Surfomics: Shaving live organisms for a fast proteomic identification of surface proteins

Journal of Proteomics

Volumn 97, Issue , 2014, Pages 164-176

  Olaya Abril, Alfonso ^a,b   Jiménez Munguía, Irene ^a,b   Gómez Gascón, Lidia ^a   Rodríguez Ortega, Manuel J ^a,b  

^a UNIVERSITY OF CÓRDOBA   (Spain)

^b Instituto de Salud Carlos III   (Spain)

Author keywords

Cell surface; Diagnostics; Shaving; Surface proteins; Vaccines

Indexed keywords

CELL MEMBRANE PROTEIN; CELL SURFACE PROTEIN; CYTOPLASM PROTEIN; IMMOBILIZED ENZYME; MICROORGANISM PROTEIN; PEPTIDE FRAGMENT; PROTEINASE K; RECOMBINANT PROTEIN; TRYPSIN; MEMBRANE PROTEIN; PROTEINASE;

BACTERIAL CELL; CELL ADHESION; CELL FRACTIONATION; CELL MEMBRANE; CELL SURFACE; CELL VIABILITY; CELLULAR DISTRIBUTION; CYTOLYSIS; FLOW CYTOMETRY; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HOST CELL; HOST PATHOGEN INTERACTION; MEMBRANE VESICLE; MICROBIAL GENOME; NONHUMAN; PLANCTOMYCETES; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN SUBUNIT; PROTEOMICS; REVIEW; SECRETORY PATHWAY; CELL ORGANELLE; CYTOTOXICITY; FRACTIONATION; IMMUNE SYSTEM; INFECTION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; VIRULENCE;

NEGIBACTERIA; POSIBACTERIA; PROTOFUNGI;

CELL SURFACE; DIAGNOSTICS; SHAVING; SURFACE PROTEINS; VACCINES;

ANIMALS; BACTERIAL PROTEINS; GRAM-NEGATIVE BACTERIA; GRAM-NEGATIVE BACTERIAL INFECTIONS; GRAM-POSITIVE BACTERIA; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMANS; PROTEOMICS;

EID: 84892874899     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.03.035     Document Type: Review

References (101)

