Stuck in the middle: Fibronectin-binding proteins in gram-positive bacteria

Frontiers in Microbiology

Volumn 7, Issue SEP, 2016, Pages

  Hymes, Jeffrey P ^a   Klaenhammer, Todd R ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Acidophilus; Fibronectin; Lactobacilli; Lactobacillus; Streptococci

Indexed keywords

FIBRONECTIN BINDING PROTEIN;

BINDING SITE; BLOODSTREAM INFECTION; CONTROLLED STUDY; DOWNSTREAM PROCESSING; ENZYME SPECIFICITY; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE PHENOTYPE CORRELATION; GRAM POSITIVE BACTERIUM; IMMUNE RESPONSE; LACTOBACILLUS ACIDOPHILUS; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SEQUENCE ANALYSIS;

EID: 84994059834     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01504     Document Type: Review

References (132)

1. Agarwal, V., Kuchipudi, A., Fulde, M., Riesbeck, K., Bergmann, S., and Blom, A. M. (2013). Streptococcus pneumoniae endopeptidase O (PepO) is a multifunctional plasminogen-and fibronectin-binding protein, facilitating evasion of innate immunity and invasion of host cells. J. Biol. Chem. 288, 6849-6863. doi: 10.1074/jbc.M112.405530
2. Altermann, E., Russell, W. M., Azcarate-Peril, M. A., Barrangou, R., Buck, B. L., McAuliffe, O., et al. (2005). Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc. Natl. Acad. Sci. U.S.A. 102, 3906-3912. doi: 10.1073/pnas.0409188102
3. Aota, S., Nomizu, M., and Yamada, K. M. (1994). The short amino acid sequence Pro-His-Ser-Arg-Asn in human fibronectin enhances cell-adhesive function. J. Biol. Chem. 269, 24756-24761.
4. 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. doi: 10.1128/JB.185.9.2910-2919.2003
5. Banyai, L., Trexler, M., Koncz, S., Gyenes, M., Sipos, G., and Patthy, L. (1990). The collagen-binding site of type-II units of bovine seminal fluid protein PDC-109 and fibronectin. Eur. J. Biochem. 193, 801-806. doi: 10.1111/j.1432-1033.1990.tb19403.x
6. Bingham, R. J., Rudino-Pinera, E., Meenan, N. A., Schwarz-Linek, U., Turkenburg, J. P., Hook, 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
7. Boekhorst, J., Wels, M., Kleerebezem, M., and Siezen, R. J. (2006). The predicted secretome of Lactobacillus plantarum WCFS1 sheds light on interactions with its environment. Microbiology 152(Pt 11), 3175-3183. doi: 10.1099/mic.0.29217-0
8. Boot, H. J., and Pouwels, P. H. (1996). Expression, secretion and antigenic variation of bacterial S-layer proteins. Mol. Microbiol. 21, 1117-1123. doi: 10.1046/j.1365-2958.1996.711442.x
9. Braun, L., Dramsi, S., Dehoux, P., Bierne, H., Lindahl, G., and Cossart, P. (1997). InlB: an invasion protein of Listeria monocytogenes with a novel type of surface association. Mol. Microbiol. 25, 285-294. doi: 10.1046/j.1365-2958.1997.4621825.x
10. Buck, B. L., Altermann, E., Svingerud, T., and Klaenhammer, T. R. (2005). Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Appl. Environ. Microbiol. 71, 8344-8351. doi: 10.1128/AEM.71.12.8344-8351.2005
11. Casillas-Ituarte, N. N., Lower, B. H., Lamlertthon, S., Fowler, V. G. Jr., and Lower, S. K. (2012). Dissociation rate constants of human fibronectin binding to fibronectin-binding proteins on living Staphylococcus aureus isolated from clinical patients. J. Biol. Chem. 287, 6693-6701. doi: 10.1074/jbc.M111.285692
12. Caswell, C. C., Oliver-Kozup, H., Han, R., Lukomska, E., and Lukomski, S. (2010). Scl1, the multifunctional adhesin of group A Streptococcus, selectively binds cellular fibronectin and laminin, and mediates pathogen internalization by human cells. FEMS Microbiol. Lett. 303, 61-68. doi: 10.1111/j.1574-6968.2009.01864.x
13. Cheng, A. G., Missiakas, D., and Schneewind, O. (2014). The giant protein Ebh is a determinant of Staphylococcus aureus cell size and complement resistance. J. Bacteriol. 196, 971-981. doi: 10.1128/JB.01366-13
