A vaccine approach for the prevention of infections by multidrug-resistant Enterococcus faecium

Journal of Biological Chemistry

Volumn 290, Issue 32, 2015, Pages 19512-19526

  Kodali, Srinivas ^a   Vinogradov, Evgeny ^b   Lin, Fiona ^a   Khoury, Nancy ^a   Hao, Li ^a   Pavliak, Vilo ^a   Jones, C Hal ^a   Laverde, Diana ^c   Huebner, Johannes ^c,d   Jansen, Kathrin U ^a   Anderson, Annaliesa S ^a   Donald, Robert G K ^a  

^a Pfizer Vaccine Research Operations and Strategy   (United States)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c UNIVERSITY OF FREIBURG   (Germany)

^d LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN-ANTIBODY REACTIONS; ANTIGENS; BACILLI; POLYSACCHARIDES; VACCINES;

CLINICAL ISOLATES; ENTEROCOCCUS FAECIUM; GLYCOCONJUGATE VACCINES; HIGH MOLECULAR WEIGHT; INFECTION MODELS; LIPOTEICHOIC ACIDS; MULTIDRUG RESISTANTS; PASSIVE PROTECTION;

ANTIBODIES;

BACTERIAL VACCINE; CARRIER PROTEIN; CRM 197 PROTEIN; LEVAN; LIPOTEICHOIC ACID; POLYSACCHARIDE CRM 197 PROTEIN CONJUGATE; UNCLASSIFIED DRUG; 5,7-DIACETAMIDO-8-O-ACETYL-3,5,7,9-TETRADEOXY-GLYCERO-TALO-NONULOSONIC ACID; ALTRURONIC ACID; ANTIINFECTIVE AGENT; ANTISERUM; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; BACTERIUM ANTIBODY; CRM197 (NON-TOXIC VARIANT OF DIPHTHERIA TOXIN); FRUCTAN; LIPOPOLYSACCHARIDE; OPSONIN; SIALIC ACID DERIVATIVE; TEICHOIC ACID; URONIC ACID; VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY ISOLATION; ANTIBODY SPECIFICITY; ARTICLE; BACTERIAL LOAD; CONJUGATION; CONTROLLED STUDY; ENTEROCOCCAL INFECTION; ENTEROCOCCUS FAECIUM INFECTION; FLOW CYTOMETRY; GLYCOSYLATION; INFECTION PREVENTION; MOLECULAR RECOGNITION; MOUSE; MULTIDRUG RESISTANCE; NONHUMAN; PASSIVE IMMUNIZATION; PHAGOCYTOSIS; PRIORITY JOURNAL; VACCINATION; ANIMAL; BIOSYNTHESIS; BLOOD; CARBOHYDRATE ANALYSIS; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; ENTEROCOCCUS FAECIUM; FEMALE; GENETICS; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMAN; IMMUNOLOGY; MICROBIOLOGY; MOLECULAR GENETICS; RABBIT;

BACTERIA (MICROORGANISMS); ENTEROCOCCUS FAECIUM; ORYCTOLAGUS CUNICULUS;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL LOAD; BACTERIAL PROTEINS; BACTERIAL VACCINES; CARBOHYDRATE SEQUENCE; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ENTEROCOCCUS FAECIUM; FEMALE; FRUCTANS; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMANS; IMMUNE SERA; LIPOPOLYSACCHARIDES; MICE; MOLECULAR SEQUENCE DATA; OPSONIN PROTEINS; RABBITS; SIALIC ACIDS; TEICHOIC ACIDS; URONIC ACIDS; VACCINES, CONJUGATE;

EID: 84939156463     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.655852     Document Type: Article

References (64)

