An internal thioester in a pathogen surface protein mediates covalent host binding
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| internalnotes | Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica Section D, Biological Crystallography 66:213–221. doi: 10.1107/S0907444909052925. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI BLAST: a new generation of protein database search programs. Nucleic Acids Research 25:3389–3402. doi: 10. 1093/nar/25.17.3389. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Research 37:W202–W208. doi: 10.1093/nar/gkp335. Bergmann R, Nerlich A, Chhatwal GS, Nitsche-Schmitz DP. 2014. Distribution of small native plasmids in Streptococcus pyogenes in India. International Journal of Medical Microbiology 304:370–378. doi: 10.1016/j. ijmm.2013.12.001. Berrow NS, Alderton D, Sainsbury S, Nettleship J, Assenberg R, Rahman N, Stuart DI, Owens RJ. 2007. A versatile ligation-independent cloning method suitable for high-throughput expression screening applications. Nucleic Acids Research 35:e45. doi: 10.1093/nar/gkm047. Chen VB, Arendall WB III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallographica Section D, Biological Crystallography 66:12–21. doi: 10.1107/S0907444909042073. Cherry S, Silverman N. 2006. Host-pathogen interactions in drosophila: new tricks from an old friend. Nature Immunology 7:911–917. doi: 10.1038/ni1388. Clark RAF, Lanigan JM, Dellapelle P, Manseau E, Dvorak HF, Colvin RB. 1982. Fibronectin and fibrin provide a provisional matrix for epidermal-cell migration during wound reepithelialization. The Journal of Investigative Dermatology 79:264–269. doi: 10.1111/1523-1747.ep12500075. Cole C, Barber JD, Barton GJ. 2008. The Jpred 3 secondary structure prediction server. Nucleic Acids Research 36: W197–W201. doi: 10.1093/nar/gkn238. Cowtan K. 2006. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallographica Section D, Biological Crystallography 62:1002–1011. doi: 10.1107/S0907444906022116. Cowtan K. 2010. Recent developments in classical density modification. Acta Crystallographica Section D, Biological Crystallography 66:470–478. doi: 10.1107/S090744490903947X. Dodds AW, Law SKA. 1998. The phylogeny and evolution of the thioester bond-containing proteins C3, C4 and alpha(2)-macroglobulin. Immunological Reviews 166:15–26. doi: 10.1111/j.1600-065X.1998.tb01249.x. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallographica Section D, Biological Crystallography 66:486–501. doi: 10.1107/S0907444910007493. Evans PR, Murshudov GN. 2013. How good are my data and what is the resolution? Acta Crystallographica Section D, Biological Crystallography 69:1204–1214. doi: 10.1107/S0907444913000061. Ganesh VK, Rivera JJ, Smeds E, Ko Y-P, Bowden MG, Wann ER, Gurusiddappa S, Fitzgerald JR, Ho¨ ok M. 2008. ¨ A structural model of the Staphylococcus aureus ClfA-fibrinogen interaction opens new avenues for the design of anti-staphylococcal therapeutics. PLOS Pathogens 4:e1000226. doi: 10.1371/journal.ppat.1000226. Guadiz G, Sporn LA, SimpsonHaidaris PJ. 1997. Thrombin cleavage-independent deposition of fibrinogen in extracellular matrices. Blood 90:2644–2653. Haidaris PJ. 1997. Induction of fibrinogen biosynthesis and secretion from cultured pulmonary epithelial cells. Blood 89:873–882. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/ 98/NT. Nucleic Acids Symposium Series 41:95–98. Holo H, Nes IF. 1989. High-frequency transformation, by electroporation, of Lactococcus lactis subsp. cremoris grown with glycine in osmotically stabilized media. Applied and Environmental Microbiology 55:3119–3123. Janssen BJ, Christodoulidou A, McCarthy A, Lambris JD, Gros P. 2006. Structure of C3b reveals conformational changes that underlie complement activity. Nature 444:213–216. doi: 10.1038/nature05172. Kang HJ, Baker EN. 2011. Intramolecular isopeptide bonds: protein crosslinks built for stress? Trends in Biochemical Sciences 36:229–237. doi: 10.1016/j.tibs.2010.09.007. Kang HJ, Coulibaly F, Clow F, Proft T, Baker EN. 2007. Stabilizing isopeptide bonds revealed in Gram-positive bacterial pilus structure. Science 318:1625–1628. doi: 10.1126/science.1145806. Katerov V, Andreev A, Schalen C, Totolian AA. 1998. Protein F, a fibronectin-binding protein of Streptococcus pyogenes, also binds human fibrinogen: isolation of the protein and mapping of the binding region. Nature Reviews Microbiology 144:119–126. doi: 10.1099/00221287-144-1-119. Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30:3059–3066. doi: 10.1093/nar/gkf436. Kirschbaum NE, Budzynski AZ. 1990. A unique proteolytic fragment of human fibrinogen containing the A-alpha COOH-terminal domain of the native molecule. The Journal of Biological Chemistry 265:13669–13676. Kline KA, Falker S, Dahlberg S, Normark S, Henriques-Normark B. 2009. Bacterial adhesins in host-microbe interactions. Cell Host & Microbe 5:580–592. doi: 10.1016/j.chom.2009.05.011. Kos VN, Desjardins CA, Griggs A, Cerqueira G, Van Tonder A, Holden MT, Godfrey P, Palmer KL, Bodi K, Mongodin EF, Wortman J, Feldgarden M, Lawley T, Gill SR, Haas BJ, Birren B, Gilmore MS. 2012. Comparative genomics of vancomycin-resistant Staphylococcus aureus strains and their positions within the clade most commonly associated with methicillin-resistant S. aureus hospital-acquired infection in the United States. mBio 3. doi: 10.1128/mBio.00112-12. Kwon H, Squire CJ, Young PG, Baker EN. 2014. Autocatalytically generated Thr-Gln ester bond cross-links stabilize the repetitive Ig-domain shaft of a bacterial cell surface adhesin. Proceedings of the National Academy of Sciences of USA 111:1367–1372. doi: 10.1073/pnas.1316855111. Law SK, Dodds AW. 1997. The internal thioester and the covalent binding properties of the complement proteins C3 and C4. Protein Science 6:263–274. doi: 10.1002/pro.5560060201. Lawrence SO, Simpson-Haidaris PJ. 2004. Regulated de novo biosynthesis of fibrinogen in extrahepatic epithelial cells in response to inflammation. Thrombosis and Haemostasis 92:234–243. doi: 10.1267/THRO04080234. Lin M, Sutherland R, Horsfall W, Totty N, Yeo E, Nayar R, Wu XF, Schuh AC. 2002. Cell surface antigen CD109 is a novel member of the alpha(2) macroglobulin/C3, C4, C5 family of thioester-containing proteins. Blood 99: 1683–1691. doi: 10.1182/blood.V99.5.1683. Linke-Winnebeck C, Paterson NG, Young PG, Middleditch MJ, Greenwood DR, Witte G, Baker EN. 2014. Structural model for covalent adhesion of the Streptococcus pyogenes pilus through a thioester bond. The Journal of Biological Chemistry 289:177–189. doi: 10.1074/jbc.M113.523761. Liu H, Naismith JH. 2009. A simple and efficient expression and purification system using two newly constructed vectors. Protein Expression and Purification 63:102–111. doi: 10.1016/j.pep.2008.09.008. Macheboeuf P, Buffalo C, Fu CY, Zinkernagel AS, Cole JN, Johnson JE, Nizet V, Ghosh P. 2011. Streptococcal M1 protein constructs a pathological host fibrinogen network. Nature 472:64–68. doi: 10.1038/nature09967. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. Journal of Applied Crystallography 40:658–674. doi: 10.1107/S0021889807021206. Mosesson MW, Finlayson JS, Umfleet RA, Galanakis D. 1972. Human fibrinogen heterogeneities: I. Structural and related studies of plasma fibrinogens which are high solubility catabolic intermediates. The Journal of Biological Chemistry 247:5210–5219. Murshudov GN, Skubak P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, Vagin AA. 2011. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallographica Section D, Biological Crystallography 67:355–367. doi: 10.1107/S0907444911001314. Oke M, Carter LG, Johnson KA, Liu H, McMahon SA, Yan X, Kerou M, Weikart ND, Kadi N, Sheikh MA, Schmelz S, Dorward M, Zawadzki M, Cozens C, Falconer H, Powers H, Overton IM, van Niekerk CAJ, Peng X, Patel P, Garrett RA, Prangishvili D, Botting CH, Coote PJ, Dryden DT, Barton GJ, Schwarz-Linek U, Challis GL, Taylor GL, White MF, Naismith JH. 2010. The Scottish structural proteomics facility: targets, methods and outputs. Journal of Structural and Functional Genomics 11:167–180. doi: 10.1007/s10969-010-9090-y. Pereira M, Rybarczyk BJ, Odrljin TM, Hocking DC, Sottile J, Simpson-Haidaris PJ. 2002. The incorporation of fibrinogen into extracellular matrix is dependent on active assembly of a fibronectin matrix. Journal of Cell Science 115:609–617. Pizarro-Cerda J ´ , Cossart P. 2006. Bacterial adhesion and entry into host cells. Cell 124:715–727. doi: 10.1016/j. cell.2006.02.012. Pointon JA, Smith WD, Saalbach G, Crow A, Kehoe MA, Banfield MJ. 2010. A highly unusual thioester bond in a pilus adhesin is required for efficient host cell interaction. The Journal of Biological Chemistry 285: 33858–33866. doi: 10.1074/jbc.M110.149385. Que YA, Haefliger JA, Francioli P, Moreillon P. 2000. Expression of Staphylococcus aureus clumping factor A in Lactococcus lactis subsp. cremoris using a new shuttle vector. Infection and Immunity 68:3516–3522. doi: 10. 1128/IAI.68.6.3516-3522.2000. Rivera J, Vannakambadi G, Ho¨ ok M, Speziale P. 2007. Fibrinogen-binding proteins of Gram-positive bacteria. ¨ Thrombosis and Haemostasis 98:503–511. Rohde M, Graham RM, Branitzki-Heinemann K, Borchers P, Preuss C, Schleicher I, Zahner D, Talay SR, Fulde M, Dinkla K, Chhatwal GS. 2011. Differences in the aromatic domain of homologous streptococcal fibronectin-binding proteins trigger different cell invasion mechanisms and survival rates. Cellular Microbiology 13:450–468. doi: 10.1111/j.1462-5822.2010.01547.x. Schneewind O, Missiakas D. 2014. Sec-secretion and sortase-mediated anchoring of proteins in Gram-positive bacteria. Biochimica Et Biophysica Acta 1843:1687–1697. doi: 10.1016/j.bbamcr.2013.11.009. Schwarz-Linek U, Banfield MJ. 2014. Yet more intramolecular cross-links in Gram-positive surface proteins. Proceedings of the National Academy of Sciences of USA 111:1229–1230. doi: 10.1073/pnas.1322482111. Schwarz-Linek U, Ho¨ ok M, Potts JR. 2006. Fibronectin-binding proteins of gram-positive cocci. ¨ Microbes and Infection 8:2291–2298. doi: 10.1016/j.micinf.2006.03.011. Sebaihia M, Wren BW, Mullany P, Fairweather NF, Minton N, Stabler R, Thomson NR, Roberts AP, Cerdeno Tarraga AM, Wang H, Holden MT, Wright A, Churcher C, Quail MA, Baker S, Bason N, Brooks K, Chillingworth T, Cronin A, Davis P, Dowd L, Fraser A, Feltwell T, Hance Z, Holroyd S, Jagels K, Moule S, Mungall K, Price C, Rabbinowitsch E, Sharp S, Simmonds M, Stevens K, Unwin L, Whithead S, Dupuy B, Dougan G, Barrell B, Parkhill J. 2006. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nature Genetics 38:779–786. doi: 10.1038/ng1830. Snyers L, De Wit L, Content J. 1990. Glucocorticoid up-regulation of high-affinity interleukin-6 receptors on human epithelial-cells. Proceedings of the National Academy of Sciences of USA 87:2838–2842. doi: 10.1073/pnas.87.7. 