Immunity to malaria is widely believed to wane in the absence of reinfection, but direct evidence for the presence or absence of durable immunological memory to malaria is limited. Here, we analysed malaria-specific CD4+ T cell responses of individuals living in an area of low malaria transmission in northern Thailand, who had had a documented clinical attack of P. falciparum and/or P. vivax in the past 6 years. CD4+ T cell effector memory (CD45RO+) IFN-γ (24 hours ex vivo restimulation) and cultured IL-10 (6 day secretion into culture supernatant) responses to malaria schizont antigens were detected only in malaria-exposed subjects and were more prominent in subjects with long-lived antibodies or memory B cells specific to malaria antigens. The number of IFN-γ-producing effector memory T cells declined significantly over the 12 months of the study, and with time since last documented malaria infection, with an estimated half life of the response of 3.3 (95% CI 1.9–10.3) years. In sharp contrast, IL-10 responses were sustained for many years after last known malaria infection with no significant decline over at least 6 years. The observations have clear implications for understanding the immunoepidemiology of naturally acquired malaria infections and for malaria vaccine development.
Vyšlo v časopise: Short-Lived IFN-γ Effector Responses, but Long-Lived IL-10 Memory Responses, to Malaria in an Area of Low Malaria Endemicity. PLoS Pathog 7(2): e32767. doi:10.1371/journal.ppat.1001281 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001281
1. GuptaS
SnowRW
DonnellyCA
MarshK
NewboldC
1999 Immunity to non-cerebral severe malaria is acquired after one or two infections. Nat Med 5 340 343
2. LanghorneJ
NdunguFM
SponaasAM
2008 Immunity to malaria: more questions than answers. Nat Immunol 9 725 732
3. PlebanskiM
FlanaganKL
LeeEA
ReeceWH
HartK
1999 Interleukin 10-mediated immunosuppression by a variant CD4 T cell epitope of Plasmodium falciparum. Immunity 10 651 660
4. UrbanBC
FergusonDJ
PainA
WillcoxN
PlebanskiM
1999 Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 400 73 77
5. UrbanBC
MwangiT
RossA
KinyanjuiS
MosoboM
2001 Peripheral blood dendritic cells in children with acute Plasmodium falciparum malaria. Blood 98 2859 2861
6. HirunpetcharatC
GoodMF
1998 Deletion of Plasmodium berghei-specific CD4+ T cells adoptively transferred into recipient mice after challenge with homologous parasite. Proc Natl Acad Sci U S A 95 1715 1720
7. WipasaJ
XuH
StowersA
2001 Apoptotic deletion of Th cells specific for the 19-kDa carboxyl-terminal fragment of merozoite surface protein 1 during malaria infection. J Immunol 167 3903 3909
8. D'Imperio LimaMR
AlvarezJM
FurtadoGC
KipnisTL
CoutinhoA
1996 Ig-isotype patterns of primary and secondary B cell responses to Plasmodium chabaudi chabaudi correlate with IFN-gamma and IL-4 cytokine production with CD45RB expression by CD4+ spleen cells. Scand J Immunol 43 263 270
9. StephensR
AlbanoFR
QuinS
PascalBJ
HarrisonV
2005 Malaria-specific transgenic CD4(+) T cells protect immunodeficient mice from lethal infection and demonstrate requirement for a protective threshold of antibody production for parasite clearance. Blood 106 1676 1684
10. RogersPR
DubeyC
SwainSL
2000 Qualitative changes accompany memory T cell generation: faster, more effective responses at lower doses of antigen. J Immunol 164 2338 2346
11. SallustoF
LenigD
ForsterR
LippM
LanzavecchiaA
1999 Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401 708 712
12. SallustoF
2009 Heterogeneity of CD4+ memory T cells: functional modules for tailored immunity. Eur J Immunol 39 2076 2082
13. FellAH
CurrierJ
1994 Inhibition of Plasmodium falciparum growth in vitro by CD4+ and CD8+ T cells from non-exposed donors. Parasite Immunol 16 579 586
14. GoodierMR
TargettGA
1997 Polyclonal T-cell responses to Plasmodium falciparum gametocytes in malaria nonexposed donors. Parasite Immunol 19 419 425
15. ZeveringY
AmanteF
SmillieA
SmithG
1992 High frequency of malaria-specific T cells in non-exposed humans. Eur J Immunol 22 689 696
16. WipasaJ
SuphavilaiC
OkellLC
CookJ
CorranPH
2010 Long-Lived Antibody and B Cell Memory Responses to the Human Malaria Parasites, Plasmodium falciparum and Plasmodium vivax. PLoS Pathog 6 e1000770
17. Artavanis-TsakonasK
RileyEM
2002 Innate immune response to malaria: rapid induction of IFN-gamma from human NK cells by live Plasmodium falciparum-infected erythrocytes. J Immunol 169 2956 2963
18. SnounouG
ViriyakosolS
ZhuXP
JarraW
PinheiroL
1993 High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol 61 315 320
19. GoodierMR
