Protective effect of DNA vaccine encoding Pseudomonas exotoxin A and PcrV against acute pulmonary P. aeruginosa infection

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Jiang, Mingzi ^a   Yao, Jing ^a   Feng, Ganzhu ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; CPG OLIGODEOXYNUCLEOTIDE; CYTOKINE; DNA VACCINE; IMMUNOGLOBULIN G; PROTEIN PCRV; PSEUDOMONAS EXOTOXIN; PSEUDOMONAS EXOTOXIN A; UNCLASSIFIED DRUG; ANTIGEN V, PSEUDOMONAS; BACTERIAL TOXIN; CPG ODN 1826; EXOTOXIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; OLIGODEOXYRIBONUCLEOTIDE; PORE FORMING CYTOTOXIC PROTEIN; PSEUDOMONAS VACCINE; TOXA PROTEIN, PSEUDOMONAS AERUGINOSA; VIRULENCE FACTOR;

ACUTE DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CELL PROLIFERATION; CYTOKINE RELEASE; DRUG EFFICACY; EMBRYO; EUKARYOTIC CELL; FEMALE; GENE DELIVERY SYSTEM; GENE INSERTION; GENE MUTATION; GENETIC CODE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOGLOBULIN BLOOD LEVEL; MOUSE; NONHUMAN; PSEUDOMONAS PNEUMONIA; SPLEEN CELL; TYPE III SECRETION SYSTEM; ANIMAL; DISEASE MODEL; DRUG EFFECTS; GENETICS; IMMUNOLOGY; LUNG; METABOLISM; MICROBIOLOGY; MUTATION; PATHOLOGY; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS;

ADP RIBOSE TRANSFERASES; ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; DISEASE MODELS, ANIMAL; EXOTOXINS; FEMALE; LUNG; MICE; MUTATION; OLIGODEOXYRIBONUCLEOTIDES; PORE FORMING CYTOTOXIC PROTEINS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; PSEUDOMONAS VACCINES; VACCINES, DNA; VIRULENCE FACTORS;

EID: 84900343586     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096609     Document Type: Article

References (66)

1. Kipnis E, Sawa T, Wiener-Kronish J (2006) Targeting mechanisms of Pseudomonas aeruginosa pathogenesis. Médecine et maladies infectieuses 36: 78-91. (Pubitemid 43294628)
2. Sharma A, Krause A, Worgall S (2011) Recent developments for Pseudomonas vaccines. Human vaccines 7: 999-1011.
3. Veesenmeyer J, Hauser A, Lisboa T, Rello J (2009) Pseudomonas aeruginosa virulence and therapy: evolving translational strategies. Crit Care Med 37: 1777-1786.
4. Pier G (2005) Application of vaccine technology to prevention of Pseudomonas aeruginosa infections. Expert review of vaccines 4: 645-656.
5. Kutzler MA, Weiner DB (2008) DNA vaccines: ready for prime time? Nat Rev Genet 9: 776-788.
6. Klinman DM, Klaschik S, Tross D, Shirota H, Steinhagen F (2010) FDA guidance on prophylactic DNA vaccines: analysis and recommendations. Vaccine 28: 2801-2805.
7. Saade F, Petrovsky N (2012) Technologies for enhanced efficacy of DNA vaccines. Expert Rev Vaccines 11: 189-209.
8. Liu M (2011) DNA vaccines: an historical perspective and view to the future. Immunol Rev 239: 62-84.
9. Gurunathan S, Klinman D, Seder R (2000) DNA vaccines: immunology, application, and optimization*. Annu Rev Immunol 18: 927-974. (Pubitemid 30365401)
10. Nabel G (2004) Genetic, cellular and immune approaches to disease therapy: past and future. Nat Med 10: 135-141.
11. Staczek J, Gilleland L, Heyde H, Gilleland H (2006) DNA vaccines against chronic lung infections by Pseudomonas aeruginosa. FEMS Immunology & Medical Microbiology 37: 147-153.
