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Immunological processes underlying the slow acquisition of humoral immunity to malaria

Published online by Cambridge University Press:  08 January 2016

VICTORIA RYG-CORNEJO ,
ANN LY  and
DIANA S. HANSEN
VICTORIA RYG-CORNEJO
Affiliation:
The Walter and Eliza Hall Institute of Medical Research, 1G Royal Parade, Parkville, Victoria 3052, Australia Department of Medical Biology, The University of Melbourne, Parkville, Victoria 3010, Australia
ANN LY
Affiliation:
The Walter and Eliza Hall Institute of Medical Research, 1G Royal Parade, Parkville, Victoria 3052, Australia Department of Medical Biology, The University of Melbourne, Parkville, Victoria 3010, Australia
DIANA S. HANSEN*
Affiliation:
The Walter and Eliza Hall Institute of Medical Research, 1G Royal Parade, Parkville, Victoria 3052, Australia Department of Medical Biology, The University of Melbourne, Parkville, Victoria 3010, Australia
*
*Corresponding author: The Walter and Eliza Hall Institute of Medical Research, 1G Royal Parade, Parkville, Victoria 3052, Australia. E-mail: [email protected]
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Summary

Malaria is one of the most serious infectious diseases with ~250 million clinical cases annually. Most cases of severe disease are caused by Plasmodium falciparum. The blood stage of Plasmodium parasite is entirely responsible for malaria-associated pathology. Disease syndromes range from fever to more severe complications, including respiratory distress, metabolic acidosis, renal failure, pulmonary oedema and cerebral malaria. The most susceptible population to severe malaria is children under the age of 5, with low levels of immunity. It is only after many years of repeated exposure, that individuals living in endemic areas develop clinical immunity. This form of protection does not result in sterilizing immunity but prevents clinical episodes by substantially reducing parasite burden. Naturally acquired immunity predominantly targets blood-stage parasites and it is known to require antibody responses. A large body of epidemiological evidence suggests that antibodies to Plasmodium antigens are inefficiently generated and rapidly lost in the absence of ongoing exposure, which suggests a defect in the development of B cell immunological memory. This review summarizes the main findings to date contributing to our understanding on cellular processes underlying the slow acquisition of humoral immunity to malaria. Some of the key outstanding questions in the field are discussed.

Keywords

malariahumoral immunityantibodiesB cells
Type
Special Issue Review
Information
Parasitology , Volume 143 , Issue 2: Naturally Acquired Immunity to Malaria , February 2016 , pp. 199 - 207
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Achtman, A. H., Khan, M., MacLennan, I. C. M. and Langhorne, J. (2003). Plasmodium chabaudi chabaudi infection in mice induces strong B cell responses and striking but temporary changes in splenic cell distribution. Journal of Immunology 171, 317–324.CrossRefGoogle Scholar
Akpogheneta, O. J., Duah, N. O., Tetteh, K. K. A., Dunyo, S., Lanar, D. E., Pinder, M. and Conway, D. J. (2008). Duration of naturally acquired antibody responses to blood-stage Plasmodium falciparum is age dependent and antigen specific. Infection and Immunity 76, 1748–1755.CrossRefGoogle ScholarPubMed
Allen, C. D. C., Okada, T., Tang, H. L. and Cyster, J. G. (2007). Imaging of germinal center selection events during affinity maturation. Science 315, 528–531.CrossRefGoogle ScholarPubMed
Amanna, I. J., Carlson, N. E. and Slifka, M. K. (2007). Duration of humoral immunity to common viral and vaccine antigens. New England Journal of Medicine 357, 1903–1915.CrossRefGoogle ScholarPubMed
