A modified surface killing assay (MSKA) as a functional in vitro assay for identifying protective antibodies against pneumococcal surface protein A (PspA)

Vaccine

Volumn 32, Issue 1, 2013, Pages 39-47

  Genschmer, Kristopher R ^a   Accavitti Loper, Mary Ann ^b   Briles, David E ^a,b,c  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

Functional assay; Pneumococcal surface protein A; Polymorphonuclear leukocytes; PspA; Streptococcus pneumoniae; Surface killing assay

Indexed keywords

BACTERIAL PROTEIN; CYTOCHALASIN D; MEMBRANE PROTEIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 16.3; MONOCLONAL ANTIBODY 1B2.21; MONOCLONAL ANTIBODY 5C6.1; MONOCLONAL ANTIBODY 6E5.5; MONOCLONAL ANTIBODY 8B2.19; MONOCLONAL ANTIBODY XIR278; PNEUMOCOCCAL SURFACE PROTEIN A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASCITES FLUID; COLONY FORMING UNIT; COMPLEMENT DEPOSITION; CONTROLLED STUDY; DYING; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IN VITRO STUDY; LETHAL DOSE; MODIFIED SURFACE KILLING ASSAY; MOUSE; NEUTROPHIL; NONHUMAN; PASSIVE IMMUNIZATION; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SERUM BACTERICIDAL ANTIBODY ASSAY; STREPTOCOCCUS PNEUMONIAE;

FUNCTIONAL ASSAY; PNEUMOCOCCAL SURFACE PROTEIN A; POLYMORPHONUCLEAR LEUKOCYTES; PSPA; STREPTOCOCCUS PNEUMONIAE; SURFACE KILLING ASSAY;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; BACTERIAL PROTEINS; HUMANS; IMMUNIZATION, PASSIVE; MICE; PHAGOCYTOSIS; PNEUMOCOCCAL INFECTIONS; PNEUMOCOCCAL VACCINES; STREPTOCOCCUS PNEUMONIAE;

EID: 84891958881     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2013.10.080     Document Type: Article

References (61)