2838. Sobel JH, Gawinowicz MA. 1996. Identification of the α chain lysine donor sites involved in factor XIIIa fibrin cross linking. The Journal of Biological Chemistry 271:19288–19297. doi: 10.1074/jbc.271.32.19288. Sun H. 2006. The interaction between pathogens and the host coagulation system. Nephron Physiology 21: 281–288. doi: 10.1152/physiol.00059.2005. Ugarova TP, Budzynski AZ, Shattil SJ, Ruggeri ZM, Ginsberg MH, Plow EF. 1993. Conformational-changes in fibrinogen elicited by its interaction with platelet membrane glycoprotein-GPIIb-IIIa. The Journal of Biological Chemistry 268:21080–21087. Walden M, Crow A, Nelson MD, Banfield MJ. 2014. Intramolecular isopeptide but not internal thioester bonds confer proteolytic and significant thermal stability to the S. pyogenes pilus adhesin Spy0125. Proteins 82: 517–527. doi: 10.1002/prot.24420. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS. 2011. Overview of the CCP4 suite and current developments. Acta Crystallographica Section D, Biological Crystallography 67:235–242. doi: 10.1107/S0907444910045749. Winter G. 2010. xia2: an expert system for macromolecular crystallography data reduction. Journal of Applied Crystallography 43:186–190. doi: 10.1107/S0021889809045701. Wong SG, Dessen A. 2014. Structure of a bacterial alpha(2)-macroglobulin reveals mimicry of eukaryotic innate immunity. Nature Communications 5:4917. doi: 10.1038/ncomms5917. Zakeri B, Fierer JO, Celik E, Chittock EC, Schwarz-Linek U, Moy VT, Howarth M. 2012. Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. Proceedings of the National Academy of Sciences of USA 109:E690–E697. doi: 10.1073/pnas.1115485109. |
| originalfilename | 6442-01-FH02-FSK-15-03509.jpg |
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| spelling | 12142 https://intelek.unisza.edu.my/intelek/pages/view.php?ref=12142 https://intelek.unisza.edu.my/intelek/pages/search.php?search=!collection407072 Restricted Document Article Journal UniSZA Unisza unisza image/jpeg inches 796 96 96 92 92 1425 1425x796 2015-07-14 10:55:51 6442-01-FH02-FSK-15-03509.jpg UniSZA Private Access An internal thioester in a pathogen surface protein mediates covalent host binding eLife To cause disease and persist in a host, pathogenic and commensal microbes must adhere to tissues. Colonization and infection depend on specific molecular interactions at the host-microbe interface that involve microbial surface proteins, or adhesins. To date, adhesins are only known to bind to host receptors non-covalently. Here we show that the streptococcal surface protein SfbI mediates covalent interaction with the host protein fibrinogen using an unusual internal thioester bond as a ‘chemical harpoon’. This cross-linking reaction allows bacterial attachment to fibrin and SfbI binding to human cells in a model of inflammation. Thioester-containing domains are unexpectedly prevalent in Gram-positive bacteria, including many clinically relevant pathogens. Our findings support bacterial-encoded covalent binding as a new molecular principle in host-microbe interactions. This represents an as yet unexploited target to treat bacterial infection and may also offer novel opportunities for engineering beneficial interactions. 4 1-24 Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica Section D, Biological Crystallography 66:213–221. doi: 10.1107/S0907444909052925. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI BLAST: a new generation of protein database search programs. Nucleic Acids Research 25:3389–3402. doi: 10. 1093/nar/25.17.3389. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Research 37:W202–W208. doi: 10.1093/nar/gkp335. Bergmann R, Nerlich A, Chhatwal GS, Nitsche-Schmitz DP. 2014. Distribution of small native plasmids in Streptococcus pyogenes in India. International Journal of Medical Microbiology 304:370–378. doi: 10.1016/j. ijmm.2013.12.001. Berrow NS, Alderton D, Sainsbury S, Nettleship J, Assenberg R, Rahman N, Stuart DI, Owens RJ. 2007. A versatile ligation-independent cloning method suitable for high-throughput expression screening applications. Nucleic Acids Research 35:e45. doi: 10.1093/nar/gkm047. Chen VB, Arendall WB III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallographica Section D, Biological Crystallography 66:12–21. doi: 10.1107/S0907444909042073. Cherry S, Silverman N. 2006. Host-pathogen interactions in drosophila: new tricks from an old friend. Nature Immunology 7:911–917. doi: 10.1038/ni1388. Clark RAF, Lanigan JM, Dellapelle P, Manseau E, Dvorak HF, Colvin RB. 1982. Fibronectin and fibrin provide a provisional matrix for epidermal-cell migration during wound reepithelialization. The Journal of Investigative Dermatology 79:264–269. doi: 10.1111/1523-1747.ep12500075. Cole C, Barber JD, Barton GJ. 2008. The Jpred 3 secondary structure prediction server. Nucleic Acids Research 36: W197–W201. doi: 10.1093/nar/gkn238. Cowtan K. 2006. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallographica Section D, Biological Crystallography 62:1002–1011. doi: 10.1107/S0907444906022116. Cowtan K. 2010. Recent developments in classical density modification. Acta Crystallographica Section D, Biological Crystallography 66:470–478. doi: 10.1107/S090744490903947X. Dodds AW, Law SKA. 1998. The phylogeny and evolution of the thioester bond-containing proteins C3, C4 and alpha(2)-macroglobulin. Immunological Reviews 166:15–26. doi: 10.1111/j.1600-065X.1998.tb01249.x. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallographica Section D, Biological Crystallography 66:486–501. doi: 10.1107/S0907444910007493. Evans PR, Murshudov GN. 2013. How good are my data and what is the resolution? Acta Crystallographica Section D, Biological Crystallography 69:1204–1214. doi: 10.1107/S0907444913000061. Ganesh VK, Rivera JJ, Smeds E, Ko Y-P, Bowden MG, Wann ER, Gurusiddappa S, Fitzgerald JR, Ho¨ ok M. 2008. ¨ A structural model of the Staphylococcus aureus ClfA-fibrinogen interaction opens new avenues for the design of anti-staphylococcal therapeutics. PLOS Pathogens 4:e1000226. doi: 10.1371/journal.ppat.1000226. Guadiz G, Sporn LA, SimpsonHaidaris PJ. 1997. Thrombin cleavage-independent deposition of fibrinogen in extracellular matrices. Blood 90:2644–2653. Haidaris PJ. 1997. Induction of fibrinogen biosynthesis and secretion from cultured pulmonary epithelial cells. Blood 89:873–882. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/ 98/NT. Nucleic Acids Symposium Series 41:95–98. Holo H, Nes IF. 1989. High-frequency transformation, by electroporation, of Lactococcus lactis subsp. cremoris grown with glycine in osmotically stabilized media. Applied and Environmental Microbiology 55:3119–3123. Janssen BJ, Christodoulidou A, McCarthy A, Lambris JD, Gros P. 2006. Structure of C3b reveals conformational changes that underlie complement activity. Nature 444:213–216. doi: 10.1038/nature05172. Kang HJ, Baker EN. 2011. Intramolecular isopeptide bonds: protein crosslinks built for stress? Trends in Biochemical Sciences 36:229–237. doi: 10.1016/j.tibs.2010.09.007. Kang HJ, Coulibaly F, Clow F, Proft T, Baker EN. 2007. Stabilizing isopeptide bonds revealed in Gram-positive bacterial pilus structure. Science 318:1625–1628. doi: 10.1126/science.1145806. Katerov V, Andreev A, Schalen C, Totolian AA. 1998. Protein F, a fibronectin-binding protein of Streptococcus pyogenes, also binds human fibrinogen: isolation of the protein and mapping of the binding region. Nature Reviews Microbiology 144:119–126. doi: 10.1099/00221287-144-1-119. Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30:3059–3066. doi: 10.1093/nar/gkf436. Kirschbaum NE, Budzynski AZ. 1990. A unique proteolytic fragment of human fibrinogen containing the A-alpha COOH-terminal domain of the native molecule. The Journal of Biological Chemistry 265:13669–13676. Kline KA, Falker S, Dahlberg S, Normark S, Henriques-Normark B. 2009. Bacterial adhesins in host-microbe interactions. Cell Host & Microbe 5:580–592. doi: 10.1016/j.chom.2009.05.011. Kos VN, Desjardins CA, Griggs A, Cerqueira G, Van Tonder A, Holden MT, Godfrey P, Palmer KL, Bodi K, Mongodin EF, Wortman J, Feldgarden M, Lawley T, Gill SR, Haas BJ, Birren B, Gilmore MS. 2012. Comparative genomics of vancomycin-resistant Staphylococcus aureus strains and their positions within the clade most commonly associated with methicillin-resistant S. aureus hospital-acquired infection in the United States. mBio 3. doi: 10.1128/mBio.00112-12. Kwon H, Squire CJ, Young PG, Baker EN. 2014. Autocatalytically generated Thr-Gln ester bond cross-links stabilize the repetitive Ig-domain shaft of a bacterial cell surface adhesin. Proceedings of the National Academy of Sciences of USA 111:1367–1372. doi: 10.1073/pnas.1316855111. Law SK, Dodds AW. 1997. The internal thioester and the covalent binding properties of the complement proteins C3 and C4. Protein Science 6:263–274. doi: 10.1002/pro.5560060201. Lawrence SO, Simpson-Haidaris PJ. 2004. Regulated de novo biosynthesis of fibrinogen in extrahepatic epithelial cells in response to inflammation. Thrombosis and Haemostasis 92:234–243. doi: 10.1267/THRO04080234. Lin M, Sutherland R, Horsfall W, Totty N, Yeo E, Nayar R, Wu XF, Schuh AC. 2002. Cell surface antigen CD109 is a novel member of the alpha(2) macroglobulin/C3, C4, C5 family of thioester-containing proteins. Blood 99: 1683–1691. doi: 10.1182/blood.V99.5.1683. Linke-Winnebeck C, Paterson NG, Young PG, Middleditch MJ, Greenwood DR, Witte G, Baker EN. 2014. Structural model for covalent adhesion of the Streptococcus pyogenes pilus through a thioester bond. The Journal of Biological Chemistry 289:177–189. doi: 10.1074/jbc.M113.523761. Liu H, Naismith JH. 2009. A simple and efficient expression and purification system using two newly constructed vectors. Protein Expression and Purification 63:102–111. doi: 10.1016/j.pep.2008.09.008. Macheboeuf P, Buffalo C, Fu CY, Zinkernagel AS, Cole JN, Johnson JE, Nizet V, Ghosh P. 2011. Streptococcal M1 protein constructs a pathological host fibrinogen network. Nature 472:64–68. doi: 10.1038/nature09967. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. Journal of Applied Crystallography 40:658–674. doi: 10.1107/S0021889807021206. Mosesson MW, Finlayson JS, Umfleet RA, Galanakis D. 1972. Human fibrinogen heterogeneities: I. Structural and related studies of plasma fibrinogens which are high solubility catabolic intermediates. The Journal of Biological Chemistry 247:5210–5219. Murshudov GN, Skubak P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, Vagin AA. 2011. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallographica Section D, Biological Crystallography 67:355–367. doi: 10.1107/S0907444911001314. Oke M, Carter LG, Johnson KA, Liu H, McMahon SA, Yan X, Kerou M, Weikart ND, Kadi N, Sheikh MA, Schmelz S, Dorward M, Zawadzki M, Cozens C, Falconer H, Powers H, Overton IM, van Niekerk CAJ, Peng X, Patel P, Garrett RA, Prangishvili D, Botting CH, Coote PJ, Dryden DT, Barton GJ, Schwarz-Linek U, Challis GL, Taylor GL, White MF, Naismith JH. 2010. The Scottish structural proteomics facility: targets, methods and outputs. Journal of Structural and Functional Genomics 11:167–180. doi: 10.1007/s10969-010-9090-y. Pereira M, Rybarczyk BJ, Odrljin TM, Hocking DC, Sottile J, Simpson-Haidaris PJ. 