Ampomah, P., Stevenson, L., Ofori, M. F., Barfod, L. and Hviid, L. (2014 a). B-cell responses to pregnancy-restricted and -unrestricted Plasmodium falciparum erythrocyte membrane protein 1 antigens in Ghanaian women naturally exposed to malaria parasites. Infection and Immunity 82, 1860–1871.CrossRefGoogle ScholarPubMed
Ampomah, P., Stevenson, L., Ofori, M. F., Barfod, L. and Hviid, L. (2014 b). Kinetics of B cell responses to Plasmodium falciparum erythrocyte membrane protein 1 in Ghanaian women naturally exposed to malaria parasites. Journal of Immunology 192, 5236–5244.CrossRefGoogle ScholarPubMed
Ayieko, C., Maue, A. C., Jura, W. G. Z. O., Noland, G. S., Ayodo, G., Rochford, R. and John, C. C. (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.CrossRefGoogle Scholar
Baird, J. K. (1995). Host age as a determinant of naturally acquired immunity to Plasmodium falciparum. Parasitology Today 11, 105–111.CrossRefGoogle ScholarPubMed
Banga, S., Coursen, J. D., Portugal, S., Tran, T. M., Hancox, L., Ongoiba, A., Traore, B., Doumbo, O. K., Huang, C.-Y., Harty, J. T. and Crompton, P. D. (2015). Impact of acute malaria on pre-existing antibodies to viral and vaccine antigens in mice and humans. PLoS ONE 10, e0125090.CrossRefGoogle ScholarPubMed
Beattie, L., Engwerda, C. R., Wykes, M. and Good, M. F. (2006). CD8+ T lymphocyte-mediated loss of marginal metallophilic macrophages following infection with Plasmodium chabaudi chabaudi AS. Journal of Immunology 177, 2518–2526.CrossRefGoogle ScholarPubMed
Beeson, J. G., Mann, E. J., Elliott, S. R., Lema, V. M., Tadesse, E., Molyneux, M. E., Brown, G. V. and Rogerson, S. J. (2004). Antibodies to variant surface antigens of Plasmodium falciparum-infected erythrocytes and adhesion inhibitory antibodies are associated with placental malaria and have overlapping and distinct targets. Journal of Infectious Diseases 189, 540–551.CrossRefGoogle ScholarPubMed
Blackman, M. J., Heidrich, H. G., Donachie, S., McBride, J. S. and Holder, A. A. (1990). A single fragment of a malaria merozoite surface protein remains on the parasite during red cell invasion and is the target of invasion-inhibiting antibodies. Journal of Experimental Medicine 172, 379–382.CrossRefGoogle ScholarPubMed
Bouharoun-Tayoun, H., Oeuvray, C., Lunel, F. and Druilhe, P. (1995). Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages. Journal of Experimental Medicine 182, 409–418.CrossRefGoogle ScholarPubMed
Boyle, M. J., Reiling, L., Feng, G., Langer, C., Osier, F. H., Aspeling-Jones, H., Cheng, Y. S., Stubbs, J., Tetteh, K. K. A., Conway, D. J., McCarthy, J. S., Müller, I., Marsh, K., Anders, R. F. and Beeson, J. G. (2015). Human antibodies fix complement to inhibit Plasmodium falciparum invasion of erythrocytes and are associated with protection against malaria. Immunity 42, 580–590.CrossRefGoogle ScholarPubMed
Butler, N. S., Pewe, L. L., Traore, B., Doumbo, O. K., Tygrett, L. T., Waldschmidt, T. J. and Harty, J. T. (2011). Therapeutic blockade of PD-L1 and LAG-3 rapidly clears established blood-stage Plasmodium infection. Nature Immunology 13, 188–195.CrossRefGoogle ScholarPubMed
Butler, N. S., Moebius, J., Pewe, L. L., Traore, B., Doumbo, O. K., Tygrett, L. T., Waldschmidt, T. J., Crompton, P. D. and Harty, J. T. (2012). Therapeutic blockade of PD-L1 and LAG-3 rapidly clears established blood-stage Plasmodium infection. Nature Immunology 13, 188–195.CrossRefGoogle Scholar
Cadman, E. T., Abdallah, A. Y., Voisine, C., Sponaas, A.-M., Corran, P., Lamb, T., Brown, D., Ndungu, F. and Langhorne, J. (2008). Alterations of splenic architecture in malaria are induced independently of Toll-like receptors 2, 4, and 9 or MyD88 and may affect antibody affinity. Infection and Immunity 76, 3924–3931.CrossRefGoogle ScholarPubMed
