Weakly stable regions and protein-protein interactions in beta-barrel membrane proteins

Current Pharmaceutical Design

Volumn 20, Issue 8, 2014, Pages 1268-1273

  Naveed, Hammad ^a   Liang, Jie ^a  

^a University of Illinois at Chicago   (United States)

Author keywords

OmpF; Protein protein interaction; Tom40; VDAC; Weakly stable regions; barrel membrane proteins

Indexed keywords

BETA BARREL MEMBRANE PROTEIN; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; OUTER MEMBRANE PROTEIN F; PROTEIN TOM40; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL;

AMINO ACID SEQUENCE; ARTICLE; CELLULAR DISTRIBUTION; HYDROGEN BOND; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; BINDING SITE; BIOLOGY; BIOPHYSICS; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; PROCEDURES; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

BINDING SITES; BIOPHYSICS; COMPUTATIONAL BIOLOGY; HUMANS; MEMBRANE PROTEINS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY;

EID: 84903577060     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/13816128113199990071     Document Type: Article

References (72)

1. Wallin E, von Heijne G. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci 1998; 7(4): 1029-38.
2. Arkin IT, Brunger AT. Statistical analysis of predicted transmembrane alpha-helices. Biochim Biophys Acta 1998; 1429(1): 113-28.
3. Cho W, Stahelin RV. Membrane-protein interactions in cell signaling and membrane trafficking. Annu Rev Biophys Biomol Struct 2005; 34: 119-51.
4. DeFelice LJ. Transporter structure and mechanism. Trends Neurosci 2004; 27(6): 352-9.
5. Delcour AH. Structure and function of pore-forming beta-barrels from bacteria. J Mol Microbiol Biotechnol 2002; 4(1): 1-10.
6. Bishop RE. Structural biology of membrane-intrinsic beta-barrel enzymes: sentinels of the bacterial outer membrane. Biochim Biophys Acta 2008; 1778(9): 1881-96.
7. Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, Gouaux JE. Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 1996; 274(5294): 1859-66.
8. Shoshan-Barmatz V, De Pinto V, Zweckstetter M, Raviv Z, Keinan N, Arbel N. VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med 2010; 31(3): 227-85.
9. Shoshan-Barmatz V, Israelson A, Brdiczka D, Sheu SS. The voltage-dependent anion channel (VDAC): function in intracellular signalling, cell life and cell death. Curr Pharm Des 2006; 12(18): 2249-70.
10. Lemasters JJ, Holmuhamedov E. Voltage-dependent anion channel (VDAC) as mitochondrial governator-thinking outside the box. Biochim Biophys Acta 2006; 1762(2): 181-90.
11. Schulz GE. The structure of bacterial outer membrane proteins. Biochim Biophys Acta 2002; 1565: 308-17.
12. Bagos PG, Liakopoulos TD, Spyropoulos IC, Hamodrakas SJ. PRED-TMBB: a web server for predicting the topology of betabarrel outer membrane proteins. Nucleic Acids Res 2004; 32(Web Server issue): W400-4.
13. Bagos PG, Liakopoulos T.D, Hamodrakas SJ. Evaluation of methods for predicting the topology of beta-barrel outer membrane proteins and a consensus prediction method. BMC Bioinformatics 2005; 6: 7.
14. A. Randall Cheng J, Sweredoski M, Baldi P. TMBpro: secondary structure, beta-contact and tertiary structure prediction of transmembrane beta-barrel proteins. Bioinformatics 2008; 24(4): 513-20.
15. Singh NK, Goodman A, Walter P, Helms V, Hayat S. TMBHMM: a frequency profile based HMM for predicting the topology of transmembrane beta barrel proteins and the exposure status of transmembrane residues. Biochim Biophys Acta 2011; 1814(5): 664-70.
