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Dynamic and Active Proteins: Biomolecular Motors in Engineered Nanostructures

  • Marisela VélezEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 940)

Abstract

In Nature, proteins perform functions that go well beyond controlled self-assembly at the nano scale. They are the principal components of diverse “biological machines” that can self-assemble into dynamic aggregates that achieve the cold conversion of chemical energy into motion to realize complex functions involved in cell division, cellular transport and cell motility. Nowadays, we have identified many of the proteins involved in these “molecular machines” and know much about their biochemistry, structure and biophysical behavior. Additionally, we have a rich toolbox of resources to engineer the basic dynamic working units into nanostructures to provide them with motion and the capacity to manipulate, transport, separate or sense single molecules to develop in vitro sensors and bioassays. This chapter summarizes some of the progress made in incorporating bio-molecular motors and dynamic self-organizing proteins into protein based functional nanostructures.

Keywords

Biomolecular motors Nanostructures Dynamic self-assembly Cytoskeletal proteins Molecular nanotechnology Single molecule Biosensors Nanoscale assemblies Biomaterials 

References

  1. 1.
    Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell. Garland, New YorkGoogle Scholar
  2. 2.
    Chan V, Asada HH, Bashir R et al (2014) Utilization and control of bioactuators across multiple length scales. Lab Chip 14:653–670PubMedCrossRefGoogle Scholar
  3. 3.
    Agarwal A, Hess H (2010) Biomolecular motors at the intersection of nanotechnology and polymer science. Prog Polym Sci 35:252–277CrossRefGoogle Scholar
  4. 4.
    Fischer T, Agarwal A, Hess H (2009) A smart dust biosensor powered by kinesin motors. Nat Nanotechnol 4:162–166PubMedCrossRefGoogle Scholar
  5. 5.
    Chen Y, Wang M, Mao C (2004) An autonomous DNA nanomotor powered by a DNA enzyme. Angew Chem Int Ed 43:3554–3557CrossRefGoogle Scholar
  6. 6.
    Bath J, Turberfield AJ (2007) DNA nanomachines. Nat Nanotechnol 2:275–284PubMedCrossRefGoogle Scholar
  7. 7.
    Forties RA, Wang MD (2014) Discovering the power of single molecules. Cell 157:4–7PubMedCrossRefGoogle Scholar
  8. 8.
    Lavelle C (2014) Pack, unpack, bend, twist, pull, push: the physical side of gene expression. Curr Opin Genet Dev 25:74–84PubMedCrossRefGoogle Scholar
  9. 9.
    Gennerich A (2014) Molecular motors: DNA takes control. Nat Nanotechnol 9:11–12PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Mavroidis C, Dubey A, Yarmush ML (2004) Molecular machines. Annu Rev Biomed Eng 6:363–395PubMedCrossRefGoogle Scholar
  11. 11.
    Schliwa M, Woehlke G (2003) Molecular motors. Nature 422:759–765PubMedCrossRefGoogle Scholar
  12. 12.
    Phillips R, Kondev J, Theriot J (2009) Physical biology of the cell. Garland Science, Taylo & Francis Group, New YorkGoogle Scholar
  13. 13.
    Vale RD, Milligan RA (2000) The way things move: looking under the hood of molecular motor proteins. Science 288:88–95PubMedCrossRefGoogle Scholar
  14. 14.
    Mattoo RH, Goloubinoff P (2014) Molecular chaperones are nanomachines that catalytically unfold misfolded and alternatively folded proteins. Cell Mol Life Sci 71:3311–3325PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Inobe T, Matouschek A (2014) Paradigms of protein degradation by the proteasome. Curr Opin Struct Biol 24:156–164PubMedCrossRefGoogle Scholar
  16. 16.
    Sowaa Y, Homma M, Ishijimad A, Berry RM (2014) Hybrid-fuel bacterial flagellar motors in Escherichia coli. PNAS 111:3436–3441CrossRefGoogle Scholar
  17. 17.
    Wang J (2013) Nanomachines: fundamentals and applications. WILEY-VCH, HobokenCrossRefGoogle Scholar
  18. 18.
    Gao W, Wang J (2014) The environmental impact of micro/nanomachines: a review. ACS Nano 8:3170–3180PubMedCrossRefGoogle Scholar
  19. 19.
    Soong RK, Bachand GD, Neves HP, Olkhovets AG, Craighead HG, Montemagno CD (2000) Powering an inorganic nanodevice with a biomolecular motor. Science 290:1555–1558PubMedCrossRefGoogle Scholar
  20. 20.