1. Theilacker, C., Jonas, D., Huebner, J., Bertz, H., and Kern, W. V. (2009) Outcomes of invasive infection due to vancomycin-resistant Enterococcus faecium during a recent outbreak. Infection 37, 540-543
2. Fernández Guerrero, M. L., Goyenechea, A., Verdejo, C., Roblas, R. F., and de Górgolas, M. (2007) Enterococcal endocarditis on native and prosthetic valves: a review of clinical and prognostic factors with emphasis on hospital-acquired infections as a major determinant of outcome. Medicine 86, 363-377
3. Joels, C. S., Matthews, B. D., Sigmon, L. B., Hasan, R., Lohr, C. E., Kercher, K. W., Norton, J., Sing, R. F., and Heniford, B. T. (2003) Clinical characteristics and outcomes of surgical patients with vancomycin-resistant enterococcal infections. Am. Surg. 69, 514-519
4. Sievert, D. M., Ricks, P., Edwards, J. R., Schneider, A., Patel, J., Srinivasan, A., Kallen, A., Limbago, B., Fridkin, S., National Healthcare Safety Network (NHSN) Team and Participating NHSN Facilities. (2013) Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009-2010. Infect. Control Hosp. Epidemiol. 34, 1-14
5. Hidron, A. I., Edwards, J. R., Patel, J., Horan, T. C., Sievert, D. M., Pollock, D. A., Fridkin, S. K., National Healthcare Safety Network Team, Participating National Healthcare Safety Network Facilities. (2008) NHSN annual update: antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007. Infect. Control Hosp. Epidemiol. 29, 996-1011; Correction (2009) Infect. Control Hosp. Epidemiol. 30, 107
6. Arias, C. A., and Murray, B. E. (2012) The rise of the Enterococcus: beyond vancomycin resistance. Nat. Rev. Microbiol. 10, 266-278
7. Willems, R. J., and van Schaik, W. (2009) Transition of Enterococcus faecium from commensal organism to nosocomial pathogen. Future Microbiol. 4, 1125-1135
8. Edmond, M. B., Ober, J. F., Dawson, J. D., Weinbaum, D. L., and Wenzel, R. P. (1996) Vancomycin-resistant enterococcal bacteremia: natural history and attributable mortality. Clin. Infect. Dis. 23, 1234-1239
9. Vergis, E. N., Hayden, M. K., Chow, J. W., Snydman, D. R., Zervos, M. J., Linden, P. K., Wagener, M. M., Schmitt, B., and Muder, R. R. (2001) Determinants of vancomycin resistance and mortality rates in enterococcal bacteremia. A prospective multicenter study. Ann. Int. Med. 135, 484-492
10. Schulte, B., Heininger, A., Autenrieth, I. B., and Wolz, C. (2008) Emergence of increasing linezolid-resistance in enterococci in a post-outbreak situation with vancomycin-resistant Enterococcus faecium. Epidemiol. Infect. 136, 1131-1133
11. Allen, G. P., and Bierman, B. C. (2009) In vitro analysis of resistance selection by linezolid in vancomycin-susceptible and -resistant Enterococcus faecalis and Enterococcus faecium. Int. J. Antimicrob. Agents 34, 21-24
12. Tran, T. T., Panesso, D., Gao, H., Roh, J. H., Munita, J. M., Reyes, J., Diaz, L., Lobos, E. A., Shamoo, Y., Mishra, N. N., Bayer, A. S., Murray, B. E., Weinstock, G. M., and Arias, C. A. (2013) Whole-genome analysis of a daptomycin-susceptible Enterococcus faecium strain and its daptomycinresistant variant arising during therapy. Antimicrob. Agents Chemother. 57, 261-268
13. Arias, C. A., Torres, H. A., Singh, K. V., Panesso, D., Moore, J., Wanger, A., and Murray, B. E. (2007) Failure of daptomycin monotherapy for endocarditis caused by an Enterococcus faecium strain with vancomycin-resistant and vancomycin-susceptible subpopulations and evidence of in vivo loss of the vanA gene cluster. Clin. Infect. Dis. 45, 1343-1346
14. Arias, C. A., Panesso, D., McGrath, D. M., Qin, X., Mojica, M. F., Miller, C., Diaz, L., Tran, T. T., Rincon, S., Barbu, E. M., Reyes, J., Roh, J. H., Lobos, E., Sodergren, E., Pasqualini, R., et al. (2011) Genetic basis for in vivo daptomycin resistance in enterococci. N. Engl. J. Med. 365, 892-900
