Myosin II isoforms in smooth muscle: Heterogeneity and function

American Journal of Physiology - Cell Physiology

Volumn 293, Issue 2, 2007, Pages

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

^a MARQUETTE UNIVERSITY   (United States)

^b CARDINAL STRITCH UNIVERSITY   (United States)

Author keywords

Expression; Nonmuscle myosin

Indexed keywords

ACTIN; ISOPROTEIN; MYOSIN; MYOSIN 2; MYOSIN LIGHT CHAIN; UNCLASSIFIED DRUG;

NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN POLYMORPHISM; REVIEW; SMOOTH MUSCLE; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE FIBER;

ACTINS; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; HUMANS; HYDROLYSIS; MOLECULAR SEQUENCE DATA; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE, SMOOTH; MYOCYTES, SMOOTH MUSCLE; MYOSIN HEAVY CHAINS; MYOSIN LIGHT CHAINS; MYOSIN TYPE II; NONMUSCLE MYOSIN TYPE IIA; NONMUSCLE MYOSIN TYPE IIB; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; SMOOTH MUSCLE MYOSINS;

EID: 34547774119     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00131.2007     Document Type: Review

References (167)

1. Adelstein RS, Conti MA. Phosphorylation of platelet myosin increases actin-activated myosin ATPase activity. Nature 256: 597-598, 1975.
2. Adelstein RS, Eisenberg E. Regulation and kinetics of the actin-myosin-ATP interaction. Annu Rev Biochem 49: 921-956, 1980.
3. 2+ sensitivity and phosphorylation of gizzard actomyosin. Biochem Biophys Res Commun 69: 35-41, 1976.
4. Ali F, Pare PD, Seow CY. Models of contractile units and their assembly in smooth muscle. Can J Physiol Pharmacol 83: 825-831, 2005.
5. Atkinson SJ, Stewart M. Molecular interactions in myosin assembly. Role of the 28-residue charge repeat in the rod. J Mol Biol 226: 7-13, 1992.
6. Babij P, Kawamoto S, White S, Adelstein RS, Periasamy M. Differential expression of SM1 and SM2 myosin isoforms in cultured vascular smooth muscle. Am J Physiol Cell Physiol 262: C607-C613, 1992.
7. 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.
8. Babu GJ, Loukianov E, Loukianova T, Pyne GJ, Huke S, Osol G, Low RB, Paul RJ, Periasamy M. Loss of SM-B myosin affects muscle shortening velocity and maximal force development. Nat Cell Biol 3: 1025-1029, 2001.
9. Babu GJ, Pyne GJ, Zhou Y, Okwuchukuasanya C, Brayden JE, Osol G, Paul RJ, Low RB, Periasamy M. Isoform switching from SM-B to SM-A myosin results in decreased contractility and altered expression of thin filament regulatory proteins. Am J Physiol Cell Physiol 287: C723-C729, 2004.
10. Bai TR, Bates JH, Brusasco V, Camoretti-Mercado B, Chitano P, Deng LH, Dowell M, Fabry B, Ford LE, Fredberg JJ, Gerthoffer WT, Gilbert SH, Gunst SJ, Hai CM, Halayko AJ, Hirst SJ, James AL, Janssen LJ, Jones KA, King GG, Lakser OJ, Lambert RK, Lauzon AM, Lutchen KR, Maksym GN, Meiss RA, Mijailovich SM, Mitchell HW, Mitchell RW, Mitzner W, Murphy TM, Pare PD, Schellenberg RR, Seow CY, Sieck GC, Smith PG, Smolensky AV, Solway J, Stephens NL, Stewart AG, Tang DD, Wang L. On the terminology for describing the length-force relationship and its changes in airway smooth muscle. J Appl Physiol 97: 2029-2034, 2004.
11. Barron JT, Barany M, Barany K. Phosphorylation of the 20,000-dalton light chain of myosin of intact arterial smooth muscle in rest and in contraction. J Biol Chem 254: 4954-4956, 1979.
12. Borrione AC, Zanellato AM, 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.
13. Bremel RD. Myosin linked calcium regulation in vertebrate smooth muscle. Nature 252: 405-407, 1974.
14. Bremel RD, Sobieszek A, Small JA. Regulation of Actin-Myosin Interaction in Vertebrate Smooth Muscle. Baltimore, MD: University Park, 1977, p. 533-549.
15. Burridge K, Bray D. Purification and structural analysis of myosins from brain and other non-muscle tissues. J Mol Biol 99: 1-14, 1975.
