Multivalent pneumococcal protein vaccines comprising pneumolysoid with epitopes/fragments of CbpA and/or PspA elicit strong and broad protection

Clinical and Vaccine Immunology

Volumn 22, Issue 10, 2015, Pages 1079-1089

  Chen, Austen ^a   Mann, Beth ^b   Gao, Geli ^b   Heath, Richard ^b   King, Janice ^c   Maissoneuve, Jeff ^d   Alderson, Mark ^d   Tate, Andrea ^d   Hollingshead, Susan K ^c   Tweten, Rodney K ^e   Briles, David E ^c   Tuomanen, Elaine I ^b   Paton, James C ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c University of Alabama at Birmingham   (United States)

^d PATH   (United States)

^e UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BINDING PROTEIN; CHOLINE BINDING PROTEIN; EPITOPE; PNEUMOCOCCAL SURFACE PROTEIN A; PNEUMOCOCCUS VACCINE; PNEUMOLYSIN; UNCLASSIFIED DRUG; CBPA PROTEIN, BACTERIA; HYBRID PROTEIN; IMMUNOGLOBULIN G; PLY PROTEIN, STREPTOCOCCUS PNEUMONIAE; RECOMBINANT VACCINE; STREPTOLYSIN; TOXOID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; IMMUNOGENICITY; INFECTION PREVENTION; INFECTION RESISTANCE; MENINGITIS; MOUSE; NONHUMAN; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; SEPSIS; STREPTOCOCCUS PNEUMONIAE; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CLASSIFICATION; DISEASE MODEL; GENETICS; IMMUNIZATION; IMMUNOLOGY; MENINGITIS, PNEUMOCOCCAL; MICROBIOLOGY; PNEUMOCOCCAL INFECTIONS; PNEUMONIA, PNEUMOCOCCAL; VACCINATION;

ANIMALS; BACTERIAL PROTEINS; DISEASE MODELS, ANIMAL; EPITOPES; IMMUNIZATION SCHEDULE; IMMUNOGLOBULIN G; MENINGITIS, PNEUMOCOCCAL; MICE, INBRED BALB C; PNEUMOCOCCAL INFECTIONS; PNEUMOCOCCAL VACCINES; PNEUMONIA, PNEUMOCOCCAL; RECOMBINANT FUSION PROTEINS; SEPSIS; STREPTOCOCCUS PNEUMONIAE; STREPTOLYSINS; TOXOIDS; VACCINATION; VACCINES, SYNTHETIC;

EID: 84943265404     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00293-15     Document Type: Article

References (66)

