Not all transmembrane helices are born equal: Towards the extension of the sequence homology concept to membrane proteins

Biology Direct

Volumn 6, Issue , 2011, Pages

  Wong, Wing Cheong ^a   Maurer Stroh, Sebastian ^a,b   Eisenhaber, Frank ^a,c,d  

^a BIOINFORMATICS INSTITUTE   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; SIGNAL PEPTIDE;

ARTICLE; BIOLOGY; CHEMICAL PHENOMENA; CHEMISTRY; COMPUTER PROGRAM; MEMBRANE; PROTEIN DATABASE; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

COMPUTATIONAL BIOLOGY; DATABASES, PROTEIN; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MEMBRANE PROTEINS; MEMBRANES; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SOFTWARE;

EID: 80054826091     PISSN: None     EISSN: 17456150     Source Type: Journal    
DOI: 10.1186/1745-6150-6-57     Document Type: Article

References (96)

1. Wong WC, Maurer-Stroh S, Eisenhaber F. More than 1,001 problems with protein domain databases: transmembrane regions, signal peptides and the issue of sequence homology. PLoS Comput Biol 2010, 6:e1000867. 10.1371/journal.pcbi.1000867, 2912341, 20686689.
2. Bork P, Gibson TJ. Applying motif and profile searches. Methods Enzymol 1996, 266:162-184.
3. Bork P, Dandekar T, Diaz-Lazcoz Y, Eisenhaber F, Huynen M, Yuan Y. Predicting function: from genes to genomes and back. J Mol Biol 1998, 283:707-725. 10.1006/jmbi.1998.2144, 9790834.
4. Eisenhaber F. Prediction of Protein Function: Two Basic Concepts and One Practical Recipe. Discovering Biomolecular Mechanisms with Computational Biology 2006, 39-54. Georgetown and New York: Landes Biosciences and Springer, Eisenhaber F, 1.
5. Doolittle RF. Of Urfs and Orfs - A primer on how to analyze derived amino acid sequences 1986, Mill Valley: University Sciene Books.
6. Koonin EV, Galperin MY. Sequence - Evolution - Function: Computational approaches in comparative genomics 2003, Boston: Kluwer Academic.
7. Eisenhaber B, Eisenhaber F. Sequence complexity of proteins and its significance in annotation. "Bioinformatics" in the Encyclopedia of Genetics, Genomics, Proteomics and Bioinformatics 2005, 4. New York: Wiley Interscience, Subramaniam S, 1.
8. Eisenhaber B, Eisenhaber F. Posttranslational modifications and subcellular localization signals: indicators of sequence regions without inherent 3D structure?. Curr Protein Pept Sci 2007, 8:197-203. 10.2174/138920307780363424, 17430201.
9. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
10. Wootton JC, Federhen S. Analysis of compositionally biased regions in sequence databases. Methods Enzymol 1996, 266:554-571.
11. Schneider G, Neuberger G, Wildpaner M, Tian S, Berezovsky I, Eisenhaber F. Application of a sensitive collection heuristic for very large protein families: evolutionary relationship between adipose triglyceride lipase (ATGL) and classic mammalian lipases. BMC Bioinformatics 2006, 7:164. 10.1186/1471-2105-7-164, 1435942, 16551354.
12. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, et al. The Pfam protein families database. Nucleic Acids Res 2010, 38:D211-D222. 10.1093/nar/gkp985, 2808889, 19920124.
13. Sammut SJ, Finn RD, Bateman A. Pfam 10 years on: 10,000 families and still growing. Brief Bioinform 2008, 9:210-219. 10.1093/bib/bbn010, 18344544.
14. Saier MH, Tran CV, Barabote RD. TCDB: the Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Res 2006, 34:D181-D186. 10.1093/nar/gkj001, 1334385, 16381841.