Carvalho, L. J. M., Ferreira-da-Cruz, M. F., Daniel-Ribeiro, C. T., Pelajo-Machado, M. and Lenzi, H. L. (2007). Germinal center architecture disturbance during Plasmodium berghei ANKA infection in CBA mice. Malaria Journal 6, 59.CrossRefGoogle ScholarPubMed
Cavanagh, D. R., Elhassan, I. M., Roper, C., Robinson, V. J., Giha, H., Holder, A. A., Hviid, L., Theander, T. G., Arnot, D. E. and McBride, J. S. (1998). A longitudinal study of type-specific antibody responses to Plasmodium falciparum merozoite surface protein-1 in an area of unstable malaria in Sudan. Journal of Immunology 161, 347–359.CrossRefGoogle Scholar
Cavanagh, D. R., Dodoo, D., Hviid, L., Kurtzhals, J. A., Theander, T. G., Akanmori, B. D., Polley, S., Conway, D. J., Koram, K. and McBride, J. S. (2004). Antibodies to the N-terminal block 2 of Plasmodium falciparum merozoite surface protein 1 are associated with protection against clinical malaria. Infection and Immunity 72, 6492–6502.CrossRefGoogle Scholar
Castillo-Méndez, S. I., Zago, C. A., Sardinha, L. R., Freitas do Rosário, A. P.Álvarez, J. M. and D'Império Lima, M. R. (2007). Characterization of the spleen B-cell compartment at the early and late blood-stage Plasmodium chabaudi malaria. Scandinavian Journal of Immunology 66, 309–319.CrossRefGoogle ScholarPubMed
Chiu, C. Y. H., Healer, J., Thompson, J. K., Chen, L., Kaul, A., Savergave, L., Raghuwanshi, A., Suen, C. S. N. L. W., Siba, P. M., Schofield, L., Müeller, I., Cowman, A. F. and Hansen, D. S. (2014). Association of antibodies to Plasmodium falciparum reticulocyte binding protein homolog 5 with protection from clinical malaria. Frontiers in Microbiology 5, 314. doi: 10.3389/fmicb.2014.00314.CrossRefGoogle ScholarPubMed
Chiu, C. Y. H., Hodder, A. N., Lin, C. S., Li Wai Suen, C. S. N., Schofield, L., Siba, P. M., Müeller, I., Cowman, A. F. and Hansen, D. S. (2015). Antibodies to the Plasmodium falciparum proteins MSPDBL1 and MSPDBL2 opsonize merozoites, inhibit parasite growth, and predict protection from clinical malaria. Journal of Infectious Diseases 212, 406–415.CrossRefGoogle Scholar
Clark, E. H., Silva, C. J., Weiss, G. E., Li, S., Padilla, C., Crompton, P. D., Hernandez, J. N. and Branch, O. H. (2012). Plasmodium falciparum malaria in the Peruvian Amazon, a region of low transmission, is associated with immunologic memory. Infection and Immunity 80, 1583–1592.CrossRefGoogle ScholarPubMed
Cohen, S., Carrington, S. and Mcgregor, I. A. (1961). Gamma-globulin and acquired immunity to human malaria. Nature 192, 733.CrossRefGoogle ScholarPubMed
Cowman, A. F. and Crabb, B. S. (2006). Invasion of red blood cells by malaria parasites. Cell 124, 755–766.CrossRefGoogle ScholarPubMed
Craig, A. G., Grau, G. E., Janse, C., Kazura, J. W., Milner, D., Barnwell, J. W., Turner, G., Langhorne, J. and Model, H. R. M. A. (2012). The role of animal models for research on severe malaria. PLoS Pathogens 8, e1002401. doi: 10.1371/journal.ppat.1002401.CrossRefGoogle ScholarPubMed
Crompton, P. D., Kayala, M. A., Traore, B., Kayentao, K., Ongoiba, A., Weiss, G. E., Molina, D. M., Burk, C. R., Waisberg, M., Jasinskas, A., Tan, X., Doumbo, S., Doumtabe, D., Kone, Y., Narum, D. L., Liang, X., Doumbo, O. K., Miller, L. H., Doolan, D. L., Baldi, P., Felgner, P. L. and Pierce, S. K. (2010). A prospective analysis of the Ab response to Plasmodium falciparum before and after a malaria season by protein microarray. Proceedings of the National Academy of Sciences of the United States of America 107, 6958–6963.CrossRefGoogle ScholarPubMed
Crotty, S. (2014). T follicular helper cell differentiation, function, and roles in disease. Immunity 41, 529–542.CrossRefGoogle ScholarPubMed