16. Burridge K, Phillips JH. Association of actin and myosin with secretory granule membranes. Nature 254: 526-529, 1975.
17. Cai S, Ferguson DG, Martin AF, Paul RJ. Smooth muscle contractility is modulated by myosin tail-S2-LMM hinge region interaction. Am J Physiol Cell Physiol 269: C1126-C1132, 1995.
18. Capriani A, Chiavegato A, Franch R, Azzarello G, Vinante O, Sartore S. Oestrogen-dependent expression of the SM2 smooth muscletype myosin isoform in rabbit myometrium. J Muscle Res Cell Motil 18: 413-427, 1997.
19. Cavaille F, Janmot C, Ropert S, d'Albis A. Isoforms of myosin and actin in human, monkey and rat myometrium. Comparison of pregnant and non-pregnant uterus proteins. Eur J Biochem 160: 507-513, 1986.
20. 2+ regulation. Proc Natl Acad Sci USA 74: 129-133, 1977.
21. Chan WL, Silberstein J, Hai CM. Mechanical strain memory in airway smooth muscle. Am J Physiol Cell Physiol 278: C895-C904, 2000.
22. Chiavegato A, Pauletto P, Sartore S. Smooth muscle-type myosin heavy chain isoforms in bovine smooth muscle and non-muscle tissues. Biol Cell 86: 27-38, 1996.
23. Cohen C, Parry DA. A conserved C-terminal assembly region in paramyosin and myosin rods. J Struct Biol 122: 180-187, 1998.
24. Cooke PH, Fay FS, Craig R. Myosin filaments isolated from skinned amphibian smooth muscle cells are side-polar. J Muscle Res Cell Motil 10: 206-220, 1989.
25. Craig R, Megerman J. Assembly of smooth muscle myosin into side-polar filaments. J Cell Biol 75: 990-996, 1977.
26. Craig R, Woodhead JL. Structure and function of myosin filaments. Curr Opin Struct Biol 16: 204-212, 2006.
27. Cross RA, Geeves MA, Kendrick-Jones J. A nucleation-elongation mechanism for the self-assembly of side polar sheets of smooth muscle myosin. EMBO J 10: 747-756, 1991.
28. DiSanto ME, Cox RH, Wang Z, Chacko S. NH2-terminal-inserted myosin II heavy chain is expressed in smooth muscle of small muscular arteries. Am J Physiol Cell Physiol 272: C1532-C1542, 1997.
29. DiSanto ME, Stein R, Chang S, Hypolite JA, Zheng Y, Zderic S, Wein AJ, Chacko S. Alteration in expression of myosin isoforms in detrusor smooth muscle following bladder outlet obstruction. Am J Physiol Cell Physiol 285: C1397-C1410, 2003.
30. Dominguez R, Freyzon Y, Trybus KM, Cohen C. Crystal structure of a vertebrate smooth muscle myosin motor domain and its complex with the essential light chain: visualization of the pre-power stroke state. Cell 94: 559-571, 1998.
31. Driska SP, Aksoy MO, Murphy RA. Myosin light chain phosphorylation associated with contraction in arterial smooth muscle. Am J Physiol Cell Physiol 240: C222-C233, 1981.
32. Eddinger TJ. Myosin heavy chain isoforms and dynamic contractile properties: skeletal versus smooth muscle. Comp Biochem Physiol B Biochem Mol Biol 119: 425-434, 1998.
33. Eddinger TJ, Korwek AA, Meer DP, Sherwood JJ. Expression of smooth muscle myosin light chain 17 and unloaded shortening in single smooth muscle cells. Am J Physiol Cell Physiol 278: C1133-C1142, 2000.
34. Eddinger TJ, Meer DP. Single rabbit stomach smooth muscle cell myosin heavy chain SMB expression and shortening velocity. Am J Physiol Cell Physiol 280: C309-C316, 2001.
35. Eddinger TJ, Meer DP. Smooth muscle heterogeneity: does the striated muscle model apply? Can J Physiol Pharmacol 75: 861-868, 1997.
36. Eddinger TJ, Meer DP, Miner AS, Meehl J, Rovner AS, Ratz PH. Potent inhibition of arterial smooth muscle tonic contractions by the selective myosin ii inhibitor, blebbistatin. J Pharmacol Exp Ther 320: 865-870, 2007.
37. Eddinger TJ, Murphy RA. Developmental changes in actin and myosin heavy chain isoform expression in smooth muscle. Arch Biochem Biophys 284: 232-237, 1991.
