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ISSN 2410-7751 (Print)
ISSN 2410-776X (Online)

 4 2013

"Biotechnologia Acta" v. 6, no. 4, 2013
https://doi.org/10.15407/biotech6.04.144
Р. 144-161, Bibliography 135, English
Universal Decimal classification: 577.083.3+579.84

POLYADHESINS: AN ARMORY OF GRAM--NEGATIVE PATHOGENS FOR PENETRATION THROUGH THE IMMUNE SHIELD

V. P. Zav’yalov1, 2

1Joint Biotechnology Laboratory, Department of Chemistry, University of Turku, Turku, Finland
2Kherson State University, Kherson, Ukraine

The rapid emergence of treatment-resistant bacterial pathogens has become a major threat to public health. The outbreak of new Shiga-toxin–producing Escherichia coli O104H4 infection occured in Germany in 2011 illustrates this problem. To colonize host tissues, pathogenic bacteria express surface adhesive organelles. The German strain uses aggregative adherence fimbriae I (AAF/I) to anchor to the intestinal mucosa and induce inflammation. AAF/I belong to the family of chaperone/usher assembled fimbrial polyadhesins. Polyadhesins are functioning as an armory for penetration through the host immune shield. The polyadhesin-binding to the target cells triggers subversive signal by aggregation of host cell receptors that allow pathogens to mislead and evade immune defense. Their binding is orchestrated with the type III secretion system, which is extremally important for bacterial virulency. Polyadhesins also are involved in biofilm formation making bacteria more resistant to immune response. Because of this, the polyadhesins are potential targets for immune countermeasures against bacterial infections, in particular for anti-adhesion therapy with antibodies to polyadhesins as one of alternatives to antibiotic therapy.

Key words: Gram-negative pathogens; polyadhesins; anti-immune armory.

© Институт биохимии им. А. В. Палладина НАН Украины, 2013

{accordion title="References" open="false"}

1. Zavyalov V., Zavialov A., Zavyalova G., Korpela T. Adhesive organelles of Gram negative pathogens assembled with the сlassical сhaperone/usher machinery: structure and function from a clinical standpoint. FEMS Microbiol. Rev. 2010, 34(3),?317–378.

2. Zavialov A., Zavyalova G., Korpela T., Zavyalov V. FGL chaperone-assembled fimbrial polyadhesins: antiimmune armament of Gram-negative bacterial pathogens. FEMS Microbiol. Rev.  2007, 31(4), 478–514.

3. Zavyalov V., Zavyalova G., Denesyuk A., Korpela T. Modelling of steric structure of a periplasmic molecular chaperone Caf1M of Yersinia pestis, a prototype member of a subfamily with characteristic structural and functional features. FEMS Immunol. Med. Microbiol.  1995, 11(1), 19–24.

4. Hung D., Knight S., Woods R. et al. Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J.  1996, 15(15), 3792–3805.

5. Nuccio S., B?umler A. Evolution of the chaperone/usher assembly pathway: fimbrial classification goes greek // Microbiol. Mol. Biol. Rev.2007. — V. 71, N 4. — P. 551–575.

6. Garnett J., Mart?nez-Santos V., Salda?a Z. Structural insights into the biogenesis and biofilm formation by the Escherichia coli common pilus. Proc. Natl. Acad. Sci. USA.  2012, 109(10), 3950–3955.
  https://doi.org/10.1073/pnas.1106733109

7. Korea C., Ghigo J., Beloin C. The sweet connection: Solving the riddle of multiple sugar-binding fimbrial adhesins in Escherichia coli: Multiple E. coli fimbriae form a versatile arsenal of sugar-binding lectins potentially involved in surface-colonisation and tissue tropism. Bioessays. 2011, 33(4),?300–311.
 https://doi.org/10.1002/bies.201000121

8. Zav’yalov V. Fimbrial polyadhesins: anti-immune armament of Yersinia. Adv. Exp. Med. Biol. 2012, V. 954, P. 183–201.
 https://doi.org/10.1007/978-1-4614-3561-7_24

9. Kovacs-Nolan J., Mine Y. Egg yolk antibodies for passive immunity. Annu. Rev. Food Sci. Technol. 2012, V. 3, P. 163–182.
 https://doi.org/10.1146/annurev-food-022811-101137

10. Oleksiewicz M., Nagy G., Nagy E. Antibacterial monoclonal antibodies: Back to the future? Arch. Biochem. Biophys.  2012, 526(2), 124–131.
 https://doi.org/10.1016/j.abb.2012.06.001

11. Allen W., Phan G., Waksman G. Pilus biogenesis at the outer membrane of Gram-negative bacterial pathogens. Curr. Opin. Struct. Biol. 2012, 22(4), 1–7.
https://doi.org/10.1016/j.sbi.2012.02.001

12. Busch A., Waksman G. Chaperone-usher pathways: diversity and pilus assembly mechanism. Phil. Trans. R. Soc. B.  2012, 367(1592), 1112–1122.