1. Navarre W.W., Schneewind O. Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 1999, 63:174-229.
2. Dreisbach A., van Dijl J.M., Buist G. The cell surface proteome of Staphylococcus aureus. Proteomics 2011, 11:3154-3168.
3. Grandi G. Genomics and proteomics in reverse vaccines. Methods Biochem Anal 2006, 49:379-393.
4. Fleischmann R.D., Adams M.D., White O., Clayton R.A., Kirkness E.F., Kerlavage A.R., et al. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 1995, 269:496-512.
5. Solis N., Cordwell S.J. Current methodologies for proteomics of bacterial surface-exposed and cell envelope proteins. Proteomics 2011, 11:3169-3189.
6. Rabilloud T., Chevallet M., Luche S., Lelong C. Two-dimensional gel electrophoresis in proteomics: past, present and future. J Proteomics 2010, 73:2064-2077.
7. Rabilloud T. Membrane proteins and proteomics: love is possible, but so difficult. Electrophoresis 2009, 30(Suppl. 1):S174-S180.
8. Görg A., Drews O., Luck C., Weiland F., Weiss W. 2-DE with IPGs. Electrophoresis 2009, 30(Suppl. 1):S122-S132.
9. Speers A.E., Wu C.C. Proteomics of integral membrane proteins-theory and application. Chem Rev 2007, 107:3687-3714.
10. Wu C.C., MacCoss M.J., Howell K.E., Yates J.R. A method for the comprehensive proteomic analysis of membrane proteins. Nat Biotechnol 2003, 21:532-538.
11. Wu C.C., Yates J.R. The application of mass spectrometry to membrane proteomics. Nat Biotechnol 2003, 21:262-267.
12. Kaushik D.K., Sehgal D. Developing antibacterial vaccines in genomics and proteomics era. Scand J Immunol 2008, 67:544-552.
13. Zagursky R.J., Anderson A.S. Application of genomics in bacterial vaccine discovery: a decade in review. Curr Opin Pharmacol 2008, 8:632-638.
14. Rappuoli R. Reverse vaccinology. Curr Opin Microbiol 2000, 3:445-450.
15. Pizza M., Scarlato V., Masignani V., Giuliani M.M., Arico B., Comanducci M., et al. Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing. Science 2000, 287:1816-1820.
16. El-Hage N., Babb K., Carroll J.A., Lindstrom N., Fischer E.R., Miller J.C., et al. Surface exposure and protease insensitivity of Borrelia burgdorferi Erp (OspEF-related) lipoproteins. Microbiology 2001, 147:821-830.
17. Rodríguez-Ortega M.J., Norais N., Bensi G., Liberatori S., Capo S., Mora M., et al. Characterization and identification of vaccine candidate proteins through analysis of the group A Streptococcus surface proteome. Nat Biotechnol 2006, 24:191-197.
18. Nakai K. Protein sorting signals and prediction of subcellular localization. Adv Protein Chem 2000, 54:277-344.
19. Musser J.M. The next chapter in reverse vaccinology. Nat Biotechnol 2006, 24:157-158.
20. Bensi G., Mora M., Tuscano G., Biagini M., Chiarot E., Bombaci M., et al. Multi high-throughput approach for highly selective identification of vaccine candidates: the group A Streptococcus case. Mol Cell Proteomics 2012, 11:M111. [015693].
21. Severin A., Nickbarg E., Wooters J., Quazi S.A., Matsuka Y.V., Murphy E., et al. Proteomic analysis and identification of Streptococcus pyogenes surface-associated proteins. J Bacteriol 2007, 189:1514-1522.
22. Doro F., Liberatori S., Rodríguez-Ortega M.J., Rinaudo C.D., Rosini R., Mora M., et al. Surfome analysis as a fast track to vaccine discovery: identification of a novel protective antigen for group B Streptococcus hyper-virulent strain COH1. Mol Cell Proteomics 2009, 8:1728-1737.
23. Garibaldi M., Rodríguez-Ortega M.J., Mandanici F., Cardaci A., Midiri A., Papasergi S., et al. Immunoprotective activities of a Streptococcus suis pilus subunit in murine models of infection. Vaccine 2010, 28:3609-3616.
24. Gómez-Gascón L., Luque I., Olaya-Abril A., Jiménez-Munguía I., Orbegozo-Medina R.A., Peralbo E., et al. Exploring the pan-surfome of Streptococcus suis: looking for common protein antigens. J Proteomics 2012, 75:5654-5666.
