Leptospira Immunoglobulin-Like Protein B (LigB) Binds to Both the C-Terminal 23 Amino Acids of Fibrinogen αC Domain and Factor XIII: Insight into the Mechanism of LigB-Mediated Blockage of Fibrinogen α Chain Cross-Linking

PLoS Neglected Tropical Diseases

Volumn 10, Issue 9, 2016, Pages

  Hsieh, Ching Lin ^a   Chang, Eric ^a   Tseng, Andrew ^a   Ptak, Christopher ^a   Wu, Li Chen ^a   Su, Chun Li ^a   McDonough, Sean P ^a   Lin, Yi Pin ^b   Chang, Yung Fu ^a  

^a Cornell University ^*  (United States)

^b WADSWORTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 13; FIBRINOGEN; LEPTOSPIRA IMMUNOGLOBULIN LIKE PROTEIN B; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG; ADHESIN; BACTERIAL ANTIGEN; FIBRINOGEN ALPHAC; PEPTIDE FRAGMENT; PROTEIN BINDING; THROMBIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; DISEASE TRANSMISSION; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNE RESPONSE; NONHUMAN; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SURFACE PLASMON RESONANCE; UPREGULATION; BINDING SITE; BLOOD CLOTTING; HOST PATHOGEN INTERACTION; HUMAN; LEPTOSPIRA; LEPTOSPIROSIS; METABOLISM; MICROBIOLOGY; PATHOGENICITY;

ADHESINS, BACTERIAL; ANTIGENS, BACTERIAL; BINDING SITES; BLOOD COAGULATION; FACTOR XIII; FIBRINOGEN; HOST-PATHOGEN INTERACTIONS; HUMANS; LEPTOSPIRA; LEPTOSPIROSIS; PEPTIDE FRAGMENTS; PROTEIN BINDING; THROMBIN;

EID: 84992084129     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0004974     Document Type: Article

References (57)

