A DIGE approach for the assessment of rat soleus muscle changes during unloading: Effect of acetyl-L-carnitine supplementation

Proteomics

Volumn 8, Issue 17, 2008, Pages 3588-3604

  Moriggi, Manuela ^a   Cassano, Pierluigi ^b   Vasso, Michele ^a,c   Capitanio, Daniele ^a   Fania, Chiara ^a,c   Musicco, Clara ^c   Pesce, Vito ^b   Gadaleta, Maria Nicola ^b,c   Gelfi, Cecilia ^a,c  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF BARI   (Italy)

^c CNR   (Italy)

Author keywords

Acetyl L carnitine; Mass spectrometry; Skeletal muscle; Two dimensional in gel electrophoresis; Unloading

Indexed keywords

CHAPERONE; CITRATE SYNTHASE; COMPLEMENTARY DNA; LEVACECARNINE; MYOSIN HEAVY CHAIN; PROTEIN; PROTEIN 14 3 3; TROPONIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ENZYME ACTIVITY; GLYCOLYSIS; HINDLIMB; IMMOBILIZATION; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; RAT; SKELETAL MUSCLE; SLOW MUSCLE; SOLEUS MUSCLE; TWO DIMENSIONAL GEL ELECTROPHORESIS; TWO DIMENSIONAL IN GEL ELECTROPHORESIS;

ACETYLCARNITINE; ANIMALS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HINDLIMB SUSPENSION; MALE; MITOCHONDRIA, MUSCLE; MUSCLE PROTEINS; MUSCLE, SKELETAL; MYOSIN HEAVY CHAINS; RATS; RATS, WISTAR; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

ANIMALIA; RATTUS;

EID: 52649085309     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200701176     Document Type: Article

References (70)

