Atypical and classical memory B cells produce plasmodium falciparum neutralizing antibodies

Journal of Experimental Medicine

Volumn 210, Issue 2, 2013, Pages 389-399

  Muellenbeck, Matthias F ^a   Ueberheide, Beatrix ^c   Amulic, Borko ^b   Epp, Alexandra ^a   Fenyo, David ^d   Busse, Christian E ^a   Esen, Meral ^e,f   Theisen, Michael ^g,h   Mordmüller, Benjamin ^e,f   Wardemann, Hedda ^a  

^a Max Planck Research Group Molecular Immunology   (Germany)

^b MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^c Proteomics Resource Center   (United States)

^d NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^e UNIVERSITY OF TÜBINGEN   (Germany)

^f Centre de Recherches Médicales de Lambaréné HÔpital Albert Schweitzer   (Gabon)

^g STATENS SERUM INSTITUT   (Denmark)

^h UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; NEUTRALIZING ANTIBODY;

ADULT; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIGEN SPECIFICITY; ARTICLE; ATYPICAL MEMORY B CELL; CLASSICAL MEMORY B CELL; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; IMMUNOFLUORESCENCE; IMMUNOGLOBULIN PRODUCTION; MALARIA FALCIPARUM; MASS SPECTROMETRY; MEMORY CELL; NORMAL HUMAN; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SINGLE CELL ANALYSIS;

ADULT; AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; B-LYMPHOCYTE SUBSETS; ERYTHROCYTES; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGIC MEMORY; MALARIA VACCINES; MALARIA, FALCIPARUM; MIDDLE AGED; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; YOUNG ADULT;

EID: 84874572370     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20121970     Document Type: Article

References (48)