1997 Evidence for CD4+ T cell responses common to Plasmodium falciparum and recall antigens. Int Immunol 9 1857 1865
20. DickS
WaterfallM
CurrieJ
MaddyA
RileyE
1996 Naive human alpha beta T cells respond to membrane-associated components of malaria-infected erythrocytes by proliferation and production of interferon-gamma. Immunology 88 412 420
21. KeatingSM
BejonP
BerthoudT
VuolaJM
TodrykS
2005 Durable human memory T cells quantifiable by cultured enzyme-linked immunospot assays are induced by heterologous prime boost immunization and correlate with protection against malaria. J Immunol 175 5675 5680
22. GoodMF
BilsboroughJ
1994 Human T-cell responses to malaria: mostly forgotten or committed to memory? Parasitol Today 10 316 319
23. StruikSS
2004 Does malaria suffer from lack of memory? Immunol Rev 201 268 290
24. ChuangchaiyaS
JangpatarapongsaK
ChootongP
SirichaisinthopJ
SattabongkotJ
2010 Immune response to Plasmodium vivax has a potential to reduce malaria severity. Clin Exp Immunol 160 233 239
25. DiLilloDJ
MatsushitaT
TedderTF
2010 B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann N Y Acad Sci 1183 38 57
26. WaltherM
JeffriesD
FinneyOC
NjieM
EbonyiA
2009 Distinct roles for FOXP3 and FOXP3 CD4 T cells in regulating cellular immunity to uncomplicated and severe Plasmodium falciparum malaria. PLoS Pathog 5 e1000364
27. MoormannAM
SumbaPO
TischDJ
EmburyP
KingCH
2009 Stability of interferon-gamma and interleukin-10 responses to Plasmodium falciparum liver stage antigen 1 and thrombospondin-related adhesive protein immunodominant epitopes in a highland population from Western Kenya. Am J Trop Med Hyg 81 489 495
28. MoormannAM
JohnCC
TischD
2006 Stability of interferon-gamma and interleukin-10 responses to Plasmodium falciparum liver stage antigen-1 and thrombospondin-related adhesive protein in residents of a malaria holoendemic area. Am J Trop Med Hyg 74 585 590
29. RoussetF
GarciaE
DefranceT
PeronneC
VezzioN
1992 Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc Natl Acad Sci U S A 89 1890 1893
30. MalisanF
BriereF
BridonJM
HarindranathN
MillsFC
1996 Interleukin-10 induces immunoglobulin G isotype switch recombination in human CD40-activated naive B lymphocytes. J Exp Med 183 937 947
31. GarraudO
DioufA
HolmI
NguerCM
SpiegelA
1999 Secretion of parasite-specific immunoglobulin G by purified blood B lymphocytes from immune individuals after in vitro stimulation with recombinant Plasmodium falciparum merozoite surface protein-119 antigen. Immunology 97 204 210
32. GarraudO
PerrautR
NambeiWS
TallA
2002 Regulation of antigen-specific immunoglobulin G subclasses in response to conserved and polymorphic Plasmodium falciparum antigens in an in vitro model. Infect Immun 70 2820 2827
33. HorowitzA
BehrensRH
OkellL
FooksAR
2010 NK cells as effectors of acquired immune responses: effector CD4+ T cell-dependent activation of NK cells following vaccination. J Immunol 185 2808 2818
34. CombadiereB
BoissonnasA
CarcelainG
LefrancE
SamriA
2004 Distinct time effects of vaccination on long-term proliferative and IFN-gamma-producing T cell memory to smallpox in humans. J Exp Med 199 1585 1593
35. Puissant-LubranoB
BossiP
GayF
CranceJM
BonduelleO
2010 Control of vaccinia virus skin lesions by long-term-maintained IFN-gamma+TNF-alpha+ effector/memory CD4+ lymphocytes in humans. J Clin Invest 120 1636 1644
36. Hanna-WakimR
YasukawaLL
SungP
ArvinAM
GansHA
2008 Immune responses to mumps vaccine in adults who were vaccinated in childhood. J Infect Dis 197 1669 1675
37. FlanaganKL
OdhiamboK
2003 Ex vivo interferon-gamma immune response to thrombospondin-related adhesive protein in coastal Kenyans: longevity and risk of Plasmodium falciparum infection. Am J Trop Med Hyg 68 421 430
38. RileyEM
Morris-JonesS
BlackmanMJ
GreenwoodBM
HolderAA
1993 A longitudinal study of naturally acquired cellular and humoral immune responses to a merozoite surface protein (MSP1) of Plasmodium falciparum in an area of seasonal malaria transmission. Parasite Immunol 15 513 524
39. ZeveringY
KhamboonruangC
RungruengthanakitK
TungviboonchaiL
RuengpipattanapanJ
1994 Life-spans of human T-cell responses to determinants from the circumsporozoite proteins of Plasmodium falciparum and Plasmodium vivax. Proc Natl Acad Sci U S A 91 6118 6122
40. BilsboroughJ
CarlisleM
1993 Identification of Caucasian CD4 T cell epitopes on the circumsporozoite protein of Plasmodium vivax. T cell memory. J Immunol 151 890 899
41. MacallanDC
WallaceD
ZhangY
De LaraC
WorthAT
2004 Rapid turnover of effector-memory CD4(+) T cells in healthy humans. J Exp Med 200 255 260
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