Staphylococcal adhesion and host cell invasion: Fibronectin-binding and other mechanisms

Frontiers in Microbiology

Volumn 8, Issue DEC, 2017, Pages

  Josse, Jérôme ^a   Laurent, Frédéric ^a,b,c,d   Diot, Alan ^a  

^a CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^b CROIX ROUSSE HOSPITAL   (France)

^c French National Reference Centre for Staphylococci   (France)

^d Institut des sciences pharmaceutiques et biologiques de Lyon   (France)

Author keywords

Adhesion; Cell invasion; Fibronectin binding protein; Non professional phagocytic cell; Staphylococci

Indexed keywords

CD36 ANTIGEN; CYTOCHALASIN D; FIBRONECTIN;

BACTERIUM ADHERENCE; CELL INVASION; COAGULASE NEGATIVE STAPHYLOCOCCUS; INTERNALIZATION; NONHUMAN; POLYMERASE CHAIN REACTION; SHORT SURVEY; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS; STAPHYLOCOCCUS EPIDERMIDIS; STAPHYLOCOCCUS PSEUDINTERMEDIUS;

EID: 85036669983     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.02433     Document Type: Short Survey

References (77)

1. Abel, J., Goldmann, O., Ziegler, C., Höltje, C., Smeltzer, M. S., Cheung, A. L., et al. (2011). Staphylococcus aureus evades the extracellular antimicrobial activity of mast cells by promoting its own uptake. J. Innate Immun. 3, 495-507. doi: 10.1159/000327714
2. Agerer, F., Lux, S., Michel, A., Rohde, M., Ohlsen, K., and Hauck, C. R. (2005). Cellular invasion by Staphylococcus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation. J. Cell Sci. 118(Pt 10), 2189-2200. doi: 10.1242/jcs.02328
3. Albrecht, T., Raue, S., Rosenstein, R., Nieselt, K., and Götz, F. (2012). Phylogeny of the staphylococcal major autolysin and its use in genus and species typing. J. Bacteriol. 194, 2630-2636. doi: 10.1128/JB.06609-11
4. Allignet, J., Aubert, S., Dyke, K. G., and El Solh, N. (2001). Staphylococcus caprae strains carry determinants known to be involved in pathogenicity: a gene encoding an autolysin-binding fibronectin and the ica operon involved in biofilm formation. Infect. Immun. 69, 712-718. doi: 10.1128/IAI.69.2.712-718.2001
5. Allignet, J., England, P., Old, I., and El Solh, N. (2002). Several regions of the repeat domain of the Staphylococcus caprae autolysin, Atlc, are involved in fibronectin binding. FEMS Microbiol. Lett. 213, 193-197. doi: 10.1111/j.1574-6968.2002.tb11305.x
6. Allignet, J., Galdbart, J. O., Morvan, A., Dyke, K. G., Vaudaux, P., Aubert, S., et al. (1999). Tracking adhesion factors in Staphylococcus caprae strains responsible for human bone infections following implantation of orthopaedic material. Microbiology 145(Pt 8), 2033-2042. doi: 10.1099/13500872-145-8-2033
7. Almeida, R. A., and Oliver, S. P. (2001). Interaction of coagulase-negative Staphylococcus species with bovine mammary epithelial cells. Microb. Pathog. 31, 205-212. doi: 10.1006/mpat.2001.0465
8. Aly, R., Shinefield, H. R., Litz, C., and Maibach, H. I. (1980). Role of teichoic acid in the binding of Staphylococcus aureus to nasal epithelial cells. J. Infect. Dis. 141, 463-465. doi: 10.1093/infdis/141.4.463
9. Ashraf, S., Cheng, J., and Zhao, X. (2017). Clumping factor A of Staphylococcus aureus interacts with annexinA2 on mammary epithelial cells. Sci. Rep. 7:40608. doi: 10.1038/srep40608
10. Askarian, F., Ajayi, C., Hanssen, A., van Sorge, N. M., Pettersen, I., Diep, D. B., et al. (2016). The interaction between Staphylococcus aureus sdrD and desmoglein 1 is important for adhesion to host cells. Sci. Rep. 6:22134. doi: 10.1038/srep22134