1. Akpogheneta, O.J., N.O. Duah, K.K. Tetteh, S. Dunyo, D.E. Lanar, M. Pinder, and D.J. Conway. 2008. Duration of naturally acquired antibody responses to blood-stage Plasmodium falciparum is age dependent and antigen specific. Infect. Immun. 76:1748-1755. http://dx.doi.org/10.1128/IAI.01333-07
2. Amanna, I.J., and M.K. Slifka. 2010. Mechanisms that determine plasma cell lifespan and the duration of humoral immunity. Immunol. Rev. 236:125- 138. http://dx.doi.org/10.1111/j.1600-065X.2010.00912.x
3. Amanna, I.J., N.E. Carlson, and M.K. Slifka. 2007. Duration of humoral immunity to common viral and vaccine antigens. N. Engl. J. Med. 357:1903- 1915. http://dx.doi.org/10.1056/NEJMoa066092
4. Bernasconi, N.L., E. Traggiai, and A. Lanzavecchia. 2002. Maintenance of serological memory by polyclonal activation of human memory B cells. Science. 298:2199-2202. http://dx.doi.org/10.1126/science.1076071
5. Bouharoun-Tayoun, H., P. Attanath, A. Sabchareon, T. Chongsuphajaisiddhi, and P. Druilhe. 1990. Antibodies that protect humans against Plasmodium falciparum blood stages do not on their own inhibit parasite growth and invasion in vitro, but act in cooperation with monocytes. J. Exp. Med. 172:1633-1641. http://dx.doi.org/10.1084/jem.172.6.1633
6. Cohen, S., I.A. McGREGOR, and S. Carrington. 1961. Gamma-globulin and acquired immunity to human malaria. Nature. 192:733-737. http://dx.doi.org/10.1038/192733a0
7. Courtin, D., M. Oesterholt, H. Huismans, K. Kusi, J. Milet, C. Badaut, O. Gaye, W. Roeffen, E.J. Remarque, R. Sauerwein, et al. 2009. The quantity and quality of African children's IgG responses to merozoite surface antigens reflect protection against Plasmodium falciparum malaria. PLoS ONE. 4:e7590. http://dx.doi.org/10.1371/journal.pone.0007590
8. Dal-Bianco, M.P., K.B. Köster, U.D. Kombila, J.F. Kun, M.P. Grobusch, G.M. Ngoma, P.B. Matsiegui, C. Supan, C.L. Salazar, M.A. Missinou, et al. 2007. High prevalence of asymptomatic Plasmodium falciparum infection in Gabonese adults. Am. J. Trop. Med. Hyg. 77:939-942.
9. de Stricker, K., J. Vuust, S. Jepsen, C. Oeuvray, and M. Theisen. 2000. Conservation and heterogeneity of the glutamate-rich protein (GLURP) among field isolates and laboratory lines of Plasmodium falciparum. Mol. Biochem. Parasitol. 111:123-130. http://dx.doi.org/10.1016/S0166-6851(00)00304-2
10. Dorfman, J.R., P. Bejon, F.M. Ndungu, J. Langhorne, M.M. Kortok, B.S. Lowe, T.W. Mwangi, T.N. Williams, and K. Marsh. 2005. B cell memory to 3 Plasmodium falciparum blood-stage antigens in a malaria-endemic area. J. Infect. Dis. 191:1623-1630. http://dx.doi.org/10.1086/429671
11. Ehrhardt, G.R., J.T. Hsu, L. Gartland, C.M. Leu, S. Zhang, R.S. Davis, and M.D. Cooper. 2005. Expression of the immunoregulatory molecule FcRH4 defines a distinctive tissue-based population of memory B cells. J. Exp. Med. 202:783-791. http://dx.doi.org/10.1084/jem.20050879
12. Ehrhardt, G.R., A. Hijikata, H. Kitamura, O. Ohara, J.Y. Wang, and M.D. Cooper. 2008. Discriminating gene expression profiles of memory B cell subpopulations. J. Exp. Med. 205:1807-1817. http://dx.doi.org/10.1084/jem.20072682
13. Esen, M., P.G. Kremsner, R. Schleucher, M. Gässler, E.B. Imoukhuede, N. Imbault, O. Leroy, S. Jepsen, B.W. Knudsen, M. Schumm, et al. 2009. Safety and immunogenicity of GMZ2 - a MSP3-GLURP fusion protein malaria vaccine candidate. Vaccine. 27:6862-6868. http://dx.doi.org/10.1016/j.vaccine.2009.09.011
14. Fowkes, F.J., J.S. Richards, J.A. Simpson, and J.G. Beeson. 2010. The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: A systematic review and meta-analysis. PLoS Med. 7:e1000218. http://dx.doi.org/10.1371/journal.pmed.1000218
15. Gardner, M.J., N. Hall, E. Fung, O. White, M. Berriman, R.W. Hyman, J.M. Carlton, A. Pain, K.E. Nelson, S. Bowman, et al. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature. 419:498-511. http://dx.doi.org/10.1038/nature01097
16. Garnham, P.C. 1949. Malarial immunity in Africans; effects in infancy and early childhood. Ann. Trop. Med. Parasitol. 43:47-61.
17. Haynes, B.F., J. Fleming, E.W. St Clair, H. Katinger, G. Stiegler, R. Kunert, J. Robinson, R.M. Scearce, K. Plonk, H.F. Staats, et al. 2005. Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science. 308:1906-1908. http://dx.doi.org/10.1126/science.1111781