1. Bryce J., Boschi-Pinto C., Shibuya K., Black R.E., WHO Child Health Epidemiology Reference Group WHO estimates of the causes of death in children. Lancet 2005, 365:1147-1152.
2. Wardlaw T., Salama P., Johansson E.W., Mason E. Pneumonia: the leading killer of children. Lancet 2006, 368:1048-1050.
3. Park I.H., Pritchard D.G., Cartee R., Brandao A., Brandileone M.C., Nahm M.H. Discovery of a new capsular serotype (6C) within serogroup 6 of Streptococcus pneumoniae. J Clin Microbiol 2007, 45:1225-1233.
4. Kadioglu A., Weiser J.N., Paton J.C., Andrew P.W. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 2008, 6:288-301.
5. Pletz M.W., Maus U., Krug N., Welte T., Lode H. Pneumococcal vaccines: mechanism of action, impact on epidemiology and adaption of the species. Int J Antimicrob Agents 2008, 32:199-206.
6. Marriott H.M., Dockrell D.H. Streptococcus pneumoniae: the role of apoptosis in host defense and pathogenesis. Int J Biochem Cell Biol 2006, 38:1848-1854.
7. Abeyta M., Hardy G.G., Yother J. Genetic alteration of capsule type but not PspA type affects accessibility of surface-bound complement and surface antigens of Streptococcus pneumoniae. Infect Immun 2003, 71:218-225.
8. Brown E.J., Joiner K.A., Gaither T.A., Hammer C.H., Frank M.M. The interaction of C3b bound to pneumococci with factor H (beta 1H globulin), factor I (C3b/C4b inactivator), and properdin factor B of the human complement system. J Immunol 1983, 131:409-415.
9. Winkelstein J.A., Abramovitz A.S., Tomasz A. Activation of C3 via the alternative complement pathway results in fixation of C3b to the pneumococcal cell wall. J Immunol 1980, 124:2502-2506.
10. Whitney C.G., Farley M.M., Hadler J., Harrison L.H., Bennett N.M., Lynfield R., et al. Decline in invasive pneumococcal disease after the introduction of protein-polysaccharide conjugate vaccine. N Engl J Med 2003, 348:1737-1746.
11. Shapiro E.D., Berg A.T., Austrian R., Schroeder D., Parcells V., Margolis A., et al. The protective efficacy of polyvalent pneumococcal polysaccharide vaccine. N Engl J Med 1991, 325:1453-1460.
12. Shinefield H.R., Black S. Efficacy of pneumococcal conjugate vaccines in large scale field trials. Pediatr Infect Dis J 2000, 19:394-397.
13. Hicks L.A., Harrison L.H., Flannery B., Hadler J.L., Schaffner W., Craig A.S., et al. 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 2007, 196:1346-1354.
14. Hsu H.E., Shutt K.A., Moore M.R., Beall B.W., Bennett N.M., Craig A.S., et al. Effect of pneumococcal conjugate vaccine on pneumococcal meningitis. N Engl J Med 2009, 360:244-256.
15. Singleton R.J., Hennessy T.W., Bulkow L.R., Hammitt L.L., Zulz T., Hurlburt D.A., et al. Invasive pneumococcal disease caused by nonvaccine serotypes among Alaska native children with high levels of 7-valent pneumococcal conjugate vaccine coverage. JAMA 2007, 297:1784-1792.
16. Barocchi M.A., Censini S., Rappuoli R. Vaccines in the era of genomics: the pneumococcal challenge. Vaccine 2007, 25:2963-2973.
17. Saxenian H., Cornejo S., Thorien K., Hecht R., Schwalbe N. An analysis of how the GAVI alliance and low- and middle-income countries can share costs of new vaccines. Health Aff (Millwood) 2011, 30:1122-1133.
18. Crain M.J., Waltman W.D., Turner J.S., Yother J., Talkington D.F., McDaniel L.S., et al. Pneumococcal surface protein A (PspA) is serologically highly variable and is expressed by all clinically important capsular serotypes of Streptococcus pneumoniae. Infect Immun 1990, 58:3293-3299.
19. Hollingshead S.K., Baril L., Ferro S., King J., Coan P., Briles D.E. Pneumococcal surface protein A (PspA) family distribution among clinical isolates from adults over 50 years of age collected in seven countries. J Med Microbiol 2006, 55:215-221.
20. Ferreira D.M., Darrieux M., Silva D.A., Leite L.C., Ferreira J.M., Ho P.L., et al. Characterization of protective mucosal and systemic immune responses elicited by pneumococcal surface protein PspA and PspC nasal vaccines against a respiratory pneumococcal challenge in mice. Clin Vaccine Immunol 2009, 16:636-645.