1. O'Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M, McCall N, Lee E, Mulholland K, Levine OS, Cherian T, Hib and Pneumococcal Global Burden of Disease Study Team. 2009. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374:893-902. http://dx.doi.org/10.1016/S0140-6736(09)61204-6.
2. World Health Organization. 2008. 23-valent pneumococcal polysaccharide vaccine. WHO position paper. Wkly Epidemiol Rec 83:373-384.
3. Weinberger DM, Trzcinski K, Lu YJ, Bogaert D, Brandes A, Galagan J, Anderson PW, Malley R, Lipsitch M. 2009. Pneumococcal capsular polysaccharide structure predicts serotype prevalence. PLoS Pathog 5:e1000476. http://dx.doi.org/10.1371/journal.ppat.1000476.
4. Feldman C, Anderson R. 2014. Review: current and new generation pneumococcal vaccines. J Infect 69:309-325. http://dx.doi.org/10.1016/j.jinf.2014.06.006.
5. Miller E, Andrews NJ, Waight PA, Slack MP, George RC. 2011. Herd immunity and serotype replacement 4 years after seven-valent pneumococcal conjugate vaccination in England and Wales: an observational cohort study. Lancet Infect Dis 11:760-768. http://dx.doi.org/10.1016 /S1473-3099(11)70090-1.
6. Pai R, Moore MR, Pilishvili T, Gertz RE, Whitney CG, Beall B, Active Bacterial Core Surveillance Team. 2005. Postvaccine genetic structure of Streptococcus pneumoniae serotype 19A from children in the United States. J Infect Dis 192:1988-1995. http://dx.doi.org/10.1086/498043.
7. Singleton RJ, Hennessy TW, Bulkow LR, Hammitt LL, Zulz T, Hurlburt DA, Butler JC, Rudolph K, Parkinson A. 2007. Invasive pneumococcal disease caused by nonvaccine serotypes among Alaska native children with high levels of 7-valent pneumococcal conjugate vaccine coverage. JAMA 297:1784-1792. http://dx.doi.org/10.1001/jama.297.16.1784.
8. 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.
9. Domingues CM, Verani JR, Montenegro Renoiner EI, de Cunto Brandileone MC, Flannery B, de Oliveira LH, Santos JB, de Moraes JC, Brazilian Pneumococcal Conjugate Vaccine Effectiveness Study Group. 2014. Effectiveness of ten-valent pneumococcal conjugate vaccine against invasive pneumococcal disease in Brazil: a matched case-control study. Lancet Respir Med 2:464-471. http://dx.doi.org/10.1016/S2213-2600(14)70060-8.
10. Moore CE, Paul J, Foster D, Mahar SA, Griffiths D, Knox K, Peto TE, Walker AS, Crook DW, Oxford Invasive Pneumococcal Surveillance Group. 2014. Reduction of invasive pneumococcal disease 3 years after the introduction of the 13-valent conjugate vaccine in the Oxfordshire region of England. J Infect Dis 210:1001-1011. http://dx.doi.org/10.1093/infdis /jiu213.
11. Carter R, Wolf J, van Opijnen T, Muller M, Obert C, Burnham C, Mann B, Li Y, Hayden RT, Pestina T, Persons D, Camilli A, Flynn PM, Tuomanen EI, Rosch JW. 2014. Genomic analyses of pneumococci from children with sickle cell disease expose host-specific bacterial adaptations and deficits in current interventions. Cell Host Microbe 15:587-599. http: //dx.doi.org/10.1016/j.chom.2014.04.005.
12. McCool TL, Cate TR, Tuomanen EI, Adrian P, Mitchell TJ, Weiser JN. 2003. Serum immunoglobulin G response to candidate vaccine antigens during experimental human pneumococcal colonization. Infect Immun 71:5724-5732. http://dx.doi.org/10.1128/IAI.71.10.5724-5732.2003.
13. Rapola S, Jäntti V, Haikala R, Syrjänen R, Carlone GM, Sampson JS, Briles DE, Paton JC, Takala AK, Kilpi TM, Käyhty H. 2000. Natural development of antibodies to pneumococcal surface protein A, pneumococcal surface adhesin A, and pneumolysin in relation to pneumococcal carriage and acute otitis media. J Infect Dis 182:1146-1152. http://dx.doi.org/10.1086/315822.
14. Simell B, Korkeila M, Pursiainen H, Kilpi TM, Käyhty H. 2001. Pneumococcal carriage and otitis media induce salivary antibodies to pneumococcal surface adhesin A, pneumolysin, and pneumococcal surface protein A in children. J Infect Dis 183:887-896. http://dx.doi.org/10.1086 /319246.
