Proteome-wide identification of predominant subcellular protein localizations in a bacterial model organism

Journal of Proteomics

Volumn 99, Issue , 2014, Pages 123-137

  Stekhoven, Daniel J ^a   Omasits, Ulrich ^a,b   Quebatte, Maxime ^c   Dehio, Christoph ^c   Ahrens, Christian H ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Experimental proteomics data; Localization change; Machine learning; Outer membrane proteome; Prokaryote; Subcellular localization

Indexed keywords

EXPERIMENTAL PROTEOMICS DATA; LOCALIZATION CHANGE; MACHINE LEARNING; OUTER MEMBRANE PROTEOME; PROKARYOTE; SUBCELLULAR LOCALIZATION;

BACTERIAL PROTEINS; BARTONELLA HENSELAE; MODELS, BIOLOGICAL; PROTEOME; PROTEOMICS;

EID: 84894271525     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.01.015     Document Type: Article

References (66)

1. Huh W.K., Falvo J.V., Gerke L.C., Carroll A.S., Howson R.W., Weissman J.S., et al. Global analysis of protein localization in budding yeast. Nature 2003, 425:686-691.
2. Matsuyama A., Arai R., Yashiroda Y., Shirai A., Kamata A., Sekido S., et al. ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat Biotechnol 2006, 24:841-847.
3. Kumar A., Agarwal S., Heyman J.A., Matson S., Heidtman M., Piccirillo S., et al. Subcellular localization of the yeast proteome. Genes Dev 2002, 16:707-719.
4. Lee K., Chuang H.Y., Beyer A., Sung M.K., Huh W.K., Lee B., et al. Protein networks markedly improve prediction of subcellular localization in multiple eukaryotic species. Nucleic Acids Res 2008, 36:e136.
5. Mintz-Oron S., Aharoni A., Ruppin E., Shlomi T. Network-based prediction of metabolic enzymes' subcellular localization. Bioinformatics 2009, 25:i247-i252.
6. Copley S.D. Moonlighting is mainstream: paradigm adjustment required. Bioessays 2012, 34:578-588.
7. Henderson B., Martin A. Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect Immun 2011, 79:3476-3491.
8. Mallick P., Kuster B. Proteomics: a pragmatic perspective. Nat Biotechnol 2010, 28:695-709.
9. Cox J., Mann M. Quantitative, high-resolution proteomics for data-driven systems biology. Annu Rev Biochem 2011, 80:273-299.
10. Ahrens C.H., Brunner E., Qeli E., Basler K., Aebersold R. Generating and navigating proteome maps using mass spectrometry. Nat Rev Mol Cell Biol 2010, 11:789-801.
11. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
12. Andersen J.S., Lam Y.W., Leung A.K.L., Ong S.E., Lyon C.E., Lamond A.I., et al. Nucleolar proteome dynamics. Nature 2005, 433:77-83.
13. Sadowski P.G., Dunkley T.P., Shadforth I.P., Dupree P., Bessant C., Griffin J.L., et al. Quantitative proteomic approach to study subcellular localization of membrane proteins. Nat Protoc 2006, 1:1778-1789.
14. Gatto L., Vizcaino J.A., Hermjakob H., Huber W., Lilley K.S. Organelle proteomics experimental designs and analysis. Proteomics 2010, 10:3957-3969.
15. Bumann D. Pathogen proteomes during infection: a basis for infection research and novel control strategies. J Proteomics 2010, 73:2267-2276.
16. Molloy M.P., Herbert B.R., Slade M.B., Rabilloud T., Nouwens A.S., Williams K.L., et al. Proteomic analysis of the Escherichia coli outer membrane. Eur J Biochem 2000, 267:2871-2881.
17. Rhomberg T.A., Karlberg O., Mini T., Zimny-Arndt U., Wickenberg U., Rottgen M., et al. Proteomic analysis of the sarcosine-insoluble outer membrane fraction of the bacterial pathogen Bartonella henselae. Proteomics 2004, 4:3021-3033.
18. Hobb R.I., Fields J.A., Burns C.M., Thompson S.A. Evaluation of procedures for outer membrane isolation from Campylobacter jejuni. Microbiology 2009, 155:979-988.
19. Li D.M., Liu Q.Y., Zhao F., Hu Y., Xiao D., Gu Y.X., et al. Proteomic and bioinformatic analysis of outer membrane proteins of the protobacterium Bartonella henselae (Bartonellaceae). Genet Mol Res 2011, 10:1789-1818.
20. Chenoweth M.R., Greene C.E., Krause D.C., Gherardini F.C. Predominant outer membrane antigens of Bartonella henselae. Infect Immun 2004, 72:3097-3105.
21. Dumetz F., Duchaud E., Claverol S., Orieux N., Papillon S., Lapaillerie D., et al. Analysis of the Flavobacterium psychrophilum outer-membrane subproteome and identification of new antigenic targets for vaccine by immunomics. Microbiology 2008, 154:1793-1801.