21. Oma K., Zhao J., Ezoe H., Akeda Y., Koyama S., Ishii K.J., et al. Intranasal immunization with a mixture of PspA and a Toll-like receptor agonist induces specific antibodies and enhances bacterial clearance in the airways of mice. Vaccine 2009, 27:3181-3188.
22. Miyaji E.N., Oliveira M.L., Carvalho E., Ho P.L. Serotype-independent pneumococcal vaccines. Cell Mol Life Sci 2013, 70:3303-3326.
23. Briles D.E., Hollingshead S.K., King J., Swift A., Braun P.A., Park M.K., et al. 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 2000, 182:1694-1701.
24. Briles D.E., Hollingshead S.K., Swiatlo E., Brooks-Walter A., Szalai A., Virolainen A., et al. PspA and PspC: their potential for use as pneumococcal vaccines. Microb Drug Resist 1997, 3:401-408.
25. Burton R.L., Nahm M.H. Development and validation of a fourfold multiplexed opsonization assay (MOPA4) for pneumococcal antibodies. Clin Vaccine Immunol 2006, 13:1004-1009.
26. Romero-Steiner S., Libutti D., Pais L.B., Dykes J., Anderson P., Whitin J.C., et al. Standardization of an opsonophagocytic assay for the measurement of functional antibody activity against Streptococcus pneumoniae using differentiated HL-60 cells. Clin Diagn Lab Immunol 1997, 4:415-422.
27. Jodar L., Butler J., Carlone G., Dagan R., Goldblatt D., Kayhty H., et al. Serological criteria for evaluation and licensure of new pneumococcal conjugate vaccine formulations for use in infants. Vaccine 2003, 21:3265-3272.
28. Burton R.L., Nahm M.H. 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 2012, 19:835-841.
29. Weinberger D.M., Trzcinski K., Lu Y.J., Bogaert D., Brandes A., Galagan J., et al. Pneumococcal capsular polysaccharide structure predicts serotype prevalence. PLoS Pathog 2009, 5:e1000476.
30. Berry A.M., Paton J.C. Additive attenuation of virulence of Streptococcus pneumoniae by mutation of the genes encoding pneumolysin and other putative pneumococcal virulence proteins. Infect Immun 2000, 68:133-140.
31. Kim J.O., Romero-Steiner S., Sorensen U.B., Blom J., Carvalho M., Barnard S., et al. Relationship between cell surface carbohydrates and intrastrain variation on opsonophagocytosis of Streptococcus pneumoniae. Infect Immun 1999, 67:2327-2333.
32. Avery O.T., Macleod C.M., McCarty M. 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 1944, 79:137-158.
33. Tettelin H., Nelson K.E., Paulsen I.T., Eisen J.A., Read T.D., Peterson S., et al. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 2001, 293:498-506.
34. Briles D.E., Crain M.J., Gray B.M., Forman C., Yother J. Strong association between capsular type and virulence for mice among human isolates of Streptococcus pneumoniae. Infect Immun 1992, 60:111-116.
35. Yother J., Forman C., Gray B.M., Briles D.E. Protection of mice from infection with Streptococcus pneumoniae by anti-phosphocholine antibody. Infect Immun 1982, 36:184-188.
36. Briles D.E., Nahm M., Schroer K., Davie J., Baker P., Kearney J., et al. Antiphosphocholine antibodies found in normal mouse serum are protective against intravenous infection with type 3 Streptococcus pneumoniae. J Exp Med 1981, 153:694-705.
37. McDaniel L.S., Ralph B.A., McDaniel D.O., Briles D.E. Localization of protection-eliciting epitopes on PspA of Streptococcus pneumoniae between amino acid residues 192 and 260. Microb Pathog 1994, 17:323-337.
38. Hollingshead S.K., Becker R., Briles D.E. Diversity of PspA: mosaic genes and evidence for past recombination in Streptococcus pneumoniae. Infect Immun 2000, 68:5889-5900.
39. Ren B., Li J., Genschmer K., Hollingshead S.K., Briles D.E. The absence of PspA or the presence of antibody to PspA each facilitate the complement-dependent phagocytosis of pneumococci in vitro. Clin Vaccine Immunol 2012, 19:1574-1582.
40. Krause R.M. The search for antibodies with molecular uniformity. Adv Immunol 1970, 12:1-56.
41. Bannur S.V., Kulgod S.V., Metkar S.S., Mahajan S.K., Sainis J.K. Protein determination by Ponceau S using digital color image analysis of protein spots on nitrocellulose membranes. Anal Biochem 1999, 267:382-389.
