Staphylococcus aureus proteins SSL6 and SElX interact with neutrophil receptors as identified using secretome phage display

Cellular Microbiology

Volumn 16, Issue 11, 2014, Pages 1646-1665

  Fevre, Cindy ^a   Bestebroer, Jovanka ^a   Mebius, Mirjam M ^a   de Haas, Carla J C ^a   van Strijp, Jos A G ^a   Fitzgerald, J Ross ^b   Haas, Pieter Jan A ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; BACTERIOPHAGE DNA; DNA FRAGMENT; P SELECTIN GLYCOPROTEIN LIGAND 1; PADGEM PROTEIN; SELX PROTEIN; SSL6 PROTEIN; UNCLASSIFIED DRUG; CD47 ANTIGEN; CD47 PROTEIN, HUMAN; MEMBRANE PROTEIN; P-SELECTIN LIGAND PROTEIN;

ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; NEUTROPHIL; NONHUMAN; NORMAL HUMAN; PHAGE DISPLAY; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; SECRETORY PATHWAY; STAPHYLOCOCCUS; CELL SURFACE DISPLAY; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PROCEDURES; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS AUREUS;

ANTIGENS, CD47; BACTERIAL PROTEINS; CELL SURFACE DISPLAY TECHNIQUES; HOST-PATHOGEN INTERACTIONS; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; NEUTROPHILS; STAPHYLOCOCCUS AUREUS;

EID: 84916630224     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12313     Document Type: Article

References (91)

1. Adcock, I.M., Caramori, G., and Chung, K.F. (2008) New targets for drug development in asthma. Lancet 372: 1073-1087.
2. Ahmed, A.B.F., Noguchi, K., Asami, Y., Nomura, K., Fujii, H., Sakata, M., etal. (2007) Evaluation of cell wall binding domain of Staphylococcus aureus autolysin as affinity reagent for bacteria and its application to bacterial detection. J Biosci Bioeng 104: 55-61.
3. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
4. Andre, G., Leenhouts, K., Hols, P., and Dufrêne, Y.F. (2008) Detection and localization of single LysM-peptidoglycan interactions. J Bacteriol 190: 7079-7086.
5. Antelmann, H., Tjalsma, H., Voigt, B., Ohlmeier, S., Bron, S., van Dijl, J.M., and Hecker, M. (2001) A proteomic view on genome-based signal peptide predictions. Genome Res 11: 1484-1502.
6. Baba, T., and Schneewind, O. (1996) Target cell specificity of a bacteriocin molecule: a C-terminal signal directs lysostaphin to the cell wall of Staphylococcus aureus. EMBO J 15: 4789-4797.
7. Bae, T., and Schneewind, O. (2003) The YSIRK-G/S motif of staphylococcal protein A and its role in efficiency of signal peptide processing. J Bacteriol 185: 2910-2919.
8. Bardoel, B.W., Vos, R., Bouman, T., Aerts, P.C., Bestebroer, J., Huizinga, E.G., etal. (2012) Evasion of Toll-like receptor 2 activation by staphylococcal superantigen-like protein 3. J Mol Med 90: 1109-1120.
9. Barnum, S.R. (2002) Complement in central nervous system inflammation. Immunol Res 26: 7-13.
10. Beekwilder, J., Rakonjac, J., Jongsma, M., and Bosch, D. (1999) A phagemid vector using the E. coli phage shock promoter facilitates phage display of toxic proteins. Gene 228: 23-31.
11. Beghetto, E., De Paolis, F., Montagnani, F., Cellesi, C., and Gargano, N. (2009) Discovery of new Mycoplasma pneumoniae antigens by use of a whole-genome lambda display library. Microbes Infect 11: 66-73.
12. Bendtsen, J.D., Nielsen, H., Widdick, D., Palmer, T., and Brunak, S. (2005) Prediction of twin-arginine signal peptides. BMC Bioinformatics 6: 167.
