The V gene repertoires of classical and atypical memory B cells in malaria-susceptible West African children

Journal of Immunology

Volumn 194, Issue 3, 2015, Pages 929-939

  Zinöcker, Severin ^a   Schindler, Christine E ^a   Skinner, Jeff ^a   Rogosch, Tobias ^b   Waisberg, Michael ^a,c   Schickel, Jean Nicolas ^d   Meffre, Eric ^d   Kayentao, Kassoum ^e   Ongoïba, Aïssata ^e   Traoré, Boubacar ^e   Pierce, Susan K ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c UNIVERSITY OF VIRGINIA   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Sociétés   (Mali)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN J CHAIN; IMMUNOGLOBULIN KAPPA CHAIN; IMMUNOGLOBULIN LAMBDA CHAIN; IMMUNOGLOBULIN LIGHT CHAIN; COMPLEMENTARITY DETERMINING REGION; IMMUNOGLOBULIN VARIABLE REGION; PARASITE ANTIGEN;

ARTICLE; ATYPICAL MEMORY B CELL; CELL SELECTION; CHILD; COMPARATIVE STUDY; D GENE; DNA SEQUENCE; FEMALE; GENE EXPRESSION; GENE FREQUENCY; GENE LOCUS; GENE REARRANGEMENT; GENOTYPE; HUMAN; HUMAN CELL; IMMUNOGLOBULIN VARIABLE REGION; INFECTION RISK; INFECTION SENSITIVITY; J GENE; MALARIA FALCIPARUM; MALE; MEMORY CELL; NUCLEOTIDE SEQUENCE; OBSERVATIONAL STUDY; REPORTER GENE; SEQUENCE ANALYSIS; SINGLE CELL ANALYSIS; SOMATIC HYPERMUTATION; V GENE; WEST AFRICAN; AFRICA; AMINO ACID SEQUENCE; B LYMPHOCYTE; CHEMISTRY; COHORT ANALYSIS; COMPLEMENTARITY DETERMINING REGION; DISEASE PREDISPOSITION; GENETIC VARIATION; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; IMMUNOPHENOTYPING; MALARIA; METABOLISM; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD;

AFRICA, WESTERN; AMINO ACID SEQUENCE; ANTIGENS, PROTOZOAN; B-LYMPHOCYTES; CHILD; CHILD, PRESCHOOL; COHORT STUDIES; COMPLEMENTARITY DETERMINING REGIONS; DISEASE SUSCEPTIBILITY; FEMALE; GENE REARRANGEMENT, B-LYMPHOCYTE; GENETIC VARIATION; HUMANS; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN LIGHT CHAINS; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGIC MEMORY; IMMUNOPHENOTYPING; MALARIA; MALARIA, FALCIPARUM; MALE; PLASMODIUM FALCIPARUM; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN;

EID: 84921461256     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402168     Document Type: Article

References (47)