1. Guerra MA, Leptospirosis: public health perspectives. Biologicals. 2013;41: 295–297. doi: 10.1016/j.biologicals.2013.06.01023850378
2. Adler B, History of leptospirosis and leptospira. Curr Top Microbiol Immunol. 2015;387: 1–9. doi: 10.1007/978-3-662-45059-8_125388129
3. Traxler RM, Callinan LS, Holman RC, Steiner C, Guerra MA, Leptospirosis-associated hospitalizations, United States, 1998–2009. Emerg Infect Dis. 2014;20: 1273–1279. doi: 10.3201/eid2008.13045025076111
4. VOELKER R, REemerging leptospirosis may be underreported in the united states. JAMA. 2014;312: 884. Available: http://dx.doi.org/10.1001/jama.2014.10414
5. Meites E, Jay MT, Deresinski S, Shieh W-J, Zaki SR, Tompkins L, et al. Reemerging Leptospirosis, California. Emerg Infect Dis. 2004;10: 406–412. doi: 10.3201/eid1003.03043115109405
6. Palaniappan RUM, Ramanujam S, Chang Y-F, Leptospirosis: pathogenesis, immunity, and diagnosis. Curr Opin Infect Dis. 2007;20: 284–29217471039
7. Faisal SM, McDonough SP, Chang YF, Leptospira: Strategies for evasion of host immunity and persistence. In: Pathogenic Spirochetes: strategies for evasion of host immunity and persistence. Springer Science and Business Media; 2012. pp. 143–172.
8. Ko AI, Goarant C, Picardeau M, Leptospira: the dawn of the molecular genetics era for an emerging zoonotic pathogen. Nat Rev Microbiol. 2009;7: 736–747. doi: 10.1038/nrmicro220819756012
9. Fernandes LG, Siqueira GH, Teixeira ARF, Silva LP, Figueredo JM, Cosate MR, et al. Leptospira spp.: Novel insights into host-pathogen interactions. Vet Immunol Immunopathol. 2016;176: 50–57. doi: 10.1016/j.vetimm.2015.12.00426727033
10. Weisel JW, Fibrinogen and fibrin. Adv Protein Chem. 2005;70: 247–299. doi: 10.1016/S0065-3233(05)70008-515837518
11. Rivera J, Vannakambadi G, Höök M, Speziale P, Fibrinogen-binding proteins of Gram-positive bacteria. Thromb Haemost. 2007;98: 503–511. doi: 10.1160/TH07-03-023317849038
12. Sun H, The Interaction Between Pathogens and the Host Coagulation System. Physiology. 2006;21: 281–288. 16868317
13. McDevitt D, Nanavaty T, House-Pompeo K, Bell E, Turner N, McIntire L, et al. Characterization of the interaction between the Staphylococcus aureus clumping factor (ClfA) and fibrinogen. Eur J Biochem. 1997;247: 416–424. 9249055
14. Liu C-Z, Shih M-H, Tsai P-J, ClfA221–550, a fibrinogen-binding segment of Staphylococcus aureus clumping factor A, disrupts fibrinogen function. Thromb Haemost. 2005;94: 286–294. doi: 10.1160/TH05-03-020516113817
15. Ponnuraj K, Bowden MG, Davis S, Gurusiddappa S, Moore D, Choe D, et al. A “dock, lock, and latch” Structural Model for a Staphylococcal Adhesin Binding to Fibrinogen. Cell. 2003;115: 217–228. doi: 10.1016/S0092-8674(03)00809-214567919
16. Pinne M, Choy HA, Haake DA, The OmpL37 surface-exposed protein is expressed by pathogenic Leptospira during infection and binds skin and vascular elastin. PLoS Negl Trop Dis. 2010;4: e815. doi: 10.1371/journal.pntd.000081520844573
17. Lin Y-P, McDonough SP, Sharma Y, Chang Y-F, Leptospira immunoglobulin-like protein B (LigB) binding to the C-terminal fibrinogen alphaC domain inhibits fibrin clot formation, platelet adhesion and aggregation. Mol Microbiol. 2011;79: 1063–1076. doi: 10.1111/j.1365-2958.2010.07510.x21219469
18. Oliveira R, Domingos RF, Siqueira GH, Fernandes LG, Souza NM, Vieira ML, et al. Adhesins of Leptospira interrogans mediate the interaction to fibrinogen and inhibit fibrin clot formation in vitro. PLoS Negl Trop Dis. 2013;7: e2396. doi: 10.1371/journal.pntd.000239624009788
19. Siqueira GH, Teixeira AF, Fernandes LG, de Souza GO, Kirchgatter K, Romero EC, et al. The recombinant LIC10508 is a plasma fibronectin, plasminogen, fibrinogen and C4BP-binding protein of Leptospira interrogans. Pathog Dis. 2016;74. pii: ftv118. doi: 10.1093/femspd/ftv118
20. Choy HA, Kelley MM, Croda J, Matsunaga J, Babbitt JT, Ko AI, et al. The Multifunctional LigB Adhesin Binds Homeostatic Proteins with Potential Roles in Cutaneous Infection by Pathogenic Leptospira interrogans. PLoS One. 2011;6: e16879. doi: 10.1371/journal.pone.001687921347378
