Кинезин: механика молекулярного мотора

Автор: Шестаков Д.А.

Журнал: Российский журнал биомеханики @journal-biomech

Статья в выпуске: 4 (66) т.18, 2014 года.

Бесплатный доступ

Молекулярные наномоторы обеспечивают самые разные механизмы биологической подвижности. Одним из наиболее распространенных и перспективных для изучения является кинезин - белок, служащий, в частности, для внутриклеточной транспортировки «грузов» вдоль особых молекулярных нитей - микротрубочек, образованных белком тубулином. Взаимодействуя с тубулином, он принимает участие в делении клетки, разборке микротрубочек, движении жгутиков и ресничек. Кинезин по структуре моторного домена и биохимическому циклу во многом схож с другим моторным белком - миозином, играющим важнейшую роль в мышечном сокращении. Энергию для работы обоих моторов доставляет реакция гидролиза АТФ. С другой стороны, кинезин имеет также существенные отличия от миозина в общем строении и фазах биомеханического взаимодействия. В наши дни установлено, как именно кинезин связывается с тубулином, как обеспечивается его последовательное и длительное (процессивное) движение по микротрубочкам, какую силу и скорость он развивает на расстояниях, измеряемых тысячами его одиночных шагов. В то же время многие вопросы, относящиеся к механике кинезинового мотора, еще находятся в процессе обсуждения - детали передачи информации от одной глобулярной головы к другой, существование промежуточных состояний биомеханического цикла, природа обратных шагов кинезина. Для выяснения этих и других деталей и дальнейшего анализа проводят биомеханические исследования, строят математические модели, в которых применяют методы механики сплошной среды, теоретической механики, математической статистики. Настоящий обзор имеет целью собрать в одной статье актуальные сведения о кинезине и его взаимодействии с тубулином и представить их в контексте современной биомеханики.