15. de Roux, A., Schmöle-Thoma, B., Schmöele-Thoma, B., Siber, G. R., Hackell, J. G., Kuhnke, A., Ahlers, N., Baker, S. A., Razmpour, A., Emini, E. A., Fernsten, P. D., Gruber, W. C., Lockhart, S., Burkhardt, O., Welte, T., and Lode, H. M. (2008) Comparison of pneumococcal conjugate polysaccharide and free polysaccharide vaccines in elderly adults: conjugate vaccine elicits improved antibacterial immune responses and immunological memory. Clin. Infect. Dis. 46, 1015-1023
16. Anderson, A. S., Miller, A. A., Donald, R. G., Scully, I. L., Nanra, J. S., Cooper, D., and Jansen, K. U. (2012) Development of a multicomponent Staphylococcus aureus vaccine designed to counter multiple bacterial virulence factors. Hum. Vaccin. Immunother. 8, 1585-1594
17. Paoletti, L. C., and Madoff, L. C. (2002) Vaccines to prevent neonatal GBS infection. Semin. Neonatol. 7, 315-323
18. Palmer, K. L., Godfrey, P., Griggs, A., Kos, V. N., Zucker, J., Desjardins, C., Cerqueira, G., Gevers, D., Walker, S., Wortman, J., Feldgarden, M., Haas, B., Birren, B., and Gilmore, M. S. (2012) Comparative genomics of enterococci: variation in Enterococcus faecalis, clade structure in E. faecium, and defining characteristics of E. gallinarum and E. casseliflavus. mBio 3, e00318-00311
19. Bychowska, A., Theilacker, C., Czerwicka, M., Marszewska, K., Huebner, J., Holst, O., Stepnowski, P., and Kaczyński, Z. (2011) Chemical structure of wall teichoic acid isolated from Enterococcus faecium strain U0317. Carbohydr. Res. 346, 2816-2819
20. Huebner, J., Wang, Y., Krueger, W. A., Madoff, L. C., Martirosian, G., Boisot, S., Goldmann, D. A., Kasper, D. L., Tzianabos, A. O., and Pier, G. B. (1999) Isolation and chemical characterization of a capsular polysaccharide antigen shared by clinical isolates of Enterococcus faecalis and vancomycin-resistant Enterococcus faecium. Infect. Immun. 67, 1213-1219
21. Arduino, R. C., Jacques-Palaz, K., Murray, B. E., and Rakita, R. M. (1994) Resistance of Enterococcus faecium to neutrophil-mediated phagocytosis. Infect. Immun. 62, 5587-5594
22. Qin, X., Galloway-Peña, J. R., Sillanpaa, J., Roh, J. H., Nallapareddy, S. R., Chowdhury, S., Bourgogne, A., Choudhury, T., Muzny, D. M., Buhay, C. J., Ding, Y., Dugan-Rocha, S., Liu, W., Kovar, C., Sodergren, E., et al. (2012) Complete genome sequence of Enterococcus faecium strain TX16 and comparative genomic analysis of Enterococcus faecium genomes. BMC Microbiol. 12, 135
23. Lam, M. M., Seemann, T., Bulach, D. M., Gladman, S. L., Chen, H., Haring, V., Moore, R. J., Ballard, S., Grayson, M. L., Johnson, P. D., Howden, B. P., and Stinear, T. P. (2012) Comparative analysis of the first complete Enterococcus faecium genome. J. Bacteriol. 194, 2334-2341
24. Willems, R. J., Top, J., van Schaik, W., Leavis, H., Bonten, M., Sirén, J., Hanage, W. P., and Corander, J. (2012) Restricted gene flow among hospital subpopulations of Enterococcus faecium. mBio 3, e00151-00112
25. Rakita, R. M., Quan, V. C., Jacques-Palaz, K., Singh, K. V., Arduino, R. C., Mee, M., and Murray, B. E. (2000) Specific antibody promotes opsonization and PMN-mediated killing of phagocytosis-resistant Enterococcus faecium. FEMS Immunol. Med. Microbiol. 28, 291-299
26. Leendertse, M., Willems, R. J., Giebelen, I. A., Roelofs, J. J., Bonten, M. J., and van der Poll, T. (2009) Neutrophils are essential for rapid clearance of Enterococcus faecium in mice. Infect. Immun. 77, 485-491
27. Thurlow, L. R., Thomas, V. C., and Hancock, L. E. (2009) Capsular polysaccharide production in Enterococcus faecalis and contribution of CpsF to capsule serospecificity. J. Bacteriol. 191, 6203-6210
28. Trevelyan, W. E., Forrest, R. S., and Harrison, J. S. (1952) Determination of yeast carbohydrates with the anthrone reagent. Nature 170, 626-627
29. Dische, Z., and Shettles, L. B. (1948) A specific color reaction of methylpentoses and a spectrophotometric micromethod for their determination. J. Biol. Chem. 175, 595-603
