Pseudomonas aeruginosa uses Dihydrolipoamide dehydrogenase (Lpd) to bind to the human terminal pathway regulators vitronectin and clusterin to inhibit terminal pathway complement attack

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Hallström, Teresia ^a   Uhde, Melanie ^a   Singh, Birendra ^b   Skerka, Christine ^a   Riesbeck, Kristian ^b   Zipfel, Peter F ^a,c  

^a HANS KNÖLL INSTITUTE   (Germany)

^b LUND UNIVERSITY   (Sweden)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CLUSTERIN; COMPLEMENT MEMBRANE ATTACK COMPLEX; DIHYDROLIPOAMIDE DEHYDROGENASE; MONOCLONAL ANTIBODY; VITRONECTIN; BACTERIAL PROTEIN; CLU PROTEIN, HUMAN; PROTEIN BINDING;

ARTICLE; BACTERIAL METABOLISM; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL DAMAGE; COMPLEMENT ACTIVATION; COMPLEMENT DEPOSITION; COMPLEMENT INHIBITION; COMPLEMENT SYSTEM; CONTROLLED STUDY; HOST PATHOGEN INTERACTION; HUMAN; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; ENZYMOLOGY; GENETICS; METABOLISM; MICROBIAL VIABILITY; PROTEIN TERTIARY STRUCTURE;

BACTERIAL PROTEINS; CLUSTERIN; COMPLEMENT ACTIVATION; COMPLEMENT MEMBRANE ATTACK COMPLEX; DIHYDROLIPOAMIDE DEHYDROGENASE; HUMANS; MICROBIAL VIABILITY; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; VITRONECTIN;

EID: 84947460665     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137630     Document Type: Article

References (51)