25. Mandanici F., Gómez-Gascón L., Garibaldi M., Olaya-Abril A., Luque I., Tarradas C., et al. A surface protein of Streptococcus suis serotype 2 identified by proteomics protects mice against infection. J Proteomics 2010, 73:2365-2369.
26. Rodríguez-Ortega M.J., Luque I., Tarradas C., Bárcena J.A. Overcoming function annotation errors in the Gram-positive pathogen Streptococcus suis by a proteomics-driven approach. BMC Genomics 2008, 9:588.
27. Olaya-Abril A., Gómez-Gascón L., Jiménez-Munguía I., Obando I., Rodríguez-Ortega M.J. Another turn of the screw in shaving Gram-positive bacteria: optimization of proteomics surface protein identification in Streptococcus pneumoniae. J Proteomics 2012, 75:3733-3746.
28. Wei Z., Fu Q., Liu X., Xiao P., Lu Z., Chen Y. Identification of Streptococcus equi ssp. zooepidemicus surface associated proteins by enzymatic shaving. Vet Microbiol 2012, 159:519-525.
29. Tjalsma H., Lambooy L., Hermans P.W., Swinkels D.W. Shedding & shaving: disclosure of proteomic expressions on a bacterial face. Proteomics 2008, 8:1415-1428.
30. Dreisbach A., Hempel K., Buist G., Hecker M., Becher D., van Dijl J.M. Profiling the surfacome of Staphylococcus aureus. Proteomics 2010, 10:3082-3096.
31. Mishra R.P., Mariotti P., Fiaschi L., Nosari S., Maccari S., Liberatori S., et al. Staphylococcus aureus FhuD2 is involved in the early phase of staphylococcal dissemination and generates protective immunity in mice. J Infect Dis 2012, 206:1041-1049.
32. Solis N., Larsen M.R., Cordwell S.J. Improved accuracy of cell surface shaving proteomics in Staphylococcus aureus using a false-positive control. Proteomics 2010, 10:2037-2049.
33. Ventura C.L., Malachowa N., Hammer C.H., Nardone G.A., Robinson M.A., Kobayashi S.D., et al. Identification of a novel Staphylococcus aureus two-component leukotoxin using cell surface proteomics. PLoS One 2010, 5:e11634.
34. Waridel P., Ythier M., Gfeller A., Moreillon P., Quadroni M. Evidence for a new post-translational modification in Staphylococcus aureus: hydroxymethylation of asparagine and glutamine. J Proteomics 2012, 75:1742-1751.
35. Ythier M., Resch G., Waridel P., Panchaud A., Gfeller A., Majcherczyk P., et al. Proteomic and transcriptomic profiling of Staphylococcus aureus surface LPXTG-proteins: correlation with agr genotypes and adherence phenotypes. Mol Cell Proteomics 2012, 11:1123-1139.
36. Benachour A., Morin T., Hebert L., Budin-Verneuil A., Le Jeune A., Auffray Y., et al. Identification of secreted and surface proteins from Enterococcus faecalis. Can J Microbiol 2009, 55:967-974.
37. Bøhle L.A., Riaz T., Egge-Jacobsen W., Skaugen M., Busk O.L., Eijsink V.G., et al. Identification of surface proteins in Enterococcus faecalis V583. BMC Genomics 2011, 12:135.
38. Berlec A., Zadravec P., Jevnikar Z., Strukelj B. Identification of candidate carrier proteins for surface display on Lactococcus lactis by theoretical and experimental analyses of the surface proteome. Appl Environ Microbiol 2011, 77:1292-1300.
39. Trémillon N., Morello E., Llull D., Mazmouz R., Gratadoux J.J., Guillot A., et al. PpiA, a surface PPIase of the cyclophilin family in Lactococcus lactis. PLoS One 2012, 7:e33516.
40. He Z., De Buck J. Localization of proteins in the cell wall of Mycobacterium avium subsp. paratuberculosis K10 by proteomic analysis. Proteome Sci 2010, 8:21.
41. Newton V., McKenna S.L., De Buck J. Presence of PPE proteins in Mycobacterium avium subsp. paratuberculosis isolates and their immunogenicity in cattle. Vet Microbiol 2009, 135:394-400.
42. Meoni E., Faenzi E., Frigimelica E., Zedda L., Skibinski D., Giovinazzi S., et al. CT043, a protective antigen that induces a CD4+ Th1 response during Chlamydia trachomatis infection in mice and humans. Infect Immun 2009, 77:4168-4176.