1. Grigoriev, A. I., Egorov, A. D., Physiological aspects of adaptation of main human body systems during and after spaceflights. Adv. Space Biol. Med. 1992, 2, 43-82.
2. llyina-Kakueva, E. I., Portugalov, V. V., Krivenkova, N. P., Space flight effects on the skeletal muscles of rats. Aviat. Space Environ. Med. 1976, 47, 700-703.
3. Musacchia, X. J., Steffen, J. M., Fell, R. D., Dombrowski, M. J., Skeletal muscle response to spaceflight, whole body suspension, and recovery in rats. J. Appl. Physiol. 1990, 69, 2248-2253.
4. Thornton, W. E., Rummel, J.A., in: Johnston, R. S., Dietlein, L.F. (Eds.), Biomedical results from Skylab, US Government Printing office, Washington DC 1977, pp. 191-197.
5. Morey-Holton, E. R., Globus, R. K., Hindlimb unloading rodent model: technical aspects. J. Appl. Physiol. 2002, 92, 1367-1377.
6. Fortney, S. M., Schneider, V.S., Greenleaf, J.E., in: Fregly, M. J., Blatteis, C. M. (Eds.), Handbook of Physiology, Oxford University Press, New York, NY 1996, pp. 889-942.
7. Stump, C. S., Tipton, C. M., Henriksen, E. J., Muscle adaptations to hindlimb suspension in mature and old Fischer 344 rats. J. Appl. Physiol. 1997, 82, 1875-1881.
8. Thomason, D. B., Booth, F. W., Atrophy of the soleus muscle by hindlimb unweighting. J. Appl. Physiol. 1990, 68, 1-12.
9. Baldwin, K. M., Herrick, R. E., McCue, S. A., Substrate oxidation capacity in rodent skeletal muscle: effects of exposure to zero gravity. J. Appl. Physiol. 1993, 75, 2466-2470.
10. Caiozzo, V. J., Haddad, F., Baker, M. J., Herrick, R. E. et al., Microgravity-induced transformations of myosin isoforms and contractile properties of skeletal muscle. J. Appl. Physiol. 1996, 81, 123-132.
11. Campione, M., Ausoni, S., Guezennec, C. Y., Schiaffino, S., Myosin and troponin changes in rat soleus muscle after hindlimb suspension. J.Appl. Physiol. 1993, 74, 1156-1160.
12. Fitts, R. H., Riley, D. R., Widrick, J. J., Physiology of a microgravity environment invited review: microgravity and skeletal muscle. J. Appl. Physiol. 2000, 89, 823-839.
13. Acheson, K. J., Decombaz, J., Piguet-Welsch, C., Montigon, F. et al., Energy, protein, and substrate metabolism in simulated microgravity. Am. J. Physiol. 1995, 269, R252-R260.
14. Booth, F. W., Baldwin, K.M., in: Rowell, L. B., Shepherd, J. T. (Eds.), Handbook of Physiology, Oxford University Press, New York, NY 1995, pp. 1075-1123.
15. Grichko, V. P., Heywood-Cooksey, A., Kidd, K. R., Fitts, R. H., Substrate profile in rat soleus muscle fibers after hindlimb unloading and fatigue. J. Appl. Physiol. 2000, 88, 473-478.
16. Henriksen, E. J., Tischler, M. E., Johnson, D. G., Increased response to insulin of glucose metabolism in the 6-day unloaded rat soleus muscle. J. Biol. Chem. 1986, 261, 10707-10712.
17. Stump, C. S., Balon, T. W., Tipton, C. M., Effects of insulin and exercise on rat hindlimb muscles after simulated microgravity. J. Appl. Physiol. 1992, 73, 2044-2053.
18. Musacchia, X. J., Steffen, J. M., Fell, R. D., Dombrowski, M. J. et al., Skeletal muscle atrophy in response to 14 days of weightlessness: vastus medialis. J. Appl. Physiol. 1992, 73, 44S-50S.
19. Fluck, M., Schmutz, S., Wittwer, M., Hoppeler, H., Des-planches, D., Transcriptional reprogramming during reloading of atrophied rat soleus muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 289, R4-14.
20. Nikawa, T., Ishidoh, K., Hirasaka, K., Ishihara, I. et al., Skeletal muscle gene expression in space-flown rats. FASEB J. 2004, 18, 522-524.
21. Stein, T., Schluter, M., Galante, A., Soteropoulos, P. et al., Energy metabolism pathways in rat muscle under conditions of simulated microgravity. J. Nutr. Biochem. 2002, 13, 471.
22. Stevenson, E. J., Giresi, P. G., Koncarevc, A., Kandarian, S. C., Global analysis of gene expression patterns during disuse atrophy in rat skeletal muscle. J. Physiol. 2003, 551, 33-48.
23. Wittwer, M., Fluck, M., Hoppeler, H., Muller, S. et al., Prolonged unloading of rat soleus muscle causes distinct adaptations of the gene profile. FASEB J. 2002, 16, 884-886.
24. Stein, T. P., Wade, C. E., Metabolic consequences of muscle disuse atrophy. J. Nutr. 2005, 135, 1824S-1828S.
