The mechanism of pentabromopseudilin inhibition of myosin motor activity

Nature Structural and Molecular Biology

Volumn 16, Issue 1, 2009, Pages 80-88

  Fedorov, Roman ^a   Böhl, Markus ^b   Tsiavaliaris, Georgios ^a   Hartmann, Falk K ^a   Taft, Manuel H ^a   Baruch, Petra ^a   Brenner, Bernhard ^a   Martin, René ^b   Knölker, Hans Joachim ^b   Gutzeit, Herwig O ^b   Manstein, Dietmar J ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE; ADENOSINE DIPHOSPHATE MAGNESIUM; ADENOSINE TRIPHOSPHATE; BLEBBISTATIN; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE; PENTABROMOPSEUDILIN; PYRROLE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DICTYOSTELIUM DISCOIDEUM; MOTOR ACTIVITY; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CHICKENS; KINETICS; MODELS, MOLECULAR; MYOSINS; PROTEIN BINDING; PROTEIN CONFORMATION; PYRROLES; RATS; SENSITIVITY AND SPECIFICITY;

DICTYOSTELIUM;

EID: 58149251895     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1542     Document Type: Article

References (50)

1. Sokac, A.M., Schietroma, C., Gundersen, C.B. & Bement, W.M. Myosin-1c couples assembling actin to membranes to drive compensatory endocytosis. Dev. Cell 11, 629-640 (2006).
2. Arden, S.D., Puri, C., Au, J.S., Kendrick-Jones, J. & Buss, F. Myosin VI is required for targeted membrane transport during cytokinesis. Mol. Biol. Cell 18, 4750-4761 (2007).
3. Zhang, H. et al. Myosin-X provides a motor-based link between integrins and the cytoskeleton. Nat. Cell Biol. 6, 523-531 (2004).
4. Cavellan, E., Asp, P., Percipalle, P. & Farrants, A.K. The WSTF-SNF2h chromatin remodeling complex interacts with several nuclear proteins in transcription. J. Biol. Chem. 281, 16264-16271 (2006).
5. van den Boom, F., Dussmann, H., Uhlenbrock, K., Abouhamed, M. & Bahler, M. The Myosin IXb motor activity targets the myosin IXb RhoGAP domain as cargo to sites of actin polymerization. Mol. Biol. Cell 18, 1507-1518 (2007).
6. Weber, K.L., Sokac, A.M., Berg, J.S., Cheney, R.E. & Bement, W.M. A microtubule binding myosin required for nuclear anchoring and spindle assembly. Nature 431, 325-329 (2004).
7. Ohri, R.V. et al. A Re(V)-catalyzed C-N bond-forming route to human lipoxygenase inhibitors. Org. Lett. 7, 2501-2504 (2005).
8. Burkholder, P.R., Pfister, R.M. & Leitz, F.H. Production of a pyrrole antibiotic by a marine bacterium. Appl. Microbiol. 14, 649-653 (1966).
9. Taft, M.H. et al. Dictyostelium myosin-5b is a conditional processive motor. J. Biol. Chem. 283, 26902-26910 (2008).
10. Hiratsuka, T. Fluorescence properties of 2′ (or 3′)-O-(2,4,6-trinitrophenyl) adenosine 5′-triphosphate and its use in the study of binding to heavy meromyosin ATPase. Biochim. Biophys. Acta 453, 293-297 (1976).
11. Webb, M.R. A continuous spectrophotometric assay for inorganic phosphate and for measuring phosphate release kinetics in biological systems. Proc. Natl. Acad. Sci. USA 89, 4884-4887 (1992).
12. Malnasi-Csizmadia, A., Kovacs, M., Woolley, R.J., Botchway, S.W. & Bagshaw, C.R. The dynamics of the relay loop tryptophan residue in the Dictyostelium myosin motor domain and the origin of spectroscopic signals. J. Biol. Chem. 276, 19483-19490 (2001).
13. Geeves, M.A., Fedorov, R. & Manstein, D.J. Molecular mechanism of actomyosin-based motility. Cell. Mol. Life Sci. 62, 1462-1477 (2005).
14. 2+-sensitive cross-bridge dissociation in the presence of magnesium pyrophosphate in skinned rabbit psoas fibers. Biophys. J. 50, 1101-1108 (1986).
15. Dominguez, R., Freyzon, Y., Trybus, K.M. & 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).
16. Sasaki, N., Ohkura, R. & Sutoh, K. Insertion or deletion of a single residue in the strut sequence of Dictyostelium myosin II abolishes strong binding to actin. J. Biol. Chem. 275, 38705-38709 (2000).
17. Boldogh, I.R., Ramcharan, S.L., Yang, H.C. & Pon, L.A. A type V myosin (Myo2p) and a Rab-like G-protein (Ypt11p) are required for retention of newly inherited mitochondria in yeast cells during cell division. Mol. Biol. Cell 15, 3994-4002 (2004).
18. Itoh, T., Watabe, A., Toh, E.A. & Matsui, Y. Complex formation with Ypt11p, a Rab-type small GTPase, is essential to facilitate the function of Myo2p, a class V myosin, in mitochondrial distribution in Saccharomyces cerevisiae. Mol. Cell. Biol. 22, 7744-7757 (2002).
19. Shepard, K.A. et al. Widespread cytoplasmic mRNA transport in yeast: identification of 22 bud-localized transcripts using DNA microarray analysis. Proc. Natl. Acad. Sci. USA 100, 11429-11434 (2003).
20. Simon, V.R., Swayne, T.C. & Pon, L.A. Actin-dependent mitochondrial motility in mitotic yeast and cell-free systems: identification of a motor activity on the mitochondrial surface. J. Cell Biol. 130, 345-354 (1995).