13. Geibel S., Waksman G. Crystallography and electron microscopy of chaperone/usher pilus systems. Adv. Exp. Med. Biol.  2011, V. 715, P. 159–174.
 https://doi.org/10.1007/978-94-007-0940-9_10

14. Kline K., Dodson K., Caparon M., Hultgren S. A tale of two pili: assembly and function of pili in bacteria. Trends Microbiol.  2010, 18(5), 224–232.
 https://doi.org/10.1016/j.tim.2010.03.002

15. Lo A., Moonens K., Remaut H. Chemical attenuation of pilus function and assembly in Gram-negative bacteria. Curr. Opin. Microbiol.  2013, 16(1), 85–92.
 https://doi.org/10.1016/j.mib.2013.02.003

16. Zavialov A., Kersley J., Korpela T. et al. Donor strand complementation mechanismin the biogenesis of non-pilus systems. Mol. Microbiol.  2002, 45(4), 983–995.
 https://doi.org/10.1046/j.1365-2958.2002.03066.x

17. Zavialov A., Berglund J., Pudney A. et al. Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved fol­ding energy drives fiber formation. Cell.  2003, 113(5), 587–596.
 https://doi.org/10.1016/S0092-8674(03)00351-9

18. Zavialov A., Tischenko V., Fooks L. et al. Resolving the energy paradox of chaperone-mediated fibre assembly. Biochem. J.  2005, 389(3), 685–694.
 https://doi.org/10.1042/BJ20050426

19. Galyov E., Smirnov O., Karlyshev A. et al. Nucleotide sequence of the Yersinia pestis gene encoding F1 antigen and the primary structure of the protein. FEBS Lett.  1990, 277(1–2), 230–232.
https://doi.org/10.1016/0014-5793(90)80852-A

20. Galyov E., Karlyshev A., Chernovskaya T. et al. Expression of the envelope antigen F1 of Yersinia pestis is mediated by the product of caf1M gene having homology with the chaperone PapD of Escherichia coli. FEBS Lett. 1991, 286(1–2), 79–82.
https://doi.org/10.1016/0014-5793(91)80945-Y

21. Karlyshev A., Galyov E., Smirnov O. et al. A new gene of the f1 operon of Y. pestis involved in the capsule biogenesis. FEBS Lett.  1992, 297(1–2), 77–80.
https://doi.org/10.1016/0014-5793(92)80331-A

22. Karlyshev A., Galyov E., Abramov V., Zavyalov V. caf1R gene and its role in the regulation of capsule formation of Y. pestis. FEBS Lett.  1992, 305(1), 37–40.
 https://doi.org/10.1016/0014-5793(92)80650-6

23. Karlyshev A., Galyov E., Smirnov O. et al. Structure and regulation of a gene cluster involved in capsule formation of Y pestis. Biological Membranes: Structure, Biogenesis and Dynamic, NATO-ASI Serias (Op den Kamp JAF, ed) Springer-Verlag, NewYork, NY. 1994, V. H-82, P. 321–330.

24. Zavyalov V., Chernovskaya T., Chapman D. et al. Influence of the conserved disulphide bond exposed to the putative binding pocket, on the structure and function of the immunoglobulin-like periplasmic molecular chaperone, Caf1M, of Yersinia pestis. Biochem. J.  1997, 324(2) 571–578.
  https://doi.org/10.1042/bj3240571

25. Chapman D., Zavialov A., Chernovskaya T. et al. Structure and functional significance of the FGL sequence of the periplasmic chape­rone, Caf1M, of Yersinia pestis. J. Bacteriol.  1999, 181(8), 2422–2429.

26. Zavialov A., Batchikova N., Korpela T. et al. Secretion of recombinant proteins via the chaperone/usher pathway in Escherichia coli. Appl. Environ. Microb.  2001, 67(4), 1805–1814.
https://doi.org/10.1128/AEM.67.4.1805-1814.2001

27. MacIntyre S., Zyrianova I., Chernovskaya T. et al. An extended hydrophobic interactive surface of Yersinia pestis Caf1M chaperone is essential for subunit binding and F1 capsule assembly. Mol. Microbiol.  2001, 39(1), 12–25.
https://doi.org/10.1046/j.1365-2958.2001.02199.x

28. Zavialov A., Knight S. A novel self-capping mechanism controls aggregation of periplasmic chaperone Caf1M. Mol. Microbiol.  2007,?64(1), 153-164.
 https://doi.org/10.1111/j.1365-2958.2007.05644.x

29. Yu X., Visweswaran G., Duck Z. et al. Caf1A usher possesses a Caf1 subunit-like domain that is crucial for Caf1 fibre secretion. Biochem. J. 2007, 418(3), 541–551.
https://doi.org/10.1042/BJ20080992