    Dong C, Dinu CZ (2013) Molecular trucks and complementary tracks for bionanotechnological applications. Curr Opin Biotechnol 24:612–619PubMedCrossRefGoogle Scholar
  21. 21.
    Howard J (2001) Mechanics of motor proteins and the cytoskeleton. Sinauer Associates, SunderlandGoogle Scholar
  22. 22.
    Cabeen MT, Jacobs-Wagner C (2010) The bacterial cytoskeleton. Annu Rev Genet 44:365–392PubMedCrossRefGoogle Scholar
  23. 23.
    Ingerson-Mahar M, Gitai Z (2012) A growing family: the expanding universe of the bacterial cytoskeleton. FEMS Microbiol Rev 36(1):256–266PubMedCrossRefGoogle Scholar
  24. 24.
    Callaway E (2008) Bacteria’s new bones. Nature 451:124–126PubMedCrossRefGoogle Scholar
  25. 25.
    Pilhofer M, Jensen GJ (2013) The bacterial cytoskeleton: more than twisted filaments. Curr Opin Cell Biol 25:125–133PubMedCrossRefGoogle Scholar
  26. 26.
    Löwe J, van den Ent F, Amos LA (2004) Molecules of the bacterial cytoskeleton. Annu Rev Biophys Biomol Struct 33:177–198PubMedCrossRefGoogle Scholar
  27. 27.
    Wintrebert P (1931) La rotation immédiate de l’oeuf pondu et la rotation d’activation chez Discoglossus pictus Otth. C R Soc Biol 106:439–442Google Scholar
  28. 28.
    Celler K, Koning RI, Koster AJ, van Wezel GP (2013) Multidimensional view of the bacterial cytoskeleton. J Bacteriol 195:1627–1636PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Lin L, Thanbichler M (2013) Nucleotide-independent cytoskeletal scaffolds in bacteria. Cytoskeleton 70:409–423PubMedCrossRefGoogle Scholar
  30. 30.
    Capetanaki Y, Papathanasiou S, Diokmetzidou A, Vatsellas G, Tsikitis M (2015) Desmin related disease: a matter of cell survival failure. Curr Opin Cell Biol 32:113–120PubMedCrossRefGoogle Scholar
  31. 31.
    Hol EM, Pekny M (2015) Glial fibrillary acidic protein (GFAP) and the astrocyte intermediate filament system in diseases of the central nervous system. Curr Opin Cell Biol 32:121–130PubMedCrossRefGoogle Scholar
  32. 32.
    Toivola DM, Boor P, Alam C, Strnad P (2015) Keratins in health and disease. Curr Opin Cell Biol 32:73–81PubMedCrossRefGoogle Scholar
  33. 33.
    Quinlan RA, Bromley EH, Pohl E (2015) A silk purse from a sow’s ear – bioinspired materials based on α-helical coiled coils. Curr Opin Cell Biol 32:131–137PubMedCrossRefGoogle Scholar
  34. 34.
    Huber F, Boire A, López MP, Koenderink GH (2015) Cytoskeletal crosstalk: when three different personalities team up. Curr Opin Cell Biol 32:39–47PubMedCrossRefGoogle Scholar
  35. 35.
    Snider NT, Omary MB (2014) Post-translational modifications of intermediate filament proteins: mechanisms and functions. Nat Rev Mol Cell Biol 15:163–177PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC (1990) Atomic structure of the actin: DNase I complex. Nature 347:37–44PubMedCrossRefGoogle Scholar
  37. 37.
    Cooper JA (1987) Effects of cytochalasin and phalloidin on actin. J Cell Biol 105:1473–1478PubMedCrossRefGoogle Scholar
  38. 38.
    Galland R, Leduc P, Guérin C, Peyrade D, Blanchoin L, Théry M (2013) Fabrication of three-dimensional electrical connections by means of directed actin self-organization. Nat Mater 12:416–421PubMedCrossRefGoogle Scholar
  39. 39.
    Mitchison T, Kirschner M (1984) Microtubule assembly nucleated by isolated centrosomes. Nature 312:232–237PubMedCrossRefGoogle Scholar
  40. 40.
    Brangwynne CP, MacKintosh FC, Kumar S, Geisse NA, Talbot J, Mahadevan L, Parker KK, Ingber DE, Weitz DA (2006) Microtubules can bear enhanced compressive loads in living cells because of lateral reinforcement. J Cell Biol 173:733–741PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Li H, DeRosier D, Nicholson WV, Nogales E, Downing KH (2002) Microtubule structure at 8 a resolution. Structure 10:1317–1328PubMedCrossRefGoogle Scholar
  42. 42.