13. Bestebroer, J., Poppelier, M.J.J.G., Ulfman, L.H., Lenting, P.J., Denis, C.V., van Kessel, K.P.M., etal. (2007) Staphylococcal superantigen-like 5 binds PSGL-1 and inhibits P-selectin-mediated neutrophil rolling. Blood 109: 2936-2943.
14. Bestebroer, J., van Kessel, K.P.M., Azouagh, H., Walenkamp, A.M., Boer, I.G.J., Romijn, R.A., etal. (2009) Staphylococcal SSL5 inhibits leukocyte activation by chemokines and anaphylatoxins. Blood 113: 328-337.
15. Bjerketorp, J., Nilsson, M., Ljungh, A., Flock, J.-I., Jacobsson, K., and Frykberg, L. (2002) A novel von Willebrand factor binding protein expressed by Staphylococcus aureus. Microbiology 148: 2037-2044.
16. Bjerketorp, J., Jacobsson, K., and Frykberg, L. (2004) The von Willebrand factor-binding protein (vWbp) of Staphylococcus aureus is a coagulase. FEMS Microbiol Lett 234: 309-314.
17. Burman, J.D., Leung, E., Atkins, K.L., O'Seaghdha, M.N., Lango, L., Bernadó, P., etal. (2008) Interaction of human complement with Sbi, a staphylococcal immunoglobulin-binding protein indications of a novel mechanism of complement evasion by Staphylococcus aureus. J Biol Chem 283: 17579-17593.
18. Chung, M.-C., Popova, T.G., Millis, B.A., Mukherjee, D.V., Zhou, W., Liotta, L.A., etal. (2006) Secreted neutral metalloproteases of Bacillus anthracis as candidate pathogenic factors. J Biol Chem 281: 31408-31418.
19. Chung, M.C., Wines, B.D., Baker, H., Langley, R.J., Baker, E.N., and Fraser, J.D. (2007) The crystal structure of staphylococcal superantigen-like protein 11 in complex with sialyl Lewis X reveals the mechanism for cell binding and immune inhibition. Mol Microbiol 66: 1342-1355.
20. Dyrløv Bendtsen, J., Nielsen, H., von Heijne, G., and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
21. Emanuelsson, O., Brunak, S., von Heijne, G., and Nielsen, H. (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2: 953-971.
22. Ernst, J.D. (2000) Bacterial inhibition of phagocytosis. Cell Microbiol 2: 379-386.
23. Fraser, J.D., and Proft, T. (2008) The bacterial superantigen and superantigen-like proteins. Immunol Rev 225: 226-243.
24. Fukushima, T., Afkham, A., Kurosawa, S., Tanabe, T., Yamamoto, H., and Sekiguchi, J. (2006) A new d, l-endopeptidase gene product, YojL (renamed CwlS), plays a role in cell separation with LytE and LytF in Bacillus subtilis. J Bacteriol 188: 5541-5550.
25. Gerard, N.P., and Gerard, C. (2002) Complement in allergy and asthma. Curr Opin Immunol 14: 705-708.
26. Gravet, A., Colin, D.A., Keller, D., Girardot, R., Monteil, H., Prévost, G., and Giradot, R. (1998) Characterization of a novel structural member, LukE-LukD, of the bi-component staphylococcal leucotoxins family. FEBS Lett 436: 202-208.
27. Guillet, V., Roblin, P., Werner, S., Coraiola, M., Menestrina, G., Monteil, H., etal. (2004) Crystal structure of leucotoxin S component new insight into the staphylococcal β-barrel pore-forming toxins. J Biol Chem 279: 41028-41037.
28. Gupta, N., Tanner, S., Jaitly, N., Adkins, J.N., Lipton, M., Edwards, R., etal. (2007) Whole proteome analysis of post-translational modifications: applications of mass-spectrometry for proteogenomic annotation. Genome Res 17: 1362-1377.
29. de Haas, C.J., Veldkamp, K.E., Peschel, A., Weerkamp, F., Van Wamel, W.J., Heezius, E.C., etal. (2004) Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J Exp Med 199: 687-695.
