Human antibodies to PhtD, PcpA, and ply reduce adherence to human lung epithelial cells and murine nasopharyngeal colonization by Streptococcus pneumoniae

Infection and Immunity

Volumn 82, Issue 12, 2014, Pages 5069-5075

  Kaur, Ravinder ^a   Surendran, Naveen ^a   Ochs, Martina ^b   Pichichero, Michael E ^a  

^a ROCHESTER GENERAL HOSPITAL   (United States)

^b SANOFI PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM ANTIBODY; HISTIDINE TRIAD PROTEIN ANTIBODY; IMMUNOGLOBULIN F(AB) FRAGMENT; PNEUMOCOCCAL CHOLINE BINDING PROTEIN A ANTIBODY; PNEUMOLYSIN ANTIBODY; RECOMBINANT VACCINE; STREPTOCOCCUS VACCINE; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; CARRIER PROTEIN; PCPA PROTEIN, STREPTOCOCCUS; PLY PROTEIN, STREPTOCOCCUS PNEUMONIAE; STREPTOLYSIN;

A549 CELL LINE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL IMMUNITY; BACTERIAL LOAD; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM MUTANT; CELL PROTECTION; CLINICAL TRIAL; CONTROLLED STUDY; CROSS REACTION; CYTOKINE PRODUCTION; DRUG PURIFICATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; HEMOLYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INOCULATION; LUNG ALVEOLUS CELL; MOUSE; NASOPHARYNX; NONHUMAN; PASSIVE IMMUNIZATION; PASSIVE TRANSPORT; PATHOGENESIS; RESPIRATORY EPITHELIUM; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE; VACCINATION; WILD TYPE; ANIMAL; C57BL MOUSE; CELL LINE; DISEASE MODEL; EPITHELIUM CELL; FEMALE; HETEROZYGOTE; IMMUNOLOGY; MICROBIOLOGY; PHYSIOLOGY; PNEUMOCOCCAL INFECTIONS; PREVENTION AND CONTROL;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL PROTEINS; CARRIER PROTEINS; CARRIER STATE; CELL LINE; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; FEMALE; HUMANS; IMMUNIZATION, PASSIVE; MICE, INBRED C57BL; NASOPHARYNX; PNEUMOCOCCAL INFECTIONS; STREPTOCOCCUS PNEUMONIAE; STREPTOLYSINS;

EID: 84911410753     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02124-14     Document Type: Article

References (54)

