Structural basis for the specific recognition of dual receptors by the homopolymeric pH 6 antigen (Psa) fimbriae of Yersinia pestis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 3, 2013, Pages 1065-1070

  Bao, Rui ^a   Nair, Manoj K M ^b,c   Tang, Wai Kwan ^a   Esser, Lothar ^a   Sadhukhan, Annapurna ^b   Holland, Robin L ^b   Xia, Di ^a   Schifferli, Dieter M ^b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c Pathogenetix Inc   (United States)

Author keywords

Adhesin receptor complex; Adhesion; Ligand binding; Phosphocholine binding; Sugar binding

Indexed keywords

BACTERIAL PROTEIN; GALACTOSE; GALACTOSYLCERAMIDE; PH 6 ANTIGEN; PHOSPHATIDYLCHOLINE; PHOSPHORYLCHOLINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; FIMBRIA; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; YERSINIA PESTIS;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; CELL LINE; CRYSTALLOGRAPHY, X-RAY; DNA, BACTERIAL; FIMBRIAE, BACTERIAL; GALACTOSE; HOST-PATHOGEN INTERACTIONS; HUMANS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLCHOLINE; PLAGUE; RECEPTORS, CELL SURFACE; SEQUENCE HOMOLOGY, AMINO ACID; STATIC ELECTRICITY; VIRULENCE; YERSINIA PESTIS;

MAMMALIA; YERSINIA PESTIS;

EID: 84872544773     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1212431110     Document Type: Article

References (32)