30. Haas, P.-J., de Haas, C.J.C., Poppelier, M.J.J.C., van Kessel, K.P.M., van Strijp, J.A.G., Dijkstra, K., etal. (2005) The structure of the C5a receptor-blocking domain of chemotaxis inhibitory protein of Staphylococcus aureus is related to a group of immune evasive molecules. J Mol Biol 353: 859-872.
31. Haas, P.J., de Haas, C.J., Kleibeuker, W., Poppelier, M.J., van Kessel, K.P., Kruijtzer, J.A., etal. (2004) N-terminal residues of the chemotaxis inhibitory protein of Staphylococcus aureus are essential for blocking formylated peptide receptor but not C5a receptor. J Immunol 173: 5704-5711.
32. Harraghy, N., Hussain, M., Haggar, A., Chavakis, T., Sinha, B., Herrmann, M., and Flock, J.-I. (2003) The adhesive and immunomodulating properties of the multifunctional Staphylococcus aureus protein Eap. Microbiology 149: 2701-2707.
33. Hartleib, J., Köhler, N., Dickinson, R.B., Chhatwal, G.S., Sixma, J.J., Hartford, O.M., etal. (2000) Protein A is the von Willebrand factor binding protein on Staphylococcus aureus. Blood 96: 2149-2156.
34. Henze, U.U., and Berger-Bächi, B. (1995) Staphylococcus aureus penicillin-binding protein 4 and intrinsic beta-lactam resistance. Antimicrob Agents Chemother 39: 2415-2422.
35. Hermans, S.J., Baker, H.M., Sequeira, R.P., Langley, R.J., Baker, E.N., and Fraser, J.D. (2012) Structural and functional properties of staphylococcal superantigen-like protein 4. Infect Immun 80: 4004-4013.
36. Holtfreter, S., Kolata, J., and Bröker, B.M. (2010) Towards the immune proteome of Staphylococcus aureus - the anti-S. aureus antibody response. Int J Med Microbiol 300: 176-192.
37. Hulstein, J.J.J., Lenting, P.J., de Laat, B., Derksen, R.H.W.M., Fijnheer, R., and de Groot, P.G. (2007) β2-Glycoprotein I inhibits von Willebrand factor-dependent platelet adhesion and aggregation. Blood 110: 1483-1491.
38. Humbles, A.A., Lu, B., Nilsson, C.A., Lilly, C., Israel, E., Fujiwara, Y., etal. (2000) A role for the C3a anaphylatoxin receptor in the effector phase of asthma. Nature 406: 998-1001.
39. Itoh, S., Hamada, E., Kamoshida, G., Yokoyama, R., Takii, T., Onozaki, K., and Tsuji, T. (2010) Staphylococcal superantigen-like protein 10 (SSL10) binds to human immunoglobulin G (IgG) and inhibits complement activation via the classical pathway. Mol Immunol 47: 932-938.
40. Itoh, S., Yokoyama, R., Kamoshida, G., Fujiwara, T., Okada, H., Takii, T., etal. (2013) Staphylococcal superantigen-like protein 10 (SSL10) inhibits blood coagulation by binding to prothrombin and factor Xa via their γ-carboxyglutamic acid (Gla) domain. J Biol Chem 288: 21569-21580.
41. Jaiswal, S., Jamieson, C.H.M., Pang, W.W., Park, C.Y., Chao, M.P., Majeti, R., etal. (2009) CD47 is up-regulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 138: 271-285.
42. Jankovic, D., Collett, M.A., Lubbers, M.W., and Rakonjac, J. (2007) Direct selection and phage display of a Gram-positive secretome. Genome Biol 8: R266.
43. Jones, R.C., Deck, J., Edmondson, R.D., and Hart, M.E. (2008) Relative quantitative comparisons of the extracellular protein profiles of Staphylococcus aureus UAMS-1 and its sarA, agr, and sarA agr regulatory mutants using one-dimensional polyacrylamide gel electrophoresis and nanocapillary liquid chromatography coupled with tandem mass spectrometry. J Bacteriol 190: 5265-5278.
