How molecular motors extract order from chaos (a key issues review)

Molecular motors are the workhorses of living cells. Seemingly by 'magic', these molecules are able to complete purposeful tasks while being immersed in a sea of thermal chaos. Here, we review the current understanding of how these machines work, present simple models based on thermal ratchets, discuss implications for statistical physics, and provide an overview of ongoing research in this important and fascinating field of study.

[1]  J. F. Stoddart,et al.  Great expectations: can artificial molecular machines deliver on their promise? , 2012, Chemical Society reviews.

[2]  Matthias Rief,et al.  The myosin coiled-coil is a truly elastic protein structure , 2002, Nature materials.

[3]  P. Dimroth,et al.  Unique rotary ATP synthase and its biological diversity. , 2008, Annual review of biophysics.

[4]  P. Cramer,et al.  Structural Basis of Transcription: RNA Polymerase II at 2.8 Ångstrom Resolution , 2001, Science.

[5]  Gerber,et al.  Atomic Force Microscope , 2020, Definitions.

[6]  M. Smoluchowski,et al.  Gültigkeitsgrenzen des zweiten Hauptsatzes der Wärmetheorie , 1927 .

[7]  Yujun Zheng,et al.  A stochastic model for kinesin bidirectional stepping. , 2014, The Journal of chemical physics.

[8]  S. Burgess,et al.  The structure of dynein-c by negative stain electron microscopy. , 2004, Journal of structural biology.

[9]  E. Mandelkow,et al.  Structures of kinesin motor proteins. , 2009, Cell motility and the cytoskeleton.

[10]  Christoph F. Schmidt,et al.  Direct observation of kinesin stepping by optical trapping interferometry , 1993, Nature.

[11]  B Ermentrout,et al.  Dynamics of single-motor molecules: the thermal ratchet model. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[12]  P. Kloeden,et al.  Numerical Solution of Stochastic Differential Equations , 1992 .

[13]  Steven M. Block,et al.  Force and velocity measured for single kinesin molecules , 1994, Cell.

[14]  K. Schütze,et al.  Force generation of organelle transport measured in vivo by an infrared laser trap , 1990, Nature.

[15]  J. Spudich,et al.  Single myosin molecule mechanics: piconewton forces and nanometre steps , 1994, Nature.

[16]  K. Kawaguchi.  Energetics of kinesin‐1 stepping mechanism , 2008, FEBS letters.

[17]  M. Delbrück,et al.  A physicist looks at biology , 1949 .

[18]  M. Schnitzer,et al.  Force production by single kinesin motors , 2000, Nature Cell Biology.

[19]  J. Howard,et al.  Kinesin Takes One 8-nm Step for Each ATP That It Hydrolyzes* , 1999, The Journal of Biological Chemistry.

[20]  Bier,et al.  Fluctuation driven ratchets: Molecular motors. , 1994, Physical review letters.

[21]  N. Thompson,et al.  Total internal reflection fluorescence. , 1984, Annual review of biophysics and bioengineering.

[22]  D. Hackney,et al.  Kinesin ATPase: rate-limiting ADP release. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[23]  I. Glynn,et al.  Annual review prize lecture. ‘All hands to the sodium pump’. , 1993, The Journal of physiology.

[24]  J. Hörber,et al.  Processive behaviour of kinesin observed using micro-fabricated cantilevers , 2011, Nanotechnology.

[25]  T Hodge,et al.  A myosin family tree. , 2000, Journal of cell science.

[26]  Magnasco.  Molecular combustion motors. , 1994, Physical review letters.

[27]  M. Schliwa,et al.  Molecular motors , 2003, Nature.

[28]  M. O’Donnell,et al.  Cellular DNA replicases: components and dynamics at the replication fork. , 2005, Annual review of biochemistry.

[29]  M. Magnasco,et al.  Forced thermal ratchets. , 1993, Physical review letters.

[30]  J. Joanny,et al.  Coordination and collective properties of molecular motors: theory. , 2010, Current opinion in cell biology.

[31]  Ryoichi Kawai,et al.  Are motor proteins power strokers, Brownian motors or both? (Invited Paper) , 2005, SPIE International Symposium on Fluctuations and Noise.

[32]  H E Huxley,et al.  The Mechanism of Muscular Contraction , 1965, Scientific American.

[33]  Yonggun Jun,et al.  High-precision test of Landauer's principle in a feedback trap. , 2014, Physical review letters.

[34]  J. Maxwell,et al.  Theory of Heat , 1892 .