Еще

Кинезин, тубулин, молекулярный мотор, наномеханика

Короткий адрес: https://sciup.org/146216151

IDR: 146216151

Список литературы Кинезин: механика молекулярного мотора

Ландау Л.Д., Лифшиц Е.М. Теория упругости. Теоретическая физика: в 10 т. Т. VII. -Изд. 5. -М.: Физматлит, 2003. -264 с.
Слёзкин Н.А. Динамика вязкой несжимаемой жидкости. -М.: Гос. изд-во техн.-теорет. лит-ры, 1955. -521 с.
Allen C., Borisy G.G. Structural polarity and directional growth of microtubules of Chlamydomonas flagella//J. Mol. Biol. -1974. -Vol. 90. -P. 381-402.
Amos L., Klug A. Arrangement of subunits in flagellar microtubules//J. Cell Sci. -1974. -Vol. 14. -P. 523-549.
Asbury C.L., Fehr A.N., Block S.M. Kinesin moves by an asymmetric hand-over-hand mechanism//Science. -2003. -Vol. 302. -P. 2130-2134.
Asenjo A.B., Weinberg Y., Sosa H. Nucleotide binding and hydrolysis induces a disorder-order transition in the kinesin neck-linker region//Nat. Struct. Mol. Biol. -2006. -Vol. 13. -P. 648-54.
Bagshaw C.R., Trentham D.R. The characterization of myosin-product complexes and of product-release steps during the magnesium ion-dependent adenosine triphosphatase reaction//Biochem. J. -1974. -Vol. 141. -P. 331-349.
Bernstein M. Flagellar kinesins: new moves with an old beat//Cell Motil. Cytoskeleton. -1995. -Vol. 32. -P. 125-128.
Block S.M. Nanometres and piconewtons: the macromolecular mechanics of kinesin//Trends Cell Biol. -1995. -Vol. 5. -P. 169-175.
Block S.M. Kinesin motor mechanics: binding, stepping, tracking, gating, and limping//Biophys. J. -2007. -Vol. 92. -P. 2986-2995.
Borisy G.G., Taylor E.W. The mechanism of action of colchicine. Binding of colchincine-3H to cellular protein//J. Cell Biol. -1967. -Vol. 34. -P. 525-533, 535-548.
Brady S.T. A novel brain ATPase with properties expected for the fast axonal transport motor//Nature. -1985. -Vol. 317. -P. 73-75.
Brown S.S. Cooperation between microtubule-and actin-based motor proteins//Annu. Rev. Cell Dev. Biol. -1999. -Vol. 15. -P. 63-80.
Caplow M. Microtubule dynamics//Curr. Opin. Cell Biol. -1992. -Vol. 4. -P. 58-65.
Carter N.J., Cross R.A. Mechanics of the kinesin step//Nature. -2005. -Vol. 435. -P. 308-312.
Carter N.J., Cross R.A. Kinesin’s moonwalk//Curr. Opin. Cell Biol. -2006. -Vol. 18. -P. 61-67.
Carter N.J., Cross R.A. Kinesin backsteps//Biochem. Soc. Trans. -2012. -Vol. 40. -P. 400-403.
Cheney R.E., O'Shea M.K., Heuser J.E., Coelho M.V., Wolenski J.S., Espreafico E.M., Forscher P., Larson R.E., Mooseker M.S. Brain myosin-V is a two-headed unconventional myosin with motor activity//Cell. -1993. -Vol. 75. -P. 13-23.
Chretien D., Wade R.H. New data on the microtubule surface lattice//Biol. Cell. -1991. -Vol. 71. -P. 161-174.
Clancy B.E., Behnke-Parks W.M., Andreasson J.O.L., Rosenfeld S.S., Block S.M. A universal pathway for kinesin stepping//Nat. Struct. Mol. Biol. -2011. -Vol. 18. -P. 1020-1027.
Coppin C.M., Finer J.T., Spudich J.A., Vale R.D. Detection of sub-8-nm movements of kinesin by high-resolution optical-trap microscopy//Proc. Natl. Acad. Sci. USA. -1996. -Vol. 93. -P. 1913-1917.
Coppin C.M., Pierce D.W., Hsu L., Vale R.D. The load dependence of kinesin's mechanical cycle//Proc. Natl. Acad. Sci. USA. -1997. -Vol. 94. -P. 8539-8544.
Coy D.L., Wagenbach M., Howard J. Kinesin takes one 8-nm step for each ATP that it hydrolyzes//J. Biol. Chem. -1999. -Vol. 274. -P. 3667-3671.
Crevel I.M., Lockhart A., Cross R.A. Weak and strong states of kinesin and ncd//J. Mol. Biol. -1996. -Vol. 257. -P. 66-76.