14. Christie, J., McNab, R., and Jenkinson, H. F. (2002). Expression of fibronectin-binding protein FbpA modulates adhesion in Streptococcus gordonii. Microbiology 148(Pt 6), 1615-1625. doi: 10.1099/00221287-148-6-1615
15. 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
16. Clark, R. A., Quinn, J. H., Winn, H. J., Lanigan, J. M., Dellepella, P., and Colvin, R. B. (1982). Fibronectin is produced by blood vessels in response to injury. J. Exp. Med. 156, 646-651. doi: 10.1084/jem.156.2.646
17. Clarke, S. R., Harris, L. G., Richards, R. G., and Foster, S. J. (2002). Analysis of Ebh, a 1.1-megadalton cell wall-associated fibronectin-binding protein of Staphylococcus aureus. Infect. Immun. 70, 6680-6687. doi: 10.1128/IAI.70.12.6680-6687.2002
18. Colombi, M., Zoppi, N., De Petro, G., Marchina, E., Gardella, R., Tavian, D., et al. (2003). Matrix assembly induction and cell migration and invasion inhibition by a 13-amino acid fibronectin peptide. J. Biol. Chem. 278, 14346-14355. doi: 10.1074/jbc.M211997200
19. Courtney, H. S., Li, Y., Dale, J. B., and Hasty, D. L. (1994). Cloning, sequencing, and expression of a fibronectin/fibrinogen-binding protein from group A streptococci. Infect. Immun. 62, 3937-3946.
20. Cue, D., Lam, H., and Cleary, P. P. (2001). Genetic dissection of the Streptococcus pyogenes M1 protein: regions involved in fibronectin binding and intracellular invasion. Microb. Pathog. 31, 231-242. doi: 10.1006/mpat.2001.0467
21. de Greeff, A., Buys, H., Verhaar, R., Dijkstra, J., van Alphen, L., and Smith, H. E. (2002). Contribution of fibronectin-binding protein to pathogenesis of Streptococcus suis serotype 2. Infect. Immun. 70, 1319-1325. doi: 10.1128/IAI.70.3.1319-1325.2002
22. DeDent, A., Bae, T., Missiakas, D. M., and Schneewind, O. (2008). Signal peptides direct surface proteins to two distinct envelope locations of Staphylococcus aureus. EMBO J. 27, 2656-2668. doi: 10.1038/emboj.2008.185
23. Ding, L., Guo, D., and Homandberg, G. A. (2008). The cartilage chondrolytic mechanism of fibronectin fragments involves MAP kinases: comparison of three fragments and native fibronectin. Osteoarthritis Cartilage 16, 1253-1262. doi: 10.1016/j.joca.2008.02.015
24. Ding, L., Guo, D., and Homandberg, G. A. (2009). Fibronectin fragments mediate matrix metalloproteinase upregulation and cartilage damage through proline rich tyrosine kinase 2, c-src, NF-kappaB and protein kinase Cdelta. Osteoarthritis Cartilage 17, 1385-1392. doi: 10.1016/j.joca.2009.03.024
25. Dramsi, S., Bourdichon, F., Cabanes, D., Lecuit, M., Fsihi, H., and Cossart, P. (2004). FbpA, a novel multifunctional Listeria monocytogenes virulence factor. Mol. Microbiol. 53, 639-649. doi: 10.1111/j.1365-2958.2004.04138.x
26. Engvall, E., and Ruoslahti, E. (1977). Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int. J. Cancer 20, 1-5. doi: 10.1002/ijc.2910200102
27. Esgleas, M., Li, Y., Hancock, M. A., Harel, J., Dubreuil, J. D., and Gottschalk, M. (2008). Isolation and characterization of alpha-enolase, a novel fibronectin-binding protein from Streptococcus suis. Microbiology 154(Pt 9), 2668-2679. doi: 10.1099/mic.0.2008/017145-0
28. Espersen, F., and Clemmensen, I. (1982). Isolation of a fibronectin-binding protein from Staphylococcus aureus. Infect. Immun. 37, 526-531.
29. Ffrench-Constant, C. (1995). Alternative splicing of fibronectin-many different proteins but few different functions. Exp. Cell Res. 221, 261-271. doi: 10.1006/excr.1995.1374
30. Fisher, M., Huang, Y. S., Li, X., McIver, K. S., Toukoki, C., and Eichenbaum, Z. (2008). Shr is a broad-spectrum surface receptor that contributes to adherence and virulence in group A streptococcus. Infect. Immun. 76, 5006-5015. doi: 10.1128/IAI.00300-08
31. Flock, J. I., Froman, G., Jonsson, K., Guss, B., Signas, C., Nilsson, B., et al. (1987). Cloning and expression of the gene for a fibronectin-binding protein from Staphylococcus aureus. EMBO J. 6, 2351-2357.