    Chretien D, Metoz E, Verde E, Karsenti E, Wade RH (1992) Lattice defects in microtubules: protofilament numbers vary within individual microtubules. J Cell Biol 117:1031–1040PubMedCrossRefGoogle Scholar
  43. 43.
    Behrens S, Rahn K, Habicht W, Böhm KJ, Rösner H, Dinjus E, Unger E (2002) Nanoscale particle arrays induced by highly ordered protein assemblies. Adv Mater 14:1621–1625CrossRefGoogle Scholar
  44. 44.
    Mitchison T, Kirschner M (1984) Dynamic instability of microtubule growth. Nature 312:237–242PubMedCrossRefGoogle Scholar
  45. 45.
    Dimitrov A, Quesnoit M, Moutel S, Cantaloube I, Poüs C, Perez F (2008) Detection of GTP-tubulin conformation in vivo reveals a role for GTP remnants in microtubule rescues. Science 322:1353–1356PubMedCrossRefGoogle Scholar
  46. 46.
    Nogales E, Wang H-W (2006) Structural mechanisms underlying nucleotide-dependent self-assembly of tubulin and its relatives. Curr Opin Struct Biol 16:221–229PubMedCrossRefGoogle Scholar
  47. 47.
    Dogterom M, Kerssemakers JWJ, Romet-Lemonne G, Janson ME (2005) Force generation by dynamic microtubules. Curr Opin Cell Biol 17:67–74PubMedCrossRefGoogle Scholar
  48. 48.
    Westermann S, Wang H-W, Avila-Sakar A, Drubin DG, Nogales E, Barnes G (2006) The Dam1 kinetochore ring complex moves processively on depolymerizing microtubule ends. Nature 440:565–569PubMedCrossRefGoogle Scholar
  49. 49.
    Davis LJ, Odde DJ, Block SM, Gross SP (2002) The importance of lattice defects in katanin-mediated microtubule severing in vitro. Biophys J 82:2916–2927PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Bouchard AM, Warrender CE, Osbourn GC (2006) Harnessing microtubule dynamic instability for nanostructure assembly. Phys Rev E 74:041902CrossRefGoogle Scholar
  51. 51.
    Tucker R, Katira P, Hess H (2008) Herding nanotransporters: localized activation via release and sequestration of control molecules. Nano Lett 8:221–226PubMedCrossRefGoogle Scholar
  52. 52.
    Spoerke ED, Bachand GD, Liu J, Sasaki D, Bunker BC (2008) Directing the polar organization of microtubules. Langmuir 24:7039–7043PubMedCrossRefGoogle Scholar
  53. 53.
    Schiff PB, Fant J, Horwitz SB (1979) Promotion of microtubule assembly in vitro by taxol. Nature 277:665–667PubMedCrossRefGoogle Scholar
  54. 54.
    Margolin W (2009) Sculpting the bacterial cell. Curr Biol 19:R812–R822PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Bi E, Lutkenhaus J (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354:161–164PubMedCrossRefGoogle Scholar
  56. 56.
    Jones LJF, Carballido-López R, Errington J (2001) Control of cell shape in bacteria. Cell 104:913–922PubMedCrossRefGoogle Scholar
  57. 57.
    Nora Ausmees JRK, Jacobs-Wagner C (2003) The bacterial cytoskeleton: an intermediate filament-like function in cell shape. Cell 115:705–713PubMedCrossRefGoogle Scholar
  58. 58.
    Mingorance J, Rivas G, Vélez M, Gómez-Puertas P, Vicente M (2010) Strong FtsZ is with the force: mechanisms to constrict bacteria. Trends Microbiol 18:348–356PubMedCrossRefGoogle Scholar
  59. 59.
    Mateos-Gil P, Paez A, Hörger I, Rivas G, Vicente M, Tarazona P, Vélez M (2012) Depolymerization dynamics of individual filaments of bacterial cytoskeletal protein FtsZ. Proc Natl Acad Sci 109:8133–8138PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Ostrov N, Gazit E (2010) Genetic engineering of biomolecular scaffolds for the fabrication of organic and metallic nanowires. Angew Chem Int Ed 49:3018–3021CrossRefGoogle Scholar
  61. 61.
    Mateos-Gil P, Márquez I, López-Navajas P, Jiménez M, Vicente M, Mingorance J, Rivas G, Vélez M (2012) FtsZ polymers bound to lipid bilayers through ZipA form dynamic two dimensional networks. Biochim Biophys Acta 1818:806–813PubMedCrossRefGoogle Scholar
  62. 62.