30. Dubnovitsky A., Duck Z., Kersley J. et al. Conserved hydrophobic clusters on the surface of the Caf1A usher C-terminal domain are important for F1 antigen assembly. J. Mol. Biol.  2010, 403(2), 243–259.
 https://doi.org/10.1016/j.jmb.2010.08.034

31. Yu X., Dubnovitsky A., Pudney A. et al. Allosteric mechanism controls traffic in the chaperone/usher pathway. Structure, 2012, 20(11), 1861–1871.
 https://doi.org/10.1016/j.str.2012.08.016

32. Yu X., Fooks L., Moslehi-Mohebi E. et al. Large is fast, small is tight: determinants of speed and affinity in subunit capture by a periplasmic chaperone. Mol. Biol. 2012, 417(4), 294–308.
 https://doi.org/10.1016/j.jmb.2012.01.020

33. Lindler L., Tall B. Yersinia pestis pH6 antigen forms fimbriae and is induced by intracellular association with macrophages. Mol. Microbiol.  1993, 8(2), 311–324.
 https://doi.org/10.1111/j.1365-2958.1993.tb01575.x

34. Yang Y., Isberg R. Transcriptional regulation of the Yersinia pseudotuberculosis pH6 antigen adhesin by two envelope-associated components. Mol. Microbiol. 1997, 24(3), 499–510.
 https://doi.org/10.1046/j.1365-2958.1997.3511719.x

35. Cathelyn J., Crosby S., Lathem W. et al. RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague. Proc. Natl. Acad. Sci. USA.  2006,?103(36), 13514–13519.
https://doi.org/10.1073/pnas.0603456103

36. Iriarte M., Vanooteghem J., Delor I. et al. The Myf fibrillae of Yersinia enterocolitica. Mol. Microbiol.  1993, 9(3), 507–520.
 https://doi.org/10.1111/j.1365-2958.1993.tb01712.x

37. Iriarte M., Cornelis G. MyfF, an element of the network regulating the synthesis of fibrillae in Yersinia enterocolitica. J. Bacteriol.  1995, 177(3), 738–744.

38. Jalajakumar M., Thomas C., Halter R., Manning P. Genes for biosynthesis and assembly of CS3 pili of CFA/II enterotoxigenic Escherichia coli: novel regulation of pilus production by bypassing an amber codon. Mol. Microbiol. 1989, 12(12), 1685–1695.
https://doi.org/10.1111/j.1365-2958.1989.tb00154.x

39. Ahrens R., Ott M., Ritter A. et al. Genetic analysis of the gene cluster encoding nonfimbrial adhesin I from an Escherichia coli uropathogen. Infect. Immun.  1993, 61(6), 2505–2512.

40. Jouve M., Garcia M., Courcoux P. et al. Adhesion to and invasion of HeLa cells by pathogenic Escherichia coli carrying the afa-3 gene cluster are mediated by the AfaE and AfaD proteins, respectively. Infect. Immun. 1997, 56(10), 4082–4089.

41. Servin A. Pathogenesis of Afa/Dr diffusely adhering Escherichia coli .  Clin. Microbiol. Rev.  2005, 18(2), 264–292.
https://doi.org/10.1128/CMR.18.2.264-292.2005

42. Anderson K., Billington J., Pettigrew D. et al. An atomic resolution model for assembly, architecture, and function of the Dr adhesions. Mol. Cell. 2004, 101(4), 647–657.
https://doi.org/10.1016/j.molcel.2004.08.003

43. Anderson K., Cota E., Simpson P. et al. Comp­lete resonance assignments of a ‘donor-strand complemented’ AfaE: the afimbrial adhesin from diffusely adherent E. coli. J. Biomol. NMR.  2004, 29(3), 409–410.
 https://doi.org/10.1023/B:JNMR.0000032498.94441.08

44. Pettigrew D., Anderson K., Billington J. et al. High resolution studies of the Afa/Dr adhesin DraE and its interaction with chloramphenicol. J. Biol. Chem.  2004,?279(45), 46851–46857.
 https://doi.org/10.1074/jbc.M409284200

45. Zalewska B., Pi?tek R., Bury K. et al. A surface-exposed DraD protein of uropathogenic Escherichia coli bearing Dr fimbriae may be expressed and secreted independently from DraC usher and DraE adhesion. Microbiology.  2005, 151(7), 2477–2486.
https://doi.org/10.1099/mic.0.28083-0

46. Zalewska-Piatek B., Bury K., Piatek R. et al. Type II secretory pathway for surface secretion of DraD invasion from the uropathogenic Escherichia coli Dr1 strain. J. Bacteriol.  2008, 190(14), 5044–5056.
https://doi.org/10.1128/JB.00224-08

