Cooperation between the two heads of smooth muscle myosin is essential for full activation of the motor function by phosphorylation

Biochemistry

Volumn 52, Issue 36, 2013, Pages 6240-6248

  Ma, Rong Na ^a,b   Mabuchi, Katsuhide ^c   Li, Jing ^b   Lu, Zekuan ^b   Wang, Chih Lueh Albert ^d   Li, Xiang Dong ^b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b INSTITUTE OF ZOOLOGY   (China)

^c BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

^d BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATP-ASE ACTIVITY; CURRENT MODELING; HEAVY CHAIN; MAXIMAL VALUES; MOTOR ACTIVITY; MOTOR FUNCTION; REGULATORY LIGHT CHAINS; SMOOTH MUSCLES;

CHAINS; MUSCLE; PROTEINS;

PHOSPHORYLATION;

ADENOSINE TRIPHOSPHATASE; MYOSIN; MYOSIN LIGHT CHAIN KINASE;

ANIMAL TISSUE; ARTICLE; GEL PERMEATION CHROMATOGRAPHY; MOTOR ACTIVITY; MOTOR PERFORMANCE; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REGULATORY MECHANISM;

ANIMALS; CHICKENS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME ACTIVATION; MICROSCOPY, ELECTRON; MUSCLE, SMOOTH; MYOSIN HEAVY CHAINS; MYOSIN LIGHT CHAINS; MYOSIN SUBFRAGMENTS; PHOSPHORYLATION;

EID: 84884230050     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400554s     Document Type: Article

References (28)