1. Pier GB, Ramphal R. Pseudomonas aeruginosa. 6th ed. New York: Churchill Livingstone; 2005.
2. Hassett DJ, Korfhagen TR, Irvin RT, Schurr MJ, Sauer K, Lau GW, et al. Pseudomonas aeruginosa biofilm infections in cystic fibrosis: insights into pathogenic processes and treatment strategies. Expert Opin Ther Targets. 2010; 14: 117-130. doi: 10.1517/14728220903454988 PMID: 20055712
3. Sadikot RT, Blackwell TS, Christman JW, Prince AS. Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am J Respir Crit Care Med. 2005; 171: 1209-1223. PMID: 15695491
4. Fujitani S, Sun H-Y, Yu VL, Weingarten JA. Pneumonia due to Pseudomonas aeruginosa: part I: epidemiology, clinical diagnosis, and source. Chest. 2011; 139: 909-919. doi: 10.1378/chest.10-0166 PMID: 21467058
5. Chastre J, Fagon J-Y. Ventilator-associated pneumonia. Am J Respir Crit Care Med. 2002; 165: 867-903. doi: 10.1164/ajrccm.165.7.2105078 PMID: 11934711
6. Laarman AJ, Bardoel BW, Ruyken M, Fernie J, Milder FJ, van Strijp JAG, et al. Pseudomonas aeruginosa alkaline protease blocks complement activation via the classical and lectin pathways. J Immunol. 2012; 188: 386-393. doi: 10.4049/jimmunol.1102162 PMID: 22131330
7. Schiller NL, Joiner KA. Interaction of complement with serum-sensitive and serum-resistant strains of Pseudomonas aeruginosa. Infect Immun. 1986; 54: 689-694. PMID: 3096887
8. Engels W, Endert J, Van Boven CP. A quantitative method for assessing the third complement factor (C3) attached to the surface of opsonized Pseudomonas aeruginosa: interrelationship between C3 fixation, phagocytosis and complement consumption. J Immunol Methods. 1985; 81: 43-53. PMID: 3926902
9. Hallström T, Mörgelin M, Barthel D, Raguse M, Kunert A, Hoffmann R, et al. Dihydrolipoamide dehydrogenase of Pseudomonas aeruginosa is a surface-exposed immune evasion protein that binds three members of the factor H family and plasminogen. J Immunol. 2012; 189: 4939-4950. doi: 10.4049/ jimmunol.1200386 PMID: 23071278
10. Hong YQ, Ghebrehiwet B. Effect of Pseudomonas aeruginosa elastase and alkaline protease on serum complement and isolated components C1q and C3. Clin Immunol Immunopathol. 1992; 62: 133-138. PMID: 1730152
11. McCully V, Burns G, Sokatch JR. Resolution of branched-chain oxo acid dehydrogenase complex of Pseudomonas aeruginosa PAO. Biochem J. 1986; 233: 737-742. PMID: 3085653
12. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, et al. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature. 2000; 406: 959-964. doi: 10.1038/35023079 PMID: 10984043
13. Zipfel PF, Hallström T, Riesbeck K. Human complement control and complement evasion by pathogenic microbes-tipping the balance. Mol Immunol. 2013; 56: 152-160. doi: 10.1016/j.molimm.2013. 05.222 PMID: 23810413
14. Walport MJ. Complement. First of two parts. N Engl J Med. 2001; 344: 1058-1066. PMID: 11287977
15. Nishida N, Walz T, Springer TA. Structural transitions of complement component C3 and its activation products. Proc Natl Acad Sci. 2006; 103: 19737-19742. doi: 10.1073/pnas.0609791104 PMID: 17172439
16. Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol. 2010; 11: 785-797. doi: 10.1038/ni.1923 PMID: 20720586
17. Bubeck D. The making of a macromolecular machine: assembly of the membrane attack complex. Biochem. 2014; 53: 1908-1915. doi: 10.1021/bi500157z
18. Hadders MA, Bubeck D, Roversi P, Hakobyan S, Forneris F, Morgan BP, et al. Assembly and regulation of the membrane attack complex based on structures of C5b6 and sC5b9. Cell Rep. 2012; 1: 200-207. doi: 10.1016/j.celrep.2012.02.003 PMID: 22832194
19. Liszewski M, Atkinson JP. Complement regulators in human disease: lessons from modern genetics. J Intern Med. 2015; 277: 294-305. doi: 10.1111/joim.12338 PMID: 25495259
20. Zipfel PF, Skerka C. Complement regulators and inhibitory proteins. Nat Rev Immunol. 2009; 9: 729-740. doi: 10.1038/nri2620 PMID: 19730437
21. Kunert A, Losse J, Gruszin C, Hühn M, Kaendler K, Mikkat S, et al. Immune evasion of the human pathogen Pseudomonas aeruginosa: elongation factor Tuf is a factor H and plasminogen binding protein. J Immunol Baltim Md 1950. 2007; 179: 2979-2988.
22. Singh B, Su Y-C, Riesbeck K. Vitronectin in bacterial pathogenesis: a host protein used in complement escape and cellular invasion. Mol Microbiol. 2010; 78: 545-560. doi: 10.1111/j.1365-2958.2010.07373. x PMID: 20807208
23. Podack ER, Preissner KT, Müller-Eberhard HJ. Inhibition of C9 polymerization within the SC5b-9 complex of complement by S-protein. Acta Pathol Microbiol Immunol Scand Suppl. 1984; 284: 89-96. PMID: 6587746
24. Preissner KT, Jenne D. Structure of vitronectin and its biological role in haemostasis. Thromb Haemost. 1991; 66: 123-132. PMID: 1718050
25. Preissner KT, Podack ER, Müller-Eberhard HJ. The membrane attack complex of complement: relation of C7 to the metastable membrane binding site of the intermediate complex C5b-7. J Immunol. 1985; 135: 445-451. PMID: 3998468
26. Guo W, Ma X, Xue C, Luo J, Zhu X, Xiang J, et al. Serum clusterin as a tumor marker and prognostic factor for patients with esophageal cancer. Dis Markers. 2014; 2014: 168960. doi: 10.1155/2014/ 168960 PMID: 25574066
27. Choi NH, Mazda T, Tomita M. A serum protein SP40, 40 modulates the formation of membrane attack complex of complement on erythrocytes. Mol Immunol. 1989; 26: 835-840. PMID: 2601725
