Modified opsonization, phagocytosis, and killing assays to measure potentially protective antibodies against pneumococcal surface protein A

Clinical and Vaccine Immunology

Volumn 20, Issue 10, 2013, Pages 1549-1558

  Daniels, Calvin C ^a   Kim, Kyung Hyo ^b   Burton, Robert L ^c   Mirza, Shaper ^d   Walker, Melissa ^a   King, Janice ^a   Hale, Yvette ^a   Coan, Patricia ^a   Rhee, Dong Kwon ^e   Nahm, Moon H ^a,c   Briles, David E ^a,f,g  

^a University of Alabama at Birmingham   (United States)

^b Ewha Womans University School of Medicine   (South Korea)

^c University of Alabama at Birmingham   (United States)

^d UNIVERSITY OF TEXAS SCHOOL OF PUBLIC HEALTH   (United States)

^e Sungkyunkwan University   (South Korea)

^f University of Alabama at Birmingham   (United States)

^g UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PNEUMOCOCCAL SURFACE PROTEIN A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DETECTION; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; HUMAN; IMMUNOASSAY; INCUBATION TIME; INFECTION PREVENTION; MOUSE; NONHUMAN; OPSONIZATION; OPSONOPHAGOCYTOSIS KILLING ASSAY; PHAGOCYTOSIS; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL;

ADULT; ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL PROTEINS; BLOOD BACTERICIDAL ACTIVITY; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; IMMUNIZATION, PASSIVE; IMMUNOASSAY; MALE; MICE; MICE, INBRED CBA; MIDDLE AGED; OPSONIN PROTEINS; PHAGOCYTOSIS; PNEUMOCOCCAL INFECTIONS; RABBITS; YOUNG ADULT;

EID: 84886741876     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00371-13     Document Type: Article

References (65)

