Development of quantitative suspension array assays for six immunoglobulin isotypes and subclasses to multiple Plasmodium falciparum antigens

Journal of Immunological Methods

Volumn 455, Issue , 2018, Pages 41-54

  Vidal, Marta ^a   Aguilar, Ruth ^a   Campo, Joseph J ^a,b   Dobaño, Carlota ^a  

^a CENTRE FOR RESEARCH IN ENVIRONMENTAL EPIDEMIOLOGY CREAL   (Spain)

^b Antigen Discovery Inc   (United States)

Author keywords

IgE; IgG; IgM; Multiplexed antigens; Plasmodium falciparum; Subclasses

Indexed keywords

AMA 1 3D7 ANTIGEN; AMA 1 FVO ANTIGEN; ANTIGEN; CELTOS ANTIGEN; CSP ANTIGEN; CSP C TERM ANTIGEN; CSP NANP ANTIGEN; DBL ALPHA ANTIGEN; EBA 175 ANTIGEN; EXP ANTIGEN; IMMUNOGLOBULIN CLASS; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN G4; IMMUNOGLOBULIN M; LSA 1 ANTIGEN; MSP 1 42 3D7 ANTIGEN; MSP 1 42 FVO ANTIGEN; MSP 2 CHI50 ANTIGEN; MSP 3 3D7 ANTIGEN; PLASMODIUM FALCIPARUM ANTIGEN; SSP2 ANTIGEN; UNCLASSIFIED DRUG; MALARIA VACCINE; PARASITE ANTIGEN; PROTOZOON ANTIBODY;

ADULT; ARTICLE; BLOOD SAMPLING; HUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; QUANTITATIVE ASSAY; BLACK PERSON; CAUCASIAN; IMMUNOLOGY; MALARIA FALCIPARUM; OBSERVER VARIATION; PROCEDURES; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; SEROLOGY; STANDARD;

ADULT; AFRICAN CONTINENTAL ANCESTRY GROUP; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; EUROPEAN CONTINENTAL ANCESTRY GROUP; HUMANS; IMMUNOGLOBULIN ISOTYPES; MALARIA VACCINES; MALARIA, FALCIPARUM; OBSERVER VARIATION; PLASMODIUM FALCIPARUM; REFERENCE STANDARDS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SEROLOGIC TESTS;

EID: 85041625948     PISSN: 00221759     EISSN: 18727905     Source Type: Journal    
DOI: 10.1016/j.jim.2018.01.009     Document Type: Article

References (56)