38. Eddinger TJ, Murphy RA. Two smooth muscle myosin heavy chains differ in their light meromyosin fragment. Biochemistry 27: 3807-3811, 1988.
39. Eddinger TJ, Schiebout JD, Swartz DR. Adherens junction associated protein distribution differs in smooth muscle tissue and acutely isolated cells. Am J Physiol Gastrointest Liver Physiol 292: G684-G697, 2007.
40. Eddinger TJ, Wolf JA. Expression of four myosin heavy chain isoforms with development in mouse uterus. Cell Motil Cytoskeleton 25: 358-368, 1993.
41. Frid MG, Aldashev AA, Dempsey EC, Stenmark KR. Smooth muscle cells isolated from discrete compartments of the mature vascular media exhibit unique phenotypes and distinct growth capabilities. Circ Res 81: 940-952, 1997.
42. Frid MG, Dempsey EC, Durmowicz AG, Stenmark KR. Smooth muscle cell heterogeneity in pulmonary and systemic vessels. Importance in vascular disease. Arterioscler Thromb Vasc Biol 17: 1203-1209, 1997.
43. Frid MG, Moiseeva EP, Stenmark KR. 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.
44. Gaylinn BD, Eddinger TJ, Martino PA, Monical PL, Hunt DF, Murphy RA. Expression of nonmuscle myosin heavy and light chains in smooth muscle. Am J Physiol Cell Physiol 257: C997-C1004, 1989.
45. Gerthoffer WT, Gunst SJ. Invited review: focal adhesion and small heat shock proteins in the regulation of actin remodeling and contractility in smooth muscle. J Appl Physiol 91: 963-972, 2001.
46. Gillis JM, Cao ML, Godfraind-De Becker A. Density of myosin filaments in the rat anococcygeus muscle, at rest and in contraction. II. J Muscle Res Cell Motil 9: 18-29, 1988.
47. 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.
48. Godfraind-De Becker A, Gillis JM. Analysis of the birefringence of the smooth muscle anococcygeus of the rat, at rest and in contraction. I. J Muscle Res Cell Motil 9: 9-17, 1988.
49. Golenhofen K. Spontaneous activity and functional classification of mammalian smooth muscle. In Physiology of Smooth Muscle, edited by E Bülbring and MF Shuba. New York: Raven, 1976.
50. Golomb E, Ma X, Jana SS, Preston YA, Kawamoto S, Shoham NG, Goldin E, Conti MA, Sellers JR, Adelstein RS. Identification and characterization of nonmuscle myosin II-C, a new member of the myosin II family. J Biol Chem 279: 2800-2808, 2004.
51. Gunst SJ, Meiss RA, Wu MF, Rowe M. Mechanisms for the mechanical plasticity of tracheal smooth muscle. Am J Physiol Cell Physiol 268: C1267-C1276, 1995.
52. Gunst SJ, Wu MF. Selected contribution: plasticity of airway smooth muscle stiffness and extensibility: role of length-adaptive mechanisms. J Appl Physiol 90: 741-749, 2001.
53. Hamada Y, Yanagisawa M, Katsuragawa Y, Coleman JR, 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.
54. Han S, Speich JE, Eddinger TJ, Berg KM, Miner AS, Call C, Ratz PH. Evidence for absence of latch-bridge formation in muscular saphenous arteries. Am J Physiol Heart Circ Physiol 291: H138-H146, 2006.
55. Harris DE, Warshaw Length vs DM. active force relationship in single isolated smooth muscle cells. Am J Physiol Cell Physiol 260: C1104-C1112, 1991.
56. Hasegawa Y, Morita F. Role of 17-kDa essential light chain isoforms of aorta smooth muscle myosin. J Biochem (Tokyo) 111: 804-809, 1992.
57. Hasegawa Y, Ueno H, Horie K, Morita F. Two isoforms of 17-kDa essential light chain of aorta media smooth muscle myosin. J Biochem (Tokyo) 103: 15-18, 1988.
58. Helper DJ, Lash JA, Hathaway DR. Distribution of isoelectric variants of the 17,000-dalton myosin light chain in mammalian smooth muscle. J Biol Chem 263: 15748-15753, 1988.
59. Herrera AM, Kuo KH, Seow CY. Influence of calcium on myosin thick filament formation in intact airway smooth muscle. Am J Physiol Cell Physiol 282: C310-C316, 2002.