11. Askarian, F., Uchiyama, S., Valderrama, J. A., Ajayi, C., Sollid, J. U. E., van Sorge, N. M., et al. (2017). Serine-aspartate repeat protein D increases Staphylococcus aureus virulence and survival in blood. Infect. Immun. 85:e00559-16. doi: 10.1128/IAI.00559-16
12. Becker, K., Heilmann, C., and Peters, G. (2014). Coagulase-negative staphylococci. Clin. Microbiol. Rev. 27, 870-926. doi: 10.1128/CMR.00109-13
13. Bingham, R. J., Rudiño-Piñera, E., Meenan, N. A. G., Schwarz-Linek, U., Turkenburg, J. P., Höök, M., et al. (2008). Crystal structures of fibronectin-binding sites from Staphylococcus aureus FnBPA in complex with fibronectin domains. Proc. Natl. Acad. Sci. U.S.A. 105, 12254-12258. doi: 10.1073/pnas.0803556105
14. Bur, S., Preissner, K. T., Herrmann, M., and Bischoff, M. (2013). The Staphylococcus aureus extracellular adherence protein promotes bacterial internalization by keratinocytes independent of fibronectin-binding proteins. J. Invest. Dermatol. 133, 2004-2012. doi: 10.1038/jid.2013.87
15. Burke, F. M., Di Poto, A., Speziale, P., and Foster, T. J. (2011). The A domain of fibronectin-binding protein B of Staphylococcus aureus contains a novel fibronectin binding site. FEBS J. 278, 2359-2371. doi: 10.1111/j.1742-4658.2011.08159.x
16. Burke, F. M., McCormack, N., Rindi, S., Speziale, P., and Foster, T. J. (2010). Fibronectin-binding protein B variation in Staphylococcus aureus. BMC Microbiol. 10:160. doi: 10.1186/1471-2180-10-160
17. Campoccia, D., Testoni, F., Ravaioli, S., Cangini, I., Maso, A., Speziale, P., et al. (2016). Orthopedic implant infections: incompetence of Staphylococcus epidermidis, Staphylococcus lugdunensis, and Enterococcus faecalis to invade osteoblasts. J. Biomed. Mater. Res. A 104, 788-801. doi: 10.1002/jbm.a.35564
18. Christner, M., Franke, G. C., Schommer, N. N., Wendt, U., Wegert, K., Pehle, P., et al. (2010). The giant extracellular matrix-binding protein of Staphylococcus epidermidis mediates biofilm accumulation and attachment to fibronectin. Mol. Microbiol. 75, 187-207. doi: 10.1111/j.1365-2958.2009.06981.x
19. Claes, J., Liesenborghs, L., Peetermans, M., Veloso, T. R., Missiakas, D., Schneewind, O., et al. (2017). Clumping factor a, von Willebrand factor-binding protein and von Willebrand factor anchor Staphylococcus aureus to the vessel wall. J. Thromb. Haemost. 15, 1009-1019. doi: 10.1111/jth.13653
20. Corrigan, R. M., Miajlovic, H., and Foster, T. J. (2009). Surface proteins that promote adherence of Staphylococcus aureus to human desquamated nasal epithelial cells. BMC Microbiol. 9:22. doi: 10.1186/1471-2180-9-22
21. Darlow, C. A., Paidakakos, N., Sikander, M., and Atkins, B. (2017). A spinal infection with Staphylococcus pseudintermedius. BMJ Case Rep. 2017:bcr-2017-221260. doi: 10.1136/bcr-2017-221260
22. Dziewanowska, K., Carson, A. R., Patti, J. M., Deobald, C. F., Bayles, K. W., and Bohach, G. A. (2000). Staphylococcal fibronectin binding protein interacts with heat shock protein 60 and integrins: role in internalization by epithelial cells. Infect. Immun. 68, 6321-6328. doi: 10.1128/IAI.68.11.6321-6328.2000
23. Edwards, A. M., Potter, U., Meenan, N. A. G., Potts, J. R., and Massey, R. C. (2011). Staphylococcus aureus keratinocyte invasion is dependent upon multiple high-affinity fibronectin-binding repeats within FnBPA. PLOS ONE 6:e18899. doi: 10.1371/journal.pone.0018899