32. Foster, T. J., Geoghegan, J. A., Ganesh, V. K., and Hook, 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
33. Frantz, C., Stewart, K. M., and Weaver, V. M. (2010). The extracellular matrix at a glance. J. Cell Sci. 123(Pt 24), 4195-4200. doi: 10.1242/jcs.023820
34. Frick, I. M., Crossin, K. L., Edelman, G. M., and Bjorck, L. (1995). Protein H-a bacterial surface protein with affinity for both immunoglobulin and fibronectin type III domains. EMBO J. 14, 1674-1679.
35. Froman, G., Switalski, L. M., Speziale, P., and Hook, M. (1987). Isolation and characterization of a fibronectin receptor from Staphylococcus aureus. J. Biol. Chem. 262, 6564-6571.
36. Geisbrecht, B. V., Hamaoka, B. Y., Perman, B., Zemla, A., and Leahy, D. J. (2005). The crystal structures of EAP domains from Staphylococcus aureus reveal an unexpected homology to bacterial superantigens. J. Biol. Chem. 280, 17243-17250. doi: 10.1074/jbc.M412311200
37. Hanenberg, H., Xiao, X. L., Dilloo, D., Hashino, K., Kato, I., and Williams, D. A. (1996). Colocalization of retrovirus and target cells on specific fibronectin fragments increases genetic transduction of mammalian cells. Nat. Med. 2, 876-882. doi: 10.1038/nm0896-876
38. Hanski, E., and Caparon, M. (1992). Protein F, a fibronectin-binding protein, is an adhesin of the group A streptococcus Streptococcus pyogenes. Proc. Natl. Acad. Sci. U.S.A. 89, 6172-6176. doi: 10.1073/pnas.89.13.6172
39. Harraghy, N., Hussain, M., Haggar, A., Chavakis, T., Sinha, B., Herrmann, M., et al. (2003). The adhesive and immunomodulating properties of the multifunctional Staphylococcus aureus protein Eap. Microbiology 149(Pt 10), 2701-2707. doi: 10.1099/mic.0.26465-0
40. Hartleib, J., Kohler, N., Dickinson, R. B., Chhatwal, G. S., Sixma, J. J., Hartford, O. M., et al. (2000). Protein A is the von Willebrand factor binding protein on Staphylococcus aureus. Blood 96, 2149-2156.
41. Hayashi, M., and Yamada, K. M. (1983). Domain structure of the carboxyl-terminal half of human plasma fibronectin. J. Biol. Chem. 258, 3332-3340.
42. Heilmann, C., Hartleib, J., Hussain, M. S., and Peters, G. (2005). The multifunctional Staphylococcus aureus autolysin aaa mediates adherence to immobilized fibrinogen and fibronectin. Infect. Immun. 73, 4793-4802. doi: 10.1128/IAI.73.8.4793-4802.2005
43. Henderson, B., Nair, S., Pallas, J., and Williams, M. A. (2011). Fibronectin: a multidomain host adhesin targeted by bacterial fibronectin-binding proteins. FEMS Microbiol. Rev. 35, 147-200. doi: 10.1111/j.1574-6976.2010.00243.x
44. Herman-Bausier, P., El-Kirat-Chatel, S., Foster, T. J., Geoghegan, J. A., and Dufrene, Y. F. (2015). Staphylococcus aureus fibronectin-binding protein A mediates cell-cell adhesion through low-affinity homophilic bonds. MBio 6, e00413-15. doi: 10.1128/mBio.00413-15
45. Heying, R., van de Gevel, J., Que, Y. A., Piroth, L., Moreillon, P., and Beekhuizen, H. (2009). Contribution of (sub)domains of Staphylococcus aureus fibronectin-binding protein to the proinflammatory and procoagulant response of human vascular endothelial cells. Thromb. Haemost. 101, 495-504.