18. Johnson, J.D., R.A. Dennull, L. Gerena, M. Lopez-Sanchez, N.E. Roncal, and N.C. Waters. 2007. Assessment and continued validation of the malaria SYBR green I-based fluorescence assay for use in malaria drug screening. Antimicrob. Agents Chemother. 51:1926-1933. http://dx.doi.org/10.1128/AAC.01607-06
19. Langhorne, J., F.M. Ndungu, A.M. Sponaas, and K. Marsh. 2008. Immunity to malaria: more questions than answers. Nat. Immunol. 9:725-732. http://dx.doi.org/10.1038/ni.f.205
20. Lucumi, E., C. Darling, H. Jo, A.D. Napper, R. Chandramohanadas, N. Fisher, A.E. Shone, H. Jing, S.A. Ward, G.A. Biagini, et al. 2010. Discovery of potent small-molecule inhibitors of multidrug-resistant Plasmodium falciparum using a novel miniaturized high-throughput luciferase-based assay. Antimicrob. Agents Chemother. 54:3597-3604. http://dx.doi.org/10.1128/AAC.00431-10
21. Manske, M., O. Miotto, S. Campino, S. Auburn, J. Almagro-Garcia, G. Maslen, J. O'Brien, A. Djimde, O. Doumbo, I. Zongo, et al. 2012. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature. 487:375-379. http://dx.doi.org/10.1038/nature11174
22. Meffre, E., A. Schaefer, H. Wardemann, P. Wilson, E. Davis, and M.C. Nussenzweig. 2004. Surrogate light chain expressing human peripheral B cells produce self-reactive antibodies. J. Exp. Med. 199:145-150. http://dx.doi.org/10.1084/jem.20031550
23. Meraldi, V., I. Nebié, A.B. Tiono, D. Diallo, E. Sanogo, M. Theisen, P. Druilhe, G. Corradin, R. Moret, and B.S. Sirima. 2004. Natural antibody response to Plasmodium falciparum Exp-1, MSP-3 and GLURP long synthetic peptides and association with protection. Parasite Immunol. 26:265-272. http://dx.doi.org/10.1111/j.0141-9838.2004.00705.x
24. Moir, S., J. Ho, A. Malaspina, W. Wang, A.C. DiPoto, M.A. O'Shea, G. Roby, S. Kottilil, J. Arthos, M.A. Proschan, et al. 2008. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J. Exp. Med. 205:1797-1805. http://dx.doi.org/10.1084/jem.20072683
25. Moir, S., C.M. Buckner, J. Ho, W. Wang, J. Chen, A.J. Waldner, J.G. Posada, L. Kardava, M.A. O'Shea, S. Kottilil, et al. 2010. B cells in early and chronic HIV infection: evidence for preservation of immune function associated with early initiation of antiretroviral therapy. Blood. 116:5571-5579. http://dx.doi.org/10.1182/blood-2010-05-285528
26. Mouquet, H., and M.C. Nussenzweig. 2012. Polyreactive antibodies in adaptive immune responses to viruses. Cell. Mol. Life Sci. 69:1435-1445. http://dx.doi.org/10.1007/s00018-011-0872-6
27. Mouquet, H., J.F. Scheid, M.J. Zoller, M. Krogsgaard, R.G. Ott, S. Shukair, M.N. Artyomov, J. Pietzsch, M. Connors, F. Pereyra, et al. 2010. Polyreactivity increases the apparent affinity of anti-HIV antibodies by heteroligation. Nature. 467:591-595. http://dx.doi.org/10.1038/nature09385
28. Murray, C.J., L.C. Rosenfeld, S.S. Lim, K.G. Andrews, K.J. Foreman, D. Haring, N. Fullman, M. Naghavi, R. Lozano, and A.D. Lopez. 2012. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet. 379:413-431. http://dx.doi.org/10.1016/S0140-6736(12)60034-8
29. Nduati, E.W., D.H. Ng, F.M. Ndungu, P. Gardner, B.C. Urban, and J. Langhorne. 2010. Distinct kinetics of memory B-cell and plasma-cell responses in peripheral blood following a blood-stage Plasmodium chabaudi infection in mice. PLoS ONE. 5:e15007. http://dx.doi.org/10.1371/journal.pone.0015007
30. Ndungu, F.M., E.T. Cadman, J. Coulcher, E. Nduati, E. Couper, D.W. Macdonald, D. Ng, and J. Langhorne. 2009. Functional memory B cells and long-lived plasma cells are generated after a single Plasmodium chabaudi infection in mice. PLoS Pathog. 5:e1000690. http://dx.doi.org/10.1371/journal.ppat.1000690
31. Ndungu, F.M., A. Olotu, J. Mwacharo, M. Nyonda, J. Apfeld, L.K. Mramba, G.W. Fegan, P. Bejon, and K. Marsh. 2012. Memory B cells are a more reliable archive for historical antimalarial responses than plasma antibodies in no-longer exposed children. Proc. Natl. Acad. Sci. USA. 109:8247-8252. http://dx.doi.org/10.1073/pnas.1200472109
32. Nogaro, S.I., J.C. Hafalla, B. Walther, E.J. Remarque, K.K. Tetteh, D.J. Conway, E.M. Riley, and M. Walther. 2011. The breadth, but not the magnitude, of circulating memory B cell responses to P. falciparum increases with age/exposure in an area of low transmission. PLoS ONE. 6:e25582. http://dx.doi.org/10.1371/journal.pone.0025582
33. Reynaud, C.A., M. Descatoire, I. Dogan, F. Huetz, S. Weller, and J.C. Weill. 2012. IgM memory B cells: a mouse/human paradox. Cell. Mol. Life Sci. 69:1625-1634. http://dx.doi.org/10.1007/s00018-012-0971-z
