Outer membrane β-barrel protein folding is physically controlled by periplasmic lipid head groups and BamA

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 16, 2014, Pages 5878-5883

  Gessmann, Dennis ^a   Chung, Yong Hee ^a   Danoff, Emily J ^a   Plummer, Ashlee M ^a   Sandlin, Clifford W ^a   Zaccai, Nathan R ^a   Fleming, Karen G ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Beta barrel transmembrane protein; Membrane protein folding

Indexed keywords

GLYCEROPHOSPHOLIPID; OUTER MEMBRANE PROTEIN; PERIPLASMIC PROTEIN; PHOSPHOETHANOLAMINE;

ALPHA CHAIN; ARTICLE; BACTERIAL MEMBRANE; BETA BARREL MACHINERY SUBUNIT A; CONTROLLED STUDY; ESCHERICHIA COLI; EUKARYOTE; GENE PRODUCT; IN VITRO STUDY; LIPID COMPOSITION; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN FOLDING; PROTON MOTIVE FORCE;

BETA-BARREL TRANSMEMBRANE PROTEIN; MEMBRANE PROTEIN FOLDING;

BACTERIAL OUTER MEMBRANE PROTEINS; BIOCATALYSIS; CELL MEMBRANE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; KINETICS; LIPIDS; MODELS, BIOLOGICAL; PERIPLASM; PHENYLALANINE; PHOSPHATIDYLETHANOLAMINES; PHOSPHATIDYLGLYCEROLS; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY;

EID: 84899126341     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1322473111     Document Type: Article

References (49)