15. Saier MH, Yen MR, Noto K, Tamang DG, Elkan C. The Transporter Classification Database: recent advances. Nucleic Acids Res 2009, 37:D274-D278. 10.1093/nar/gkn862, 2686586, 19022853.
16. Yen MR, Choi J, Saier MH. Bioinformatic analyses of transmembrane transport: novel software for deducing protein phylogeny, topology, and evolution. J Mol Microbiol Biotechnol 2009, 17:163-176. 10.1159/000239667, 2814153, 19776645.
17. Anantharaman V, Aravind L. Novel eukaryotic enzymes modifying cell-surface biopolymers. Biol Direct 2010, 5:1. 10.1186/1745-6150-5-1, 2824669, 20056006.
18. Henricson A, Sonnhammer EL, Baillie DL, Gomes AV. Functional characterization in Caenorhabditis elegans of transmembrane worm-human orthologs. BMC Genomics 2004, 5:85. 10.1186/1471-2164-5-85, 533873, 15533247.
19. Schultz J. HTTM, a horizontally transferred transmembrane domain. Trends Biochem Sci 2004, 29:4-7. 10.1016/j.tibs.2003.11.002, 14729325.
20. Schultz J, Milpetz F, Bork P, Ponting CP. SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 1998, 95:5857-5864. 10.1073/pnas.95.11.5857, 34487, 9600884.
21. Letunic I, Doerks T, Bork P. SMART 6: recent updates and new developments. Nucleic Acids Res 2009, 37:D229-D232. 10.1093/nar/gkn808, 2686533, 18978020.
22. Koonin EV, Makarova KS, Rogozin IB, Davidovic L, Letellier MC, Pellegrini L. The rhomboids: a nearly ubiquitous family of intramembrane serine proteases that probably evolved by multiple ancient horizontal gene transfers. Genome Biol 2003, 4:R19. 10.1186/gb-2003-4-3-r19, 153459, 12620104.
23. Feng L, Yan H, Wu Z, Yan N, Wang Z, Jeffrey PD, Shi Y. Structure of a site-2 protease family intramembrane metalloprotease. Science 2007, 318:1608-1612. 10.1126/science.1150755, 18063795.
24. Wu Z, Yan N, Feng L, Oberstein A, Yan H, Baker RP, Gu L, Jeffrey PD, Urban S, Shi Y. Structural analysis of a rhomboid family intramembrane protease reveals a gating mechanism for substrate entry. Nat Struct Mol Biol 2006, 13:1084-1091. 10.1038/nsmb1179, 17099694.
25. Horn F, Bettler E, Oliveira L, Campagne F, Cohen FE, Vriend G. GPCRDB information system for G protein-coupled receptors. Nucleic Acids Res 2003, 31:294-297. 10.1093/nar/gkg103, 165550, 12520006.
26. Wistrand M, Sonnhammer EL. Improved profile HMM performance by assessment of critical algorithmic features in SAM and HMMER. BMC Bioinformatics 2005, 6:99. 10.1186/1471-2105-6-99, 1097716, 15831105.
27. Bogner-Strauss JG, Prokesch A, Sanchez-Cabo F, Rieder D, Hackl H, Duszka K, Krogsdam A, Di CB, Walenta E, Klatzer A, et al. Reconstruction of gene association network reveals a transmembrane protein required for adipogenesis and targeted by PPARgamma. Cell Mol Life Sci 2010, 67:4049-4064. 10.1007/s00018-010-0424-5, 20552250.
28. Borhan B, Souto ML, Imai H, Shichida Y, Nakanishi K. Movement of retinal along the visual transduction path. Science 2000, 288:2209-2212. 10.1126/science.288.5474.2209, 10864869.
29. Bosch L, Ramon E, Del Valle LJ, Garriga P. Structural and functional role of helices I and II in rhodopsin. A novel interplay evidenced by mutations at Gly-51 and Gly-89 in the transmembrane domain. J Biol Chem 2003, 278:20203-20209. 10.1074/jbc.M301319200, 12660238.
