Myosin isoform heterogeneity in single smooth muscle cells

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 117, Issue 1, 1997, Pages 29-38

  Eddinger, Thomas J ^a   Meer, Daniel P ^a  

^a MARQUETTE UNIVERSITY   (United States)

Author keywords

heavy chain isoforms; isozymes; myosin; quantitation; RT PCR; Smooth muscle; vesicular

Indexed keywords

MESSENGER RNA; MYOSIN HEAVY CHAIN;

ANIMAL CELL; CELLULAR DISTRIBUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; RNA SPLICING; SMOOTH MUSCLE FIBER; STRUCTURE ANALYSIS;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

EID: 0030906790     PISSN: 03050491     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0305-0491(96)00312-4     Document Type: Review

References (80)

1. Babij, P. Tissue-specific and developmentally regulated alternative splicing of a visceral isoform of smooth muscle myosin heavy chain. Nucleic Acids Res. 21:1467-1471;1993.
2. Babij, P.; Periasamy, M. Myosin heavy chain isoform diversity in smooth muscle is produced by differential RNA processing. J. Mol. Biol. 210:673-679;1989.
3. Babij, P.; Kelly, C.; Periasamy, M. Characterization of a mammalian smooth muscle myosin heavy-chain gene: Complete nucleotide and protein coding sequence and analysis of the 5′ end of the gene. Proc. Natl. Acad. Sci. USA 88:10676-10680;1991.
4. Babij, P.; Kawamoto, S.; White, S.; Adelstein, R.; Periasamy, M. Differential expression of Sm1 and SM2 myosin isoforms in cultured vascular smooth muscle. Am. J. Physiol. 262: C607-C613;1992.
5. Borrione, A.C.; Zanellato, A.M.C.; Scannapieco, G.; Pauletto, P.; Sartore, S. Myosin heavy-chain isoforms in adult and developing rabbit vascular smooth muscle. Eur. J. Biochem. 183:413-417;1989.
6. Brozovich, F.V.; Walsh, M.P.; Morgan, K.G. Regulation of force in skinned, single cells ot ferret aortic smooth muscle. Pflügers Arch. 416:742-749;1990.
7. Burridge, K.; Bray, D. Purification and structural analysis of myosin from brain and other non-muscle tissues. J. Mol. Biol. 99:1-14;1975.
8. Campbell, G.R.; Campbell, J.H.; Manderson, J.A.; Horgan, S.; Rennick, R.E. Arterial smooth muscle: A multifunctional mesenchymal cell. Arch. Pathol. Lab. Med. 112:977-986; 1988.
9. Cavaille, F.; Janmot, C.; Ropert, S.; d'Albis, A. Isoforms of myosin and actin in human, monkey and rat myometrium. Eur. J. Biochem. 160:507-513;1986.
10. Chamley-Campbell, J.H.; Campbell, G.R. What controls smooth muscle phenotype? Athersclerosis 40:347-357;1981.
11. Chelly, J.; Montarras, D.; Pinset, C.; Berwald-Netter, Y.; Kaplan, J.-C.; Kahn, A. Quantitative estimation of minor mRNAs by cDNA-polymerase chain reaction. Application to dystrophin mRNA in cultured myogenic and brain cells. Eur. J. Biochem. 187:691-698;1990.
12. Cummins, P.; Price, K.M.; Littler, W.A. Foetal myosin light chain in human ventricle. J. Muscle Res. Cell Mot. 1:357-366;1980.
13. DeLozanne, A.; Spudich, J.A. Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 236:1086-1091;1987.
14. DeNofriö, D.; Hoock, R.C.; Herman, I.M. Functional sorting of actin isoforms in microvascular pericytes. J. Cell Biol. 109: 191-202;1989.
