NADH Oxidase Functions as an Adhesin in Streptococcus pneumoniae and Elicits a Protective Immune Response in Mice

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Muchnik, Lena ^a,b   Adawi, Asad ^a,b   Ohayon, Ariel ^a,b   Dotan, Shahar ^c   Malka, Itai ^a,b   Azriel, Shalhevet ^a,b   Shagan, Marilou ^a,b   Portnoi, Maxim ^a,b   Kafka, Daniel ^a,b   Nahmani, Hannie ^b   Porgador, Angel ^b   Gershoni, Johnatan M ^d   Morrison, Donald A ^e   Mitchell, Andrea ^f   Tal, Michael ^c   Ellis, Ronald ^c   Dagan, Ron ^a   Nebenzahl, Yaffa Mizrachi ^a,b  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^c NasVax Ltd   (Israel)

^d TEL AVIV UNIVERSITY   (Israel)

^e UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^f UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; CONTACTIN; CONTACTIN 4; ENZYME ANTIBODY; KALININ; NEUTRALIZING ANTIBODY; PEPTIDE DERIVATIVE; RECOMBINANT ENZYME; RECOMBINANT REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; RECOMBINANT VACCINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIOPHAGE; BACTERIUM ADHERENCE; CELL STRAIN; CELL STRAIN A549; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; EPITHELIUM CELL; FEMALE; HUMAN; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; IN VITRO STUDY; LONGITUDINAL STUDY; MOUSE; NONHUMAN; NOX GENE; NUCLEOTIDE SEQUENCE; PNEUMOCOCCAL INFECTION; STREPTOCOCCUS PNEUMONIAE; TARGET CELL;

ADHESINS, BACTERIAL; AEROBIOSIS; AGING; ANAEROBIOSIS; ANIMALS; BACTERIAL ADHESION; BACTERIAL VACCINES; CELL LINE; CHILD, PRESCHOOL; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; IMMUNITY; INFANT; MICE; MULTIENZYME COMPLEXES; NADH, NADPH OXIDOREDUCTASES; PEPTIDES; STREPTOCOCCUS PNEUMONIAE;

BACTERIA (MICROORGANISMS); MUS; STREPTOCOCCUS PNEUMONIAE;

EID: 84875984604     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061128     Document Type: Article

References (62)