44. Jongerius, I., Köhl, J., Pandey, M.K., Ruyken, M., van Kessel, K.P.M., van Strijp, J.A.G., and Rooijakkers, S.H.M. (2007) Staphylococcal complement evasion by various convertase-blocking molecules. J Exp Med 204: 2461-2471.
45. Juncker, A.S., Willenbrock, H., von Heijne, G., Brunak, S., Nielsen, H., and Krogh, A. (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12: 1652-1662.
46. Kaneko, J., Ozawa, T., Tomita, T., and Kamio, Y. (1997) Sequential binding of Staphylococcal gamma-hemolysin to human erythrocytes and complex formation of the hemolysin on the cell surface. Biosci Biotechnol Biochem 61: 846-851.
47. Karlström, Å., Jacobsson, K., Flock, M., Flock, J.-I., and Guss, B. (2004) Identification of a novel collagen-like protein, SclC, in Streptococcus equi using signal sequence phage display. Vet Microbiol 104: 179-188.
48. Krebber, A., Burmester, J., and Plückthun, A. (1996) Inclusion of an upstream transcriptional terminator in phage display vectors abolishes background expression of toxic fusions with coat protein g3p. Gene 178: 71-74.
49. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E.L. (2001) Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. J Mol Biol 305: 567-580.
50. Kroh, H.K., Panizzi, P., and Bock, P.E. (2009) Von Willebrand factor-binding protein is a hysteretic conformational activator of prothrombin. Proc Natl Acad Sci USA 106: 7786-7791.
51. Laarman, A.J., Ruyken, M., Malone, C.L., van Strijp, J.A.G., Horswill, A.R., and Rooijakkers, S.H.M. (2011) Staphylococcus aureus metalloprotease aureolysin cleaves complement C3 to mediate immune evasion. J Immunol 186: 6445-6453.
52. Lambris, J.D., Dobson, N.J., and Ross, G.D. (1980) Release of endogenous C3b inactivator from lymphocytes in response to triggering membrane receptors for beta 1H globulin. J Exp Med 152: 1625-1644.
53. Langley, R., Wines, B., Willoughby, N., Basu, I., Proft, T., and Fraser, J.D. (2005) The staphylococcal superantigen-like protein 7 binds IgA and complement C5 and inhibits IgA-Fc alpha RI binding and serum killing of bacteria. J Immunol 174: 2926-2933.
54. Lee, L.Y.L., Liang, X., Höök, M., and Brown, E.L. (2004) Identification and characterization of the C3 binding domain of the Staphylococcus aureus extracellular fibrinogen-binding protein (Efb). J Biol Chem 279: 50710-50716.
55. Leversen, N.A., de Souza, G.A., Målen, H., Prasad, S., Jonassen, I., and Wiker, H.G. (2009) Evaluation of signal peptide prediction algorithms for identification of mycobacterial signal peptides using sequence data from proteomic methods. Microbiology 155: 2375-2383.
56. Lindberg, F.P., Bullard, D.C., Caver, T.E., Gresham, H.D., Beaudet, A.L., and Brown, E.J. (1996) Decreased resistance to bacterial infection and granulocyte defects in IAP-deficient mice. Science 274: 795-798.
57. Matsuo, Y., and Nishikawa, K. (1994) Prediction of the structural similarity between spermidine/putrescine-binding protein and maltose-binding protein. FEBS Lett 345: 23-26.
58. Möller, S., Croning, M.D.R., and Apweiler, R. (2001) Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17: 646-653.
59. Nickerson, N., Ip, J., Passos, D.T., and McGavin, M.J. (2010) Comparison of Staphopain A (ScpA) and B (SspB) precursor activation mechanisms reveals unique secretion kinetics of proSspB (Staphopain B), and a different interaction with its cognate Staphostatin, SspC. Mol Microbiol 75: 161-177.