1. Balakrishnan I, Crook P, Morris R, Gillespie SH. 2000. Early predictors of mortality in pneumococcal bacteraemia. J. Infect. 40:256-261. http://dx.doi.org/10.1053/jinf.2000.0653.
2. Bogaert D, De Groot R, Hermans PW. 2004. Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect. Dis. 4:144-154. http://dx.doi.org/10.1016/S1473-3099(04)00938-7.
3. Pichichero ME. 2013. Otitis media. Pediatr. Clin. North Am. 60:391-407. http://dx.doi.org/10.1016/j.pcl.2012.12.007.
4. Kadioglu A, Weiser JN, Paton JC, Andrew PW. 2008. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat. Rev. Microbiol. 6:288-301. http://dx.doi.org/10.1038/nrmicro1871.
5. Plumptre CD, Ogunniyi AD, Paton JC. 2013. Surface association of Pht proteins of Streptococcus pneumoniae. Infect. Immun. 81:3644-3651. http://dx.doi.org/10.1128/IAI.00562-13.
6. Weinberger DM, Malley R, Lipsitch M. 2011. Serotype replacement in disease after pneumococcal vaccination. Lancet 378:1962-1973. http://dx.doi.org/10.1016/S0140-6736(10)62225-8.
7. Pauksens K, Nilsson AC, Caubet M, Pascal TG, Van Belle P, Poolman JT, Vandepapeliere PG, Verlant V, Vink PE. 2014. Randomized controlled study of the safety and immunogenicity of pneumococcal vaccine formulations containing PhtD and detoxified pneumolysin with alum or adjuvant system AS02V in elderly adults. Clin. Vaccine Immunol. 21:651-660. http://dx.doi.org/10.1128/CVI.00807-13.
8. Darrieux M, Goulart C, Briles D, Leite LC. 2013. Current status and perspectives on protein-based pneumococcal vaccines. Crit. Rev. Microbiol. http://dx.doi.org/10.3109/1040841X.2013.813902.
9. Khan MN, Pichichero ME. 2012. Vaccine candidates PhtD and PhtE of Streptococcus pneumoniae are adhesins that elicit functional antibodies in humans. Vaccine 30:2900-2907. http://dx.doi.org/10.1016/j.vaccine.2012.02.023.
10. Kaur R, Casey JR, Pichichero ME. 2011. Serum antibody response to five Streptococcus pneumoniae proteins during acute otitis media in otitisprone and non-otitis-prone children. The Pediatric infectious disease journal. 30:645-650. http://dx.doi.org/10.1097/INF.0b013e31821c2d8b.
11. Verhoeven D, Xu Q, Pichichero ME. 2014. Vaccination with a Streptococcus pneumoniae trivalent recombinant PcpA, PhtD and PlyD1 protein vaccine candidate protects against lethal pneumonia in an infant murine model. Vaccine 32:3205-3210. http://dx.doi.org/10.1016/j.vaccine.2014.04.004.
12. Ogunniyi AD, Grabowicz M, Mahdi LK, Cook J, Gordon DL, Sadlon TA, Paton JC. 2009. Pneumococcal histidine triad proteins are regulated by the Zn2+-dependent repressor AdcR and inhibit complement deposition through the recruitment of complement factor H. FASEB J. 23:731-738. http://dx.doi.org/10.1096/fj.08-119537.
13. Loisel E, Chimalapati S, Bougault C, Imberty A, Gallet B, Di Guilmi AM, Brown J, Vernet T, Durmort C. 2011. Biochemical characterization of the histidine triad protein PhtD as a cell surface zinc-binding protein of pneumococcus. Biochemistry 50:3551-3558. http://dx.doi.org/10.1021/bi200012f.
14. Adamou JE, Heinrichs JH, Erwin AL, Walsh W, Gayle T, Dormitzer M, Dagan R, Brewah YA, Barren P, Lathigra R, Langermann S, Koenig S, Johnson S. 2001. Identification and characterization of a novel family of pneumococcal proteins that are protective against sepsis. Infect. Immun. 69:949-958. http://dx.doi.org/10.1128/IAI.69.2.949-958.2001.
15. Holmlund E, Quiambao B, Ollgren J, Jaakkola T, Neyt C, Poolman J, Nohynek H, Kayhty H. 2009. Antibodies to pneumococcal proteins PhtD, CbpA, and LytC in Filipino pregnant women and their infants in relation to pneumococcal carriage. Clin. Vaccine Immunol. 16:916-923. http://dx.doi.org/10.1128/CVI.00050-09.
16. Pichichero ME, Kaur R, Casey JR, Xu Q, Almudevar A, Ochs M. 2012. Antibody response to Streptococcus pneumoniae proteins PhtD, LytB, PcpA, PhtE and Ply after nasopharyngeal colonization and acute otitis media in children. Hum. Vaccines Immunother. 8:799-805. http://dx.doi.org/10.4161/hv.19820.
17. Brooks-Walter A, Briles DE, Hollingshead SK. 1999. The pspC gene of Streptococcus pneumoniae encodes a polymorphic protein, PspC, which elicits cross-reactive antibodies to PspA and provides immunity to pneumococcal bacteremia. Infect. Immun. 67:6533-6542.
18. Glover DT, Hollingshead SK, Briles DE. 2008. Streptococcus pneumoniae surface protein PcpA elicits protection against lung infection and fatal sepsis. Infect. Immun. 76:2767-2776. http://dx.doi.org/10.1128/IAI.01126-07.