15. Driska, S.P.; Porter, R. Isolation of smooth muscle cells from swine carotid artery by digestion with papain. Am. J. Physiol. 251:C474-C481;1986.
16. Eddinger, T.J.; Murphy, R.A. Two smooth muscle myosin heavy chains differ in their light meromyosin fragment. Biochemistry 27:3807-3811;1988.
17. Eddinger, T.J.; R.A. Murphy. Changes in smooth and non-muscle myosin heavy chain content with development in smooth muscle. Biophys. J. 53:579a;1988.
18. Eddinger, T.J.; Murphy, R.A. Developmental changes in actin and myosin heavy chain isoform expression in smooth muscle. Arch. Biochem. Biophys. 284:232-237;1991.
19. Eddinger, T.J.; Wolf, J.A. Expression of four myosin heavy chain isoforms with development in mouse uterus. Cell Motil. Cytoskel. 25:358-368;1993.
20. Eddinger, T.J.; Gaylinn, B.D.; Monical, P.L.; Murphy, R.A. Evidence for non-muscle myosin in smooth muscle cells. Biophys. J. 53:579a;1988.
21. Ferre, F. Quantitative or semi-quantitative PCR: Reality versus myth. PCR Methods Appl. 2:1-9;1992.
22. Ferre, F.; Marchese, A.; Pezzoli, P.; Griffin, S.; Buxton, E.; Boyer, V. Quantitative PCR: An overview. In: Mullis, K.B.; Ferre, F.; Gibbs, R.A., eds. The polymerase chain reaction. Boston, MA: Birkhauser; 1994:67-88.
23. Frid, M.G.; Moiseeva, E.P.; Stenmark, K.R. Multiple phenotypically distinct smooth muscle cell populations exist in the adult and developing bovine pulmonary arterial media in vivo. Circ. Res. 75:669-681;1994.
24. Garland, C.J.; Keatings, W.R. Constrictor actions of acetylcholine, 5-hydroxytryptamine and histamine on bovine coronary artery inner and outer muscle. J. Physiol. 327:363-376; 1982.
25. Garland, C.J.; Keatings, W.R. Action of vasodilator agents on inner and outer muscle of bovine coronary arteries. Eur. J. Pharmacol. 87:327-330;1983.
26. Gaylinn, B.D.; Eddinger, T.J.; Martino, P.A.; Monical, P.L.; Hunt, D.F.; Murphy, R.A. Expression of nonmuscle myosin heavy and light chains in smooth muscle. Am. J. Physiol. 257: C997-C1004;1989.
27. Gilliland, G.; Perrin, S.; Blanchard, K.; Bunn, H.F. Analysis of cytokine mRNA and DNA: detection and quantitation by competitive polymerase chain reaction. Proc. Natl. Acad. Sci. USA 87:2725-2729;1990.
28. Giuriato, L.; Scatena, M.; Chiavegato, A.; Tonello, M.; Scannapieco, G.; Pauletto, P.; Sartore, S. Non-muscle myosin isoforms and cell heterogeneity in developing rabbit vascular smooth muscle. J. Cell Sci. 101:233-246:1992.
29. Grainger, D.J.; Hesketh, T.R., Metcalfe, J.C.; Weissberg, P.L. A large accumulation of non-muscle mysoin occurs at first entry into M phase in rat vascular smooth-muscle cells. Biochem. J. 277:145-151;1991.
30. Hamada, Y.; Yanagisawa, M.; Katsuragawa, Y.; Coleman, J.R.; Nagata, S.; Matsuda, G.; Masaki, T. Distinct vascular and intestinal smooth muscle myosin heavy chain mRNAs are encoded by a single-copy gene in the chicken. Biochem. Biophys. Res. Commun. 170:53-58;1990.
31. Hasegawa, Y.; Morita, F. Role of 17-dKa essential light chain isoforms of aorta smooth muscle myosin. J. Biochem. 111: 804-809;1992.
