Increased contractile activity decreases RNA-protein interaction in the 3'-UTR of cytochrome C mRNA

American Journal of Physiology - Cell Physiology

Volumn 271, Issue 4 40-4, 1996, Pages

  Yan, Zhen ^b   Salmons, Stanley ^b   Dang, Yan Li ^b   Hamilton, Marc T ^b   Booth, Frank W ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b NONE

Author keywords

3' untranslated region; chronic stimulation; inhibitor; ribonucleic acid protein binding; skeletal muscle

Indexed keywords

CYTOCHROME C; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION; MUSCLE CONTRACTILITY; MUSCLE EXCITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE;

ANIMALIA;

EID: 0029862518     PISSN: 03636143     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.1996.271.4.c1157     Document Type: Article

References (54)

1. Annex, B. H., W. E. Kraus, G. L. Dohm, and R. S. Williams. Mitochondrial biogenesis in striated muscles: rapid induction of citrate synthase mRNA by nerve stimulation. Am. J. Physiol. 260 (Cell Physiol. 29): C266-C270, 1991.
2. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. Current Protocols in Molecular Biology. New York: Wiley, 1991, vol. 2, p. 11.2.1-11.2.7.
3. Babij, P., and F. W. Booth. α-Actin and cytochrome c mRNAs in atrophied adult rat skeletal muscle. Am. J. Physiol. 254 (Cell Physiol. 23): C651-C656, 1988.
4. Baldwin, K. M., G. H. Klinkerfuss, R. L. Terjung, P. A. Molé, and J. O. Holloszy. Respiratory capacity of white, red, and intermediate muscle: adaptative response to exercise. Am. J. Physiol. 222: 373-378, 1972.
5. Bernstein, P., S. W. Peltz, and J. Ross. The poly(A)-poly(A)-binding protein complex is a major determinant of mRNA stability in vitro. Mol. Cell. Biol. 9: 659-670, 1989.
6. Berry, M. J., L. Banu, Y. Y. Chen, S. J. Mandel, J. D. Kieffer, J. W. Harney, and P. R. Larsen. Recognition of UGA as a selenocysteine codon in type I deiodinase requires sequences in the 3′ untranslated region. Nature Lond. 353: 273-276, 1991.
7. Carson, J. A., Z. Yan, F. W. Booth, M. E. Coleman, R. J. Schwartz, and C. S. Stump. Regulation of skeletal α-actin promoter in young chickens during hypertrophy caused by stretch overload. Am. J. Physiol. 268 (Cell Physiol. 37): C918-C924, 1995.
8. Casey, J. L., D. M. Koeller, V. C. Ramin, R. D. Klausner, and J. B. Harford. Iron regulation of transferrin receptor mRNA levels requires iron-responsive elements and a rapid turnover determinant in the 3′ untranslated region of the mRNA. EMBO J. 8: 3693-3699, 1989.
9. Chomczynski, P., and N. Sacchi. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156-159, 1987.
10. Ciske, P. E., and J. A. Faulkner. Chronic electrical stimulation of nongrafted and grafted skeletal muscles in rats. J. Appl. Physiol. 59: 1434-1439, 1985.
11. Davies, K. J., L. Packer, and G. A. Brooks. Biochemical adaptation of mitochondria, muscle, whole-animal respiration to endurance training. Arch. Biochem. Biophys. 209: 539-554, 1981.
12. Dodson, R. E., and D. J. Shapiro. An estrogen-inducible protein binds specifically to a sequence in the 3′ untranslated region of estrogen-stabilized vitellogenin mRNA. Mol. Cell. Biol. 14: 3130-3138, 1994.
13. Eisenberg, B. R., and S. Salmons. The reorganization of subcellular structure in muscle undergoing fast-to-slow type transformation. A stereological study. Cell Tissue Res. 220: 449-471, 1981.
14. Evans, M. J., and R. C. Scarpulla. Both upstream and intron sequence elements are required for elevated expression of the rat somatic cytochrome c gene in COS-1 cells. Mol. Cell. Biol. 8: 35-41, 1988.