42. Zhang B., Hirahashi J., Cullere X., Mayadas T.N. Elucidation of molecular events leading to neutrophil apoptosis following phagocytosis: cross-talk between caspase 8, reactive oxygen species, and MAPK/ERK activation. J Biol Chem 2003, 278:28443-28454.
43. McDaniel L.S., Scott G., Kearney J.F., Briles D.E. Monoclonal antibodies against protease-sensitive pneumococcal antigens can protect mice from fatal infection with Streptococcus pneumoniae. J Exp Med 1984, 160:386-397.
44. Daniels C.C., Briles T.C., Mirza S., Hakansson A.P., Briles D.E. Capsule does not block antibody binding to PspA, a surface virulence protein of Streptococcus pneumoniae. Microb Pathog 2006, 40:228-233.
45. Elliott J.A., Winn W.C. Treatment of alveolar macrophages with cytochalasin D inhibits uptake and subsequent growth of Legionella pneumophila. Infect Immun 1986, 51:31-36.
46. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., et al. Neutrophil extracellular traps kill bacteria. Science 2004, 303:1532-1535.
47. Ren B., Szalai A.J., Hollingshead S.K., Briles D.E. Effects of PspA and Antibodies to PspA on activation and deposition of complement on the pneumococcal surface. Infect Immun 2003, 72:114-122.
48. Li J., Glover D.T., Szalai A.J., Hollingshead S.K., Briles D.E. PspA and PspC minimize immune adherence and transfer of pneumococci from erythrocytes to macrophages through their effects on complement activation. Infect Immun 2007, 75:5877-5885.
49. Mukerji R., Mirza S., Roche A.M., Widener R.W., Croney C.M., Rhee D.K., et al. 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 2012, 189:5327-5335.
50. Briles D.E., Hollingshead S.K., Jonsdottir I. Animal models of invasive pneumococcal disease. Pneumococcal vaccines: the impact of conjugate vaccine 2008, 47-58. ASM Press, Washington, DC. G.R. Siber, K.P. Klugman, P.H. Mäkelä (Eds.).
51. McDaniel L.S., Scott G., Kearney J.F., Briles D.E. Monoclonal antibodies against protease sensitive pneumococcal antigens can protect mice from fatal infection with Streptococcus pneumoniae. J Exp Med 1984, 160:386-397.
52. Briles D.E., Hollingshead S.K., King J., Swift A., Braun P.A., Park M.K., et al. Immunization of humans with rPspA elicits antibodies, which passively protect mice from fatal infection with Streptococcus pneumoniae bearing heterologous PspA. J Infect Dis 2000, 182:1694-1701.
53. Hakansson A., Roche H., Mirza S., McDaniel L.S., Brooks-Walter A., Briles D.E. Characterization of the binding of human lactoferrin to pneumococcal surface protein A (PspA). Infect Immun 2001, 69:3372-3381.
54. Ren B., Szalai A.J., Hollingshead S.K., Briles D.E. Effects of PspA and antibodies to PspA on activation and deposition of complement on the pneumococcal surface. Infect Immun 2004, 72:114-122.
55. Darrieux M., Miyaji E.N., Ferreira D.M., Lopes L.M., Lopes A.P., Ren B., et al. 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 2007, 75:5930-5938.
56. Ochs M.M., Bartlett W., Briles D.E., Hicks B., Jurkuvenas A., Lau P., et al. Vaccine-induced human antibodies to PspA augment complement C3 deposition on Streptococcus pneumoniae. Microb Pathog 2008, 44:204-214.
57. Ren B., Li J., Genschmer K., Hollingshead S.K., Briles D.E. The absence of PspA or presence of antibody to PspA facilitates the complement-dependent phagocytosis of pneumococci in vitro. Clin Vaccine Immunol 2012, 19:1574-1582.
58. Briles D.E., Tart R.C., Wu H.Y., Ralph B.A., Russell M.W., McDaniel L.S. Systemic and mucosal protective immunity to pneumococcal surface protein A. Ann NY Acad Sci 1996, 797:118-126.
59. Briles D.E., Forman C., Horowitz J.C., Volanakis J.E., Benjamin W.H., McDaniel L.S., et al. Antipneumococcal effects of C-reactive protein and monoclonal antibodies to pneumococcal cell wall and capsular antigens. Infect Immun 1989, 57:1457-1464.
60. Smith M.R., Wood W.B. Surface phagocytosis: further evidence of its destructive action upon fully encapsulated pneumococci in the absence of type-specific antibody. J Exp Med 1958, 107:1-12.
61. Briles D.E., Hollingshead S.K., Nabors G.S., Paton J.C., Brooks-Walter A. The potential for using protein vaccines to protect against otitis media caused by Streptococcus pneumoniae. Vaccine 2000, 19(Suppl. 1):S87-S95.