60. Nielsen, H., Engelbrecht, J., Brunak, S., and von Heijne, G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10: 1-6.
61. Nugent, K.M., Huff, E., Cole, R.M., and Theodore, T.S. (1974) Cellular location of degradative enzymes in Staphylococcus aureus. J Bacteriol 120: 1012-1016.
62. Oldenborg, P.-A. (2013) CD47: a cell surface glycoprotein which regulates multiple functions of hematopoietic cells in health and disease. ISRN Hematol 2013: 614619.
63. Oldenborg, P.-A., Zheleznyak, A., Fang, Y.-F., Lagenaur, C.F., Gresham, H.D., and Lindberg, F.P. (2000) Role of CD47 as a marker of self on red blood cells. Science 288: 2051-2054.
64. Perret, M., Badiou, C., Lina, G., Burbaud, S., Benito, Y., Bes, M., etal. (2012) Cross-talk between Staphylococcus aureus leukocidins-intoxicated macrophages and lung epithelial cells triggers chemokine secretion in an inflammasome-dependent manner. Cell Microbiol 14: 1019-1036.
65. Pinho, M.G., and Errington, J. (2003) Dispersed mode of Staphylococcus aureus cell wall synthesis in the absence of the division machinery. Mol Microbiol 50: 871-881.
66. Postma, B., Poppelier, M.J., van Galen, J.C., Prossnitz, E.R., van Strijp, J.A., de Haas, C.J., and van Kessel, K.P. (2004) Chemotaxis inhibitory protein of Staphylococcus aureus binds specifically to the C5a and formylated peptide receptor. J Immunol 172: 6994-7001.
67. Prat, C., Bestebroer, J., de Haas, C.J.C., van Strijp, J.A.G., and van Kessel, K.P.M. (2006) A new staphylococcal anti-inflammatory protein that antagonizes the formyl peptide receptor-like 1. J Immunol 177: 8017-8026.
68. Prat, C., Haas, P.-J., Bestebroer, J., de Haas, C.J.C., van Strijp, J.A.G., and van Kessel, K.P.M. (2009) A homolog of formyl peptide receptor-like 1 inhibitor from Staphylococcus aureus (FLIPr-Like) that inhibits FPRL1 and FPR. J Immunol 183: 6569-6578.
69. PSORT programs for localization prediction http://www.psort.org/.
70. Pugsley, A.P. (1993) The complete general secretory pathway in gram-negative bacteria. Microbiol Rev 57: 50-108.
71. Rahman, O., Cummings, S., Harrington, D., and Sutcliffe, I. (2008) Methods for the bioinformatic identification of bacterial lipoproteins encoded in the genomes of Gram-positive bacteria. World J Microbiol Biotechnol 24: 2377-2382.
72. Ravipaty, S., and Reilly, J.P. (2010) Comprehensive characterization of methicillin-resistant Staphylococcus aureus subsp. aureus COL secretome by two-dimensional liquid chromatography and mass spectrometry. Mol Cell Proteomics 9: 1898-1919.
73. Reinhold, M.I., Green, J.M., Lindberg, F.P., Ticchioni, M., and Brown, E.J. (1999) Cell spreading distinguishes the mechanism of augmentation of T cell activation by integrin-associated protein/CD47 and CD28. Int Immunol 11: 707-718.
74. Rooijakkers, S.H.M., Ruyken, M., Roos, A., Daha, M.R., Presanis, J.S., Sim, R.B., etal. (2005) Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat Immunol 6: 920-927.
75. Rosander, A., Bjerketorp, J., Frykberg, L., and Jacobsson, K. (2002) Phage display as a novel screening method to identify extracellular proteins. J Microbiol Methods 51: 43-55.
76. Rosander, A., Frykberg, L., Ausmees, N., and Müller, P. (2003) Identification of extracytoplasmic proteins in Bradyrhizobium japonicum using phage display. Mol Plant Microbe Interact 16: 727-737.
