Interaction of Leptospira elongation factor Tu with plasminogen and complement factor H: A metabolic leptospiral protein with moonlighting activities

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Wolff, Danielly G ^a   Castiblanco Valencia, Mónica M ^b   Abe, Cecília M ^a   Monaris, Denize ^a   Morais, Zenaide M ^b   Souza, Gisele O ^b   Vasconcellos, Sílvio A ^b   Isaac, Lourdes ^b   Abreu, Patrícia A E ^a   Barbosa, Angela S ^a  

^a INSTITUTO BUTANTAN   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT FACTOR H; ELONGATION FACTOR TU; LYSINE; PLASMIN; PLASMINOGEN; PROTEIN BINDING;

ANIMAL; BLOOD CLOTTING; CHEMISTRY; ENZYMOLOGY; HOST PATHOGEN INTERACTION; IMMUNE EVASION; IMMUNOLOGY; INNATE IMMUNITY; LEPTOSPIRA; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

ANIMALS; BLOOD COAGULATION; COMPLEMENT FACTOR H; FIBRINOLYSIN; HOST-PATHOGEN INTERACTIONS; IMMUNE EVASION; IMMUNITY, INNATE; LEPTOSPIRA; LYSINE; PEPTIDE ELONGATION FACTOR TU; PLASMINOGEN; PROTEIN BINDING; PROTEIN TRANSPORT;

EID: 84894283827     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081818     Document Type: Article

References (42)