1. 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.
2. Langhorne, J., F. M. Ndungu, A. M. Sponaas, and K. Marsh. 2008. Immunity to malaria: more questions than answers. Nat. Immunol. 9: 725-732.
3. Crompton, P. D., J. Moebius, S. Portugal, M. Waisberg, G. Hart, L. S. Garver, L. H. Miller, C. Barillas-Mury, and S. K. Pierce. 2014. Malaria immunity in man and mosquito: insights into unsolved mysteries of a deadly infectious disease. Annu. Rev. Immunol. 32: 157-187.
4. Okiro, E. A., A. Al-Taiar, H. Reyburn, R. Idro, J. A. Berkley, and R. W. Snow. 2009. Age patterns of severe paediatric malaria and their relationship to Plasmodium falciparum transmission intensity. Malar. J. 8: 4.
5. Tran, T. M., S. Li, S. Doumbo, D. Doumtabe, C. Y. Huang, S. Dia, A. Bathily, J. Sangala, Y. Kone, A. Traore, et al. 2013. An intensive longitudinal cohort study of Malian children and adults reveals no evidence of acquired immunity to Plasmodium falciparum infection. Clin. Infect. Dis. 57: 40-47.
6. Cohen, S., I. A. McGregor, and S. Carrington. 1961. Gamma-globulin and acquired immunity to human malaria. Nature 192: 733-737.
7. 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.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. Ndungu, F. M., K. Lundblom, J. Rono, J. Illingworth, S. Eriksson, and A. Färnert. 2013. Long-lived Plasmodium falciparum specific memory B cells in naturally exposed Swedish travelers. Eur. J. Immunol. 43: 2919-2929.
14. 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.
15. 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.
16. 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.
17. Doi, H., S. Tanoue, and D. E. Kaplan. 2014. Peripheral CD27-CD21-B-cells represent an exhausted lymphocyte population in hepatitis C cirrhosis. Clin. Immunol. 150: 184-191.
18. Dauby, N., C. Kummert, S. Lecomte, C. Liesnard, M. L. Delforge, C. Donner, and A. Marchant. 2014. Primary human cytomegalovirus infection induces the expansion of virus-specific activated and atypical memory B cells. J. Infect. Dis. 210: 1275-1285.
19. Portugal, S., S. K. Pierce, and P. D. Crompton. 2013. Young lives lost as B cells falter: what we are learning about antibody responses in malaria. J. Immunol. 190: 3039-3046.
20. Muellenbeck, M. F., B. Ueberheide, B. Amulic, A. Epp, D. Fenyo, C. E. Busse, M. Esen, M. Theisen, B. Mordmüller, and H. Wardemann. 2013. Atypical and classical memory B cells produce Plasmodium falciparum neutralizing antibodies. J. Exp. Med. 210: 389-399.
21. Ampomah, P., L. Stevenson, M. F. Ofori, L. Barfod, and L. Hviid. 2014. Kinetics of B cell responses to Plasmodium falciparum erythrocyte membrane protein 1 in Ghanaian women naturally exposed to malaria parasites. J. Immunol. 192: 5236-5244.
22. Illingworth, J., N. S. Butler, S. Roetynck, J. Mwacharo, S. K. Pierce, P. Bejon, P. D. Crompton, K. Marsh, and F. M. Ndungu. 2013. Chronic exposure to Plasmodium falciparum is associated with phenotypic evidence of B and T cell exhaustion. J. Immunol. 190: 1038-1047.
23. 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.
24. Portugal, S., D. Doumtabe, B. Traore, L. H. Miller, M. Troye-Blomberg, O. K. Doumbo, A. Dolo, S. K. Pierce, and P. D. Crompton. 2012. B cell analysis of ethnic groups in Mali with differential susceptibility to malaria. Malar. J. 11: 162-168.
25. Scholzen, A., A. C. Teirlinck, E. M. Bijker, M. Roestenberg, C. C. Hermsen, S. L. Hoffman, and R. W. Sauerwein. 2014. BAFF and BAFF receptor levels correlate with B cell subset activation and redistribution in controlled human malaria infection. J. Immunol. 192: 3719-3729.
26. Ayieko, C, A. C. Maue, W. G. Jura, G. S. Noland, G. Ayodo, R. Rochford, and C. C. John. 2013. Changes in B cell populations and merozoite surface protein-1-specific memory B cell responses after prolonged absence of detectable P. falciparum infection. PLoS One 8: e67230.