de Souza, J. B. and Riley, E. M. (2002). Cerebral malaria: the contribution of studies in animal models to our understanding of immunopathogenesis. Microbes and Infection 4, 291–300.CrossRefGoogle ScholarPubMed
Dodoo, D., Staalsoe, T., Giha, H., Kurtzhals, J. A., Akanmori, B. D., Koram, K., Dunyo, S., Nkrumah, F. K., Hviid, L. and Theander, T. G. (2001). Antibodies to variant antigens on the surfaces of infected erythrocytes are associated with protection from malaria in Ghanaian children. Infection and Immunity 69, 3713–3718.CrossRefGoogle ScholarPubMed
Donati, D., Zhang, L. P., Chêne, A., Chen, Q., Flick, K., Nyström, M., Wahlgren, M. and Bejarano, M. T. (2004). Identification of a polyclonal B-cell activator in Plasmodium falciparum. Infection and Immunity 72, 5412–5418.CrossRefGoogle ScholarPubMed
Donati, D., Mok, B., Chêne, A., Xu, H., Thangarajh, M., Glas, R., Chen, Q., Wahlgren, M. and Bejarano, M. T. (2006). Increased B cell survival and preferential activation of the memory compartment by a malaria polyclonal B cell activator. Journal of Immunology 177, 3035–3044.CrossRefGoogle ScholarPubMed
Fowkes, F. J.I., Richards, J. S., Simpson, J. A. and Beeson, J. G. (2010). The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: a systematic review and meta-analysis. PLoS Medicine 7, e1000218.CrossRefGoogle ScholarPubMed
Good, K. L., Avery, D. T. and Tangye, S. G. (2009). Resting human memory B cells are intrinsically programmed for enhanced survival and responsiveness to diverse stimuli compared to naive B cells. Journal of Immunology 182, 890–901. doi: 10.4049/jimmunol.182.2.890.CrossRefGoogle ScholarPubMed
Gupta, S., Snow, R. W., Donnelly, C. A., Marsh, K. and Newbold, C. (1999). Immunity to non-cerebral severe malaria is acquired after one or two infections. Nature Medicine 5, 340–343.CrossRefGoogle ScholarPubMed
Hammarlund, E., Lewis, M. W., Hansen, S. G., Strelow, L. I., Nelson, J. A., Sexton, G. J., Hanifin, J. M. and Slifka, M. K. (2003). Duration of antiviral immunity after smallpox vaccination. Nature Medicine 9, 1131–1137.CrossRefGoogle ScholarPubMed
Hansen, D. S. (2012). Inflammatory responses associated with the induction of cerebral malaria: lessons from experimental murine models. PLoS Pathogens 8, e1003045.CrossRefGoogle ScholarPubMed
Hill, D. L., Eriksson, E. M., Suen, C. S. N. L. W., Chiu, C. Y., Ryg-Cornejo, V., Robinson, L. J., Siba, P. M., Müeller, I., Hansen, D. S. and Schofield, L. (2013). Opsonising Antibodies to P. falciparum merozoites associated with immunity to clinical malaria. PLoS ONE 8, e74627. doi: 10.1371/journal.pone.0074627.CrossRefGoogle Scholar
Hviid, L., Barfod, L. and Fowkes, F. J. I. (2015). Trying to remember: immunological B cell memory to malaria. Trends in Parasitology 31, 89–94.CrossRefGoogle ScholarPubMed
Illingworth, J., Butler, N. S., Roetynck, S., Mwacharo, J., Pierce, S. K., Bejon, P., Crompton, P. D., Marsh, K. and Ndungu, F. M. (2013). Chronic exposure to Plasmodium falciparum is associated with phenotypic evidence of B and T cell exhaustion. Journal of Immunology 190, 1038–1047.CrossRefGoogle ScholarPubMed
Ismail, H. A., Tijani, M. K., Langer, C., Reiling, L., White, M. T., Beeson, J. G., Wahlgren, M., Nwuba, R. and Persson, K. E. (2014). Subclass responses and their half-lives for antibodies against EBA175 and PfRh2 in naturally acquired immunity against Plasmodium falciparum malaria. Malaria Journal 13, 425.CrossRefGoogle Scholar
Jacob, J., Kassir, R. and KELSOE, G. (1991). In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl) acetyl. I. The architecture and dynamics of responding cell populations. Journal of Experimental Medicine 173, 1165–1175.CrossRefGoogle ScholarPubMed