1. Dagan R, Greenberg D, Jacobs M (2004) Pneumococcal infection; Feigin RD CJ, Demmler GJ, Kaplan S, editor: Saunders.
2. van der Poll T, Opal SM, (2009) Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet 374: 1543-1556.
3. Weinberger DM, Dagan R, Givon-Lavi N, Regev-Yochay G, Malley R, et al. (2008) Epidemiologic evidence for serotype-specific acquired immunity to pneumococcal carriage. J Infect Dis 197: 1511-1518.
4. Hicks LA, Harrison LH, Flannery B, Hadler JL, Schaffner W, et al. (2007) Incidence of pneumococcal disease due to non-pneumococcal conjugate vaccine (PCV7) serotypes in the United States during the era of widespread PCV7 vaccination, 1998-2004. J Infect Dis 196: 1346-1354.
5. Dagan R, Givon-Lavi N, Greenberg D, Fritzell B, Siegrist CA, (2010) Nasopharyngeal carriage of Streptococcus pneumoniae shortly before vaccination with a pneumococcal conjugate vaccine causes serotype-specific hyporesponsiveness in early infancy. J Infect Dis 201: 1570-1579.
6. Lofling J, Vimberg V, Battig P, Henriques-Normark B, (2011) Cellular interactions by LPxTG-anchored pneumococcal adhesins and their streptococcal homologues. Cell Microbiol 13: 186-197.
7. Moschioni M, Donati C, Muzzi A, Masignani V, Censini S, et al. (2008) Streptococcus pneumoniae contains 3 rlrA pilus variants that are clonally related. J Infect Dis 197: 888-896.
8. Bagnoli F, Moschioni M, Donati C, Dimitrovska V, Ferlenghi I, et al. (2008) A second pilus type in Streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells. J Bacteriol 190: 5480-5492.
9. Cundell DR, Weiser JN, Shen J, Young A, Tuomanen EI, (1995) Relationship between colonial morphology and adherence of Streptococcus pneumoniae. Infect Immun 63: 757-761.
10. Ogunniyi AD, Grabowicz M, Briles DE, Cook J, Paton JC, (2007) Development of a vaccine against invasive pneumococcal disease based on combinations of virulence proteins of Streptococcus pneumoniae. Infect Immun 75: 350-357.
11. Anderton JM, Rajam G, Romero-Steiner S, Summer S, Kowalczyk AP, et al. (2007) E-cadherin is a receptor for the common protein pneumococcal surface adhesin A (PsaA) of Streptococcus pneumoniae. Microb Pathog 42: 225-236.
12. Pracht D, Elm C, Gerber J, Bergmann S, Rohde M, et al. (2005) PavA of Streptococcus pneumoniae modulates adherence, invasion, and meningeal inflammation. Infect Immun 73: 2680-2689.
13. Rosenow C, Ryan P, Weiser JN, Johnson S, Fontan P, et al. (1997) Contribution of novel choline-binding proteins to adherence, colonization and immunogenicity of Streptococcus pneumoniae. Mol Microbiol 25: 819-829.
14. Zhang JR, Mostov KE, Lamm ME, Nanno M, Shimida S, et al. (2000) The polymeric immunoglobulin receptor translocates pneumococci across human nasopharyngeal epithelial cells. Cell 102: 827-837.
15. Elm C, Rohde M, Vaerman JP, Chhatwal GS, Hammerschmidt S, (2004) Characterization of the interaction of the pneumococcal surface protein SpsA with the human polymeric immunoglobulin receptor (hpIgR). Indian J Med Res 119 Suppl: 61-65.
16. Hammerschmidt S, Talay SR, Brandtzaeg P, Chhatwal GS, (1997) SpsA, a novel pneumococcal surface protein with specific binding to secretory immunoglobulin A and secretory component. Mol Microbiol 25: 1113-1124.
17. Pesakhov S, Benisty R, Sikron N, Cohen Z, Gomelsky P, et al. (2007) Effect of hydrogen peroxide production and the Fenton reaction on membrane composition of Streptococcus pneumoniae. Biochim Biophys Acta 1768: 590-597.
18. Yamamoto Y, Pargade V, Lamberet G, Gaudu P, Thomas F, et al. (2006) The Group B Streptococcus NADH oxidase Nox-2 is involved in fatty acid biosynthesis during aerobic growth and contributes to virulence. Mol Microbiol 62: 772-785.
19. Yu J, Bryant AP, Marra A, Lonetto MA, Ingraham KA, et al. (2001) Characterization of the Streptococcus pneumoniae NADH oxidase that is required for infection. Microbiology 147: 431-438.
20. Portnoi M, Ling E, Feldman G, Dagan R, Mizrachi-Nebenzahl Y, (2006) The vaccine potential of Streptococcus pneumoniae surface lectin- and non-lectin proteins. Vaccine 24: 1868-1873.