24. Edwards, A. M., Potts, J. R., Josefsson, E., and Massey, R. C. (2010). Staphylococcus aureus host cell invasion and virulence in sepsis is facilitated by the multiple repeats within FnBPA. PLOS Pathog. 6:e1000964. doi: 10.1371/journal.ppat.1000964
25. Eichenberger, E. M., Thaden, J. T., Sharma-Kuinkel, B., Park, L. P., Rude, T. H., Ruffin, F., et al. (2015). Polymorphisms in fibronectin binding proteins A and B among Staphylococcus aureus bloodstream isolates are not associated with arthroplasty infection. PLOS ONE 10:e0141436. doi: 10.1371/journal.pone.0141436
26. Ellington, J. K., Reilly, S. S., Ramp, W. K., Smeltzer, M. S., Kellam, J. F., and Hudson, M. C. (1999). Mechanisms of Staphylococcus aureus invasion of cultured osteoblasts. Microb. Pathog. 26, 317-323. doi: 10.1006/mpat.1999.0272
27. Foster, T. J., Geoghegan, J. A., Ganesh, V. K., and Höök, M. (2014). Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat. Rev. Microbiol. 12, 49-62. doi: 10.1038/nrmicro3161
28. Fowler, T., Johansson, S., Wary, K. K., and Höök, M. (2003). Src kinase has a central role in in vitro cellular internalization of Staphylococcus aureus. Cell. Microbiol. 5, 417-426. doi: 10.1046/j.1462-5822.2003.00290.x
29. Fowler, T., Wann, E. R., Joh, D., Johansson, S., Foster, T. J., and Höök, M. (2000). Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMS and host cell beta1 integrins. Eur. J. Cell Biol. 79, 672-679. doi: 10.1078/0171-9335-00104
30. Goldmann, O., Tuchscherr, L., Rohde, M., and Medina, E. (2016). a-hemolysin enhances Staphylococcus aureus internalization and survival within mast cells by modulating the expression of β1 integrin. Cell. Microbiol. 18, 807-819. doi: 10.1111/cmi.12550
31. Grundmeier, M., Hussain, M., Becker, P., Heilmann, C., Peters, G., and Sinha, B. (2004). Truncation of fibronectin-binding proteins in Staphylococcus aureus strain Newman leads to deficient adherence and host cell invasion due to loss of the cell wall anchor function. Infect. Immun. 72, 7155-7163. doi: 10.1128/IAI.72.12.7155-7163.2004
32. Hell, W., Meyer, H. G., and Gatermann, S. G. (1998). Cloning of aas, a gene encoding a Staphylococcus saprophyticus surface protein with adhesive and autolytic properties. Mol. Microbiol. 29, 871-881. doi: 10.1046/j.1365-2958.1998.00983.x
33. Hell, W., Reichl, S., Anders, A., and Gatermann, S. (2003). The autolytic activity of the recombinant amidase of Staphylococcus saprophyticus is inhibited by its own recombinant GW repeats. FEMS Microbiol. Lett. 227, 47-51. doi: 10.1016/S0378-1097(03)00647-5
34. Hirschhausen, N., Schlesier, T., Schmidt, M. A., Götz, F., Peters, G., and Heilmann, C. (2010). A novel staphylococcal internalization mechanism involves the major autolysin Atl and heat shock cognate protein Hsc70 as host cell receptor. Cell. Microbiol. 12, 1746-1764. doi: 10.1111/j.1462-5822.2010.01506.x
35. Hos, N. J., Rieg, S., Kern, W. K., Jonas, D., Fowler, V. G., Higgins, P. G., et al. (2015). Amino acid alterations in fibronectin binding protein a (FnBPA) and bacterial genotype are associated with cardiac device related infection in Staphylococcus aureus bacteraemia. J. Infect. 70, 153-159. doi: 10.1016/j.jinf.2014.09.005
36. Hussain, M., Haggar, A., Heilmann, C., Peters, G., Flock, J. I., and Herrmann, M. (2002). Insertional inactivation of Eap in Staphylococcus aureus strain Newman confers reduced staphylococcal binding to fibroblasts. Infect. Immun. 70, 2933-2940. doi: 10.1128/IAI.70.6.2933-2940.2002
