Skip to main content
Top
Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

B cell sub-types following acute malaria and associations with clinical immunity

Authors: Richard T. Sullivan, Isaac Ssewanyana, Samuel Wamala, Felistas Nankya, Prasanna Jagannathan, Jordan W. Tappero, Harriet Mayanja-Kizza, Mary K. Muhindo, Emmanuel Arinaitwe, Moses Kamya, Grant Dorsey, Margaret E. Feeney, Eleanor M. Riley, Chris J. Drakeley, Bryan Greenhouse

Published in: Malaria Journal | Issue 1/2016

Login to get access

Abstract

Background

Repeated exposure to Plasmodium falciparum is associated with perturbations in B cell sub-set homeostasis, including expansion atypical memory B cells. However, B cell perturbations immediately following acute malaria infection have been poorly characterized, especially with regard to their relationship with immunity to malaria.

Methods

To better understand the kinetics of B cell sub-sets following malaria, the proportions of six B cell sub-sets were assessed at five time points following acute malaria in four to 5 years old children living in a high transmission region of Uganda. B cell sub-set kinetics were compared with measures of clinical immunity to malaria—lower parasite density at the time of malaria diagnosis and recent asymptomatic parasitaemia.

Results

Atypical memory B cell and transitional B cell proportions increased following malaria. In contrast, plasmablast proportions were highest at the time of malaria diagnosis and rapidly declined following treatment. Increased proportions of atypical memory B cells were associated with greater immunity to malaria, whereas increased proportions of transitional B cells were associated with evidence of less immunity to malaria.