15. Fitts, R. H., F. W. Booth, W. W. Winder, and J. O. Holloszy. Skeletal muscle respiratory capacity, endurance, and glycogen utilization. Am. J. Physiol. 228: 1029-1033, 1975.
16. Gillis, P., and J. S. Malter. The adenosine-uridine binding factor recognizes the AU-rich elements of cytokine, lymphokine, and oncogene mRNAs. J. Biol. Chem. 266: 3172-3177, 1991.
17. Gilman, M. Current Protocols in Molecular Biology. New York: Wiley, 1989, p. 4.7.1-4.7.6.
18. Gorospe, M., and C. Baglioni. Degradation of unstable interleukin-1α mRNA in rabbit reticulocyte cell-free system. Localization of an instability determinant to a cluster of AUUUA motifs. J. Biol. Chem. 269: 11845-11851, 1994.
19. Gupte, S. S., and C. R. Hackenbrock. The role of cytochrome c diffusion in mitochondrial electron transport. J. Biol. Chem. 263: 5248-5253, 1988.
20. Hatefi, Y. The mitochondrial electron transport and oxidative phosphorylation system. Annu. Rev. Biochem. 54: 1015-1069, 1985.
21. Henriksson, J., M. M. Chi, C. S. Hintz, D. A. Young, K. K. Kaiser, S. Salmons, and O. H. Lowry. Chronic stimulation of mammalian muscle: changes in enzymes of six metabolic pathways. Am. J. Physiol. 251 (Cell Physiol. 20): C614-C632, 1986.
22. Holloszy, J. O. Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J. Biol. Chem. 242: 2278-2282, 1967.
23. Holloszy, J. O., and E. F. Coyle. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J. Appl. Physiol. 56: 831-838, 1984.
24. Jarvis, J. C., and S. Salmons. A family of neuromuscular stimulators with optical transcutaneous control. J. Med. Eng. Technol. 15: 53-57, 1991.
25. Jemmerson, R., C. Mueller, and D. Flaa. Differences in heavy chain amino acid sequences affecting the specificity of antibodies for variants of cytochrome c. Mol. Immunol. 30: 1107-1114, 1993.
26. Kraus, W. E., T. S. Bernard, and R. S. Williams. Interactions between sustained contractile activity and β-adrenergic receptors in regulation of gene expression in skeletal muscles. Am. J. Physiol. 256 (Cell Physiol. 25): C506-C514, 1989.
27. Lake, R. A., D. Wotten, and M. J. Owen. A 3′ transcriptional enhancer regulates tissue-specific expression of the human CD2 gene. EMBO J. 9: 3129-3136, 1990.
28. Layne, E. Spectrophotometric and turbidometric methods for measuring proteins. Methods Enzymol. 3: 448-450, 1957.
29. Lehninger, A. L. Biochemistry (2nd ed.). New York: Worth, 1975, p. 381.
30. Mayne, C. N., T. Mokrush, J. C. Jarvis, S. J. Gilroy, and S. Salmons. Stimulation-induced expression of slow muscle myosin in a fast muscle of the rat. Evidence of an unrestricted adaptive capacity. FEBS Lett. 327: 297-300, 1993.
31. Molé, P. A., L. B. Oscai, and J. O. Holloszy. Adaptation of muscle to exercise. Increase in levels of palmityl CoA synthetase, carnitine palmityltransferase, and palmityl CoA dehydrogenase, and in the capacity of oxidize fatty acids. J. Clin. Invest. 50: 2323-2330, 1971.
32. Moseley, P. L., E. S. Wallen, J. D. McCafferty, S. Flanagan, and J. A. Kern. Heat stress regulates the human 70-kDa heat-shock gene through the 3′-untranslated region. Am. J. Physiol. 264 (Lung Cell. Mol. Physiol. 8): L533-L537, 1993.
33. Müllner, E. W., and L. C. Kühn. A stem-loop in the 3′ untranslated region mediates iron-dependent regulation of transferrin receptor mRNA stability in the cytoplasm. Cell 53: 815-825, 1988.
34. Munro, H. N., and A. Fleck. Analysis of tissues and body fluids for nitrogenous constituents. In: Mammalian Protein Metabolism, edited by H. N. Munro. New York: Academic, 1969, vol. III, p. 424-525.