21. Goodson, H.V., Anderson, B.L., Warrick, H.M., Pon, L.A. & Spudich, J.A. Synthetic lethality screen identifies a novel yeast myosin I gene (MYO5): myosin I proteins are required for polarization of the actin cytoskeleton. J. Cell Biol. 133, 1277-1291 (1996).
22. Lord, M., Laves, E. & Pollard, T.D. Cytokinesis depends on the motor domains of myosin-II in fission yeast but not in budding yeast. Mol. Biol. Cell 16, 5346-5355 (2005).
23. Westermann, B. & Neupert, W. Mitochondria-targeted green fluorescent proteins: convenient tools for the study of organelle biogenesis in Saccharomyces cerevisiae. Yeast 16, 1421-1427 (2000).
24. Mnaimneh, S. et al. Exploration of essential gene functions via titratable promoter alleles. Cell 118, 31-44 (2004).
25. Allingham, J.S., Smith, R. & Rayment, I. The structural basis of blebbistatin inhibition and specificity for myosin II. Nat. Struct. Mol. Biol. 12, 378-379 (2005).
26. Cheung, A. et al. A small-molecule inhibitor of skeletal muscle myosin II. Nat. Cell Biol. 4, 83-88 (2002).
27. Nyitrai, M. et al. What limits the velocity of fast-skeletal muscle contraction in mammals? J. Mol. Biol. 355, 432-442 (2006).
28. Reubold, T.F., Eschenburg, S., Becker, A., Kull, F.J. & Manstein, D.J. A structural model for actin-induced nucleotide release in myosin. Nat. Struct. Biol. 10, 826-830 (2003).
29. Coureux, P.D. et al. A structural state of the myosin V motor without bound nucleotide. Nature 425, 419-423 (2003).
30. Reubold, T.F., Eschenburg, S., Becker, A., Kull, F.J. & Manstein, D.J. A structural model for actin-induced nucleotide release in myosin. Nat. Struct. Biol. 10, 826-830 (2003).
31. Coureux, P.D. et al. A structural state of the myosin V motor without bound nucleotide. Nature 425, 419-423 (2003).
32. Dunn, T.A. et al. A novel role of myosin VI in human prostate cancer. Am. J. Pathol. 169, 1843-1854 (2006).
33. Tavares, M., Rezlan, E., Vostroknoutova, I., Khouadja, H. & Mebazaa, A. New pharmacologic therapies for acute heart failure. Crit. Care Med. 36, S112-S120 (2008).
34. Green, J.L. et al. The MTIP-myosin A complex in blood stage malaria parasites. J. Mol. Biol. 355, 933-941 (2006).
35. Manstein, D.J. & Hunt, D.M. Overexpression of myosin motor domains in Dictyostelium: screening of transformants and purification of the affinity tagged protein. J. Muscle Res. Cell Motil. 16, 325-332 (1995).
36. Margossian, S.S. & Lowey, S. Preparation of myosin and its subfragments from rabbit skeletal muscle. Meth. Enzymol. 85, B55-B71 (1982).
37. Lehrer, S.S. & Kerwar, G. Intrinsic fluorescence of actin. Biochemistry 11, 1211-1217 (1972).
38. Criddle, A.H., Geeves, M.A. & Jeffries, T. The use of actin labelled with N-(1-pyrenyl)iodoacetamide to study the interaction of actin with myosin subfragments and troponin/tropomyosin. Biochem. J. 232, 343-349 (1985).
39. Agarwal, S. & Knölker, H.-J. A novel pyrrole synthesis. Org. Biomol. Chem. 2, 3060-3062 (2004).
40. Furch, M., Geeves, M.A. & Manstein, D.J. Modulation of actin affinity and actomyosin adenosine triphosphatase by charge changes in the myosin motor domain. Biochemistry 37, 6317-6326 (1998).
41. Batra, R., Geeves, M.A. & Manstein, D.J. Kinetic analysis of Dictyostelium discoideum myosin motor domains with glycine-to-alanine mutations in the reactive thiol region. Biochemistry 38, 6126-6134 (1999).
42. 2+ ion concentration and heavy chain phosphorylation regulate the motor activity of a class I myosin. J. Biol. Chem. 280, 6064-6071 (2005).
43. Fedorov, R., Witte, G., Urbanke, C., Manstein, D.J. & Curth, U. 3D structure of Thermus aquaticus single-stranded DNA-binding protein gives insight into the functioning of SSB proteins. Nucleic Acids Res. 34, 6708-6717 (2006).
44. Brenner, B. Technique for stabilizing the striation pattern in maximally calcium-activated skinned rabbit psoas fibers. Biophys. J. 41, 99-102 (1983).
45. Kraft, T. et al. Equilibration and exchange of fluorescently labeled molecules in skinned skeletal muscle fibers visualized by confocal microscopy. Biophys. J. 69, 1246-1258 (1995).
46. Brenner, B. & Eisenberg, E. Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution. Proc. Natl. Acad. Sci. USA 83, 3542-3546 (1986).
47. 2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contraction. Proc. Natl. Acad. Sci. USA 85, 3265-3269 (1988).
48. Edman, K.A. The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres. J. Physiol. (Lond.) 291, 143-159 (1979).
49. Brunger, A.T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921 (1998).
50. Schmidt, M.W. et al. The general atomic and molecular electronic structure system. J. Comput. Chem. 14, 1347-1363 (1993).