    Loose M, Mitchison TJ (2014) The bacterial cell division proteins FtsA and FtsZ self-organize into dynamic cytoskeletal patterns. Nat Cell Biol 16:38–46PubMedCrossRefGoogle Scholar
  63. 63.
    Case RB, Rice S, Hart CL, Ly B, Vale RD (2000) Role of the kinesin neck linker and catalytic core in microtubule-based motility. Curr Biol 10:157–160PubMedCrossRefGoogle Scholar
  64. 64.
    Wu XS, Rao K, Zhang H, Wang F, Sellers JR, Matesic LE, Copeland NG, Jenkins NA, Hammer JA (2002) Identification of an organelle receptor for myosin-Va. Nat Cell Biol 4:271–278PubMedCrossRefGoogle Scholar
  65. 65.
    de Lanerolle P (2012) Nuclear actin and myosins at a glance. J Cell Sci 125:4945–4949PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Huxley AF, Simmons RM (1971) Proposed mechanism of force generation in striated muscle. Nature 233:533–538PubMedCrossRefGoogle Scholar
  67. 67.
    Astumian RD (1997) Thermodynamics and kinetics of a brownian motor. Science 276:917–922PubMedCrossRefGoogle Scholar
  68. 68.
    Block SM (2007) Kinesin motor mechanics: binding, stepping, tracking, gating, and limping. Biophys J 92:2986–2995PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Spudich JA (2001) The myosin swinging cross-bridge model. Nat Rev Mol Cell Biol 2:387–392PubMedCrossRefGoogle Scholar
  70. 70.
    Tyska MJ, Mooseker MS (2003) Myosin-V motility: these levers were made for walking. Trends Cell Biol 13:447–451PubMedCrossRefGoogle Scholar
  71. 71.
    Pierobon P, Achouri S, Courty S, Dunn AR, Spudich JA, Dahan M, Cappello G (2009) Velocity, processivity, and individual steps of single myosin V molecules in live cells. Biophys J 96:4268–4275PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Mehta AD, Rock RS, Rief M, Spudich JA, Mooseker MS, Cheney RE (1999) Myosin-V is a processive actin-based motor. Nature 400:590–593PubMedCrossRefGoogle Scholar
  73. 73.
    Schindler TD, Chen L, Lebel P, Nakamura M, Bryant Z (2014) Engineering myosins for long-range transport on actin filaments. Nat Nanotechnol 9:33–38PubMedCrossRefGoogle Scholar
  74. 74.
    Nakamura M, Chen L, Howes SC, Schindler TD, Nogales E, Bryant Z (2014) Remote control of myosin and kinesin motors using light-activated gearshifting. Nat Nanotechnol 9:693–697PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Frederick Gittes BM, Nettleton J, Howard J (1993) Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J Cell Biol 120:923–934CrossRefGoogle Scholar
  76. 76.
    Hirokawa N, Takemura R (2004) Kinesin superfamily proteins and their various functions and dynamics. Exp Cell Res 301:50–59PubMedCrossRefGoogle Scholar
  77. 77.
    Gunawardena S, Goldstein LSB (2004) Cargo-carrying motor vehicles on the neuronal highway: transport pathways and neurodegenerative disease. J Neurobiol 58:258–271PubMedCrossRefGoogle Scholar
  78. 78.
    Sharp DJ, Rogers GC, Scholey JM (2000) Microtubule motors in mitosis. Nature 407:41–47PubMedCrossRefGoogle Scholar
  79. 79.
    Insinna C, Besharse JC (2008) Intraflagellar transport and the sensory outer segment of vertebrate photoreceptors. Dev Dyn 237:1982–1992PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Cl A (2005) Kinesin: world’s tiniest biped. Curr Opin Cell Biol 17:89–97CrossRefGoogle Scholar
  81. 81.
    Coy DL, Wagenbach M, Howard J (1999) Kinesin takes one 8-nm step for each ATP that it hydrolyzes. J Biol Chem 274:3667–3671PubMedCrossRefGoogle Scholar
  82. 82.
    Hancock WO, Howard J (1999) Kinesin’s processivity results from mechanical and chemical coordination between the ATP hydrolysis cycles of the two motor domains. Proc Natl Acad Sci 96:13147–13152PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Coy DL, Hancock WO, Wagenbach M, Howard J (1999) Kinesin/’s tail domain is an inhibitory regulator of the motor domain. Nat Cell Biol 1:288–292PubMedCrossRefGoogle Scholar
  84. 84.