60. Hewett TE, Martin AF, Paul RJ. Correlations between myosin heavy chain isoforms and mechanical parameters in rat myometrium. J Physiol 460: 351-364, 1993.
61. Hill MA, Davis MJ, Meininger GA, Potocnik SJ, Murphy TV. Arteriolar myogenic signalling mechanisms: Implications for local vascular function. Clin Hemorheol Microcirc 34: 67-79, 2006.
62. 2+ signaling pathways underlying myogenic reactivity. J Appl Physiol 91: 973-983, 2001.
63. Ho G, Chisholm RL. 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 272: 4522-4527, 1997.
64. Hodge TP, Cross R, Kendrick-Jones J. Role of the COOH-terminal nonhelical tailpiece in the assembly of a vertebrate nonmuscle myosin rod. J Cell Biol 118: 1085-1095, 1992.
65. Holifield B, Helgason T, Jemelka S, Taylor A, Navran S, Allen J, Seidel C. Differentiated vascular myocytes: are they involved in neointimal formation? J Clin Invest 97: 814-825, 1996.
66. Ikebe M, Komatsu S, Woodhead JL, Mabuchi K, Ikebe R, Saito J, Craig R, Higashihara M. The tip of the coiled-coil rod determines the filament formation of smooth muscle and nonmuscle myosin. J Biol Chem 276: 30293-30300, 2001.
67. Itoh K, Adelstein RS. Neuronal cell expression of inserted isoforms of vertebrate nonmuscle myosin heavy chain II-B. J Biol Chem 270: 14533-14540, 1995.
68. Jezior JR, Brady JD, Rosenstein DI, McCammon KA, Miner AS, Ratz PH. Dependency of detrusor contractions on calcium sensitization and calcium entry through LOE-908-sensitive channels. Br J Pharmacol 134: 78-87, 2001.
69. Jontes JD, Milligan RA. Brush border myosin-I structure and ADP-dependent conformational changes revealed by cryoelectron microscopy and image analysis. J Cell Biol 139: 683-693, 1997.
70. 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.
71. Kawamoto S, Adelstein RS. Characterization of myosin heavy chains in cultured aorta smooth muscle cells. A comparative study. J Biol Chem 262: 7282-7288, 1987.
72. Kawamoto S, Adelstein RS. Chicken nonmuscle myosin heavy chains: differential expression of two mRNAs and evidence for two different polypeptides. J Cell Biol 112: 915-924, 1991.
73. Kelley CA, Sellers JR, Gard DL, Bui D, Adelstein RS, Baines IC. Xenopusnonmuscle myosin heavy chain isoforms have different subcellular localizations and enzymatic activities. J Cell Biol 134: 675-687, 1996.
74. Kelley CA, Sellers JR, Goldsmith PK, Adelstein RS. Smooth muscle myosin is composed of homodimeric heavy chains. J Biol Chem 267: 2127-2130, 1992.
75. Kelley CA, Takahashi M, Yu JH, Adelstein RS. 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.
76. Kerrick WG, Hoar PE. Inhibition of smooth muscle tension by cyclic AMP-dependent protein kinase. Nature 292: 253-255, 1981.
77. Kerrick WG, Hoar PE, Cassidy PS. Calcium-activated tension: the role of myosin light chain phosphorylation. Fed Proc 39: 1558-1563, 1980.
78. Krendel M, Mooseker MS. Mysosins: tails (and heads) of functional diversity. Physiology 20: 239-251, 2005.
79. Kumar CC, Mohan SR, Zavodny PJ, Narula SK, Leibowitz PJ. Characterization and differential expression of human vascular smooth muscle myosin light chain 2 isoform in nonmuscle cells. Biochemistry 28: 4027-4035, 1989.
80. Kuo KH, Wang L, Pare PD, Ford LE, Seow CY. Myosin thick filament lability induced by mechanical strain in airway smooth muscle. J Appl Physiol 90: 1811-1816, 2001.
81. Kuro-o M, Nagai R, Tsuchimochi H, Katoh H, Yazaki Y, Ohkubo A, Takaku F. Developmentally regulated expression of vascular smooth muscle myosin heavy chain isoforms. J Biol Chem 264: 18272-18275, 1989.
82. Lash JA, Helper DJ, Klug M, Nicolozakes AW, Hathaway DR. Nucleotide and deduced amino acid sequence of cDNAs encoding two isoforms for the 17,000 dalton myosin light chain in bovine aortic smooth muscle. Nucleic Acids Res 18: 7176, 1990.