Conclusions

These findings highlight the dynamic changes in multiple B cell sub-sets following acute, uncomplicated malaria, and how these sub-sets are associated with developing immunity to malaria.
Literature
1.
go back to reference WHO. World Malaria Report. World Health Organization: Geneva; 2013. WHO. World Malaria Report. World Health Organization: Geneva; 2013.
2.
go back to reference Beadle C, McElroy PD, Oster CN, Beier JC, Oloo AJ, Onyango FK, et al. Impact of transmission intensity and age on Plasmodium falciparum density and associated fever: implications for malaria vaccine trial design. J Infect Dis. 1995;172:1047–54.CrossRefPubMed Beadle C, McElroy PD, Oster CN, Beier JC, Oloo AJ, Onyango FK, et al. Impact of transmission intensity and age on Plasmodium falciparum density and associated fever: implications for malaria vaccine trial design. J Infect Dis. 1995;172:1047–54.CrossRefPubMed
4.
go back to reference Langhorne J, Ndungu FM, Sponaas A-M, Marsh K. Immunity to malaria: more questions than answers. Nat Immunol. 2008;9:725–32.CrossRefPubMed Langhorne J, Ndungu FM, Sponaas A-M, Marsh K. Immunity to malaria: more questions than answers. Nat Immunol. 2008;9:725–32.CrossRefPubMed
5.
6.
go back to reference King CL, Davies DH, Felgner P, Baum E, Jain A, Randall A, et al. Biosignatures of exposure/transmission and immunity. Am J Trop Med Hyg. 2015;93:15–37.CrossRef King CL, Davies DH, Felgner P, Baum E, Jain A, Randall A, et al. Biosignatures of exposure/transmission and immunity. Am J Trop Med Hyg. 2015;93:15–37.CrossRef
7.
go back to reference Cohen S, McGregor IA, Carrington S. Gamma-globulin and acquired immunity to human malaria. Nature. 1961;192:733–7.CrossRefPubMed Cohen S, McGregor IA, Carrington S. Gamma-globulin and acquired immunity to human malaria. Nature. 1961;192:733–7.CrossRefPubMed
8.
go back to reference Bejon P, Warimwe G, Mackintosh CL, Mackinnon MJ, Kinyanjui SM, Musyoki JN, et al. Analysis of immunity to febrile malaria in children that distinguishes immunity from lack of exposure. Infect Immun. 2009;77:1917–23.CrossRefPubMedPubMedCentral Bejon P, Warimwe G, Mackintosh CL, Mackinnon MJ, Kinyanjui SM, Musyoki JN, et al. Analysis of immunity to febrile malaria in children that distinguishes immunity from lack of exposure. Infect Immun. 2009;77:1917–23.CrossRefPubMedPubMedCentral
9.
go back to reference White MT, Griffin JT, Akpogheneta O, Conway DJ, Koram KA, Riley EM, et al. Dynamics of the antibody response to Plasmodium falciparum infection in African children. J Infect Dis. 2014;210:1115–22.CrossRefPubMed White MT, Griffin JT, Akpogheneta O, Conway DJ, Koram KA, Riley EM, et al. Dynamics of the antibody response to Plasmodium falciparum infection in African children. J Infect Dis. 2014;210:1115–22.CrossRefPubMed
10.
go back to reference Akpogheneta OJ, Duah NO, Tetteh KKA, Dunyo S, Lanar DE, Pinder M, et al. Duration of naturally acquired antibody responses to blood-stage Plasmodium falciparum is age dependent and antigen specific. Infect Immun. 2008;76:1748–55.CrossRefPubMedPubMedCentral Akpogheneta OJ, Duah NO, Tetteh KKA, Dunyo S, Lanar DE, Pinder M, et al. Duration of naturally acquired antibody responses to blood-stage Plasmodium falciparum is age dependent and antigen specific. Infect Immun. 2008;76:1748–55.CrossRefPubMedPubMedCentral
11.
go back to reference Weiss GE, Traore B, Kayentao K, Ongoiba A, Doumbo S, Doumtabe D, et al. The Plasmodium falciparum-specific human memory B cell compartment expands gradually with repeated malaria infections. PLoS Pathog. 2010;6:e1000912.CrossRefPubMedPubMedCentral Weiss GE, Traore B, Kayentao K, Ongoiba A, Doumbo S, Doumtabe D, et al. The Plasmodium falciparum-specific human memory B cell compartment expands gradually with repeated malaria infections. PLoS Pathog. 2010;6:e1000912.CrossRefPubMedPubMedCentral
12.
13.
go back to reference Weiss GE, Crompton PD, Li S, Walsh LA, Moir S, Traore B, et al. Atypical memory B cells are greatly expanded in individuals living in a malaria-endemic area. J Immunol. 2009;183:2176–82.CrossRefPubMedPubMedCentral Weiss GE, Crompton PD, Li S, Walsh LA, Moir S, Traore B, et al. Atypical memory B cells are greatly expanded in individuals living in a malaria-endemic area. J Immunol. 2009;183:2176–82.CrossRefPubMedPubMedCentral