    Howard J, Hudspeth AJ, Vale RD (1989) Movement of microtubules by single kinesin molecules. Nature 342:154–158PubMedCrossRefGoogle Scholar
  85. 85.
    Gazit E (2007) Use of biomolecular templates for the fabrication of metal nanowires. FEBS J 274:317–322PubMedCrossRefGoogle Scholar
  86. 86.
    Patolsky F, Weizmann Y, Willner I (2004) Actin-based metallic nanowires as bio-nanotransporters. Nat Mater 3:692–695PubMedCrossRefGoogle Scholar
  87. 87.
    Behrens S, Wu J, Habicht W, Unger E (2004) Silver nanoparticle and nanowire formation by microtubule templates. Chem Mater 16:3085–3090CrossRefGoogle Scholar
  88. 88.
    Boal AK, Headley TJ, Tissot RG, Bunker BC (2004) Microtubule-templated biomimetic mineralization of lepidocrocite. Adv Funct Mater 14:19–24CrossRefGoogle Scholar
  89. 89.
    Dinu CZ, Bale SS, Zhu G, Dordick JS (2009) Tubulin encapsulation of carbon nanotubes into functional hybrid assemblies. Small 5:310–315PubMedCrossRefGoogle Scholar
  90. 90.
    Kim T, Cheng L-J, Kao M-T, Hasselbrink EF, Guo L, Meyhofer E (2009) Biomolecular motor-driven molecular sorter. Lab Chip 9:1282–1285PubMedCrossRefGoogle Scholar
  91. 91.
    Turner D, Chang C, Fang K, Cuomo P, Murphy D (1996) Kinesin movement on glutaraldehyde-fixed microtubules. Anal Biochem 242:20–25PubMedCrossRefGoogle Scholar
  92. 92.
    Turner DC, Chang C, Fang K, Brandow SL, Murphy DB (1995) Selective adhesion of functional microtubules to patterned silane surfaces. Biophys J 69:2782–2789PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Limberis L, Magda JJ, Stewart RJ (2001) Polarized alignment and surface immobilization of microtubules for kinesin-powered nanodevices. Nano Lett 1:277–280CrossRefGoogle Scholar
  94. 94.
    Doot RK, Hess H, Vogel V (2007) Engineered networks of oriented microtubule filaments for directed cargo transport. Soft Matter 3:349–356CrossRefGoogle Scholar
  95. 95.
    Agayan RR, Tucker R, Nitta T, Ruhnow F, Walter WJ, Diez S, Hess H (2013) Optimization of isopolar microtubule arrays. Langmuir 29:2265–2272PubMedCrossRefGoogle Scholar
  96. 96.
    Katira P, Hess H (2010) Two-stage capture employing active transport enables sensitive and fast biosensors. Nano Lett 10:567–572PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Hess H (2011) Engineering applications of biomolecular motors. Annu Rev Biomed Eng 13:429–450PubMedCrossRefGoogle Scholar
  98. 98.
    Lard M, ten Siethoff L, Generosi J, Månsson A, Linke H (2014) Molecular motor transport through hollow nanowires. Nano Lett 14:3041–3046PubMedCrossRefGoogle Scholar
  99. 99.
    Fujimoto K, Kitamura M, Yokokawa M, Kanno I, Kotera H, Yokokawa R (2013) Colocalization of quantum dots by reactive molecules carried by motor proteins on polarized microtubule arrays. ACS Nano 7:447–455PubMedCrossRefGoogle Scholar
  100. 100.
    Suzuki H, Yamada A, Oiwa K, Nakayama H, Mashiko S (1997) Control of actin moving trajectory by patterned poly(methylmethacrylate) tracks. Biophys J 72:1997–2001PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Nicolau DV, Suzuki H, Mashiko S, Taguchi T, Yoshikawa S (1999) Actin motion on microlithographically functionalized myosin surfaces and tracks. Biophys J 77:1126–1134PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Sundberg M, Bunk R, Albet-Torres N, Kvennefors A, Persson F, Montelius L, Nicholls IA, Ghatnekar-Nilsson S, Omling P, Tågerud S, Månsson A (2006) Actin filament guidance on a chip: toward high-throughput assays and lab-on-a-chip applications. Langmuir 22:7286–7295PubMedCrossRefGoogle Scholar
  103. 103.
    Clemmens J, Hess H, Lipscomb R, Hanein Y, Böhringer KF, Matzke CM, Bachand GD, Bunker BC, Vogel V (2003) Mechanisms of microtubule guiding on microfabricated kinesin-coated surfaces: chemical and topographic surface patterns. Langmuir 19:10967–10974CrossRefGoogle Scholar
  104. 104.