1. Wardlaw T, Johannson EW, Hodge M, World Health Organization. 2006. Pneumonia: the forgotten killer of children. The United Nations Children's Fund (UNICEF)/World Health Organization (WHO), Geneva, Switzerland. http://whqlibdoc.who.int/publications/2006/9280640489-eng.pdf.
2. Haber M, Barskey A, Baughman W, Barker L, Whitney CG, Shaw KM, Orenstein W, Stephens DS. 2007. Herd immunity and pneumococcal conjugate vaccine: a quantitative model. Vaccine 25:5390-5398.
3. Hammitt LL, Bruden DL, Butler JC, Baggett HC, Hurlburt DA, Reasonover A, Hennessy TW. 2006. Indirect effect of conjugate vaccine on adult carriage of Streptococcus pneumoniae: an explanation of trends in invasive pneumococcal disease. J. Infect. Dis. 193:1487-1494.
4. Scott JR, Millar EV, Lipsitch M, Moulton LH, Weatherholtz R, Perilla MJ, Jackson DM, Beall B, Craig MJ, Reid R, Santosham M, O'Brien KL. 2012. Impact of more than a decade of pneumococcal conjugate vaccine use on carriage and invasive potential in Native American communities. J. Infect. Dis. 205:280-288.
5. Pilishvili T, Lexau C, Farley MM, Hadler J, Harrison LH, Bennett NM, Reingold A, Thomas A, Schaffner W, Craig AS, Smith PJ, Beall BW, Whitney CG, Moore MR, Active Bacterial Core Surveillance/Emerging Infections Program Network. 2010. Sustained reductions in invasive pneumococcal disease in the era of conjugate vaccine. J. Infect. Dis. 201:32-41.
6. Croney CM, Coats MT, Nahm MH, Briles DE, Crain MJ. 2012. PspA family distribution, unlike capsular serotype, remained unaltered following introduction of the heptavalent-pneumococcal conjugate vaccine. Clin. Vaccine Immunol. 19:891-896.
7. Black S, Shinefield H, Cohen R, Floret D, Gaudelus J, Olivier C, Reinert P. 2004. Clinical effectiveness of seven-valent pneumococcal conjugate vaccine (Prevenar) against invasive pneumococcal diseases: prospects for children in France. Arch. Pediatr. 11:843-853. (In French.)
8. 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.
9. Hsu HE, Shutt KA, Moore MR, Beall BW, Bennett NM, Craig AS, Farley MM, Jorgensen JH, Lexau CA, Petit S, Reingold A, Schaffner W, Thomas A, Whitney CG, Harrison LH. 2009. Effect of pneumococcal conjugate vaccine on pneumococcal meningitis. N. Engl. J. Med. 360:244-256.
10. Weinberger DM, Malley R, Lipsitch M. 2011. Serotype replacement in disease after pneumococcal vaccination. Lancet 378:1962-1973.
11. Ampofo K, Pavia AT, Chris S, Hersh AL, Bender JM, Blaschke AJ, Weng HY, Korgenski KE, Daly J, Mason EO, Byington CL. 2012. The changing epidemiology of invasive pneumococcal disease at a tertiary children's hospital through the 7-valent pneumococcal conjugate vaccine era: a case for continuous surveillance. Pediatr. Infect. Dis. J. 31:228-234.
12. Wroe PC, Lee GM, Finkelstein JA, Pelton SI, Hanage WP, Lipsitch M, Stevenson AE, Rifas-Shiman SL, Kleinman K, Dutta-Linn MM, Hinrichsen VL, Lakoma M, Huang SS. 2012. Pneumococcal carriage and antibiotic resistance in young children before 13-valent conjugate vaccine. Pediatr. Infect. Dis. J. 31:249-254.
13. AlonsoDeVelasco E, Verheul AF, Verhoef J, Snippe H. 1995. Streptococcus pneumoniae: virulence factors, pathogenesis, and vaccines. Microbiol. Rev. 59:591-603.
14. Barocchi MA, Censini S, Rappuoli R. 2007. Vaccines in the era of genomics: the pneumococcal challenge. Vaccine 25:2963-2973.
15. Briles DE, Paton JC, Hollingsehad SK, Boslego JW. 2010. Pneumococcal common proteins and other vaccine strategies, p 482-488. In Levine MM, Dougan G, Good MF, Liu MA, Nabel GJ, Nataro NP, Rappouli R (ed), New generation vaccines, 4th ed. Informa Healthcare USA, Inc., New York, NY.
16. Miyaji EN, Oliveira MLS, Carvalho E, Ho PL. 2012. Serotype-independent pneumococcal vaccines. Cell. Mol. Life Sci. doi:10.1007/s00018-012-1234-8.
17. Tu A-HT, Fulgham RL, McCory MA, Briles DE, Szalai AJ. 1999. Pneumococcal surface protein A (PspA) inhibits complement activation by Streptococcus pneumoniae. Infect. Immun. 67:4720-4724.
18. Li J, Glover DT, Szalai AJ, Hollingshead SK, Briles DE. 2007. PspA and PspC minimize immune adherence and transfer of pneumococci from erythrocytes to macrophages through their effects on complement activation. Infect. Immun. 75:5877-5885.
19. 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.