37. Hussain, M., Steinbacher, T., Peters, G., Heilmann, C., and Becker, K. (2015). The adhesive properties of the Staphylococcus lugdunensis multifunctional autolysin AtlL and its role in biofilm formation and internalization. Int. J. Med. Microbiol. 305, 129-139. doi: 10.1016/j.ijmm.2014.11.010
38. Jönsson, K., Signäs, C., Müller, H. P., and Lindberg, M. (1991). Two different genes encode fibronectin binding proteins in Staphylococcus aureus. The complete nucleotide sequence and characterization of the second gene. Eur. J. Biochem. 202, 1041-1048. doi: 10.1111/j.1432-1033.1991.tb16468.x
39. Kerro Dego, O., van Dijk, J. E., and Nederbragt, H. (2002). Factors involved in the early pathogenesis of bovine Staphylococcus aureus mastitis with emphasis on bacterial adhesion and invasion. A review. Vet. Q. 24, 181-198. doi: 10.1080/01652176.2002.9695135
40. Kerro-Dego, O., Prysliak, T., Perez-Casal, J., and Potter, A. A. (2012). Role of GapC in the pathogenesis of Staphylococcus aureus. Vet. Microbiol. 156, 443-447. doi: 10.1016/j.vetmic.2011.11.018
41. Khalil, H., Williams, R. J., Stenbeck, G., Henderson, B., Meghji, S., and Nair, S. P. (2007). Invasion of bone cells by Staphylococcus epidermidis. Microbes Infect. 9, 460-465. doi: 10.1016/j.micinf.2007.01.002
42. Kintarak, S., Whawell, S. A., Speight, P. M., Packer, S., and Nair, S. P. (2004). Internalization of Staphylococcus aureus by human keratinocytes. Infect. Immun. 72, 5668-5675. doi: 10.1128/IAI.72.10.5668-5675.2004
43. Löffler, B., Tuchscherr, L., Niemann, S., and Peters, G. (2014). Staphylococcus aureus persistence in non-professional phagocytes. Int. J. Med. Microbiol. 304, 170-176. doi: 10.1016/j.ijmm.2013.11.011
44. Lowy, F. D. (1998). Staphylococcus aureus infections. N. Engl. J. Med. 339, 520-532. doi: 10.1056/NEJM199808203390806
45. Lozano, C., Rezusta, A., Ferrer, I., Pérez-Laguna, V., Zarazaga, M., Ruiz-Ripa, L., et al. (2017). Staphylococcus pseudintermedius human infection cases in Spain: dog-to-human transmission. Vector Borne Zoonotic Dis. 17, 268-270. doi: 10.1089/vbz.2016.2048
46. Maali, Y., Martins-Simões, P., Valour, F., Bouvard, D., Rasigade, J. P., Bes, M., et al. (2016). Pathophysiological mechanisms of Staphylococcus non-aureus bone and joint infection: interspecies homogeneity and specific behavior of S. pseudintermedius. Front. Microbiol. 7:1063. doi: 10.3389/fmicb.2016.01063
47. Malachowa, N., Kobayashi, S. D., Porter, A. D., Braughton, K. R., Scott, D. P., Gardner, D. J., et al. (2016). Contribution of Staphylococcus aureus coagulases and clumping factor A to abscess formation in a rabbit model of skin and soft tissue infection. PLOS ONE 11:e0158293. doi: 10.1371/journal.pone.0158293
48. McAdow, M., Kim, H. K., Dedent, A. C., Hendrickx, A. P. A., Schneewind, O., and Missiakas, D. M. (2011). Preventing Staphylococcus aureus sepsis through the inhibition of its agglutination in blood. PLOS Pathog. 7:e1002307. doi: 10.1371/journal.ppat.1002307
49. McDonnell, C. J., Garciarena, C. D., Watkin, R. L., McHale, T. M., McLoughlin, A., Claes, J., et al. (2016). Inhibition of major integrin αv β3 reduces Staphylococcus aureus attachment to sheared human endothelial cells. J. Thromb. Haemost. 14, 2536-2547. doi: 10.1111/jth.13501
50. Minhas, T., Ludlam, H. A., Wilks, M., and Tabaqchali, M. (1995). Detection by PCR and analysis of the distribution of a fibronectin-binding protein gene (fbn) among staphylococcal isolates. J. Med. Microbiol. 42, 96-101. doi: 10.1099/00222615-42-2-96