John, C. C., O'Donnell, R. A., Sumba, P. O., Moormann, A. M., de Koning-Ward, T. F., King, C. L., Kazura, J. W. and Crabb, B. S. (2004). Evidence that invasion-inhibitory antibodies specific for the 19-kDa fragment of merozoite surface protein-1 (MSP-1 19) can play a protective role against blood-stage Plasmodium falciparum infection in individuals in a malaria endemic area of Africa. Journal of Immunology 173, 666–672.CrossRefGoogle Scholar
Kinyanjui, S. M., Bull, P., Newbold, C. I. and Marsh, K. (2003). Kinetics of antibody responses to plasmodium falciparum-infected erythrocyte variant surface antigens. Journal of Infectious Diseases 187, 667–674.CrossRefGoogle ScholarPubMed
Kinyanjui, S. M., Conway, D. J., Lanar, D. E. and Marsh, K. (2007). IgG antibody responses to Plasmodium falciparum merozoite antigens in Kenyan children have a short half-life. Malaria Journal 6, 82.CrossRefGoogle ScholarPubMed
Langhorne, J., Ndungu, F. M., Sponaas, A.-M. and Marsh, K. (2008). Immunity to malaria: more questions than answers. Nature Immunology 9, 725–732.CrossRefGoogle ScholarPubMed
Liu, Y. J., Zhang, J., Lane, P. J., Chan, E. Y. and MacLennan, I. C. (1991). Sites of specific B cell activation in primary and secondary responses to T cell-dependent and T cell-independent antigens. European Journal of Immunology 21, 2951–2962.CrossRefGoogle Scholar
Maple, P. A., Jones, C. S., Wall, E. C., Vyseb, A., Edmunds, W. J., Andrews, N. J. and Miller, E. (2000). Immunity to diphtheria and tetanus in England and Wales. Vaccine 19, 167–173.CrossRefGoogle ScholarPubMed
Marsh, K. and Kinyanjui, S. (2006). Immune effector mechanisms in malaria. Parasite Immunology 28, 51–60.CrossRefGoogle ScholarPubMed
Marsh, K., Otoo, L., Hayes, R. J., Carson, D. C. and Greenwood, B. M. (1989). Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 293–303.CrossRefGoogle ScholarPubMed
McGregor, I. A., Carrington, S. P. and Cohen, S. (1963). Treatment of East African P. falciparum malaria with West African human γ-globulin. Transactions of the Royal Society of Tropical Medicine and Hygiene 57, 170–175.CrossRefGoogle Scholar
Mebius, R. E. and Kraal, G. (2005). Structure and function of the spleen. Nature Reviews Immunology 5, 606–616.CrossRefGoogle ScholarPubMed
Migot, F., Chougnet, C., Henzel, D., Dubois, B., Jambou, R., Fievet, N. and Deloron, P. (1995). Anti-malaria antibody-producing B cell frequencies in adults after a Plasmodium falciparum outbreak in Madagascar. Clinical and Experimental Immunology 102, 529–534.CrossRefGoogle ScholarPubMed
Miller, L. H., Baruch, D. I., Marsh, K. and Doumbo, O. K. (2002). The pathogenic basis of malaria. Nature 415, 673–679.CrossRefGoogle ScholarPubMed
Millington, O. R., Di Lorenzo, C., Phillips, R. S., Garside, P. and Brewer, J. M. (2006). Suppression of adaptive immunity to heterologous antigens during Plasmodium infection through hemozoin-induced failure of dendritic cell function. Journal of Biology 5, 5.CrossRefGoogle ScholarPubMed
Moir, S., Ho, J., Malaspina, A., Wang, W., DiPoto, A. C., O'Shea, M. A., Roby, G., Kottilil, S., Arthos, J., Proschan, M. A., Chun, T. W. and Fauci, A. S. (2008). Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. Journal of Experimental Medicine 205, 1797–1805.CrossRefGoogle Scholar
Morell, A., Terry, W. D. and Waldmann, T. A. (1970). Metabolic properties of IgG subclasses in man. Journal of Clinical Investigation 49, 673–680.CrossRefGoogle ScholarPubMed
Muellenbeck, M. F., Ueberheide, B., Amulic, B., Epp, A., Fenyo, D., Busse, C. E., Esen, M., Theisen, M., Mordmuller, B. and Wardemann, H. (2013). Atypical and classical memory B cells produce Plasmodium falciparum neutralizing antibodies. Journal of Experimental Medicine 210, 389–399.CrossRefGoogle ScholarPubMed