Cross R.A. The kinetic mechanism of kinesin//Trends Biochem. Sci. -2004. -Vol. 29. -P. 301-309.
Dagenbach E.M., Endow S.A. A new kinesin tree//J. Cell Sci. -2004. -Vol. 117. -P. 3-7.
David-Pfeuty T., Erickson H.P., Pantaloni D. Guanosinetriphosphatase activity of tubulin associated with microtubule assembly//Proc. Natl. Acad. Sci. USA. -1977. -Vol. 74. -P. 5372-5376.
Delius M., Leigh D.A. Walking molecules//Chem. Soc. Rev. -2011. -Vol. 40. -P. 3656-3676.
Derenyi I., Vicsek T. The kinesin walk: a dynamic model with elastically coupled heads//Proc. Natl. Acad. Sci. USA. -1996. -Vol. 93. -P. 6775-6779.
Endres N.F., Yoshioka C., Milligan R.A., Vale R.D. A lever-arm rotation drives motility of the minus-end-directed kinesin Ncd//Nature. -2006. -Vol. 439. -P. 875-878.
Fallesen T.L., Macosko J.C., Holzwarth G. Force-velocity relationship for multiple kinesin motors pulling a magnetic bead//Eur. Biophys. J. -2011. -Vol. 40. -P. 1071-1079.
Ferenz N.P., Gable A., Wadsworth P. Mitotic functions of kinesin-5//Semin. Cell Dev. Biol. -2010. -Vol. 21. -P. 255-259.
Feynman R.P. Ratchet and pawl//The Feynman lectures on physics. -Massachusetts: Addison-Wesley, 1963. -Vol. 1. -P. 443-451.
Fisher M.E., Kim Y.C. Kinesin crouches to sprint but resists pushing//Proc. Natl. Acad. Sci. USA. -2005. -Vol. 102. -P. 16209-16214.
Friel C.T., Bagshaw C.R., Howard J. Analysing the ATP turnover cycle of microtubule motors//Methods Mol. Biol. -2011. -Vol. 777. -P. 177-192.
Geeves M.A., Holmes K.C. The molecular mechanism of muscle contraction//Adv. Protein Chem. -2005. -Vol. 71. -P. 161-193.
Gibbons I.R. Studies on the protein components of cilia from tetrahymena pyriformis//Proc. Natl. Acad. Sci. USA. -1963. -Vol. 50. -P. 1002-1010.
Gittes F., Meyhofer E., Baek S., Howard J. Directional loading of the kinesin motor molecule as it buckles a microtubule//Biophys. J. -1996. -Vol. 70. -P. 418-429.
Gittes F., Mickey B., Nettleton J., Howard J. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape//J. Cell Biol. -1993. -Vol. 120. -P. 923-934.
Goldstein L.S. Kinesin molecular motors: transport pathways, receptors, and human disease//Proc. Natl. Acad. Sci. USA. -2001. -Vol. 98. -P. 6999-7003.
Hackney D.D. The tethered motor domain of a kinesin-microtubule complex catalyzes reversible synthesis of bound ATP//Proc. Natl. Acad. Sci. USA. -2005. -Vol. 102. -P. 18338-18343.
Hallen M.A., Liang Z.Y., Endow S.A. Two-state displacement by the kinesin-14 Ncd stalk//Biophys. Chem. -2011. -Vol. 154. -P. 56-65.
Hancock W.O., Howard J. Kinesin’s processivity results from mechanical and chemical coordination between the ATP hydrolysis cycles of the two motor domains//Proc. Natl. Acad. Sci. USA. -1999. -Vol. 96. -P. 13147-13152.
Heneen W.K. Kinetochores and microtubules in multipolar mitosis and chromosome orientation//Exp. Cell Res. -1975. -Vol. 91. -P. 57-62.
Hidaka M., Koga T., Gotoh A., Sanada M., Hirose K., Uchida T. Alzheimer's disease-related protein hGas7b interferes with kinesin motility//J. Biochem. -2012. -Vol. 151. -P. 593-598.
Higuchi H., Muto E., Inoue Y., Yanagida T. Kinetics of force generation by single kinesin molecules activated by laser photolysis of caged ATP//Proc. Natl. Acad. Sci. USA. -1997. -Vol. 94. -P. 4395-4400.
Hirokawa N. Cross-linker system between neurofilaments, microtubules, and membranous organelles in frog axons revealed by the quick-freeze, deep-etching method//J. Cell Biol. -1982. -Vol. 94. -P. 129-142.
Hirokawa N. Quick freeze, deep etch of the cytoskeleton//Methods Enzymol. -1986. -Vol. 134. -P. 598-612.