30. Lees, A., Nelson, B. L., and Mond, J. J. (1996) Activation of soluble polysaccharides with 1-cyano-4-dimethylaminopyridinium tetrafluoroborate for use in protein-polysaccharide conjugate vaccines and immunological reagents. Vaccine 14, 190-198
31. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275
32. Sawardeker, J. S., Sloneker, J. H., and Jeanes, A. (1965) Quantitative determination of monosaccharides as their alditol acetates by gas-liquid chromatography. Anal. Chem. 10.1021/ac60231a048
33. Ciucanu, J., and Kerek, F. (1984) A simple and rapid method for the permethylation of carbohydrates. Carbohydr. Res. 131, 209-217
34. Clarke, A. J. (1993) Compositional analysis of peptidoglycan by high-performance anion-exchange chromatography. Anal. Biochem. 212, 344-350
35. Huebner, J., Quaas, A., Krueger, W. A., Goldmann, D. A., and Pier, G. B. (2000) Prophylactic and therapeutic efficacy of antibodies to a capsular polysaccharide shared among vancomycin-sensitive and -resistant enterococci. Infect. Immun. 68, 4631-4636
36. Schoenhofen, I. C., Vinogradov, E., Whitfield, D. M., Brisson, J.-R., and Logan, S. M. (2009) The CMP-legionaminic acid pathway in Campylobacter: biosynthesis involving novel GDP-linked precursors. Glycobiology 19, 715-725
37. Jolley, K. A., and Maiden, M. C. (2010) BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11, 595
38. Schwartz, S., Zhang, Z., Frazer, K. A., Smit, A., Riemer, C., Bouck, J., Gibbs, R., Hardison, R., and Miller, W. (2000) PipMaker-a web server for aligning two genomic DNA sequences. Genome Res. 10, 577-586
39. Matulová, M., Husárová, S., Capek, P., Sancelme, M., and Delort, A.-M. (2011) NMR structural study of fructans produced by Bacillus sp. 3B6, bacterium isolated in cloud water. Carbohydr. Res. 346, 501-507
40. St Swierzko, A., Shashkov, A. S., Senchenkova, S. N., Toukach, F. V., Ziolkowski, A., Cedzynski, M., Paramonov, N. A., Kaca, W., and Knirel, Y. A. (1996) Structural and serological studies of the O-specific polysaccharide of the bacterium Proteus mirabilis O10 containing L-altruronic acid, a new component of O-antigens. FEBS Lett. 398, 297-302
41. Theilacker, C., Kaczynski, Z., Kropec, A., Fabretti, F., Sange, T., Holst, O., and Huebner, J. (2006) Opsonic antibodies to Enterococcus faecalis strain 12030 are directed against lipoteichoic acid. Infect. Immun. 74, 5703-5712
42. Weidenmaier, C., and Peschel, A. (2008) Teichoic acids and related cellwall glycopolymers in Gram-positive physiology and host interactions. Nat. Rev. Microbiol. 6, 276-287
43. Knirel, Y. A., Shashkov, A. S., Tsvetkov, Y. E., Jansson, P.-E., and Zãhringer, U. (2003) 5,7-Diamino-3,5,7,9-tetradeoxynon-2-ulosonic acids in bacterial glycopolymers: chemistry and biochemistry. Adv. Carbohydr. Chem. Biochem. 58, 371-417
44. Palmer, K. L., Carniol, K., Manson, J. M., Heiman, D., Shea, T., Young, S., Zeng, Q., Gevers, D., Feldgarden, M., Birren, B., and Gilmore, M. S. (2010) High-quality draft genome sequences of 28 Enterococcus sp. isolates. J. Bacteriol. 192, 2469-2470
45. van Schaik, W., Top, J., Riley, D. R., Boekhorst, J., Vrijenhoek, J. E., Schapendonk, C. M., Hendrickx, A. P., Nijman, I. J., Bonten, M. J., Tettelin, H., and Willems, R. J. (2010) Pyrosequencing-based comparative genome analysis of the nosocomial pathogen Enterococcus faecium and identification of a large transferable pathogenicity island. BMC Genomics 11, 239
46. Clewell, D. B., Tomich, P. K., Gawron-Burke, M. C., Franke, A. E., Yagi, Y., and An, F. Y. (1982) Mapping of Streptococcus faecalis plasmids pAD1 and pAD2 and studies relating to transposition of Tn917. J. Bacteriol. 152, 1220-1230
47. Teng, F., Singh, K. V., Bourgogne, A., Zeng, J., and Murray, B. E. (2009) Further characterization of the epa gene cluster and Epa polysaccharides of Enterococcus faecalis. Infect. Immun. 77, 3759-3767