43. Cirulli C., Marino G., Amoresano A. Membrane proteome in Escherichia coli probed by MS3 mass spectrometry: a preliminary report. Rapid Commun Mass Spectrom 2007, 21:2389-2397.
44. Van Gerven N., Sleutel M., Deboeck F., De Greve H., Hernalsteens J.P. Surface display of the receptor-binding domain of the F17a-G fimbrial adhesin through the autotransporter AIDA-I leads to permeability of bacterial cells. Microbiology 2009, 155:468-476.
45. Walters M.S., Mobley H.L. Identification of uropathogenic Escherichia coli surface proteins by shotgun proteomics. J Microbiol Methods 2009, 78:131-135.
46. Manfredi P., Renzi F., Mally M., Sauteur L., Schmaler M., Moes S., et al. The genome and surface proteome of Capnocytophaga canimorsus reveal a key role of glycan foraging systems in host glycoproteins deglycosylation. Mol Microbiol 2011, 81:1050-1060.
47. Gesslbauer B., Poljak A., Handwerker C., Schuler W., Schwendenwein D., Weber C., et al. Comparative membrane proteome analysis of three Borrelia species. Proteomics 2012, 12:845-858.
48. Voigt B., Hieu C.X., Hempel K., Becher D., Schluter R., Teeling H., et al. Cell surface proteome of the marine planctomycete Rhodopirellula baltica. Proteomics 2012, 12:1781-1791.
49. Braconi D., Amato L., Bernardini G., Arena S., Orlandini M., Scaloni A., et al. Surfome analysis of a wild-type wine Saccharomyces cerevisiae strain. Food Microbiol 2011, 28:1220-1230.
50. Insenser M.R., Hernáez M.L., Nombela C., Molina M., Molero G., Gil C. Gel and gel-free proteomics to identify Saccharomyces cerevisiae cell surface proteins. J Proteomics 2010, 73:1183-1195.
51. Hernáez M.L., Ximénez-Embún P., Martínez-Gomariz M., Gutiérrez-Blázquez M.D., Nombela C., Gil C. Identification of Candida albicans exposed surface proteins in vivo by a rapid proteomic approach. J Proteomics 2010, 73:1404-1409.
52. Vialás V., Perumal P., Gutiérrez D., Ximénez-Embún P., Nombela C., Gil C., et al. Cell surface shaving of Candida albicans biofilms, hyphae, and yeast form cells. Proteomics 2012, 12:2331-2339.
53. Castro-Borges W., Dowle A., Curwen R.S., Thomas-Oates J., Wilson R.A. Enzymatic shaving of the tegument surface of live schistosomes for proteomic analysis: a rational approach to select vaccine candidates. PLoS Negl Trop Dis 2011, 5:e993.
54. Pérez-Sánchez R., Valero M.L., Ramajo-Hernández A., Siles-Lucas M., Ramajo-Martín V., Oleaga A. A proteomic approach to the identification of tegumental proteins of male and female Schistosoma bovis worms. Mol Biochem Parasitol 2008, 161:112-123.
55. Hernández-González A., Valero M.L., del Pino M.S., Oleaga A., Siles-Lucas M. Proteomic analysis of in vitro newly excysted juveniles from Fasciola hepatica. Mol Biochem Parasitol 2010, 172:121-128.
56. Santivañez S.J., Hernández-González A., Chile N., Oleaga A., Arana Y., Palma S., et al. Proteomic study of activated Taenia solium oncospheres. Mol Biochem Parasitol 2010, 171:32-39.
57. Ebeling W., Hennrich N., Klockow M., Metz H., Orth H.D., Lang H. Proteinase K from Tritirachium album Limber. Eur J Biochem 1974, 47:91-97.
58. Müller A., Hinrichs W., Wolf W.M., Saenger W. Crystal structure of calcium-free proteinase K at 1.5-A resolution. J Biol Chem 1994, 269:23108-23111.
59. Hilleringmann M., Giusti F., Baudner B.C., Masignani V., Covacci A., Rappuoli R., et al. Pneumococcal pili are composed of protofilaments exposing adhesive clusters of Rrg A. PLoS Pathog 2008, 4:e1000026.
60. Hilleringmann M., Ringler P., Muller S.A., De Angelis G., Rappuoli R., Ferlenghi I., et al. Molecular architecture of Streptococcus pneumoniae TIGR4 pili. EMBO J 2009, 28:3921-3930.