30. Li J, Edwards PC, Burghammer M, Villa C, Schertler GF. Structure of bovine rhodopsin in a trigonal crystal form. J Mol Biol 2004, 343:1409-1438. 10.1016/j.jmb.2004.08.090, 15491621.
31. Watanabe R, Murakami Y, Marmor MD, Inoue N, Maeda Y, Hino J, Kangawa K, Julius M, Kinoshita T. Initial enzyme for glycosylphosphatidylinositol biosynthesis requires PIG-P and is regulated by DPM2. EMBO J 2000, 19:4402-4411. 10.1093/emboj/19.16.4402, 302040, 10944123.
32. Wimley WC, White SH. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat Struct Biol 1996, 3:842-848. 10.1038/nsb1096-842, 8836100.
33. Wimley WC, . Creamer TPWSH Solvation energies of amino acid side chains and backbone in a family of host-guest pentapeptides. Biochemistry 1996, 35:5109-5124. 10.1021/bi9600153, 8611495, Creamer TPWSH.
34. Moore DT, Berger BW, DeGrado WF. Protein-protein interactions in the membrane: sequence, structural, and biological motifs. Structure 2008, 16:991-1001. 10.1016/j.str.2008.05.007, 18611372.
35. White SH, Wimley WC. Hydrophobic interactions of peptides with membrane interfaces. Biochim Biophys Acta 1998, 1376:339-352.
36. White SH, Wimley WC. Membrane protein folding and stability : physical principles. Annu Rev Biophys Biomol Struc 1999, 28:365.
37. Andreeva A, Howorth D, Chandonia JM, Brenner SE, Hubbard TJ, Chothia C, Murzin AG. Data growth and its impact on the SCOP database: new developments. Nucleic Acids Res 2008, 36:D419-D425. 2238974, 18000004.
38. Murzin AG, Brenner SE, Hubbard T, Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 1995, 247:536-540.
39. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22:1658-1659. 10.1093/bioinformatics/btl158, 16731699.
40. Zar JH. Biostatistical analysis 1998, Upper Saddle River: Pearson Prentice Hall.
41. Sal-Man N, Shai Y. Arginine mutations within a transmembrane domain of Tar, an Escherichia coli aspartate receptor, can drive homodimer dissociation and heterodimer association in vivo. Biochem J 2005, 385:29-36. 10.1042/BJ20041022, 1134670, 15330757.
42. Dawson JP, Melnyk RA, Deber CM, Engelman DM. Sequence context strongly modulates association of polar residues in transmembrane helices. J Mol Biol 2003, 331:255-262. 10.1016/S0022-2836(03)00714-9, 12875850.
43. Melnyk RA, Kim S, Curran AR, Engelman DM, Bowie JU, Deber CM. The affinity of GXXXG motifs in transmembrane helix-helix interactions is modulated by long-range communication. J Biol Chem 2004, 279:16591-16597. 10.1074/jbc.M313936200, 14766751.
44. Senes A, Engel DE, DeGrado WF. Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr Opin Struct Biol 2004, 14:465-479. 10.1016/j.sbi.2004.07.007, 15313242.
45. Schiffer M, Ainsworth CF, Deng YL, Johnson G, Pascoe FH, Hanson DK. Proline in a transmembrane helix compensates for cavities in the photosynthetic reaction center. J Mol Biol 1995, 252:472-482. 10.1006/jmbi.1995.0512, 7563066.
46. Polinsky A, Goodman M, Williams KA, Deber CM. Minimum energy conformations of proline-containing helices. Biopolymers 1992, 32:399-406. 10.1002/bip.360320416, 1623135.
47. Nilsson I, Saaf A, Whitley P, Gafvelin G, Waller C, von HG. Proline-induced disruption of a transmembrane alpha-helix in its natural environment. J Mol Biol 1998, 284:1165-1175. 10.1006/jmbi.1998.2217, 9837734.