46. Hill, C. (2012). Virulence or niche factors: what's in a name? J. Bacteriol. 194, 5725-5727. doi: 10.1128/JB.00980-12
47. Hirschhausen, N., Schlesier, T., Peters, G., and Heilmann, C. (2012). Characterization of the modular design of the autolysin/adhesin Aaa from Staphylococcus aureus. PLoS ONE 7:e40353. doi: 10.1371/journal.pone.0040353
48. Hoffmann, C., Ohlsen, K., and Hauck, C. R. (2011). Integrin-mediated uptake of fibronectin-binding bacteria. Eur. J. Cell Biol. 90, 891-896. doi: 10.1016/j.ejcb.2011.03.001
49. Holmes, A. R., McNab, R., Millsap, K. W., Rohde, M., Hammerschmidt, S., Mawdsley, J. L., et al. (2001). The pavA gene of Streptococcus pneumoniae encodes a fibronectin-binding protein that is essential for virulence. Mol. Microbiol. 41, 1395-1408. doi: 10.1046/j.1365-2958.2001.02610.x
50. Hussain, M., Becker, K., von Eiff, C., Schrenzel, J., Peters, G., and Herrmann, M. (2001). Identification and characterization of a novel 38.5-kilodalton cell surface protein of Staphylococcus aureus with extended-spectrum binding activity for extracellular matrix and plasma proteins. J. Bacteriol. 183, 6778-6786. doi: 10.1128/JB.183.23.6778-6786.2001
51. Hymes, J. P., Johnson, B. R., Barrangou, R., and Klaenhammer, T. R. (2016). Functional analysis of an S-layer-associated fibronectin-binding protein in Lactobacillus acidophilus NCFM. Appl. Environ. Microbiol. 82, 2676-2685. doi: 10.1128/AEM.00024-16
52. Hynes, R. O. (1973). Alteration of cell-surface proteins by viral transformation and by proteolysis. Proc. Natl. Acad. Sci. U.S.A. 70, 3170-3174. doi: 10.1073/pnas.70.11.3170
53. Hynes, R. O., Schwarzbauer, J. E., and Tamkun, J. W. (1987). Isolation and analysis of cDNA and genomic clones of fibronectin and its receptor. Methods Enzymol. 144, 447-463. doi: 10.1016/0076-6879(87)44194-3
54. Hyn�nen, U., and Palva, A. (2013). Lactobacillus surface layer proteins: structure, function and applications. Appl. Microbiol. Biotechnol. 97, 5225-5243. doi: 10.1007/s00253-013-4962-2
55. Hynonen, U., Westerlund-Wikstrom, B., Palva, A., and Korhonen, T. K. (2002). Identification by flagellum display of an epithelial cell-and fibronectin-binding function in the SlpA surface protein of Lactobacillus brevis. J. Bacteriol. 184, 3360-3367. doi: 10.1128/JB.184.12.3360-3367.2002
56. Ingham, K. C., Brew, S. A., Migliorini, M. M., and Busby, T. F. (1993). Binding of heparin by type III domains and peptides from the carboxy terminal hep-2 region of fibronectin. Biochemistry 32, 12548-12553. doi: 10.1021/bi00097a035
57. Jadoun, J., Ozeri, V., Burstein, E., Skutelsky, E., Hanski, E., and Sela, S. (1998). Protein F1 is required for efficient entry of Streptococcus pyogenes into epithelial cells. J. Infect. Dis. 178, 147-158. doi: 10.1086/515589
58. Jeng, A., Sakota, V., Li, Z., Datta, V., Beall, B., and Nizet, V. (2003). Molecular genetic analysis of a group A Streptococcus operon encoding serum opacity factor and a novel fibronectin-binding protein, SfbX. J. Bacteriol. 185, 1208-1217. doi: 10.1128/JB.185.4.1208-1217.2003
59. Joh, D., Wann, E. R., Kreikemeyer, B., Speziale, P., and Hook, M. (1999). Role of fibronectin-binding MSCRAMMs in bacterial adherence and entry into mammalian cells. Matrix Biol. 18, 211-223. doi: 10.1016/S0945-053X(99)00025-6
60. Joh, H. J., House-Pompeo, K., Patti, J. M., Gurusiddappa, S., and Hook, M. (1994). Fibronectin receptors from gram-positive bacteria: comparison of active sites. Biochemistry 33, 6086-6092. doi: 10.1021/bi00186a007
61. Johnson, B., Selle, K., O'Flaherty, S., Goh, Y. J., and Klaenhammer, T. (2013). Identification of extracellular surface-layer associated proteins in Lactobacillus acidophilus NCFM. Microbiology 159(Pt 11), 2269-2282. doi: 10.1099/mic.0.070755-0