1. Henderson B, Martin A (2011) Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect Immun 79: 3476-3491. doi:10.1128/IAI. 00179-11. PubMed: 21646455.
2. Copley SD (2012) Moonlighting is mainstream: paradigm adjustment required. Bioessays 34: 578-588. doi:10.1002/bies.201100191. PubMed: 22696112.
3. Krab IM, Parmeggiani A (1998) EF-Tu, a GTPase odyssey. Biochim Biophys Acta 1443: 1-22. doi:10.1016/S0167-4781(98)00169-9. PubMed: 9838020.
4. Caldas TD, El Yaagoubi A, Richarme G (1998) Chaperone properties of bacterial elongation factor EF-Tu. J Biol Chem 273: 11478-11482. doi:10.1074/jbc.273.19.11478. PubMed: 9565560.
5. Richarme G (1998) Protein-disulfide isomerase activity of elongation factor EF-Tu. Biochem Biophys Res Commun 252: 156-161. doi: 10.1006/bbrc.1998. 9591. PubMed: 9813162.
6. Dallo SF, Kannan TR, Blaylock MW, Baseman JB (2002) Elongation factor Tu and E1 beta subunit of pyruvate dehydrogenase complex act as fibronectin binding proteins in Mycoplasma pneumoniae. Mol Microbiol 46: 1041-1051. doi:10.1046/j.1365-2958.2002.03207.x. PubMed: 12421310.
7. Granato D, Bergonzelli GE, Pridmore RD, Marvin L, Rouvet M et al. (2004) Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins. Infect Immun 72: 2160-2169. doi:10.1128/IAI.72.4.2160-2169.2004. PubMed: 15039339.
8. Kunert A, Losse J, Gruszin C, Hühn M, Kaendler K et al. (2007) Immune evasion of the human pathogen Pseudomonas aeruginosa: elongation factor Tuf is a factor H and plasminogen binding protein. J Immunol 179: 2979-2988. PubMed: 17709513.
9. Fraga TR, Barbosa AS, Isaac L (2011) Leptospirosis: aspects of innate immunity, immunopathogenesis and immune evasion from the complement system. Scand J Immunol 73: 408-419. doi:10.1111/j.1365-3083.2010.02505.x. PubMed: 21204903.
10. Vieira ML, Vasconcellos SA, Gonçales AP, de Morais ZM, Nascimento AL (2009) Plasminogen acquisition and activation at the surface of Leptospira species lead to fibronectin degradation. Infect Immun 77: 4092-4101. doi:10.1128/IAI.00353-09. PubMed: 19581392.
11. Verma A, Brissette CA, Bowman AA, Shah ST, Zipfel PF et al. (2010) Leptospiral endostatin-like protein A is a bacterial cell surface receptor for human plasminogen. Infect Immun 78: 2053-2059. doi:10.1128/IAI.01282-09. PubMed: 20160016.
12. Ponting CP, Marshall JM, Cederholm-Williams SA (1992) Plasminogen: a structural review. Blood Coagul Fibrinolysis 3: 605-614. doi: 10.1097/00001721-199210000-00012. PubMed: 1333289.
13. Barthel D, Schindler S, Zipfel PF (2012) Plasminogen is a complement inhibitor. J Biol Chem 287: 18831-18842. doi:10.1074/jbc.M111.323287. PubMed: 22451663.
14. Barthel D, Singh B, Riesbeck K, Zipfel PF (2012) Haemophilus influenzae uses the surface protein E to acquire human plasminogen and to evade innate immunity. J Immunol 188: 379-385. doi:10.4049/jimmunol.1101927. PubMed: 22124123.
15. Barbosa AS, Monaris D, Silva LB, Morais ZM, Vasconcellos SA et al. (2010) Functional characterization of LcpA, a surface-exposed protein of Leptospira spp. that binds the human complement regulator C4BP. Infect Immun 78: 3207-3216. doi:10.1128/IAI.00279-10. PubMed: 20404075.
16. Ramos CR, Abreu PA, Nascimento AL, Ho PL (2004) A high-copy T7 Escherichia coli expression vector for the production of recombinant proteins with a minimal N-terminal His-tagged fusion peptide. Braz J Med Biol Res 37: 1103-1109. PubMed: 15273812.
17. Barbosa AS, Abreu PA, Neves FO, Atzingen MV, Watanabe MM et al. (2006) A newly identified leptospiral adhesion mediates attachment to laminin. Infect Immun 74: 6356-6364. doi:10.1128/IAI.00460-06. PubMed: 16954400.
18. Castiblanco-Valencia MM, Fraga TR, Silva LB, Monaris D, Abreu PA et al. (2012) Leptospiral immunoglobulin-like proteins interact with human complement regulators factor H, FHL-1, FHR-1, and C4BP. J Infect Dis 205: 995-1004. doi:10.1093/infdis/jir875. PubMed: 22291192.
19. Pinne M, Haake DA (2009) A Comprehensive Approach to Identification of Surface-Exposed, Outer Membrane-Spanning Proteins of Leptospira interrogans. PLOS ONE 4: e6071. doi:10.1371/journal.pone.0006071. PubMed: 19562037.
20. Matsunaga J, Barocchi MA, Croda J, Young TA, Sanchez Y et al. (2003) Pathogenic Leptospira species express surface- exposed proteins belonging to the bacterial immunoglobulin superfamily. Mol Microbiol 49: 929-945. doi:10.1046/j.1365-2958.2003.03619.x. PubMed: 12890019.
21. Choy HA, Kelley MM, Chen TL, Møller AK, Matsunaga J et al. (2007) Physiological osmotic induction of Leptospira interrogans adhesion: LigA and LigB bind extracellular matrix proteins and fibrinogen. Infect Immun 75: 2441-2450. doi:10.1128/IAI.01635-06. PubMed: 17296754.
22. Lin YP, Chang YF (2007) A domain of the Leptospira LigB contributes to high affinity binding of fibronectin. Biochem Biophys Res Commun 362: 443-448. doi:10.1016/j.bbrc.2007.07.196. PubMed: 17707344.