32. Hasegawa, Y.; Veno, H.; Horie, K.; Morita, F. Two isoforms of 17-kDa essential light chain of aorta media smooth muscle myosin. J. Biochem. 103:15-18;1988.
33. Helper, D.J.; Lash, J.A.; Hathaway, D.R. Distribution of isoelectric variants of the 17,000-dalton myosin light chain in mammalian smooth muscle. J. Biol. Chem. 263:15748-15753; 1988.
34. Hewitt, T.E.; Martin, A.F.; Paul, R.J. Correlations between myosin heavy chain isoforms and mechanical parameters in rat myometrium. J. Physiol. 460:151-364;1993.
35. Hoh, J.F.Y. Neural regulation of mammalian fast and slow muscle myosins: An electrophoretic analysis. Biochemistry 14: 742-747;1975.
36. Hoh, J.F.Y.; Yeoh, G.P.S. Rabbit skeletal myosin isoenzymes from fetal, fast-twitch and slow-twitch muscles. Nature 280: 321-323;1979.
37. Hoh, J.F.Y.; McGrath, P.A.; Hale, P.T. Electrophoretic analysis of multiple forms of rat cardiac myosin: Effects of hypophysectomy and thyroxine replacement. J. Mol. Cell Cardiol. 10: 1053-1076;1978.
38. Katsuragawa, Y.; Yanagisawa, M.; Inoue, A.; Masaki, T. Two distinct nonmuscle myosin-heavy-chain mRNAs are differentially expressed in various chicken tissues: Identification of a novel gene family of vertebrate non-sarcomeric myosin heavy chains. Eur. J. Biochem. 184:611-616;1989.
39. Kawamoto, S.; Adelstein, R.S. Characterization of myosin heavy chains in cultured aorta smooth muscle cells. J. Biol. Chem. 262:7282-7288;1987.
40. Kawamoto, S.; Adelstein, R.S. Chicken nonmuscle myosin heavy chains: Differential expression ot two mRNAs and evidence tor two different polypeptides. J. Cell Biol. 112:915-924;1991.
41. Kelly, C.A.; Adelstein, R.S. Characterization of isotorm diversity in smooth muscle myosin heavy chains. Can. J. Physiol. Pharmacol. 72:1351-1360;1994.
42. Kelley, C.A.; Sellers, J.R.; Goldsmith, P.K.; Adelstein, R.S. Smooth muscle myosin is composed ot homodimeric heavy chains. J. Biol. Chem. 267:2127-2130;1992.
43. Kelley, C.A.; Takahashi. M.; Yu, J.H.; Adelstein, R.S. An insert of seven amino acids confers functional differences between smooth muscle myosins from the intestines and vasculature. J. Biol. Chem. 268:12848-12854;1993.
44. Knecht, D.A.; Loomis, W.F. Antisense RNA inactivation of myosin heavy chain gene expression in Dictyostelium discoideum. Science 236:1081-1086;1987.
45. Kumar, C.C.; Mohan, S.R.; Zhvodny, P.J.; Nrarula, S. K.; Leibowitz, P.J. Characterization and differential expression of human vascular smooth muscle myosin light chain 2 isoform in nonmuscle cells. Biochemistry 28:4027-4035;1989.
46. Kuro-o, M.; Nagai, R.; Tsuchimochi, H.; Katoh, H., Yazaki, Y.; Ohkuho, A.; Takahu, F. Developmentally regulated expression of vascular smooth muscle myosin heavy chain isoforms. J. Biol. Chem. 264:18272-18275;1989.
47. Li, H.; Gyllenstein, U.B.; Cui, X.; Saiki, R.K.; Erlich, H.A.; Arnheim, N. Amplification and analysis of DNA sequences in single human sperm and diploid cells. Nature 315:414-417; 1988.
48. Little, T.L.; Xia, J.; Duling, B.R. Dye tracers define differential endothelial and smooth muscle coupling patterns within the arteriolar wall. Circ. Res. 76:498-504;1995.
