Photocontrol of mitotic kinesin Eg5 facilitated by thiol-reactive photochromic molecules incorporated into the loop L5 functional loop

Journal of Biochemistry

Volumn 155, Issue 3, 2014, Pages 195-206

  Ishikawa, Kumiko ^a   Tamura, Yuhki ^a   Maruta, Shinsaku ^a  

^a SOKA UNIVERSITY   (Japan)

Author keywords

Eg5; inhibitor; kinesin; loop L5; photochromic molecule

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMINO ACID; CYSTEINE; CYSTEINE DERIVATIVE; KINESIN; KINESIN EG5; MONOMER; THIOL; UNCLASSIFIED DRUG;

ABSORPTION SPECTROSCOPY; ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ISOMERIZATION; MITOSIS; MOTOR PERFORMANCE; POINT MUTATION; RING OPENING; TUBULIN POLYMERIZATION ASSAY; ULTRAVIOLET IRRADIATION; ULTRAVIOLET RADIATION;

EG5; INHIBITOR; KINESIN; LOOP L5; PHOTOCHROMIC MOLECULE;

ABSORPTION; ANIMALS; AZO COMPOUNDS; CYSTEINE; KINESIN; KINETICS; MICE; MICROTUBULES; MITOSIS; MOLECULAR PROBES; MUTANT PROTEINS; PHOTOCHEMICAL PROCESSES; PROTEIN STRUCTURE, SECONDARY; SPECTRUM ANALYSIS; SULFHYDRYL COMPOUNDS; SUS SCROFA;

EID: 84896744841     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvt111     Document Type: Article

References (36)