23. Lin YP, Chang YF (2008) The C-terminal variable domain of LigB from Leptospira mediates binding to fibronectin. J Vet Sci 9: 133-144. doi: 10.4142/jvs.2008.9.2.133. PubMed: 18487934.
24. Lin YP, Raman R, Sharma Y, Chang YF (2008) Calcium binds to leptospiral immunoglobulin-like protein, LigB, and modulates fibronectin binding. J Biol Chem 283: 25140-25149. doi:10.1074/jbc.M801350200. PubMed: 18625711.
25. Lin YP, Lee DW, McDonough SP, Nicholson LK, Sharma Y et al. (2009) Repeated domains of Leptospira immunoglobulin-like proteins interact with elastin and tropoelastin. J Biol Chem 284: 19380-19391. doi:10.1074/jbc.M109. 004531. PubMed: 19473986.
26. Lin YP, Greenwood A, Nicholson LK, Sharma Y, McDonough SP et al. (2009) Fibronectin binds to and induces conformational change in a disordered region of leptospiral immunoglobulin-like protein B. J Biol Chem 284: 23547-23557. doi:10.1074/jbc.M109.031369. PubMed: 19581300.
27. Lin YP, Greenwood A, Yan W, Nicholson LK, Sharma Y et al. (2009) A novel fibronectin type III module binding motif identified on C-terminus of Leptospira immunoglobulin-like protein, LigB. Biochem Biophys Res Commun 389: 57-62. doi:10.1016/j.bbrc.2009.08.089. PubMed: 19699715.
28. Lin YP, McDonough SP, Sharma Y, Chang YF (2010) The terminal immunoglobulin-like repeats of LigA and LigB of Leptospira enhance their binding to gelatin binding domain of fibronectin and host cells. PLOS ONE 5: e11301. doi:10.1371/journal.pone.0011301. PubMed: 20585579.
29. Jeffery CJ (2003) Moonlighting proteins: old proteins learning new tricks. Trends Genet 19: 415-417. PubMed: 12902157.
30. Dallo SF, Zhang B, Denno J, Hong S, Tsai A et al. (2012) Association of Acinetobacter baumannii EF-Tu with cell surface, outer membrane vesicles, and fibronectin. Scientific. World Journal: 128705.
31. Schaumburg J, Diekmann O, Hagendorff P, Bergmann S, Rohde M et al. (2004) The cell wall subproteome of Listeria monocytogenes. Proteomics 4: 2991-3006. doi:10.1002/pmic.200400928. PubMed: 15378750.
32. Meri T, Murgia R, Stefanel P, Meri S, Cinco M (2005) Regulation of complement activation at the C3-level by serum resistant leptospires. Microb Pathog 39: 139-147. doi:10.1016/j.micpath.2005.07.003. PubMed: 16169184.
33. Barbosa AS, Abreu PA, Vasconcellos SA, Morais ZM, Gonçales AP et al. (2009) Immune evasion of Leptospira species by acquisition of human complement regulator C4BP. Infect Immun 77: 1137-1143. doi: 10.1128/IAI.01310- 08. PubMed: 19114549.
34. Vieira ML, Atzingen MV, Oliveira R, Mendes RS, Domingos RF et al. (2012) Plasminogen binding proteins and plasmin generation on the surface of Leptospira spp.: the contribution to the bacteria-host interactions. J Biomed Biotechnol, 2012: 758513. PubMed: 23118516
35. Whaley K, Ruddy S (1976) Modulation of the alternative complement pathways by beta 1 H globulin. J Exp Med 144: 1147-1163. doi: 10.1084/jem.144.5.1147. PubMed: 62817.
36. Weiler JM, Daha MR, Austen KF, Fearon DT (1976) Control of the amplification convertase of complement by the plasma protein beta1H. Proc Natl Acad Sci U S A 73: 3268-3272. doi:10.1073/pnas.73.9.3268. PubMed: 1067618.
37. Pangburn MK, Schreiber RD, Müller-Eberhard HJ (1977) Human complement C3b inactivator: isolation, characterization, and demonstration of an absolute requirement for the serum protein beta1H for cleavage of C3b and C4b in solution. J Exp Med 146: 257-270. doi: 10.1084/jem.146.1.257. PubMed: 301546.
38. Verma A, Hellwage J, Artiushin S, Zipfel PF, Kraiczy P et al. (2006) LfhA, a novel factor H-binding protein of Leptospira interrogans. Infect Immun 74: 2659-2666. doi:10.1128/IAI.74.5.2659-2666.2006. PubMed: 16622202.
39. Stevenson B, Choy HA, Pinne M, Rotondi ML, Miller MC et al. (2007) Leptospira interrogans endostatin-like outer membrane proteins bind host fibronectin, laminin and regulators of complement. PLOS ONE 2: e1188. doi:10.1371/journal.pone.0001188. PubMed: 18000555.
40. Nieves W, Heang J, Asakrah S, Höner zu Bentrup K, Roy CJ et al. (2010) Immunospecific responses to bacterial elongation factor Tu during Burkholderia infection and immunization. PLOS ONE 5: e14361. doi:10.1371/journal.pone.0014361. PubMed: 21179405.
41. Sharma J, Mishra BB, Li Q, Teale JM (2011) TLR4-dependent activation of inflammatory cytokine response in macrophages by Francisella elongation factor Tu. Cell Immunol 269: 69-73. doi:10.1016/j.cellimm.2011.03.023. PubMed: 21497800.
42. Balasubramanian S, Kannan TR, Baseman JB (2008) The surface-exposed carboxyl region of Mycoplasma pneumoniae elongation factor Tu interacts with fibronectin. Infect Immun 76: 3116-3123. doi:10.1128/IAI.00173-08. PubMed: 18411296.