and Leinwand LA. Modulation of myosin filament organization by C-protein family members. Mol Biol Cell 7: 113-127, 1996.
77. Shah SB, Su FC, Jordan K, Milner DJ, Friden J, Capetanaki Y, and Lieber RL. Evidence for increased myofibrillar mobility in desmin-null mouse skeletal muscle. J Exp Biol 205: 321-325, 2002.
78. Sinn HW, Balsamo J, Lilien J, and Lin JJ. Localization of the novel Xin protein to the adherens junction complex in cardiac and skeletal muscle during development. Dev Dyn 225: 1-13, 2002.
79. Talbot JA and Morgan DL. Quantitative analysis of sarcomere non-uniformities in active muscle following a stretch. J Muscle Res Cell Motil 17: 261-268, 1996.
80. Thompson HS, Scordilis SP, Clarkson PM, and Lohrer WA. A single bout of eccentric exercise increases HSP27 and HSC/HSP70 in human skeletal muscle. Acta Physiol Scand 171: 187-193, 2001.
81. Trombitas K, Greaser M, Labeit S, Jin JP, Kellermayer M, Helmes M, and Granzier H. Titin extensibility in situ: entropic elasticity of permanently folded and permanently unfolded molecular segments. J Cell Biol 140: 853-859, 1998.
82. Tsukamoto Y, Senda T, Nakano T, Nakada C, Hida T, Ishiguro N, Kondo G, Baba T, Sato K, Osaki M, Mori S, Ito H, and Moriyama M. Arpp, a new homolog of carp, is preferentially expressed in type 1 skeletal muscle fibers and is markedly induced by denervation. Lab Invest 82: 645-655, 2002.
83. Tusher VG, Tibshirani R, and Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121, 2001.
84. Wang DZ, Reiter RS, Lin JL, Wang Q, Williams HS, Krob SL, Schultheiss TM, Evans S, and Lin JJ. Requirement of a novel gene, Xin, in cardiac morphogenesis. Development 126: 1281-1294, 1999.
85. Warren GL, Ingalls CP, Lowe DA, and Armstrong RB. Excitation-contraction uncoupling: major role in contraction-induced muscle injury. Exerc Sport Sci Rev 29: 82-87, 2001.
86. Warren GL, Lowe DA, Hayes DA, Karwoski CJ, Prior BM, and Armstrong RB. Excitation failure in eccentric contraction-induced injury of mouse soleus muscle. J Physiol 468: 487-499, 1993.
87. Warren GL, Lowe DA, Inman CL, Orr OM, Hogan HA, Bloomfield SA, and Armstrong RB. Estradiol effect on anterior crural muscles-tibial bone relationship and susceptibility to injury. J Appl Physiol 80: 1660-1665, 1996.
88. Willmann R, Kusch J, Sultan KR, Schneider AG, and Pette D. Muscle LIM protein is upregulated in fast skeletal muscle during transition toward slower phenotypes. Am J Physiol Cell Physiol 280: C273-C279, 2001.
89. Wretman C, Lionikas A, Widegren U, Lannergren J, Westerblad H, and Henriksson J. Effects of concentric and eccentric contractions on phosphorylation of MAPK (erk1/2) and MAPK (p38) in isolated rat skeletal muscle. J Physiol 535: 155-164, 2001.
90. Yamasaki R, Wu Y, McNabb M, Greaser M, Labeit S, and Granzier H. Protein kinase A phosphorylates titin's cardiac-specific N2B domain and reduces passive tension in rat cardiac myocytes. Circ Res 90: 1181-1188, 2002.
91. Zou Y, Evans S, Chen J, Kuo HC, Harvey RP, and Chien KR. CARP, a cardiac ankyrin repeat protein, is downstream in the Nkx2-5 homeobox gene pathway. Development 124: 793-804, 1997.