21. Avery OT, Macleod CM, McCarty M, (1944) Studies on the Chemical Nature of the Substance Inducing Transformation of Pneumococcal Types: Induction of Transformation by a Desoxyribonucleic Acid Fraction Isolated from Pneumococcus Type Iii. J Exp Med 79: 137-158.
22. Briles DE, Nahm M, Schroer K, Davie J, Baker P, et al. (1981) Antiphosphocholine antibodies found in normal mouse serum are protective against intravenous infection with type 3 Streptococcus pneumoniae. J Exp Med 153: 694-705.
23. Watson DA, Musher DM, (1990) Interruption of capsule production in Streptococcus pneumoniae serotype 3 by insertion of transposon Tn916. Infect Immun 58: 3135-3138.
24. Mizrachi Nebenzahl Y, Porat N, Lifshitz S, Novick S, Levi A, et al. (2004) Virulence of Streptococcus pneumoniae may be determined independently of capsular polysaccharide. FEMS Microbiol Lett 233: 147-152.
25. Mizrachi Nebenzahl Y, Bernstein A, Portnoi M, Shagan M, Rom S, et al. (2007) Streptococcus pneumoniae surface-exposed glutamyl tRNA synthetase, a putative adhesin, is able to induce a partially protective immune response in mice. J Infect Dis 196: 945-953.
26. Lifshitz S, Dagan R, Shani-Sekler M, Grossman N, Fleminger G, et al. (2002) Age-dependent preference in human antibody responses to Streptococcus pneumoniae polypeptide antigens. Clin Exp Immunol 127: 344-353.
27. Havarstein LS, Gaustad P, Nes IF, Morrison DA, (1996) Identification of the streptococcal competence-pheromone receptor. Mol Microbiol 21: 863-869.
28. Lieber M, Smith B, Szakal A, Nelson-Rees W, Todaro G, (1976) A continuous tumor-cell line from a human lung carcinoma with properties of type II alveolar epithelial cells. Int J Cancer 17: 62-70.
29. Balis JU, Bumgarner SD, Paciga JE, Paterson JF, Shelley SA, (1984) Synthesis of lung surfactant-associated glycoproteins by A549 cells: description of an in vitro model for human type II cell dysfunction. Exp Lung Res 6: 197-213.
30. Asano K, Chee CB, Gaston B, Lilly CM, Gerard C, et al. (1994) Constitutive and inducible nitric oxide synthase gene expression, regulation, and activity in human lung epithelial cells. Proc Natl Acad Sci U S A 91: 10089-10093.
31. Talbot UM, Paton AW, Paton JC, (1996) Uptake of Streptococcus pneumoniae by respiratory epithelial cells. Infect Immun 64: 3772-3777.
32. Daniely D, Portnoi M, Shagan M, Porgador A, Givon-Lavi N, et al. (2006) Pneumococcal 6-phosphogluconate-dehydrogenase, a putative adhesin, induces protective immune response in mice. Clin Exp Immunol 144: 254-263.
33. Blau K, Portnoi M, Shagan M, Kaganovich A, Rom S, et al. (2007) Flamingo cadherin: a putative host receptor for Streptococcus pneumoniae. J Infect Dis 195: 1828-1837.
34. Eldridge JH, Beagley KW, McGhee JR, (1987) Immunoregulation in the Peyer's patch microenvironment. Cellular basis for the enhanced responses by the B cells of X-linked immunodeficient CBA/N mice. J Immunol 139: 2255-2262.
35. Gingles NA, Alexander JE, Kadioglu A, Andrew PW, Kerr A, et al. (2001) Role of genetic resistance in invasive pneumococcal infection: identification and study of susceptibility and resistance in inbred mouse strains. Infect Immun 69: 426-434.
36. Freund NT, Enshell-Seijffers D, Gershoni JM, (2009) Phage display selection, analysis, and prediction of B cell epitopes. Curr Protoc Immunol Chapter 9: Unit 9 8.
37. Siegel JL, Hurst SF, Liberman ES, Coleman SE, Bleiweis AS, (1981) Mutanolysin-induced spheroplasts of Streptococcus mutants are true protoplasts. Infect Immun 31: 808-815.
38. Sela BA, Wang JL, Edelman GM, (1975) Isolation of lectins of different specificities on a single affinity adsorbent. J Biol Chem 250: 7535-7538.
39. Matsuzaki S, Jardon K, Maleysson E, D'Arpiany F, Canis M, et al. (2010) Carbon dioxide pneumoperitoneum, intraperitoneal pressure, and peritoneal tissue hypoxia: a mouse study with controlled respiratory support. Surg Endosc 24: 2871-2880.
40. Hoskins J, Alborn WE Jr, Arnold J, Blaszczak LC, Burgett S, et al. (2001) Genome of the bacterium Streptococcus pneumoniae strain R6. J Bacteriol 183: 5709-5717.
41. Poolman B, (1993) Energy transduction in lactic acid bacteria. FEMS Microbiol Rev 12: 125-147.