47. Korotkova N., Yarova-Yarovaya Y., Tchesnokova V. et al. Escherichia coli DraE adhesin-associated bacterial internalization by epithelial cells is promoted independently by decay-accelerating factor and carcinoembryonic antigen-related cell adhesion molecule binding and does not require the DraD invasion. Infect. Immun.  2008, 76(9), 3869–3880.
https://doi.org/10.1128/IAI.00427-08

48. Guignot J., Hudault S., Kansau I. et al. DAF and CEACAMs receptor-mediated internalization and intracellular lifestyle of Afa/Dr diffusely adhering Escherichia coli into epithelial cells. Infect. Immun.  2009, 77(1), 517–531.
 https://doi.org/10.1128/IAI.00695-08

49. Clouthier S., Collinson S., Kay W. Unique fimbriae-like structures encoded by sefD of the SEF14 fimbrial gene cluster of Salmonella enteritidis. Mol. Microbiol.  1994, 12(6), 893–901.
 https://doi.org/10.1111/j.1365-2958.1994.tb01077.x

50. Wolf M., De Haan L., Cassels F. et al. The CS6 colonization factor of human enterotoxigenic Escherichia coli contains two heterologous major subunits. FEMS Microbiol. Lett.  1997, 148(1), 35–42.
 https://doi.org/10.1111/j.1574-6968.1997.tb10263.x

51. Chessa D., Dorsey C., Winter M., B?umler A. Binding specificity of Salmonella plasmid-encoded fimbriae assessed by glycomics. J. Biol. Chem.? 2008, 283(13), 8118–8124.
 https://doi.org/10.1074/jbc.M710095200

52. Bakker D., Vader C., Roosendaal B. et al. Structure and function of periplasmic chaperone-like proteins involved in the biosynthesis of K88 and K99 fimbriae in enteroto­xigenic Escherichia coli. Mol. Microbiol.  1991, 5(4), 875–886.
https://doi.org/10.1111/j.1365-2958.1991.tb00761.x

53. Adams L., Simmons C., Rezmann L. et al. Identification and characterization of a K88- and CS31A-like operon of a rabbit enteropathogenic and K99 fimbriae in enterotoxigenic Escherichia coli. Mol. Microbiol.  1997,?65(12), 875–886.

54. Scaletsky I., Michalski J., Torres A. et al. Identification and characterization of the locus for diffuse adherence, which encodes a novel afimbrial adhesion found in atypical enteropathogenic Escherichia coli. Infect. Immun.  2005, 73(8), 4753–4765.
https://doi.org/10.1128/IAI.73.8.4753-4765.2005

55. Van Molle I., Moonens K., Garcia-Pino A. et al. Structural and thermodynamic characterization of pre- and postpolymerization states in the F4 fimbrial subunit FaeG. J. Mol. Biol.  2009, 394(5), 957–967.
https://doi.org/10.1016/j.jmb.2009.09.059

56. Cantey J., Blake R., Williford J., Moseley S. Characterization of the Escherichia coli AF/R1 pilus operon: novel genes necessary for transcriptional regulation and for pilus-mediated adherence. Infect. Immun. 1999, 67(5), 2292–2298.

57. Imberechts H., Wild P., Charlier G. et al. Characterization of F18 fimbrial genes fedE and fedF involved in adhesion and length of enterotoxemic Escherichia coli strain 107/86. Microb. Pathog. 1996, 21(3), 183–192.
 https://doi.org/10.1006/mpat.1996.0053

58. Smeds A., Hemmann K., Jakava-Viljanen M. et al. Characterization of the adhesin of Esche­ri­chia coli F18 fimbriae. Infect. Immun. 2001, 69(12), 7941–7945.
 https://doi.org/10.1128/IAI.69.12.7941-7945.2001

59. Moonens K., Bouckaert J., Coddens A. et al. Structural insight in histo-blood group binding by the F18 fimbrial adhesin FedF. Mol. Microbiol.  2012, 86(1), 82–95.
  https://doi.org/0.1111/j.1365-2958.2012.08174.x

60. Mart?nez-Santos V., Medrano-L?pez A., Salda?a Z. et al. Transcriptional regulation of the ecp operon by EcpR, IHF, and H-NS in attaching and effacing Escherichia coli. J. Bacteriol.  2012, 194(18), 5020–5033.
 https://doi.org/10.1128/JB.00915-12

61. Bann J., Pinkner J., Frieden C., Hultgren S. Catalysis of protein folding by chaperones in pathogenic bacteria. Proc. Natl. Acad. Sci. USA.  2004, 101(50), 17389–17393.
https://doi.org/10.1073/pnas.0408072101

62. Nishiyama M., Vetsch M., Puorger C. et al. Identification and characterization of the chape­rone subunit complex-binding domain from the Type 1 pilus assembly platform FimD. J. Mol. Biol.  2003, 330(3), 513–525.
 https://doi.org/10.1016/S0022-2836(03)00591-6