22. Daley D.O., Rapp M., Granseth E., Melen K., Drew D., von Heijne G. Global topology analysis of the Escherichia coli inner membrane proteome. Science 2005, 308:1321-1323.
23. Casabona M.G., Vandenbrouck Y., Attree I., Coute Y. Proteomic characterization of Pseudomonas aeruginosa PAO1 inner membrane. Proteomics 2013, 13:2419-2423.
24. Pieper R., Huang S.T., Clark D.J., Robinson J.M., Alami H., Parmar P.P., et al. Integral and peripheral association of proteins and protein complexes with Yersinia pestis inner and outer membranes. Proteome Sci 2009, 7:5.
25. Papanastasiou M., Orfanoudaki G., Koukaki M., Kountourakis N., Sardis M.F., Aivaliotis M., et al. The Escherichia coli peripheral inner membrane proteome. Mol Cell Proteomics 2013, 12:599-610.
26. Imperi F., Ciccosanti F., Perdomo A.B., Tiburzi F., Mancone C., Alonzi T., et al. Analysis of the periplasmic proteome of Pseudomonas aeruginosa, a metabolically versatile opportunistic pathogen. Proteomics 2009, 9:1901-1915.
27. Wu S., Brown R.N., Payne S.H., Meng D., Zhao R., Tolic N., et al. Top-down characterization of the post-translationally modified intact periplasmic proteome from the bacterium Novosphingobium aromaticivorans. Int J Proteomics 2013, 2013:279590.
28. Riedel K., Carranza P., Gehrig P., Potthast F., Eberl L. Towards the proteome of Burkholderia cenocepacia H111: setting up a 2-DE reference map. Proteomics 2006, 6:207-216.
29. Brown R.N., Romine M.F., Schepmoes A.A., Smith R.D., Lipton M.S. Mapping the subcellular proteome of Shewanella oneidensis MR-1 using sarkosyl-based fractionation and LC-MS/MS protein identification. J Proteome Res 2010, 9:4454-4463.
30. Brown R.N., Sanford J.A., Park J.H., Deatherage B.L., Champion B.L., Smith R.D., et al. A comprehensive subcellular proteomic survey of Salmonella Grown under phagosome-mimicking versus standard laboratory conditions. Int J Proteomics 2012, 2012:123076.
31. Han M.J., Yun H., Lee J.W., Lee Y.H., Lee S.Y., Yoo J.S., et al. Genome-wide identification of the subcellular localization of the Escherichia coli B proteome using experimental and computational methods. Proteomics 2011, 11:1213-1227.
32. Nair R., Rost B. Inferring sub-cellular localization through automated lexical analysis. Bioinformatics 2002, 18(Suppl. 1):S78-S86.
33. Lu Z., Szafron D., Greiner R., Lu P., Wishart D.S., Poulin B., et al. Predicting subcellular localization of proteins using machine-learned classifiers. Bioinformatics 2004, 20:547-556.
34. Yu C.S., Lin C.J., Hwang J.K. Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci 2004, 13:1402-1406.
35. Gardy J.L., Laird M.R., Chen F., Rey S., Walsh C.J., Ester M., et al. PSORTb v. 2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 2005, 21:617-623.
36. Shatkay H., Hoglund A., Brady S., Blum T., Donnes P., Kohlbacher O. SherLoc: high-accuracy prediction of protein subcellular localization by integrating text and protein sequence data. Bioinformatics 2007, 23:1410-1417.
37. Yu N.Y., Wagner J.R., Laird M.R., Melli G., Rey S., Lo R., et al. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 2010, 26:1608-1615.
38. Goldberg T., Hamp T., Rost B. LocTree2 predicts localization for all domains of life. Bioinformatics 2012, 28:i458-i465.
39. Omasits U., Quebatte M., Stekhoven D.J., Fortes C., Roschitzki B., Robinson M.D., et al. Directed shotgun proteomics guided by saturated RNA-Seq identifies a complete expressed prokaryotic proteome. Genome Res 2013, 23:1916-1927.
40. Quebatte M., Dehio M., Tropel D., Basler A., Toller I., Raddatz G., et al. The BatR/BatS two-component regulatory system controls the adaptive response of Bartonella henselae during human endothelial cell infection. J Bacteriol 2010, 192:3352-3367.
41. Filip C., Fletcher G., Wulff J.L., Earhart C.F. Solubilization of the cytoplasmic membrane of Escherichia coli by the ionic detergent sodium-lauryl sarcosinate. J Bacteriol 1973, 115:717-722.
42. Kim S., Mischerikow N., Bandeira N., Navarro J.D., Wich L., Mohammed S., et al. The generating function of CID, ETD, and CID/ETD pairs of tandem mass spectra: applications to database search. Mol Cell Proteomics 2010, 9:2840-2852.