1. Kamm, K. E. and Stull, J. T. (1989) Regulation of smooth muscle contractile elements by second messengers Annu. Rev. Physiol. 51, 299-313
2. Lowey, S. and Trybus, K. M. (2010) Common structural motifs for the regulation of divergent class II myosins J. Biol. Chem. 285, 16403-16407
3. Margossian, S. S. and Lowey, S. (1973) Substructure of the myosin molecule. IV. Interactions of myosin and its subfragments with adenosine triphosphate and F-actin J. Mol. Biol. 74, 313-330
4. Mockrin, S. C. and Spudich, J. A. (1976) Calcium control of actin-activated myosin adenosine triphosphatase from Dictyostelium discoideum Proc. Natl. Acad. Sci. U. S. A. 73, 2321-2325
5. Ito, K., Liu, X., Katayama, E., and Uyeda, T. Q. (1999) Cooperativity between two heads of dictyostelium myosin II in in vitro motility and ATP hydrolysis Biophys. J. 76, 985-992
6. Manstein, D. J., Ruppel, K. M., and Spudich, J. A. (1989) Expression and characterization of a functional myosin head fragment in Dictyostelium discoideum Science 246, 656-658
7. Sweeney, H. L. (1998) Regulation and tuning of smooth muscle myosin Am. J. Respir. Crit. Care Med. 158, S95-99
8. Ikebe, M. and Hartshorne, D. J. (1985) Proteolysis of smooth muscle myosin by Staphylococcus aureus protease: preparation of heavy meromyosin and subfragment 1 with intact 20 000-dalton light chains Biochemistry 24, 2380-2387
9. Marston, S. B. and Taylor, E. W. (1980) Comparison of the myosin and actomyosin ATPase mechanisms of the four types of vertebrate muscles J. Mol. Biol. 139, 573-600
10. Greene, L. E., Sellers, J. R., Eisenberg, E., and Adelstein, R. S. (1983) Binding of gizzard smooth muscle myosin subfragment 1 to actin in the presence and absence of adenosine 5′-triphosphate Biochemistry 22, 530-535
11. Taylor, E. W. (1977) Transient phase of adenosine triphosphate hydrolysis by myosin, heavy meromyosin, and subfragment 1 Biochemistry 16, 732-739
12. Ikebe, M., Mitra, S., and Hartshorne, D. J. (1993) Cleavage at site A, Glu-642 to Ser-643, of the gizzard myosin heavy chain decreases affinity for actin J. Biol. Chem. 268, 25948-25951
13. Sata, M., Matsuura, M., and Ikebe, M. (1996) Characterization of the motor and enzymatic properties of smooth muscle long S1 and short HMM: role of the two-headed structure on the activity and regulation of the myosin motor Biochemistry 35, 11113-11118
14. Konishi, K., Kojima, S., Katoh, T., Yazawa, M., Kato, K., Fujiwara, K., and Onishi, H. (2001) Two new modes of smooth muscle myosin regulation by the interaction between the two regulatory light chains, and by the S2 domain J. Biochem. 129, 365-372
15. Lu, Z., Shen, M., Cao, Y., Zhang, H. M., Yao, L. L., and Li, X. D. (2012) Calmodulin bound to the first IQ motif is responsible for calcium-dependent regulation of myosin 5a J. Biol. Chem. 287, 16530-16540
16. Li, X. D., Mabuchi, K., Ikebe, R., and Ikebe, M. (2004) Ca2+-induced activation of ATPase activity of myosin Va is accompanied with a large conformational change Biochem. Biophys. Res. Commun. 315, 538-545
17. Li, X. D., Jung, H. S., Wang, Q., Ikebe, R., Craig, R., and Ikebe, M. (2008) The globular tail domain puts on the brake to stop the ATPase cycle of myosin Va Proc. Natl. Acad. Sci. U. S. A. 105, 1140-1145
18. Kodama, T., Fukui, K., and Kometani, K. (1986) The initial phosphate burst in ATP hydrolysis by myosin and subfragment-1 as studied by a modified malachite green method for determination of inorganic phosphate J. Biochem. 99, 1465-1472
19. Persechini, A., Kamm, K. E., and Stull, J. T. (1986) Different phosphorylated forms of myosin in contracting tracheal smooth muscle J. Biol. Chem. 261, 6293-6299
20. Li, X. D., Saito, J., Ikebe, R., Mabuchi, K., and Ikebe, M. (2000) The interaction between the regulatory light chain domains on two heads is critical for regulation of smooth muscle myosin Biochemistry 39, 2254-2260
21. Trybus, K. M. and Lowey, S. (1985) Mechanism of smooth muscle myosin phosphorylation J. Biol. Chem. 260, 15988-15995
22. Trybus, K. M., Freyzon, Y., Faust, L. Z., and Sweeney, H. L. (1997) Spare the rod, spoil the regulation: necessity for a myosin rod Proc. Natl. Acad. Sci. U. S. A. 94, 48-52
23. Kammerer, R. A., Schulthess, T., Landwehr, R., Lustig, A., Engel, J., Aebi, U., and Steinmetz, M. O. (1998) An autonomous folding unit mediates the assembly of two-stranded coiled coils Proc. Natl. Acad. Sci. U. S. A. 95, 13419-13424
24. Decarreau, J. A., James, N. G., Chrin, L. R., and Berger, C. L. (2011) Switch I closure simultaneously promotes strong binding to actin and ADP in smooth muscle myosin J. Biol. Chem. 286, 22300-22307
25. Facemyer, K. C., Sellers, J. R., and Cremo, C. R. (1995) Two heads are required for phosphorylation-dependent regulation of smooth muscle myosin Biophys. J. 68, 228S
26. Sweeney, H. L., Chen, L. Q., and Trybus, K. M. (2000) Regulation of asymmetric smooth muscle myosin II molecules J. Biol. Chem. 275, 41273-41277
27. Cremo, C. R., Wang, F., Facemyer, K., and Sellers, J. R. (2001) Phosphorylation-dependent regulation is absent in a nonmuscle heavy meromyosin construct with one complete head and one head lacking the motor domain J. Biol. Chem. 276, 41465-41472
28. Burgess, S. A., Yu, S., Walker, M. L., Hawkins, R. J., Chalovich, J. M., and Knight, P. J. (2007) Structures of smooth muscle Myosin and heavy meromyosin in the folded, shutdown state J. Mol. Biol. 372, 1165-1178