Body weight-dependent troponin T alternative splicing is evolutionarily conserved from insects to mammals and is partially impaired in skeletal muscle of obese rats

Journal of Experimental Biology

Volumn 214, Issue 9, 2011, Pages 1523-1532

  Schilder, Rudolf J ^a   Kimball, Scot R ^a   Marden, James H ^b   Jefferson, Leonard S ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Alternative splicing; Body composition; Body weight; Energetics; Gastrocnemius; Metabolic rate; Muscle performance; Obesity; Skeletal muscle; Tnnt3; Troponin T; Weight sensing

Indexed keywords

TNNT3 PROTEIN, RAT; TROPONIN T;

ALTERNATIVE RNA SPLICING; ANIMAL; ARTICLE; BODY COMPOSITION; BODY WEIGHT; ENERGY METABOLISM; GENETICS; INSECT; MALE; MAMMAL; METABOLISM; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; OBESITY; ORGAN SIZE; RAT; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT; ZUCKER RAT;

ALTERNATIVE SPLICING; ANIMALS; BODY COMPOSITION; BODY WEIGHT; CONSERVED SEQUENCE; ENERGY METABOLISM; EVOLUTION, MOLECULAR; INSECTS; MALE; MAMMALS; MUSCLE, SKELETAL; OBESITY; ORGAN SIZE; RATS; RATS, SPRAGUE-DAWLEY; RATS, ZUCKER; TROPONIN T;

ANIMALIA; HEXAPODA; MAMMALIA; RATTUS;

EID: 79954995446     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.051763     Document Type: Article

References (58)