14.
go back to reference Weiss GE, Clark EH, Li S, Traore B, Kayentao K, Ongoiba A, et al. A positive correlation between atypical memory B cells and Plasmodium falciparum transmission intensity in cross-sectional studies in Peru and Mali. PLoS ONE. 2011;6:e15983.CrossRefPubMedPubMedCentral Weiss GE, Clark EH, Li S, Traore B, Kayentao K, Ongoiba A, et al. A positive correlation between atypical memory B cells and Plasmodium falciparum transmission intensity in cross-sectional studies in Peru and Mali. PLoS ONE. 2011;6:e15983.CrossRefPubMedPubMedCentral
15.
go back to reference Illingworth J, Butler NS, Roetynck S, Mwacharo J, Pierce SK, Bejon P, et al. Chronic exposure to Plasmodium falciparum is associated with phenotypic evidence of B and T cell exhaustion. J Immunol. 2013;190:1038–47.CrossRefPubMedPubMedCentral Illingworth J, Butler NS, Roetynck S, Mwacharo J, Pierce SK, Bejon P, et al. Chronic exposure to Plasmodium falciparum is associated with phenotypic evidence of B and T cell exhaustion. J Immunol. 2013;190:1038–47.CrossRefPubMedPubMedCentral
16.
go back to reference Simone O, Bejarano MT, Pierce SK, Antonaci S, Wahlgren M, Troye-Blomberg M, et al. TLRs innate immunereceptors and Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) CIDR1-driven human polyclonal B-cell activation. Acta Trop. 2011;119:144–50.CrossRefPubMedPubMedCentral Simone O, Bejarano MT, Pierce SK, Antonaci S, Wahlgren M, Troye-Blomberg M, et al. TLRs innate immunereceptors and Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) CIDR1-driven human polyclonal B-cell activation. Acta Trop. 2011;119:144–50.CrossRefPubMedPubMedCentral
17.
go back to reference Donati D, Zhang LP, Chen Q, Chene A, Flick K, Nystrom M, et al. Identification of a polyclonal B-cell activator in Plasmodium falciparum. Infect Immun. 2004;72:5412–8.CrossRefPubMedPubMedCentral Donati D, Zhang LP, Chen Q, Chene A, Flick K, Nystrom M, et al. Identification of a polyclonal B-cell activator in Plasmodium falciparum. Infect Immun. 2004;72:5412–8.CrossRefPubMedPubMedCentral
18.
go back to reference Perez-Andres M, Paiva B, Nieto WG, Caraux A, Schmitz A, Almeida J, et al. Human peripheral blood B-cell compartments: a crossroad in B-cell traffic. Cytometry B Clin Cytom. 2010;78B:S47–60.CrossRef Perez-Andres M, Paiva B, Nieto WG, Caraux A, Schmitz A, Almeida J, et al. Human peripheral blood B-cell compartments: a crossroad in B-cell traffic. Cytometry B Clin Cytom. 2010;78B:S47–60.CrossRef
19.
go back to reference Asito AS, Moormann AM, Kiprotich C, Ng’ang’a ZW, Ploutz-Snyder R, Rochford R. Alterations on peripheral B cell subsets following an acute uncomplicated clinical malaria infection in children. Malar J. 2008;7:238.CrossRefPubMedPubMedCentral Asito AS, Moormann AM, Kiprotich C, Ng’ang’a ZW, Ploutz-Snyder R, Rochford R. Alterations on peripheral B cell subsets following an acute uncomplicated clinical malaria infection in children. Malar J. 2008;7:238.CrossRefPubMedPubMedCentral
20.
go back to reference Sullivan RT, Kim CC, Fontana MF, Feeney ME, Jagannathan P, Boyle MJ, et al. FCRL5 delineates functionally impaired memory B cells associated with Plasmodium falciparum exposure. PLoS Pathog. 2015;11:e1004894.CrossRefPubMedPubMedCentral Sullivan RT, Kim CC, Fontana MF, Feeney ME, Jagannathan P, Boyle MJ, et al. FCRL5 delineates functionally impaired memory B cells associated with Plasmodium falciparum exposure. PLoS Pathog. 2015;11:e1004894.CrossRefPubMedPubMedCentral
21.
go back to reference Portugal S, Tipton CM, Sohn H, Kone Y, Wang J, Li S, et al. Malaria-associated atypical memory B cells exhibit markedly reduced B cell receptor signaling and effector function. ELife. 2015;4:e07218.CrossRef Portugal S, Tipton CM, Sohn H, Kone Y, Wang J, Li S, et al. Malaria-associated atypical memory B cells exhibit markedly reduced B cell receptor signaling and effector function. ELife. 2015;4:e07218.CrossRef
22.