51. Moormeier, D. E., and Bayles, K. W. (2017). Staphylococcus aureus biofilm: a complex developmental organism. Mol. Microbiol. 104, 365-376. doi: 10.1111/mmi.13634
52. Nazarali, A., Singh, A., Moens, N. M. M., Gatineau, M., Sereda, C., Fowler, D., et al. (2015). Association between methicillin-resistant Staphylococcus pseudintermedius carriage and the development of surgical site infections following tibial plateau leveling osteotomy in dogs. J. Am. Vet. Med. Assoc. 247, 909-916. doi: 10.2460/javma.247.8.909
53. Oviedo-Boyso, J., Bravo-Patiño, A., Cajero-Juárez, M., Valdez-Alarcón, J. J., and Baizabal-Aguirre, V. M. (2009). TNF-alpha reduces the level of Staphylococcus epidermidis internalization by bovine endothelial cells. FEMS Microbiol. Lett. 292, 92-99. doi: 10.1111/j.1574-6968.2008.01469.x
54. Oviedo-Boyso, J., Cortés-Vieyra, R., Huante-Mendoza, A., Yu, H. B., Valdez-Alarcón, J. J., Bravo-Patiño, A., et al. (2011). The hosphoinositide-3-Kinase-Akt signaling pathway is important for Staphylococcus aureus internalization by endothelial cells. Infect. Immun. 79, 4569-4577. doi: 10.1128/IAI.05303-11
55. Palma, M., Haggar, A., and Flock, J. I. (1999). Adherence of Staphylococcus aureus is enhanced by an endogenous secreted protein with broad binding activity. J. Bacteriol. 181, 2840-2845
56. Pasztor, L., Ziebandt, A. K., Nega, M., Schlag, M., Haase, S., Franz-Wachtel, M., et al. (2010). Staphylococcal major autolysin (Atl) is involved in excretion of cytoplasmic proteins. J. Biol. Chem. 285, 36794-36803. doi: 10.1074/jbc.M110.167312
57. Patti, J. M., Allen, B. L., McGavin, M. J., and Höök, M. (1994). MSCRAMM-mediated adherence of microorganisms to host tissues. Annu. Rev. Microbiol. 48, 585-617. doi: 10.1146/annurev.mi.48.100194.003101
58. Peacock, S. J., Day, N. P., Thomas, M. G., Berendt, A. R., and Foster, T. J. (2000). Clinical isolates of Staphylococcus aureus exhibit diversity in fnb genes and adhesion to human fibronectin. J. Infect. 41, 23-31. doi: 10.1053/jinf.2000.0657
59. Pereira, E. M., Teixeira, C. A. A., Alvarenga, A. L. M., Schuenck, R. P., Giambiagi-Demarval, R., Holandino, C., et al. (2012). A Brazilian lineage of Staphylococcus lugdunensis presenting rough colony morphology may adhere to and invade lung epithelial cells. J. Med. Microbiol. 61(Pt 4), 463-469. doi: 10.1099/jmm.0.033001-0
60. Pietrocola, G., Gianotti, V., Richards, A., Nobile, G., Geoghegan, J. A., Rindi, S., et al. (2015). Fibronectin binding proteins SpsD and SpsL both support invasion of canine epithelial cells by Staphylococcus pseudintermedius. Infect. Immun. 83, 4093-4102. doi: 10.1128/IAI.00542-15
61. Roche, F. M., Downer, R., Keane, F., Speziale, P., Park, P. W., and Foster, T. J. (2004). The N-terminal A domain of fibronectin-binding proteins A and B promotes adhesion of Staphylococcus aureus to elastin. J. Biol. Chem. 279, 38433-38440. doi: 10.1074/jbc.M402122200
62. Schwarz-Linek, U., Werner, J. M., Pickford, A. R., Gurusiddappa, S., Kim, J. H., Pilka, E. S., et al. (2003). Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature 423, 177-181. doi: 10.1038/nature01589
63. Selbach, M., and Backert, S. (2005). Cortactin: an achilles' heel of the actin cytoskeleton targeted by pathogens. Trends Microbiol. 13, 181-189. doi: 10.1016/j.tim.2005.02.007