1. Anandacoomarasamy, A., Caterson, I., Sambrook, P., Fransen, M. and March, L. (2008). The impact of obesity on the musculoskeletal system. Int. J. Obes. (Lond.) 32, 2112-2122.
2. Anthony, J. C., Yoshizawa, F., Anthony, T. G., Vary, T. C., Jefferson, L. S. and Kimball, S. R. (2000). Leucine stimulates translation initiation in skeletal muscle of postabsorptive rats via a rapamycin-sensitive pathway. J. Nutr. 130, 2413-2419.
3. Atherton, P. J., Szewczyk, N. J., Selby, A., Rankin, D., Hillier, K., Smith, K., Rennie, M. J. and Loughna, P. T. (2009). Cyclic stretch reduces myofibrillar protein synthesis despite increases in FAK and anabolic signalling in L6 cells. J. Physiol. 587, 3719-3727.
4. Biewener, A. A. (1989). Scaling body support in mammals: limb posture and muscle mechanics. Science 245, 45-48. (Pubitemid 19180244)
5. Blaustein, M., Pelisch, F., Tanos, T., Muñoz, M. J., Wengier, D., Quadrana, L., Sanford, J. R., Muschietti, J. P., Kornblihtt, A. R., Cáceres, J. F. et al. (2005). Concerted regulation of nuclear and cytoplasmic activities of SR proteins by AKT. Nat. Struct. Mol. Biol. 12, 1037-1044. (Pubitemid 41746773)
6. Blaustein, M., Quadrana, L., Risso, G., Mata, M. D. L., Pelisch, F. and Srebrow, A. (2009). SF2/ASF regulates proteomic diversity by affecting the balance between translation initiation mechanisms. J. Cell. Biochem. 107, 826-833.
7. Bolster, D. R., Kubica, N., Crozier, S. J., Williamson, D. L., Farrell, P. A., Kimball, S. R. and Jefferson, L. S. (2003). Immediate response of mammalian target of rapamycin (mTOR)-mediated signalling following acute resistance exercise in rat skeletal muscle. J. Physiol. 553, 213-220. (Pubitemid 37483929)
8. Bray, G. A. (1977). The Zucker-fatty rat: a review. Fed. Proc. 36, 148-153.
9. Briggs, M. M. and Schachat, F. (1996). Physiologically regulated alternative splicing patterns of fast troponin T RNA are conserved in mammals. Am. J. Physiol. Cell Physiol. 270, C298-C305.
10. Brotto, M. A. (2005). Coupled expression of troponin T and troponin I isoforms in single skeletal muscle fibers correlates with contractility. Am. J. Physiol. Cell Physiol. 290, C567-C576.
11. Chandra, M., Tschirgi, M. L., Rajapakse, I. and Campbell, K. B. (2006). Troponin T modulates sarcomere length-dependent recruitment of cross-bridges in cardiac muscle. Biophys. J. 90, 2867-2876.
12. Galgani, J. and Ravussin, E. (2008). Energy metabolism, fuel selection and body weight regulation. Int. J. Obes. Relat. Metab. Disord. 32 Suppl. 7, S109-S119.
13. Goldsmith, R., Joanisse, D. R., Gallagher, D., Pavlovich, K., Shamoon, E., Leibel, R. L. and Rosenbaum, M. (2010). Effects of experimental weight perturbation on skeletal muscle work efficiency, fuel utilization, and biochemistry in human subjects. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R79-R88.
14. Gomes, A. V., Barnes, J. A., Harada, K. and Potter, J. D. (2004). Role of troponin T in disease. Mol. Cell. Biochem. 263, 115-129. (Pubitemid 39256150)
15. Greaser, M. L., Moss, R. L. and Reiser, P. J. (1988). Variations in contractile properties of rabbit single muscle fibres in relation to troponin T isoforms and myosin light chains. J. Physiol. 406, 85-98.
16. Hartner, K. T., Kirschbaum, B. J. and Pette, D. (1989). The multiplicity of troponin T isoforms. Distribution in normal rabbit muscles and effects of chronic stimulation. Eur. J. Biochem. 179, 31-38. (Pubitemid 19097655)
17. Ho, T. H., Charlet, B. N., Poulos, M. G., Singh, G., Swanson, M. S. and Cooper, T. A. (2004). Muscleblind proteins regulate alternative splicing. EMBO J. 23, 3103-3112. (Pubitemid 39093604)
18. Hornberger, T. A., Armstrong, D. D., Koh, T. J., Burkholder, T. J. and Esser, K. A. (2005). Intracellular signaling specificity in response to uniaxial vs. multiaxial stretch: implications for mechanotransduction. Am. J. Physiol. Cell Physiol. 288, C185-C194. (Pubitemid 39658441)
19. Hulens, M., Vansant, G., Lysens, R., Claessens, A. L., Muls, E. and Brumagne, S. (2001). Study of differences in peripheral muscle strength of lean versus obese women: an allometric approach. Int. J. Obes. Relat. Metab. Disord. 25, 676-681. (Pubitemid 32417637)
20. Jackson, A. W., Lee, D.-C., Sui, X., Morrow, J. R., Church, T. S., Maslow, A. L. and Blair, S. N. (2009). Muscular strength is inversely related to prevalence and incidence of obesity in adult men. Obesity (Silver Spring) 18, 1988-1995.