48. Hsu, C. T., Ganong, A. L., Reinap, B., Mourelatos, Z., Huebner, J., and Wang, J. Y. (2006) Immunochemical characterization of polysaccharide antigens from six clinical strains of Enterococci. BMC Microbiol. 6, 62
49. Koczan, J. M., McGrath, M. J., Zhao, Y., and Sundin, G. W. (2009) Contribution of Erwinia amylovora exopolysaccharides amylovoran and levan to biofilm formation: implications in pathogenicity. Phytopathology 99, 1237-1244
50. Cescutti, P., Impallomeni, G., Garozzo, D., Sturiale, L., Herasimenka, Y., Lagatolla, C., and Rizzo, R. (2003) Exopolysaccharides produced by a clinical strain of Burkholderia cepacia isolated from a cystic fibrosis patient. Carbohydr. Res. 338, 2687-2695
51. Harding, S. E., Abdelhameed, A. S., Morris, G. A., Adams, G., Laloux, O., Cerny, L., Bonnier, B., Duvivier, P., Conrath, K., and Lenfant, C. (2012) Solution properties of capsular polysaccharides from Streptococcus pneumoniae. Carbohydr. Polym. 90, 237-242
52. Theilacker, C., Kaczyński, Z., Kropec, A., Sava, I., Ye, L., Bychowska, A., Holst, O., and Huebner, J. (2011) Serodiversity of opsonic antibodies against Enterococcus faecalis-glycans of the cell wall revisited. PLoS ONE 6, e17839
53. Hancock, L. E., and Gilmore, M. S. (2002) The capsular polysaccharide of Enterococcus faecalis and its relationship to other polysaccharides in the cell wall. Proc. Natl. Acad. Sci. U.S.A. 99, 1574-1579
54. Tóth, A., Medgyes, A., Bajza, I., Lipták, A., Batta, G., Kontrohr, T., Péterffy, K., and Pozsgay, V. (2000) Synthesis of the repeating unit of the O-specific polysaccharide of Shigella sonnei and quantitation of its serologic activity. Bioorg. Med. Chem. Lett. 10, 19-21
55. Hermansson, K., Kenne, L., Lindberg, B., Arie, B., Brown, R. G., and Stewart, J. E. (1990) Structural studies of the capsular polysaccharide from Aerococcus viridans var. homari. Carbohydr. Res. 208, 145-152
56. Knirel, Y. A., Rietschel, E. T., Marre, R., and Zähringer, U. (1994) The structure of the O-specific chain of Legionella pneumophila serogroup 1 lipopolysaccharide. Eur. J. Biochem. 221, 239-245
57. Palusiñska-Szysz, M., and Russa, R. (2009) Chemical structure and biological significance of lipopolysaccharide from Legionella. Recent Pat. Anti-infect. Drug Discov. 4, 96-107
58. Zunk, M., and Kiefel, M. J. (2014) The occurrence and biological significance of the [small α]-keto-sugars pseudaminic acid and legionaminic acid within pathogenic bacteria. RSC Adv. 4, 3413-3421
59. Carlin, A. F., Lewis, A. L., Varki, A., and Nizet, V. (2007) Group B streptococcal capsular sialic acids interact with siglecs (immunoglobulin-like lectins) on human leukocytes. J. Bacteriol. 189, 1231-1237
60. Vimr, E., and Lichtensteiger, C. (2002) To sialylate, or not to sialylate: that is the question. Trends Microbiol. 10, 254-257
61. MacLean, L. L., Vinogradov, E., Pagotto, F., and Perry, M. B. (2011) Characterization of the lipopolysaccharide O-antigen of Cronobacter turicensis HPB3287 as a polysaccharide containing a 5,7-diacetamido-3,5,7,9-tetradeoxy-D-glycero-D-galacto-non-2-ulosonic acid (legionaminic acid) residue. Carbohydr. Res. 346, 2589-2594
62. Toniolo, C., Balducci, E., Romano, M. R., Proietti, D., Ferlenghi, I., Grandi, G., Berti, F., Ros, I. M., and Janulczyk, R. (2015) Streptococcus agalactiae capsule polymer length and attachment is determined by the proteins CpsABCD. J. Biol. Chem. 290, 9521-9532
63. Morath, S., Geyer, A., and Hartung, T. (2001) Structure-function relationship of cytokine induction by lipoteichoic acid from Staphylococcus aureus. J. Exp. Med. 193, 393-397
64. Clutterbuck, E. A., Lazarus, R., Yu, L.-M., Bowman, J., Bateman, E. A., Diggle, L., Angus, B., Peto, T. E., Beverley, P. C., Mant, D., and Pollard, A. J. (2012) Pneumococcal conjugate and plain polysaccharide vaccines have divergent effects on antigen-specific B cells. J. Infect. Dis. 205, 1408-1416