Localization of cardiac α-myosin heavy chain mRNA is regulated by its 3' untranslated region via mechanical activity and translational block

Journal of Cell Science

Volumn 110, Issue 23, 1997, Pages 2969-2978

  Goldspink, Paul H ^a   Sharp, W W ^a   Russell, Brenda ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

3' Untranslated region; Contraction; Localization of mRNA; Myocyte

Indexed keywords

BETA GALACTOSIDASE; CYCLOHEXIMIDE; MESSENGER RNA; MYOSIN HEAVY CHAIN; VERAPAMIL;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HEART MUSCLE CELL; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; MUSCLE FIBRIL; NEWBORN; NONHUMAN; PLASMID; PRIORITY JOURNAL; RAT;

ANIMALS; BETA-GALACTOSIDASE; CALCIUM; CELL MEMBRANE; CELL NUCLEUS; CELLS, CULTURED; CYCLOHEXIMIDE; HEART; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOFIBRILS; MYOSIN HEAVY CHAINS; PROTEIN BIOSYNTHESIS; RATS; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; TRANSFECTION; VERAPAMIL;

ANIMALIA;

EID: 0031440111     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (45)

1. Clark, W. A. (1976). Selective control of fibroblast proliferation and its effect on cardiac muscle differentiation. Dev. Biol. 52, 263-282.
2. Cripe, L., Morris, E. and Fulton, A. B. (1993). Vimentin mRNA location changes during muscle development. Proc. Nat. Acad. Sci. USA 90, 2724-2728.
3. Dix, D. J. and Eisenberg, B. R. (1990). Myosin mRNA accumulation and myofibrillogenesis at the myotendinous junction of stretched muscle fibers. J. Cell Biol. 111, 1885-1894.
4. Driever, W. and Nusslein-Volhard, C. (1989). The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo. Nature 337, 138-143.
5. Eisenberg, B. R. (1987). Quantitative morphometry of isolated cells. In Isolated Muscle Cells as a Physiological Model (M. Lieberman et al.). Am. J. Physiol.: Cell Physiol. 22, C349-C363.
6. Eisenberg, B. R., Mathias, R. T. and Gilai, A. (1987). The intracellular localization of markers within injected or cut frog muscle fibers. Am. J. Physiol. 6, C50-C55.
7. Eisenberg, B. R., Goldspink, P. H. and Wenderoth, M. P. (1991). Distribution of myosin heavy chain mRNA in normal and hyperthyroid heart. J. Mol. Cell. Cardiol. 23, 287-296.
8. Epstein, H. F. and Fischman, D. A. (1991). Molecular analysis of protein assembly in muscle development. Science 251, 1039-1044.
9. Garcia, J. and Beam, K. G. (1994). Measurement of calcium transients and slow calcium current in myotubes. J. Gen. Physiol. 103, 107-123.
10. Garner, C. C., Tucker, R. P. and Matus A. (1988). Selective localization of messenaer RNA for cytoskeletal protein MAP2 on dendrites. Nature 336, 674-677.
11. Gavis, E. R. and Lehmann, R. (1994). Translational regulation of nanos by RNA localization. Nature 369, 315-318.
12. Goldspink, P. H. and Russell, B. (1996). Physiological role of phosphorylation of the cAMP response element binding protein in rat cardiac nuclei. Cell Tissue Res. 285, 379-386.
13. Goldspink, P. H., Thomason, D. B. and Russell, B. (1996). Beating affects the post-transcriptional regulation of α-myosin mRNA in cardiac cultures. (Heart Circ. Physiol. 40), Am. J. Physiol. 271, H2584-H2590.
14. Hesketh, J., Campbell, G. and Loveridge, N. (1991). Myosin heavy chain mRNA is present in both myofibrillar and subsarcolemmal regions of muscle fibres. Biochem J. 279, 309-310.
15. Hesketh, J., Campbell, G., Piechaczyk, M. and Blanchard, J.-M. (1994). Targeting of c-myc and β-globin coding sequences to cytoskeletal-bound polysomes by c-myc 3′ untranslated region. Biochem J. 298, 143-148.
16. Hoock, T. C., Newcomb, P. M. and Herman, I. M. (1991). β-Actin and its mRNA are localized at the plasma membrane and the region of moving cytoplasm during the cellular response to injury. J. Cell Biol. 112, 653-664.
17. Isaacs, W. B. and Fulton, A. B. (1987). Cotranslational assembly of myosin heavy chain in developing cultured skeletal muscle. Proc. Nat. Acad. Sci. USA 84, 6174-6178.
18. Ivester, C. T., Tuxworth, W. J., Cooper IV, G. and McDermott, P. J. (1995). Contraction accelerates myosin heavy chain synthesis rates in adult cardiocytes by an increase in the rate of translation initiation. J. Biol. Chem. 270, 21950-21957.
19. Jackson R. J. and Standart, N. (1990). Do the poly A tail and 3′untranslated region control mRNA translation? Cell 62, 15-24.