35. Nagley, P., and A. W. Linnane. Mitochondrial DNA deficient petite mutants of yeast. Biochem. Biophys. Res. Commun. 39: 989-996, 1970.
36. Neufer, P. D., and G. L. Dohm. Exercise induces a transient increase in transcription of the GLUT-4 gene in skeletal muscle. Am. J. Physiol. 265 (Cell Physiol. 34): C1597-C1603, 1993.
37. Ostareck-Lederer, A., D. H. Ostareck, N. Standart, and B. J. Thiele. Translation of 15-lipoxygenase mRNA is inhibited by a protein that binds to a repeated sequence in the 3′ untranslated region. EMBO J. 13: 1476-1481, 1994.
38. Pette, D., M. E. Smith, H. W. Staudte, and G. Vrbová. Effects of long-term electrical stimulation on some contractile and metabolic characteristics of fast rabbit muscles. Pfluegers Arch. 338: 257-272, 1973.
39. Reichmann, H., H. Hoppler, O. Mathieu-Costello, F. von Bergen, and D. Pette. Biochemical and ultrastructural changes of skeletal muscle mitochondria after chronic electrical stimulation in rabbits. Pfluegers Arch. 404: 1-9, 1985.
40. Rondon, I. J., L. A. MacMillian, B. S. Beckman, M. A. Goldberg, T. Schneider, H. F. Bunn, and J. S. Malter. Hypoxia upregulates the activity of a novel erythropoietin mRNA binding protein. J. Biol. Chem. 266: 16594-16598, 1991.
41. Ross, J., and G. Kobs. H4 histone messenger RNA decay in cell-free extracts initiates at or near the 3′ terminus and proceeds 3′ to 5′. J. Mol. Biol. 188: 579-593, 1986.
42. Saccomanno, C. F., M. Bordonaro, J. S. Chen, and J. L. Nordstrom. A faster ribonuclease protection assay. Biotechniques 13: 847-849, 1992.
43. Sachs, A. B. Messenger RNA degradation in eukaryotes. Cell 74: 413-421, 1993.
44. St. Johnston, D. The intracellular localization of messenger RNAs. Cell 81: 161-170, 1995.
45. Sambrook, J., E. F. Fritsch, and T. Maniatis. Molecular Cloning: A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor, 1989, p. 1.40; p. E18-E19.
46. Scarpulla, R. C., K. M. Agne, and R. Wu. Isolation and structure of a rat cytochrome c gene. J. Biol. Chem. 256: 6480-6486, 1981.
47. Seedorf, U., E. Leberer, B. J. Kirschbaum, and D. Pette. Neural control of gene expression in skeletal muscle. Effects of chronic stimulation on lactate dehydrogenase isoenzymes and citrate synthase. Biochem. J. 239: 115-120, 1986.
48. Sonenberg, N. mRNA translation: influence of the 5′ and 3′ untranslated regions. Curr. Opin. Genet. Dev. 4: 310-315, 1994.
49. Standart, N., and M. Dale. Regulated polyadenylation of clam maternal mRNAs in vitro. Dev. Genet. 14: 492-499, 1993.
50. Takahashi, M., D. T. McCurdy, D. A. Essig, and D. A. Hood. Delta-aminolaevulinate synthase expression in muscle after contractions and recovery. Biochem. J. 291: 219-223, 1993.
51. Taniuchi, H., M. Basile, M. Taniuchi, and D. Veloso. Evidence for formation of two thioether bonds to link heme to apocytochrome c by partially purified cytochrome c synthetase. J. Biol. Chem. 258: 10963-10966, 1983.
52. Williams, R. S., M. Garcia-Moll, J. Mellor, S. Salmons, and W. Harlan. Adaptation of skeletal muscle to increased contractile activity. Expression of nuclear genes encoding mitochondrial proteins. J. Biol. Chem. 262: 2764-2767, 1987.
53. Yan, Z., S. Salmons, J. Jarvis, and F. W. Booth. Increased muscle carnitine palmitoyltransferase II mRNA after increased contractile activity. Am. J. Physiol. 268 (Endocrinol. Metab. 31): E277-E281, 1995.
54. You, Y., C.-Y. A. Chen, and A.-B. Shyu. U-rich sequence-binding proteins (URBPs) interacting with a 20-nucleotide U-rich sequence in the 3′ untranslated region of c-fos mRNA may be involved in the first step of c-fos mRNA degradation. Mol. Cell. Biol. 12: 2931-2940, 1992.