16. Wimley WC. Toward genomic identification of beta-barrel membrane proteins: composition and architecture of known structures. Protein Sci 2002; 11(2): 301-12.
17. Freeman TC Jr., Wimley WC. A highly accurate statistical approach for the prediction of transmembrane beta-barrels. Bioinformatics 2010; 26(16): 1965-74.
18. Jackups R Jr., Liang J. Interstrand pairing patterns in beta-barrel membrane proteins: the positive-outside rule, aromatic rescue, and strand registration prediction. J Mol Biol 2005; 354(4): 979-93.
19. Jackups R, Jr., Cheng S, Liang J. Sequence motifs and antimotifs in beta-barrel membrane proteins from a genome-wide analysis: the ala-tyr dichotomy and chaperone binding motifs. J Mol Biol 2006; 363(2): 611-23.
20. Jackups R Jr., Liang J. Combinatorial analysis for sequence and spatial motif discovery in short sequence fragments. IEEE/ACM Trans Comput Biol Bioinform 2010; 7(3): 524-36
21. Jimenez-Morales D, Liang J. Pattern of amino acid substitutions in transmembrane domains of beta-barrel membrane proteins for detecting remote homologs in bacteria and mitochondria. PLoS One 2011; 6(11): e26400.
22. Liang J, Naveed H, Jimenez-Morales D, Adamian L, Lin M. Computational studies of membrane proteins: Models and predictions for biological understanding. Biochim Biophys Acta 2012; 1818(4): 927-41.
23. Moon CP, Fleming KG. Side-chain hydrophobicity scale derived from transmembrane protein folding into lipid bilayers. Proc Natl Acad Sci USA 2011; 108(25): 10174-7.
24. Fleming PJ, Freites JA, Moon CP, Tobias DJ, Fleming KG. Outer membrane phospholipase a in phospholipid bilayers: A model system for concerted computational and experimental investigations of amino acid side chain partitioning into lipid bilayers. Biochim Biophys Acta 2012; 1818(2): 126-34.
25. Ulmschneider JP, Smith JC, White SH, Ulmschneider MB. In silico partitioning and transmembrane insertion of hydrophobic peptides under equilibrium conditions. J Am Chem Soc 2011; 133(39): 15487-95.
26. Gumbart J, Roux B. Determination of membrane-insertion free energies by molecular dynamics simulations. Biophys J 2012; 102(4): 795-801.
27. Hsieh D, Davis A, Nanda V. A knowledge-based potential highlights unique features of membrane alpha-helical and beta-barrel protein insertion and folding. Protein Sci 2012; 21(1): 50-62.
28. Heniko S, Heniko GJ. Amino acid substitution matrices. Adv Protein Chem, 2000; 54: 73-97.
29. Waldispuhl J, Berger B, Clote P, Steyaert JM. transfold: a web server for predicting the structure and residue contacts of transmembrane beta-barrels. Nucleic Acids Res 2006; 34(Web Server issue): W189-93.
30. Ujwal R, Cascio D, Colletier JP, et al. The crystal structure of mouse VDAC1 at 2.3 a resolution reveals mechanistic insights into metabolite gating. Proc Natl Acad Sci USA 2008; 105(46): 17742-7.
31. Remaut H, Tang C, Henderson NS, et al. Fiber formation across the bacterial outer membrane by the chaperone/usher pathway. Cell 2008; 133(4): 640-52.
32. Naveed H, Xu Y, Jackups R, Jr., Liang J. Predicting threedimensional structures of transmembrane domains of beta-barrel membrane proteins. J Am Chem Soc 2012; 134(3): 1775-81.
33. Bayley H, Cremer PS. Stochastic sensors inspired by biology. Nature 2001; 413(6852): 226-30.
