A continuous network of lipid nanotubes fabricated from the gliding motility of kinesin powered microtubule filaments

Langmuir

Volumn 29, Issue 9, 2013, Pages 2992-2999

  Bouxsein, Nathan F ^a   Carroll Portillo, Amanda ^a   Bachand, Marlene ^a   Sasaki, Darryl Y ^b   Bachand, George D ^a  

^a SANDIA NATIONAL LABORATORIES   (United States)

^b SANDIA NATIONAL LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRANCHED NETWORK; COOPERATIVE INTERACTIONS; DIFFUSIVE TRANSPORT; ENERGY SOURCE; KINESINS; LIPID NANOTUBES; LIPID SOURCES; MEMBRANE SURFACE; MICROTUBULE FILAMENTS; MICROTUBULES; MILLIMETER-SCALE; MODEL SYSTEM; MOLECULAR MOTORS; MULTILAMELLAR LIPOSOMES; NANOTUBE NETWORKS; PHOSPHOLIPID VESICLES; SURFACE DENSITY; TRANSPORT APPLICATIONS; TRANSPORT SYSTEMS;

BIFURCATION (MATHEMATICS); LIPOSOMES; SEMICONDUCTOR QUANTUM DOTS; SURFACES; TWO DIMENSIONAL;

NANOTUBES;

KINESIN; NANOTUBE; PHOSPHOLIPID;

ADHESION; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; MECHANICS; METABOLISM; METHODOLOGY; MICROTUBULE; MOVEMENT (PHYSIOLOGY); NANOTECHNOLOGY; PROTEIN CONFORMATION; SURFACE PROPERTY;

ADHESIVENESS; KINESIN; MECHANICAL PROCESSES; MICROTUBULES; MODELS, MOLECULAR; MOVEMENT; NANOTECHNOLOGY; NANOTUBES; PHOSPHOLIPIDS; PROTEIN CONFORMATION; SURFACE PROPERTIES;

EID: 84874593387     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la304238u     Document Type: Article

References (60)