83. Lau CL, Chacko S. Identification of two types of smooth muscle cells from rabbit urinary bladder. Tissue Cell 28: 339-355, 1996.
84. Lauzon AM, Fagnant PM, Warshaw DM, Trybus KM. Coiled-coil unwinding at the smooth muscle myosin head-rod junction is required for optimal mechanical performance. Biophys J 80: 1900-1904, 2001.
85. Lauzon AM, Trybus KM, Warshaw DM. Molecular mechanics of two smooth muscle heavy meromyosin constructs that differ by an insert in the motor domain. Acta Physiol Scand 164: 357-361, 1998.
86. Lauzon AM, Tyska MJ, Rovner AS, Freyzon Y, Warshaw DM, Trybus KM. A 7-amino-acid insert in the heavy chain nucleotide binding loop alters the kinetics of smooth muscle myosin in the laser trap. J Muscle Res Cell Motil 19: 825-837, 1998.
87. Lenz S, Lohse P, Seidel U, Arnold HH. The alkali light chains of human smooth and nonmuscle myosins are encoded by a single gene. Tissue-specific expression by alternative splicing pathways. J Biol Chem 264: 9009-9015, 1989.
88. Liu J, Wendt T, Taylor D, Taylor K. Refined model of the 10S conformation of smooth muscle myosin by cryo-electron microscopy 3D image reconstruction. J Mol Biol 329: 963-972, 2003.
89. Lofgren M, Ekblad E, Morano I, Arner A. Nonmuscle myosin motor of smooth muscle. J Gen Physiol 121: 301-310, 2003.
90. Low RB, Mitchell J, Woodcock-Mitchell J, Rovner AS, White SL. Smooth-muscle myosin heavy-chain SM-B isoform expression in developing and adult rat lung. Am J Respir Cell Mol Biol 20: 651-657, 1999.
91. Low RB, White SL. Myosin heavy chain (SMMHC) SM-B isoform is differentially expressed in developing and adult smooth muscle tissues of the rat. Chest 114: 31S-33S, 1998.
92. Low RB, White SL, Low ES, Neuville P, Bochaton-Piallat ML, Gabbiani G. Age dependence of smooth muscle myosin expression by cultured rat aortic smooth muscle cells. Differentiation 65: 151-159, 1999.
93. Lu RC, Wong A. The amino acid sequence and stability predictions of the hinge region in myosin subfragment 2. J Biol Chem 260: 3456-3461, 1985.
94. Malmqvist U, Arner A. Correlation between isoform composition of the 17 kDa myosin light chain and maximal shortening velocity in smooth muscle. Pflügers Arch 418: 523-530, 1991.
95. Marini M, Bruschi M, Pecci A, Romagnoli R, Musante L, Candiano G, Ghiggeri GM, Balduini C, Seri M, Ravazzolo R. Non-muscle myosin heavy chain IIA and IIB interact and co-localize in living cells: relevance for MYH9-related disease. Int J Mol Med 17: 729-736, 2006.
96. McLachlan AD, Karn J. Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle. Nature 299: 226-231, 1982.
97. McLachlan AD, Karn J. Periodic features in the amino acid sequence of nematode myosin rod. J Mol Biol 164: 605-626, 1983.
98. Meer DP, Eddinger TJ. Expression of smooth muscle myosin heavy chains and unloaded shortening in single smooth muscle cells. Am J Physiol Cell Physiol 273: C1259-C1266, 1997.
99. Mehta D, Gunst SJ. Actin polymerization stimulated by contractile activation regulates force development in canine tracheal smooth muscle. J Physiol 519: 829-840, 1999.
100. Mohammad MA, Sparrow MP. The distribution of heavy-chain isoforms of myosin in airways smooth muscle from adult and neonate humans. Biochem J 260: 421-426, 1989.
101. Monical PL, Owens GK, Murphy RA. Expression of myosin regulatory light-chain isoforms and regulation of phosphorylation in smooth muscle. Am J Physiol Cell Physiol 264: C1466-C1472, 1993.
102. Morano I, Chai GX, Baltas LG, Lamounier-Zepter V, Lutsch G, Kott M, Haase H, Bader M. Smooth-muscle contraction without smooth-muscle myosin. Nat Cell Biol 2: 371-375, 2000.
103. 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.
104. Mougios V, Barany M. Isoforms of the phosphorylatable myosin light chain in arterial smooth muscle. Biochim Biophys Acta 872: 305-308, 1986.