63. Choudhury D., Thompson A., Stojanoff V. et al. X-ray structure of the FimC-FimH chape­rone–adhesin complex from uropathogenic Escherichia coli. Science.  1999,?285(5430), 1061–1066.
 https://doi.org/10.1126/science.285.5430.1061

64. Sauer F., Futterer K., Pinkner J. et al. Structural basis of chaperone function and pilus biogenesis. Science. 1999,?285(5430), 1058–1061.
 https://doi.org/10.1126/science.285.5430.1058

65. Sauer F., Pinkner J., Waksman G., Hultgren S. Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation. Cell. 2002, 111(4), 543–551.
 https://doi.org/10.1016/S0092-8674(02)01050-4

66. Remaut H., Rose R., Hannan T. et al. Donor-strand exchange in chaperone-assisted pilus assembly proceeds through a concerted ?- strand displacement mechanism. Mol. Cell. 2006, 22(6), 831–842.
 https://doi.org/10.1016/j.molcel.2006.05.033

67. Verger D., Bullitt E., Hultgren S., Waksman G. Crystal structure of the P pilus rod subunit PapA. PLoS Pathogens. 2007, V. 3, P. e73.
 https://doi.org/10.1371/journal.ppat.0030073

68. Bork P., Holm L., Sander C. The immunoglobulin fold: structural classification, sequence patterns and common core. J. Mol. Biol.  1994, 242(4), 309–320.
 https://doi.org/10.1016/s0022-2836(84)71582-8

69. DeLano W. Unraveling hot spots in binding interfaces: progress and challenges. Curr. Opin. Struct. Biol.  2002, 12(1), 14–20.
 https://doi.org/10.1016/S0959-440X(02)00283-X

70. Jacob-Dubuisson F., Striker R., Hultgren S. Chaperone assisted self-assembly of pili independent of cellular energy. J. Biol. Chem. 1994, 269(17), 12447–12455.

71. Fronzes R., Remaut H., Waksman G. Architectures and biogenesis of non-flagellar protein appendages in Gram-negative bacteria. EMBO J.  2008, 27(17), 2271–2280.
 https://doi.org/10.1038/emboj.2008.155

72. Thanassi D., Saulino E., Hultgren S. The chaperone/usher pathway: a major terminal branch of the general secretory pathway. Curr. Opin. Microbiol. 1998, 1(2), 223–231.
https://doi.org/10.1016/S1369-5274(98)80015-5

73. Soto G., Hultgren S. Bacterial adhesins: common themes and variations in architecture and assembly. J. Bacteriol.  1999,?181(4), 1059–1071.

74. Knight S., Berglund J., Choudhury D. Bacterial adhesins: structural studies reveal chaperone function and pilus biogenesis. Curr. Opin. Chem. Biol.  2000, 4(6), 653–660.
 https://doi.org/10.1016/S1367-5931(00)00144-7

75. Sauer F., Barnhart M., Choudhury D. et al. Chaperone-assisted pilus assembly and bacterial attachment. Curr. Opin. Chem. Biol.  2000, 10(5), 548–556.
 https://doi.org/10.1016/s0959-440x(00)00129-9

76. Sauer F., Remaut H., Hultgren S., Waksman G. Fiber assembly by the chaperone–usher pathway. Biochim. Biophys. Acta.  2004,?1694(1–3), 259–267.
https://doi.org/10.1016/j.bbamcr.2004.02.010

77. Van den Broeck W., Cox E., Oudega C., Goddeeris B. The F4 fimbrial antigen of Escherichia coli and its receptors. Vet. Microbiol.  2000, 71(3–4), 223–244.
 https://doi.org/10.1016/S0378-1135(99)00174-1

78. Roy S., Rahman M., Yu X. et al. Crystal structure of enterotoxigenic Escherichia coli colonization factor CS6 reveals a novel type of functional assembly. Mol. Microbiol.  2012,  86(5), 1100–1115.
  https://doi.org/10.1111/mmi.12044

79. Chen T., Elberg S. Scanning electron microscopic study of virulent Yersinia pestis and Yersinia pseudotuberculosis type 1. Infect. Immun. 1977, 15(3), 972–977.

80. Pham T., Goluszko P., Popov V. et al. Molecular cloning and characterization of Dr-II A nonfimbrial adhesin-I-like adhesin isolated from gestational pyelonephritis-associated Escherichia coli that binds to decayaccelerating factor. Infect. Immun.  1997, 65(10), 4309–4318.

81. Lalioui L., Jouve M., Gounon P., Le Bougu?nec C. Molecular cloning and characterization of the afa-7 and afa-8 gene clusters encoding afimbrial adhesins in Escherichia coli strains associated with diarrhea or septicemia in calves. Infect. Immun.? 1999, 67(10), 5048–5059.

