Measuring the elasticity of clathrin-coated vesicles via atomic force microscopy

Biophysical Journal

Volumn 90, Issue 9, 2006, Pages 3333-3344

  Jin, Albert J ^a   Prasad, Kondury ^b   Smith, Paul D ^a   Lafer, Eileen M ^b   Nossal, Ralph ^c  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BIOGENESIS; BIOPHYSICS; CELL FUNCTION; CELL STRUCTURE; COMPLEX FORMATION; COMPRESSION; ELASTICITY; MEASUREMENT; MEMBRANE VESICLE; MOLECULAR MODEL; PROTEIN DEFECT; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; RIGIDITY;

EID: 33646155956     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.068742     Document Type: Article

References (63)

1. Mousavi, S. A., L. Malerod, T. Berg, and R. Kjeken. 2004. Clathrin-dependent endocytosis. Biochem. J. 377:1-16.
2. Conner, S. D., and S. L. Schmid. 2003. Regulated portals of entry into the cell. Nature. 422:37-44.
3. Brodsky, F. M., C. Y. Chen, C. Knuehl, M. C. Towler, and D. E. Wakeham. 2001. Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell Dev. Biol. 17:517-568.
4. Marsh, M., and H. T. McMahon. 1999. Cell biology - the structural era of endocytosis. Science. 285:215-220.
5. Lafer, E. M. 2002. Clathrin-protein interactions. Traffic. 3:513-520.
6. Chen, Y. J., P. J. Zhang, E. H. Egelman, and J. E. Hinshaw. 2004. The stalk region of dynamin drives the constriction of dynamin tubes. Nat. Struct. Mol. Biol. 11:574-575.
7. Wenk, M. R., and P. De Camilli. 2004. Protein-lipid interactions and phosphoinositide metabolism in membrane traffic: insights from vesicle recycling in nerve terminals. Proc. Natl. Acad. Sci. USA. 101:8262-8269.
8. Blondeau, F., B. Ritter, P. D. Allaire, S. Wasiak, M. Girard, N. K. Hussain, A. Angers, V. Legendre-Guillemin, L. Roy, D. Boismenu, R. E. Kearney, A. W. Bell, J. J. M. Bergeron, and P. S. McPherson. 2004. Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc. Natl. Acad. Sci. USA. 101:3833-3838.
9. Yamashita, T., T. Hige, and T. Takahashi. 2005. Vesicle endocytosis requires dynamin-dependent GTP hydrolysis at a fast CNS synapse. Science. 307:124-127.
10. Jin, A. J., and R. Nossal. 2000. Rigidity of triskelion arms and clathrin nets. Biophys. J. 78:1183-1194.
11. Binnig, G., C. F. Quate, and C. Gerber. 1986. Atomic force microscope. Phys. Rev. Lett. 56:930-933.
12. Hansma, H. G. 2001. Surface biology of DNA by atomic force microscopy. Annu. Rev. Phys. Chem. 52:71-92.
13. Wang, K., J. G. Forbes, and A. J. Jin. 2001. Single molecule measurements of titin elasticity. Prog. Biophys. Mol. Biol. 77:1-44.
14. Zlatanova, J., and S. H. Leuba. 2003. Chromatin fibers, one-at-a-time. J. Mol. Biol. 331:1-19.
15. Pelling, A. E., Y. Li, W. Shi, and J. K. Gimzewski. 2005. Nanoscale visualization and characterization of Myxococcus xanthus cells with atomic force microscopy. Proc. Natl. Acad. Sci. USA. 102:6484-6489.
16. Fotin, A., Y. F. Cheng, P. Sliz, N. Grigorieff, S. C. Harrison, T. Kirchhausen, and T. Walz. 2004. Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature. 432:573-579.
17. Smith, C. J., N. Grigorieff, and B. M. F. Pearse. 1998. Clathrin coats at 21 Å resolution: a cellular assembly designed to recycle multiple membrane receptors. EMBO J. 17:4943-4953.
18. Vigers, G., R. Crowther, and B. Pearse. 1986. Location of the 100 kD-50 kD accessory proteins in clathrin coats. EMBO J. 5:2079-2085.
19. Nandi, P. K., G. Irace, P. P. Vanjaarsveld, R. E. Lippoldt, and H. Edelhoch. 1982. Instability of coated vesicles in concentrated sucrose solutions. Proc. Natl. Acad. Sci. USA. 79:5881-5885.
