The effect of declining exposure on T cell-mediated immunity to Plasmodium falciparum - an epidemiological "natural experiment"

BMC Medicine

Volumn 14, Issue 1, 2016, Pages

  Bediako, Yaw ^a,c   Ngoi, Joyce Mwongeli ^a   Nyangweso, George ^a   Wambua, Juliana ^a   Opiyo, Michael ^a   Nduati, Eunice Wambui ^a   Bejon, Philip ^a,b   Marsh, Kevin ^a,b   Ndungu, Francis Maina ^a  

^a KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c THE FRANCIS CRICK INSTITUTE   (United Kingdom)

Author keywords

Immunity; Malaria; T cells

Indexed keywords

ALPHA INTERFERON; CXCL9 CHEMOKINE; EOTAXIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TUMOR NECROSIS FACTOR;

ARTICLE; CD4+ T LYMPHOCYTE; CELL ISOLATION; CELL PROLIFERATION; CELL STIMULATION; CELLULAR IMMUNITY; CHILD; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DISEASE DURATION; ENVIRONMENTAL EXPOSURE; FEMALE; FEVER; HUMAN; HUMAN CELL; INFECTION RISK; KENYA; MALARIA FALCIPARUM; MALE; NONHUMAN; PARASITE IMMUNITY; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASMODIUM FALCIPARUM; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; T LYMPHOCYTE;

EID: 84995639967     PISSN: None     EISSN: 17417015     Source Type: Journal    
DOI: 10.1186/s12916-016-0683-6     Document Type: Article

References (58)