Hirokawa N. Axonal transport and the cytoskeleton//Curr. Opin. Neurobiol. -1993. -Vol. 3. -P. 724-731.
Hirokawa N. From electron microscopy to molecular cell biology, molecular genetics and structural biology: intracellular transport and kinesin superfamily proteins, KIFs: genes, structure, dynamics and functions//J. Electron Microsc. (Tokyo). -2011. -Vol. 60, supp. 1. -P. S63-S92.
Hirokawa N., Noda Y., Tanaka Y., Niwa S. Kinesin superfamily motor proteins and intracellular transport//Nat. Rev. Mol. Cell Biol. -2009. -Vol. 10. -P. 682-696.
Holmes K.C., Angert I., Kull F.J., Jahn W., Schroder R.R. Electron cryo-microscopy shows how strong binding of myosin to actin releases nucleotide//Nature. -2003. -Vol. 425. -P. 423-427.
Houdusse A., Cohen C. Structure of the regulatory domain of scallop myosin at 2 A resolution: implications for regulation//Structure. -1996. -Vol. 15. -P. 21-32.
Hua W., Chung J., Gelles J. Distinguishing inchworm and hand-over-hand processive kinesin movement by neck rotation measurements//Science. -2002. -Vol. 295. -P. 844-848.
Hunt A.J., Gittes F., Howard J. The force exerted by a single kinesin molecule against a viscous load//Biophys. J. -1994. -Vol. 67. -P. 766-781.
Huxley A.F., Simmons R.M. Proposed mechanism of force generation in striated muscle//Nature. -1971. -Vol. 233. -P. 533-538.
Hyeon C., Klumpp S., Onuchic J.N. Kinesin's backsteps under mechanical load//Phys. Chem. Chem. Phys. -2009. -Vol. 11. -P. 4899-4910.
Itoh H., Takahashi A., Adachi K., Noji H., Yasuda R., Yoshida M., Kinosita K. Jr. Mechanically driven ATP synthesis by F1-ATPase//Nature. -2004. -Vol. 427. -P. 465-468.
Kapitein L.C., Peterman E.J., Kwok B.H., Kim J.H., Kapoor T.M., Schmidt C.F. The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks//Nature. -2005. -Vol. 435. -P. 114-118.
Kaseda K., Higuchi H., Hirose K. Alternate fast and slow stepping of a heterodimeric kinesin molecule//Nat. Cell Biol. -2003. -Vol. 5. -P. 1079-1082.
Kikkawa M., Hirokawa N. High-resolution cryo-EM maps show the nucleotide binding pocket of KIF1A in open and closed conformations//EMBO J. -2006. -Vol. 25. -P. 4187-4194.
Kojima H., Muto E., Higuchi H., Yanagida T. Mechanics of single kinesin molecules measured by optical trapping nanometry//Biophys. J. -1997. -Vol. 73. -P. 2012-2022.
Kull F.J., Endow S.A. Force generation by kinesin and myosin cytoskeletal motor proteins//J. Cell Sci. -2013. -Vol. 126. -P. 9-19.
Kull F.J., Sablin E.P., Lau R., Fletterick R.J., Vale R.D. Crystal structure of the kinesin motor domain reveals a structural similarity to myosin//Nature. -1996. -Vol. 380. -P. 550-555.
Kull F.J., Vale R.D., Fletterick R.J. The case for a common ancestor: kinesin and myosin motor proteins and G proteins//J. Muscle Res. Cell Motil. -1998. -Vol. 19. -P. 877-886.
Kunwar A., Mogilner A. Robust transport by multiple motors with nonlinear force-velocity relations and stochastic load sharing//Phys. Biol. -2010. -Vol. 7. -P. 16012.
Kuznetsov S.A., Gelfand V.I. Bovine brain kinesin is a microtubule-activated ATPase//Proc. Natl. Acad. Sci. USA. -1986. -Vol. 83. -P. 8530-8534.
Lang M.J., Asbury C.L., Shaevitz J.W., Block S.M. An automated two-dimensional optical force clamp for single molecule studies//Biophys. J. -2002. -Vol. 83. -P. 491-501.
Lawrence C.J., Dawe R.K., Christie K.R., Cleveland D.W., Dawson S.C., Endow S.A., Goldstein L.S., Goodson H.V., Hirokawa N., Howard J., Malmberg R.L., McIntosh J.R., Miki H., Mitchison T.J., Okada Y., Reddy A.S., Saxton W.M., Schliwa M., Scholey J.M., Vale R.D., Walczak C.E., Wordeman L. A standardized kinesin nomenclature//J. Cell Biol. -2004. -Vol. 167. -P. 19-22.