2002. The incorporation of fibrinogen into extracellular matrix is dependent on active assembly of a fibronectin matrix. Journal of Cell Science 115:609–617. Pizarro-Cerda J ´ , Cossart P. 2006. Bacterial adhesion and entry into host cells. Cell 124:715–727. doi: 10.1016/j. cell.2006.02.012. Pointon JA, Smith WD, Saalbach G, Crow A, Kehoe MA, Banfield MJ. 2010. A highly unusual thioester bond in a pilus adhesin is required for efficient host cell interaction. The Journal of Biological Chemistry 285: 33858–33866. doi: 10.1074/jbc.M110.149385. Que YA, Haefliger JA, Francioli P, Moreillon P. 2000. Expression of Staphylococcus aureus clumping factor A in Lactococcus lactis subsp. cremoris using a new shuttle vector. Infection and Immunity 68:3516–3522. doi: 10. 1128/IAI.68.6.3516-3522.2000. Rivera J, Vannakambadi G, Ho¨ ok M, Speziale P. 2007. Fibrinogen-binding proteins of Gram-positive bacteria. ¨ Thrombosis and Haemostasis 98:503–511. Rohde M, Graham RM, Branitzki-Heinemann K, Borchers P, Preuss C, Schleicher I, Zahner D, Talay SR, Fulde M, Dinkla K, Chhatwal GS. 2011. Differences in the aromatic domain of homologous streptococcal fibronectin-binding proteins trigger different cell invasion mechanisms and survival rates. Cellular Microbiology 13:450–468. doi: 10.1111/j.1462-5822.2010.01547.x. Schneewind O, Missiakas D. 2014. Sec-secretion and sortase-mediated anchoring of proteins in Gram-positive bacteria. Biochimica Et Biophysica Acta 1843:1687–1697. doi: 10.1016/j.bbamcr.2013.11.009. Schwarz-Linek U, Banfield MJ. 2014. Yet more intramolecular cross-links in Gram-positive surface proteins. Proceedings of the National Academy of Sciences of USA 111:1229–1230. doi: 10.1073/pnas.1322482111. Schwarz-Linek U, Ho¨ ok M, Potts JR. 2006. Fibronectin-binding proteins of gram-positive cocci. ¨ Microbes and Infection 8:2291–2298. doi: 10.1016/j.micinf.2006.03.011. 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| spellingShingle | An internal thioester in a pathogen surface protein mediates covalent host binding |
| summary | To cause disease and persist in a host, pathogenic and commensal microbes must adhere to tissues. Colonization and infection depend on specific molecular interactions at the host-microbe interface that involve microbial surface proteins, or adhesins. To date, adhesins are only known to bind to host receptors non-covalently. Here we show that the streptococcal surface protein SfbI mediates covalent interaction with the host protein fibrinogen using an unusual internal thioester bond as a ‘chemical harpoon’. This cross-linking reaction allows bacterial attachment to fibrin and SfbI binding to human cells in a model of inflammation. Thioester-containing domains are unexpectedly prevalent in Gram-positive bacteria, including many clinically relevant pathogens. Our findings support bacterial-encoded covalent binding as a new molecular principle in host-microbe interactions. This represents an as yet unexploited target to treat bacterial infection and may also offer novel opportunities for engineering beneficial interactions. |
| title | An internal thioester in a pathogen surface protein mediates covalent host binding |
| title_full | An internal thioester in a pathogen surface protein mediates covalent host binding |
| title_fullStr | An internal thioester in a pathogen surface protein mediates covalent host binding |
| title_full_unstemmed | An internal thioester in a pathogen surface protein mediates covalent host binding |
| title_short | An internal thioester in a pathogen surface protein mediates covalent host binding |
| title_sort | internal thioester in a pathogen surface protein mediates covalent host binding |