1. World Health Organization. World Malaria Report. Geneva: WHO; 2014.
2. Noor AM, Kinyoki DK, Mundia CW, Kabaria CW, Mutua JW, Alegana VA, et al. The changing risk of Plasmodium falciparum malaria infection in Africa: 2000-10: a spatial and temporal analysis of transmission intensity. Lancet. 2014;383:1739-47.
3. Marsh K, Kinyanjui S. Immune effector mechanisms in malaria. Parasite Immunol. 2006;28:51-60.
4. Tran TM, Li S, Doumbo S, Doumtabe D, Huang C-Y, Dia S, et al. An intensive longitudinal cohort study of Malian children and adults reveals no evidence of acquired immunity to Plasmodium falciparum infection. Clin Infect Dis. 2013;57:40-7.
5. Cohen S, McGregor IA, Carrington S. Gamma-globulin and acquired immunity to human malaria. Nature. 1961;192:733-7.
6. Langhorne J, Ndungu FM, Sponaas A-M, Marsh K. Immunity to malaria: more questions than answers. Nat Immunol. 2008;9:725-32.
7. Portugal S, Moebius J, Skinner J, Doumbo S, Doumtabe D, Kone Y, et al. Exposure-dependent control of malaria-induced inflammation in children. PLoS Pathog. 2014;10:e1004079.
8. + γδ T cells are associated with clinical tolerance to malaria. Sci Transl Med. 2014;6(251):251ra117.
9. 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.
10. Butler NS, Moebius J, Pewe LL, Traore B, Doumbo OK, Tygrett LT, et al. Therapeutic blockade of PD-L1 and LAG-3 rapidly clears established blood-stage Plasmodium infection. Nat Immunol. 2011;13:188-95.
11. Hafalla JCR, Claser C, Couper KN, Grau GE, Renia L, de Souza JB, et al. The CTLA-4 and PD-1/PD-L1 inhibitory pathways independently regulate host resistance to Plasmodium-induced acute immune pathology. PLoS Pathog. 2012;8:e1002504.
12. Horne-Debets JM, Faleiro R, Karunarathne DS, Liu XQ, Lineburg KE, Poh CM, et al. PD-1 dependent exhaustion of CD8+ T cells drives chronic malaria. Cell Rep. 2013;5:1204-13.
13. 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.
14. Pinzon-Charry A, Woodberry T, Kienzle V, McPhun V, Minigo G, Lampah DA, et al. Apoptosis and dysfunction of blood dendritic cells in patients with falciparum and vivax malaria. J Exp Med. 2013;210:1635-46.
15. 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.
16. O'Garra A, Vieira P. TH1 cells control themselves by producing interleukin-10. Nat Rev Immunol. 2007;7:425-8.
17. Linke A, Kühn R, Müller W, Honarvar N, Li C, Langhorne J. Plasmodium chabaudi chabaudi: differential susceptibility of gene-targeted mice deficient in IL-10 to an erythrocytic-stage infection. Exp Parasitol. 1996;84:253-63.
18. Li C, Corraliza I, Langhorne J. A defect in interleukin-10 leads to enhanced malarial disease in Plasmodium chabaudi chabaudi infection in mice. Infect Immun. 1999;67:4435-42.
19. Freitas do Rosario AP, Langhorne J. T cell-derived IL-10 and its impact on the regulation of host responses during malaria. Int J Parasitol. 2012;42:549-55.
20. Lepers JP, Deloron P, Fontenille D, Coulanges P. Reappearance of falciparum malaria in central highland plateaux of Madagascar. Lancet. 1988;1:586.
21. Jelinek T, TropNetEurop. Imported falciparum malaria in Europe: 2007 data from TropNetEurop. Euro Surveill. 2008;13(23).
22. Struik SS, Riley EM. Does malaria suffer from lack of memory? Immunol Rev. 2004;201:268-90.
23. 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.
24. Kinyanjui SM, Conway DJ, Lanar DE, Marsh K. IgG antibody responses to Plasmodium falciparum merozoite antigens in Kenyan children have a short half-life. Malar J. 2007;6:82.
25. Waa JV, Jensen JB, Akood MA, Bayoumi R. Longitudinal study on the in vitro immune response to Plasmodium falciparum in Sudan. Infect Immun. 1984;45:505-10.
26. Migot F, Chougnet C, Raharimalala L, Astagneau P, Lepers JP, Deloron P. Human immune responses to the Plasmodium falciparum ring infected erythrocyte surface antigen (Pf155/RESA) after a decrease in malaria transmission in Madagascar. Am J Trop Med Hyg. 1993;48:432-9.
27. Ndungu FM, Olotu A, Mwacharo J, Nyonda M, Apfeld J, Mramba LK, et al. Memory B cells are a more reliable archive for historical antimalarial responses than plasma antibodies in no-longer exposed children. Proc Natl Acad Sci. 2012;109:8247-52.
28. Moncunill G, Mayor A, Bardají 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. 2013;8:e73360.
29. Jennings RM, De Souza JB, Todd JE, Armstrong M, Flanagan KL, Riley EM, et al. Imported Plasmodium falciparum malaria: are patients originating from disease-endemic areas less likely to develop severe disease? A prospective, observational study. Am J Trop Med Hyg. 2006;75:1195-9.
30. Plebanski M, Flanagan KL, Lee EA, Reece WH, Hart K, Gelder C, et al. Interleukin 10-mediated immunosuppression by a variant CD4 T cell epitope of Plasmodium falciparum. Immunity. 1999;10:651-60.
31. Hirunpetcharat C, Good MF. Deletion of Plasmodium berghei-specific CD4+ T cells adoptively transferred into recipient mice after challenge with homologous parasite. Proc Natl Acad Sci. 1998;95:1715-20.
32. Wipasa J, Xu H, Stowers A, Good MF. Apoptotic deletion of Th cells specific for the 19-kDa carboxyl-terminal fragment of merozoite surface protein 1 during malaria infection. J Immunol. 2001;167:3903-9.