Liu X., Gong H., Huang K. Oncogenic role of kinesin proteins and targeting kinesin therapy//Cancer Sci. -2013. -Vol. 104. -P. 651-656.
Luduena R.F. Multiple forms of tubulin: different gene products and covalent modifications//Int. Rev. Cytol. -1998. -Vol. 178. -P. 207-275.
Lymn R.W., Taylor E.W. Mechanism of adenosine triphosphate hydrolysis by actomyosin//Biochemistry. -1971. -Vol. 10. -P. 4617-4624.
Maes C., Wieren M.H. A Markov model for kinesin//Journal of Statistical Physics. -2003. -Vol. 112. -P. 329-355.
Marx A., Hoenger A., Mandelkow E. Structures of kinesin motor proteins//Cell Motil. Cytoskeleton. -2009. -Vol. 66. -P. 958-966.
Marx A., Müller J., Mandelkow E.M., Hoenger A., Mandelkow E. Interaction of kinesin motors, microtubules, and MAPs//J. Muscle Res. Cell Motil. -2006. -Vol. 27. -P. 125-137.
Meurer-Grob P., Kasparian J., Wade R.H. Microtubule structure at improved resolution//Biochemistry. -2001. -Vol. 40. -P. 8000-8008.
Meyhofer E., Howard J. The force generated by a single kinesin molecule against an elastic load//Proc. Natl. Acad. Sci. USA. -1995. -Vol. 92. -P. 574-578.
Moores C.A., Yu M., Guo J., Beraud C., Sakowicz R., Milligan R.A. A mechanism for microtubule depolymerization by KinI kinesins//Mol. Cell. -2002. -Vol. 9. -P. 903-909.
Nishiyama M., Higuchi H., Yanagida T. Chemomechanical coupling of the forward and backward steps of single kinesin molecules//Nat. Cell Biol. -2002. -Vol. 10. -P. 790-797.
Nishiyama M., Muto E., Inoue Y., Yanagida T., Higuchi H. Substeps within the 8-nm step of the ATPase cycle of single kinesin molecules//Nat. Cell Biol. -2001. -Vol. 3. -P. 425-428.
Nogales E., Wolf S.G., Downing K.H. Structure of the alpha beta tubulin dimer by electron crystallography//Nature. -1998. -Vol. 391. -P. 199-203.
Orozco J.T., Wedaman K.P., Signor D., Brown H., Rose L., Scholey J.M. Movement of motor and cargo along cilia//Nature. -1999. -Vol. 398. -P. 674.
Rayment I., Holden H.M., Whittaker M., Yohn C.B., Lorenz M., Holmes K.C., Milligan R.A. Structure of the actin-myosin complex and its implications for muscle contraction//Science. -1993. -Vol. 261. -P. 58-65.
Rice S., Lin A.W., Safer D., Hart C.L., Naber N., Carragher B.O., Cain S.M., Pechatnikova E., Wilson-Kubalek E.M., Whittaker M., Pate E., Cooke R., Taylor E.W., Milligan R.A., Vale R.D. A structural change in the kinesin motor protein that drives motility//Nature. -1999. -Vol. 402. -P. 778-784.
Rodionov V.I., Gyoeva F.K., Gelfand V.I. Kinesin is responsible for centrifugal movement of pigment granules in melanophores//Proc. Natl. Acad. Sci. USA. -1991. -Vol. 88. -P. 4956-4960.
Rosenfeld S.S., Fordyce P.M., Jefferson G.M., King P.H., Block S.M. Stepping and stretching. How kinesin uses internal strain to walk processively//J. Biol. Chem. -2003. -Vol. 278. -P. 18550-18556.
Rosenfeld S.S., Jefferson G.M., King P.H. ATP reorients the neck linker of kinesin in two sequential steps//J. Biol. Chem. -2001. -Vol. 276. -P. 40167-40174.
Sablin E.P., Kull F.J., Cooke R., Vale R.D., Fletterick R.J. Crystal structure of the motor domain of the kinesin-related motor ncd//Nature. -1996. -Vol. 380. -P. 555-559.
Sack S., Muller J., Marx A., Thormahlen M., Mandelkow E.M., Brady S.T., Mandelkow E. X-ray structure of motor and neck domains from rat brain kinesin//Biochemistry. -1997. -Vol. 36. -P. 16155-16165.