Mueller, S. N. and Germain, R. N. (2009). Stromal cell contributions to the homeostasis and functionality of the immune system. Nature Reviews Immunology 9, 618–629. doi: 10.1038/nri2588.CrossRefGoogle Scholar
Nduati, E., Gwela, A., Karanja, H., Mugyenyi, C., Langhorne, J., Marsh, K. and Urban, B. C. (2011). The plasma concentration of the B cell activating factor is increased in children with acute malaria. Journal of Infectious Diseases 204, 962–970.CrossRefGoogle Scholar
Ndungu, F. M., Cadman, E. T., Coulcher, J., Nduati, E., Couper, E., Macdonald, D. W., Ng, D. and Langhorne, J. (2009). Functional memory B cells and long-lived plasma cells are generated after a single Plasmodium chabaudi infection in mice. PLoS Pathogens 5, e1000690.CrossRefGoogle ScholarPubMed
Ndungu, F. M., Olotu, A., Mwacharo, J., Nyonda, M., Apfeld, J., Mramba, L. K., Fegan, G. W., Bejon, P. and Marsh, K. (2012). Memory B cells are a more reliable archive for historical antimalarial responses than plasma antibodies in no-longer exposed children. Proceedings of the National Academy of Sciences of the United States of America 109, 8247–8252.CrossRefGoogle ScholarPubMed
Ndungu, F. M., Lundblom, K., Rono, J., Illingworth, J., Eriksson, S. and Färnert, A. (2013). Long-lived Plasmodium falciparum specific memory B cells in naturally exposed Swedish travelers. European Journal of Immunology 43, 2919–2929.CrossRefGoogle ScholarPubMed
Nogaro, S. I., Hafalla, J. C., Walther, B., Remarque, E. J., Tetteh, K. K., Conway, D. J., Riley, E. M. and Walther, M. (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.CrossRefGoogle ScholarPubMed
Obeng-Adjei, N., Portugal, S., Tran, T. M., Yazew, T. B., Skinner, J., Li, S., Jain, A., Felgner, P. L., Doumbo, O. K., Kayentao, K., Ongoiba, A., Traore, B. and Crompton, P. D. (2015). Circulating Th1-cell-type Tfh cells that exhibit impaired B cell help are preferentially activated during acute malaria in children. Cell Reports 13, 425–439. doi: 10.1016/j.celrep.2015.09.004.CrossRefGoogle ScholarPubMed
Osier, F. H., Feng, G., Boyle, M. J., Langer, C., Zhou, J., Richards, J. S., McCallum, F. J., Reiling, L., Jaworowski, A., Anders, R. F., Marsh, K. and Beeson, J. G. (2014). Opsonic phagocytosis of Plasmodium falciparum merozoites: mechanism in human immunity and a correlate of protection against malaria. BMC Medicine 12, 108. doi: 10.1186/1741-7015-12-108.CrossRefGoogle Scholar
Pérez-Mazliah, D., Ng, D. H. L., Freitas do Rosário, A. P., McLaughlin, S., Mastelic-Gavillet, B., Sodenkamp, J., Kushinga, G. and Langhorne, J. (2015). Disruption of IL-21 signaling affects T cell-B cell interactions and abrogates protective humoral immunity to malaria. PLoS Pathogens 11, e1004715.CrossRefGoogle ScholarPubMed
Persson, K. E. M., Fowkes, F. J. I., McCallum, F. J., Gicheru, N., Reiling, L., Richards, J. S., Wilson, D. W., Lopaticki, S., Cowman, A. F., Marsh, K. and Beeson, J. G. (2013). Erythrocyte-binding antigens of Plasmodium falciparum are targets of human inhibitory antibodies and function to evade naturally acquired immunity. Journal of Immunology 191, 785–794.CrossRefGoogle ScholarPubMed
Portugal, S., Doumtabe, D., Traore, B., Miller, L. H., Troye-Blomberg, M., Doumbo, O. K., Dolo, A., Pierce, S. K. and Crompton, P. D. (2012). B cell analysis of ethnic groups in Mali with differential susceptibility to malaria. Malaria Journal 11, 162. doi: 10.1186/1475-2875-11-162.CrossRefGoogle ScholarPubMed
Portugal, S., Moebius, J., Skinner, J., Doumbo, S., Doumtabe, D., Kone, Y., Dia, S., Kanakabandi, K., Sturdevant, D. E., Virtaneva, K., Porcella, S. F., Li, S., Doumbo, O. K., Kayentao, K., Ongoiba, A., Traore, B. and Crompton, P. D. (2014). Exposure-dependent control of malaria-induced inflammation in children. PLoS Pathogens 10, e1004079.CrossRefGoogle ScholarPubMed