27. Crompton, P. D., B. Traore, K. Kayentao, S. Doumbo, A. Ongoiba, S. A. Diakite, M. A. Krause, D. Doumtabe, Y. Kone, G Weiss, et al. 2008. Sickle cell trait is associated with a delayed onset of malaria: implications for time-to-event analysis in clinical studies of malaria. J. Infect. Dis. 198: 1265-1275.
28. 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.
29. Wardemann, H., and J. Kofer. 2013. Expression cloning of human B cell immunoglobulins. Methods Mol. Biol. 971: 93-111.
30. Ewing, B., L. Hillier, M. C. Wendl, and P. Green. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8: 175-185.
31. Rogosch, T, S. Kerzel, K. H. Hoi, Z. Zhang, R. F. Maier, G. C. Ippolito, and M. Zemlin. 2012. Immunoglobulin analysis tool: a novel tool for the analysis of human and mouse heavy and light chain transcripts. Front. Immunol. 3: 176.
32. Lefranc, M. P. 2014. Immunoglobulin and T cell receptor genes: IMGT(®) and the birth and rise of Immunoinformatics. Front. Immunol. 5: 22.
33. Brochet, X., M. P. Lefranc, and V. Giudicelli. 2008. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res. 36: W503-W508.
34. Giudicelli, V., X. Brochet, and M. P. Lefranc. 2011. IMGT/V-QUEST: IMGT standardized analysis of the immunoglobulin (IG) and T cell receptor (TR) nucleotide sequences. Cold Spring Harb. Protoc. 2011: 695-715.
35. Alamyar, E., P. Duroux, M. P. Lefranc, and V. Giudicelli. 2012. IMGT(®) tools for the nucleotide analysis of immunoglobulin (IG) and T cell receptor (TR) V-(D)-J repertoires, polymorphisms, and IG mutations: IMGT/V-QUEST and IMGT/HighV-QUEST for NGS. Methods Mol. Biol. 882: 569-604.
36. Yaari, G., M. Uduman, and S. H. Kleinstein. 2012. Quantifying selection in high-throughput immunoglobulin sequencing data sets. Nucleic Acids Res. 40: e134.
37. Williams, T N., T. W. Mwangi, S. Wambua, N. D. Alexander, M. Kortok, R. W. Snow, and K. Marsh. 2005. Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases. J. Infect. Dis. 192: 178-186.
38. Shannon, C. E. 1997. The mathematical theory of communication. 1963. MD Comput. 14: 306-317.
39. Wu, T. T., G. Johnson, and E. A. Kabat. 1993. Length distribution of CDRH3 in antibodies. Proteins 16: 1-7.
40. Kyte, J., and R. F Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157: 105-132.
41. Kardava, L., S. Moir, N. Shah, W. Wang, R. Wilson, C. M. Buckner, B. H. Santich, L. J. Kim, E. E. Spurlin, A. K. Nelson, et al. 2014. Abnormal B cell memory subsets dominate HIV-specific responses in infected individuals. J. Clin. Invest. 124: 3252-3262.
42. Briney, B. S., J. R. Willis, B. A. McKinney, and J. E. Crowe, Jr. 2012. High-throughput antibody sequencing reveals genetic evidence of global regulation of the naive and memory repertoires that extends across individuals. Genes Immun. 13: 469-473.
43. Mroczek, E. S., G. C. Ippolito, T. Rogosch, K. H. Hoi, T. A. Hwangpo, M. G. Brand, Y Zhuang, C. R. Liu, D. A. Schneider, M. Zemlin, et al. 2014. Differences in the composition of the human antibody repertoire by B cell subsets in the blood. Front. Immunol. 5: 96.
44. Wu, Y C, D. Kipling, H. S. Leong, V. Martin, A. A. Ademokun, and D. K. Dunn-Walters. 2010. High-throughput immunoglobulin repertoire analysis distinguishes between human IgM memory and switched memory B-cell populations. Blood 116: 1070-1078.
45. Tian, C, G. K. Luskin, K. M. Dischert, J. N. Higginbotham, B. E. Shepherd, and J. E. Crowe, Jr. 2007. Evidence for preferential Ig gene usage and differential TdT and exonuclease activities in human naive and memory B cells. Mol. Immunol. 44: 2173-2183.
46. Arnaout, R., W. Lee, P. Cahill, T. Honan, T. Sparrow, M. Weiand, C. Nusbaum, K Rajewsky, and S. B. Koralov. 2011. High-resolution description of antibody heavy-chain repertoires in humans. PLoS One 6: e22365.
47. Boyd, S. D., E. L. Marshall, J. D. Merker, J. M. Maniar, L. N. Zhang, B. Sahaf, C. D. Jones, B. B. Simen, B. Hanczaruk, K. D. Nguyen, et al. 2009. Measurement and clinical monitoring of human lymphocyte clonality by massively parallel VDJ pyrosequencing. Sci. Transl. Med. 1: 12ra23.