82. De Greve H., Wyns L., Bouckaert J. Combining sites of bacterial fimbriae. Curr. Opin. Struct. Biol.  2007, 17(5), 506–512.
https://doi.org/10.1016/j.sbi.2007.06.011

83. Westerlund-Wikstr?m B., Korhonen T. Molecular structure of adhesin domains in Escherichia coli fimbriae. Int. J. Med. Microbiol.  2005, 295(6–7), 479–486.
https://doi.org/10.1016/j.ijmm.2005.06.010

84. Bouckaert J., Berglund J., Schembri M. et al. Receptor binding studies disclose a novel class of high-affinity inhibitors of the Escherichia coli FimH adhesion. Mol. Microbiol.  2005, 55(2), 441–455.
 https://doi.org/10.1111/j.1365-2958.2004.04415.x

85. Bouckaert J., Mackenzie J., de Paz J. et al. The affinity of the FimH fimbrial adhesin is receptor-driven and quasiindependent of Escherichia coli pathotypes. Mol. Microbiol.  2006,  61(6), 1556–1568.
 https://doi.org/10.1111/j.1365-2958.2006.05352.x

86. Li Y., Poole S., Rasulova F. et al. A receptor-binding site as revealed by the crystal structure of CfaE, the colonization factor antigen I fimbrial adhesin of enterotoxigenic Escherichia coli. J. Biol. Chem. 2006, 282(33), 23970–23980.
https://doi.org/10.1074/jbc.M700921200

87. Lindberg F., Lund B., Johansson L., Normark S. Localization of the receptor binding protein adhesin at the tip of the bacterial pilus. Nature.  1987, 328(6125), 84–87.
 https://doi.org/10.1038/328084a0

88. Kuehn M., Heuser J., Normark S., Hultgren S. P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips. Nature.  1992, 356(6366), 252–255.
 https://doi.org/10.1038/356252a0

89. Korotkova N., Cota E., Lebedin Y. et al. A subfamily of Dr adhesions of Escherichia coli bind independently to decay-accelerating factor and the N-domain of carcinoembrionic antigen.  J. Biol. Chem. 2006, 281(39), 29120–29130.
 https://doi.org/10.1074/jbc.M605681200

90. Korotkova N., Le Trong I., Samudrala R. et al. Crystal structure and mutational analysis of the DaaE adhesin of Escherichia coli. J. Biol. Chem.  2006, 281(31), 22367–22377.
https://doi.org/10.1074/jbc.M604646200

91. Korotkova N., Yang Y., Le Trong I. et al. Binding of Dr adhesins of Escherichia coli to carcinoembryonic antigen triggers receptor dissociation.  J. Biol. Chem.  2008,?67(2), 420–434.
 https://doi.org/10.1111/j.1365-2958.2007.06054.x

92. Runco L., Myrczek S., Bliska J., Thanassi D. Biogenesis of the fraction 1 capsule and analysis of the ultrastructure of Yersinia pestis. J. Biol. Chem.  2008,  190(9), 3381–3385.
 https://doi.org/10.1128/jb.01840-07

93. Du Y., Rosqvist R., Forsberg ?. Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. J. Biol. Chem.  2002, 70(3), 1453–1460.
 https://doi.org/10.1128/iai.70.3.1453-1460.2002

94. Liu F., Chen H., Galv?n E. et al. Effects of Psa and F1 on the adhesive and invasive interactions of Yersinia pestis with human respiratory tract epithelial cells J. Biol. Chem. 2006, 74(10), 5636–5644.
 https://doi.org/10.1128/iai.00612-06

95. Levine M., Ristaino P., Marley G. et al. Coli surface antigens 1 and 3 of colonization factor antigen II-positive enterotoxigenic Escherichia coli: morphology, purification, and immune responses in humans. J. Biol. Chem.  1984, 44(2), 409–420.

96. Knutton S., McConnel M., Rowe B., McNeish A. Adhesion and ultrastructural properties of human enterotoxigenic Escherichia coli producing colonization factor antigens III and IV.  J. Biol. Chem. 1989, 57(11), 3364–3371.

97. Salih O., Remaut H., Waksman G., Orlova E. Structural analysis of the Saf pilus by electron microscopy and image processing. J. Mol. Biol.  2008, 379(1), 174–187.
 https://doi.org/10.1016/j.jmb.2008.03.056

98. Cornelis G., Wolf-Watz H. The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells.  Mol. Microbiol.  1997, 23(5), 861–867.
https://doi.org/10.1046/j.1365-2958.1997.2731623.x

99. Viboud G., Bliska J. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu. Rev. Microbiol.  2005, V. 59, P. 69–89.
 https://doi.org/10.1146/annurev.micro.59.030804.121320

100. Cornelis G. The type III secretion injectisome, a complex nanomachine for intracellular ‘toxin’ delivery. J. Biol. Chem.  2010, 391(7), 745–751.
 https://doi.org/10.1515/bc.2010.079