12. Price BM, Galloway DR, Baker NR, Gilleland LB, Staczek J, et al. (2001) Protection against Pseudomonas aeruginosa chronic lung infection in mice by genetic immunization against outer membrane protein F (OprF) of P. aeruginosa. Infection and immunity 69: 3510-3515. (Pubitemid 32332260)
13. Price BM, Barten Legutki J, Galloway DR, Specht BU, Gilleland LB, et al. (2002) Enhancement of the protective efficacy of an oprF DNA vaccine against Pseudomonas aeruginosa. FEMS Immunology & Medical Microbiology 33: 89-99. (Pubitemid 34607525)
14. Saha S, Takeshita F, Sasaki S, Matsuda T, Tanaka T, et al. (2006) Multivalent DNA vaccine protects mice against pulmonary infection caused by Pseudomonas aeruginosa. Vaccine 24: 6240-6249. (Pubitemid 44247243)
15. Saha S, Takeshita F, Matsuda T, Jounai N, Kobiyama K, et al. (2007) Blocking of the TLR5 activation domain hampers protective potential of flagellin DNA vaccine. The Journal of Immunology 179: 1147-1154.
16. Shiau J, Tang T, Shih Y, Tai C, Sung Y, et al. (2000) Mice immunized with DNA encoding a modified Pseudomonas aeruginosa exotoxin A develop protective immunity against exotoxin intoxication. Vaccine 19: 1106-1112. (Pubitemid 32008275)
17. Denis-Mize KS, Price BM, Baker NR, Galloway DR (2000) Analysis of immunization with DNA encoding Pseudomonas aeruginosa exotoxin A. FEMS Immunol Med Microbiol 27: 147-154. (Pubitemid 30047093)
18. Sadikot R, Blackwell T, Christman J, Prince A (2005) Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am J Respir Crit Care Med 171: 1209-1223. (Pubitemid 40740727)
19. Bleves S, Viarre V, Salacha R, Michel G, Filloux A, et al. (2010) Protein secretion systems in Pseudomonas aeruginosa: A wealth of pathogenic weapons. International journal of medical microbiology : IJMM 300: 534-543.
20. Kudoh I, Wiener-Kronish JP, Hashimoto S, Pittet J-F, Frank D (1994) Exoproduct secretions of Pseudomonas aeruginosa strains influence severity of alveolar epithelial injury. American Journal of Physiology-Lung Cellular and Molecular Physiology 267: L551-L556. (Pubitemid 24351854)
21. Sawa T, Ohara M, Kurahashi K, Twining SS, Frank DW, et al. (1998) In Vitro Cellular Toxicity PredictsPseudomonas aeruginosa Virulence in Lung Infections. Infection and immunity 66: 3242-3249. (Pubitemid 28303122)
22. Shaver CM, Hauser AR (2004) Relative Contributions of Pseudomonas aeruginosa ExoU, ExoS, and ExoT to Virulence in the Lung. Infection and Immunity 72: 6969-6977. (Pubitemid 39552365)
23. Jyot J, Balloy V, Jouvion G, Verma A, Touqui L, et al. (2011) Type II secretion system of Pseudomonas aeruginosa: in vivo evidence of a significant role in death due to lung infection. J Infect Dis 203: 1369-1377.
24. Cianciotto NP (2005) Type II secretion: a protein secretion system for all seasons. Trends Microbiol 13: 581-588.
25. Wolf P, Elsässer-Beile U (2009) Pseudomonas exotoxin A: From virulence factor to anti-cancer agent. International Journal of Medical Microbiology 299: 161-176.
26. Schultz MJ, Speelman P, Zaat SAJ, Hack CE, van Deventer SJH, et al. (2000) The effect of Pseudomonas exotoxin A on cytokine production in whole blood exposed to Pseudomonas aeruginosa. FEMS Immunology & Medical Microbiology 29: 227-232.
27. Schultz MJ, Rijneveld AW, Florquin S, Speelman P, Van Deventer SJ, et al. (2001) Impairment of host defence by exotoxin A in Pseudomonas aeruginosa pneumonia in mice. J Med Microbiol 50: 822-827. (Pubitemid 32802845)
28. Chieda Y, Iiyama K, Lee JM, Kusakabe T, Yasunaga-Aoki C, et al. (2011) Virulence of an exotoxin A-deficient strain of Pseudomonas aeruginosa toward the silkworm, Bombyx mori. Microb Pathog 51: 407-414.
29. Chen TY, Shang HF, Chen TL, Lin CP, Hui CF, et al. (1999) Recombinant protein composed of Pseudomonas exotoxin A, outer membrane proteins I and F as vaccine against P. aeruginosa infection. Appl Microbiol Biotechnol 52: 524-533.