15. Zhang Q, Choo S, Finn A. 2002. Immune responses to novel pneumococcal proteins pneumolysin, PspA, PsaA, and CbpA in adenoidal B cells from children. Infect Immun 70:5363-5369. http://dx.doi.org/10.1128 /IAI.70.10.5363-5369.2002.
16. Briles DE, Paton JC, Swiatlo E, Hollingshead S, Crain M. 2006. Pneumococcal vaccines, p 289-298. In Frischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-positive pathogens, 2nd ed. ASM Press, Washington, DC.
17. Paton JC. 1996. The contribution of pneumolysin to the pathogenicity of Streptococcus pneumoniae. Trends Microbiol 4:103-106. http://dx.doi.org /10.1016/0966-842X(96)81526-5.
18. Paton JC. 1998. Novel pneumococcal surface proteins: role in virulence and vaccine potential. Trends Microbiol 6:85-87. http://dx.doi.org/10.1016/S0966-842X(98)01220-7.
19. Paton JC. 2004. New pneumococcal vaccines: basic science developments, p 382-402. In Tuomanen EI, Mitchell TJ, Morrison DA, Spratt BG (ed), The pneumococcus. ASM Press, Washington, DC.
20. 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.
21. Watson DA, Musher DM, Verhoef J. 1995. Pneumococcal virulence factors and host immune responses to them. Eur J Clin Microbiol Infect Dis 14:479-490. http://dx.doi.org/10.1007/BF02113425.
22. Mukerji R, Mirza S, Roche AM, Widener RW, Croney CM, Rhee DK, Weiser JN, Szalai AJ, Briles DE. 2012. Pneumococcal surface protein A inhibits complement deposition on the pneumococcal surface by competing with the binding of C-reactive protein to cell-surface phosphocholine. J Immunol 189:5327-5335. http://dx.doi.org/10.4049/jimmunol.1201967.
23. Paton JC, Lock RA, Lee CJ, Li JP, Berry AM, Mitchell TJ, Andrew PW, Hansman D, Boulnois GJ. 1991. Purification and immunogenicity of genetically obtained pneumolysin toxoids and their conjugation to Streptococcus pneumoniae type 19F polysaccharide. Infect Immun 59:2297-2304.
24. 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.
25. Ogunniyi AD, Folland RL, Briles DE, Hollingshead SK, Paton JC. 2000. Immunization of mice with combinations of pneumococcal virulence proteins elicits enhanced protection against challenge with Streptococcus pneumoniae. Infect Immun 68:3028-3033. http://dx.doi.org/10.1128/IAI.68.5.3028-3033.2000.
26. 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. http://dx.doi.org/10.1128/IAI.01103-06.
27. Ogunniyi AD, Woodrow MC, Poolman JT, Paton JC. 2001. Protection against Streptococcus pneumoniae elicited by immunization with pneumolysin and CbpA. Infect Immun 69:5997-6003. http://dx.doi.org/10.1128 /IAI.69.10.5997-6003.2001.
28. Briles DE, Hollingshead SK, Paton JC, Ades EW, Novak L, van Ginkel FW, Benjamin WH, Jr. 2003. Immunizations with pneumococcal surface protein A and pneumolysin are protective against pneumonia in a murine model of pulmonary infection with Streptococcus pneumoniae. J Infect Dis 188:339-348. http://dx.doi.org/10.1086/376571.
29. 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.
30. Farrand AJ, LaChapelle S, Hotze EM, Johnson AE, Tweten RK. 2010. Only two amino acids are essential for cytolytic toxin recognition of cholesterol at the membrane surface. Proc Natl Acad Sci U S A 107:4341-4346. http://dx.doi.org/10.1073/pnas.0911581107.
31. McDaniel LS, Yother J, Vijayakumar M, McGarry L, Guild WR, Briles DE. 1987. Use of insertional inactivation to facilitate studies of biological properties of pneumococcal surface protein A (PspA). J Exp Med 165: 381-394. http://dx.doi.org/10.1084/jem.165.2.381.
32. Tu AH, Fulgham RL, McCrory MA, Briles DE, Szalai AJ. 1999. Pneumococcal surface protein A inhibits complement activation by Streptococcus pneumoniae. Infect Immun 67:4720-4724.
33. Shaper M, Hollingshead SK, Benjamin WH, Jr, Briles DE. 2004. PspA protects Streptococcus pneumoniae from killing by apolactoferrin, and antibody to PspA enhances killing of pneumococci by apolactoferrin. Infect Immun 72:5031-5040. http://dx.doi.org/10.1128/IAI.72.9.5031-5040.2004.