Portugal, S., Tipton, C. M., Sohn, H., Kone, Y., Wang, J., Li, S., Skinner, J., Virtaneva, K., Sturdevant, D. E., Porcella, S. F., Doumbo, O. K., Doumbo, S., Kayentao, K., Ongoiba, A., Traore, B., Sanz, I., Pierce, S. K. and Crompton, P. D. (2015). Malaria-associated atypical memory B cells exhibit markedly reduced B cell receptor signaling and effector function. eLife 4, e07218. doi: 10.7554/eLife.07218.CrossRefGoogle ScholarPubMed
Radbruch, A., Muehlinghaus, G., Luger, E. O., Inamine, A., Smith, K. G. C., Dörner, T. and Hiepe, F. (2006). Competence and competition: the challenge of becoming a long-lived plasma cell. Nature Reviews Immunology 6, 741–750. doi: 10.1038/nri1886.CrossRefGoogle ScholarPubMed
Richards, J. S., Stanisic, D. I., Fowkes, F. J. I., Tavul, L., Dabod, E., Thompson, J. K., Kumar, S., Chitnis, C. E., Narum, D. L., Michon, P., Siba, P. M., Cowman, A. F., Müeller, I. and Beeson, J. G. (2010). Association between naturally acquired antibodies to erythrocyte-binding antigens of Plasmodium falciparum and protection from malaria and high-density parasitemia. Clinical Infectious Diseases 51, e50–e60.CrossRefGoogle ScholarPubMed
Richards, J. S., Arumugam, T. U., Reiling, L., Healer, J., Hodder, A. N., Fowkes, F. J. I., Cross, N., Langer, C., Takeo, S., Uboldi, A. D., Thompson, J. K., Gilson, P. R., Coppel, R. L., Siba, P. M., King, C. L., Torii, M., Chitnis, C. E., Narum, D. L., Müeller, I., Crabb, B. S., Cowman, A. F., Tsuboi, T. and Beeson, J. G. (2013). Identification and prioritization of merozoite antigens as targets of protective human immunity to Plasmodium falciparum malaria for vaccine and biomarker development. Journal of Immunology 191, 795–809.CrossRefGoogle ScholarPubMed
Ryg-Cornejo, V., Ioannidis, L. J., Ly, A., Chiu, C. Y., Tellier, J., Hill, D. L., Preston, S. P., Pellegrini, M., Yu, D., Nutt, S. L., Kallies, A. and Hansen, D. S. (2016) Severe malaria infections impair germinal centre responses by inhibiting T follicular helper cell differentiation. Cell Reports 14, 1–14.CrossRefGoogle ScholarPubMed
Scherf, A., Lopez-Rubio, J. J. and Riviere, L. (2008). Antigenic variation in Plasmodium falciparum. Annual Review of Microbiology 62, 445–470.CrossRefGoogle ScholarPubMed
Schofield, L. (2007). Intravascular infiltrates and organ-specific inflammation in malaria pathogenesis. Immunology and Cell Biology 85, 130–137.CrossRefGoogle ScholarPubMed
Schofield, L. and Grau, G. E. (2005). Immunological processes in malaria pathogenesis. Nature Reviews Immunology 5, 722–735.CrossRefGoogle ScholarPubMed
Scholzen, A., Teirlinck, A. C., Bijker, E. M., Roestenberg, M., Hermsen, C. C., Hoffman, S. L. and Sauerwein, R. W. (2014). BAFF and BAFF receptor levels correlate with B cell subset activation and redistribution in controlled human malaria infection. Journal of Immunology 192, 3719–3729.CrossRefGoogle ScholarPubMed
Smith, K. G., Hewitson, T. D., Nossal, G. J. and Tarlinton, D. M. (1996). The phenotype and fate of the antibody-forming cells of the splenic foci. European Journal of Immunology 26, 444–448.CrossRefGoogle ScholarPubMed
Stephens, R., Ndungu, F. M. and Langhorne, J. (2009). Germinal centre and marginal zone B cells expand quickly in a second Plasmodium chabaudi malaria infection producing mature plasma cells. Parasite Immunology 31, 20–31.CrossRefGoogle Scholar
Stephens, R., Culleton, R. L. and Lamb, T. J. (2012). The contribution of Plasmodium chabaudi to our understanding of malaria. Trends in Parasitology 28, 73–82.CrossRefGoogle ScholarPubMed
Stevenson, M. M. and Kraal, G. (1989). Histological-changes in the spleen and liver of C57bl/6 and a/J mice during Plasmodium-Chabaudi as infection. Experimental and Molecular Pathology 51, 80–95.CrossRefGoogle Scholar