105. Murakami N, Elzinga M. Immunohistochemical studies on the distribution of cellular myosin II isoforms in brain and aorta. Cell Motil Cytoskeleton 22: 281-295, 1992.
106. Murakami N, Mehta P, Elzinga M. Studies on the distribution of cellular myosin with antibodies to isoform-specific synthetic peptides. FEBS Lett 288: 247, 1991.
107. Murphy RA, Walker JS, Strauss JD. Myosin isoforms and functional diversity in vertebrate smooth muscle. Comp Biochem Physiol B Biochem Mol Biol 117: 51-60, 1997.
108. Nabeshima Y, Nabeshima Y, Nonomura Y, Fujii-Kuriyama Y. Nonmuscle and smooth muscle myosin light chain mRNAs are generated from a single gene by the tissue-specific alternative RNA splicing. J Biol Chem 262: 10608-10612, 1987.
109. 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.
110. Nagai R, Larson DM, Periasamy M. Characterization of a mammalian smooth muscle myosin heavy chain cDNA clone and its expression in various smooth muscle types. Proc Natl Acad Sci USA 85: 1047-1051, 1988.
111. Nakasawa T, Takahashi M, Matsuzawa F, Aikawa S, Togashi Y, Saitoh T, Yamagishi A, Yazawa M. Critical regions for assembly of vertebrate nonmuscle myosin II. Biochemistry 44: 174-183, 2005.
112. Nelson WD, Blakely SE, Nesmelov YE, Thomas DD. Site-directed spin labeling reveals a conformational switch in the phosphorylation domain of smooth muscle myosin. Proc Natl Acad Sci USA 102: 4000-4005, 2005.
113. Nyitray L, Mocz G, Szilagyi L, Balint M, Lu RC, Wong A, Gergely J. The proteolytic substructure of light meromyosin. Localization of a region responsible for the low ionic strength insolubility of myosin. J Biol Chem 258: 13213-13220, 1983.
114. Offer G, Sessions R. Computer modelling of the alpha-helical coiled coil: packing of side-chains in the inner core. J Mol Biol 249: 967-987, 1995.
115. Parisi JA, Eddinger TJ. Smooth muscle myosin heavy chain isoform distribution in the swine stomach. J Histochem Cytochem 50: 385-393, 2002.
116. Patzak A, Petzhold D, Wronski T, Martinka P, Babu GJ, Periasamy M, Haase H, Morano I. Constriction velocities of renal afferent and efferent arterioles of mice are not related to SMB expression. Kidney Int 68: 2726-2734, 2005.
117. Phillips CL, Yamakawa K, Adelstein RS. Cloning of the cDNA encoding human nonmuscle myosin heavy chain-B and analysis of human tissues with isoform-specific antibodies. J Muscle Res Cell Motil 16: 379-389, 1995.
118. Pratusevich VR, Seow CY, Ford LE. Plasticity in canine airway smooth muscle. J Gen Physiol 105: 73-94, 1995.
119. Qi D, Mitchell RW, Burdyga T, Ford LE, Kuo KH, Seow CY. Myosin light chain phosphorylation facilitates in vivo myosin filament reassembly after mechanical perturbation. Am J Physiol Cell Physiol 282: C1298-C1305, 2002.
120. Rayment I, Holden HM, Sellers JR, Fananapazir L, Epstein ND. Structural interpretation of the mutations in the beta-cardiac myosin that have been implicated in familial hypertrophic cardiomyopathy. Proc Natl Acad Sci USA 92: 3864-3868, 1995.
121. Rovner AS, Fagnant PM, Lowey S, Trybus KM. The carboxyl-terminal isoforms of smooth muscle myosin heavy chain determine thick filament assembly properties. J Cell Biol 156: 113-123, 2002.
122. Rovner AS, Fagnant PM, Trybus KM. Phosphorylation of a single head of smooth muscle myosin activates the whole molecule. Biochemistry 45: 5280-5289, 2006.
123. Rovner AS, Freyzon Y, Trybus KM. An insert in the motor domain determines the functional properties of expressed smooth muscle myosin isoforms. J Muscle Res Cell Motil 18: 103-110, 1997.
124. Rovner AS, Murphy RA, Owens GK. Expression of smooth muscle and nonmuscle myosin heavy chains in cultured vascular smooth muscle cells. J Biol Chem 261: 14740-14745, 1986.
125. Rovner AS, Thompson MM, Murphy RA. Two different heavy chains are found in smooth muscle myosin. Am J Physiol Cell Physiol 250: C861-C870, 1986.