[35]  G. Woehlke,et al.  Kinetic and Mechanistic Basis of the Nonprocessive Kinesin-3 Motor NcKin3* , 2006, Journal of Biological Chemistry.

[36]  M. Smoluchowski,et al.  Experimentell nachweisbare, der üblichen Thermodynamik widersprechende Molekularphänomene , 1927 .

[37]  R. A. Laymon,et al.  A three-domain structure of kinesin heavy chain revealed by DNA sequence and microtubule binding analyses , 1989, Cell.

[38]  J. Spudich,et al.  Fluorescent actin filaments move on myosin fixed to a glass surface. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[39]  V. Ramakrishnan,et al.  Ribosome Structure and the Mechanism of Translation , 2002, Cell.

[40]  L S Goldstein,et al.  Kinesin molecular motors: Transport pathways, receptors, and human disease , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[41]  E. Mandelkow,et al.  The Crystal Structure of Dimeric Kinesin and Implications for Microtubule-Dependent Motility , 1997, Cell.

[42]  C. Jarzynski.  Nonequilibrium Equality for Free Energy Differences , 1996, cond-mat/9610209.

[43]  Polly M. Fordyce,et al.  Stepping and Stretching , 2003, The Journal of Biological Chemistry.

[44]  A. Huxley,et al.  Structural Changes in Muscle During Contraction: Interference Microscopy of Living Muscle Fibres , 1954, Nature.

[45]  Stephen M. Barnett,et al.  Information erasure without an energy cost , 2010, Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[46]  Mark J. Schnitzer,et al.  Single kinesin molecules studied with a molecular force clamp , 1999, Nature.

[47]  E. Eisenberg,et al.  Rate-limiting step in the actomyosin adenosinetriphosphatase cycle: studies with myosin subfragment 1 cross-linked to actin. , 1985, Biochemistry.

[48]  David G Grier,et al.  Observation of flux reversal in a symmetric optical thermal ratchet. , 2005, Physical review letters.

[49]  C. Van den Broeck,et al.  Efficiency of isothermal molecular machines at maximum power. , 2012, Physical review letters.

[50]  E. Raff,et al.  Evidence that the head of kinesin is sufficient for force generation and motility in vitro. , 1990, Science.

[51]  Francisco J Cao,et al.  Feedback control in a collective flashing ratchet. , 2004, Physical review letters.

[52]  O. Schmitt.  The heat of shortening and the dynamic constants of muscle , 2017 .

[53]  K E Drexler,et al.  Molecular engineering: An approach to the development of general capabilities for molecular manipulation. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[54]  A. Knight,et al.  Coupling ATP hydrolysis to mechanical work , 1999, Nature Cell Biology.

[55]  J. Houtgraaf,et al.  A concise review of DNA damage checkpoints and repair in mammalian cells. , 2006, Cardiovascular revascularization medicine : including molecular interventions.

[56]  E. Taylor,et al.  Mechanism of adenosine triphosphate hydrolysis by actomyosin. , 1971, Biochemistry.

[57]  Toshio Ando,et al.  Video imaging of walking myosin V by high-speed atomic force microscopy , 2010, Nature.

[58]  Y. Tonomura,et al.  MECHANISM OF MUSCULAR CONTRACTION , 1953 .

[59]  J. Mateos,et al.  AC-driven Brownian motors: A Fokker-Planck treatment , 2008, 0810.5612.

[60]  H. Huxley,et al.  Structural Basis of the Cross-Striations in Muscle , 1953, Nature.

[61]  R. Nakamoto,et al.  The rotary mechanism of the ATP synthase. , 2008, Archives of biochemistry and biophysics.

[62]  Tiina Lehto,et al.  Observing structure, function and assembly of single proteins by AFM. , 2002, Progress in biophysics and molecular biology.

[63]  W. Astbury,et al.  X -ray studies of the molecular structure of myosin , 1940, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[64]  R. Landauer,et al.  Irreversibility and heat generation in the computing process , 1961, IBM J. Res. Dev..

[65]  A. Huxley.  Muscle structure and theories of contraction. , 1957, Progress in biophysics and biophysical chemistry.

[66]  N. Hirokawa,et al.  Kinesin and dynein superfamily proteins in organelle transport and cell division. , 1998, Current opinion in cell biology.

[67]  Ryo Nitta,et al.  KIF1A Alternately Uses Two Loops to Bind Microtubules , 2004, Science.

[68]  Joshua W. Shaevitz,et al.  Probing the kinesin reaction cycle with a 2D optical force clamp , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[69]  Vladimir Gelfand,et al.  Bovine brain kinesin is a microtubule-activated ATPase. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[70]  Takeshi Sakamoto,et al.  Direct observation of the mechanochemical coupling in myosin Va during processive movement , 2008, Nature.