21. Choy HA, Kelley MM, Chen TL, Moller AK, Matsunaga J, Haake DA, Physiological osmotic induction of Leptospira interrogans adhesion: LigA and LigB bind extracellular matrix proteins and fibrinogen. Infect Immun. 2007;75: 2441–2450. doi: 10.1128/IAI.01635-0617296754
22. Lin Y-P, Chang Y-F, A domain of the Leptospira LigB contributes to high affinity binding of fibronectin. Biochem Biophys Res Commun. 2007;362: 443–448. doi: 10.1016/j.bbrc.2007.07.19617707344
23. Murray GL, The molecular basis of leptospiral pathogenesis. Curr Top Microbiol Immunol. 2015;387: 139–185. doi: 10.1007/978-3-662-45059-8_725388135
24. Levett PN, Leptospirosis. Clin Microbiol Rev. 2001;14: 296–326. doi: 10.1128/CMR.14.2.296–326.200111292640
25. Taylor AJ, Paris DH, Newton PN, A Systematic Review of the Mortality from Untreated Leptospirosis. PLoS Negl Trop Dis. 2015;9: e0003866. Available: http://dx.doi.org/10.1371%2Fjournal.pntd.0003866doi: 10.1371/journal.pntd.000386626110270
26. Mosesson MW, Fibrinogen and fibrin structure and functions. J Thromb Haemost. 2005;3: 1894–1904. doi: 10.1111/j.1538-7836.2005.01365.x16102057
27. Ptak CP, Hsieh C-L, Lin Y-P, Maltsev AS, Raman R, Sharma Y, et al. NMR solution structure of the terminal immunoglobulin-like domain from the leptospira host-interacting outer membrane protein, LigB. Biochemistry. 2014;53: 5249–5260. doi: 10.1021/bi500669u25068811
28. Lin Y-P, Lee D-W, McDonough SP, Nicholson LK, Sharma Y, Chang Y-F, Repeated domains of leptospira immunoglobulin-like proteins interact with elastin and tropoelastin. J Biol Chem. 2009;284: 19380–19391. doi: 10.1074/jbc.M109.00453119473986
29. Kuo C-J, Ptak CP, Hsieh C-L, Akey BL, Chang Y-F, Elastin, a novel extracellular matrix protein adhering to mycobacterial antigen 85 complex. J Biol Chem. 2013;288: 3886–3896. doi: 10.1074/jbc.M112.41567923250738
30. Manford A, Xia T, Saxena AK, Stefan C, Hu F, Emr SD, et al. Crystal structure of the yeast Sac1: implications for its phosphoinositide phosphatase function. EMBO J. 2010;29: 1489–1498. doi: 10.1038/emboj.2010.5720389282
31. Thomer L, Schneewind O, Missiakas D, Multiple ligands of von Willebrand factor-binding protein (vWbp) promote Staphylococcus aureus clot formation in human plasma. J Biol Chem. 2013;288: 28283–28292. doi: 10.1074/jbc.M113.49312223960083
32. Burton RA, Tsurupa G, Medved L, Tjandra N, Identification of an Ordered Compact Structure within the Recombinant Bovine Fibrinogen αC-Domain Fragment by NMR. Biochemistry. 2006;45: 2257–2266. doi: 10.1021/bi052380c16475814
33. Tsurupa G, Tsonev L, Medved L, Structural organization of the fibrin(ogen) alpha C-domain. Biochemistry. 2002;41: 6449–6459. 12009908
34. Drozdetskiy A, Cole C, Procter J, Barton GJ, JPred4: a protein secondary structure prediction server. Nucleic Acids Res. 2015;43: W389–94. doi: 10.1093/nar/gkv33225883141
35. Tsurupa G, Medved L, Identification and characterization of novel tPA- and plasminogen-binding sites within fibrin(ogen) alpha C-domains. Biochemistry. 2001;40: 801–808. 11170397
36. Raman R, Ptak CP, Hsieh C-L, Oswald RE, Chang Y-F, Sharma Y, The perturbation of tryptophan fluorescence by phenylalanine to alanine mutations identifies the hydrophobic core in a subset of bacterial Ig-like domains. Biochemistry. 2013;52: 4589–4591. doi: 10.1021/bi400128r23800025
37. Tsurupa G, Pechik I, Litvinov RI, Hantgan RR, Tjandra N, Weisel JW, et al. On the mechanism of alphaC polymer formation in fibrin. Biochemistry. 2012;51: 2526–2538. doi: 10.1021/bi201784822397628
38. Muszbek L, Bereczky Z, Bagoly Z, Komáromi I, Katona É, Factor XIII: A Coagulation Factor With Multiple Plasmatic and Cellular Functions. Physiol Rev. 2011;91: 931–972. doi: 10.1152/physrev.00016.201021742792
39. Smith KA, Adamson PJ, Pease RJ, Brown JM, Balmforth AJ, Cordell PA, et al. Interactions between factor XIII and the αC region of fibrinogen. Blood. 2011;117: 3460–3468. doi: 10.1182/blood-2010-10-31360121224475
40. Muta T, Iwanaga S, The role of hemolymph coagulation in innate immunity. Curr Opin Immunol. 1996;8: 41–47. doi: 10.1016/S0952-7915(96)80103-88729445