1. Ackerman, M.E., Mikhailova, A., Brown, E.P., Dowell, K.G., Walker, B.D., Bailey-Kellogg, C., et al. Polyfunctional HIV-specific antibody responses are associated with spontaneous HIV control. PLoS Pathog., 12(1), 2016, e1005315, 10.1371/journal.ppat.1005315.
2. Aguilar, R., Machevo, S., Menendez, C., Bardaji, A., Nhabomba, A., Alonso, P.L., et al. Comparison of placental blood microscopy and the ICT HRP2 rapid diagnostic test to detect placental malaria. Trans. R. Soc. Trop. Med. Hyg. 106:9 (2012), 573–575, 10.1016/j.trstmh.2012.05.001.
3. Aguilar, R., Casabonne, D., O'Callaghan-Gordo, C., Vidal, M., Campo, J.J., Mutalima, N., et al. Assessment of the combined effect of Epstein-Barr virus and Plasmodium falciparum infections on endemic Burkitt lymphoma using a multiplex serological approach. Front. Immunol., 2017, 10.3389/fimmu.2017.01284 (Provissionally accepted).
4. Ahmed Ismail, H., Tijani, M.K., Langer, C., Reiling, L., White, M.T., Beeson, J.G., et al. Subclass responses and their half-lives for antibodies against EBA175 and PfRh2 in naturally acquired immunity against Plasmodium falciparum malaria. Malar. J., 13, 2014, 425, 10.1186/1475-2875-13-425.
5. Angov, E., Aufiero, B.M., Turgeon, A.M., Van Handenhove, M., Ockenhouse, C.F., Kester, K.E., et al. Development and pre-clinical analysis of a Plasmodium falciparum merozoite surface protein-1(42) malaria vaccine. Mol. Biochem. Parasitol. 128:2 (2003), 195–204 (DOI: S016668510300077X).
6. Angov, E., Hillier, C.J., Kincaid, R.L., Lyon, J.A., Heterologous protein expression is enhanced by harmonizing the codon usage frequencies of the target gene with those of the expression host. PLoS One, 3(5), 2008, e2189, 10.1371/journal.pone.0002189.
7. Arama, C., Skinner, J., Doumtabe, D., Portugal, S., Tran, T.M., Jain, A., et al. Genetic resistance to malaria is associated with greater enhancement of immunoglobulin (Ig)M than IgG responses to a broad array of Plasmodium falciparum antigens. Open Forum Infect Dis., 2(3), 2015, ofv118, 10.1093/ofid/ofv118 (ofv118 [pii]).
8. Aranda, C., Aponte, J.J., Saute, F., Casimiro, S., Pinto, J., Sousa, C., et al. Entomological characteristics of malaria transmission in Manhica, a rural area in southern Mozambique. J. Med. Entomol. 42:2 (2005), 180–186.
9. Basile, A.J., Horiuchi, K., Panella, A.J., Laven, J., Kosoy, O., Lanciotti, R.S., et al. Multiplex microsphere immunoassays for the detection of IgM and IgG to arboviral diseases. PLoS One, 8(9), 2013, e75670, 10.1371/journal.pone.0075670.
10. Bouharoun-Tayoun, H., Druilhe, P., Plasmodium falciparum malaria: evidence for an isotype imbalance which may be responsible for delayed acquisition of protective immunity. Infect. Immun. 60:4 (1992), 1473–1481.
11. Bouharoun-Tayoun, H., Oeuvray, C., Lunel, F., Druilhe, P., Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages. J. Exp. Med. 182:2 (1995), 409–418.
12. Boyle, M.J., Reiling, L., Feng, G., Langer, C., Osier, F.H., Aspeling-Jones, H., et al. Human antibodies fix complement to inhibit Plasmodium falciparum invasion of erythrocytes and are associated with protection against malaria. Immunity 42:3 (2015), 580–590, 10.1016/j.immuni.2015.02.012 (S1074-7613(15)00087-4 [pii]).
13. Branch, O.H., Udhayakumar, V., Hightower, A.W., Oloo, A.J., Hawley, W.A., Nahlen, B.L., et al. A longitudinal investigation of IgG and IgM antibody responses to the merozoite surface protein-1 19-kilo Dalton domain of Plasmodium falciparum in pregnant women and infants: associations with febrile illness, parasitemia, and anemia. Am. J. Trop. Med. Hyg. 58:2 (1998), 211–219.
14. Brown, E.P., Licht, A.F., Dugast, A.S., Choi, I., Bailey-Kellogg, C., Alter, G., et al. High-throughput, multiplexed IgG subclassing of antigen-specific antibodies from clinical samples. J. Immunol. Methods 386:1–2 (2012), 117–123, 10.1016/j.jim.2012.09.007.