Sanhaji M., Friel C.T., Wordeman L., Louwen F., Yuan J. Mitotic centromere-associated kinesin (MCAK): a potential cancer drug target//Oncotarget. -2011. -Vol. 12. -P. 935-947.
Sellers J.R. Kinesin and NCD, two structural cousins of myosin//J. Muscle Res. Cell Motil. -1996. -Vol. 17. -P. 173-175.
Sellers J.R. Myosins: a diverse superfamily//Biochim. Biophys. Acta. -2000. -Vol. 1496. -P. 3-22.
Sellers J.R., Veigel C. Walking with myosin V//Curr. Opin. Cell Biol. -2006. -Vol. 18. -P. 68-73.
Sheetz M.P. Motor and cargo interactions//Eur. J. Biochem. -1999. -Vol. 262. -P. 19-25.
Schnitzer M.J., Block S.M. Kinesin hydrolyses one ATP per 8-nm step//Nature. -1997. -Vol. 388. -P. 386-390.
Schnitzer M.J., Visscher K., Block S.M. Force production by single kinesin motors//Nat. Cell Biol. -2000. -Vol. 2. -P. 718-723.
Svoboda K., Block S.M. Force and velocity measured for single kinesin molecules//Cell. -1994. -Vol. 77. -P. 773-784.
Svoboda K.C., Schmidt F., Schnapp B.J., Block S.M. Direct observation of kinesin stepping by optical trapping interferometry//Nature. -1993. -Vol. 365. -P. 721-727.
Taniguchi Y., Nishiyama M., Ishii Y., Yanagida T. Entropy rectifies the Brownian steps of kinesin//Nat. Chem. Biol. -2005. -Vol. 1. -P. 342-347.
Taylor E.W., Borisy G.G. Kinesin processivity//J. Cell Biol. -2000. -Vol. 151. -P. F27-F29.
Terada S., Kinjo M., Aihara M., Takei Y., Hirokawa N. Kinesin-1/Hsc70-dependent mechanism of slow axonal transport and its relation to fast axonal transport//EMBO J. -2010. -Vol. 29. -P. 843-854.
Tilney L.G., Bryan J., Bush D.J., Fujiwara K., Mooseker M.S., Murphy D.B., Snyder D.H. Microtubules: evidence for 13 protofilaments//J. Cell Biol. -1973. -Vol. 59. -P. 267-275.
Toprak E., Yildiz A., Hoffman M.T., Rosenfeld S.S., Selvin P.R. Why kinesin is so processive//Proc. Natl. Acad. Sci. USA. -2009. -Vol. 106. -P. 12717-12722.
Vale R.D., Funatsu T., Pierce D.W., Romberg L., Harada Y., Yanagida T. Direct observation of single kinesin molecules moving along microtubules//Nature. -1996. -Vol. 380. -P. 451-453.
Vale R.D., Milligan R.A. The way things move: looking under the hood of molecular motor proteins//Science. -2000. -Vol. 288. -P. 88-95.
Vale R.D., Reese T.S., Sheetz M.P. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility//Cell. -1985. -Vol. 42. -P. 39-50.
Vale R.D. Switches, latches, and amplifiers: common themes of G proteins and molecular motors//J. Cell Biol. -1996. -Vol. 135. -P. 291-302.
Visscher K., Schnitzer M.J., Block S.M. Single kinesin molecules studied with a molecular force clamp//Nature. -1999. -Vol. 400. -P. 184-189.
Voter W.A., Erickson H.P. Tubulin rings: curved filaments with limited flexibility and two modes of association//J. Supramol. Struct. -1979. -Vol. 10. -P. 419-431.
Walker R.A. Ncd and kinesin motor domains interact with both alpha-and beta-tubulin//Proc. Natl. Acad. Sci. USA. -1995. -Vol. 92. -P. 5960-5964.
Wang M.D., Schnitzer M.J., Yin H., Landick R., Gelles J., Block. S.M. Force and velocity measured for single molecules of RNA polymerase//Science. -1998. -Vol. 282. -P. 902-907.
Wade R.H. On and around microtubules: an overview//Mol. Biotechnol. -2009. -Vol. 43. -P. 177-191.
Wilson E.B. The cell in development and heredity. -New York: MacMillan Publishing Co., 1928. -377 p.
Yildiz A., Tomishige M., Gennerich A., Vale R.D. Intramolecular strain coordinates kinesin stepping behavior along microtubules//Cell. -2008. -Vol. 134. -P. 1030-1041.
Yildiz A., Tomishige M., Vale R.D., Selvin P.R. Kinesin walks hand-over-hand//Science. -2004. -Vol. 303. -P. 676-678.

Еще

Статья научная