go back to reference Muellenbeck MF, Ueberheide B, Amulic B, Epp A, Fenyo D, Busse CE, et al. Atypical and classical memory B cells produce Plasmodium falciparum neutralizing antibodies. J Exp Med. 2013;210:389–99.CrossRefPubMedPubMedCentral Muellenbeck MF, Ueberheide B, Amulic B, Epp A, Fenyo D, Busse CE, et al. Atypical and classical memory B cells produce Plasmodium falciparum neutralizing antibodies. J Exp Med. 2013;210:389–99.CrossRefPubMedPubMedCentral
23.
go back to reference Nogaro SI, Hafalla JC, Walther B, Remarque EJ, Tetteh KKA, Conway DJ, et al. 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. 2011;6:e25582.CrossRefPubMedPubMedCentral Nogaro SI, Hafalla JC, Walther B, Remarque EJ, Tetteh KKA, Conway DJ, et al. 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. 2011;6:e25582.CrossRefPubMedPubMedCentral
24.
go back to reference Ladeia-Andrade S, Ferreira MU, de Carvalho ME, Curado I, Coura JR. Age-dependent acquisition of protective immunity to malaria in riverine populations of the Amazon basin of Brazil. Am J Trop Med Hyg. 2009;80:452–9.PubMed Ladeia-Andrade S, Ferreira MU, de Carvalho ME, Curado I, Coura JR. Age-dependent acquisition of protective immunity to malaria in riverine populations of the Amazon basin of Brazil. Am J Trop Med Hyg. 2009;80:452–9.PubMed
25.
go back to reference Ampomah P, Stevenson L, Ofori MF, Barfod L, Hviid L. Kinetics of B cell responses to Plasmodium falciparum erythrocyte membrane protein 1 in Ghanaian women naturally exposed to malaria parasites. J Immunol. 2014;192:5236–44.CrossRefPubMedPubMedCentral Ampomah P, Stevenson L, Ofori MF, Barfod L, Hviid L. Kinetics of B cell responses to Plasmodium falciparum erythrocyte membrane protein 1 in Ghanaian women naturally exposed to malaria parasites. J Immunol. 2014;192:5236–44.CrossRefPubMedPubMedCentral
26.
go back to reference Nduati EW, Ng DHL, Ndungu FM, Gardner P, Urban BC, Langhorne J. Distinct kinetics of memory B-cell and plasma-cell responses in peripheral blood following a blood-stage Plasmodium chabaudi infection in mice. PLoS ONE. 2010;5:e15007.CrossRefPubMedPubMedCentral Nduati EW, Ng DHL, Ndungu FM, Gardner P, Urban BC, Langhorne J. Distinct kinetics of memory B-cell and plasma-cell responses in peripheral blood following a blood-stage Plasmodium chabaudi infection in mice. PLoS ONE. 2010;5:e15007.CrossRefPubMedPubMedCentral
27.
go back to reference Kilama M, Smith DL, Hutchinson R, Kigozi R, Yeka A, Lavoy G, et al. Estimating the annual entomological inoculation rate for Plasmodium falciparum transmitted by Anopheles gambiae s.l. using three sampling methods in three sites in Uganda. Malar J. 2014;13:111.CrossRefPubMedPubMedCentral Kilama M, Smith DL, Hutchinson R, Kigozi R, Yeka A, Lavoy G, et al. Estimating the annual entomological inoculation rate for Plasmodium falciparum transmitted by Anopheles gambiae s.l. using three sampling methods in three sites in Uganda. Malar J. 2014;13:111.CrossRefPubMedPubMedCentral
28.
go back to reference Jagannathan P, Muhindo MK, Kakuru A, Arinaitwe E, Greenhouse B, Tappero J, et al. Increasing incidence of malaria in children despite insecticide-treated bed nets and prompt anti-malarial therapy in Tororo, Uganda. Malar J. 2012;11:435.CrossRefPubMedPubMedCentral Jagannathan P, Muhindo MK, Kakuru A, Arinaitwe E, Greenhouse B, Tappero J, et al. Increasing incidence of malaria in children despite insecticide-treated bed nets and prompt anti-malarial therapy in Tororo, Uganda. Malar J. 2012;11:435.CrossRefPubMedPubMedCentral
29.
go back to reference Katrak S, Gasasira A, Arinaitwe E, Kakuru A, Wanzira H, Bigira V, et al. Safety and tolerability of artemether-lumefantrine versus dihydroartemisinin-piperaquine for malaria in young HIV-infected and uninfected children. Malar J. 2009;8:272.CrossRefPubMedPubMedCentral Katrak S, Gasasira A, Arinaitwe E, Kakuru A, Wanzira H, Bigira V, et al. Safety and tolerability of artemether-lumefantrine versus dihydroartemisinin-piperaquine for malaria in young HIV-infected and uninfected children. Malar J. 2009;8:272.CrossRefPubMedPubMedCentral
30.
go back to reference Arinaitwe E, Sandison TG, Wanzira H, Kakuru A, Homsy J, Kalamya J, et al. Artemether-lumefantrine versus dihydroartemisinin-piperaquine for falciparum malaria: a longitudinal, randomized trial in young Ugandan children. Clin Infect Dis. 2009;49:1629–37.CrossRefPubMed Arinaitwe E, Sandison TG, Wanzira H, Kakuru A, Homsy J, Kalamya J, et al. Artemether-lumefantrine versus dihydroartemisinin-piperaquine for falciparum malaria: a longitudinal, randomized trial in young Ugandan children. Clin Infect Dis. 2009;49:1629–37.CrossRefPubMed