1. Bocquet, L.; Charlaix, E. Nanofluidics, from bulk to interfaces Chem. Soc. Rev. 2010, 39, 1073-1095
2. Eijkel, J. C. T.; van den Berg, A. Nanofluidics: what is it and what can we expect from it? Microfluid. Nanofluid. 2005, 1, 249-267
3. Korten, T.; MaÌŠnsson, A.; Diez, S. Towards the application of cytoskeletal motor proteins in molecular detection and diagnostic devices Curr. Opin. Biotechnol. 2010, 21, 477-488
4. Hess, H.; Bachand, G. D.; Vogel, V. Powering nanodevices with biomolecular motors Chem.-Eur. J. 2004, 10, 2110-2116
5. Hess, H. Engineering applications of biomolecular motors Annu. Rev. Biomed. Eng. 2011, 13, 429-450
6. Goel, A.; Vogel, V. Harnessing biological motors to engineer systems for nanoscale transport and assembly Nat. Nanotechnol. 2008, 3, 465-475
7. Thorn, K. S.; Ubersax, J. A.; Vale, R. D. Engineering the processive run length of the kinesin motor J. Cell Biol. 2000, 151, 1093-1100
8. Visscher, K.; Schnitzer, M. J.; Block, S. M. Single kinesin molecules studied with a molecular force clamp Nature 1999, 400, 184-189
9. Svoboda, K.; Block, S. M. Force and velocity measured for single kinesin molecules Cell 1994, 77, 773
10. Bachand, G. D.; Hess, H.; Ratna, B.; Satir, P.; Vogel, V. "Smart dust" biosensors powered by biomolecular motors Lab Chip 2009, 9, 1661-1666
11. Agarwal, A.; Hess, H. Biomolecular motors at the intersection of nanotechnology and polymer science Prog. Polym. Sci. 2010, 35, 252-277
12. Dayel, M. J.; Hom, E.; Verkman, A. Diffusion of green fluorescent protein in the aqueous-phase lumen of endoplasmic reticulum Biophys. J. 1999, 76, 2843
13. Cole, N. B.; Smith, C. L.; Sciaky, N.; Terasaki, M.; Edidin, M.; Lippincott-Schwartz, J. Diffusional mobility of Golgi proteins in membranes of living cells Science 1996, 797-800
14. Alberts, B.; Johnson, A.; Lewis, J.; Raff, M.; Roberts, K.; Walter, P. Essent. Cell Biol., 3rd Ed.; Garland Science: New York, 2009.
15. Leduc, C.; Campàs, O.; Joanny, J. F.; Prost, J.; Bassereau, P. Mechanism of membrane nanotube formation by molecular motors Biochim. Biophys. Acta 2010, 1798, 1418-1426
16. Leduc, C.; Campàs, O.; Zeldovich, K. B.; Roux, A.; Jolimaitre, P.; Bourel-Bonnet, L.; Goud, B.; Joanny, J. F.; Bassereau, P.; Prost, J. Cooperative extraction of membrane nanotubes by molecular motors Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 17096
17. Roux, A.; Cappello, G.; Cartaud, J.; Prost, J.; Goud, B.; Bassereau, P. A minimal system allowing tubulation with molecular motors pulling on giant liposomes Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 5394
18. He, S.; Lam, A. T. C.; Jeune-Smith, Y.; Hess, H. Modeling negative cooperativity in streptavidin adsorption onto biotinylated microtubules Langmuir 2012, 28, 10635-10639
19. Howard, J.; Hudspeth, A.; Vale, R. Movement of microtubules by single kinesin molecules Nature 1989, 342, 154
20. Duke, T.; Holy, T. E.; Leibler, S. "Gliding assays" for motor proteins: a theoretical analysis Phys. Rev. Lett. 1995, 74, 330-333
21. Karlsson, M.; Sott, K.; Davidson, M.; Cans, A.-S.; Linderholm, P.; Chiu, D.; Orwar, O. Formation of geometrically complex lipid nanotube-vesicle networks of higher-order topologies Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 11573-8
22. Raucher, D.; Sheetz, M. P. Characteristics of a membrane reservoir buffering membrane tension Biophys. J. 1999, 77, 1992-2002
23. Derényi, I.; Jülicher, F.; Prost, J. Formation and interaction of membrane tubes Phys. Rev. Lett. 2002, 88, 238101
24. de Gennes, P.-G.; Prost, J. The Physics of Liquid Crystals; Clarendon Press: Oxford, 1995.
25. Van der Linden, E.; Dröge, J. Deformability of lamellar droplets Physica A 1993, 193, 439-447
26. Helfrich, W. Steric interaction of fluid membranes in multilayer systems Z. Naturforsch., A 1978, 33, 305-315
27. Nallet, F.; Roux, D.; Prost, J. Dynamic light scattering study of dilute lamellar phases Phys. Rev. Lett. 1989, 62, 276-279
28. Tristram-Nagle, S.; Petrache, H. I.; Nagle, J. F. Structure and interactions of fully hydrated dioleoylphosphatidylcholine bilayers Biophys. J. 1998, 75, 917-925
29. Pan, J.; Tristram-Nagle, S.; Kučerka, N.; Nagle, J. F. Temperature dependence of structure, bending rigidity, and bilayer interactions of dioleoylphosphatidylcholine bilayers Biophys. J. 2008, 94, 117-124
30. Koster, G.; Cacciuto, A.; Derényi, I.; Frenkel, D.; Dogterom, M. Force barriers for membrane tube formation Phys. Rev. Lett. 2005, 94, 68101
31. Koster, G.; VanDuijn, M.; Hofs, B.; Dogterom, M. Membrane tube formation from giant vesicles by dynamic association of motor proteins Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 15583
32. Schnitzer, M. J.; Visscher, K.; Block, S. M. Force production by single kinesin motors Nat. Cell Biol. 2000, 2, 718-723