101. Diepold A., Amstutz M., Abel S. et al. Deciphering the assembly of the Yersinia type III secretion injectisome. EMBO J. 2010, 29(11), 1928–1940.
 https://doi.org/10.1038/emboj.2010.84

102. Marketon M., Depaolo R., Debord K. et al. Plague bacteria target immune cells during infection. Science. 2005, 309(5741), 1739–1741.
 https://doi.org/10.1126/science.1114580

103. Velan B., Bar-Haim E., Zauberman A. et al. Discordance in the effects of Yersinia pestis on dendritic cell functions: induction of maturation and paralysis of migration. Infect. Immun. 2006, 74(11), 6365–6376.
 https://doi.org/10.1128/IAI.00974-06

104. Felek S., Tsang T., Krukonis E. Three Yersinia pestis adhesins facilitate Yop delivery to eukaryotic cells and contribute to plague virulence. Infect. Immun.  2010,?78(10), 4134–4150.
 https://doi.org/10.1128/IAI.00167-10

105. Nowicki B., Moulds J., Hull R., Hull S. A hemagglutinin of uropathogenic Escheri­chia coli recognizes the Dr blood group antigen. Infect. Immun.  1988, 56(5), 1057–1060.

106. Fujita T., Inoue T., Ogawa K. et al. The mechanism of action of decay-accelerating factor (DAF) DAF inhibits the assembly of C3 convertases by dissociating C2a and Bb. J. Exp. Med.  1987, 166(5), 1221–1228.
 https://doi.org/10.1084/jem.166.5.1221

107. Lublin D., Atkinson J. Decay-accelerating factor: biochemistry, molecular biology, and function.  Annu. Rev. Immunol.  1989, V. 7, P. 35–58.
 https://doi.org/10.1146/annurev.iy.07.040189.000343

108. Westerlund B., Kuusela P., Risteli J. et al. The O75X adhesin of uropathogenic Esche­ri­chia coli is a type IV collagen-binding protein. Mol. Microbiol. 1989, 3(3), 329–337.
 https://doi.org/10.1111/j.1365-2958.1989.tb00178.x

109. Berger C., Billker O., Meyer T. et al. Differential recognition of members of the carcinoembryonic antigen family by Afa/Dr adhesins of diffusely adhering Escherichia coli (Afa/Dr DAEC). Mol. Microbiol.  2004,?52(4), 963–983.
 https://doi.org/10.1111/j.1365-2958.2004.04033.x

110. ?brink B. CEA adhesion molecules: multifunctional proteins with signal-regulatory properties.  Curr. Opin. Cell. Biol.  1997,  9(5), 616–626.
 https://doi.org/10.1016/S0955-0674(97)80114-7

111. Grunert F., Kuroki M. CEA family members expressed on hematopoeitic cells and their possible role in cell adhesion and signaling. Cell Adhesion and Communication Mediated by the CEA Family-Basic and Clinical Perspective (Stanners CP, ed) Harwood Academic Publishers, Amsterdam. 1999, P. 99–120.

112. Benchimol S., Fuks A., Jothy S. et al. Carcinoembryonic antigen, a human tumor marker, functions as an intercellular adhesion molecule. Cell.  1989, 57(2), 327–334.
https://doi.org/10.1016/0092-8674(89)90970-7

113. Kammerer R., Hahn S., Singer B. et al. Biliary glycoprotein (CD66a), a cell adhesion molecule of the immunoglobulin superfamily, on human lymphocytes: structure, expression and involvement in T cell activation. Eur. J. Immunol.  1998, 28(11), 3664–3674.
 https://doi.org/10.1002/(SICI)1521-4141(199811)28:11<3664::AID-IMMU3664>3.0.CO;2-D

114. Kammerer R., Stober D., Singer B. et al. Carcinoembryonic antigen-related cell adhe­sion molecule 1 on murine dendritic cells is a potent regulator of T cell stimulation. J. Immunol.  2001, 166(11), 6537–6544.
https://doi.org/10.4049/jimmunol.166.11.6537

115. Nakajima A., Iijima H., Neurath M. et al. Activation-induced expression of carcinoembryonic antigen-cell adhesion molecule 1 regulates mouse T lymphocyte function. J. Immunol.  2002, 168(3), 1028–1035.
https://doi.org/10.4049/jimmunol.168.3.1028

116. Fahlgren A., Baranov V., Frangsmyr L. et al. Interferon-gamma tempers the expression of carcinoembryonic antigen family molecules in human colon cells: a possible role in innate mucosal defence. Scand. J. Immunol.? 2003,  58(6), 628–641.
 https://doi.org/10.1111/j.1365-3083.2003.01342.x

117. Van Molle I., Joensuu J., Buts L. et al. Chloroplasts assemble the major subunit FaeG of Escherichia coli F4 (K88) fimbriae to strand-swapped dimmers. J. Mol. Biol.  2007, 368(3), 791–799.
https://doi.org/10.1016/j.jmb.2007.02.051

118. Zav’yalov V., Abramov V., Cherepanov P. et al. pH6 antigen (PsaA protein) of Yersinia pestis, a novel bacterial Fc-receptor. FEMS Immunol. Med. Microbiol.  1996, 14(1), 53–57.
 https://doi.org/10.1111/j.1574-695X.1996.tb00267.x

119. Payne D., Tatham D., Williamson E., Titball R. pH6 antigen of Yersinia pestis binds to ?1-linked galactosyl residues in glycosphingolipids.  Infect. Immun. 1998,?66(9), 4545–4548.