62. Jonsson, K., McDevitt, D., McGavin, M. H., Patti, J. M., and Hook, M. (1995). Staphylococcus aureus expresses a major histocompatibility complex class II analog. J. Biol. Chem. 270, 21457-21460. doi: 10.1074/jbc.270.37.21457
63. Jonsson, K., Signas, C., Muller, 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
64. Katayama, S., Nozu, N., Okuda, M., Hirota, S., Yamasaki, T., and Hitsumoto, Y. (2009). Characterization of two putative fibronectin-binding proteins of Clostridium perfringens. Anaerobe 15, 155-159. doi: 10.1016/j.anaerobe.2009.03.001
65. Katayama, S., Tagomori, M., Morita, N., Yamasaki, T., Nariya, H., Okada, M., et al. (2015). Determination of the Clostridium perfringens-binding site on fibronectin. Anaerobe 34, 174-181. doi: 10.1016/j.anaerobe.2014.11.007
66. Keane, F. M., Loughman, A., Valtulina, V., Brennan, M., Speziale, P., and Foster, T. J. (2007). Fibrinogen and elastin bind to the same region within the A domain of fibronectin binding protein A, an MSCRAMM of Staphylococcus aureus. Mol. Microbiol. 63, 711-723. doi: 10.1111/j.1365-2958.2006.05552.x
67. Keski-Oja, J., Mosher, D. F., and Vaheri, A. (1977). Dimeric character of fibronectin, a major cell surface-associated glycoprotein. Biochem. Biophys. Res. Commun. 74, 699-706. doi: 10.1016/0006-291X(77)90359-X
68. Klebe, R. J. (1974). Isolation of a collagen-dependent cell attachment factor. Nature 250, 248-251. doi: 10.1038/250248a0
69. Knox, P., Crooks, S., and Rimmer, C. S. (1986). Role of fibronectin in the migration of fibroblasts into plasma clots. J. Cell Biol. 102, 2318-2323. doi: 10.1083/jcb.102.6.2318
70. Kreikemeyer, B., Oehmcke, S., Nakata, M., Hoffrogge, R., and Podbielski, A. (2004). Streptococcus pyogenes fibronectin-binding protein F2: expression profile, binding characteristics, and impact on eukaryotic cell interactions. J. Biol. Chem. 279, 15850-15859. doi: 10.1074/jbc.M313613200
71. Kuusela, P. (1978). Fibronectin binds to Staphylococcus aureus. Nature 276, 718-720. doi: 10.1038/276718a0
72. Lammers, A., Nuijten, P. J., and Smith, H. E. (1999). The fibronectin binding proteins of Staphylococcus aureus are required for adhesion to and invasion of bovine mammary gland cells. FEMS Microbiol. Lett. 180, 103-109. doi: 10.1111/j.1574-6968.1999.tb08783.x
73. Lamont, R. J. (2004). Bacterial Invasion of Host Cells. New York, NY: Cambridge University Press.
74. LaPenta, D., Rubens, C., Chi, E., and Cleary, P. P. (1994). Group A streptococci efficiently invade human respiratory epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 91, 12115-12119. doi: 10.1073/pnas.91.25.12115
75. Li, W., Wan, Y., Tao, Z., Chen, H., and Zhou, R. (2013). A novel fibronectin-binding protein of Streptococcus suis serotype 2 contributes to epithelial cell invasion and in vivo dissemination. Vet. Microbiol. 162, 186-194. doi: 10.1016/j.vetmic.2012.09.004
76. Lightfoot, Y. L., Selle, K., Yang, T., Goh, Y. J., Sahay, B., Zadeh, M., et al. (2015). SIGNR3-dependent immune regulation by Lactobacillus acidophilus surface layer protein A in colitis. EMBO J. 34, 881-895. doi: 10.15252/embj.201490296
77. Lowy, F. D. (1998). Staphylococcus aureus infections. N. Engl. J. Med. 339, 520-532. doi: 10.1056/NEJM199808203390806
78. Massey, R. C., Kantzanou, M. N., Fowler, T., Day, N. P., Schofield, K., Wann, E. R., et al. (2001). Fibronectin-binding protein A of Staphylococcus aureus has multiple, substituting, binding regions that mediate adherence to fibronectin and invasion of endothelial cells. Cell. Microbiol. 3, 839-851. doi: 10.1046/j.1462-5822.2001.00157.x
79. Matsuka, Y. V., Medved, L. V., Brew, S. A., and Ingham, K. C. (1994). The NH2-terminal fibrin-binding site of fibronectin is formed by interacting fourth and fifth finger domains. Studies with recombinant finger fragments expressed in Escherichia coli. J. Biol. Chem. 269, 9539-9546.