20. Choi, E. J., A. J. Jin, S.-L. Niu, P. D. Smith, and B. J. Litman. 2004. Visualizing individual rhodopsin (a G-Protein-coupled receptor) molecules in native disk and reconstituted membranes via atomic force microscopy. Tech. Proc. 2004 Nanotech. Trade Show. 1:63-66.
21. Tokumasu, F., A. J. Jin, G. W. Feigenson, and J. A. Dvorak. 2003. Nanoscopic lipid domain dynamics revealed by atomic force microscopy. Biophys. J. 84:2609-2618.
22. Tokumasu, F., A. J. Jin, G. W. Feigenson, and J. A. Dvorak. 2002. Atomic force microscope: a new technology for the elucidation of lipid membrane domain formation and phase behavior. Rec. Res. Dev. Biophys. 1:135-152.
23. Hutter, J. L., and J. Bechhoefer. 1993. Calibration of atomic-force microscope tips. Rev. Sci. Instrum. 64:1868-1873.
24. Villarrubia, J. S. 1997. Algorithms for scanned probe microscope image simulation, surface reconstruction, and tip estimation. J. Res. Natl. Inst. Stand. Technol. 102:425-454.
25. Vick, D., M. J. Brett, and K. Westra. 2002. Porous thin films for the characterization of atomic force microscope tip morphology. Thin Solid Films. 408:79-86.
26. Kohyama, T., D.M. Kroll, and G. Gompper. 2003. Budding of crystalline domains in fluid membranes. Phys. Rev. E. 68:061905-061919.
27. Baumgart, T., S. T. Hess, and W. W. Webb. 2003. Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature. 425:821-824.
28. Rawicz, W., K. C. Olbrich, T. McIntosh, D. Needham, and E. Evans. 2000. Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys. J. 79:328-339.
29. Gozdz, W. T., and G. Gompper. 1999. Shapes and shape transformations of two-component membranes of complex topology. Phys. Rev. E. 59:4305-4316.
30. Seifert, U. 1997. Configurations of fluid membranes and vesicles. Adv. Phys. 46:13-137.
31. Carpick, R. W., D. Y. Sasaki, M. S. Marcus, M. A. Eriksson, and A. R. Burns. 2004. Polydiacetylene films: a review of recent investigations into chromogenic transitions and nanomechanical properties. J. Phys. Cond. Matter. 16:R679-R697.
32. Gu, X. H., T. Nguyen, L. P. Sung, M. R. VanLandingham, M. J. Fasolka, J. W. Martin, Y. C. Jean, D. Nguyen, N. K. Chang, and T. Y. Wu. 2004. Advanced techniques for nanocharacterization of polymeric coating surfaces. JCT Res. 1:191-200.
33. Dimitriadis, E. K., F. Horkay, J. Maresca, B. Kachar, and R. S. Chadwick. 2002. Determination of elastic moduli of thin layers of soft material using the atomic force microscope. Biophys. J. 82:2798-2810.
34. Xiao, T., and K. Liao. 2003. Non-linear elastic response of fullerene balls under uniform and axial deformations. Nanotechnology. 14:1197-1202.
35. Jin, A. J., and M. E. Fisher. 1993. Effective interface Hamiltonians for short-range critical wetting. Phys. Rev. B. 47:7365-7388.
36. Podgornik, R., S. Svetina, and B. Zeks. 1995. Parametrization invariance and shape equations of elastic axisymmetrical vesicles. Phys. Rev. E. 51:544-547.
37. Naito, H., M. Okuda, and O. Y. Zhongcan. 1995. New solutions to the Helfrich variation problem for the shapes of lipid bilayer vesicles - beyond Delaunays surfaces. Phys. Rev. Lett. 74:4345-4348.
38. Kawakatsu, T., D. Andelman, K. Kawasaki, and T. Taniguchi. 1993. Phase-transitions and shapes of two-component membranes and vesicles. 1. Strong segregation limit. J. Phys. II. 3:971-997.
39. Lee, C. H., W. C. Lin, and J. P. Wang. 2001. All-optical measurements of the bending rigidity of lipid-vesicle membranes across structural phase transitions. Phys. Rev. E. 64:020901.
40. Lopez, R. 1997. Surfaces of constant mean curvature bounded by two planar curves. Ann. Glob. Anal. Geom. 15:201-210.
41. Wong, E. W., P. E. Sheehan, and C. M. Lieber. 1997. Nanobeam mechanics: elasticity, strength, and toughness of nanorods and nanotubes. Science. 277:1971-1975.