120. Deisenhofer J. Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragment B of protein A from Staphylococcus aureus at 2.9- and 2.8-? resolution.  Biochemistry.  1981, 20(9), 2361–2370.
 https://doi.org/10.1021/bi00512a001

121. Makoveichuk E., Cherepanov P., Lundberg S. et al. pH6 antigen of Yersinia pestis interacts with plasma lipoproteins and cell membranes. Lipid Res.  2003, 44(2), 320–330.
 https://doi.org/10.1194/jlr.M200182-JLR200

122. Galv?n E., Chen H., Schifferli D. The Psa fimbriae of Yersinia pestis interact with phosphatidylcholine on alveolar epithelial cells and pulmonary surfactant. Infect. Immun.  2006.  75(3), 1272–1279.
 https://doi.org/10.1128/IAI.01153-06

123. Bao R., Nair M., Tang W. et al. Structural basis for the specific recognition of dual receptors by the homopolymeric pH 6 antigen (Psa) fimbriae of Yersinia pestis. Proc. Natl. Acad. Sci. USA.  2013,?110(3), 1065–1070.
 https://doi.org/10.1073/pnas.1212431110

124. Pouttu R., Westerlund-Wikstrom B., Lang H. et al. Matb, a common fimbrillin gene of Escherichia coli, expressed in a genetically conserved, virulent clonal group. J. Bacteriol.  2001, 183(16), 4727–4736.
https://doi.org/10.1128/JB.183.16.4727-4736.2001

125. Rendon M., Saldana Z., Erdem A. et al. Com­men­sal and pathogenic Escherichia coli use a common pilus adherence factor for epithelial cell colonization.  Proc. Natl. Acad. Sci. USA.  2007, 104(25), 10637–10642.
https://doi.org//10.1073/pnas.0704104104

126. Saldana Z., Erdem A., Schuller S. et al. The Escherichia coli common pilus and the bundle-forming pilus act in concert during the formation of localized adherence by enteropathogenic E. coli. J. Bacteriol.  2009, 191(11), 3451–3461.
https://doi.org/10.1128/JB.01539-08

127. Blackburn D., Husband A., Saldana Z. et al. Distribution of the Escherichia coli common pilus among diverse strains of human enterotoxigenic E. coli. J. Clin. Microbiol.  2009, 47(6), 1781–1784.
 https://doi.org/10.1128/JCM.00260-09

128. Avelino F., Saldana Z., Islam S. et al. The majority of enteroaggregative Escherichia coli strains produce the E. coli common pilus when adhering to cultured epithelial cells. Int. J. Med. Microbiol.  2010, 300(7), 440–448.
 https://doi.org/0.1016/j.ijmm.2010.02.002

129. Croxen M., Finlay B. Molecular mechanisms of Escherichia coli pathogenicity.Nat. Rev. Microbiol.  2010, 8(1), 26–38.

130. Picard B., Garcia J., Gouriou S. et al. The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect. Immun.? 1999, 67(2), 546–553.

131. Lehti T., Bauchart P., Heikkinen J. et al. Mat fimbriae promote biofilm formation by me­nin­gitis-associated Escherichia coli. Microbiology.  2010, 156(8), 2408–2417.
 https://doi.org/10.1099/mic.0.039610-0

132. Zhang W., Sack D. Progress and hurdles in the development of vaccines against enterotoxigenic Escherichia coli in humans. Expert Rev. Vaccines.  2012, 11(6), 677–694.
 https://doi.org/10.1586/erv.12.37

133. De Jong B., Ekdahl B. The comparative burden of salmonellosis in the European Union member states, associated and candidate countries. BMC Public Health.  2006, V. 6, P. 4.
 https://doi.org/10.1186/1471-2458-6-4

134. Giske C., Monnet D., Cars O., Carmeli Y. Clinical and economic impact of common multidrug-resistant Gram-negative bacilli.  Antimicrob. Agents Chemother. 2008, 52(3), 813–821.
 https://doi.org/10.1128/AAC.01169-07

135.Rasko D., Webster D., Sahl J. et al. Origins of the E. coli strain causing an outbreak of hemoly­tic–uremic syndrome in Germany. N. Engl. J. Med.  2011, 365(8), 709–717.
 https://doi.org/10.1056/NEJMoa1106920

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