15. Calissano, C., Modiano, D., Sirima, B.S., Konate, A., Sanou, I., Sawadogo, A., et al. IgE antibodies to Plasmodium falciparum and severity of malaria in children of one ethnic group living in Burkina Faso. Am. J. Trop. Med. Hyg. 69:1 (2003), 31–35.
16. Campo, J.J., Dobano, C., Sacarlal, J., Guinovart, C., Mayor, A., Angov, E., et al. Impact of the RTS,S malaria vaccine candidate on naturally acquired antibody responses to multiple asexual blood stage antigens. PLoS One, 6(10), 2011, e25779, 10.1371/journal.pone.0025779.
17. Cavanagh, D.R., Dobano, C., Elhassan, I.M., Marsh, K., Elhassan, A., Hviid, L., et al. Differential patterns of human immunoglobulin G subclass responses to distinct regions of a single protein, the merozoite surface protein 1 of Plasmodium falciparum. Infect. Immun. 69:2 (2001), 1207–1211, 10.1128/IAI.69.2.1207-1211.2001.
18. Cham, G.K., Kurtis, J., Lusingu, J., Theander, T.G., Jensen, A.T., Turner, L., A semi-automated multiplex high-throughput assay for measuring IgG antibodies against Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) domains in small volumes of plasma. Malar. J., 7, 2008, 108, 10.1186/1475-2875-7-108.
19. Chung, A.W., Kumar, M.P., Arnold, K.B., Yu, W.H., Schoen, M.K., Dunphy, L.J., et al. Dissecting polyclonal vaccine-induced humoral immunity against HIV using systems serology. Cell 163:4 (2015), 988–998, 10.1016/j.cell.2015.10.027.
20. Cohen, S., Mc, G.I., Carrington, S., Gamma-globulin and acquired immunity to human malaria. Nature 192 (1961), 733–737.
21. Dodig, S., Interferences in quantitative immunochemical methods. Biochemia Medica 19:1 (2009), 50–62.
22. Doolan, D.L., Dobano, C., Baird, J.K., Acquired immunity to malaria. Clin. Microbiol. Rev. 22:1 (2009), 13–36, 10.1128/CMR.00025-08 (Table of Contents).
23. Dutta, S., Lee, S.Y., Batchelor, A.H., Lanar, D.E., Structural basis of antigenic escape of a malaria vaccine candidate. Proc. Natl. Acad. Sci. U. S. A. 104:30 (2007), 12488–12493, 10.1073/pnas.0701464104.
24. Eisen, H.N., Chakraborty, A.K., Evolving concepts of specificity in immune reactions. Proc. Natl. Acad. Sci. U. S. A. 107:52 (2010), 22373–22380, 10.1073/pnas.1012051108 (1012051108 [pii]).
25. Fouda, G.G., Leke, R.F., Long, C., Druilhe, P., Zhou, A., Taylor, D.W., et al. Multiplex assay for simultaneous measurement of antibodies to multiple Plasmodium falciparum antigens. Clin. Vaccine Immunol. 13:12 (2006), 1307–1313, 10.1128/CVI.00183-06.
26. Gottschalk, P.G., Dunn, J.R., The five-parameter logistic: a characterization and comparison with the four-parameter logistic. Anal. Biochem. 343:1 (2005), 54–65, 10.1016/j.ab.2005.04.035.
27. Gunn, B.M., Alter, G., Modulating antibody functionality in infectious disease and vaccination. Trends Mol. Med. 22:11 (2016), 969–982, 10.1016/j.molmed.2016.09.002.
28. Hillier, C.J., Ware, L.A., Barbosa, A., Angov, E., Lyon, J.A., Heppner, D.G., et al. Process development and analysis of liver-stage antigen 1, a preerythrocyte-stage protein-based vaccine for Plasmodium falciparum. Infect. Immun. 73:4 (2005), 2109–2115, 10.1128/IAI.73.4.2109-2115.2005.
29. Israelsson, E., Balogun, H., Vasconcelos, N.M., Beser, J., Roussilhon, C., Rogier, C., et al. Antibody responses to a C-terminal fragment of the Plasmodium falciparum blood-stage antigen Pf332 in Senegalese individuals naturally primed to the parasite. Clin. Exp. Immunol. 152:1 (2008), 64–71, 10.1111/j.1365-2249.2008.03607.x.
30. Jones, D.D., DeIulio, G.A., Winslow, G.M., Antigen-driven induction of polyreactive IgM during intracellular bacterial infection. J. Immunol. 189:3 (2012), 1440–1447, 10.4049/jimmunol.1200878.