48. Williams KA, Deber CM. Proline residues in transmembrane helices: structural or dynamic role?. Biochemistry 1991, 30:8919-8923. 10.1021/bi00101a001, 1892808.
49. Cohen J. Statistical power analysis for the behavioral sciences 1988, Routledge Academic.
50. Everitt BS, Hand DJ. Finite mixture distributions 2011, London New York: Chapman and Hall.
51. Cunningham F, Rath A, Johnson RM, Deber CM. Distinctions between hydrophobic helices in globular proteins and transmembrane segments as factors in protein sorting. J Biol Chem 2009, 284:5395-5402.
52. Bendtsen JD, Nielsen H, von HG, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004, 340:783-795. 10.1016/j.jmb.2004.05.028, 15223320.
53. Sal-Man N, Gerber D, Shai Y. The composition rather than position of polar residues (QxxS) drives aspartate receptor transmembrane domain dimerization in vivo. Biochemistry 2004, 43:2309-2313. 10.1021/bi0356294, 14979727.
54. Parker MW, Postma JP, Pattus F, Tucker AD, Tsernoglou D. Refined structure of the pore-forming domain of colicin A at 2.4 A resolution. J Mol Biol 1992, 224:639-657. 10.1016/0022-2836(92)90550-4, 1373773.
55. Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R, Postle K, Riley M, Slatin S, Cavard D. Colicin biology. Microbiol Mol Biol Rev 2007, 71:158-229. 10.1128/MMBR.00036-06, 1847374, 17347522.
56. Smajs D, Dolezalova M, Macek P, Zidek L. Inactivation of colicin Y by intramembrane helix-helix interaction with its immunity protein. FEBS J 2008, 275:5325-5331. 10.1111/j.1742-4658.2008.06662.x, 18803667.
57. Zhang YL, Cramer WA. Intramembrane helix-helix interactions as the basis of inhibition of the colicin E1 ion channel by its immunity protein. J Biol Chem 1993, 268:10176-10184.
58. Fiedler S, Broecker J, Keller S. Protein folding in membranes. Cell Mol Life Sci 2010, 67:1779-1798. 10.1007/s00018-010-0259-0, 20101433.
59. Park Y, Hayat S, Helms V. Prediction of the burial status of transmembrane residues of helical membrane proteins. BMC Bioinformatics 2007, 8:302. 10.1186/1471-2105-8-302, 2000914, 17708758.
60. Doolittle RF, Blombach E. Amino-acid sequence investigations of fibrinopeptides from various mammals: evolutionary implications. Nature 1964, 202:147-152. 10.1038/202147a0, 14156289.
61. Fitch WM, Margoliash E. Construction of phylogenetic trees: a method based on mutational distances as estimated from cytochrome c sequences is of general applicability. Science 1967, 155:279-284. 10.1126/science.155.3760.279, 5334057.
62. Dayhoff MO. Computer analysis of protein evolution. Sci Am 1969, 221:86-95.
63. Jardine N, van Rijsbergen CJ, Jardine CJ. Evolutionary rates and the inference of evolutionary tree forms. Nature 1969, 224:185.
64. Brew K, Vanaman TC, Hill RL. Comparison of the amino acid sequence of bovine alpha-lactalbumin and hens egg white lysozyme. J Biol Chem 1967, 242:3747-3749.
65. Palmer KA, Scheraga HA, Riordan JF, Vallee BL. A preliminary three-dimensional structure of angiogenin. Proc Natl Acad Sci USA 1986, 83:1965-1969. 10.1073/pnas.83.7.1965, 323210, 3457369.
66. Allen SC, Acharya KR, Palmer KA, Shapiro R, Vallee BL, Scheraga HA. A comparison of the predicted and X-ray structures of angiogenin. Implications for further studies of model building of homologous proteins. J Protein Chem 1994, 13:649-658. 10.1007/BF01890464, 7702747.
