Modulation of myosin filament activation by telokin in smooth muscle: Liberation of myosin kinase and phosphatase from supramolecular complexes

Biophysical Chemistry

Volumn 113, Issue 1, 2005, Pages 25-40

  Sobieszek, Apolinary ^a   Andruchov, Oleg Y ^b   Grabarek, Zenon ^c   Kulikova, Natalia ^a   Liebetrau, Claudia ^d   Matusovsky, Oleg S ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b UNIVERSITY OF SALZBURG   (Austria)

^c BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Endogenous kinase and phosphatase; Myosin filament; Regulation of phosphorylation; Smooth muscle; Telokin

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALMODULIN; MYOSIN; MYOSIN LIGHT CHAIN KINASE; MYOSIN LIGHT CHAIN PHOSPHATASE; PROTEIN; TELOKIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AVIAN STOMACH; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SEDIMENTATION; SMOOTH MUSCLE; SUPRAMOLECULAR CHEMISTRY; TURKEY (BIRD);

ACTOMYOSIN; ANIMALS; CATALYTIC DOMAIN; MACROMOLECULAR SUBSTANCES; MICROFILAMENTS; MUSCLE, SMOOTH; MYOSIN-LIGHT-CHAIN KINASE; MYOSIN-LIGHT-CHAIN PHOSPHATASE; MYOSINS; PEPTIDES; PHOSPHORYLATION; PROTEIN BINDING; SUBSTRATE SPECIFICITY; TURKEY;

CAVIA PORCELLUS; MAMMALIA; SUS SCROFA;

EID: 11144256526     PISSN: 03014622     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bpc.2004.07.038     Document Type: Article

References (46)