19. Johnston JW, Briles DE, Myers LE, Hollingshead SK. 2006. Mn2+-dependent regulation of multiple genes in Streptococcus pneumoniae through PsaR and the resultant impact on virulence. Infect. Immun. 74: 1171-1180. http://dx.doi.org/10.1128/IAI.74.2.1171-1180.2006.
20. Hava DL, Camilli A. 2002. Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol. Microbiol. 45:1389-1406. http://dx.doi.org/10.1046/j.1365-2958.2002.03106.x.
21. Sanchez-Beato AR, Lopez R, Garcia JL. 1998. Molecular characterization of PcpA: a novel choline-binding protein of Streptococcus pneumoniae. FEMS Microbiol. Lett. 164:207-214. http://dx.doi.org/10.1111/j.1574-6968.1998.tb13087.x.
22. Xu Q, Pichichero ME. 2014. Co-colonization by Haemophilus influenzae with Streptococcus pneumoniae enhances pneumococcal-specific antibody response in young children. Vaccine 32:706-711. http://dx.doi.org/10.1016/j.vaccine.2013.11.096.
23. Xu Q, Casey JR, Pichichero ME. 2014. Higher natural acquisitive mucosal antibody levels to pneumococcal vaccine candidate proteins correlate with reduced acute otitis media caused by Streptococcus pneumoniae in young children, abstr G295c. In Abstr. 54th Intersci. Conf. Antimicrob. Agents Chemother. http://www.icaac.org/.
24. Marriott HM, Mitchell TJ, Dockrell DH. 2008. Pneumolysin: a doubleedged sword during the host-pathogen interaction. Curr. Mol. Med. 8:497-509. http://dx.doi.org/10.2174/156652408785747924.
25. Price KE, Greene NG, Camilli A. 2012. Export requirements of pneumolysin in Streptococcus pneumoniae. J. Bacteriol. 194:3651-3660. http://dx.doi.org/10.1128/JB.00114-12.
26. Balachandran P, Hollingshead SK, Paton JC, Briles DE. 2001. The autolytic enzyme LytA of Streptococcus pneumoniae is not responsible for releasing pneumolysin. J. Bacteriol. 183:3108-3116. http://dx.doi.org/10.1128/JB.183.10.3108-3116.2001.
27. Quin LR, Moore QC, III, McDaniel LS. 2007. Pneumolysin, PspA, and PspC contribute to pneumococcal evasion of early innate immune responses during bacteremia in mice. Infect. Immun. 75:2067-2070. http://dx.doi.org/10.1128/IAI.01727-06.
28. Paton JC, Andrew PW, Boulnois GJ, Mitchell TJ. 1993. Molecular analysis of the pathogenicity of Streptococcus pneumoniae: the role of pneumococcal proteins. Annu. Rev. Microbiol. 47:89-115. http://dx.doi.org/10.1146/annurev.mi.47.100193.000513.
29. Paton JC, Ferrante A. 1983. Inhibition of human polymorphonuclear leukocyte respiratory burst, bactericidal activity, and migration by pneumolysin. Infect. Immun. 41:1212-1216.
30. Feldman C, Munro NC, Jeffery PK, Mitchell TJ, Andrew PW, Boulnois GJ, Guerreiro D, Rohde JA, Todd HC, Cole PJ, et al. 1991. Pneumolysin induces the salient histologic features of pneumococcal infection in the rat lung in vivo. Am. J. Respir. Cell Mol. Biol. 5:416-423. http://dx.doi.org/10.1165/ajrcmb/5.5.416.
31. Alexander JE, Lock RA, Peeters CC, Poolman JT, Andrew PW, Mitchell TJ, Hansman D, Paton JC. 1994. Immunization of mice with pneumolysin toxoid confers a significant degree of protection against at least nine serotypes of Streptococcus pneumoniae. Infect. Immun. 62:5683-5688.
32. Shak JR, Ludewick HP, Howery KE, Sakai F, Yi H, Harvey RM, Paton JC, Klugman KP, Vidal JE. 2013. Novel role for the Streptococcus pneumoniae toxin pneumolysin in the assembly of biofilms. mBio 4:e00655-13. http://dx.doi.org/10.1128/mBio.00655-13.
33. Khan MN, Sharma SK, Filkins LM, Pichichero ME. 2012. PcpA of Streptococcus pneumoniae mediates adherence to nasopharyngeal and lung epithelial cells and elicits functional antibodies in humans. Microbes Infect. 14:1102-1110. http://dx.doi.org/10.1016/j.micinf.2012.06.007.
34. Oloo EO, Yethon JA, Ochs MM, Carpick B, Oomen R. 2011. Structureguided antigen engineering yields pneumolysin mutants suitable for vaccination against pneumococcal disease. J. Biol. Chem. 286:12133-12140. http://dx.doi.org/10.1074/jbc.M110.191148.
35. Salha D, Szeto J, Myers L, Claus C, Sheung A, Tang M, Ljutic B, Hanwell D, Ogilvie K, Ming M, Messham B, van den Dobbelsteen G, Hopfer R, Ochs MM, Gallichan S. 2012. Neutralizing antibodies elicited by a novel detoxified pneumolysin derivative, PlyD1, provide protection against both pneumococcal infection and lung injury. Infect. Immun. 80: 2212-2220. http://dx.doi.org/10.1128/IAI.06348-11.
36. Mitchell TJ, Andrew PW, Saunders FK, Smith AN, Boulnois GJ. 1991. Complement activation and antibody binding by pneumolysin via a region of the toxin homologous to a human acute-phase protein. Mol. Microbiol. 5:1883-1888. http://dx.doi.org/10.1111/j.1365-2958.1991.tb00812.x.