30. Johansen HK, Espersen F, Cryz SJ Jr, Hougen HP, Fomsgaard A, et al. (1994) Immunization with Pseudomonas aeruginosa vaccines and adjuvant can modulate the type of inflammatory response subsequent to infection. Infect Immun 62: 3146-3155. (Pubitemid 24232094)
31. Lang AB, Horn MP, Imboden MA, Zuercher AW (2004) Prophylaxis and therapy of Pseudomonas aeruginosa infection in cystic fibrosis and immunocompromised patients. Vaccine 22 Suppl 1: S44-48. (Pubitemid 39575371)
32. Tanomand A, Farajnia S, Najar Peerayeh S, Majidi J (2013) Cloning, expression and characterization of recombinant exotoxin A-flagellin fusion protein as a new vaccine candidate against Pseudomonas aeruginosa infections. Iran Biomed J 17: 1-7.
33. Hauser AR, Cobb E, Mariscal D, Engel JN, Rello J (2002) Type III protein secretion is associated with poor clinical outcomes in patients with ventilator-associated pneumonia caused by Pseudomonas aeruginosa. Critical Care Medicine 30: 521-528. (Pubitemid 34214611)
34. Ajayi T, Allmond LR, Sawa T, Wiener-Kronish JP (2003) Single-Nucleotide-Polymorphism Mapping of the Pseudomonas aeruginosa Type III Secretion Toxins for Development of a Diagnostic Multiplex PCR System.
35. Sato H, Frank DW (2011) Multi-functional characteristics of the Pseudomonas aeruginosa type III needle-tip protein, PcrV; comparison to orthologs in other Gram-negative bacteria. Frontiers in microbiology 2.
36. Sawa T, Yahr TL, Ohara M, Kurahashi K, Gropper MA, et al. (1999) Active and passive immunization with the Pseudomonas V antigen protects against type III intoxication and lung injury. Nature medicine 5: 392-398. (Pubitemid 29180576)
37. Goure J, Pastor A, Faudry E, Chabert J, Dessen A, et al. (2004) The V antigen of Pseudomonas aeruginosa is required for assembly of the functional PopB/PopD translocation pore in host cell membranes. Infect Immun 72: 4741-4750. (Pubitemid 38989335)
38. Gebus C, Faudry E, Bohn YS, Elsen S, Attree I (2008) Oligomerization of PcrV and LcrV, protective antigens of Pseudomonas aeruginosa and Yersinia pestis. J Biol Chem 283: 23940-23949.
39. Engel J, Balachandran P (2009) Role of Pseudomonas aeruginosa type III effectors in disease. Curr Opin Microbiol 12: 61-66.
40. Sato H, Frank DW (2011) Multi-Functional Characteristics of the Pseudomonas aeruginosa Type III Needle-Tip Protein, PcrV; Comparison to Orthologs in other Gram-negative Bacteria. Front Microbiol 2: 142.
41. Galle M, Carpentier I, Beyaert R (2012) Structure and function of the Type III secretion system of Pseudomonas aeruginosa. Curr Protein Pept Sci 13: 831-842.
42. Allmond LR, Ajayi T, Moriyama K, Wiener-Kronish JP, Sawa T (2004) V-antigen genotype and phenotype analyses of clinical isolates of Pseudomonas aeruginosa. J Clin Microbiol 42: 3857-3860. (Pubitemid 39045731)
43. Klinman DM, Klaschik S, Sato T, Tross D (2009) CpG oligonucleotides as adjuvants for vaccines targeting infectious diseases. Adv Drug Deliv Rev 61: 248-255.
44. Bode C, Zhao G, Steinhagen F, Kinjo T, Klinman DM (2011) CpG DNA as a vaccine adjuvant. Expert Rev Vaccines 10: 499-511.
45. Jensen KM, Melchjorsen J, Dagnaes-Hansen F, Sorensen UB, Laursen RR, et al. (2012) Timing of Toll-like receptor 9 agonist administration in pneumococcal vaccination impacts both humoral and cellular immune responses as well as nasopharyngeal colonization in mice. Infect Immun 80: 1744-1752.
46. Li H, Ghosh SK (2010) CpG ODN 1826 Enhances the Efficacy of Idiotype DNA Vaccine Administered Intrasplenically. Open Vaccine Journal 3: 127-133.
47. Jiang T, Zhao H, Li X-F, Deng Y-Q, Liu J, et al. (2011) CpG oligodeoxynucleotides protect against the 2009 H1N1 pandemic influenza virus infection in a murine model. Antiviral Research 89: 124-126.
48. Yuan S, Qiao T, Chen W (2011) CpG oligodeoxynucleotide 1826 enhances the Lewis lung cancer response to radiotherapy in murine tumor. Cancer Biotherapy & Radiopharmaceuticals 26: 203-208.