126. Saez CG, Myers JC, Shows TB, Leinwand LA. Human nonmuscle myosin heavy chain mRNA: generation of diversity through alternative polyadenylylation. Proc Natl Acad Sci USA 87: 1164-1168, 1990.
127. Sanders KM, Koh SD, Ward SM. Interstitial cells of cajal as pacemakers in the gastrointestinal tract. Annu Rev Physiol 68: 307-343, 2006.
128. Sartore S, De Marzo N, Borrione AC, Zanellato AM, Saggin L, Fabbri L, Schiaffino S. Myosin heavy-chain isoforms in human smooth muscle. Eur J Biochem 179: 79-85, 1989.
129. Schultz SG, Wood JD, Raurer BB. A Critical, Comprehensive Presentation of Physiological Knowledge and Concepts. Rockville, MD.: Am. Physiol. Soc., 1989.
130. Sellers J. Myosins. New York: Oxford Univ. Press, 1999.
131. Seow CY. Myosin filament assembly in an ever-changing myofilament lattice of smooth muscle. Am J Physiol Cell Physiol 289: C1363-C1368, 2005.
132. Seow CY, Pratusevich VR, Ford LE. Series-to-parallel transition in the filament lattice of airway smooth muscle. J Appl Physiol 89: 869-876, 2000.
133. Shenfeld OZ, Morgan CW, Ratz PH. Bethanechol activates a postreceptor negative feedback mechanism in rabbit urinary bladder smooth muscle. J Urol 159: 252-257, 1998.
134. Sherwood JJ, Eddinger TJ. Shortening velocity and myosin heavy- and light-chain isoform mRNA in rabbit arterial smooth muscle cells. Am J Physiol Cell Physiol 282: C1093-C1102, 2002.
135. Sherwood JJ, Waller GS, Warshaw DM, Lowey S. A point mutation in the regulatory light chain reduces the step size of skeletal muscle myosin. Proc Natl Acad Sci USA 101: 10973-10978, 2004.
136. Shohet RV, Conti MA, Kawamoto S, Preston YA, Brill DA, Adelstein RS. Cloning of the cDNA encoding the myosin heavy chain of a vertebrate cellular myosin. Proc Natl Acad Sci USA 86: 7726-7730, 1989.
137. Simons M, Wang M, McBride OW, Kawamoto S, Yamakawa K, Gdula D, Adelstein RS, Weir L. Human nonmuscle myosin heavy chains are encoded by two genes located on different chromosomes. Circ Res 69: 530-539, 1991.
138. Sinard JH, Rimm DL, Pollard TD. Identification of functional regions on the tail of Acanthamoeba myosin-II using recombinant fusion proteins. II. Assembly properties of tails with NH2- and COOH-terminal deletions. J Cell Biol 111: 2417-2426, 1990.
139. Small JV, Squire JM. Structural basis of contraction in vertebrate smooth muscle. J Mol Biol 67: 117-149, 1972.
140. Smolensky AV, Ragozzino J, Gilbert SH, Seow CY, Ford LE. Length-dependent filament formation assessed from birefringence increases during activation of porcine tracheal muscle. J Physiol 563: 517-527, 2005.
141. Sobieszek A. Vertebrate Smooth Muscle Myosin. Enzymatic and structural properites. Baltimore, MD: University Park, 1977, p. 413-443.
142. Sobieszek A, Small JV. Myosin-linked calcium regulation in vertebrate smooth muscle. J Mol Biol 102: 75-92, 1976.
143. Sohn RL, Vikstrom KL, Strauss M, Cohen C, Szent-Gyorgyi AG, Leinwand LA. A 29 residue region of the sarcomeric myosin rod is necessary for filament formation. J Mol Biol 266: 317-330, 1997.
144. Somlyo AP, Somlyo AV. Vascular smooth muscle. I. Normal structure, pathology, biochemistry, and biophysics. Pharmacol Rev 20: 197-272, 1968.
145. Sparrow MP, Mohammad MA, Arner A, Hellstrand P, Ruegg JC. Myosin composition and functional properties of smooth muscle from the uterus of pregnant and non-pregnant rats. Pflügers Arch 412: 624-633, 1988.
146. Straussman R, Squire JM, Ben-Ya'acov A, Ravid S. Skip residues and charge interactions in myosin II coiled-coils: implications for molecular packing. J Mol Biol 353: 613-628, 2005.