20. Ren B, Li J, Genschmer K, Hollingshead SK, Briles DE. 2012. The absence of PspA or presence of antibody to PspA facilitates the complement-dependent phagocytosis of pneumococci in vitro. Clin. Vaccine Immunol. 19:1574-1582.
21. 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.
22. 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. (Erratum, 72:7379.)
23. Daniels CC, Briles TC, Mirza S, Hakansson AP, Briles DE. 2006. Capsule does not block antibody binding to PspA, a surface virulence protein of Streptococcus pneumoniae. Microb. Pathog. 40:228-233.
24. McDaniel LS, Scott G, Widenhofer K, Carroll J, Briles DE. 1986. Analysis of a surface protein of Streptococcus pneumoniae recognised by protective monoclonal antibodies. Microb. Pathog. 1:519-531.
25. Yother J, White JM. 1994. Novel surface attachment mechanism for the Streptococcus pneumoniae protein PspA. J. Bacteriol. 176:2976-2985.
26. Crain MJ, Waltman WD, Jr, Turner JS, Yother J, Talkington DF, McDaniel LS, Gray BM, Briles DE. 1990. Pneumococcal surface protein A (PspA) is serologically highly variable and is expressed by all clinically important capsular serotypes of Streptococcus pneumoniae. Infect. Immun. 58:3293-3299.
27. Hollingshead SK, Baril L, Ferro S, King J, Coan P, Briles DE, Pneumococcal Proteins Epi Study Group. 2006. Pneumococcal surface protein A (PspA) family distribution among clinical isolates from adults over 50 years of age collected in seven countries. J. Med. Microbiol. 55:215-221.
28. Brandileone MC, Andrade AL, Teles EM, Zanella RC, Yara TI, Di Fabio JL, Hollingshead SK. 2004. Typing of pneumococcal surface protein A (PspA) in Streptococcus pneumoniae isolated during epidemiological surveillance in Brazil: towards novel pneumococcal protein vaccines. Vaccine 22:3890-3896.
29. Briles DE, Hollingshead SK, King J, Swift A, Braun PA, Park MK, Ferguson LM, Nahm MH, Nabors GS. 2000. Immunization of humans with recombinant pneumococcal surface protein A (rPspA) elicits antibodies that passively protect mice from fatal infection with Streptococcus pneumoniae bearing heterologous PspA. J. Infect. Dis. 182:1694-1701.
30. Briles DE, Hollingshead S, Brooks-Walter A, Nabors GS, Ferguson L, Schilling M, Gravenstein S, Braun P, King J, Swift A. 2000. The potential to use PspA and other pneumococcal proteins to elicit protection against pneumococcal infection. Vaccine 18:1707-1711.
31. 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.
32. Nabors GS, Braun PA, Herrmann DJ, Heise ML, Pyle DJ, Gravenstein S, Schilling M, Ferguson LM, Hollingshead SK, Briles DE, Becker RS. 2000. Immunization of healthy adults with a single recombinant pneumococcal surface protein A (PspA) variant stimulates broadly cross-reactive antibodies to heterologous PspA molecules. Vaccine 18:1743-1754.
33. Daniels CC, Coan P, King J, Hale J, Benton KA, Briles DE, Hollingshead 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.
34. Ochs MM, Bartlett W, Briles DE, Hicks B, Jurkuvenas A, Lau P, Ren B, Millar A. 2008. Vaccine-induced human antibodies to PspA augment complement C3 deposition on Streptococcus pneumoniae. Microb. Pathog. 44:204-214.
35. Ren B, Szalai AJ, Hollingshead SK, Briles DE. 2004. Effects of PspA and antibodies to PspA on activation and deposition of complement on the pneumococcal surface. Infect. Immun. 72:114-122.
36. Briles DE, Tart RC, Wu HY, Ralph BA, Russell MW, McDaniel LS. 1996. Systemic and mucosal protective immunity to pneumococcal surface protein A. Ann. N. Y. Acad. Sci. 797:118-126.
37. Bitsaktsis C, Iglesias BV, Li Y, Colino J, Snapper CM, Hollingshead SK, Pham G, Gosselin DR, Gosselin EJ. 2012. Mucosal immunization with an unadjuvanted vaccine that targets Streptococcus pneumoniae PspA to human Fcγ receptor type I protects against pneumococcal infection through complement- and lactoferrin-mediated bactericidal activity. Infect. Immun. 80:1166-1180.
38. Burton RL, Nahm MH. 2006. Development and validation of a fourfold multiplexed opsonization assay (MOPA4) for pneumococcal antibodies. Clin. Vaccine Immunol. 13:1004-1009.
39. Burton RL, Nahm MH. 2012. Development of a fourfold multiplexed opsonophagocytosis assay for pneumococcal antibodies against additional serotypes and discovery of serological subtypes in Streptococcus pneumoniae serotype 20. Clin. Vaccine Immunol. 19:835-841.