1. J.D. Johnson, and C.H. Snyder Calcium regulation of smooth muscle contractile proteins Adv. Second Messenger Phosphoprot. Res. 30 1995 153 174
2. A.P. Somlyo, and A.V. Somlyo Signal transduction and regulation in smooth muscle Nature 372 1994 231 236
3. N.J. Olson, R.B. Pearson, D.S. Needleman, M.Y. Hurwitz, B.E. Kemp, and A.R. Means Regulatory and structural motifs of chicken gizzard myosin light chain kinase Proc. Natl. Acad. Sci. U. S. A. 87 1990 2284 2288
4. P.J. Gallagher, B.P. Herring, and J.T. Stull Myosin light chain kinases J. Muscle Res. Cell Motil. 18 1997 1 16
5. A. Sobieszek D. Raeburn M.A. Gienbycz Smooth Muscle Myosin: Molecule Conformation, Filament Assembly and Associated Regulatory Enzymes Airways Smooth Muscle: Biochemical Control of Contraction and Relaxation vol. 1 1994 Birkhauser Verlag Basel 1 29
6. L.H. Ye, K. Hayakawa, H. Kishi, M. Imamura, A. Nakamura, T. Okagaki, T. Takagi, A. Iwata, T. Tanaka, and K. Kohama The structure and function of the actin-binding domain of myosin light chain kinase of smooth muscle J. Biol. Chem. 272 1997 32182 32189
7. R. Dabrowska, S. Hinkins, M.P. Walsh, and D.J. Hartshorne The binding of smooth muscle myosin light chain kinase to actin Biochem. Biophys. Res. Commun. 107 1982 1524 1531
8. M. Ikebe, M. Stepinska, B.E. Kemp, A.R. Means, and D.J. Hartshorne Proteolysis of smooth muscle myosin light chain kinase. Formation of inactive and calmodulin-independent fragments J. Biol. Chem. 262 1987 13828 13834
9. A. Sobieszek Phosphorylation reaction of vertebrate smooth muscle myosin: an enzyme kinetic analysis Biochemistry 24 1985 1266 1274
10. A. Sobieszek Smooth muscle myosin as a calmodulin binding protein. Affinity increase on filament assembly J. Muscle Res. Cell Motil. 11 1990 114 124
11. A. Sobieszek Regulation of smooth muscle myosin light chain kinase. Allosteric effects and co-operative activation by calmodulin J. Mol. Biol. 220 1991 947 957
12. L. Smith, M. Parizi-Robinson, M.S. Zhu, G. Zhi, R. Fukui, K.E. Kamm, and J.T. Stull Properties of long myosin light chain kinase binding to F-actin in vitro and in vivo J. Biol. Chem. 277 2002 35597 35604
13. D.J. Hartshorne, M. Ito, and F. Erdödi Myosin light chain phosphatase: subunit composition, interactions and regulation J. Muscle Res. Cell Motil. 19 1998 325 341
14. A. Sobieszek, E.B. Babiychuk, B. Ortner, and J. Borkowski Purification and characterization of a kinase-associated, myofibrillar smooth muscle myosin light chain phosphatase possessing a calmodulin-targeting subunit J. Biol. Chem. 272 1997 7027 7033
15. A. Sobieszek, J. Borkowski, and V.S. Babiychuk Purification and characterization of a smooth muscle myosin light chain kinase-phosphatase complex J. Biol. Chem. 272 1997 7034 7041
16. J.L. Hodgkinson Actin and the smooth muscle regulatory proteins: a structural perspective J. Muscle Res. Cell Motil. 21 2000 115 130
17. B.G. Allen, and M.P. Walsh The biochemical basis of the regulation of smooth-muscle contraction Trends Biochem. Sci. 19 1994 362 368
18. M. Ito, R. Dabrowska, V. Guerriero Jr., and D.J. Hartshorne Identification in turkey gizzard of an acidic protein related to the C-terminal portion of smooth muscle myosin light chain kinase J. Biol. Chem. 264 1989 13971 13974
19. T. Okagaki, A. Nakamura, T. Suzuki, K. Ohmi, and K. Kohama Assembly of smooth muscle myosin by the 38 k protein, a homologue of a subunit of pre-mRNA splicing factor-2 J. Cell Biol. 148 2000 653 663
20. K. Nieznanski, and A. Sobieszek Telokin (kinase-related protein) modulates the oligomeric state of smooth-muscle myosin light-chain kinase and its interaction with myosin filaments Biochem. J. 322 1997 65 71
21. P.J. Gallagher, and B.P. Herring The carboxyl terminus of the smooth muscle myosin light chain kinase is expressed as an independent protein, telokin J. Biol. Chem. 266 1991 23945 23952
22. M.O. Shoemaker, W. Lau, R.L. Shattuck, A.P. Kwiatkowski, P.E. Matrisian, L. Guerra-Santos, E. Wilson, T.J. Lukas, L.J. van Eldik, and D.M. Watterson Use of DNA sequence and mutant analyses and antisense oligodeoxynucleotides to examine the molecular basis of nonmuscle myosin light chain kinase autoinhibition, calmodulin recognition, and activity J. Cell Biol. 111 1990 1107 1125
23. M. Collinge, P.E. Matrisian, W.E. Zimmer, R.L. Shattuck, T.J. Lukas, L.J. van Eldik, and D.M. Watterson Structure and expression of a calcium-binding protein gene contained within a calmodulin-regulated protein kinase Mol. Cell. Biol. 12 1992 2359 2371