49. Fukushima J, Yamamoto S, Morihara K, Atsumi Y, Takeuchi H, et al. (1989) Structural gene and complete amino acid sequence of Pseudomonas aeruginosa IFO 3455 elastase. Journal of bacteriology 171: 1698-1704. (Pubitemid 19080811)
50. Lee PC, Stopford CM, Svenson AG, Rietsch A (2010) Control of effector export by the Pseudomonas aeruginosa type III secretion proteins PcrG and PcrV. Mol Microbiol 75: 924-941.
51. Challa S, Barrette R, Rood D, Zinckgraf J, French R, et al. (2007) Non-toxic Pseudomonas aeruginosa exotoxin A expressing the FMDV VP1 G-H loop for mucosal vaccination of swine against foot and mouth disease virus. Vaccine 25: 3328-3337. (Pubitemid 46527997)
52. Lukac M, Pier G, Collier R (1988) Toxoid of Pseudomonas aeruginosa exotoxin A generated by deletion of an active-site residue. Infection and immunity 56: 3095-3098.
53. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63.
54. Roy-Burman A, Savel RH, Racine S, Swanson BL, Revadigar NS, et al. (2001) Type III protein secretion is associated with death in lower respiratory and systemic Pseudomonas aeruginosa infections. J Infect Dis 183: 1767-1774. (Pubitemid 32523239)
55. Deng W, Li CY, Tong J, Zhang W, Wang DX (2012) Regulation of ENaC-mediated alveolar fluid clearance by insulin via PI3K/Akt pathway in LPS-induced acute lung injury. Respir Res 13: 29.
56. Galle M, Jin S, Bogaert P, Haegman M, Vandenabeele P, et al. (2012) The Pseudomonas aeruginosa type III secretion system has an exotoxin S/T/Y independent pathogenic role during acute lung infection. PLoS One 7: e41547.
57. Vance RE, Rietsch A, Mekalanos JJ (2005) Role of the type III secreted exoenzymes S, T, and Y in systemic spread of Pseudomonas aeruginosa PAO1 in vivo. Infect Immun 73: 1706-1713. (Pubitemid 40470759)
58. Carroll S, Collier R (1987) Active site of Pseudomonas aeruginosa exotoxin A. Glutamic acid 553 is photolabeled by NAD and shows functional homology with glutamic acid 148 of diphtheria toxin. Journal of Biological Chemistry 262: 8707-8711.
59. Lukac M, Collier RJ (1988) Restoration of enzymic activity and cytotoxicity of mutant, E553C, Pseudomonas aeruginosa exotoxin A by reaction with iodoacetic acid. J Biol Chem 263: 6146-6149.
60. Chen TY, Lin CP, Loa CC, Chen TL, Shang HF, et al. (1999) A nontoxic Pseudomonas exotoxin A induces active immunity and passive protective antibody against Pseudomonas exotoxin A intoxication. J Biomed Sci 6: 357-363. (Pubitemid 29436369)
61. Goure J, Pastor A, Faudry E, Chabert J, Dessen A, et al. (2004) The V Antigen of Pseudomonas aeruginosa Is Required for Assembly of the Functional PopB/PopD Translocation Pore in Host Cell Membranes. Infection and Immunity 72: 4741-4750. (Pubitemid 38989335)
62. Uppada SB, Bhat AA, Sah A, Donthamshetty RN (2011) Enhanced humoral and mucosal immune responses after intranasal immunization with chimeric multiple antigen peptide of LcrV antigen epitopes of Yersinia pestis coupled to palmitate in mice. Vaccine 29: 9352-9360.
63. Dibra D, Li S (2013) The cell-to-cell coordination between activated T cells and CpG-stimulated macrophages synergistically induce elevated levels of IL-10 via NF-kappaB1, STAT3, and CD40/CD154. Cell Commun Signal 11: 95.
64. Yao Y, Simard AR, Shi FD, Hao J (2013) IL-10-producing lymphocytes in inflammatory disease. Int Rev Immunol 32: 324-336.
65. Schultz MJ, Speelman P, Zaat SA, Hack CE, van Deventer SJ, et al. (2000) The effect of pseudomonas exotoxin A on cytokine production in whole blood exposed to Pseudomonas aeruginosa. FEMS Immunol Med Microbiol 29: 227-232.
66. Weimer ET, Lu H, Kock ND, Wozniak DJ, Mizel SB (2009) A Fusion Protein Vaccine Containing OprF Epitope 8, OprI, and Type A and B Flagellins Promotes Enhanced Clearance of Nonmucoid Pseudomonas aeruginosa. Infection and Immunity 77: 2356-2366.