25. Stephens, F. B., Constantin-Teodosiu, D., Greenhaff, P. L., New insights concerning the role of carnitine in the regulation of fuel metabolism in skeletal muscle. J. Physiol. 2007, 581, 431-444.
26. lossa, S., Mollica, M. P., Lionetti, L., Crescenzo, R. et al., Acetyl-L-carnitine supplementation differently influences nutrient partitioning, serum leptin concentration and skeletal muscle mitochondrial respiration in young and old rats. J. Nutr. 2002, 132, 636-642.
27. Pesce, V., Fracasso, F., Musicco, C., Lezza, A. M. et al., Acetyl-L-carnitine dietary supplementation to old rats increases mitochondrial transcription factor A content in rat hindlimb skeletal muscles. Ann. N. Y.Acad. Sci. 2004, 1019, 430-433.
28. Cassano, P., Sciancalepore, A. G., Pesce, V., Fluck, M. et al., Acetyl-L-carnitine feeding to unloaded rats triggers in soleus muscle the coordinated expression of genes involved in mitochondrial biogenesis. Biochim. Biophys. Acta 2006, 1757, 1421-1428.
29. Isfort, R. J., Wang, F., Greis, K. D., Sun, Y. et al., Proteomic analysis of rat soleus muscle undergoing hindlimb suspension-induced atrophy and reweighting hypertrophy. Proteomics 2002, 2, 543-550.
30. Seo, Y., Lee, K., Park, K., Bae, K., Choi, I., A proteomic assessment of muscle contractile alterations during unloading and reloading. J. Biochem. (Tokyo) 2006, 139, 71-80.
31. Marouga, R., David, S., Hawkins, E., The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal. Bioanal. Chem. 2005, 382, 669-678.
32. Karp, N. A., Kreil, D. P., Lilley, K. S., Determining a significant change in protein expression with DeCyder during a pair-wise comparison using two-dimensional difference gel electrophoresis. Proteomics 2004, 4, 1421-1432.
33. Karp, N. A., Lilley, K. S., Maximising sensitivity for detecting changes in protein expression: experimental design using minimal CyDyes. Proteomics 2005, 5, 3105-3115.
34. Tonge, R., Shaw, J., Middleton, B., Rowlinson, R. et al., Validation and development of fluorescence two-dimensional differential gel electrophoresis proteomics technology. Proteomics 2001, 1, 377-396.
35. Gelfi, C., Vigano, A., De Palma, S., Ripamonti, M, et al., 2-D protein maps of rat gastrocnemius and soleus muscles: a tool for muscle plasticity assessment. Proteomics 2006, 6, 321-340.
36. Danieli Betto, D., Zerbato, E., Betto, R., Type 1, 2A, and 2B myosin heavy chain electrophoretic analysis of rat muscle fibers. Biochem. Biophys. Res. Commun. 1986, 138, 981-987.
37. Srere, P. A., Cytrate synthase. Methods Enzymol. 1969, 13, 3-5.
38. Pesce, V., Cormio, A., Fracasso, R, Lezza, A. M. et al., Rat hindlimb unloading: Soleus and Extensor Digitorum Longus histochemistry, mitochondrial DNA content and mitochondrial DNA deletions. Biosci. Rep. 2002, 22, 115-125.
39. Squire, J. M., Morris, E. P., A new look at thin filament regulation in vertebrate skeletal muscle. FASEB J. 1998, 12, 761-771.
40. de Tombe, P. P., Belus, A., Piroddi, N., Scellini, B. et al., Myofilament calcium sensitivity does not affect cross-bridge activation-relaxation kinetics. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292, R1129-R1136.
41. Yu, Z. B., Gao, R, Feng, H. Z., Jin, J. P., Differential regulation of myofilament protein isoforms underlying the contractility changes in skeletal muscle unloading. Am. J. Physiol. Cell. Physiol. 2007, 292, C1192-C1203.
42. Agarkova, I., Perriard, J. C., The M-band: an elastic web that crosslinks thick filaments in the center of the sarcomere. Trends Cell Biol. 2005, 15, 477-485.
43. Takada, F., Vander Woude, D. L, Tong, H. Q., Thompson, T. G. et al., Myozenin: an alpha-actinin- and gamma-filamin-binding protein of skeletal muscle Z lines. Proc. Natl. Acad. Sci. USA 2001, 98, 1595-1600.
44. Salmikangas, P., van der Ven, P. F., Lalowski, M., Taivainen, A. et al., Myotilin, the limb-girdle muscular dystrophy 1A (LGMDIA) protein, cross-links actin filaments and controls sarcomere assembly. Hum. Mol. Genet. 2003, 12, 189-203.
45. Ho, G., Chisholm, R. L., Substitution mutations in the myosin essential light chain lead to reduced actin-activated ATPase activity despite stoichiometric binding to the heavy chain. J. Biol. Chem. 1997, 272, 4522-4527.
46. Lopez-Alemany, R., Suelves, M., Diaz-Ramos, A., Vidal, B., Munoz-Canoves, P., Alpha-enolase plasminogen receptor in myogenesis. Front. Biosci. 2005, 10, 30-36.