42. Nossal, R. 2001. Energetics of clathrin basket assembly. Traffic. 2:138-147.
43. Edidin, M. 2001. Shrinking patches and slippery rafts: scales of domains in the plasma membrane. Trends Cell Biol. 11:492-496.
44. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
45. Nossal, R. 2005. Assembly of clathrin baskets. Macromol. Symp. 219:1-8.
46. Ford, M. G. J., I. G. Mills, B. J. Peter, Y. Vallis, G. J. K. Praefcke, P. R. Evans, and H. T. McMahon. 2002. Curvature of clathrin-coated pits driven by epsin. Nature. 419:361-366.
47. Habermann, B. 2004. The BAR-domain family of proteins: a case of bending and binding? The membrane bending and GTPase-binding functions of proteins from the BAR-domain family. EMBO Rep. 5:250-255.
48. Hurley, J. H., and B. Wendland. 2002. Endocytosis: driving membranes around the bend. Cell. 111:143-146.
49. Brown, C. M., and N. O. Petersen. 1999. Free clathrin triskelions are required for the stability of clathrin-associated adaptor protein (AP-2) coated pit nucleation sites. Biochem. Cell Biol. 77:439-448.
50. Baba, T., C. Rauch, M. Xue, N. Terada, Y. Fujii, H. Ueda, I. Takayama, S. Ohno, E. Farge, and S. B. Sato. 2001. Clathrin-dependent and clathrin-independent endocytosis are differentially sensitive to insertion of poly (ethylene glycol)-derivatized cholesterol in the plasma membrane. Traffic. 2:501-512.
51. Heuser, J. E., and R. G. W. Anderson. 1989. Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J. Cell Biol. 108:389-400.
52. Gaidarov, I., F. Santini, R. A. Warren, and J. H. Keen. 1999. Spatial control of coated-pit dynamics in living cells. Nat. Cell Biol. 1:1-7.
53. Wu, X. F., X. H. Zhao, L. Baylor, S. Kaushal, E. Eisenberg, and L. E. Greene. 2001. Clathrin exchange during clathrin-mediated endocytosis. J. Cell Biol. 155:291-300.
54. Ehrlich, M., W. Boll, A. van Oijen, R. Hariharan, K. Chandran, M. L. Nibert, and T. Kirchhausen. 2004. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell. 118:591-605.
55. Merrifield, C. J. 2004. Seeing is believing: imaging actin dynamics at single sites of endocytosis. Trends Cell Biol. 14:352-358.
56. Wakeham, D. E., C.-Y. Chen, B. Greene, P. K. Hwang, and F. M. Brodsky. 2003. Clathrin self-assembly involves coordinated weak interactions favorable for cellular regulation. EMBO J. 22:4980-4990.
57. Huster, D., A. J. Jin, K. Arnold, and K. Gawrisch. 1997. Water permeability of polyunsaturated lipid membranes measured by O-17 NMR. Biophys. J. 73:855-864.
58. Alfsen, A., C. Paillerets, K. Prasad, P. K. Nandi, R. E. Lippoldt, and H. Edelhoch. 1984. Organization and dynamics of lipids in bovine brain coated and uncoated vesicles. Eur. Biophys. J. 11:129-136.
59. de Paillerets, C., M. Bomsel, H. Weintraub, D. Pepin, and A. Alfsen. 1987. Clustering in coated vesicles of polyunsaturated phospholipids segregated from plasma and Golgi membranes of adrenocortical cells. FEBS Lett. 219:113-118.
60. Olbrich, K., W. Rawicz, D. Needham, and E. Evans. 2000. Water permeability and mechanical strength of polyunsaturated lipid bilayers. Biophys. J. 79:321-327.
61. Jin, A. J., D. Huster, K. Gawrisch, and R. Nossal. 1999. Light scattering characterization of extruded lipid vesicles. Eur. Biophys. J. Biophys. Lett. 28:187-199.
62. Parsegian, V. A., and E. A. Evans. 1996. Long and short range intermolecular and intercolloidal forces. Curr. Opin. Colloid Interface Sci. 1:53-60.
63. Baumann, C. G., S. B. Smith, V. A. Bloomfield, and C. Bustamante. 1997. Ionic effects on the elasticity of single DNA molecules. Proc. Natl. Acad. Sci. USA. 94:6185-6190.