33. Urban BC, Ferguson DJ, Pain A, Willcox N, Plebanski M, Austyn JM, Roberts DJ. Plasmodium falciparum infected erythrocytes modulate the maturation of dendritic cells. Nature. 1999;400:73-7.
34. Wipasa J, Okell L, Sakkhachornphop S, Suphavilai C, Chawansuntati K, Liewsaree W, et al. Short-lived IFN-γ effector responses, but long-lived IL-10 memory responses, to malaria in an area of low malaria endemicity. PLoS Pathog. 2011;7:e1001281.
35. Snow RW, Kibuchi E, Karuri SW, Sang G, Gitonga CW, Mwandawiro C, et al. Changing malaria prevalence on the Kenyan coast since 1974: climate, drugs and vector control. PLoS One. 2015;10:e0128792.
36. O'Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, et al. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet. 2008;372:1555-62.
37. Bejon P, Mwacharo J, Kai O, Todryk S, Keating S, Lowe B, et al. The Induction and Persistence of T Cell IFN- Responses after Vaccination or Natural Exposure Is Suppressed by Plasmodium falciparum. J Immunol. 2007;179:4193-201.
38. Mbogo CM, Mwangangi JM, Nzovu J, Gu W, Yan G, Gunter JT, et al. Spatial and temporal heterogeneity of Anopheles mosquitoes and Plasmodium falciparum transmission along the Kenyan coast. Am J Trop Med Hyg. 2003;68:734-42.
39. O'Meara WP, Mwangi TW, Williams TN, McKenzie FE, Snow RW, Marsh K. Relationship between exposure, clinical malaria, and age in an area of changing transmission intensity. Am J Trop Med Hyg. 2008;79:185-91.
40. Rougemont M, Van Saanen M, Sahli R, Hinrikson HP, Bille J, Jaton K. Detection of four Plasmodium species in blood from humans by 18S rRNA gene subunit-based and species-specific real-time PCR assays. J Clin Microbiol. 2004;42:5636-43.
41. Quah BJC, Warren HS, Parish CR. Monitoring lymphocyte proliferation in vitro and in vivo with the intracellular fluorescent dye carboxyfluorescein diacetate succinimidyl ester. Nat Protoc. 2007;2:2049-56.
42. Seder RA, Darrah PA, Roederer M. T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol. 2008;8:247-58.
43. Gitau EN, Tuju J, Stevenson L, Kimani E, Karanja H, Marsh K, et al. T-cell responses to the DBLα-Tag, a short semi-conserved region of the Plasmodium falciparum membrane erythrocyte protein 1. Hviid L, editor. PLoS One. 2012;7:e30095.
44. Grossman Z, Meier-Schellersheim M, Sousa AE, Victorino RM, Paul WE. CD4+ T-cell depletion in HIV infection: are we closer to understanding the cause? Nat Med. 2002;8:319-23.
45. Okoye A, Meier-Schellersheim M, Brenchley JM, Hagen SI, Walker JM, Rohankhedkar M, et al. Progressive CD4+ central-memory T cell decline results in CD4+ effector-memory insufficiency and overt disease in chronic SIV infection. J Exp Med. 2007;204:2171-85.
46. Roetynck S, Olotu A, Simam J, Marsh K, Stockinger B, Urban B, et al. Phenotypic and functional profiling of CD4 T cell compartment in distinct populations of healthy adults with different antigenic exposure. PLoS One. 2013;8:e55195.
47. O'Connor RA, Jenson JS, Devaney E. NO contributes to proliferative suppression in a murine model of filariasis. Infect Immun. 2000;68:6101-7.
48. Maizels RM, Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol. 2003;3:733-44.
49. McNeil AC, Shupert WL, Iyasere CA, Hallahan CW, Mican J, Davey RT, et al. High-level HIV-1 viremia suppresses viral antigen-specific CD4+ T cell proliferation. Proc Natl Acad Sci. 2001;98:13878-83.
50. Rochman I, Paul WE, Ben-Sasson SZ. IL-6 increases primed cell expansion and survival. J Immunol. 2005;174:4761-7.
51. Dienz O, Rincon M. The effects of IL-6 on CD4 T cell responses. Clin Immunol. 2009;130:27-33.
52. Whiting D, Hsieh G, Yun JJ, Banerji A, Yao W, Fishbein MC, et al. Chemokine monokine induced by IFN-/CXC chemokine ligand 9 stimulates T lymphocyte proliferation and effector cytokine production. J Immunol. 2004;172:7417-24.
53. Ayroldi E, Zollo O, Cannarile L, D'Adamio F, Grohmann U, Delfino DV, et al. Interleukin-6 (IL-6) prevents activation-induced cell death: IL-2 - independent inhibition of Fas/fasL expression and cell death. Blood. 1998;92:4212-9.
54. Ben-Sasson SZ, Hu-Li J, Quiel J, Cauchetaux S, Ratner M, Shapira I, et al. IL-1 acts directly on CD4 T cells to enhance their antigen-driven expansion and differentiation. Proc Natl Acad Sci. 2009;106:7119-24.
55. Walther M, Tongren JE, Andrews L, Korbel D, King E, Fletcher H, et al. Upregulation of TGF-β, FOXP3, and CD4 + CD25+ regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity. 2005;23:287-96.
56. Walther M, Jeffries D, Finney OC, Njie M, Ebonyi A, Deininger S, et al. Distinct roles for FOXP3+ and FOXP3- CD4+ T cells in regulating cellular immunity to uncomplicated and severe Plasmodium falciparum malaria. PLoS Pathog. 2009;5:e1000364.
57. Perri G, Solbiati M, Vento S, Checchi G, Luzzati R, Bonora S, et al. West African immigrants and new patterns of malaria imported to North Eastern Italy. J Travel Med. 1994;1:147-51.
58. Boutlis CS, Yeo TW, Anstey NM. Malaria tolerance - for whom the cell tolls? Trends Parasitol. 2006;22:371-7.