31. Kariu, T., Ishino, T., Yano, K., Chinzei, Y., Yuda, M., CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts. Mol. Microbiol. 59:5 (2006), 1369–1379, 10.1111/j.1365-2958.2005.05024.x.
32. Kocken, C.H., Withers-Martinez, C., Dubbeld, M.A., van der Wel, A., Hackett, F., Valderrama, A., et al. High-level expression of the malaria blood-stage vaccine candidate Plasmodium falciparum apical membrane antigen 1 and induction of antibodies that inhibit erythrocyte invasion. Infect. Immun. 70:8 (2002), 4471–4476.
33. Laurens, M.B., Thera, M.A., Coulibaly, D., Ouattara, A., Kone, A.K., Guindo, A.B., et al. Extended safety, immunogenicity and efficacy of a blood-stage malaria vaccine in malian children: 24-month follow-up of a randomized, double-blinded phase 2 trial. PLoS One, 8(11), 2013, e79323, 10.1371/journal.pone.0079323 (PONE-D-13-16558 [pii]).
34. Mayor, A., Rovira-Vallbona, E., Srivastava, A., Sharma, S.K., Pati, S.S., Puyol, L., et al. Functional and immunological characterization of a Duffy binding-like alpha domain from Plasmodium falciparum erythrocyte membrane protein 1 that mediates rosetting. Infect. Immun. 77:9 (2009), 3857–3863, 10.1128/IAI.00049-09.
35. Mbengue, B., Niang, B., Niang, M.S., Varela, M.L., Fall, B., Fall, M.M., et al. Inflammatory cytokine and humoral responses to Plasmodium falciparum glycosylphosphatidylinositols correlates with malaria immunity and pathogenesis. Immun. Inflammation Dis. 4:1 (2016), 24–34, 10.1002/iid3.89.
36. Medeiros, M.M., Fotoran, W.L., Dalla Martha, R.C., Katsuragawa, T.H., Pereira da Silva, L.H., Wunderlich, G., Natural antibody response to Plasmodium falciparum merozoite antigens MSP5, MSP9 and EBA175 is associated to clinical protection in the Brazilian Amazon. BMC Infect. Dis., 13, 2013, 608, 10.1186/1471-2334-13-608.
37. Moncunill, G., Mayor, A., Bardaji, A., Puyol, L., Nhabomba, A., Barrios, D., et al. Cytokine profiling in immigrants with clinical malaria after extended periods of interrupted exposure to Plasmodium falciparum. PLoS One, 8(8), 2013, e73360, 10.1371/journal.pone.0073360.
38. Nhabomba, A.J., Guinovart, C., Jimenez, A., Manaca, M.N., Quinto, L., Cistero, P., et al. Impact of age of first exposure to Plasmodium falciparum on antibody responses to malaria in children: a randomized, controlled trial in Mozambique. Malar. J., 13, 2014, 121, 10.1186/1475-2875-13-121.
39. Ochsenbein, A.F., Fehr, T., Lutz, C., Suter, M., Brombacher, F., Hengartner, H., et al. Control of early viral and bacterial distribution and disease by natural antibodies. Science 286:5447 (1999), 2156–2159 (8051 [pii).
40. Ondigo, B.N., Park, G.S., Gose, S.O., Ho, B.M., Ochola, L.A., Ayodo, G.O., et al. Standardization and validation of a cytometric bead assay to assess antibodies to multiple Plasmodium falciparum recombinant antigens. Malar. J., 11, 2012, 427, 10.1186/1475-2875-11-427.
41. Osier, F.H., Feng, G., Boyle, M.J., Langer, C., Zhou, J., Richards, J.S., et al. Opsonic phagocytosis of Plasmodium falciparum merozoites: mechanism in human immunity and a correlate of protection against malaria. BMC Med., 12, 2014, 108, 10.1186/1741-7015-12-108 (1741-7015-12-108 [pii].).
42. Otsyula, N., Angov, E., Bergmann-Leitner, E., Koech, M., Khan, F., Bennett, J., et al. Results from tandem phase 1 studies evaluating the safety, reactogenicity and immunogenicity of the vaccine candidate antigen Plasmodium falciparum FVO merozoite surface protein-1 (MSP1(42)) administered intramuscularly with adjuvant system AS01. Malar. J., 12, 2013, 29, 10.1186/1475-2875-12-29 (1475-2875-12-29 [pii]).