28. Jenne DE, Tschopp J. Molecular structure and functional characterization of a human complement cytolysis inhibitor found in blood and seminal plasma: identity to sulfated glycoprotein 2, a constituent of rat testis fluid. Proc Natl Acad Sci. 1989; 86: 7123-7127. PMID: 2780565
29. Schvartz I, Seger D, Shaltiel S. Vitronectin. Int J Biochem Cell Biol. 1999; 31: 539-544. PMID: 10399314
30. Millis AJ, Luciani M, McCue HM, Rosenberg ME, Moulson CL. Clusterin regulates vascular smooth muscle cell nodule formation and migration. J Cell Physiol. 2001; 186: 210-219. doi: 10.1002/1097- 4652(200102)186:2<210::AID-JCP1019>3.0.CO;2-N PMID: 11169458
31. Silkensen JR, Skubitz KM, Skubitz AP, Chmielewski DH, Manivel JC, Dvergsten JA, et al. Clusterin promotes the aggregation and adhesion of renal porcine epithelial cells. J Clin Invest. 1995; 96: 2646-2653. doi: 10.1172/JCI118330 PMID: 8675630
32. Arko RJ, Chen CY, Schalla WO, Sarafian SK, Taylor CL, Knapp JS, et al. Binding of S protein by Neisseria gonorrhoeae and potential role in invasion. J Clin Microbiol. 1991; 29: 70-75. PMID: 1704384
33. Attia AS, Ram S, Rice PA, Hansen EJ. Binding of vitronectin by the Moraxella catarrhalis UspA2 protein interferes with late stages of the complement cascade. Infect Immun. 2006; 74: 1597-1611. PMID: 16495531
34. Griffiths NJ, Hill DJ, Borodina E, Sessions RB, Devos NI, Feron CM, et al. Meningococcal surface fibril (Msf) binds to activated vitronectin and inhibits the terminal complement pathway to increase serum resistance. Mol Microbiol. 2011; 82: 1129-1149. doi: 10.1111/j.1365-2958.2011.07876.x PMID: 22050461
35. Leroy-Dudal J, Gagnière H, Cossard E, Carreiras F, Di Martino P. Role of alphavbeta5 integrins and vitronectin in Pseudomonas aeruginosa PAK interaction with A549 respiratory cells. Microbes Infect Inst Pasteur. 2004; 6: 875-881.
36. Singh B, Jalalvand F, Mörgelin M, Zipfel P, Blom AM, Riesbeck K. Haemophilus influenzae protein E recognizes the C-terminal domain of vitronectin and modulates the membrane attack complex. Mol Microbiol. 2011; 81: 80-98. doi: 10.1111/j.1365-2958.2011.07678.x PMID: 21542857
37. Kostrzynska M, Paulsson M, Schmidt KH, Wadström T. Comparative studies on binding of vitronectin and fibronectin to groups A and C streptococci. Microbios. 1992; 71: 179-192. PMID: 1282649
38. Li DQ, Lundberg F, Ljungh Anull. Characterization of vitronectin-binding proteins of Staphylococcus epidermidis. Curr Microbiol. 2001; 42: 361-367. doi: 10.1007/s002840010230 PMID: 11400058
39. Liang OD, Flock JI, Wadström T. Isolation and characterisation of a vitronectin-binding surface protein from Staphylococcus aureus. Biochim Biophys Acta. 1995; 1250: 110-116. PMID: 7612648
40. Tyriak I, Ljungh S. Binding of extracellular matrix molecules by enterococci. Curr Microbiol. 2003; 46: 435-442. doi: 10.1007/s00284-002-3879-2 PMID: 12732951
41. Zipfel PF, Skerka C. Staphylococcus aureus: the multi headed hydra resists and controls human complement response in multiple ways. Int J Med Microbiol IJMM. 2014; 304: 188-194. doi: 10.1016/j.ijmm. 2013.11.004 PMID: 24461453
42. Akesson P, Sjöholm AG, Björck L. Protein SIC, a novel extracellular protein of Streptococcus pyogenes interfering with complement function. J Biol Chem. 1996; 271: 1081-1088. PMID: 8557634
43. Kurosu T, Chaichana P, Yamate M, Anantapreecha S, Ikuta K. Secreted complement regulatory protein clusterin interacts with dengue virus nonstructural protein 1. Biochem Biophys Res Commun. 2007; 362: 1051-1056. doi: 10.1016/j.bbrc.2007.08.137 PMID: 17825259
44. Li DQ, Ljungh A. Binding of human clusterin by Staphylococcus epidermidis. FEMS Immunol Med Microbiol. 2001; 31: 197-202. PMID: 11720815
45. Partridge SR, Baker MS, Walker MJ, Wilson MR. Clusterin, a putative complement regulator, binds to the cell surface of Staphylococcus aureus clinical isolates. Infect Immun. 1996; 64: 4324-4329. PMID: 8926106
46. Liang OD, Rosenblatt S, Chhatwal GS, Preissner KT. Identification of novel heparin-binding domains of vitronectin. FEBS Lett. 1997; 407: 169-172. PMID: 9166893
47. Sheehan M, Morris CA, Pussell BA, Charlesworth JA. Complement inhibition by human vitronectin involves non-heparin binding domains. Clin Exp Immunol. 1995; 101: 136-141. PMID: 7542572
48. Bergmann S, Lang A, Rohde M, Agarwal V, Rennemeier C, Grashoff C, et al. Integrin-linked kinase is required for vitronectin-mediated internalization of Streptococcus pneumoniae by host cells. J Cell Sci. 2009; 122: 256-267. doi: 10.1242/jcs.035600 PMID: 19118218
49. Hallström T, Blom AM, Zipfel PF, Riesbeck K. Nontypeable Haemophilus influenzae protein E binds vitronectin and is important for serum resistance. J Immunol Baltim Md 1950. 2009; 183: 2593-2601. doi: 10.4049/jimmunol.0803226
50. Lopez CM, Wallich R, Riesbeck K, Skerka C, Zipfel PF. Candida albicans uses the surface protein Gpm1 to attach to human endothelial cells and to keratinocytes via the adhesive protein vitronectin. PloS One. 2014; 9: e90796. doi: 10.1371/journal.pone.0090796 PMID: 24625558
51. Voss S, Hallström T, Saleh M, Burchhardt G, Pribyl T, Singh B, et al. The choline-binding protein PspC of Streptococcus pneumoniae interacts with the C-terminal heparin-binding domain of vitronectin. J Biol Chem. 2013; 288: 15614-15627. doi: 10.1074/jbc.M112.443507 PMID: 23603906