21. Karni, R., Hippo, Y., Lowe, S. W. and Krainer, A. R. (2008). The splicing-factor oncoprotein SF2/ASF activates mTORC1. Proc. Natl. Acad. Sci. USA 105, 15323-15327.
22. Katta, A., Karkala, S. K., Wu, M., Meduru, S., Desai, D. H., Rice, K. M. and Blough, E. R. (2009). Lean and obese Zucker rats exhibit different patterns of p70s6 kinase regulation in the tibialis anterior muscle in response to high-force muscle contraction. Muscle Nerve 39, 503-511.
23. Kemp, J. G., Blazev, R., Stephenson, D. G. and Stephenson, G. M. M. (2009). Morphological and biochemical alterations of skeletal muscles from the genetically obese (ob/ob) mouse. Int. J. Obes. Relat. Metab. Disord. 33, 831-841.
24. Kim, Y. B., Peroni, O. D., Franke, T. F. and Kahn, B. B. (2000). Divergent regulation of Akt1 and Akt2 isoforms in insulin target tissues of obese Zucker rats. Diabetes 49, 847-856. (Pubitemid 30340003)
25. Kimball, S. R. and Jefferson, L. S. (2006). Signaling pathways and molecular mechanisms through which branched-chain amino acids mediate translational control of protein synthesis. J. Nutr. 136, 227S-231S. (Pubitemid 43156513)
26. Kimball, S. R., Jefferson, L. S., Nguyen, H. V., Suryawan, A., Bush, J. A. and Davis, T. A. (2000). Feeding stimulates protein synthesis in muscle and liver of neonatal pigs through an mTOR-dependent process. Am. J. Physiol. Endocrinol. Metab. 279, E1080-E1087.
27. Lafortuna, C. L., Maffiuletti, N. A., Agosti, F. and Sartorio, A. (2005). Gender variations of body composition, muscle strength and power output in morbid obesity. Int. J. Obes. (Lond.) 29, 833-841. (Pubitemid 40897022)
28. Lang, C. H., Frost, R. A. and Vary, T. C. (2007). Regulation of muscle protein synthesis during sepsis and inflammation. Am. J. Physiol. Endocrinol. Metab. 293, E453-E459. (Pubitemid 47205087)
29. Larson, D. E., Ferraro, R. T., Robertson, D. S. and Ravussin, E. (1995). Energy metabolism in weight-stable postobese individuals. Am. J. Clin. Nutr. 62, 735-739.
30. Levin, B. E. (2006). Central regulation of energy homeostasis intelligent design: how to build the perfect survivor. Obesity (Silver Spring) 14 Suppl. 5, 192S-196S.
31. Levine, J. A., Lanningham-Foster, L. M., McCrady, S. K., Krizan, A. C., Olson, L. R., Kane, P. H., Jensen, M. D. and Clark, M. M. (2005). Interindividual variation in posture allocation: possible role in human obesity. Science 307, 584-586. (Pubitemid 40165681)
32. Lynch, K. W. (2007). Regulation of alternative splicing by signal transduction pathways. Adv. Exp. Med. Biol. 623, 161-174.
33. MacFarland, S. M., Jin, J. P. and Brozovich, F. V. (2002). Troponin T isoforms modulate calcium dependence of the kinetics of the cross-bridge cycle: studies using a transgenic mouse line. Arch. Biochem. Biophys. 405, 241-246. (Pubitemid 35191738)
34. Marden, J. H., Fitzhugh, G. H., Wolf, M. R., Arnold, K. D. and Rowan, B. (1999). Alternative splicing, muscle calcium sensitivity, and the modulation of dragonfly flight performance. Proc. Natl. Acad. Sci. USA 96, 15304-15309. (Pubitemid 30019807)
35. Marden, J. H., Fitzhugh, G. H., Girgenrath, M., Wolf, M. R. and Girgenrath, S. (2001). Alternative splicing, muscle contraction and intraspecific variation: associations between troponin T transcripts, Ca(2+) sensitivity and the force and power output of dragonfly flight muscles during oscillatory contraction. J. Exp. Biol. 204, 3457-3470. (Pubitemid 34861325)
36. Marden, J. H., Fescemyer, H. W., Saastamoinen, M., Macfarland, S. P., Vera, J. C., Frilander, M. J. and Hanski, I. (2008). Weight and nutrition affect pre-mRNA splicing of a muscle gene associated with performance, energetics and life history. J. Exp. Biol. 211, 3653-3660.
37. McMinn, J. E., Baskin, D. G. and Schwartz, M. W. (2000). Neuroendocrine mechanisms regulating food intake and body weight. Obes. Rev. 1, 37-46.
38. Medford, R. M., Nguyen, H. T., Destree, A. T., Summers, E. and Nadal-Ginard, B. (1984). A novel mechanism of alternative RNA splicing for the developmentally regulated generation of troponin T isoforms from a single gene. Cell 38, 409-421. (Pubitemid 14022035)
39. Morton, G. J., Cummings, D. E., Baskin, D. G., Barsh, G. S. and Schwartz, M. W. (2006). Central nervous system control of food intake and body weight. Nature 443, 289-295. (Pubitemid 44435142)