67. Wagner GP. The biological homology concept. Annu Rev Ecol Syst 1989, 20:51-69.
68. Varshavsky A. 'Spalog' and 'sequelog': neutral terms for spatial and sequence similarity. Curr Biol 2004, 14:R181-R183. 10.1016/j.cub.2004.02.014, 15028230.
69. Doolittle RF. Similar amino acid sequences: chance or common ancestry?. Science 1981, 214:149-159. 10.1126/science.7280687, 7280687.
70. Doolittle RF. Similar amino acid sequences revisited. Trends Biochem Sci 1989, 14:244-245. 10.1016/0968-0004(89)90055-8, 2773041.
71. Reeck GR, de HC, Teller DC, Doolittle RF, Fitch WM, Dickerson RE, Chambon P, McLachlan AD, Margoliash E, Jukes TH, et al. "Homology" in proteins and nucleic acids: a terminology muddle and a way out of it. Cell 1987, 50:667. 10.1016/0092-8674(87)90322-9, 3621342.
72. Doolittle RF. Convergent evolution: the need to be explicit. Trends Biochem Sci 1994, 19:15-18. 10.1016/0968-0004(94)90167-8, 8140615.
73. Eddy SR. What is a hidden Markov model?. Nat Biotechnol 2004, 22:1315-1316. 10.1038/nbt1004-1315, 15470472.
74. Eddy SR. A probabilistic model of local sequence alignment that simplifies statistical significance estimation. PLoS Comput Biol 2008, 4:e1000069. 10.1371/journal.pcbi.1000069, 2396288, 18516236.
75. Ng PC, Henikoff JG, Henikoff S. PHAT: a transmembrane-specific substitution matrix. Predicted hydrophobic and transmembrane. Bioinformatics 2000, 16:760-766. 10.1093/bioinformatics/16.9.760, 11108698.
76. Muller T, Rahmann S, Rehmsmeier M. Non-symmetric score matrices and the detection of homologous transmembrane proteins. Bioinformatics 2001, 17:S182-S189. 10.1093/bioinformatics/17.suppl_1.S182, 11473008.
77. Gilks WR, Audit B, de AD, Tsoka S, Ouzounis CA. Modeling the percolation of annotation errors in a database of protein sequences. Bioinformatics 2002, 18:1641-1649. 10.1093/bioinformatics/18.12.1641, 12490449.
78. Gilks WR, Audit B, de AD, Tsoka S, Ouzounis CA. Percolation of annotation errors through hierarchically structured protein sequence databases. Math Biosci 2005, 193:223-234. 10.1016/j.mbs.2004.08.001, 15748731.
79. Wong WC, Maurer-Stroh S, Eisenhaber F. The Janus-faced E-values of HMMER2: extreme value distribution or logistic function?. J Bioinform Comput Biol 2011, 9:179-206. 10.1142/S0219720011005264, 21328712.
80. Carfi A, Willis SH, Whitbeck JC, Krummenacher C, Cohen GH, Eisenberg RJ, Wiley DC. Herpes simplex virus glycoprotein D bound to the human receptor HveA. Mol Cell 2001, 8:169-179. 10.1016/S1097-2765(01)00298-2, 11511370.
81. Misu K, Fujimura-Kamada K, Ueda T, Nakano A, Katoh H, Tanaka K. Cdc50p, a conserved endosomal membrane protein, controls polarized growth in Saccharomyces cerevisiae. Mol Biol Cell 2003, 14:730-747. 10.1091/mbc.E02-06-0314, 150004, 12589066.
82. Xu C, Rice WJ, He W, Stokes DL. A structural model for the catalytic cycle of Ca(2+)-ATPase. J Mol Biol 2002, 316:201-211. 10.1006/jmbi.2001.5330, 11829513.
83. Abendroth J, Mitchell DD, Korotkov KV, Johnson TL, Kreger A, Sandkvist M, Hol WG. The three-dimensional structure of the cytoplasmic domains of EpsF from the type 2 secretion system of Vibrio cholerae. J Struct Biol 2009, 166:303-315. 10.1016/j.jsb.2009.03.009, 2730350, 19324092.