    Ishigure Y, Nitta T (2014) Understanding the guiding of kinesin/microtubule-based microtransporters in microfabricated tracks. Langmuir 30:12089–12096PubMedCrossRefGoogle Scholar
  105. 105.
    Riveline D, Ott A, Jülicher F, Winkelmann DA, Cardoso O, Lacapère J-J, Magnúsdóttir S, Viovy JL, Gorre-Talini L, Prost J (1998) Acting on actin: the electric motility assay. Eur Biophys J 27:403–408PubMedCrossRefGoogle Scholar
  106. 106.
    van den Heuvel MGL, de Graaff MP, Dekker C (2006) Molecular sorting by electrical steering of microtubules in kinesin-coated channels. Science 312:910–914PubMedCrossRefGoogle Scholar
  107. 107.
    Hutchins BM, Platt M, Hancock WO, Williams ME (2007) Directing transport of CoFe2O4-functionalized microtubules with magnetic fields. Small 3:126–131PubMedCrossRefGoogle Scholar
  108. 108.
    Taesung K, Ming-Tse K, Edgar M, Ernest FH (2007) Biomolecular motor-driven microtubule translocation in the presence of shear flow: analysis of redirection behaviours. Nanotechnology 18:025101CrossRefGoogle Scholar
  109. 109.
    Kumar KRS, Kamei T, Fukaminato T, Tamaoki N (2014) Complete ON/OFF photoswitching of the motility of a nanobiomolecular machine. ACS Nano 8:4157–4165PubMedCrossRefGoogle Scholar
  110. 110.
    Schroeder V, Korten T, Linke H, Diez S, Maximov I (2013) Dynamic guiding of motor-driven microtubules on electrically heated, smart polymer tracks. Nano Lett 13:3434–3438PubMedCrossRefGoogle Scholar
  111. 111.
    Hiyama S, Moritani Y, Gojo R, Takeuchi S, Sutoh K (2010) Biomolecular-motor-based autonomous delivery of lipid vesicles as nano- or microscale reactors on a chip. Lab Chip 10:2741–2748PubMedCrossRefGoogle Scholar
  112. 112.
    Muthukrishnan G, Hutchins BM, Williams ME, Hancock WO (2006) Transport of semiconductor nanocrystals by kinesin molecular motors. Small 2:626–630PubMedCrossRefGoogle Scholar
  113. 113.
    Yokokawa R, Tarhan MC, Kon T, Fujita H (2008) Simultaneous and bidirectional transport of kinesin-coated microspheres and dynein-coated microspheres on polarity-oriented microtubules. Biotechnol Bioeng 101:1–8PubMedCrossRefGoogle Scholar
  114. 114.
    Bottier C, Fattaccioli J, Tarhan MC, Yokokawa R, Morin FO, Kim B, Collard D, Fujita H (2009) Active transport of oil droplets along oriented microtubules by kinesin molecular motors. Lab Chip 9:1694–1700PubMedCrossRefGoogle Scholar
  115. 115.
    Ryuji Yokokawa ST, Nishiura M, Ohkura R, Kon T, Sutoh K, Fujita H (2004) Hybrid nano transfer system by biomolecular linear motors. J Microelectromech Syst 13:612–619CrossRefGoogle Scholar
  116. 116.
    Tarhan MC, Yokokawa R, Bottier C, Collard D, Fujita H (2010) A nano-needle/microtubule composite gliding on a kinesin-coated surface for target molecule transport. Lab Chip 10:86–91PubMedCrossRefGoogle Scholar
  117. 117.
    Boal AK, Bachand GD, Rivera SB, Bunker BC (2006) Interactions between cargo-carrying biomolecular shuttles. Nanotechnology 17:349CrossRefGoogle Scholar
  118. 118.
    Brunner C, Wahnes C, Vogel V (2007) Cargo pick-up from engineered loading stations by kinesin driven molecular shuttles. Lab Chip 7:1263–1271PubMedCrossRefGoogle Scholar
  119. 119.
    Bachand GD, Rivera SB, Boal AK, Gaudioso J, Liu J, Bunker BC (2004) Assembly and transport of nanocrystal CdSe quantum Dot nanocomposites using microtubules and kinesin motor proteins. Nano Lett 4:817–821CrossRefGoogle Scholar
  120. 120.
    Diez S, Reuther C, Dinu C, Seidel R, Mertig M, Pompe W, Howard J (2003) Stretching and transporting DNA molecules using motor proteins. Nano Lett 3:1251–1254CrossRefGoogle Scholar
  121. 121.