1. Tamm LK, Hong H, Liang B (2004) Folding and assembly of beta-barrel membrane proteins. Biochim Biophys Acta 1666(1-2):250-263. (Pubitemid 39425208)
2. Wimley WC (2003) The versatile beta-barrel membrane protein. Curr Opin Struct Biol 13(4):404-411.
3. Nikaido H (1989) Outer membrane barrier as a mechanism of antimicrobial resistance. Antimicrob Agents Chemother 33(11):1831-1836.
4. Bajaj H, et al. (2012) Antibiotic uptake through membrane channels: Role of Providencia stuartii OmpPst1 porin in carbapenem resistance. Biochemistry 51(51): 10244-10249.
5. Manczak M, Reddy PH (2012) Abnormal interaction of VDAC1 with amyloid beta and phosphorylated tau causes mitochondrial dysfunction in Alzheimer's disease. Hum Mol Genet 21(23):5131-5146.
6. Sasaki K, et al. (2012) VDAC: Old protein with new roles in diabetes. Am J Physiol Cell Physiol 303(10):C1055-C1060.
7. Bender A, et al. (2013) TOM40 mediates mitochondrial dysfunction induced by α-synuclein accumulation in Parkinson' s disease. PLoS ONE 8(4):e62277.
8. Voulhoux R, Bos MP, Geurtsen J, Mols M, Tommassen J (2003) Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299(5604): 262-265. (Pubitemid 36125214)
9. Wu T, et al. (2005) Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121(2):235-245. (Pubitemid 40546391)
10. Kim S, et al. (2007) Structure and function of an essential component of the outer membrane protein assembly machine. Science 317(5840):961-964. (Pubitemid 47301326)
11. Gatzeva-Topalova PZ, Walton TA, Sousa MC (2008) Crystal structure of YaeT: Conformational flexibility and substrate recognition. Structure 16(12):1873-1881.
12. Knowles TJ, et al. (2008) Fold and function of polypeptide transport-associated domains responsible for delivering unfolded proteins to membranes. Mol Microbiol 68(5):1216-1227. (Pubitemid 351670197)
13. Kleinschmidt JH, den Blaauwen T, Driessen AJ, Tamm LK (1999) Outer membrane protein A of Escherichia coli inserts and folds into lipid bilayers by a concerted mechanism. Biochemistry 38(16):5006-5016.
14. Huysmans GH, Radford SE, Brockwell DJ, Baldwin SA (2007) The N-terminal helix is a post-assembly clamp in the bacterial outer membrane protein PagP. J Mol Biol 373(3):529-540. (Pubitemid 47488393)
15. Burgess NK, Dao TP, Stanley AM, Fleming KG (2008) Beta-barrel proteins that reside in the Escherichia coli outer membrane in vivo demonstrate varied folding behavior in vitro. J Biol Chem 283(39):26748-26758.
16. Stanley AM, Fleming KG (2008) The process of folding proteins into membranes: Challenges and progress. Arch Biochem Biophys 469(1):46-66. (Pubitemid 350212853)
17. Moon CP, Fleming KG (2011) Side-chain hydrophobicity scale derived from transmembrane protein folding into lipid bilayers. Proc Natl Acad Sci USA 108(25): 10174-10177.
18. Rigel NW, Ricci DP, Silhavy TJ (2013) Conformation-specific labeling of BamA and suppressor analysis suggest a cyclic mechanism for β-barrel assembly in Escherichia coli. Proc Natl Acad Sci USA 110(13):5151-5156.
19. Hagan CL, Kahne D (2011) The reconstituted Escherichia coli Bam complex catalyzes multiple rounds of β-barrel assembly. Biochemistry 50(35):7444-7446.
20. Zeth K, Thein M (2010) Porins in prokaryotes and eukaryotes: Common themes and variations. Biochem J 431(1):13-22.
21. White DA, Lennarz WJ, Schnaitman CA (1972) Distribution of lipids in the wall and cytoplasmic membrane subfractions of the cell envelope of Escherichia coli. J Bacteriol 109(2):686-690.
22. Lugtenberg EJ, Peters R (1976) Distribution of lipids in cytoplasmic and outer membranes of Escherichia coli K12. Biochim Biophys Acta 441(1):38-47.
23. Danoff EJ, Fleming KG (2011) The soluble, periplasmic domain of OmpA folds as an independent unit and displays chaperone activity by reducing the self-association propensity of the unfolded OmpA transmembrane β-barrel. Biophys Chem 159(1): 194-204.
24. Patel GJ, Kleinschmidt JH (2013) The lipid bilayer-inserted membrane protein BamA of Escherichia coli facilitates insertion and folding of outer membrane protein A from its complex with Skp. Biochemistry 52(23):3974-3986.
25. Patel GJ, Behrens-Kneip S, Holst O, Kleinschmidt JH (2009) The periplasmic chaperone Skp facilitates targeting, insertion, and folding of OmpA into lipid membranes with a negative membrane surface potential. Biochemistry 48(43):10235-10245.
26. Kleinschmidt JH, Tamm LK (2002) Secondary and tertiary structure formation of the beta-barrel membrane protein OmpA is synchronized and depends on membrane thickness. J Mol Biol 324(2):319-330. (Pubitemid 35379031)
27. Ebie Tan A, Burgess NK, DeAndrade DS, Marold JD, Fleming KG (2010) Self-association of unfolded outer membrane proteins. Macromol Biosci 10(7):763-767.
28. Huysmans GH, Radford SE, Baldwin SA, Brockwell DJ (2012) Malleability of the folding mechanism of the outer membrane protein PagP: Parallel pathways and the effect of membrane elasticity. J Mol Biol 416(3):453-464.
29. Tommassen J (2010) Assembly of outer-membrane proteins in bacteria and mitochondria. Microbiology 156(Pt 9):2587-2596.
30. de Cock H, Struyvé M, Kleerebezem M, van der Krift T, Tommassen J (1997) Role of the carboxy-terminal phenylalanine in the biogenesis of outer membrane protein PhoE of Escherichia coli K-12. J Mol Biol 269(4):473-478. (Pubitemid 27267861)
31. Struyvé M, Moons M, Tommassen J (1991) Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol 218(1): 141-148. (Pubitemid 121003335)
32. Noinaj N, et al. (2013) Structural insight into the biogenesis of β-barrel membrane proteins. Nature 501(7467):385-390.
33. Harwood JL, Russell NJ (1984) Lipids in Plants and Microbes (George Allen & Unwin, London).
34. Cowan SW, et al. (1992) Crystal structures explain functional properties of two E. coli porins. Nature 358(6389):727-733.
35. Wu S, et al. (2011) Interaction between bacterial outer membrane proteins and periplasmic quality control factors: A kinetic partitioning mechanism. Biochem J 438(3):505-511.
36. Gentle I, Gabriel K, Beech P, Waller R, Lithgow T (2004) The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J Cell Biol 164(1):19-24. (Pubitemid 38082453)
37. Boggs JM (1987) Lipid intermolecular hydrogen bonding: Influence on structural organization and membrane function. Biochim Biophys Acta 906(3):353-404.
38. Zhang YP, Lewis RN, McElhaney RN (1997) Calorimetric and spectroscopic studies of the thermotropic phase behavior of the n-saturated 1,2-diacylphosphatidylglycerols. Biophys J 72(2 Pt 1):779-793. (Pubitemid 27044883)
39. Murzyn K, Róg T, Pasenkiewicz-Gierula M (2005) Phosphatidylethanolamine-phosphatidylglycerol bilayer as a model of the inner bacterial membrane. Biophys J 88(2): 1091-1103. (Pubitemid 40975941)
40. Ruiz N, Kahne D, Silhavy TJ (2006) Advances in understanding bacterial outer-membrane biogenesis. Nat Rev Microbiol 4(1):57-66. (Pubitemid 43135287)
41. Robert V, et al. (2006) Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif. PLoS Biol 4(11):e377.
42. Kutik S, et al. (2008) Dissecting membrane insertion of mitochondrial beta-barrel proteins. Cell 132(6):1011-1024. (Pubitemid 351381741)
43. Qiu J, et al. (2013) Coupling of mitochondrial import and export translocases by receptor-mediated supercomplex formation. Cell 154(3):596-608.
44. Walther DM, Papic D, Bos MP, Tommassen J, Rapaport D (2009) Signals in bacterial beta-barrel proteins are functional in eukaryotic cells for targeting to and assembly in mitochondria. Proc Natl Acad Sci USA 106(8):2531-2536.
45. Walther DM, Bos MP, Rapaport D, Tommassen J (2010) The mitochondrial porin, VDAC, has retained the ability to be assembled in the bacterial outer membrane. Mol Biol Evol 27(4):887-895.
46. Berrow NS, et al. (2007) A versatile ligation-independent cloning method suitable for high-throughput expression screening applications. Nucleic Acids Res 35(6):e45.
47. Raetz CR, et al. (2006) Kdo2-Lipid A of Escherichia coli, a defined endotoxin that activates macrophages via TLR-4. J Lipid Res 47(5):1097-1111. (Pubitemid 43764706)
48. Nölting B (2006) Protein Folding Kinetics, Biophysical Methods (Springer, Berlin), 2nd Ed.
49. Moon CP, Zaccai NR, Fleming PJ, Gessmann D, Fleming KG (2013) Membrane protein thermodynamic stability may serve as the energy sink for sorting in the periplasm. Proc Natl Acad Sci USA 110(11):4285-4290.