34. Rodríguez, L.E., H. Curtidor, M. Ocampo, J. Garcia, A. Puentes, J. Valbuena, R. Vera, R. López, and M.E. Patarroyo. 2005. Identifying Plasmodium falciparum merozoite surface antigen 3 (MSP3) protein peptides that bind specifically to erythrocytes and inhibit merozoite invasion. Protein Sci. 14:1778-1786. http://dx.doi.org/10.1110/ps.041304505
35. Roestenberg, M., G.A. O'Hara, C.J. Duncan, J.E. Epstein, N.J. Edwards, A. Scholzen, A.J. van der Ven, C.C. Hermsen, A.V. Hill, and R.W. Sauerwein. 2012. Comparison of clinical and parasitological data from controlled human malaria infection trials. PLoS ONE. 7:e38434. http://dx.doi.org/10.1371/journal.pone.0038434
36. Scheid, J.F., H. Mouquet, B. Ueberheide, R. Diskin, F. Klein, T.Y. Oliveira, J. Pietzsch, D. Fenyo, A. Abadir, K. Velinzon, et al. 2011. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science. 333:1633-1637. http://dx.doi.org/10.1126/science.1207227
37. Singh, S., S. Soe, S. Weisman, J.W. Barnwell, J.L. Pérignon, and P. Druilhe. 2009. A conserved multi-gene family induces cross-reactive antibodies effective in defense against Plasmodium falciparum. PLoS ONE. 4:e5410. http://dx.doi.org/10.1371/journal.pone.0005410
38. Smilkstein, M., N. Sriwilaijaroen, J.X. Kelly, P. Wilairat, and M. Riscoe. 2004. Simple and inexpensive fluorescence-based technique for high-throughput antimalarial drug screening. Antimicrob. Agents Chemother. 48:1803- 1806. http://dx.doi.org/10.1128/AAC.48.5.1803-1806.2004
39. Struik, S.S., and E.M. Riley. 2004. Does malaria suffer from lack of memory? Immunol. Rev. 201:268-290. http://dx.doi.org/10.1111/j.0105-2896.2004.00181.x
40. Taylor, R.R., A. Egan, D. McGuinness, A. Jepson, R. Adair, C. Drakely, and E. Riley. 1996. Selective recognition of malaria antigens by human serum antibodies is not genetically determined but demonstrates some features of clonal imprinting. Int. Immunol. 8:905-915. http://dx.doi.org/10.1093/intimm/8.6.905
41. Theisen, M., S. Soe, K. Brunstedt, F. Follmann, L. Bredmose, H. Israelsen, S.M. Madsen, and P. Druilhe. 2004. A Plasmodium falciparum GLURPMSP3 chimeric protein; expression in Lactococcus lactis, immunogenicity and induction of biologically active antibodies. Vaccine. 22:1188-1198. http://dx.doi.org/10.1016/j.vaccine.2003.09.017
42. Tiller, T., E. Meffre, S. Yurasov, M. Tsuiji, M.C. Nussenzweig, and H. Wardemann. 2008. Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J. Immunol. Methods. 329:112-124. http://dx.doi.org/10.1016/j.jim.2007.09.017
43. Tongren, J.E., C.J. Drakeley, S.L. McDonald, H.G. Reyburn, A. Manjurano, W.M. Nkya, M.M. Lemnge, C.D. Gowda, J.E. Todd, P.H. Corran, and E.M. Riley. 2006. Target antigen, age, and duration of antigen exposure independently regulate immunoglobulin G subclass switching in malaria. Infect. Immun. 74:257-264. http://dx.doi.org/10.1128/IAI.74.1.257-264.2006
44. Wardemann, H., S. Yurasov, A. Schaefer, J.W. Young, E. Meffre, and M.C. Nussenzweig. 2003. Predominant autoantibody production by early human B cell precursors. Science. 301:1374-1377. http://dx.doi.org/10.1126/science.1086907
45. Weiss, G.E., P.D. Crompton, S. Li, L.A. Walsh, S. Moir, B. Traore, K. Kayentao, A. Ongoiba, O.K. Doumbo, and S.K. Pierce. 2009. Atypical memory B cells are greatly expanded in individuals living in a malaria-endemic area. J. Immunol. 183:2176-2182. http://dx.doi.org/10.4049/jimmunol.0901297
46. Weiss, G.E., B. Traore, K. Kayentao, A. Ongoiba, S. Doumbo, D. Doumtabe, Y. Kone, S. Dia, A. Guindo, A. Traore, et al. 2010. The Plasmodium falciparum-specific human memory B cell compartment expands gradually with repeated malaria infections. PLoS Pathog. 6:e1000912. http://dx.doi.org/10.1371/journal.ppat.1000912
47. Weiss, G.E., E.H. Clark, S. Li, B. Traore, K. Kayentao, A. Ongoiba, J.N. Hernandez, O.K. Doumbo, S.K. Pierce, O.H. Branch, and P.D. Crompton. 2011. A positive correlation between atypical memory B cells and Plasmodium falciparum transmission intensity in cross-sectional studies in Peru and Mali. PLoS ONE. 6:e15983. http://dx.doi.org/10.1371/journal.pone.0015983
48. Wipasa, J., C. Suphavilai, L.C. Okell, J. Cook, P.H. Corran, K. Thaikla, W. Liewsaree, E.M. Riley, and J.C. Hafalla. 2010. Long-lived antibody and B Cell memory responses to the human malaria parasites, Plasmodium falciparum and Plasmodium vivax. PLoS Pathog. 6:e1000770. http://dx.doi.org/10.1371/journal.ppat.1000770