80. McCourt, J., O'Halloran, D. P., McCarthy, H., O'Gara, J. P., and Geoghegan, J. A. (2014). Fibronectin-binding proteins are required for biofilm formation by community-associated methicillin-resistant Staphylococcus aureus strain LAC. FEMS Microbiol. Lett. 353, 157-164. doi: 10.1111/1574-6968.12424
81. McDonald, J. A., Kelley, D. G., and Broekelmann, T. J. (1982). Role of fibronectin in collagen deposition: Fab' to the gelatin-binding domain of fibronectin inhibits both fibronectin and collagen organization in fibroblast extracellular matrix. J. Cell Biol. 92, 485-492. doi: 10.1083/jcb.92.2.485
82. Meenan, N. A., Visai, L., Valtulina, V., Schwarz-Linek, U., Norris, N. C., Gurusiddappa, S., et al. (2007). The tandem beta-zipper model defines high affinity fibronectin-binding repeats within Staphylococcus aureus FnBPA. J. Biol. Chem. 282, 25893-25902. doi: 10.1074/jbc.M703063200
83. Molinari, G., Talay, S. R., Valentin-Weigand, P., Rohde, M., and Chhatwal, G. S. (1997). The fibronectin-binding protein of Streptococcus pyogenes, SfbI, is involved in the internalization of group A streptococci by epithelial cells. Infect. Immun. 65, 1357-1363.
84. Moran, G. J., Amii, R. N., Abrahamian, F. M., and Talan, D. A. (2005). Methicillin-resistant Staphylococcus aureus in community-acquired skin infections. Emerg. Infect. Dis. 11, 928-930. doi: 10.3201/eid1106.040641
85. Mosher, D. F., and Proctor, R. A. (1980). Binding and factor XIIIa-mediated cross-linking of a 27-kilodalton fragment of fibronectin to Staphylococcus aureus. Science 209, 927-929. doi: 10.1126/science.7403857
86. Munoz-Provencio, D., Perez-Martinez, G., and Monedero, V. (2010). Characterization of a fibronectin-binding protein from Lactobacillus casei BL23. J. Appl. Microbiol. 108, 1050-1059. doi: 10.1111/j.1365-2672.2009.04508.x
87. Novokhatny, V., Schwarz, F., Atha, D., and Ingham, K. (1992). Domain structure and domain-domain interactions in the carboxy-terminal heparin binding region of fibronectin. J. Mol. Biol. 227, 1182-1191. doi: 10.1016/0022-2836(92)90530-W
88. Olsen, A. L., Sackey, B. K., Marcinkiewicz, C., Boettiger, D., and Wells, R. G. (2012). Fibronectin extra domain-A promotes hepatic stellate cell motility but not differentiation into myofibroblasts. Gastroenterology 142, 928.e3-937.e3. doi: 10.1053/j.gastro.2011.12.038
89. O'Neill, E., Pozzi, C., Houston, P., Humphreys, H., Robinson, D. A., Loughman, A., et al. (2008). A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J. Bacteriol. 190, 3835-3850. doi: 10.1128/JB.00167-08
90. Osanai, A., Li, S. J., Asano, K., Sashinami, H., Hu, D. L., and Nakane, A. (2013). Fibronectin-binding protein, FbpA, is the adhesin responsible for pathogenesis of Listeria monocytogenes infection. Microbiol. Immunol. 57, 253-262. doi: 10.1111/1348-0421.12030
91. Owens, R. J., and Baralle, F. E. (1986a). Exon structure of the collagen-binding domain of human fibronectin. FEBS Lett. 204, 318-322. doi: 10.1016/0014-5793(86)80836-5
92. Owens, R. J., and Baralle, F. E. (1986b). Mapping the collagen-binding site of human fibronectin by expression in Escherichia coli. EMBO J. 5, 2825-2830.
93. Ozeri, V., Rosenshine, I., Mosher, D. F., Fassler, R., and Hanski, E. (1998). Roles of integrins and fibronectin in the entry of Streptococcus pyogenes into cells via protein F1. Mol. Microbiol. 30, 625-637. doi: 10.1046/j.1365-2958.1998.01097.x
94. 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.