42. Konings WN, Otto R, (1983) Energy transduction and solute transport in streptococci. Antonie Van Leeuwenhoek 49: 247-257.
43. Auzat I, Chapuy-Regaud S, Le Bras G, Dos Santos D, Ogunniyi AD, et al. (1999) The NADH oxidase of Streptococcus pneumoniae: its involvement in competence and virulence. Mol Microbiol 34: 1018-1028.
44. Chhatwal GS, (2002) Anchorless adhesins and invasins of Gram-positive bacteria: a new class of virulence factors. Trends Microbiol 10: 205-208.
45. Hammerschmidt S, Wolff S, Hocke A, Rosseau S, Muller E, et al. (2005) Illustration of pneumococcal polysaccharide capsule during adherence and invasion of epithelial cells. Infect Immun 73: 4653-4667.
46. Hauck CR, Agerer F, Muenzner P, Schmitter T, (2006) Cellular adhesion molecules as targets for bacterial infection. Eur J Cell Biol 85: 235-242.
47. Malley R, Trzcinski K, Srivastava A, Thompson CM, Anderson PW, et al. (2005) CD4+ T cells mediate antibody-independent acquired immunity to pneumococcal colonization. Proc Natl Acad Sci U S A 102: 4848-4853.
48. Ring A, Weiser JN, Tuomanen EI, (1998) Pneumococcal trafficking across the blood-brain barrier. Molecular analysis of a novel bidirectional pathway. J Clin Invest 102: 347-360.
49. Yamauchi S, Mita S, Matsubara T, Fukuta M, Habuchi H, et al. (2000) Molecular cloning and expression of chondroitin 4-sulfotransferase. J Biol Chem 275: 8975-8981.
50. Van Eerdewegh P, Little RD, Dupuis J, Del Mastro RG, Falls K, et al. (2002) Association of the ADAM33 gene with asthma and bronchial hyperresponsiveness. Nature 418: 426-430.
51. Roche AM, King SJ, Weiser JN, (2007) Live attenuated Streptococcus pneumoniae strains induce serotype-independent mucosal and systemic protection in mice. Infect Immun 75: 2469-2475.
52. Goldblatt D, Hussain M, Andrews N, Ashton L, Virta C, et al. (2005) Antibody responses to nasopharyngeal carriage of Streptococcus pneumoniae in adults: a longitudinal household study. J Infect Dis 192: 387-393.
53. Ling E, Feldman G, Portnoi M, Dagan R, Overweg K, et al. (2004) Glycolytic enzymes associated with the cell surface of Streptococcus pneumoniae are antigenic in humans and elicit protective immune responses in the mouse. Clin Exp Immunol 138: 290-298.
54. Gordon SB, Irving GR, Lawson RA, Lee ME, Read RC, (2000) Intracellular trafficking and killing of Streptococcus pneumoniae by human alveolar macrophages are influenced by opsonins. Infect Immun 68: 2286-2293.
55. Ochs MM, Bartlett W, Briles DE, Hicks B, Jurkuvenas A, et al. (2008) Vaccine-induced human antibodies to PspA augment complement C3 deposition on Streptococcus pneumoniae. Microb Pathog 44: 204-214.
56. Dalia AB, Standish AJ, Weiser JN, (2010) Three surface exoglycosidases from Streptococcus pneumoniae, NanA, BgaA, and StrH, promote resistance to opsonophagocytic killing by human neutrophils. Infect Immun 78: 2108-2116.
57. Briles DE, Ades E, Paton JC, Sampson JS, Carlone GM, et al. (2000) Intranasal immunization of mice with a mixture of the pneumococcal proteins PsaA and PspA is highly protective against nasopharyngeal carriage of Streptococcus pneumoniae. Infect Immun 68: 796-800.
58. Adamou JE, Heinrichs JH, Erwin AL, Walsh W, Gayle T, et al. (2001) Identification and characterization of a novel family of pneumococcal proteins that are protective against sepsis. Infect Immun 69: 949-958.
59. Giefing C, Meinke AL, Hanner M, Henics T, Bui MD, et al. (2008) Discovery of a novel class of highly conserved vaccine antigens using genomic scale antigenic fingerprinting of pneumococcus with human antibodies. J Exp Med 205: 117-131.
60. Beachey EH, Giampapa CS, Abraham SN, (1988) Bacterial adherence. Adhesin receptor-mediated attachment of pathogenic bacteria to mucosal surfaces. Am Rev Respir Dis 138: S45-48.
61. Frolet C, Beniazza M, Roux L, Gallet B, Noirclerc-Savoye M, et al. (2010) New adhesin functions of surface-exposed pneumococcal proteins. BMC Microbiol 10: 190.
62. Brown J, Tobyn M, Brown S, Connolly T, Dennis A, et al. (2012) Enabling clinical development of an HIV attachment inhibitor through innovative pharmaceutical development: novel extended-release delivery of prodrug. J Int AIDS Soc 15: 18266.