40. Romero-Steiner S, Libutti D, Pais LB, Dykes J, Anderson P, Whitin JC, Keyserling HL, Carlone GM. 1997. Standardization of an opsonophagocytic assay for the measurement of functional antibody activity against Streptococcus pneumoniae using differentiated HL-60 cells. Clin. Diagn. Lab. Immunol. 4:415-422.
41. Briles DE, Forman C, Horowitz JC, Volanakis JE, Benjamin WH, Jr, McDaniel LS, Eldridge J, Brooks J. 1989. Antipneumococcal effects of C-reactive protein and monoclonal antibodies to pneumococcal cell wall and capsular antigens. Infect. Immun. 57:1457-1464.
42. Giefing C, Meinke AL, Hanner M, Henics T, Bui MD, Gelbmann D, Lundberg U, Senn BM, Schunn M, Habel A, Henriques-Normark B, Ortqvist A, Kalin M, von Gabain A, Nagy E. 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.
43. Ren B, McCrory MA, Pass C, Bullard DC, Ballantyne CM, Xu Y, Briles DE, Szalai AJ. 2004. The virulence function of Streptococcus pneumoniae surface protein A involves inhibition of complement activation and impairment of complement receptor-mediated protection. J. Immunol. 173:7506-7512.
44. Balachandran P, Brooks-Walter A, Virolainen-Julkunen A, Hollingshead SK, Briles DE. 2002. The 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.
45. 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.
46. Ogunniyi AD, LeMessurier KS, Graham RM, Watt JM, Briles DE, Stroeher UH, Paton JC. 2007. Contributions of pneumolysin, pneumococcal surface protein A (PspA), and PspC to pathogenicity of Streptococcus pneumoniae D39 in a mouse model. Infect. Immun. 75:1843-1851.
47. 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.
48. 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.
49. 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.
50. Coral MCV, Fonseca N, Castañeda E, Di Fabio JL, Hollingshead SK, Briles DE. 2001. Pneumococcal surface protein A of invasive Streptococcus pneumoniae isolates from Colombian children. Emerg. Infect. Dis. 7:832-836.
51. Hollingshead SK, Becker RS, Briles DE. 2000. Diversity of PspA: mosaic genes and evidence for past recombination in Streptococcus pneumoniae. Infect. Immun. 68:5889-5900.
52. Lee H, Nahm MH, Kim KH. 2010. The effect of age on the response to the pneumococcal polysaccharide vaccine. BMC Infect. Dis. 10:60. doi:10.1186/1471-2334-10-60.
53. Yu J, Lin J, Benjamin WH, Jr, Waites KB, Lee CH, Nahm MH. 2005. Rapid multiplex assay for serotyping pneumococci with monoclonal and polyclonal antibodies. J. Clin. Microbiol. 43:156-162.
54. Nahm MH, Olander JV, Magyarlaki M. 1997. Identification of cross-reactive antibodies with low opsonophagocytic activity for Streptococcus pneumoniae. J. Infect. Dis. 176:698-703.
55. 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.
56. Wofsy L, Burr B. 1969. The use of affinity chromatography for the specific purification of antibodies and antigens. J. Immunol. 103:380-382.
57. Sun Y, Hwang Y, Nahm MH. 2001. Avidity, potency, and cross-reactivity of monoclonal antibodies to pneumococcal capsular polysaccharide serotype 6B. Infect. Immun. 69:336-344.
58. Baril L, Briles DE, Crozier P, King J, Punar M, Hollingshead SK, McCormick JB. 2004. Characterization of antibodies to PspA and PsaA in adults over 50 years of age with invasive pneumococcal disease. Vaccine 23:789-793.
59. 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.
60. Virolainen A, Russell W, Crain MJ, Rapola S, Käyhty H, Briles DE. 2000. Human antibodies to pneumococcal surface protein A in health and disease. Pediatr. Infect. Dis. J. 19:134-138.
61. Austrian R. 1979. Pneumococcal vaccine: development and prospects. Am. J. Med. 67:547-549.
62. Siber GR, Chang I, Baker S, Fernsten P, O'Brien KL, Santosham M, Klugman KP, Madhi SA, Paradiso P, Kohberger R. 2007. Estimating the protective concentration of anti-pneumococcal capsular polysaccharide antibodies. Vaccine 25:3816-3826.
63. Darrieux M, Miyaji EN, Ferreira DM, Lopes LM, Lopes AP, Ren B, Briles DE, Hollingshead SK, Leite LC. 2007. Fusion proteins containing family 1 and family 2 PspA fragments elicit protection against Streptococcus pneumoniae that correlates with antibody-mediated enhancement of complement deposition. Infect. Immun. 75:5930-5938.
64. Dalia AB, Weiser JN. 2011. Minimization of bacterial size allows for complement evasion and is overcome by the agglutinating effect of antibody. Cell Host Microbe 10:486-496.
65. 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.