40. Nassar, R., Malouf, N. N., Mao, L., Rockman, H. A., Oakeley, A. E., Frye, J. R., Herlong, J. R., Sanders, S. P. and Anderson, P. A. (2005). cTnT1, a cardiac troponin T isoform, decreases myofilament tension and affects the left ventricular pressure waveform. Am. J. Physiol. Heart Circ. Physiol. 288, H1147-H1156. (Pubitemid 40270018)
41. Ogut, O., Granzier, H. and Jin, J. P. (1999). Acidic and basic troponin T isoforms in mature fast-twitch skeletal muscle and effect on contractility. Am. J. Physiol. 276, C1162-C1170. (Pubitemid 29244672)
42. Pan, B. S. and Potter, J. D. (1992). Two genetically expressed troponin T fragments representing alpha and beta isoforms exhibit functional differences. J. Biol. Chem. 267, 23052-23056.
43. Perry, S. (1998). Troponin T: genetics, properties and function. J. Muscle Res. Cell Motil. 19, 575-602. (Pubitemid 28380399)
44. Rosenkilde, M., Nordby, P., Nielsen, L. B., Stallknecht, B. M. and Helge, J. W. (2010). Fat oxidation at rest predicts peak fat oxidation during exercise and metabolic phenotype in overweight men. Int. J. Obes. Relat. Metab. Disord. 34, 871-877.
45. Salati, L. M. and Amir-Ahmady, B. (2001). Dietary regulation of expression of glucose-6-phosphate dehydrogenase. Annu. Rev. Nutr. 21, 121-140. (Pubitemid 32695267)
46. Salati, L. M., Szeszel-Fedorowicz, W., Tao, H., Gibson, M. A., Amir-Ahmady, B., Stabile, L. P. and Hodge, D. L. (2004). Nutritional regulation of mRNA processing. J. Nutr. 134, 2437S-2443S. (Pubitemid 39201618)
47. Sanford, J. R., Ellis, J. D., Cazalla, D. and Cáceres, J. F. (2005). Reversible phosphorylation differentially affects nuclear and cytoplasmic functions of splicing factor 2/alternative splicing factor. Proc. Natl. Acad. Sci. USA 102, 15042-15047. (Pubitemid 41513331)
48. Sasai, N., Agata, N., Inoue-Miyazu, M., Kawakami, K., Kobayashi, K., Sokabe, M. and Hayakawa, K. (2010). Involvement of PI3K/Akt/TOR pathway in stretch-induced hypertrophy of myotubes. Muscle Nerve 41, 100-106.
49. Schachat, F. H., Diamond, M. S. and Brandt, P. W. (1987). Effect of different troponin T-tropomyosin combinations on thin filament activation. J. Mol. Biol. 198, 551-554.
50. Schwartz, M. W., Woods, S. C., Porte, D., Seeley, R. J. and Baskin, D. G. (2000). Central nervous system control of food intake. Nature 404, 661-671. (Pubitemid 30205071)
51. Spangenburg, E. E. (2009). Changes in muscle mass with mechanical load: possible cellular mechanisms. Appl. Physiol. Nutr. Metab. 34, 328-335.
52. Stefancsik, R., Randall, J. D., Mao, C. and Sarkar, S. (2003). Structure and sequence of the human fast skeletal troponin T (TNNT3) gene: insight into the evolution of the gene and the origin of the developmentally regulated isoforms. Comp. Funct. Genomics 4, 609-625. (Pubitemid 38088671)
53. Stevens, L., Bozzo, C., Nemirovskaya, T., Montel, V., Falempin, M. and Mounier, Y. (2003). Contractile properties of rat single muscle fibers and myosin and troponin isoform expression after hypergravity. J. Appl. Physiol. 94, 2398-2405. (Pubitemid 36605303)
54. Varma, V., Yao-Borengasser, A., Rasouli, N., Nolen, G. T., Phanavanh, B., Starks, T., Gurley, C., Simpson, P., McGehee, R. E., Jr, Kern, P. A. et al. (2009). Muscle inflammatory response and insulin resistance: synergistic interaction between macrophages and fatty acids leads to impaired insulin action. Am. J. Physiol. Endocrinol. Metab. 296, E1300-E1310.
55. Wang, J. and Jin, J. P. (1997). Primary structure and developmental acidic to basic transition of 13 alternatively spliced mouse fast skeletal muscle troponin T isoforms. Gene 193, 105-114. (Pubitemid 27303610)
56. Wisse, B. E. (2004). The inflammatory syndrome: the role of adipose tissue cytokines in metabolic disorders linked to obesity. J. Am. Soc. Nephrol. 15, 2792-2800. (Pubitemid 41103388)
57. Xiong, Z., Shaibani, A., Li, Y.-P., Yan, Y., Zhang, S., Yang, Y., Yang, F., Wang, H. and Yang, X.-F. (2006). Alternative splicing factor ASF/SF2 is down regulated in inflamed muscle. J. Clin. Pathol. 59, 855-861. (Pubitemid 44211749)
58. Yu, Z. B., Gao, F., Feng, H. Z. and Jin, J.-P. (2006). Differential regulation of myofilament protein isoforms underlying the contractility changes in skeletal muscle unloading. Am. J. Physiol. Cell Physiol. 292, C1192-C1203. (Pubitemid 46440404)