20. Kato, S., Ivester, C. T., Cooper IV, G., Zile, M. R. and McDermott, P. J. (1995). Growth effects of electrically stimulated contraction on adult feline cardiocytes in primary culture. Am. J. Physiol. 268, H2495-H2504.
21. Kim-Ha, J., Webster, P. J., Smith, J. L. and MacDonald, P. M. (1993). Multiple RNA regulatory elements mediate distinct steps in localization of oskar mRNA. Development 119, 169-178.
22. Kislauskis, E. H., Li, Z., Singer, R. H. and Taneja, K. L. (1993). Isoform specific 3′ untranslated sequences sort α-cardiac and β-cytoplasmic actin messenger RNAs to different compartments. J. Cell Biol. 123, 165-172.
23. Kislauskis, E. H., Zhu, X. and Singer, R. H. (1997). β-Actin messenger RNA localization and protein synthesis augment cell motility. J. Cell Biol. 136, 1263-1270.
24. Kleiman, R., Banker, G. and Steward, O. (1993). Inhibition of protein synthesis alters the subcellular distribution of mRNA in neurons but does not prevent dendritic transport of RNA. Proc. Nat. Acad. Sci. USA 90, 11192-11196.
25. Larramendi, P. C. H. (1988). Method for obtaining a cross section layer of tissue culture for EM without pelleting or re-embedding. J. Elect. Microsc. Tech. 10, 119-121.
26. Lawrence, J. B. and Singer, R. H. (1986). Intracellular localization of messenger RNA's for cytoskeletal proteins. Cell 45, 407-415.
27. Lim, K. and Chae, C. B. (1989). A simply assay for DNA transfection by incubation of the cells in culture dishes with substrates for beta galactosidase. Biotechniques 7, 576-579.
28. Litman, P., Barg, J., Rindzoonski, L. and Ginzburg, I. (1993). Subcellular localization of Tau mRNA in differentiating neuronal cell culture: Implications for neuronal polarity. Neuron 10, 627-638.
29. Luby-Phelps, K. (1987). Hindered diffusion of inert tracer particles in the cytoplasm of mouse 3T3 cells. Proc. Nat. Acad Sci. USA 84, 4910-4913.
30. MacDonald, P. M., Kerr, K., Smith, J. L. and Leask, A. (1993). RNA regulatory element BLE1 directs the early of bicoid mRNA localization. Development 118, 1233-1243.
31. McDermott, P. J. and Morgan, H. E. (1989). Contraction modulates the capacity for protein synthesis during growth of neonatal heart cells in culture. Circ. Res. 64, 542-553.
32. Melton, D. A. (1987). Translocation of a localized maternal mRNA to the vegetal pole of Xenopus oocytes. Nature 328, 80-82.
33. Morris, E. J. and Fulton, A. B. (1994). Rearrangement of mRNAs for costamere proteins during costamere development in cultured skeletal muscle from chicken. J. Cell Sci. 107, 377-386.
34. Nairn, A. C. and Palfrey, H. C. (1996). Regulation of protein synthesis by calcium. In Translational Control (ed. J. Hershey et al.), pp. 295-318. Cold Spring Harbor Laboratory Press, New York.
35. 2+ transients. J. Biol. Chem. 262, 9785-9792.
36. Qi, M., Ojamaa, K., Eleftheriades, E. G., Klein, I. and Samarel, A. M. (1994). Regulation of rat ventricular myosin heavy chain expression by serum and contractile activity. Am. J. Physiol. 267, C520-C528.
37. Russell, B. and Dix, D. J. (1992). Mechanisms for intracellular distribution of mRNA: In situ hybridization studies in muscle. Am. J. Physiol. 262, C1-C8.
38. Russell, B., Wenderoth, M. P. and Goldspink, P. H. (1992). Remodelling of myofibrils: subcellular distribution of myosin heavy chain mRNA and protein. Am. J. Physiol. 262, R339-R345.
39. Samarel, A. M. and Engelmann, G. L. (1991). Contractile activity modulates myosin heavy chain-B expression in neonatal rat heart cells. Am. J. Physiol. 261, H1067-H1077.
40. Sharp, W., W., Terracio, L., Borg, T. K. and Samarel, A. M. (1993). Contractile activity modulates actin synthesis and turnover in cultured neonatal rat heart cells. Circ. Res. 73, 172-183.
41. Sundell, C. L. and Singer, R. H. (1990). Actin mRNA localizes in the absence of protein synthesis. J. Cell Biol. 111, 2397-2403.
42. Sussman, M. A., Sakhi, S., Barrientos, P., Ito, M. and Kedes, L. (1994). Tropomodulin in rat cardiac muscle: Localization of protein is independent of messenger RNA distribution during myofibrillar development. Circ. Res. 75, 221-232.
43. Wilhelm, J. and Vale, R. D. (1993). RNA on the move: the mRNA localization pathway. J. Cell Biol. 123, 269-274.
44. Wilson, I. A., Brindle, K. M. and Fulton, A. B. (1995). Differential localization of the mRNA of the M and B isoforms of creatine kinase in myoblasts. Biochem. J. 308, 599-605.
45. 2+ and ionophore A23187 on protein synthesis in intact rabbit reticulocytes. Int. J. Biochem. 23, 605-608.