Physical determinants of β-barrel membrane protein folding in lipid vesicles

Biophysical Journal

Volumn 100, Issue 9, 2011, Pages 2131-2140

  Dewald, Alison H ^a   Hodges, Jacqueline C ^a   Columbus, Linda ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEISSERIA;

EID: 79959717411     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.03.025     Document Type: Article

References (45)

1. Booth, P. J., and A. R. Curran. 1999. Membrane protein folding. Curr. Opin. Struct. Biol. 9:115-121. (Pubitemid 29471983)
2. Cramer, W. A., D. M. Engelman,..., D. C. Rees. 1992. Forces involved in the assembly and stabilization of membrane proteins. FASEB J. 6:3397-3402. (Pubitemid 23007105)
3. Mackenzie, K. R. 2006. Folding and stability of alpha-helical integral membrane proteins. Chem. Rev. 106:1931-1977.
4. Kleinschmidt, J. H. 2003. Membrane protein folding on the example of outer membrane protein A of Escherichia coli. Cell. Mol. Life Sci. 60:1547-1558. (Pubitemid 37041354)
5. Kleinschmidt, J. H. 2006. Folding kinetics of the outer membrane proteins OmpA and FomA into phospholipid bilayers. Chem. Phys. Lipids. 141:30-47. (Pubitemid 43744430)
6. Tamm, L. K., H. Hong, and B. Liang. 2004. Folding and assembly of β-barrel membrane proteins. Biochim. Biophys. Acta. 1666:250-263. (Pubitemid 39425208)
7. Patel, G. J., S. Behrens-Kneip,..., J. H. Kleinschmidt. 2009. The periplasmic chaperone Skp facilitates targeting, insertion, and folding of OmpA into lipid membranes with a negative membrane surface potential. Biochemistry. 48:10235-10245.
8. Pocanschi, C. L., G. J. Patel,..., J. H. Kleinschmidt. 2006. Curvature elasticity and refolding of OmpA in large unilamellar vesicles. Biophys. J. 91:L75-L77. (Pubitemid 44526463)
9. Surrey, T., and F. Jähnig. 1992. Refolding and oriented insertion of a membrane protein into a lipid bilayer. Proc. Natl. Acad. Sci. USA. 89:7457-7461.
10. Surrey, T., and F. Jähnig. 1995. Kinetics of folding and membrane insertion of a β-barrel membrane protein. J. Biol. Chem. 270:28199-28203.
11. Kleinschmidt, J. H., and L. K. Tamm. 1996. Folding intermediates of a β-barrel membrane protein. Kinetic evidence for a multi-step membrane insertion mechanism.Biochemistry. 35:12993-13000. (Pubitemid 26349447)
12. Kleinschmidt, J. H., and L. K. Tamm. 2002. Secondary and tertiary structure formation of the β-barrel membrane protein OmpA is synchronized and depends on membrane thickness. J. Mol. Biol. 324:319-330. (Pubitemid 35379031)
13. Hong, H., N. H. Joh,..., L. K. Tamm. 2009. Methods for measuring the thermodynamic stability of membrane proteins. Methods Enzymol. 455:213-236.
14. Hong, H., S. Park,..., L. K. Tamm. 2007. Role of aromatic side chains in the folding and thermodynamic stability of integral membrane proteins. J. Am. Chem. Soc. 129:8320-8327. (Pubitemid 47035142)
15. Hong, H., and L. K. Tamm. 2004. Elastic coupling of integral membrane protein stability to lipid bilayer forces. Proc. Natl. Acad. Sci. USA. 101:4065-4070. (Pubitemid 38405884)
16. Stanley, A. M., and K. G. Fleming. 2008. The process of folding proteins into membranes: challenges and progress. Arch. Biochem. Biophys. 469:46-66. (Pubitemid 350212853)
17. Surrey, T., A. Schmid, and F. Jähnig. 1996. Folding and membrane insertion of the trimeric β-barrel protein OmpF. Biochemistry. 35:2283-2288. (Pubitemid 26071660)
18. Mahalakshmi, R., C. M. Franzin,..., F. M. Marassi. 2007. NMR structural studies of the bacterial outer membrane protein OmpX in oriented lipid bilayer membranes. Biochim. Biophys. Acta. 1768:3216-3224. (Pubitemid 350236082)
19. Shanmugavadivu, B., H.-J. Apell,..., J. H. Kleinschmidt. 2007. Correct folding of the β-barrel of the human membrane protein VDAC requires a lipid bilayer. J. Mol. Biol. 368:66-78. (Pubitemid 46441214)
20. Pocanschi, C. L., H.-J. Apell,..., J. H. Kleinschmidt. 2006. The major outer membrane protein of Fusobacterium nucleatum (FomA) folds and inserts into lipid bilayers via parallel folding pathways. J. Mol. Biol. 355:548-561. (Pubitemid 41785756)