24. S. Yoshikai, and M. Ikebe Molecular cloning of the chicken gizzard telokin gene and cDNA Arch. Biochem. Biophys. 299 1992 242 247
25. S. Labeit, D.P. Barlow, M. Gautel, T. Gibson, J. Holt, C.-L. Hsieh, U. Francke, K. Leonard, J. Wardale, A. Whiting, and J. Trinick A regular pattern of two types of 100-residue motif in the sequence of titin Nature 345 1990 273 276
26. S. Einheber, and D.A. Fischman Isolation and characterization of a cDNA clone encoding avian skeletal muscle C-protein: an intracellular member of the immunoglobulin superfamily Proc. Natl. Acad. Sci. U. S. A. 87 1990 2157 2161
27. G.M. Benian, J.E. Kiff, N. Neckelmann, D.G. Moerman, and R.H. Waterston Sequence of an unusually large protein implicated in regulation of myosin activity in C. elegans Nature 342 1989 45 50
28. H.M. Holden, M. Ito, D.J. Hartshorne, and I. Rayment X-ray structure determination of telokin, the C-terminal domain of myosin light chain kinase, at 2.8 A resolution J. Mol. Biol. 227 1992 840 851
29. V.P. Shirinsky, A.V. Vorotnikov, K.G. Birukov, A.K. Nanaev, M. Collinge, T.J. Lukas, J.R. Sellers, and D.M. Watterson A kinase-related protein stabilizes unphosphorylated smooth muscle myosin minifilaments in the presence of ATP J. Biol. Chem. 268 1993 16578 16583
30. J. Kendrick-Jones, R.C. Smith, R. Craig, and S. Citi Polymerization of vertebrate non-muscle and smooth muscle myosin J. Mol. Biol. 198 1987 241 252
31. T. Masato, T. Numata, T. Katoh, F. Morita, and M. Yazawa Crosslinking of telokin to chicken gizzard smooth muscle myosin J. Biochem. (Tokyo) 121 1997 225 230
32. X.Q. Wu, T.A.J. Haystead, R.K. Nakamoto, A.V. Somlyo, and A.P. Somlyo Acceleration of myosin light chain dephosphorylation and relaxation of smooth muscle by telokin-synergism with cyclic nucleotide-activated kinase J. Biol. Chem. 273 1998 11362 11369
33. A.M. Filenko, V.M. Danilova, and A. Sobieszek Smooth muscle myosin light chain kinase, supramolecular organization, modulation of activity, and related conformational changes Biophys. J. 73 1997 1593 1606
34. A. Sobieszek, O.Y. Andruchov, and K. Nieznanski Kinase-related protein (telokin) is phosphorylated by smooth-muscle myosin light-chain kinase and modulates the kinase activity Biochem. J. 328 1997 425 430
35. A. Sobieszek, and R.D. Bremel Preparation and properties of vertebrate smooth-muscle myofibrils and actomyosin Eur. J. Biochem. 55 1975 49 60
36. A. Sobieszek, and J.V. Small Regulation of the actin-myosin interaction in vertebrate smooth muscle: activation via a myosin light chain kinase and effect of tropomyosin J. Mol. Biol. 112 1977 559 576
37. A. Sobieszek Bulk isolation of the 20,000-Da light chain of smooth muscle myosin: separation of the unphosphorylated and phosphorylated species Anal. Biochem. 172 1988 43 50
38. A. Sobieszek, and P. Jertschin Urea-glycerol-acrylamide gel electrophoresis of acidic low molecular weight proteins: rapid determination of myosin light chain phosphoryalation in myosin, actomyosin and whole muscle samples Electrophoresis 7 1986 417 425
39. K. Albrecht, A. Schneider, C. Liebetrau, J.C. Rüegg, and G. Pfitzer Exogenous caldesmon promotes relaxation of guinea-pig skinned Taenia coli smooth muscles: inhibition of cooperative reattachment of latch bridges? Pflugers Arch. 434 1997 534 542
40. 2+ sensitivity of smooth muscle and nonmuscle myosin: II. Modulated by G proteins, kinases, and myosin phosphatase Physiol. Rev. 83 2003 1325 1358
41. M. Eto, T. Ohmori, M. Suzuki, K. Furuya, and F. Morita A novel protein phosphatase-1 inhibitory protein potentiated by protein kinase C. Isolation from porcine aorta media and characterization J. Biochem. (Tokyo) 118 1995 1104 1107
42. D.L. Silver, A.V. Vorotnikov, D.M. Watterson, V.P. Shirinsky, and J.R. Sellers Sites of interaction between kinase-related protein and smooth muscle myosin J. Biol. Chem. 272 1997 25353 25359
43. B.P. Herring, and A.F. Smith Telokin expression is mediated by a smooth muscle cell-specific promoter Am. J. Physiol., Cell Physiol. 270 1996 C1656 C1665
44. A. Sobieszek Vectorial phosphorylation of filamentous smooth muscle myosin by calmodulin and myosin light chain kinase complex J. Muscle Res. Cell Motil. 22 2001 505 511
45. D.S. Kudryashov, A.V. Vorotnikov, T.V. Dudnakova, O.V. Stepanova, T.J. Lukas, J.R. Sellers, D.M. Watterson, and V.P. Shirinsky Smooth muscle myosin filament assembly under control of a kinase-related protein (KRP) and caldesmon J. Muscle Res. Cell Motil. 23 2002 341 351
46. J. Kendrick-Jones Role of myosin light chains in calcium regulation Nature 249 1974 631 634