34. Genschmer KR, Accavitti-Loper MA, Briles DE. 2013. A modified surface killing assay (MSKA) as a functional in vitro assay for identifying protective antibodies against pneumococcal surface protein A (PspA). Vaccine 32:39-47. http://dx.doi.org/10.1016/j.vaccine.2013.10.080.
35. Briles DE, King JD, Gray MA, McDaniel LS, Swiatlo E, Benton KA. 1996. PspA, a protection-eliciting pneumococcal protein: immunogenicity of isolated native PspA in mice. Vaccine 14:858-867. http://dx.doi.org /10.1016/0264-410X(96)82948-3.
36. McDaniel LS, Ralph BA, McDaniel DO, Briles DE. 1994. Localization of protection-eliciting epitopes on PspA of Streptococcus pneumoniae between amino acid residues 192 and 260. Microb Pathog 17:323-337. http: //dx.doi.org/10.1006/mpat.1994.1078.
37. McDaniel LS, Sheffield JS, Delucchi P, Briles DE. 1991. PspA, a surface protein of Streptococcus pneumoniae, is capable of eliciting protection against pneumococci of more than one capsular type. Infect Immun 59: 222-228.
38. 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.
39. Hollingshead SK, Becker R, Briles DE. 2000. Diversity of PspA: mosaic genes and evidence for past recombination in Streptococcus pneumoniae. Infect Immun 68:5889-5900. http://dx.doi.org/10.1128/IAI.68.10.5889-5900.2000.
40. Iannelli F, Oggioni MR, Pozzi G. 2002. Allelic variation in the highly polymorphic locus pspC of Streptococcus pneumoniae. Gene 284:63-71. http://dx.doi.org/10.1016/S0378-1119(01)00896-4.
41. McDaniel LS, Sheffield JS, Swiatlo E, Yother J, Crain MJ, Briles DE. 1992. Molecular localization of variable and conserved regions of pspA and identification of additional pspA homologous sequences in Streptococcus pneumoniae. Microb Pathog 13:261-269. http://dx.doi.org/10.1016 /0882-4010(92)90036-N.
42. Daniels CC, Coan P, King J, Hale J, Benton KA, Briles DE, Hollings-head SK. 2010. The proline-rich region of pneumococcal surface proteins A and C contains surface-accessible epitopes common to all pneumococci and elicits antibody-mediated protection against sepsis. Infect Immun 78:2163-2172. http://dx.doi.org/10.1128/IAI.01199-09.
43. Melin M, Coan P, Hollingshead S. 2012. Development of cross-reactive antibodies to the proline-rich region of pneumococcal surface protein A in children. Vaccine 30:7157-7160. http://dx.doi.org/10.1016/j.vaccine.2012.10.004.
44. Balachandran P, Brooks-Walter A, Virolainen-Julkunen A, Hollingshead SK, Briles DE. 2002. Role of pneumococcal surface protein C in nasopharyngeal carriage and pneumonia and its ability to elicit protection against carriage of Streptococcus pneumoniae. Infect Immun 70:2526-2534. http://dx.doi.org/10.1128/IAI.70.5.2526-2534.2002.
45. Orihuela CJ, Gao G, Francis KP, Yu J, Tuomanen EI. 2004. Tissuespecific contributions of pneumococcal virulence factors to pathogenesis. J Infect Dis 190:1661-1669. http://dx.doi.org/10.1086/424596.
46. Zhang Y, Masi AW, Barniak V, Mountzouros K, Hostetter MK, Green BA. 2001. Recombinant PhpA protein, a unique histidine motifcontaining protein from Streptococcus pneumoniae, protects mice against intranasal pneumococcal challenge. Infect Immun 69:3827-3836. http: //dx.doi.org/10.1128/IAI.69.6.3827-3836.2001.
47. Cheng Q, Finkel D, Hostetter MK. 2000. Novel purification scheme and functions for a C3-binding protein from Streptococcus pneumoniae. Biochemistry 39:5450-5457. http://dx.doi.org/10.1021/bi992157d.
48. Dave S, Brooks-Walter A, Pangburn MK, McDaniel LS. 2001. PspC, a pneumococcal surface protein, binds human factor H. Infect Immun 69: 3435-3437. http://dx.doi.org/10.1128/IAI.69.5.3435-3437.2001.
49. 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. http://dx.doi.org/10.1046/j.1365-2958.1997.5391899.x.
50. Janulczyk R, Iannelli F, Sjoholm AG, Pozzi G, Bjorck L. 2000. Hic, a novel surface protein of Streptococcus pneumoniae that interferes with complement function. J Biol Chem 275:37257-37263. http://dx.doi.org /10.1074/jbc.M004572200.
