Hierarchical self-assembly of F-actin and cationic lipid complexes: Stacked three-layer tubule networks

Science

Volumn 288, Issue 5473, 2000, Pages 2035-2039

  Wong, Gerard C L ^a   Tang, Jay X ^a   Lin, Alison ^a   Li, Youli ^a   Janmey, Paul A ^a   Safinya, Cyrus R ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; DNA; POLYELECTROLYTE;

ARTICLE; BACTERIAL CELL WALL; CONFOCAL MICROSCOPY; LIPID BILAYER; LIPID COMPOSITION; LIPID MEMBRANE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; STRUCTURE ANALYSIS; X RAY DIFFRACTION;

ACTINS; ANISOTROPY; CATIONS; CRYSTALLIZATION; ELECTROCHEMISTRY; ELECTROLYTES; FATTY ACIDS, MONOUNSATURATED; FREEZE FRACTURING; LIPID BILAYERS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MOLECULAR CONFORMATION; PROTEIN CONFORMATION; QUATERNARY AMMONIUM COMPOUNDS; X-RAY DIFFRACTION;

BACTERIA (MICROORGANISMS);

EID: 0034674445     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.288.5473.2035     Document Type: Article

References (48)

1. W. M. Gelbart, A. Ben-Shaul, D. Roux, Eds., Micelles, Membranes, Microemulsions, and Monolayers (Springer-Verlag, New York, 1994).
2. S. A. Safran, Statistical Thermodynamics of Surfaces, Interfaces, and Membranes (Addison-Wesley, Reading, MA, 1994).
3. R. Lipowsky and E. Sackmann, Eds., Structure and Dynamics of Membranes (Elsevier Science, New York, 1995).
4. W. Helfrich, Z. Naturforsch. C 28, 693 (1973).
5. J. M. Schnur, Science 262, 1669 (1993).
6. M. S. Spector, R. R. Price, J. M. Schnur, Adv. Mater. 11, 337 (1999).
7. R. Oda, I. Hue, M. Schmutz, S. J. Candau, F. C. MacKintosh, Nature 399, 566 (1999).
8. B. N. Thomas, C. R. Safinya, R. J. Plano, N. A. Clark, Science 267, 1635 (1995).
9. B. N. Thomas et al., J. Am. Chem. Soc. 120, 12178 (1998).
10. B. N. Thomas, C. M. Lindemann, N. A. Clark, Phys. Rev. E 59, 3040 (1999).
11. S. Chiruvolu et al., Science 266, 1222 (1994).
12. B. Klosgen and W. Helfrich, Eur. Biophys. J. 22, 340 (1993).
13. D. Papahadjopoulos et al., Biochim. Biophys. Acta 394, 483 (1975).
14. D. D. Lasic, Liposomes in Gene Delivery (CRC Press, Boca Raton, FL, 1997).
15. J. O. Rädler, I. Koltover, T. Salditt, C. R. Safinya, Science 275, 810 (1997).
16. I. Koltover, T. Salditt, J. O. Rädler, C. R. Safinya, Science 281, 78 (1998).
17. R. Bruinsma, Eur. Phys. J. B 4, 75 (1998).
18. D. Harries, S. May, W. Gelbart, A. Ben Shaul, Biophys. J. 75, 159 (1998).
19. 2, above and below the DNA rod in the lamellar complex and permits near complete neutralization. F-actin has a charge density that is at least four times less than that of DNA.
20. W. Häckl, M. Bärmann, E. Sackmann, Phys. Rev. Lett. 80, 1786 (1998).
21. H. Miyata, S. Nishiyama, K.-I. Akashi, K. Kinosita, Proc. Natl. Acad. Sci. U.S.A. 96, 2048 (1999).
22. H. Lodish et al., Molecular Cell Biology (Freeman, New York, ed. 4, 1999).
23. 2, and 25 mM tris at pH 7.4 was used to regulate the mean F-actin length in length-dependence studies.
24. 1 (HWHM). The actin-membrane complex samples are sealed in 1.5-mm quartz capillaries.
25. A. Laliberte and C. Gicquaud, J. Cell Biol. 106, 1221 (1988).
26. A. Renault et al., Biophys. J. 76, 1580 (1999).
27. If we restrict the F-actin filaments to an average length of 500 Å with gelsolin, an actin severing and capping protein, then the superlattice ordering is suppressed in the resultant actin-membrane complexes.