61. Mora M., Bensi G., Capo S., Falugi F., Zingaretti C., Manetti A.G., et al. Group A Streptococcus produce pilus-like structures containing protective antigens and Lancefield T antigens. Proc Natl Acad Sci U S A 2005, 102:15641-15646.
62. Lancefield R.C. Studies on the antigenic composition of group a hemolytic streptococci: I. Effects of proteolytic enzymes on streptococcal cells. J Exp Med 1943, 78:465-476.
63. Chhatwal G.S. Anchorless adhesins and invasins of Gram-positive bacteria: a new class of virulence factors. Trends Microbiol 2002, 10:205-208.
64. Gancedo C., Flores C.L. Moonlighting proteins in yeasts. Microbiol Mol Biol Rev 2008, 72:197-210.
65. 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.
66. Jeffery C.J. Moonlighting proteins-an update. Mol Biosyst 2009, 5:345-350.
67. Ucker D.S., Jain M.R., Pattabiraman G., Palasiewicz K., Birge R.B., Li H. Externalized glycolytic enzymes are novel, conserved, and early biomarkers of apoptosis. J Biol Chem 2012, 287:10325-10343.
68. Kohler C., Wolff S., Albrecht D., Fuchs S., Becher D., Buttner K., et al. Proteome analyses of Staphylococcus aureus in growing and non-growing cells: a physiological approach. Int J Med Microbiol 2005, 295:547-565.
69. Aguilera L., Ferreira E., Giménez R., Fernández F.J., Taulés M., Aguilar J., et al. Secretion of the housekeeping protein glyceraldehyde-3-phosphate dehydrogenase by the LEE-encoded type III secretion system in enteropathogenic Escherichia coli. Int J Biochem Cell Biol 2012, 44:955-962.
70. Bendtsen J.D., Kiemer L., Fausboll A., Brunak S. Non-classical protein secretion in bacteria. BMC Microbiol 2005, 5:58.
71. Nombela C., Gil C., Chaffin W.L. Non-conventional protein secretion in yeast. Trends Microbiol 2006, 14:15-21.
72. Weidenmaier C., Peschel A. Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 2008, 6:276-287.
73. Henningham A., Chiarot E., Gillen C.M., Cole J.N., Rohde M., Fulde M., et al. Conserved anchorless surface proteins as group A streptococcal vaccine candidates. J Mol Med (Berl) 2012, 90:1197-1207.
74. Tjalsma H., Scholler-Guinard M., Lasonder E., Ruers T.J., Willems H.L., Swinkels D.W. Profiling the humoral immune response in colon cancer patients: diagnostic antigens from Streptococcus bovis. Int J Cancer 2006, 119:2127-2135.
75. Kolberg J., Hammerschmidt S., Frank R., Jonak J., Sanderova H., Aase A. The surface-associated elongation factor Tu is concealed for antibody binding on viable pneumococci and meningococci. FEMS Immunol Med Microbiol 2008, 53:222-230.
76. Bergmann S., Rohde M., Chhatwal G.S., Hammerschmidt S. Alpha-enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Mol Microbiol 2001, 40:1273-1287.
77. Bergmann S., Rohde M., Hammerschmidt S. Glyceraldehyde-3-phosphate dehydrogenase of Streptococcus pneumoniae is a surface-displayed plasminogen-binding protein. Infect Immun 2004, 72:2416-2419.
78. Dallo S.F., Kannan T.R., Blaylock M.W., Baseman J.B. Elongation factor Tu and E1 beta subunit of pyruvate dehydrogenase complex act as fibronectin binding proteins in Mycoplasma pneumoniae. Mol Microbiol 2002, 46:1041-1051.
79. Feng Y., Pan X., Sun W., Wang C., Zhang H., Li X., et al. Streptococcus suis enolase functions as a protective antigen displayed on the bacterial cell surface. J Infect Dis 2009, 200:1583-1592.
80. Jin H., Agarwal S., Pancholi V. Surface export of GAPDH/SDH, a glycolytic enzyme, is essential for Streptococcus pyogenes virulence. MBio 2011, 2:e00068-11.
81. Ling E., Feldman G., Portnoi M., Dagan R., Overweg K., Mulholland F., et al. Glycolytic enzymes associated with the cell surface of Streptococcus pneumoniae are antigenic in humans and elicit protective immune responses in the mouse. Clin Exp Immunol 2004, 138:290-298.