21. Huysmans, G. H. M., S. E. Radford,..., S. A. Baldwin. 2007. The N-terminal helix is a post-assembly clamp in the bacterial outer membrane protein PagP. J. Mol. Biol. 373:529-540. (Pubitemid 47488393)
22. Burgess, N. K., T. P. Dao,..., K. G. Fleming. 2008. β-barrel proteins that reside in the Escherichia coli outer membrane in vivo demonstrate varied folding behavior in vitro. J. Biol. Chem. 283:26748-26758.
23. Kong, H. J., and D. J. Mooney. 2007. Microenvironmental regulation of biomacromolecular therapies. Nat. Rev. Drug Discov. 6:455-463. (Pubitemid 47064568)
24. Torchilin, V. P. 2005. Recent advances with liposomes as pharmaceutical carriers. Nat. Rev. Drug Discov. 4:145-160. (Pubitemid 40282557)
25. Kleinschmidt, J. H., T. den Blaauwen,..., L. K. Tamm. 1999. Outer membrane protein A of Escherichia coli inserts and folds into lipid bilayers by a concerted mechanism. Biochemistry. 38:5006-5016.
26. Kleinschmidt, J. H., and L. K. Tamm. 1999. Time-resolved distance determination by tryptophan fluorescence quenching: probing intermediates in membrane protein folding. Biochemistry. 38:4996-5005.
27. Ebie Tan, A., N. K. Burgess,..., K. G. Fleming. 2010. Self-association of unfolded outer membrane proteins. Macromol. Biosci. 10:763-767.
28. Rasband, W. Image J. 1997-2009. U. S. National Institutes of Health, Bethesda, Maryland. http://rsb.info.nih.gov/ij/.
29. Senff, L. M., W. S. Wegener,..., R. A. Makula. 1976. Phospholipid composition and phospholipase A activity of Neisseria gonorrhoeae. J. Bacteriol. 127:874-880.
30. 31P-NMR spectroscopy. Biophys. J. 83:994-1003. (Pubitemid 34803632)
31. Petrache, H. I., S. W. Dodd, and M. F. Brown. 2000. Area per lipid and acyl length distributions in fluid phosphatidylcholines determined by 2H NMR spectroscopy. Biophys. J. 79:3172-3192.
32. Dill, K. A., and P. J. Flory. 1980. Interphases of chain molecules: monolayers and lipid bilayer membranes. Proc. Natl. Acad. Sci. USA. 77:3115-3119.
33. Alves, M., and M. Peric. 2006. An EPR study of the interfacial properties of phosphatidylcholine vesicles with different lipid chain lengths. Biophys. Chem. 122:66-73. (Pubitemid 44177502)
34. Grit, M., and D. J. Crommelin. 1993. Chemical stability of liposomes: implications for their physical stability. Chem. Phys. Lipids. 64:3-18. (Pubitemid 23290861)
35. Ho, R. J. Y., M. Schmetz, and D. W. Deamer. 1987. Nonenzymatic hydrolysis of phosphatidylcholine prepared as liposomes and mixed micelles. Lipids. 22:156-158.
36. Cafiso, D. S. 1995. Influence of charges and dipoles on macromolecular adsorption and permeability. In Permeability and Stability of Lipid Bilayers. E. A. Disalvo and S. A. Simon, editors. CRC Press, Boca Raton, FL. 179-195.
37. Yang, Y., K. M. Mayer,..., J. H. Hafner. 2008. Probing the lipid membrane dipole potential by atomic force microscopy. Biophys. J. 95:5193-5199.
38. Brockman, H. 1994. Dipole potential of lipid membranes. Chem. Phys. Lipids. 73:57-79. (Pubitemid 24299188)
39. Clarke, R. J. 2001. The dipole potential of phospholipid membranes and methods for its detection. Adv. Colloid Interface Sci. 89-90:263-281. (Pubitemid 32092488)
40. Murray, D., and B. Honig. 2002. Electrostatic control of the membrane targeting of C2 domains. Mol. Cell. 9:145-154. (Pubitemid 34127778)
41. Tendian, S. W., and B. R. Lentz. 1990. Evaluation of membrane phase behavior as a tool to detect extrinsic protein-induced domain formation: binding of prothrombin to phosphatidylserine/phosphatidylcholine vesicles. Biochemistry. 29:6720-6729. (Pubitemid 20223569)
42. Seelig, A., and J. Seelig. 1977. Effect of a single cis double bond on the structures of a phospholipid bilayer. Biochemistry. 16:45-50. (Pubitemid 8030063)
43. Silvius, J. R. 1982. Thermotropic Phase Transitions of Pure Lipids in Model Membranes and Their Modifications by Membrane Proteins. John Wiley & Sons, New York.
44. Clarke, R. J. 1997. Effect of lipid structure on the dipole potential of phosphatidylcholine bilayers. Biochim. Biophys. Acta. 1327:269-278. (Pubitemid 27300144)
45. Lakowicz, J. R. 2006. Protein fluorescence. In Principles of Fluorescence Spectroscopy.. Springer, New York. 530-573.