28. A. E. Blaurock, J. Mol. Biol. 56, 35 (1971).
29. N. P. Franks, T. Arunachalam, E. Caspi, Nature 276, 530 (1978).
30. Although the F-actin cationic lipid complexes always show the superlattice peaks resulting from stacked three-layer membranes, the XRD from G-actin complexes show only hints of the superlattice ordering. This may be due to the coexistence of two-layer G-actin complexes (with alternating lipid bilayer and G-actin monolayers) with a very small fraction of the G-actin that has polymerized into very long F-actin, forming the three-layer membrane. Because G-actin (or very short F-actin) does not contain any condensed counterion because of its globular shape (or extreme finite size for short F-actin), G-actin attached to cationic membrane releases only the bound counterions of the membrane. In the process, G-actin lowers its own entropy (which is negligible for long F-actin) and reduces some of the entropy of the lipids [by their ordering on its surface as suggested by the EM freeze-fracture and molecular dynamics simulations studies (31)]. Thus, there is a delicate balance between how much entropy is gained each time G-actin attaches a membrane and releases anionic lipid counterions and the entropy lost because of the lipid ordering on the G-actin surface. In the case of long F-actin, the situation is very different because an additional large amount of bound cationic counterions is also released upon complexation. Thus, for G-actin complexes, a two-layer membrane may be entropically more favorable than a three-layer membrane. Alternatively, G-actin complexes composed of three-layer membranes with antiphase-type defects would tend to wash out the superlattice peaks.
31. S. Bandyopadhyay, M. Tarek, M. L. Klein, J. Phys. Chem. B 103, 10075 (1999).
32. C. S. O'Hern, T. C. Lubensky, J. Toner, Phys. Rev. Lett. 83, 2745 (1999).
33. M. Sara and U. B. Sleytr, Prog. Biophys. Mol. Biol. 65, 83 (1996).
34. J. X. Tang and P. A. Janmey, J. Biol. Chem. 271, 8556 (1996).
35. J. Hanson, Proc. R. Soc. London Ser. B 183, 39 (1973).
36. L. Rioux and D. Gicquaud, J. Ultrastruct. Res. 93, 42 (1985).
37. K. A. Taylor and D. W. Taylor, J. Struct. Biol. 108, 140 (1992).
38. N. Dan, Biophys. J. 71, 1267 (1996).
39. D. R. Nelson, T. Piran, S. Weinberg, Eds., Statistical Mechanics of Membranes and Interfaces (World Scientific, Singapore, 1989).
40. Y. Kantor and D. R. Nelson, Phys. Rev. Lett. 57, 791 (1986).
41. F. F. Abraham and D. R. Nelson, Science 249, 393 (1990).
42. J. A. Aronovitz and T. C. Lubensky, Phys. Rev. Lett. 60, 2634 (1988).
43. C. F. Schmidt et al., Science 259, 952 (1993).
44. L. Radzihovsky and J. Toner, Phys. Rev. Lett. 75, 4752 (1995).
45. M. Bowick, M. Falcioni, G. Thorleifsson, Phys. Rev. Lett. 79, 885 (1997).
46. M. Bowick and A. Travesset, Phys. Rev. E 59, 5659 (1998).
47. B. M. Discher et al., Science 284, 1143 (1999).
48. We thank R. Golestanian, I. Koltover, R. Menes, P. Pincus, and D. Roux for discussions. In particular, we acknowledge L. Zarif for discussions on the EM work. This work was supported by NIH grants GM59288 and AR38910, NSF grant DMR-9972246, the Cystic Fibrosis Foundation (grant 00G0), and the University of California Biotechnology Research and Education Program (grant 99-14). The Materials Research Laboratory at University of California at Santa Barbara is supported by NSF grants DMR-9632716 and DMR-0080034.