43. Pandey, K.C., Singh, S., Pattnaik, P., Pillai, C.R., Pillai, U., Lynn, A., et al. Bacterially expressed and refolded receptor binding domain of Plasmodium falciparum EBA-175 elicits invasion inhibitory antibodies. Mol. Biochem. Parasitol. 123:1 (2002), 23–33, 10.1016/S0166-6851(02)00122-6.
44. Perlmann, P., Perlmann, H., Flyg, B.W., Hagstedt, M., Elghazali, G., Worku, S., et al. Immunoglobulin E, a pathogenic factor in Plasmodium falciparum malaria. Infect. Immun. 65:1 (1997), 116–121.
45. Perlmann, P., Perlmann, H., Looareesuwan, S., Krudsood, S., Kano, S., Matsumoto, Y., et al. Contrasting functions of IgG and IgE antimalarial antibodies in uncomplicated and severe Plasmodium falciparum malaria. Am. J. Trop. Med. Hyg. 62:3 (2000), 373–377.
46. Perraut, R., Richard, V., Varela, M.L., Trape, J.F., Guillotte, M., Tall, A., et al. Comparative analysis of IgG responses to Plasmodium falciparum MSP1p19 and PF13-DBL1alpha1 using ELISA and a magnetic bead-based duplex assay (MAGPIX(R)-Luminex) in a Senegalese meso-endemic community. Malar. J., 13, 2014, 410, 10.1186/1475-2875-13-410.
47. Plassmeyer, M.L., Reiter, K., Shimp, R.L. Jr., Kotova, S., Smith, P.D., Hurt, D.E., et al. Structure of the Plasmodium falciparum circumsporozoite protein, a leading malaria vaccine candidate. J. Biol. Chem. 284:39 (2009), 26951–26963, 10.1074/jbc.M109.013706.
48. Reddy, K.S., Amlabu, E., Pandey, A.K., Mitra, P., Chauhan, V.S., Gaur, D., Multiprotein complex between the GPI-anchored CyRPA with PfRH5 and PfRipr is crucial for Plasmodium falciparum erythrocyte invasion. Proc. Natl. Acad. Sci. U. S. A. 112:4 (2015), 1179–1184, 10.1073/pnas.1415466112.
49. Rinchai, D., Presnell, S., Vidal, M., Dutta, S., Chauhan, V., Cavanagh, D., et al. Blood interferon signatures putatively link lack of protection conferred by the RTS,S recombinant malaria vaccine to an antigen-specific IgE response. F1000Res(4), 2015, 919, 10.12688/f1000research.7093.2.
50. Rogers, W.O., Malik, A., Mellouk, S., Nakamura, K., Rogers, M.D., Szarfman, A., et al. Characterization of Plasmodium falciparum sporozoite surface protein 2. Proc. Natl. Acad. Sci. U. S. A. 89:19 (1992), 9176–9180.
51. Rogier, E., Moss, D.M., Chard, A.N., Trinies, V., Doumbia, S., Freeman, M.C., et al. Evaluation of immunoglobulin G responses to Plasmodium falciparum and Plasmodium vivax in Malian school children using multiplex bead assay. Am. J. Trop. Med. Hyg. 96:2 (2017), 312–318, 10.4269/ajtmh.16-0476.
52. Scopel, K.K., Fontes, C.J., Ferreira, M.U., Braga, E.M., Factors associated with immunoglobulin G subclass polarization in naturally acquired antibodies to Plasmodium falciparum merozoite surface proteins: a cross-sectional survey in Brazilian Amazonia. Clin. Vaccine Immunol. 13:7 (2006), 810–813, 10.1128/CVI.00095-06.
53. Smits, G.P., van Gageldonk, P.G., Schouls, L.M., van der Klis, F.R., Berbers, G.A., Development of a bead-based multiplex immunoassay for simultaneous quantitative detection of IgG serum antibodies against measles, mumps, rubella, and varicella-zoster virus. Clin. Vaccine Immunol. 19:3 (2012), 396–400, 10.1128/CVI.05537-11.
54. Tongren, J.E., Drakeley, C.J., McDonald, S.L., Reyburn, H.G., Manjurano, A., Nkya, W.M., et al. Target antigen, age, and duration of antigen exposure independently regulate immunoglobulin G subclass switching in malaria. Infect. Immun. 74:1 (2006), 257–264, 10.1128/IAI.74.1.257-264.2006.
55. Wang, Q., Zhao, Z., Zhang, X., Li, X., Zhu, M., Li, P., et al. Naturally acquired antibody responses to Plasmodium vivax and Plasmodium falciparum merozoite surface protein 1 (MSP1) C-terminal 19 kDa domains in an area of unstable malaria transmission in Southeast Asia. PLoS One, 11(3), 2016, e0151900, 10.1371/journal.pone.0151900.
56. WHO, World Malaria Report 2015. http://wwwwhoint/malaria/publications/world-malaria-report-2015/report/en/, 2015.