64. Shinji, H., Yosizawa, Y., Tajima, A., Iwase, T., Sugimoto, S., Seki, K., et al. (2011). Role of fibronectin-binding proteins A and B in in vitro cellular infections and in vivo septic infections by Staphylococcus aureus. Infect. Immun. 79, 2215-2223. doi: 10.1128/IAI.00133-11
65. Sinha, B., François, P. P., Nüsse, O., Foti, M., Hartford, O. M., Vaudaux, P., et al. (1999). Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell. Microbiol. 1, 101-117. doi: 10.1046/j.1462-5822.1999.00011.x
66. Sitkiewicz, I., Babiak, I., and Hryniewicz, W. (2011). Characterization of transcription within Sdr region of Staphylococcus aureus. Antonie Van Leeuwenhoek 99, 409-416. doi: 10.1007/s10482-010-9476-7
67. Switalski, L. M., Rydén, C., Rubin, K., Ljungh, A., Höök, M., and Wadström, T. (1983). Binding of fibronectin to Staphylococcus strains. Infect. Immun. 42, 628-633
68. Szabados, F., Kleine, B., Anders, A., Kaase, M., Sakinç, T., Schmitz, I., et al. (2008). Staphylococcus saprophyticus ATCC 15305 is internalized into human urinary bladder carcinoma cell line 5637. FEMS Microbiol. Lett. 285, 163-169. doi: 10.1111/j.1574-6968.2008.01218.x
69. Szabados, F., Marlinghaus, L., Korte, M., Neumann, S., Kaase, M., and Gatermann, S. G. (2011). Fbl is not involved in the invasion of eukaryotic epithelial and endothelial cells by Staphylococcus lugdunensis. FEMS Microbiol. Lett. 324, 48-55. doi: 10.1111/j.1574-6968.2011.02382.x
70. Testoni, F., Montanaro, L., Poggi, A., Visai, L., Campoccia, D., and Arciola, C. R. (2011). Internalization by osteoblasts of two Staphylococcus aureus clinical isolates differing in their adhesin gene pattern. Int. J. Artif. Organs 34, 789-798. doi: 10.5301/ijao.5000058
71. Tran Van Nhieu, G., and Isberg, R. R. (1993). Bacterial internalization mediated by beta 1 chain integrins is determined by ligand affinity and receptor density. EMBO J. 12, 1887-1895
72. Truong-Bolduc, Q. C., Khan, N. S., Vyas, J. M., and Hooper, D. C. (2017). Tet38 efflux pump affects Staphylococcus aureus internalization by epithelial cells through interaction with CD36 and contributes to bacterial escape from acidic and nonacidic phagolysosomes. Infect. Immun. 85:e00862-16. doi: 10.1128/IAI.00862-16
73. Valour, F., Trouillet-Assant, S., Rasigade, J. P., Lustig, S., Chanard, E., Meugnier, H., et al. (2013). Staphylococcus epidermidis in orthopedic device infections: the role of bacterial internalization in human osteoblasts and biofilm formation. PLOS ONE 8:e67240. doi: 10.1371/journal.pone.0067240
74. Wang, J. H., Zhang, K., Wang, N., Qiu, X. M., Wang, Y. B., and He, P. (2013). Involvement of phosphatidylinositol 3-kinase/Akt signaling pathway in β1 integrin-mediated internalization of Staphylococcus aureus by alveolar epithelial cells. J. Microbiol. 51, 644-650. doi: 10.1007/s12275-013-3040-x
75. Wann, E. R., Gurusiddappa, S., and Hook, M. (2000). The fibronectin-binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J. Biol. Chem. 275, 13863-13871. doi: 10.1074/jbc.275.18.13863
76. Williams, R. J., Henderson, B., Sharp, L. J., and Nair, S. P. (2002). Identification of a fibronectin-binding protein from Staphylococcus epidermidis. Infect. Immun. 70, 6805-6810. doi: 10.1128/IAI.70.12.6805-6810.2002
77. Yang, Y. H., Jiang, Y. L., Zhang, J., Wang, L., Bai, X. H., Zhang, S. J., et al. (2014). Structural insights into SraP-mediated Staphylococcus aureus adhesion to host cells. PLOS Pathog. 10:e1004169. doi: 10.1371/journal.ppat.1004169