47. Vander Jagt, D. L, Robinson, B., Taylor, K. K., Hunsaker, L. A., Aldose reductase from human skeletal and heart muscle. Interconvertible forms related by thiol-disulfide exchange. J. Biol. Chem. 1990, 265, 20982-20987.
48. Cros, N., Muller, J., Bouju, S., Pietu, G. et al., Upregulation of M-creatine kinase and glyceraldehyde3-phosphate dehydrogenase: two markers of muscle disuse. Am. J. Physiol. 1999, 276, R308-R316.
49. Ascenzi, P., Bocedi, A., Antonini, G., Bolognesi, M., Fasano, M., Reductive nitrosylation and peroxynitrite-mediated oxidation of heme-hemopexin. FEBS J. 2007, 274, 551-562.
50. Altun, M., Edstrom, E., Spooner, E., Flores-Moralez, A. et al., Iron load and redox stress in skeletal muscle of aged rats. Muscle Nerve 2007, 36, 223-233.
51. Kanatous, S. B., Garry, D. J., Gene deletional strategies reveal novel physiological roles for myoglobin in striated muscle. Respir. Physiol. Neurobiol. 2006, 151, 151-158.
52. De Palma, S., Ripamonti, M., Vigano, A., Moriggi, M. et al., Metabolic modulation induced by chronic hypoxia in rats using a comparative proteomic analysis of skeletal muscle tissue. J. Proteome Res. 2007, 6, 1974-1984.
53. Gelfi, C., Vigano, A., Ripamonti, M., Pontoglio, A. et al., The human muscle proteome in aging. J. Proteome Res. 2006, 5, 1344-1353.
54. Lawler, J. M., Song, W., Demaree, S. R., Hindlimb unloading increases oxidative stress and disrupts antioxidant capacity in skeletal muscle. Free Radic. Biol. Med. 2003, 35, 9-16.
55. Davare, M. A., Saneyoshi, T, Guire, E. S., Nygaard, S. C., Soderling, T. R., Inhibition of calcium/calmodulin-depend-ent protein kinase kinase by protein 14-3-3. J. Biol. Chem. 2004, 279, 52191-52199.
56. Fu, H., Subramanian, R. R., Masters, S. C., 14-3-3 proteins: structure, function, and regulation. Annu. Rev. Pharmacol. Toxicol. 2000, 40, 617-647.
57. di Prampero, P. E., Narici, M. V, Muscles in microgravity: from fibres to human motion. J. Biomech. 2003, 36, 403-412.
58. Berchtold, M. W., Brinkmeier, H., Muntener, M., Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease. Physiol. Rev. 2000, 80, 1215-1265.
59. 2+/calmodulin-dependent kinases in skeletal muscle plasticity. J. Appl. Physiol. 2005, 99, 414-423.
60. Pette, D., Staron, R. S., Mammalian skeletal muscle fiber type transitions. Int. Rev. Cytol. 1997, 170, 143-223.
61. Gros, G., Dodgson, S. J., Velocity of CO2 exchange in muscle and liver. Annu. Rev. Physiol. 1988, 50, 669-694.
62. Cote, C., Riverin, H., Barras, M. J., Tremblay, R. R. et al., Effect of carbonic anhydrase III inhibition on substrate utilization and fatigue in rat soleus. Can. J. Physiol. Pharmacol. 1993, 71, 277-283.
63. Cote, C. H., Ambrosio, F., Perreault, G., Metabolic and contractile influence of carbonic anhydrase III in skeletal muscle is age dependent. Am. J. Physiol. 1999, 276, R559-R565.
64. Zimmerman, U. J., Wang, P., Zhang, X., Bogdanovich, S., Forster, R., Anti-oxidative response of carbonic anhydrase III in skeletal muscle. IUBMB Life 2004, 56, 343-347.
65. Arcuri, C., Giambanco, I., Bianchi, R., Donato, R., Annexin V, annexin VI, S100A1 and S100B in developing and adult avian skeletal muscles. Neuroscience 2002, 109, 371-388.
66. Kusano, H., Shimizu, S., Koya, R. C., Fujita, H. et al., Human gelsolin prevents apoptosis by inhibiting apoptotic mitochondrial changes via closing VDAC. Oncogene 2000, 19, 4807-4814.
67. Roman, I., Figys, J., Steurs, G., Zizi, M., Direct measurement of VDAC-actin interaction by surface plasmon resonance. Biochim. Biophys. Acta 2006, 1758, 479-486.
68. Anderson, T. J., Tchernyshyov, I., Diez, R., Cole, R. N. et al., Discovering robust protein biomarkers for disease from relative expression reversals in 2-D DIGE data. Proteomics 2007, 7, 1197-1207.
69. Fodor, I. K., Nelson, D. O., Alegria-Hartman, M., Robbins, K. et al., Statistical challenges in the analysis of two-dimensional difference gel electrophoresis experiments using DeCyder. Bioinformatics 2005, 21, 3733-3740.
70. Wredenberg, A., Wibom, R., Wilhelmsson, H., Graff, C. et al., Increased mitochondrial mass in mitochondrial myopathy mice. Proc. Natl. Acad. Sci. USA 2002, 99, 15066-15071.