43. Qeli E., Ahrens C.H. PeptideClassifier for protein inference and targeted quantitative proteomics. Nat Biotechnol 2010, 28:647-650.
44. Chenoweth M.R., Somerville G.A., Krause D.C., O'Reilly K.L., Gherardini F.C. Growth characteristics of Bartonella henselae in a novel liquid medium: primary isolation, growth-phase-dependent phage induction, and metabolic studies. Appl Environ Microbiol 2004, 70:656-663.
45. Litwin C.M., Rawlins M.L., Swenson E.M. Characterization of an immunogenic outer membrane autotransporter protein, Arp, of Bartonella henselae. Infect Immun 2007, 75:5255-5263.
46. Dalbey R.E., Wang P., Kuhn A. Assembly of bacterial inner membrane proteins. Annu Rev Biochem 2011, 80:161-187.
47. Franz B., Kempf V.A. Adhesion and host cell modulation: critical pathogenicity determinants of Bartonella henselae. Parasit Vectors 2011, 4:54.
48. Harms A., Dehio C. Intruders below the radar: molecular pathogenesis of Bartonella spp. Clin Microbiol Rev 2012, 25:42-78.
49. Juncker A.S., Willenbrock H., Von Heijne G., Brunak S., Nielsen H., Krogh A. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 2003, 12:1652-1662.
50. Berven F.S., Flikka K., Jensen H.B., Eidhammer I. BOMP: a program to predict integral beta-barrel outer membrane proteins encoded within genomes of Gram-negative bacteria. Nucleic Acids Res 2004, 32:W394-W399.
51. Struyve M., Moons M., Tommassen J. Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol 1991, 218:141-148.
52. Omasits U., Ahrens C.H., Müller S., Wollscheid B. Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 2013, 10.1093/bioinformatics/btt607.
53. Price C.E., Driessen A.J. Biogenesis of membrane bound respiratory complexes in Escherichia coli. Biochim Biophys Acta 1803, 2010:748-766.
54. Efremov R.G., Baradaran R., Sazanov L.A. The architecture of respiratory complex I. Nature 2010, 465:441-445.
55. Wallden K., Rivera-Calzada A., Waksman G. Type IV secretion systems: versatility and diversity in function. Cell Microbiol 2010, 12:1203-1212.
56. Fronzes R., Schafer E., Wang L., Saibil H.R., Orlova E.V., Waksman G. Structure of a type IV secretion system core complex. Science 2009, 323:266-268.
57. Aseev L.V., Boni I.V. Extraribosomal functions of bacterial ribosomal proteins. Mol Biol 2011, 45:739-750.
58. Vayssier-Taussat M., Le Rhun D., Deng H.K., Biville F., Cescau S., Danchin A., et al. The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes. PLoS Pathog 2010, 6:e1000946.
59. Schulein R., Guye P., Rhomberg T.A., Schmid M.C., Schroder G., Vergunst A.C., et al. A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells. Proc Natl Acad Sci U S A 2005, 102:856-861.
60. Schmid M.C., Scheidegger F., Dehio M., Balmelle-Devaux N., Schulein R., Guye P., et al. A translocated bacterial protein protects vascular endothelial cells from apoptosis. PLoS Pathog 2006, 2:e115.
61. Pulliainen A.T., Pieles K., Brand C.S., Hauert B., Bohm A., Quebatte M., et al. Bacterial effector binds host cell adenylyl cyclase to potentiate Galphas-dependent cAMP production. Proc Natl Acad Sci U S A 2012, 109:9581-9586.
62. Truttmann M.C., Rhomberg T.A., Dehio C. Combined action of the type IV secretion effector proteins BepC and BepF promotes invasome formation of Bartonella henselae on endothelial and epithelial cells. Cell Microbiol 2011, 13:284-299.
63. Riess T., Andersson S.G., Lupas A., Schaller M., Schafer A., Kyme P., et al. Bartonella adhesin a mediates a proangiogenic host cell response. J Exp Med 2004, 200:1267-1278.
64. Lu Y.Y., Franz B., Truttmann M.C., Riess T., Gay-Fraret J., Faustmann M., et al. Bartonella henselae trimeric autotransporter adhesin BadA expression interferes with effector translocation by the VirB/D4 type IV secretion system. Cell Microbiol 2013, 15:759-778.
65. Werner J.A., Feng S., Kasten R.W., Hodzic E., Chomel B.B., Barthold S.W. Cloning, characterization, and expression of Bartonella henselae p26. Clin Vaccine Immunol 2006, 13:830-836.
66. Bateman A., Bycroft M. The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J Mol Biol 2000, 299:1113-1119.