31.
go back to reference Colonna-Romano G, Bulati M, Aquino A, Pellicanò M, Vitello S, Lio D, et al. A double-negative (IgD−CD27−) B cell population is increased in the peripheral blood of elderly people. Mech Ageing Dev. 2009;130:681–90.CrossRefPubMed Colonna-Romano G, Bulati M, Aquino A, Pellicanò M, Vitello S, Lio D, et al. A double-negative (IgD−CD27−) B cell population is increased in the peripheral blood of elderly people. Mech Ageing Dev. 2009;130:681–90.CrossRefPubMed
33.
go back to reference Wei C, Anolik J, Cappione A, Zheng B, Pugh-Bernard A, Brooks J, et al. A new population of cells lacking expression of CD27 represents a notable component of the B cell memory compartment in systemic lupus erythematosus. J Immunol. 1950;2007(178):6624–33. Wei C, Anolik J, Cappione A, Zheng B, Pugh-Bernard A, Brooks J, et al. A new population of cells lacking expression of CD27 represents a notable component of the B cell memory compartment in systemic lupus erythematosus. J Immunol. 1950;2007(178):6624–33.
34.
go back to reference Jacobi AM, Reiter K, Mackay M, Aranow C, Hiepe F, Radbruch A, et al. Activated memory B cell subsets correlate with disease activity in systemic lupus erythematosus: delineation by expression of CD27, IgD, and CD95. Arthritis Rheum. 2008;58:1762–73.CrossRefPubMed Jacobi AM, Reiter K, Mackay M, Aranow C, Hiepe F, Radbruch A, et al. Activated memory B cell subsets correlate with disease activity in systemic lupus erythematosus: delineation by expression of CD27, IgD, and CD95. Arthritis Rheum. 2008;58:1762–73.CrossRefPubMed
35.
go back to reference Ehrhardt GRA, Hijikata A, Kitamura H, Ohara O, Wang J-Y, Cooper MD. Discriminating gene expression profiles of memory B cell subpopulations. J Exp Med. 2008;205:1807–17.CrossRefPubMedPubMedCentral Ehrhardt GRA, Hijikata A, Kitamura H, Ohara O, Wang J-Y, Cooper MD. Discriminating gene expression profiles of memory B cell subpopulations. J Exp Med. 2008;205:1807–17.CrossRefPubMedPubMedCentral
36.
go back to reference Ehrhardt GRA, Hsu JT, Gartland L, Leu C-M, Zhang S, Davis RS, et al. Expression of the immunoregulatory molecule FcRH4 defines a distinctive tissue-based population of memory B cells. J Exp Med. 2005;202:783–91.CrossRefPubMedPubMedCentral Ehrhardt GRA, Hsu JT, Gartland L, Leu C-M, Zhang S, Davis RS, et al. Expression of the immunoregulatory molecule FcRH4 defines a distinctive tissue-based population of memory B cells. J Exp Med. 2005;202:783–91.CrossRefPubMedPubMedCentral
37.
go back to reference Zeger SL, Liang K-Y. Longitudinal data analysis for discrete and continuous outcomes. Biometrics. 1986;42:121–30.CrossRefPubMed Zeger SL, Liang K-Y. Longitudinal data analysis for discrete and continuous outcomes. Biometrics. 1986;42:121–30.CrossRefPubMed
38.
go back to reference Owusu-Agyei S, Koram KA, Baird JK, Utz GC, Binka FN, Nkrumah FK, et al. Incidence of symptomatic and asymptomatic Plasmodium falciparum infection following curative therapy in adult residents of northern Ghana. Am J Trop Med Hyg. 2001;65:197–203.PubMed Owusu-Agyei S, Koram KA, Baird JK, Utz GC, Binka FN, Nkrumah FK, et al. Incidence of symptomatic and asymptomatic Plasmodium falciparum infection following curative therapy in adult residents of northern Ghana. Am J Trop Med Hyg. 2001;65:197–203.PubMed
39.
go back to reference Whittle HC, Brown J, Marsh K, Blackman M, Jobe O, Shenton F. The effects of Plasmodium falciparum malaria on immune control of B lymphocytes in Gambian children. Clin Exp Immunol. 1990;80:213–8.CrossRefPubMedPubMedCentral Whittle HC, Brown J, Marsh K, Blackman M, Jobe O, Shenton F. The effects of Plasmodium falciparum malaria on immune control of B lymphocytes in Gambian children. Clin Exp Immunol. 1990;80:213–8.CrossRefPubMedPubMedCentral
40.