34. Seitz T, Bocola M, Claren J, Sterner R. Stabilisation of a (betaalpha) 8-barrel protein designed from identical half barrels. J Mol Biol 2007; 372(1): 114-29.
35. Seitz T, Thoma R, Schoch GA, et al. Enhancing the stability and solubility of the glucocorticoid receptor ligand-binding domain by high-throughput library screening. J Mol Biol 2010; 403(4): 562-77.
36. Haltia T, Freire E. Forces and factors that contribute to the structural stability of membrane proteins. Biochim Biophys Acta 1995; 1241(2): 295-322.
37. Stanley AM, Fleming KG. The role of a hydrogen bonding network in the transmembrane beta-barrel OMPLA. J Mol Biol 2007; 370(5): 912-24.
38. Naveed H, Jackups R, Jr., Liang J. Predicting weakly stable regions, oligomerization state, and protein-protein interfaces in transmembrane domains of outer membrane proteins. Proc Natl Acad Sci USA 2009; 106(31): 12735-40.
39. Adamian L, Naveed H, Liang J. Lipid-binding surfaces of membrane proteins: evidence from evolutionary and structural analysis. Biochim Biophys Acta 2011; 1808(4): 1092-102.
40. Phale PS, Philippsen A, Kiefhaber T, et al. Stability of trimeric ompf porin: the contributions of the latching loop l2. Biochemistry 1998; 37(45): 15663-70.
41. Evanics F, Hwang PM, Cheng Y, Kay LE, Prosser RS. Topology of an outer-membrane enzyme: Measuring oxygen and water contacts in solution NMR studies of pagp. J Am Chem Soc 2006; 128(25): 8256-64.
42. Ferguson AD, Hofmann E, Coulton JW, Diederichs K, Welte W. Siderophore-mediated iron transport: crystal structure of fhua with bound lipopolysaccharide. Science 1998; 282(5397): 2215-20.
43. Van Gelder P, Saint N, Phale P, et al. Voltage sensing in the phoe and ompf outer membrane porins of escherichia coli: role of charged residues. J Mol Biol 1997; 269(4): 468-72.
44. Lehnert U, Xia Y, Royce TE, et al. Computational analysis of membrane proteins: genomic occurrence, structure prediction and helix interactions. Q Rev Biophys 2004; 37(2): 121-46.
45. Liu Y, Gerstein M, Engelman DM. Transmembrane protein domains rarely use covalent domain recom-bination as an evolutionary mechanism. Proc Natl Acad Sci USA 2004; 101(10): 3495-7.
46. Bordner AJ. Predicting protein-protein binding sites in membrane proteins. BMC Bioinformatics 2009; 10: 312.
47. Cowan SW, Schirmer T, Rummel G, et al. Crystal structures explain functional properties of two e. coli porins. Nature 1992; 358(6389): 727-33.
48. Naveed H, Jimenez-Morales D, Tian J, Pasupuleti V, Kenney LJ, Liang J. Engineered oligomerization state of ompf protein through computational design decouples oligomer dissociation from unfolding. J Mol Biol Mar 2012.
49. Surrey T, Schmid A, Jahnig F. Folding and membrane insertion of the trimeric beta-barrel protein ompf. Biochemistry 1996; 35(7): 2283-8.
50. de Cock H, Hendriks R, de Vrije T, Tommassen J. Assembly of an in vitro synthesized escherichia coli outer membrane porin into its stable trimeric configuration. J Biol Chem 1990; 265(8): 4646-51.
51. Van Gelder P, Tommassen J. Demonstration of a folded monomeric form of porin phoe of escherichia coli in vivo. J Bacteriol 1996; 178(17): 5320-2.
52. Visudtiphole V, Thomas MB, Chalton DA, Lakey JH. Refolding of escherichia coli outer membrane protein f in detergent creates LPSfree trimers and asymmetric dimers. Biochem J 2005; 392(Pt 2): 375-81.
53. Reid J, Fung H, Gehring K, Klebba P.E, Nikaido H. Targeting of porin to the outer membrane of escherichia coli. rate of trimer assembly and identification of a dimer intermediate. J Biol Chem 1988; 263(16): 7753-9.