    Dinu CZ, Opitz J, Pompe W, Howard J, Mertig M, Diez S (2006) Parallel manipulation of bifunctional DNA molecules on structured surfaces using kinesin-driven microtubules. Small 2:1090–1098PubMedCrossRefGoogle Scholar
  122. 122.
    Bachand GD, Rivera SB, Carroll-Portillo A, Hess H, Bachand M (2006) Active capture and transport of virus particles using a biomolecular motor-driven, nanoscale antibody sandwich assay. Small 2:381–385PubMedCrossRefGoogle Scholar
  123. 123.
    Martin BD, Soto CM, Blum AS, Sapsford KE, Whitley JL, Johnson JE, Chatterji A, Ratna BR (2006) An engineered virus as a bright fluorescent tag and scaffold for cargo proteins—capture and transport by gliding microtubules. J Nanosci Nanotechnol 6:2451–2460PubMedCrossRefGoogle Scholar
  124. 124.
    Lin C-T, Kao M-T, Kurabayashi K, Meyhofer E (2008) Self-contained, biomolecular motor-driven protein sorting and concentrating in an ultrasensitive microfluidic chip. Nano Lett 8:1041–1046PubMedCrossRefGoogle Scholar
  125. 125.
    Lard M, ten Siethoff L, Kumar S, Persson M, te Kronnie G, Linke H, Månsson A (2013) Ultrafast molecular motor driven nanoseparation and biosensing. Biosens Bioelectron 48:145–152PubMedCrossRefGoogle Scholar
  126. 126.
    Bachand GD, Hess H, Ratna B, Satir P, Vogel V (2009) “Smart dust” biosensors powered by biomolecular motors. Lab Chip 9:1661–1666PubMedCrossRefGoogle Scholar
  127. 127.
    Schmidt C, Vogel V (2010) Molecular shuttles powered by motor proteins: loading and unloading stations for nanocargo integrated into one device. Lab Chip 10:2195–2198PubMedCrossRefGoogle Scholar
  128. 128.
    Hess H (2006) Self-assembly driven by molecular motors. Soft Matter 2:669–677CrossRefGoogle Scholar
  129. 129.
    Aoyama S, Shimoike M, Hiratsuka Y (2013) Self-organized optical device driven by motor proteins. Proc Natl Acad Sci 110:16408–16413PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Hess H, Clemmens J, Brunner C, Doot R, Luna S, Ernst K-H, Vogel V (2005) Molecular self-assembly of “nanowires” and “nanospools” using active transport. Nano Lett 5:629–633PubMedCrossRefGoogle Scholar
  131. 131.
    Liu H, Spoerke ED, Bachand M, Koch SJ, Bunker BC, Bachand GD (2008) Biomolecular motor-powered self-assembly of dissipative nanocomposite rings. Adv Mater 20:4476–4481CrossRefGoogle Scholar
  132. 132.
    Ryuzo K, Akira K, Yoshihito O, Jian Ping G (2010) Microtubule bundle formation driven by ATP: the effect of concentrations of kinesin, streptavidin and microtubules. Nanotechnology 21:145603CrossRefGoogle Scholar
  133. 133.
    Lam AT, Curschellas C, Krovvidi D, Hess H (2014) Controlling self-assembly of microtubule spools via kinesin motor density. Soft Matter 10:8731–8736PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Surrey T, Nédélec F, Leibler S, Karsenti E (2001) Physical properties determining self-organization of motors and microtubules. Science 292:1167–1171PubMedCrossRefGoogle Scholar
  135. 135.
    He Y, Liu DR (2010) Autonomous multistep organic synthesis in a single isothermal solution mediated by a DNA walker. Nat Nanotechnol 5:778–782PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Goel A, Vogel V (2008) Harnessing biological motors to engineer systems for nanoscale transport and assembly. Nat Nanotechnol 3:465–475PubMedCrossRefGoogle Scholar
  137. 137.
    Zheng Z, Daniel WL, Giam LR, Huo F, Senesi AJ, Zheng G, Mirkin CA (2009) Multiplexed protein arrays enabled by polymer pen lithography: addressing the inking challenge. Angewandte Chemie (International ed. in English) 48:7626–7629Google Scholar
  138. 138.
    Lund K, Manzo AJ, Dabby N, Michelotti N, Johnson-Buck A, Nangreave J, Taylor S, Pei R, Stojanovic MN, Walter NG, Winfree E, Yan H (2010) Molecular robots guided by prescriptive landscapes. Nature 465:206–210PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Yin P, Choi HMT, Calvert CR, Pierce NA (2008) Programming biomolecular self-assembly pathways. Nature 451:318–322PubMedCrossRefGoogle Scholar
  140. 140.