Tongren, J. E., Drakeley, C. J., McDonald, S. L., Reyburn, H. G., Manjurano, A., Nkya, W. M., Lemnge, M. M., Gowda, C. D., Todd, J. E., Corran, P. H. and Riley, E. M. (2006). Target antigen, age, and duration of antigen exposure independently regulate immunoglobulin G subclass switching in malaria. Infection and Immunity 74, 257–264.CrossRefGoogle ScholarPubMed
Urban, B. C., Hien, T. T., Day, N. P., Phu, N. H., Roberts, R., Pongponratn, E., Jones, M., Mai, N. T. H., Bethell, D., Turner, G. D. H., Ferguson, D., White, N. J. and Roberts, D. J. (2005). Fatal Plasmodium falciparum malaria causes specific patterns of splenic architectural disorganization. Infection and Immunity 73, 1986–1994.CrossRefGoogle ScholarPubMed
Victora, G. D., Schwickert, T. A., Fooksman, D. R., Kamphorst, A. O., Meyer-Hermann, M., Dustin, M. L. and Nussenzweig, M. C. (2010). Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell 143, 592–605.CrossRefGoogle ScholarPubMed
Weiss, G. E., Crompton, P. D., Li, S., Walsh, L. A., Moir, S., Traore, B., Kayentao, K., Ongoiba, A., Doumbo, O. K. and Pierce, S. K. (2009). Atypical memory B cells are greatly expanded in individuals living in a malaria-endemic area. Journal of Immunology 183, 2176–2182.CrossRefGoogle Scholar
Weiss, G. E., Traore, B., Kayentao, K., Ongoiba, A., Doumbo, S., Doumtabe, D., Kone, Y., Dia, S., Guindo, A., Traore, A., Huang, C. Y., Miura, K., Mircetic, M., Li, S., Baughman, A., Narum, D. L., Miller, L. H., Doumbo, O. K., Pierce, S. K. and Crompton, P. D. (2010). The Plasmodium falciparum-specific human memory B cell compartment expands gradually with repeated malaria infections. PLoS Pathogens 6, e1000912.CrossRefGoogle ScholarPubMed
Weiss, G. E., Clark, E. H., Li, S., Traore, B., Kayentao, K., Ongoiba, A., Hernandez, J. N., Doumbo, O. K., Pierce, S. K., Branch, O. H. and Crompton, P. D. (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.CrossRefGoogle ScholarPubMed
White, M. T., Griffin, J. T., Akpogheneta, O., Conway, D. J., Koram, K. A., Riley, E. M. and Ghani, A. C. (2014 a). Dynamics of the antibody response to Plasmodium falciparum infection in African children. Journal of Infectious Diseases 210, 1115–1122.CrossRefGoogle ScholarPubMed
White, N. J., Pukrittayakamee, S., Hien, T. T., Faiz, M. A., Mokuolu, O. A. and Dondorp, A. M. (2014 b). Malaria. Lancet 383, 723–735.CrossRefGoogle ScholarPubMed
Wilmore, J. R., Maue, A. C., Lefebvre, J. S., Haynes, L. and Rochford, R. (2013). Acute Plasmodium chabaudi infection dampens humoral responses to a secondary T-dependent antigen but enhances responses to a secondary T-independent antigen. Journal of Immunology 191, 4731–4739.CrossRefGoogle ScholarPubMed
Wipasa, J., Suphavilai, C., Okell, L. C., Cook, J., Corran, P. H., Thaikla, K., Liewsaree, W., Riley, E. M. and Hafalla, J. C. (2010). Long-lived antibody and B cell memory responses to the human malaria parasites, Plasmodium falciparum and Plasmodium vivax. PLoS Pathogens 6, e1000770.CrossRefGoogle Scholar
World Health Organization (2014). World Malaria Report 2014. World Health Organisation, Geneva, Switzerland.Google Scholar
Zander, R. A., Obeng-Adjei, N., Guthmiller, J. J., Kulu, D. I., Li, J., Ongoiba, A., Traore, B., Crompton, P. D. and Butler, N. S. (2015). PD-1 co-inhibitory and OX40 co-stimulatory crosstalk regulates helper T cell differentiation and anti-plasmodium humoral immunity. Cell Host and Microbe 17, 628–641.CrossRefGoogle ScholarPubMed
Zinöcker, S., Schindler, C. E., Skinner, J., Rogosch, T., Waisberg, M., Schickel, J.-N., Meffre, E., Kayentao, K., Ongoiba, A., Traore, B. and Pierce, S. K. (2015). The V gene repertoires of classical and atypical memory B cells in malaria-susceptible West African children. Journal of Immunology 194, 929–939.CrossRefGoogle Scholar