1. Stenseth NC, et al. (2008) Plague: Past, present, and future. PLoS Med 5(1):e3.
2. Viboud GI, Bliska JB (2005) Yersinia outer proteins: Role in modulation of host cell signaling responses and pathogenesis. Annu Rev Microbiol 59:69-89. (Pubitemid 41507424)
3. Felek S, Tsang TM, Krukonis ES (2010) Three Yersinia pestis adhesins facilitate Yop delivery to eukaryotic cells and contribute to plague virulence. Infect Immun 78(10):4134-4150.
4. Zavialov A, Zav'yalova G, Korpela T, Zav'yalov V (2007) FGL chaperone-assembled fimbrial polyadhesins: anti-immune armament of Gram-negative bacterial pathogens. FEMS Microbiol Rev 31(4):478-514. (Pubitemid 46920253)
5. Galván EM, Chen H, Schifferli DM (2007) The Psa fimbriae of Yersinia pestis interact with phosphatidylcholine on alveolar epithelial cells and pulmonary surfactant. Infect Immun 75(3):1272-1279. (Pubitemid 46385819)
6. Du Y, Rosqvist R, Forsberg A (2002) Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect Immun 70(3):1453-1460. (Pubitemid 34163423)
7. Liu F, Chen H, Galván EM, Lasaro MA, Schifferli DM (2006) Effects of Psa and F1 on the adhesive and invasive interactions of Yersinia pestis with human respiratory tract epithelial cells. Infect Immun 74(10):5636-5644. (Pubitemid 44484547)
8. Ben-Efraim S, Aronson M, Bichowsky-Slomnicki L (1961) New antigenic component of Pasteurella pestis formed under specified conditions of pH and temperature. J Bacteriol 81(5):704-714.
9. Yang Y, Merriam JJ, Mueller JP, Isberg RR (1996) The psa locus is responsible for thermoinducible binding of Yersinia pseudotuberculosis to cultured cells. Infect Immun 64(7):2483-2489. (Pubitemid 26226808)
10. Huang XZ, Lindler LE (2004) The pH 6 antigen is an antiphagocytic factor produced by Yersinia pestis independent of Yersinia outer proteins and capsule antigen. Infect Immun 72(12):7212-7219.
11. Galván EM, Nair MK, Chen H, Del Piero F, Schifferli DM (2010) Biosafety level 2 model of pneumonic plague and protection studies with F1 and Psa. Infect Immun 78(8):3443-3453.
12. Cathelyn JS, Crosby SD, Lathem WW, Goldman WE, Miller VL (2006) RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague. Proc Natl Acad Sci USA 103(36):13514-13519. (Pubitemid 44380139)
13. Lindler LE, Klempner MS, Straley SC (1990) Yersinia pestis pH 6 antigen: Genetic, biochemical, and virulence characterization of a protein involved in the pathogenesis of bubonic plague. Infect Immun 58(8):2569-2577. (Pubitemid 20228241)
14. Payne D, Tatham D, Williamson ED, Titball RW (1998) The pH 6 antigen of Yersinia pestis binds to beta1-linked galactosyl residues in glycosphingolipids. Infect Immun 66(9):4545-4548. (Pubitemid 28402741)
15. Iriarte M, et al. (1993) The Myf fibrillae of Yersinia enterocolitica. Mol Microbiol 9(3):507-520. (Pubitemid 23248763)
16. Runco LM, Myrczek S, Bliska JB, Thanassi DG (2008) Biogenesis of the fraction 1 capsule and analysis of the ultrastructure of Yersinia pestis. J Bacteriol 190(9):3381-3385. (Pubitemid 351581434)
17. Lindler LE, Tall BD (1993) Yersinia pestis pH 6 antigen forms fimbriae and is induced by intracellular association with macrophages. Mol Microbiol 8(2):311-324. (Pubitemid 23124548)
18. Salih O, Remaut H, Waksman G, Orlova EV (2008) Structural analysis of the Saf pilus by electron microscopy and image processing. J Mol Biol 379(1):174-187.
19. Arondel V, Benning C, Somerville CR (1993) Isolation and functional expression in Escherichia coli of a gene encoding phosphatidylethanolamine methyltransferase (EC 2.1.1.17) from Rhodobacter sphaeroides. J Biol Chem 268(21):16002-16008. (Pubitemid 23222107)
20. Kilpper-Bälz R, Wenzig P, Schleifer KH (1985) Molecular relationships and classification of some viridans streptococci as Streptococcus oralis and emended description of Streptococcus oralis (Bridge and Sneath 1982). Int J Syst Bacteriol 35(4):482-488. (Pubitemid 16214470)
21. Hakenbeck R, Madhour A, Denapaite D, Brückner R (2009) Versatility of choline metabolism and choline-binding proteins in Streptococcus pneumoniae and commensal streptococci. FEMS Microbiol Rev 33(3):572-586.
22. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: Fine-tuning polysaccharide recognition. Biochem J 382(Pt 3):769-781. (Pubitemid 39312891)
23. Laughrey ZR, Kiehna SE, Riemen AJ, Waters ML (2008) Carbohydrate-pi interactions: What are they worth? J Am Chem Soc 130(44):14625-14633.
24. Dougherty DA, Stauffer DA (1990) Acetylcholine binding by a synthetic receptor: implications for biological recognition. Science 250(4987):1558-1560. (Pubitemid 120034365)
25. Hermoso JA, et al. (2005) Insights into pneumococcal pathogenesis from the crystal structure of the modular teichoic acid phosphorylcholine esterase Pce. Nat Struct Mol Biol 12(6):533-538. (Pubitemid 43085884)
26. Padlan EA, Davies DR, Rudikoff S, Potter M (1976) Structural basis for the specificity of phosphorylcholine-binding immunoglobulins. Immunochemistry 13(11):945-949.
27. Wah DA, Fernández-Tornero C, Sanz L, Romero A, Calvete JJ (2002) Sperm coating mechanism from the 1.8 A crystal structure of PDC-109- phosphorylcholine complex. Structure 10(4):505-514. (Pubitemid 34304229)
28. Karlsson K-A (1989) Animal glycosphingolipids as membrane attachment sites for bacteria. Annu Rev Biochem 58:309-350.
29. Van Molle I, et al. (2007) Chloroplasts assemble the major subunit FaeG of Escherichia coli F4 (K88) fimbriae to strand-swapped dimers. J Mol Biol 368(3):791-799. (Pubitemid 46527622)
30. Li YF, et al. (2009) Structure of CFA/I fimbriae from enterotoxigenic Escherichia coli. Proc Natl Acad Sci USA 106(26):10793-10798.
31. Poole ST, et al. (2007) Donor strand complementation governs intersubunit interaction of fimbriae of the alternate chaperone pathway. Mol Microbiol 63(5):1372-1384.
32. Zavialov AV, et al. (2003) Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell 113(5):587-596. (Pubitemid 36694184)