54. Watanabe Y. Efect of various mild surfactants on the reassembly of an oligomeric integral membrane protein ompf porin. J Protein Chem 2002; 21(3): 169-75.
55. Colombini M. VDAC: the channel at the interface between mitochondria and the cytosol. Mol Cell Biochem 2004; 256-7(1-2): 107-15.
56. Zalk R, Israelson A, Garty ES, Azoulay-Zohar H, Shoshan-Barmatz V. Oligomeric states of the voltage-dependent anion channel and cytochrome c release from mitochondria. Biochem J 2005; 386(Pt 1): 73-83.
57. Hoogenboom B.W, Suda K, Engel A, Fotiadis D. The supramolecular assemblies of voltage-dependent anion channels in the native membrane. J Mol Biol 2007; 370(2): 246-55.
58. Goncalves RP, Buzhynskyy N, Prima V, Sturgis JN, Scheuring S. Supramolecular assembly of VDAC in native mitochondrial outer membranes. J Mol Biol 2007; 369(2): 413-8.
59. Geula S, Naveed H, Liang J, Shoshan-Barmatz V. Structure-based analysis of VDAC1 protein: defining oligomer contact sites. J Biol Chem 2012; 287(3): 2179-90.
60. Keinan N, Tyomkin D, Shoshan-Barmatz V. Oligomerization of the mitochondrial protein voltage-dependent anion channel is coupled to the induction of apoptosis. Mol Cell Biol 2010; 30(24): 5698-709.
61. Shoshan-Barmatz V, Keinan N, Abu-Hamad S, Tyomkin D, Aram L. Apoptosis is regulated by the VDAC1 n-terminal region and by VDAC oligomerization: release of cytochrome c, AIF and smac/diablo. Biochim Biophys Acta 2010; 1797(6-7): 1281-91.
62. Ahting U, Thieffry M, Engelhardt H, Hegerl R, Neupert W, Nussberger S. Tom40, the pore-forming com-ponent of the proteinconducting TOM channel in the outer membrane of mitochondria. J Cell Biol 2001; 153(6): 1151-60.
63. Hill K, Model K, Ryan M.T, et al. Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins [see comment]. Nature 1998; 395(6701): 516-21.
64. Kunkele KP, Heins S, Dembowski M, et al. The preprotein translocation channel of the outer membrane of mitochondria. Cell 1998; 93(6): 1009-19.
65. Zeth K. Structure and evolution of mitochondrial outer membrane proteins of beta-barrel topology. Biochim Biophys Acta 2010; 1797(6-7): 1292-9.
66. Werhahna W, Jnschb L, Braun H. Identification of novel subunits of the tom complex from arabidopsis thaliana. Plant Physiol Biochem 2003; 41(5): 407-16.
67. Gessmann D, Mager F, Naveed H, et al. Improving the resistance of a eukaryotic beta-barrel protein to thermal and chemical perturbations. J Mol Biol 2011; 413(1): 150-61.
68. Bershtein S, Wu W, Shakhnovich EI. Soluble oligomerization provides a beneficial fitness e[1]ect on destabilizing mutations. Proc Natl Acad Sci USA 2012; 109(13): 4857-62.
69. Majd S, Yusko EC, Billeh YN, Macrae MX, Yang J, Mayer M. Applications of biological pores in nanomedicine, sensing, and nanoelectronics. Curr Opin Biotechnol 2010; 21(4): 439-76.
70. Butler TZ, Pavlenok M, Derrington IM, Niederweis M, Gundlach JH. Single-molecule DNA detection with an engineered mspa protein nanopore. Proc Natl Acad Sci USA 2008; 105(52): 20647-52.
71. Adiga SP, Jin C, Curtiss LA, Monteiro-Riviere NA, Narayan RJ. Nanoporous membranes for medical and biological applications. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2009; 1(5): 568-81.
72. Banerjee A, Mikhailova E, Cheley S, et al. Molecular bases of cyclodextrin adapter interactions with engineered protein nanopores. Proc Natl Acad Sci USA 2010; 107(18): 8165-70.