1. Greene, A.C., Trent, A.M., and Bachand, G.D. (2008) Controlling kinesin motor proteins in nanoengineered systems through a metal-binding on/off switch. Biotechnol. Bioeng. 101, 478-486
2. Hess, H., Matzke, C.M., Doot, R.K., Clemmens, J., Bachand, G.D., Bunker, B.C., and Vogel, V. (2003) Molecular shuttles operating undercover: a new photolithographic approach for the fabrication of structured surfaces supporting directed motility. Nano Lett. 3, 1651-1655 (Pubitemid 38037179)
3. Rau, H. (1990) Photochromism: Molecules and Systems (Durr, H. and Bouas-Laurent, H., eds.) pp. 165-192, Elsevier, Amsterdam
4. Ichimura, K., Seki, T., Kawanishi, Y., Suzuki, Y., Sakuragi, M., and Tamaki, T. (1996) Photocontrol of liquid crystal alignment by "command surface" in Photoreactive Materials for Ultrahigh Density Optical Memory (Irie, M., ed.) pp. 55-88, Amsterdam, Elsevier
5. Irie, M., Fukaminato, T., Sasaki, T., Tamai, N., and Kawai, T. (2002) Organic chemistry: a digital fluorescent molecular photoswitch. Nature 420, 759-760 (Pubitemid 36019615)
6. Yamada, M.D., Nakajima, Y., Maeda, H., and Maruta, S. (2007) Photocontrol of kinesin ATPase activity using an azobenzene derivative. J. Biochem. 142, 691-698 (Pubitemid 351197702)
7. Ionov, L., Stamm, M., and Diez, S. (2006) Reversible switching of microtubule motility using thermoresponsive polymer surfaces. Nano Lett. 6, 1982-1987 (Pubitemid 44555241)
8. Bartels, E., Wassermann, N.H., and Erlanger, B.F. (1971) Photochromic activators of the acetylcholine receptor. Proc. Natl Acad. Sci. USA. 68, 1820-1823
9. Beharry, A.A., Wong, L., Tropepe, V., and Woolley, G.A. (2011) Fluorescence imaging of azobenzene photoswitching in vivo. Angew Chem. Int. Ed. Engl. 50, 1325-1327
10. Banghart, M., Borges, K., Isacoff, E., Trauner, D., and Kramer, R.H. (2004) Light-activated ion channels for remote control of neuronal firing. Nat. Neurosci. 7, 1381-1386 (Pubitemid 41057762)
11. Lien, L., Jaikaran, D.C.J., Zhang, Z., and Woolley, G.A. (1996) Photomodulated blocking of gramicidin ion channels. J. Am. Chem. Soc. 118, 12222-12223 (Pubitemid 27006571)
12. Volgraf, M., Gorostiza, P., Numano, R., Kramer, R.H., Isacoff, E.Y., and Trauner, D. (2006) Allosteric control of an ionotropic glutamate receptor with an optical switch. Nat. Chem. Biol. 2, 47-52
13. Sawin, K.E., LeGuellec, K., Philippe, M., and Mitchison, T.J. (1992) Mitotic spindle organization by a plus-end-directed microtubule motor. Nature 359, 540-543
14. Cole, D.G., Saxton, W.M., Sheehan, K.B., and Scholey, J.M. (1994) A "slow" homotetrameric kinesin-related motor protein purified from Drosophila embryos. J. Biol. Chem. 269, 22913-22916
15. Turner, J., Anderson, R., Guo, J., Beraud, C., Fletterick, R., and Sakowicz, R. (2001) Crystal structure of the mitotic spindle kinesin Eg5 reveals a novel conformation of the neck-linker. J. Biol. Chem. 276, 25496-25502
16. Behnke-Parks, W.M., Vendome, J., Honig, B., Maliga, Z., Moores, C., and Rosenfeld, S.S. (2011) Loop L5 acts as a conformational latch in the mitotic kinesin Eg5. J. Biol. Chem. 286, 5242-5253
17. Goulet, A., Behnke-Parks, W.M., Sindelar, C.V., Major, J., Rosenfeld, S.S., and Moores, C.A. (2012) The structural basis of force generation by the mitotic motor kinesin-5. J. Biol. Chem. 287, 44654-44666
18. Larson, A.G., Naber, N., Cooke, R., Pate, E., and Rice, S.E. (2010) The conserved L5 loop establishes the prepowerstroke conformation of the Kinesin-5 motor, Eg5. Biophys. J. 98, 2619-2627
19. Mayer, T.U., Kapoor, T.M., Haggarty, S.J., King, R.W., Schreiber, S.L., and Mitchison, T.J. (1999) Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 286, 971-974
20. DeBonis, S., Skoufias, D.A., Lebeau, L., Lopez, R., Robin, G., Margolis, R.L., Wade, R.H., and Kozielski, F. (2004) In vitro screening for inhibitors of the human mitotic kinesin Eg5 with antimitotic and antitumor activities. Mol. Cancer Ther. 3, 1079-1090 (Pubitemid 39295005)
21. Tcherniuk, S., van Lis, R., Kozielski, F., and Skoufias, D.A. (2010) Mutations in the human kinesin Eg5 that confer resistance to monastrol and S-trityl-L-cysteine in tumor derived cell lines. Biochem. Pharmacol. 79, 864-872
22. Brier, S., Lemaire, D., DeBonis, S., Forest, E., and Kozielski, F. (2006) Molecular dissection of the inhibitor binding pocket of mitotic kinesin Eg5 reveals mutants that confer resistance to antimitotic agents. J. Mol. Biol. 360, 360-376 (Pubitemid 43927825)
23. Kim, E.D., Buckley, R., Learman, S., Richard, J., Parke, C., Worthylake, D.K., Wojcik, E.J., Walker, R.A., and Kim, S. (2010) Allosteric drug discrimination is coupled to mechanochemical changes in the kinesin-5 motor core. J. Biol. Chem. 285, 18650-18661
24. Kaan, H.Y., Ulaganathan, V., Hackney, D.D., and Kozielski, F. (2009) An allosteric transition trapped in an intermediate state of a new kinesin-inhibitor complex. Biochem. J. 425, 55-60
25. Harrington, T.D., Naber, N., Larson, A.G., Cooke, R., Rice, S.E., and Pate, E. (2011) Analysis of the interaction of the Eg5 Loop5 with the nucleotide site. J. Theor. Biol. 289, 107-115
26. Rosenfeld, S.S., Xing, J., Jefferson, G.M., and King, P.H. (2005) Docking and rolling, a model of how the mitotic motor Eg5 works. J. Biol. Chem. 280, 35684-35695 (Pubitemid 41532761)
27. Hackney, D.D. (1988) Kinesin ATPase: rate-limiting ADP release. Proc. Natl Acad. Sci. USA. 85, 6314-6318
28. Youngburg, G.E. and Youngburg, M.V. (1930) A system of blood phosphorus analysis. J. Lab. Clin. Med. 16, 158-166
29. Dixon, M. and Webb, E.C. (1979) Enzymes. pp. 345-353, Academic Press, New York
30. Ogo, N., Oishi, S., Matsuno, K., Sawada, J., Fujii, N., and Asai, A. (2007) Synthesis and biological evaluation of L-cysteine derivatives as mitotic kinesin Eg5 inhibitors. Bioorg. Med. Chem. Lett. 17, 3921-3924 (Pubitemid 46920939)
31. Wang, F., Good, J.A., Rath, O., Kaan, H.Y., Sutcliffe, O.B., Mackay, S.P., and Kozielski, F. (2012) Triphenylbutanamines: kinesin spindle protein inhibitors with in vivo antitumor activity. J. Med. Chem. 55, 1511-1525
32. Behrendt, R., Renner, C., Schenk, M., Wang, F., Wachtveitl, J., Oesterhelt, D., and Moroder, L. (1999) Photomodulation of the conformation of cyclic peptides with azobenzene moieties in the peptide backbone. Angew. Chem. Int. Ed. Engl. 38, 2771-2774 (Pubitemid 29462851)
33. Abualhasan, M.N., Good, J.A., Wittayanarakul, K., Anthony, N.G., Berretta, G., Rath, O., Kozielski, F., Sutcliffe, O.B., and Mackay, S.P. (2012) Doing the methylene shuffle-further insights into the inhibition of mitotic kinesin Eg5 with S-trityl L-cysteine. Eur. J. Med. Chem. 54, 483-498
34. DeBonis, S., Simorre, J.P., Crevel, I., Lebeau, L., Skoufias, D.A., Blangy, A., Ebel, C., Gans, P., Cross, R., Hackney, D.D., Wade, R.H., and Kozielski, F. (2003) Interaction of the mitotic inhibitor monastrol with human kinesin Eg5. Biochemistry 42, 338-349 (Pubitemid 36105752)
35. Skoufias, D.A., DeBonis, S., Saoudi, Y., Lebeau, L., Crevel, I., Cross, R., Wade, R.H., Hackney, D., and Kozielski, F. (2006) S-trityl-L-cysteine is a reversible, tight binding inhibitor of the human kinesin Eg5 that specifically blocks mitotic progression. J. Biol. Chem. 281, 17559-17569 (Pubitemid 44035555)
36. Indorato, R.L., Debonis, S., Kozielski, F., Garcia-Saez, I., and Skoufias, D.A. (2013) STLC-resistant cell lines as tools to classify chemically divergent Eg5 targeting agents according to their mode of action and target specificity. Biochem. Pharmacol., S0006-2952(13)00574-1