go back to reference Bockstal V, Geurts N, Magez S. Acute disruption of bone marrow B lymphopoiesis and apoptosis of transitional and marginal zone B cells in the spleen following a blood-stage Plasmodium chabaudi infection in mice. J Parasitol Res. 2011;2011:534697.CrossRefPubMedPubMedCentral Bockstal V, Geurts N, Magez S. Acute disruption of bone marrow B lymphopoiesis and apoptosis of transitional and marginal zone B cells in the spleen following a blood-stage Plasmodium chabaudi infection in mice. J Parasitol Res. 2011;2011:534697.CrossRefPubMedPubMedCentral
41.
go back to reference van der Vlugt LEPM, Zinsou JF, Ozir-Fazalalikhan A, Kremsner PG, Yazdanbakhsh M, Adegnika AA, et al. Interleukin 10 (IL-10)-producing CD1dhi regulatory B cells from Schistosoma haematobium-infected individuals induce IL-10-positive T cells and suppress effector T-cell cytokines. J Infect Dis. 2014;210:1207–16.CrossRefPubMed van der Vlugt LEPM, Zinsou JF, Ozir-Fazalalikhan A, Kremsner PG, Yazdanbakhsh M, Adegnika AA, et al. Interleukin 10 (IL-10)-producing CD1dhi regulatory B cells from Schistosoma haematobium-infected individuals induce IL-10-positive T cells and suppress effector T-cell cytokines. J Infect Dis. 2014;210:1207–16.CrossRefPubMed
42.
go back to reference Jagannathan P, Eccles-James I, Bowen K, Nankya F, Auma A, Wamala S, et al. IFNγ/IL-10 co-producing cells dominate the CD4 response to malaria in highly exposed children. PLoS Pathog. 2014;10:e1003864.CrossRefPubMedPubMedCentral Jagannathan P, Eccles-James I, Bowen K, Nankya F, Auma A, Wamala S, et al. IFNγ/IL-10 co-producing cells dominate the CD4 response to malaria in highly exposed children. PLoS Pathog. 2014;10:e1003864.CrossRefPubMedPubMedCentral
43.
go back to reference Bouaziz J-D, Calbo S, Maho-Vaillant M, Saussine A, Bagot M, Bensussan A, et al. IL-10 produced by activated human B cells regulates CD4(+) T-cell activation in vitro. Eur J Immunol. 2010;40:2686–91.CrossRefPubMed Bouaziz J-D, Calbo S, Maho-Vaillant M, Saussine A, Bagot M, Bensussan A, et al. IL-10 produced by activated human B cells regulates CD4(+) T-cell activation in vitro. Eur J Immunol. 2010;40:2686–91.CrossRefPubMed
44.
go back to reference Blair PA, Noreña LY, Flores-Borja F, Rawlings DJ, Isenberg DA, Ehrenstein MR, et al. CD19+CD24hiCD38hi B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity. 2010;32:129–40.CrossRefPubMed Blair PA, Noreña LY, Flores-Borja F, Rawlings DJ, Isenberg DA, Ehrenstein MR, et al. CD19+CD24hiCD38hi B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity. 2010;32:129–40.CrossRefPubMed
45.
go back to reference Blink EJ, Light A, Kallies A, Nutt SL, Hodgkin PD, Tarlinton DM. Early appearance of germinal center-derived memory B cells and plasma cells in blood after primary immunization. J Exp Med. 2005;201:545–54.CrossRefPubMedPubMedCentral Blink EJ, Light A, Kallies A, Nutt SL, Hodgkin PD, Tarlinton DM. Early appearance of germinal center-derived memory B cells and plasma cells in blood after primary immunization. J Exp Med. 2005;201:545–54.CrossRefPubMedPubMedCentral
46.
go back to reference Blanchard-Rohner G, Pulickal AS, Jol-van der Zijde CM, Snape MD, Pollard AJ. Appearance of peripheral blood plasma cells and memory B cells in a primary and secondary immune response in humans. Blood. 2009;114:4998–5002.CrossRefPubMedPubMedCentral Blanchard-Rohner G, Pulickal AS, Jol-van der Zijde CM, Snape MD, Pollard AJ. Appearance of peripheral blood plasma cells and memory B cells in a primary and secondary immune response in humans. Blood. 2009;114:4998–5002.CrossRefPubMedPubMedCentral
47.
go back to reference Moir S, Ho J, Malaspina A, Wang W, DiPoto AC, O’Shea MA, et al. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J Exp Med. 2008;205:1797–805.CrossRefPubMedPubMedCentral Moir S, Ho J, Malaspina A, Wang W, DiPoto AC, O’Shea MA, et al. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J Exp Med. 2008;205:1797–805.CrossRefPubMedPubMedCentral
Metadata
Title
B cell sub-types following acute malaria and associations with clinical immunity
Authors
Richard T. Sullivan
Isaac Ssewanyana
Samuel Wamala
Felistas Nankya
Prasanna Jagannathan
Jordan W. Tappero
Harriet Mayanja-Kizza
Mary K. Muhindo
Emmanuel Arinaitwe
Moses Kamya
Grant Dorsey
Margaret E. Feeney
Eleanor M. Riley
Chris J. Drakeley
Bryan Greenhouse
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1190-0

Other articles of this Issue 1/2016

Malaria Journal 1/2016 Go to the issue