    Clemmens J, Hess H, Doot R, Matzke CM, Bachand GD, Vogel V (2004) Motor-protein “roundabouts”: microtubules moving on kinesin-coated tracks through engineered networks. Lab Chip 4:83–86PubMedCrossRefGoogle Scholar
  141. 141.
    Hess H, Howard J, Vogel V (2002) A piconewton forcemeter assembled from microtubules and kinesins. Nano Lett 2:1113–1115CrossRefGoogle Scholar
  142. 142.
    Coti KK, Belowich ME, Liong M, Ambrogio MW, Lau YA, Khatib HA, Zink JI, Khashab NM, Stoddart JF (2009) Mechanised nanoparticles for drug delivery. Nanoscale 1:16–39PubMedCrossRefGoogle Scholar
  143. 143.
    Ye X, Hemida M, Zhang HM, Hanson P, Ye Q, Yang D (2012) Current advances in Phi29 pRNA biology and its application in drug delivery. Wiley Interdiscip Rev RNA 3:469–481PubMedCrossRefGoogle Scholar
  144. 144.
    Lipowsky R, Chai Y, Klumpp S, Liepelt S, Müller MJI (2006) Molecular motor traffic: from biological nanomachines to macroscopic transport. Physica A Stat Mech Appl 372:34–51CrossRefGoogle Scholar
  145. 145.
    Jülicher F, Ajdari A, Prost J (1997) Modeling molecular motors. Rev Mod Phys 69:1269–1282CrossRefGoogle Scholar
  146. 146.
    Leduc C, Ruhnow F, Howard J, Diez S (2007) Detection of fractional steps in cargo movement by the collective operation of kinesin-1 motors. Proc Natl Acad Sci 104:10847–10852PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    Konrad JB, Roland S, Peter M, Eberhard U (2001) Motor protein-driven unidirectional transport of micrometer-sized cargoes across isopolar microtubule arrays. Nanotechnology 12:238CrossRefGoogle Scholar
  148. 148.
    Haimo LT, Thaler CD (1994) Regulation of organelle transport: lessons from color change in fish. BioEssays 16:727–733CrossRefGoogle Scholar
  149. 149.
    van Delden RA, Koumura N, Harada N, Feringa BL (2002) Unidirectional rotary motion in a liquid crystalline environment: color tuning by a molecular motor. Proc Natl Acad Sci 99:4945–4949PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832PubMedCrossRefGoogle Scholar
  151. 151.
    Koenderink GH, Dogic Z, Nakamura F, Bendix PM, MacKintosh FC, Hartwig JH, Stossel TP, Weitz DA (2009) An active biopolymer network controlled by molecular motors. Proc Natl Acad Sci 106:15192–15197PubMedPubMedCentralCrossRefGoogle Scholar
  152. 152.
    Li Q, Fuks G, Moulin E, Maaloum M, Rawiso M, Kulic I, Foy JT, Giuseppone N (2015) Macroscopic contraction of a gel induced by the integrated motion of light-driven molecular motors. Nat Nanotechnol 10:161–165PubMedCrossRefGoogle Scholar
  153. 153.
    Sano K-I, Kawamura R, Tominaga T, Oda N, Ijiro K, Osada Y (2011) Self-repairing filamentous actin hydrogel with hierarchical structure. Biomacromolecules 12:4173–4177PubMedCrossRefGoogle Scholar
  154. 154.
    Yeghiazarian L, Mahajan S, Montemagno C, Cohen C, Wiesner U (2005) Directed motion and cargo transport through propagation of polymer-gel volume phase transitions. Adv Mater 17:1869–1873CrossRefGoogle Scholar
  155. 155.
    Yoshida R (2010) Self-oscillating gels driven by the belousov–zhabotinsky reaction as novel smart materials. Adv Mater 22:3463–3483PubMedCrossRefGoogle Scholar
  156. 156.
    Howse JR, Topham P, Crook CJ, Gleeson AJ, Bras W, Jones RAL, Ryan AJ (2006) Reciprocating power generation in a chemically driven synthetic muscle. Nano Lett 6:73–77PubMedCrossRefGoogle Scholar
  157. 157.
    Keber FC, Loiseau E, Sanchez T, DeCamp SJ, Giomi L, Bowick MJ, Marchetti MC, Dogic Z, Bausch AR (2014) Topology and dynamics of active nematic vesicles. Science 345:1135–1139PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Instituto de Catálisis y PetroleoquímicaCantoblancoSpain

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