33. Marsh, D.; King, M. D. Prediction of the critical micelle concentrations of mono- and di-acyl phospholipids Chem. Phys. Lipids 1986, 42, 271-277
34. Cevc, G.; Marsh, D. Phospholipid Bilayers: Physical Principles and Models; John Wiley and Sons Ltd.: New York, 1987.
35. Fallesen, T. L.; Macosko, J. C.; Holzwarth, G. Force-velocity relationship for multiple kinesin motors pulling a magnetic bead Eur. Biophys. J. 2011, 1-9
36. Kumar, S.; ten Siethoff, L.; Persson, M.; Lard, M.; te Kronnie, G.; Linke, H.; MaÌŠnsson, A. Antibodies covalently immobilized on actin filaments for fast myosin driven analyte transport PLoS One 2012, 7, e46298
37. Cuvelier, D.; Chiaruttini, N.; Bassereau, P.; Nassoy, P. Pulling long tubes from firmly adhered vesicles Europhys. Lett. 2005, 71, 1015
38. Shenoy, S.; Moldovan, R.; Fitzpatrick, J.; Vanderah, D. J.; Deserno, M.; Lösche, M. In-plane homogeneity and lipid dynamics in tethered bilayer lipid membranes (tBLMs) Soft Matter 2010, 6, 1263-1274
39. Wong, J.; Chilkoti, A.; Moy, V. T. Direct force measurements of the streptavidin-biotin interaction Biomol. Eng. 1999, 16, 45-55
40. Evans, E. Probing the relation between force-lifetime-and chemistry in single molecular bonds Annu. Rev. Biophys. Biomol. Struct. 2001, 30, 105-128
41. Evans, E.; Ludwig, F. Dynamic strengths of molecular anchoring and material cohesion in fluid biomembranes J. Phys.: Condens. Matter 2000, 12, A315
42. Lasek, R. J.; Brady, S. T. Attachment of transported vesicles to microtubules in axoplasm is facilitated by Amp-pnp Nature 1985, 316, 645-647
43. MaÌŠnsson, A.; Sundberg, M.; Balaz, M.; Bunk, R.; Nicholls, I. A.; Omling, P.; TaÌŠgerud, S.; Montelius, L. In vitro sliding of actin filaments labelled with single quantum dots Biochem. Biophys. Res. Commun. 2004, 314, 529-34
44. Carroll-Portillo, A.; Bachand, M.; Greene, A. C.; Bachand, G. D. In vitro capture, transport, and detection of protein analytes using kinesin-based nanoharvesters Small 2009, 5, 1835-40
45. Bachand, G. D.; Rivera, S. B.; Boal, A. K.; Gaudioso, J.; Liu, J.; Bunker, B. C. Assembly and transport of nanocrystal CdSe quantum dot nanocomposites using microtubules and kinesin motor proteins Nano Lett. 2004, 4, 817-821
46. Nitzsche, B.; Ruhnow, F.; Diez, S. Quantum-dot-assisted characterization of microtubule rotations during cargo transport Nat. Nanotechnol. 2008, 3, 552-6
47. Filippov, A.; Orädd, G.; Lindblom, G. Influence of cholesterol and water content on phospholipid lateral diffusion in bilayers Langmuir 2003, 19, 6397-6400
48. Daniels, D. R.; Turner, M. S. Diffusion on membrane tubes: a highly discriminatory test of the Saffman-Delbruck theory Langmuir 2007, 23, 6667-70
49. Domanov, Y. A.; Aimon, S.; Toombes, G. E. S.; Renner, M.; Quemeneur, F.; Triller, A.; Turner, M. S.; Bassereau, P. Mobility in geometrically confined membranes Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 12605
50. Merkel, R.; Sackmann, E.; Evans, E. Molecular friction and epitactic coupling between monolayers in supported bilayers J. Phys. (Paris) 1989, 50, 1535-1555
51. Harris, T. Diffusion with "collisions" between particles J. Appl. Probab. 1965, 2, 323-338
52. Lizana, L.; Ambjörnsson, T. Diffusion of finite-sized hard-core interacting particles in a one-dimensional box: Tagged particle dynamics Phys. Rev. E: Stat., Nonlinear, Soft Matter Phys. 2009, 80, 051103
53. Leduc, C.; Padberg-Gehle, K.; Varga, V.; Helbing, D.; Diez, S.; Howard, J. Molecular crowding creates traffic jams of kinesin motors on microtubules Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 6100-5
54. Conway, L.; Wood, D.; Tüzel, E.; Ross, J. L. Motor transport of self-assembled cargos in crowded environments Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 20814-9
55. Baas, P. W.; Deitch, J. S.; Black, M. M.; Banker, G. A. Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite Proc. Natl. Acad. Sci. U. S. A. 1988, 85, 8335-9
56. Ehrhardt, D. W. Straighten up and fly right: microtubule dynamics and organization of non-centrosomal arrays in higher plants Curr. Opin. Cell Biol. 2008, 20, 107-16
57. Sawin, K. E.; Tran, P. T. Cytoplasmic microtubule organization in fission yeast Yeast 2006, 23, 1001-14
58. Coy, D. L.; Wagenbach, M.; Howard, J. Kinesin takes one 8-nm step for each ATP that it hydrolyzes J. Biol. Chem. 1999, 274, 3667-3671
59. Longair, M. H.; Baker, D. A.; Armstrong, J. D. Simple neurite tracer: Open source software for reconstruction, visualization and analysis of neuronal processes Bioinformatics 2011, 27, 2453-2454
60. Schindelin, J.; Arganda-Carreras, I.; Frise, E.; Kaynig, V.; Longair, M.; Pietzsch, T.; Preibisch, S.; Rueden, C.; Saalfeld, S.; Schmid, B. Fiji: an open-source platform for biological-image analysis Nat. Methods 2012, 9, 676-682