147. Sweeney HL, Rosenfeld SS, Brown F, Faust L, Smith J, Xing J, Stein LA, Sellers JR. Kinetic tuning of myosin via a flexible loop adjacent to the nucleotide binding pocket. J Biol Chem 273: 6262-6270, 1998.
148. Szymanski PT, Chacko TK, Rovner AS, Goyal RK. Differences in contractile protein content and isoforms in phasic and tonic smooth muscles. Am J Physiol Cell Physiol 275: C684-C692, 1998.
149. Takahashi M, Kawamoto S, Adelstein RS. Evidence for inserted sequences in the head region of nonmuscle myosin specific to the nervous system. Cloning of the cDNA encoding the myosin heavy chain-B isoform of vertebrate nonmuscle myosin. J Biol Chem 267: 17864-17871, 1992.
150. Taubman MB, Grant JW, Nadal-Ginard B. Cloning and characterization 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.
151. Tonino P, Simon M, Craig R. Mass determination of native smooth muscle myosin filaments by scanning transmission electron microscopy. J Mol Biol 318: 999-1007, 2002.
152. Tsao AE, Eddinger TJ. Smooth muscle myosin heavy chains combine to form three native myosin isoforms. Am J Physiol Heart Circ Physiol 264: H1653-H1662, 1993.
153. Tuck SA, Maghni K, Poirier A, Babu GJ, Periasamy M, Bates JH, Leguillette R, Lauzon AM. Time course of airway mechanics of the (+)insert myosin isoform knockout mouse. Am J Respir Cell Mol Biol 30: 326-332, 2004.
154. Ueno H, Harrington WF. Local melting in the subfragment-2 region of myosin in activated muscle and its correlation with contractile force. J Mol Biol 190: 69-82, 1986.
155. Ueno H, Harrington WF. Temperature-dependence of local melting in the myosin subfragment-2 region of the rigor cross-bridge. J Mol Biol 190: 59-68, 1986.
156. VanBuren P, Waller GS, Harris DE, Trybus KM, Warshaw DM, Lowey S. The essential light chain is required for full force production by skeletal muscle myosin. Proc Natl Acad Sci USA 91: 12403-12407, 1994.
157. Warshaw DM. Lever arms and necks: a common mechanistic theme across the myosin superfamily. J Muscle Res Cell Motil 25: 467-474, 2004.
158. Watanabe M, Takemori S, Yagi N. X-ray diffraction study on mammalian visceral smooth muscles in resting and activated states. J Muscle Res Cell Motil 14: 469-475, 1993.
159. Wendt T, Taylor D, Messier T, Trybus KM, Taylor KA. Visualization of head-head interactions in the inhibited state of smooth muscle myosin. J Cell Biol 147: 1385-1390, 1999.
160. Wendt T, Taylor D, Trybus KM, Taylor K. Three-dimensional image reconstruction of dephosphorylated smooth muscle heavy meromyosin reveals asymmetry in the interaction between myosin heads and placement of subfragment 2. Proc Natl Acad Sci USA 98: 4361-4366, 2001.
161. White S, Martin AF, Periasamy M. Identification of a novel smooth muscle myosin heavy chain cDNA: isoform diversity in the S1 head region. Am J Physiol Cell Physiol 264: C1252-C1258, 1993.
162. White SL, Zhou MY, Low RB, Periasamy M. Myosin heavy chain isoform expression in rat smooth muscle development. Am J Physiol Cell Physiol 275: C581-C589, 1998.
163. Wingard CJ, Browne AK, Murphy RA. Dependence of force on length at constant cross-bridge phosphorylation in the swine carotid media. J Physiol 488: 729-739, 1995.
164. Xu JQ, Gillis JM, Craig R. Polymerization of myosin on activation of rat anococcygeus smooth muscle. J Muscle Res Cell Motil 18: 381-393, 1997.
165. Xu JQ, Harder BA, Uman P, Craig R. Myosin filament structure in vertebrate smooth muscle. J Cell Biol 134: 53-66, 1996.
166. Zanellato AM, Borrione AC, Giuriato L, Tonello M, Scannapieco G, Pauletto P, Sartore S. Myosin isoforms and cell heterogeneity in vascular smooth muscle. I. Developing and adult bovine aorta. Dev Biol 141: 431-446, 1990.
167. Zanellato AM, Borrione AC, Tonello M, Scannapieco G, Pauletto P, Sartore S. Myosin isoform expression and smooth muscle cell heterogeneity in normal and atherosclerotic rabbit aorta. Arteriosclerosis 10: 996-1009, 1990.