[71]  R. Leighton,et al.  The Feynman Lectures on Physics; Vol. I , 1965 .

[72]  L. Amos.  Molecular motors: not quite like clockwork , 2008, Cellular and Molecular Life Sciences.

[73]  Hiroaki Takagi,et al.  Fluctuation analysis of mechanochemical coupling depending on the type of biomolecular motors. , 2008, Physical review letters.

[74]  K. Hirose,et al.  Three-dimensional cryoelectron microscopy of dimeric kinesin and ncd motor domains on microtubules. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[75]  S. Chu,et al.  Observation of a single-beam gradient force optical trap for dielectric particles. , 1986, Optics letters.

[76]  F. Jülicher,et al.  Modeling molecular motors , 1997 .

[77]  C S Peskin,et al.  Cellular motions and thermal fluctuations: the Brownian ratchet. , 1993, Biophysical journal.

[78]  R. Astumian.  Thermodynamics and kinetics of a Brownian motor. , 1997, Science.

[79]  R. Vale.  Millennial musings on molecular motors , 1999 .

[80]  Robert A Cross,et al.  The kinetic mechanism of kinesin. , 2004, Trends in biochemical sciences.

[81]  R. Vale,et al.  Kinesin Walks Hand-Over-Hand , 2004, Science.

[82]  L. Goldstein,et al.  Bead movement by single kinesin molecules studied with optical tweezers , 1990, Nature.

[83]  Steven M Block,et al.  Kinesin motor mechanics: binding, stepping, tracking, gating, and limping. , 2007, Biophysical journal.

[84]  K. Hotta.  [Mechanism of muscular contraction and its regulation]. , 1972, Nihon seirigaku zasshi. Journal of the Physiological Society of Japan.

[85]  Hugh E. Huxley: birth of the filament sliding model of muscle contraction. , 2002, Trends in cell biology.

[86]  A. Huxley,et al.  Tension development in highly stretched vertebrate muscle fibres , 1966, The Journal of physiology.

[87]  S. Endow,et al.  A kinesin family tree. , 2000, Journal of cell science.

[88]  Steven P. Gross,et al.  Molecular Motors: Strategies to Get Along , 2004, Current Biology.

[89]  K. Verhey,et al.  Traffic control: regulation of kinesin motors , 2009, Nature Reviews Molecular Cell Biology.

[90]  T. Yanagida,et al.  Motility of single one-headed kinesin molecules along microtubules. , 2001, Biophysical journal.

[91]  S. Endow.  Microtubule motors in spindle and chromosome motility. , 1999, European journal of biochemistry.

[92]  Matthias Rief,et al.  Myosin-V is a processive actin-based motor , 1999, Nature.

[93]  N. Hirokawa,et al.  A processive single-headed motor: kinesin superfamily protein KIF1A. , 1999, Science.

[94]  D. Manstein,et al.  Molecular mechanism of actomyosin-based motility , 2005, Cellular and Molecular Life Sciences CMLS.

[95]  Anne Houdusse,et al.  Structural and functional insights into the Myosin motor mechanism. , 2010, Annual review of biophysics.

[96]  Reinhard Jahn,et al.  SNAREs — engines for membrane fusion , 2006, Nature Reviews Molecular Cell Biology.

[97]  Drexler Ke,et al.  Molecular engineering: An approach to the development of general capabilities for molecular manipulation. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[98]  F. Marchesoni,et al.  Artificial Brownian motors: Controlling transport on the nanoscale , 2008, 0807.1283.

[99]  M. Fisher,et al.  Molecular motors: a theorist's perspective. , 2007, Annual review of physical chemistry.

[100]  Yoshiyuki Sowa,et al.  Bacterial flagellar motor , 2004, Quarterly Reviews of Biophysics.

[101]  Steven M. Block,et al.  Kinesin Moves by an Asymmetric Hand-OverHand Mechanism , 2003 .

[102]  S. Quake,et al.  The Biological Frontier of Physics , 2006 .

[103]  Henry Hess,et al.  Engineering applications of biomolecular motors. , 2011, Annual review of biomedical engineering.

[104]  Timothy J. Mitchison,et al.  Mitotic spindle organization by a plus-end-directed microtubule motor , 1992, Nature.

[105]  Martin Bier,et al.  The stepping motor protein as a feedback control ratchet , 2007, Biosyst..

[106]  James A. Spudich,et al.  The myosin swinging cross-bridge model , 2001, Nature Reviews Molecular Cell Biology.