49. McConnell, J.D.; Ewalt, D.H.; Boone, T.B. Developmental gulation of myosin heavy chain in the urinary bladder. J. Cell Biol. 107:36A;1988.
50. Meer, D.P.; Eddinger, T.J. Heterogeneity of smooth muscle myosin heavy chain expression at the single cell level. Am. J. Physiol. 270:C1819-1824;1996.
51. Mohammad, M.A.; Sparrow, M.P. Changes in myosin heavy chain stoichiometry in pig tracheal smooth muscle during development. FEBS Lett. 228:109-112;1988.
52. Mohammad, M.A.; Sparrow, M.P. The distribution of heavy-chain isoforms of myosin in airways smooth muscle from adult and neonate humans. Biochem. J. 260:421-426;1989.
53. Morano, I.; Erb, G.; Sogl, B. Expression of myosin heavy and light chains changes during pregnancy in the rat uterus. Pflügers Arch. 423:434-441;1993.
54. Murakami, N.; Mehta, P.; Elzinga, M. Studies on the distribution of cellular myosin with antibodies to isoform-specific synthetic peptides. FEBS Lett. 278:23-25;1991.
55. Murphy, R.A.; Driska, S.P.; Cohen, D.M. Variations in actin to myosin ratios and cellular force generation in vertebrate smooth muscles. In: Casteels, R.; Godfraind, T.; Rüegg, J.C., eds. Excitation-contraction coupling in smooth muscle. Amsterdam: Elsevier/North-Holland Biomedical Press: 1977: 417-424.
56. Nagai, R.; Larson, D.N.M.; Periasamy, M. Characterization of a mammalian smooth muscle myosin heavy chain cDNA clone and its expression in various smooth muscle types. Proc. Narl. Acad. Sci. USA 85:1047-1051;1988.
57. Nagai, R.; Kuro-o, M.; Babij, P.; Periasamy, M. Identification of two types of smooth muscle myosin heavy chain isoforms by cDNA cloning and immunoblot analysis. J. Biol. Chem. 264:9734-9737;1989.
58. Neylon, C.B.; Avdonin, P.V.; Dilley, R.J.; Larsen, M.A.; Tkachuk, V.A.; Bobik, A. Differential electrical responses to vasoactive agonists in morphologically distinct smooth muscle cell types. Circ. Res. 75:733-741;1994.
59. Noonan, K.E.; Beck, C.; Holzmayer, T.A.; Chin, J.E.; Wunder, J.S.; Andrulis, I.L; Gazdar, A.F.; Willman, C.L.; Griffith, B.; Von Hoff, D.D; Roninson, I.B. Quantitative analysis of MDR1 (multidrug resistance) gene expression in human tumors by polymerase chain reaction. Proc. Natl. Acad. Sci. USA 87:7160-7164;1990.
60. Pereschini, A.; Kamm, K.E.; Stull, J.E. Different phosphorylated forms of myosin in contracting tracheal smooth muscle. J. Biol. Chem. 261:6293-6299;1986.
61. Rappolee, D.A.; Wang, A.; Mark, D.; Werb, Z. Novel method tor studying mRNA phenotypes in single or small numbers of cells. J. Cell. Biochem. 39:1-11;1989.
62. Rappolee, D.A.; Mark, D.; Banda, M.J.; Werb, Z. Wound macrophages express TFGα and other growth factors in vivo. Analysis by mRNA phenotyping. Science 241:708-712:1988.
63. Rovner, A.S.; Thompson, M.M.; Murphy, R.A. Two different heavy chains are found in smooth muscle myosin. Am. J. Physiol. 250:C861-C870;1986.
64. Rovner, A.S.; Murphy, R.A.; Owens, G.K. Expression of smooth muscle and nonmuscle myosin heavy chains in cultured vascular smooth muscle cells. J. Biol. Chem. 261: 14740-14745;1986.