37. Virolainen A, Jero J, Kayhty H, Karma P, Eskola J, Leinonen M. 1995. Nasopharyngeal antibodies to pneumococcal pneumolysin in children with acute otitis media. Clin. Diagn. Lab. Immunol. 2:704-707.
38. Talbot UM, Paton AW, Paton JC. 1996. Uptake of Streptococcus pneumoniae by respiratory epithelial cells. Infect. Immun. 64:3772-3777.
39. Kallio A, Sepponen K, Hermand P, Denoel P, Godfroid F, Melin M. 2014. Role of Pht proteins in attachment of Streptococcus pneumoniae to respiratory epithelial cells. Infect. Immun. 82:1683-1691. http://dx.doi.org/10.1128/IAI.00699-13.
40. Luo R, Mann B, Lewis WS, Rowe A, Heath R, Stewart ML, Hamburger AE, Sivakolundu S, Lacy ER, Bjorkman PJ, Tuomanen E, Kriwacki RW. 2005. Solution structure of choline binding protein A, the major adhesin of Streptococcus pneumoniae. EMBO J. 24:34-43. http://dx.doi.org/10.1038/sj.emboj.7600490.
41. Rajam G, Anderton JM, Carlone GM, Sampson JS, Ades EW. 2008. Pneumococcal surface adhesin A (PsaA): a review. Crit. Rev. Microbiol. 34:163-173. http://dx.doi.org/10.1080/10408410802383610.
42. Overweg K, Pericone CD, Verhoef GG, Weiser JN, Meiring HD, De Jong AP, De Groot R, Hermans PW. 2000. Differential protein expression in phenotypic variants of Streptococcus pneumoniae. Infect. Immun. 68:4604-4610. http://dx.doi.org/10.1128/IAI.68.8.4604-4610.2000.
43. Weiser JN, Markiewicz Z, Tuomanen EI, Wani JH. 1996. Relationship between phase variation in colony morphology, intrastrain variation in cell wall physiology, and nasopharyngeal colonization by Streptococcus pneumoniae. Infect. Immun. 64:2240-2245.
44. Kim JO, Weiser JN. 1998. Association of intrastrain phase variation in quantity of capsular polysaccharide and teichoic acid with the virulence of Streptococcus pneumoniae. J. Infect. Dis. 177:368-377. http://dx.doi.org/10.1086/514205.
45. Rosenow C, Ryan P, Weiser JN, Johnson S, Fontan P, Ortqvist A, Masure HR. 1997. Contribution of novel choline-binding proteins to adherence, colonization and immunogenicity of Streptococcus pneumoniae. Mol. Microbiol. 25:819-829. http://dx.doi.org/10.1111/j.1365-2958.1997.mmi494.x.
46. Berry AM, Paton JC. 1996. Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae. Infect. Immun. 64:5255-5262.
47. Romero-Steiner S, Pilishvili T, Sampson JS, Johnson SE, Stinson A, Carlone GM, Ades EW. 2003. Inhibition of pneumococcal adherence to human nasopharyngeal epithelial cells by anti-PsaA antibodies. Clin. Diagn. Lab. Immunol. 10:246-251. http://dx.doi.org/10.1128/CDLI.10.2.246-251.2003.
48. Tai SS. 2006. Streptococcus pneumoniae protein vaccine candidates: properties, activities and animal studies. Crit. Rev. Microbiol. 32:139-153. http://dx.doi.org/10.1080/10408410600822942.
49. Godfroid F, Hermand P, Verlant V, Denoel P, Poolman JT. 2011. Preclinical evaluation of the Pht proteins as potential cross-protective pneumococcal vaccine antigens. Infect. Immun. 79:238-245. http://dx.doi.org/10.1128/IAI.00378-10.
50. Denoel P, Philipp MT, Doyle L, Martin D, Carletti G, Poolman JT. 2011. A protein-based pneumococcal vaccine protects rhesus macaques from pneumonia after experimental infection with Streptococcus pneumoniae. Vaccine 29:5495-5501. http://dx.doi.org/10.1016/j.vaccine.2011.05.051.
51. Seiberling M, Bologa M, Brookes R, Ochs M, Go K, Neveu D, Kamtchoua T, Lashley P, Yuan T, Gurunathan S. 2012. Safety and immunogenicity of a pneumococcal histidine triad protein D vaccine candidate in adults. Vaccine 30:7455-7460. http://dx.doi.org/10.1016/j.vaccine.2012.10.080.
52. Francis JP, Richmond PC, Pomat WS, Michael A, Keno H, Phuanukoonnon S, Nelson JB, Whinnen M, Heinrich T, Smith WA, Prescott SL, Holt PG, Siba PM, Lehmann D, van den Biggelaar AH. 2009. Maternal antibodies to pneumolysin but not to pneumococcal surface protein A delay early pneumococcal carriage in high-risk Papua New Guinean infants. Clin. Vaccine Immunol. 16:1633-1638. http://dx.doi.org/10.1128/CVI.00247-09.
53. Rubins JB, Paddock AH, Charboneau D, Berry AM, Paton JC, Janoff EN. 1998. Pneumolysin in pneumococcal adherence and colonization. Microb. Pathog. 25:337-342. http://dx.doi.org/10.1006/mpat.1998.0239.
54. Neill DR, Coward WR, Gritzfeld JF, Richards L, Garcia-Garcia FJ, Dotor J, Gordon SB, Kadioglu A. 2014. Density and duration of pneumococcal carriage is maintained by transforming growth factor beta1 and T regulatory cells. Am. J. Respir. Crit. Care Med. 189:1250-1259. http://dx.doi.org/10.1164/rccm.201401-0128OC.