95. Pancholi, V., and Fischetti, V. A. (1992). A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J. Exp. Med. 176, 415-426. doi: 10.1084/jem.176.2.415
96. Pancholi, V., and Fischetti, V. A. (1998). alpha-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. J. Biol. Chem. 273, 14503-14515. doi: 10.1074/jbc.273.23.14503
97. Pickford, A. R., and Campbell, I. D. (2004). NMR studies of modular protein structures and their interactions. Chem. Rev. 104, 3557-3566. doi: 10.1021/cr0304018
98. Potts, J. R., and Campbell, I. D. (1994). Fibronectin structure and assembly. Curr. Opin. Cell Biol. 6, 648-655. doi: 10.1016/0955-0674(94)90090-6
99. Pracht, D., Elm, C., Gerber, J., Bergmann, S., Rohde, M., Seiler, M., et al. (2005). PavA of Streptococcus pneumoniae modulates adherence, invasion, and meningeal inflammation. Infect. Immun. 73, 2680-2689. doi: 10.1128/IAI.73.5.2680-2689.2005
100. Rakonjac, J. V., Robbins, J. C., and Fischetti, V. A. (1995). DNA sequence of the serum opacity factor of group A streptococci: identification of a fibronectin-binding repeat domain. Infect. Immun. 63, 622-631.
101. Ribet, D., and Cossart, P. (2015). How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect. 17, 173-183. doi: 10.1016/j.micinf.2015.01.004
102. Rostagno, A., Williams, M. J., Baron, M., Campbell, I. D., and Gold, L. I. (1994). Further characterization of the NH2-terminal fibrin-binding site on fibronectin. J. Biol. Chem. 269, 31938-31945.
103. Sara, M., and Sleytr, U. B. (2000). S-Layer proteins. J. Bacteriol. 182, 859-868. doi: 10.1128/JB.182.4.859-868.2000
104. Schmidt, S., and Friedl, P. (2010). Interstitial cell migration: integrin-dependent and alternative adhesion mechanisms. Cell Tissue Res. 339, 83-92. doi: 10.1007/s00441-009-0892-9
105. Schwarzbauer, J. E. (1991). Identification of the fibronectin sequences required for assembly of a fibrillar matrix. J. Cell Biol. 113, 1463-1473. doi: 10.1083/jcb.113.6.1463
106. Schwarzbauer, J. E., Tamkun, J. W., Lemischka, I. R., and Hynes, R. O. (1983). Three different fibronectin mRNAs arise by alternative splicing within the coding region. Cell 35(2 Pt 1), 421-431. doi: 10.1016/0092-8674(83)90175-7
107. Schwarz-Linek, U., Pilka, E. S., Pickford, A. R., Kim, J. H., Hook, M., Campbell, I. D., et al. (2004). High affinity streptococcal binding to human fibronectin requires specific recognition of sequential F1 modules. J. Biol. Chem. 279, 39017-39025. doi: 10.1074/jbc.M405083200
108. 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/nature0189
109. Sela, S., Aviv, A., Tovi, A., Burstein, I., Caparon, M. G., and Hanski, E. (1993). Protein F: an adhesin of Streptococcus pyogenes binds fibronectin via two distinct domains. Mol. Microbiol. 10, 1049-1055. doi: 10.1111/j.1365-2958.1993.tb00975.x
110. Signas, C., Raucci, G., Jonsson, K., Lindgren, P. E., Anantharamaiah, G. M., Hook, M., et al. (1989). Nucleotide sequence of the gene for a fibronectin-binding protein from Staphylococcus aureus: use of this peptide sequence in the synthesis of biologically active peptides. Proc. Natl. Acad. Sci. U.S.A. 86, 699-703. doi: 10.1073/pnas.86.2.699
111. Sinha, B., Francois, P., Que, Y. A., Hussain, M., Heilmann, C., Moreillon, P., et al. (2000). Heterologously expressed Staphylococcus aureus fibronectin-binding proteins are sufficient for invasion of host cells. Infect. Immun. 68, 6871-6878. doi: 10.1128/IAI.68.12.6871-6878.2000
112. Sinha, B., Francois, P. P., Nusse, 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
113. Sottile, J., and Hocking, D. C. (2002). Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions. Mol. Biol. Cell 13, 3546-3559. doi: 10.1091/mbc.E02-01-0048
114. Sottile, J., Schwarzbauer, J., Selegue, J., and Mosher, D. F. (1991). Five type I modules of fibronectin form a functional unit that binds to fibroblasts and Staphylococcus aureus. J. Biol. Chem. 266, 12840-12843.