77. Seiffert, M., Cant, C., Chen, Z., Rappold, I., Brugger, W., Kanz, L., etal. (1999) Human signal-regulatory protein is expressed on normal, but not on subsets of leukemic myeloid cells and mediates cellular adhesion involving its counterreceptor CD47. Blood 94: 3633-3643.
78. Sibbald, M.J.J.B., Ziebandt, A.K., Engelmann, S., Hecker, M., de Jong, A., Harmsen, H.J.M., etal. (2006) Mapping the pathways to staphylococcal pathogenesis by comparative secretomics. Microbiol Mol Biol Rev 70: 755-788.
79. SPdb: A Signal Peptide Database http://proline.bic.nus.edu.sg/spdb/.
80. Szurmant, H., Bu, L., Brooks, C.L., and Hoch, J.A. (2008) An essential sensor histidine kinase controlled by transmembrane helix interactions with its auxiliary proteins. Proc Natl Acad Sci USA 105: 5891-5896.
81. Tjalsma, H., Noback, M.A., Bron, S., Venema, G., Yamane, K., and van Dijl, J.M. (1997) Bacillus subtilis contains four closely related type i signal peptidases with overlapping substrate specificities constitutive and temporally controlled expression of different sip genes. J Biol Chem 272: 25983-25992.
82. Ventura, C.L., Malachowa, N., Hammer, C.H., Nardone, G.A., Robinson, M.A., Kobayashi, S.D., and DeLeo, F.R. (2010) Identification of a novel Staphylococcus aureus two-component leukotoxin using cell surface proteomics. PLoS ONE 5: e11634.
83. Wahlström, E., Vitikainen, M., Kontinen, V.P., and Sarvas, M. (2003) The extracytoplasmic folding factor PrsA is required for protein secretion only in the presence of the cell wall in Bacillus subtilis. Microbiology 149: 569-577.
84. Waldner, M.J., and Neurath, M.F. (2008) Cytokines in colitis associated cancer: potential drug targets? Inflamm Allergy Drug Targets 7: 187-194.
85. Wall, T., Roos, S., Jacobsson, K., Rosander, A., and Jonsson, H. (2003) Phage display reveals 52 novel extracellular and transmembrane proteins from Lactobacillus reuteri DSM 20016T. Microbiology 149: 3493-3505.
86. Willingham, S.B., Volkmer, J.-P., Gentles, A.J., Sahoo, D., Dalerba, P., Mitra, S.S., etal. (2012) The CD47-signal regulatory protein alpha (SIRPα) interaction is a therapeutic target for human solid tumors. Proc Natl Acad Sci USA 109: 6662-6667.
87. Wilson, G.J., Seo, K.S., Cartwright, R.A., Connelley, T., Chuang-Smith, O.N., Merriman, J.A., etal. (2011) A novel core genome-encoded superantigen contributes to lethality of community-associated MRSA necrotizing pneumonia. PLoS Pathog 7: e1002271.
88. Wines, B.D., Willoughby, N., Fraser, J.D., and Hogarth, P.M. (2006) A competitive mechanism for Staphylococcal toxin SSL7 inhibiting the leukocyte IgA receptor, Fcalpha RI, is revealed by SSL7 binding at the Calpha 2/Calpha 3 interface of IgA. J Biol Chem 281: 1389-1393.
89. Yokoyama, R., Itoh, S., Kamoshida, G., Takii, T., Fujii, S., Tsuji, T., and Onozaki, K. (2012) Staphylococcal superantigen-like protein 3 binds to the Toll-like receptor 2 extracellular domain and inhibits cytokine production induced by Staphylococcus aureus, cell wall component, or lipopeptides in murine macrophages. Infect Immun 80: 2816-2825.
90. Zhang, L., Jacobsson, K., Vasi, J., Lindberg, M., and Frykberg, L. (1998) A second IgG-binding protein in Staphylococcus aureus. Microbiology 144: 985-991.
91. Zhang, Z., and Henzel, W.J. (2004) Signal peptide prediction based on analysis of experimentally verified cleavage sites. Protein Sci 13: 2819-2824.