51. Jarva H, Janulczyk R, Hellwage J, Zipfel PF, Björck L, Meri S. 2002. Streptococcus pneumoniae evades complement attack and opsonophagocytosis by expressing the pspC locus-encoded Hic protein that binds to short consensus repeats 8-11 of factor H. J Immunol 168:1886-1894. http://dx.doi.org/10.4049/jimmunol.168.4.1886.
52. Orihuela CJ, Mahdavi J, Thornton J, Mann B, Wooldridge KG, Abouseada N, Oldfield NJ, Self T, Ala'Aldeen DA, Tuomanen EI. 2009. Laminin receptor initiates bacterial contact with the blood brain barrier in experimental meningitis models. J Clin Invest 119:1638-1646. http://dx.doi.org/10.1172/JCI36759.
53. 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.
54. Mann B, Thornton J, Heath R, Wade KR, Tweten RK, Gao G, El Kasmi K, Jordan JB, Mitrea DM, Kriwacki R, Maisonneuve J, Alderson M, Tuomanen EI. 2014. Broadly protective protein-based pneumococcal vaccine composed of pneumolysin toxoid-CbpA peptide recombinant fusion protein. J Infect Dis 209:1116-1125. http://dx.doi.org/10.1093/infdis /jit502.
55. Harvey RM, Ogunniyi AD, Chen AY, Paton JC. 2011. Pneumolysin with low hemolytic activity confers an early growth advantage to Streptococcus pneumoniae in the blood. Infect Immun 79:4122-4130. http://dx.doi.org /10.1128/IAI.05418-11.
56. Harvey RM, Hughes CE, Paton AW, Trappetti C, Tweten RK, Paton JC. 2014. The impact of pneumolysin on the macrophage response to Streptococcus pneumoniae is strain-dependent. PLoS One 9:e103625. http://dx.doi.org/10.1371/journal.pone.0103625.
57. National Health and Medical Research Council. 2004. Australian code of practice for the care and use of animals for scientific purposes, 7th ed. Australian Government, National Health and Medical Research Council, Canberra, Australian Capital Territory, Australia. https://www.nhmrc.gov.au/-files-nhmrc/publications/attachments/ea16-animal-code.pdf.
58. Parliament of South Australia. 1985. Animal Welfare Act 1985. Parliament of South Australia, Adelaide, South Australia, Australia.
59. Jalonen E, Paton JC, Koskela M, Kerttula Y, Leinonen M. 1989. Measurement of antibody responses to pneumolysin - a promising method for the presumptive aetiological diagnosis of pneumococcal pneumonia. J Infect 19:127-134. http://dx.doi.org/10.1016/S0163-4453(89)91864-1.
60. Paton JC, Lock RA, Hansman DJ. 1983. Effect of immunization with pneumolysin on survival time of mice challenged with Streptococcus pneumoniae. Infect Immun 40:548-552.
61. Braun JS, Novak R, Gao G, Murray PJ, Shenep JL. 1999. Pneumolysin, a protein toxin of Streptococcus pneumoniae, induces nitric oxide production from macrophages. Infect Immun 67:3750-3756.
62. Cockeran R, Theron AJ, Steel HC, Matlola NM, Mitchell TJ, Feldman C, Anderson R. 2001. Proinflammatory interactions of pneumolysin with human neutrophils. J Infect Dis 183:604-611. http://dx.doi.org/10.1086 /318536.
63. Kadioglu A, Gingles NA, Grattan K, Kerr A, Mitchell TJ, Andrew PW. 2000. Host cellular immune response to pneumococcal lung infection in mice. Infect Immun 68:492-501. http://dx.doi.org/10.1128/IAI.68.2.492-501.2000.
64. 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.
65. Witzenrath M, Pache F, Lorenz D, Koppe U, Gutbier B, Tabeling C, Reppe K, Meixenberger K, Dorhoi A, Ma J, Holmes A, Trendelenburg G, Heimesaat MM, Bereswill S, van der Linden M, Tschopp J, Mitchell TJ, Suttorp N, Opitz B. 2011. The NLRP3 inflammasome is differentially activated by pneumolysin variants and contributes to host defense in pneumococcal pneumonia. J Immunol 187:434-440. http://dx.doi.org /10.4049/jimmunol.1003143.
66. Mirza S, Wilson L, Benjamin WH, Jr, Novak J, Barnes S, Hollingshead SK, Briles DE. 2011. Serine protease PrtA from Streptococcus pneumoniae plays a role in the killing of S. pneumoniae by apolactoferrin. Infect Immun 79:2440-2450. http://dx.doi.org/10.1128/IAI.00489-10.