82. Nieves W., Heang J., Asakrah S., Honer Bentrup K., Roy C.J., Morici L.A. Immunospecific responses to bacterial elongation factor Tu during Burkholderia infection and immunization. PLoS One 2010, 5:e14361.
83. Oliveira S.C., Splitter G.A. Immunization of mice with recombinant L7/L12 ribosomal protein confers protection against Brucella abortus infection. Vaccine 1996, 14:959-962.
84. Yang X., Walters N., Robison A., Trunkle T., Pascual D.W. Nasal immunization with recombinant Brucella melitensis bp26 and trigger factor with cholera toxin reduces B. melitensis colonization. Vaccine 2007, 25:2261-2268.
85. Zhang A., Chen B., Mu X., Li R., Zheng P., Zhao Y., et al. Identification and characterization of a novel protective antigen, enolase of Streptococcus suis serotype 2. Vaccine 2009, 27:1348-1353.
86. Fernández-Arenas E., Molero G., Nombela C., Diez-Orejas R., Gil C. Low virulent strains of Candida albicans: unravelling the antigens for a future vaccine. Proteomics 2004, 4:3007-3020.
87. Fernández-Arenas E., Molero G., Nombela C., Diez-Orejas R., Gil C. Contribution of the antibodies response induced by a low virulent Candida albicans strain in protection against systemic candidiasis. Proteomics 2004, 4:1204-1215.
88. Pitarch A., Diez-Orejas R., Molero G., Pardo M., Sánchez M., Gil C., et al. Analysis of the serologic response to systemic Candida albicans infection in a murine model. Proteomics 2001, 1:550-559.
89. Macdonald I.A., Kuehn M.J. Offense and defense: microbial membrane vesicles play both ways. Res Microbiol 2012, 163:607-618.
90. McBroom A.J., Kuehn M.J. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol Microbiol 2007, 63:545-558.
91. Amano A., Takeuchi H., Furuta N. Outer membrane vesicles function as offensive weapons in host-parasite interactions. Microbes Infect 2010, 12:791-798.
92. Lee E.Y., Choi D.Y., Kim D.K., Kim J.W., Park J.O., Kim S., et al. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics 2009, 9:5425-5436.
93. Gurung M., Moon D.C., Choi C.W., Lee J.H., Bae Y.C., Kim J., et al. Staphylococcus aureus produces membrane-derived vesicles that induce host cell death. PLoS One 2011, 6:e27958.
94. Rivera J., Cordero R.J., Nakouzi A.S., Frases S., Nicola A., Casadevall A. Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. Proc Natl Acad Sci U S A 2010, 107:19002-19007.
95. Prados-Rosales R., Baena A., Martínez L.R., Luque-García J., Kalscheuer R., Veeraraghavan U., et al. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J Clin Invest 2011, 121:1471-1483.
96. Albuquerque P.C., Nakayasu E.S., Rodrigues M.L., Frases S., Casadevall A., Zancope-Oliveira R.M., et al. Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell Microbiol 2008, 10:1695-1710.
97. Oliveira D.L., Nakayasu E.S., Joffe L.S., Guimaraes A.J., Sobreira T.J., Nosanchuk J.D., et al. Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLoS One 2010, 5:e11113.
98. Rodrigues M.L., Nakayasu E.S., Oliveira D.L., Nimrichter L., Nosanchuk J.D., Almeida I.C., et al. Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot Cell 2008, 7:58-67.
99. Vallejo M.C., Nakayasu E.S., Matsuo A.L., Sobreira T.J., Longo L.V., Ganiko L., et al. Vesicle and vesicle-free extracellular proteome of Paracoccidioides brasiliensis: comparative analysis with other pathogenic fungi. J Proteome Res 2012, 11:1676-1685.
100. Dreisbach A., van der Kooi-Pol M.M., Otto A., Gronau K., Bonarius H.P., Westra H., et al. Surface shaving as a versatile tool to profile global interactions between human serum proteins and the Staphylococcus aureus cell surface. Proteomics 2011, 11:2921-2930.
101. Boleij A., Laarakkers C.M., Gloerich J., Swinkels D.W., Tjalsma H. Surface-affinity profiling to identify host-pathogen interactions. Infect Immun 2011, 79:4777-4783.