84. Sun L, Gu S, Sun Y, Zheng D, Wu Q, Li X, Dai J, Dai J, Ji C, Xie Y, et al. Cloning and characterization of a novel human phosphatidic acid phosphatase type 2, PAP2d, with two different transcripts PAP2d_v1 and PAP2d_v2. Mol Cell Biochem 2005, 272:91-96. 10.1007/s11010-005-7640-6, 16010976.
85. Qu L, McMullan LK, Rice CM. Isolation and characterization of noncytopathic pestivirus mutants reveals a role for nonstructural protein NS4B in viral cytopathogenicity. J Virol 2001, 75:10651-10662. 10.1128/JVI.75.22.10651-10662.2001, 114647, 11602707.
86. Watanabe R, Murakami Y, Marmor MD, Inoue N, Maeda Y, Hino J, Kangawa K, Julius M, Kinoshita T. Initial enzyme for glycosylphosphatidylinositol biosynthesis requires PIG-P and is regulated by DPM2. EMBO J 2000, 19:4402-4411. 10.1093/emboj/19.16.4402, 302040, 10944123.
87. Ciufo LF, Boyd A. Identification of a lumenal sequence specifying the assembly of Emp24p into p24 complexes in the yeast secretory pathway. J Biol Chem 2000, 275:8382-8388. 10.1074/jbc.275.12.8382, 10722670.
88. Kihara A, Sakuraba H, Ikeda M, Denpoh A, Igarashi Y. Membrane topology and essential amino acid residues of Phs1, a 3-hydroxyacyl-CoA dehydratase involved in very long-chain fatty acid elongation. J Biol Chem 2008, 283:11199-11209. 10.1074/jbc.M708993200, 18272525.
89. Uwanogho DA, Hardcastle Z, Balogh P, Mirza G, Thornburg KL, Ragoussis J, Sharpe PT. Molecular cloning, chromosomal mapping, and developmental expression of a novel protein tyrosine phosphatase-like gene. Genomics 1999, 62:406-416. 10.1006/geno.1999.5950, 10644438.
90. Fukuda M. Lysosomal membrane glycoproteins. Structure, biosynthesis, and intracellular trafficking. J Biol Chem 1991, 266:21327-21330.
91. Settles AM, Yonetani A, Baron A, Bush DR, Cline K, Martienssen R. Sec-independent protein translocation by the maize Hcf106 protein. Science 1997, 278:1467-1470. 10.1126/science.278.5342.1467, 9367960.
92. Weiner JH, Bilous PT, Shaw GM, Lubitz SP, Frost L, Thomas GH, Cole JA, Turner RJ. A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell 1998, 93:93-101. 10.1016/S0092-8674(00)81149-6, 9546395.
93. Aravind L, Ponting CP. The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol Lett 1999, 176:111-116. 10.1111/j.1574-6968.1999.tb13650.x, 10418137.
94. Lunin VV, Dobrovetsky E, Khutoreskaya G, Zhang R, Joachimiak A, Doyle DA, Bochkarev A, Maguire ME, Edwards AM, Koth CM. Crystal structure of the CorA Mg2+ transporter. Nature 2006, 440:833-837. 10.1038/nature04642, 16598263.
95. Montal M. Structure-function correlates of Vpu, a membrane protein of HIV-1. FEBS Lett 2003, 552:47-53. 10.1016/S0014-5793(03)00849-4, 12972151.
96. Kusano S, Kukimoto-Niino M, Akasaka R, Toyama M, Terada T, Shirouzu M, Shindo T, Yokoyama S. Crystal structure of the human receptor activity-modifying protein 1 extracellular domain. Protein Sci 2008, 17:1907-1914. 10.1110/ps.036012.108, 2578806, 18725456.