65. Saez, C.G.; J.C. Myers; Shows, T.B.; Leinwang, L.A. Human nonmuscle myosin heavy chain mRNA: Generation of diversity through alternative polyadenylation. Proc. Natl. Acad. Sci. USA 87:1164-1168;1990.
66. Sartore, S.; Borrione, A.C.; Zanellato, A.M.C.; Tonello, M.; Scannapieco, G.; Pauletto, P.; Dal Palu, C. Myosin heavy chain isoforms in bovine smooth muscle and in smooth muscle cells grown in vitro. A monoclonal antibody study. J. Muscle Res. Cell Motil. 10:167-168;1989.
67. . Sartore, S.; DeMarzo, N.; Borrione, A.C.; Zanellato, A.M.C.; Saggin, L.; Fabbri; Schianffino, S. Myosin heavy chain isoforms in human smooth muscle. Eur. J. Biochem. 179:79-85; 1989.
68. Seidel, C.L.; Wallace, C.L.; Dennison, D.K..; Allen, J.C. Vascular myosin expression during cytokinesis, attachment, and hypertrophy. Am. J. Physiol. 256:C793-C798;1989.
69. Simmons, M.; Wang, M.; McBride, O.W.; Kawamoto, S.; Yamakawa, K.; Gidula, D.; Adelstein, R.S.; Weir, L. Human nonmuscle myosin heavy chains are encoded by two genes located on different chromosomes. Circ. Res. 69:530-539; 1991.
70. Small, J.V.; Furst, D.O.; De Mey, J. Localization of filamen in smooth muscle. J. Cell Biol. 102:210-220;1986.
71. Sparrow, M.P.; Mitchell, H.W. Contraction of smooth muscle of pig airway tissues from before birth to maturity. J. Appl. Physiol. 68:468-477;1990.
72. Sparrow, M.P., Mohammad, M.A.; Arner, A.; Hellstrand, P.; Rüegg, J.C. Myosin composition and functional properties of smooth muscle from the uterus of pregnant and non-pregnant rats. Pflügers Arch. 412:624-633;1988.
73. Takano-Ohmuro, H., Obinata, T.; Kawashima, M.; Masaki, T.; Tanaka, T. Embryonic chicken skeletal, cardiac, and smooth muscles express a common embryo-specific myosin light chain. J. Cell Biol. 100:2025-2030;1985.
74. Taubman, M.B.; Grant, J.W.; Nadal-Ginard, B. Cloning and aracterization of mammalian myosin regulatory light chain (RLC) cDNA: The RLC gene is expressed in smooth, sarcomeric and nonmuscle tissues. J. Cell Biol. 104:1505-1513; 1987.
75. Tsao, A.E.; Eddinger, T.J. Smooth muscle myosin heavy chains combine to form three native myosin isoforms. Am. J. Physiol. 264: H1653-1662;1993.
76. Wang, A.; Doyle, M.V.; Mark, D.F. Quantitation of mRNA by the polymerase chain reaction. Proc. Natl. Acad. Sci. USA 86:9717-9721;1989.
77. Whalen, R.G.; Butler-Browne, G.S.; Gros, F. Identification of a novel form of myosin light chain present in embryonic muscle tissue and cultured muscle cells. J. Mol. Biol. 126:415-431;1978.
78. White, S.; Martin, A.F.; Periasamy, M. Identification of a novel smooth muscle myosin heavy chain cDNA: Isoform diversity in the S1 head region. Am. J. Physiol. 264:C1252-C1258;1992.
79. Wissler, R.W. The arterial medial cell, smooth muscle or multifunctional mesenchyme. J. Atheroscler. Res. 8:201-213; 1968.
80. Zanellato, A.M.C., Borrione, A.C.; Giuriato, L.; Tonello, M.; Scannapieco, G.; Pauletto, P.; Sartore, S. Myosin isoforms and cell heterogeneity in vascular smooth muscle. II. Developing and adult bovine aorta. Dev. Biol. 141:431-446; 1990.