41. Simpson-Haidaris PJ, Courtney M-A, Wright TW, Goss R, Harmsen A, Gigliotti F, Mansfield JM, Induction of Fibrinogen Expression in the Lung Epithelium during Pneumocystis carinii Pneumonia. Infect Immun. 1998;66: 4431–4439. 9712798
42. Gulati S, Gulati A, Pulmonary manifestations of leptospirosis. Lung India. 2012;29: 347–353. doi: 10.4103/0970-2113.10282223243349
43. Chavakis T, Wiechmann K, Preissner KT, Herrmann M, Staphylococcus aureus interactions with the endothelium: the role of bacterial “secretable expanded repertoire adhesive molecules” (SERAM) in disturbing host defense systems. Thromb Haemost. 2005;94: 278–285. doi: 10.1267/THRO0502027816113816
44. Wann ER, Gurusiddappa S, Hook M, The fibronectin-binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J Biol Chem. 2000;275: 13863–13871. 10788510
45. Davis SL, Gurusiddappa S, McCrea KW, Perkins S, Hook M, SdrG, a fibrinogen-binding bacterial adhesin of the microbial surface components recognizing adhesive matrix molecules subfamily from Staphylococcus epidermidis, targets the thrombin cleavage site in the Bbeta chain. J Biol Chem. 2001;276: 27799–27805. doi: 10.1074/jbc.M10387320011371571
46. Walsh EJ, Miajlovic H, Gorkun O V, Foster TJ, Identification of the Staphylococcus aureus MSCRAMM clumping factor B (ClfB) binding site in the alphaC-domain of human fibrinogen. Microbiology. 2008;154: 550–558. doi: 10.1099/mic.0.2007/010868-018227259
47. Vazquez V, Liang X, Horndahl JK, Ganesh VK, Smeds E, Foster TJ, et al. Fibrinogen is a ligand for the Staphylococcus aureus microbial surface components recognizing adhesive matrix molecules (MSCRAMM) bone sialoprotein-binding protein (Bbp). J Biol Chem. 2011;286: 29797–29805. doi: 10.1074/jbc.M110.21498121642438
48. Ko Y-P, Liang X, Smith CW, Degen JL, Hook M, Binding of Efb from Staphylococcus aureus to fibrinogen blocks neutrophil adherence. J Biol Chem. 2011;286: 9865–9874. doi: 10.1074/jbc.M110.19968721247890
49. Tennent GA, Brennan SO, Stangou AJ, O’Grady J, Hawkins PN, Pepys MB, Human plasma fibrinogen is synthesized in the liver. Blood. 2006;109: 1971–1974. 17082318
50. Kellum JA, Song M, Li J, Science review: Extracellular acidosis and the immune response: clinical and physiologic implications. Crit Care. 2004;8: 331–336. doi: 10.1186/cc290015469594
51. Gibot S, Alauzet C, Massin F, Sennoune N, Faure GC, Bene M-C, et al. Modulation of the triggering receptor expressed on myeloid cells-1 pathway during pneumonia in rats. J Infect Dis. 2006;194: 975–983. doi: 10.1086/50695016960786
52. Babich V, Knipe L, Hewlett L, Meli A, Dempster J, Hannah MJ, et al. Differential effect of extracellular acidosis on the release and dispersal of soluble and membrane proteins secreted from the Weibel-Palade body. J Biol Chem. 2009;284: 12459–12468. doi: 10.1074/jbc.M80923520019258324
53. Patronov A, Salamanova E, Dimitrov I, Flower DR, Doytchinova I, Histidine hydrogen bonding in MHC at pH 5 and pH 7 modeled by molecular docking and molecular dynamics simulations. Curr Comput Aided Drug Des. 2014;10: 41–49. 24138415
54. Bhattacharyya R, Saha RP, Samanta U, Chakrabarti P, Geometry of interaction of the histidine ring with other planar and basic residues. J Proteome Res. 2003;2: 255–263. 12814265
55. Walsh EJ, O’Brien LM, Liang X, Hook M, Foster TJ, Clumping factor B, a fibrinogen-binding MSCRAMM (microbial surface components recognizing adhesive matrix molecules) adhesin of Staphylococcus aureus, also binds to the tail region of type I cytokeratin 10. J Biol Chem. 2004;279: 50691–50699. doi: 10.1074/jbc.M40871320015385531
56. Byrnes JR, Duval C, Wang Y, Hansen CE, Ahn B, Mooberry MJ, et al. Factor XIIIa-dependent retention of red blood cells in clots is mediated by fibrin alpha-chain crosslinking. Blood. 2015;126: 1940–1948. doi: 10.1182/blood-2015-06-65226326324704
57. Fernandes LG, de Morais ZM, Vasconcellos SA, Nascimento ALTOLeptospira interrogans reduces fibrin clot formation by modulating human thrombin activity via exosite I. Pathog Dis. 2015;73. pii: ftv001. doi: 10.1093/femspd/ftv001