115. Spitzfaden, C., Grant, R. P., Mardon, H. J., and Campbell, I. D. (1997). Module-module interactions in the cell binding region of fibronectin: stability, flexibility and specificity. J. Mol. Biol. 265, 565-579. doi: 10.1006/jmbi.1996.0736
116. Stones, D. H., and Krachler, A. M. (2015). Fatal attraction: how bacterial adhesins affect host signaling and what we can learn from them. Int. J. Mol. Sci. 16, 2626-2640. doi: 10.3390/ijms16022626
117. Talay, S. R., Ehrenfeld, E., Chhatwal, G. S., and Timmis, K. N. (1991). Expression of the fibronectin-binding components of Streptococcus pyogenes in Escherichia coli demonstrates that they are proteins. Mol. Microbiol. 5, 1727-1734. doi: 10.1111/j.1365-2958.1991.tb01921.x
118. Tamkun, J. W., DeSimone, D. W., Fonda, D., Patel, R. S., Buck, C., Horwitz, A. F., et al. (1986). Structure of integrin, a glycoprotein involved in the transmembrane linkage between fibronectin and actin. Cell 46, 271-282. doi: 10.1016/0092-8674(86)90744-0
119. Terao, Y., Kawabata, S., Nakata, M., Nakagawa, I., and Hamada, S. (2002). Molecular characterization of a novel fibronectin-binding protein of Streptococcus pyogenes strains isolated from toxic shock-like syndrome patients. J. Biol. Chem. 277, 47428-47435. doi: 10.1074/jbc.M209133200
120. Tomasini-Johansson, B. R., Kaufman, N. R., Ensenberger, M. G., Ozeri, V., Hanski, E., and Mosher, D. F. (2001). A 49-residue peptide from adhesin F1 of Streptococcus pyogenes inhibits fibronectin matrix assembly. J. Biol. Chem. 276, 23430-23439. doi: 10.1074/jbc.M103467200
121. Tong, S. Y., Davis, J. S., Eichenberger, E., Holland, T. L., and Fowler, V. G. Jr (2015). Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin. Microbiol. Rev. 28, 603-661. doi: 10.1128/CMR.00134-14
122. Tressel, T., McCarthy, J. B., Calaycay, J., Lee, T. D., Legesse, K., Shively, J. E., et al. (1991). Human plasma fibronectin. Demonstration of structural differences between the A-and B-chains in the III CS region. Biochem. J. 274(Pt 3), 731-738. doi: 10.1042/bj2740731
123. Trial, J., Rossen, R. D., Rubio, J., and Knowlton, A. A. (2004a). Inflammation and ischemia: macrophages activated by fibronectin fragments enhance the survival of injured cardiac myocytes. Exp. Biol. Med. (Maywood) 229, 538-545.
124. Trial, J., Rubio, J. A., Birdsall, H. H., Rodriguez-Barradas, M., and Rossen, R. D. (2004b). Monocyte activation by circulating fibronectin fragments in HIV-1-infected patients. J. Immunol. 173, 2190-2198. doi: 10.4049/jimmunol.173.3.2190
125. Vakonakis, I., Staunton, D., Ellis, I. R., Sarkies, P., Flanagan, A., Schor, A. M., et al. (2009). Motogenic sites in human fibronectin are masked by long range interactions. J. Biol. Chem. 284, 15668-15675. doi: 10.1074/jbc.M109.003673
126. Velez, M. P., De Keersmaecker, S. C., and Vanderleyden, J. (2007). Adherence factors of Lactobacillus in the human gastrointestinal tract. FEMS Microbiol. Lett. 276, 140-148. doi: 10.1111/j.1574-6968.2007.00908.x
127. Walia, B., Castaneda, F. E., Wang, L., Kolachala, V. L., Bajaj, R., Roman, J., et al. (2004). Polarized fibronectin secretion induced by adenosine regulates bacterial-epithelial interaction in human intestinal epithelial cells. Biochem. J. 382(Pt 2), 589-596. doi: 10.1042/BJ20040021
128. 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
129. Williams, M. J., Phan, I., Harvey, T. S., Rostagno, A., Gold, L. I., and Campbell, I. D. (1994). Solution structure of a pair of fibronectin type 1 modules with fibrin binding activity. J. Mol. Biol. 235, 1302-1311. doi: 10.1006/jmbi.1994.1083
130. Wilson, C. L., and Schwarzbauer, J. E. (1992). The alternatively spliced V region contributes to the differential incorporation of plasma and cellular fibronectins into fibrin clots. J. Cell Biol. 119, 923-933. doi: 10.1083/jcb.119.4.923
131. Wisplinghoff, H., Bischoff, T., Tallent, S. M., Seifert, H., Wenzel, R. P., and Edmond, M. B. (2004). Nosocomial bloodstream infections in US hospitals: analysis of 24, 179 cases from a prospective nationwide surveillance study. Clin. Infect. Dis. 39, 309-317. doi: 10.1086/421946
132. Woods, A., Couchman, J. R., Johansson, S., and Hook, M. (1986). Adhesion and cytoskeletal organisation of fibroblasts in response to fibronectin fragments. EMBO J. 5, 665-670.