Short-Lived IFN-γ Effector Responses, but Long-Lived IL-10 Memory Responses, to Malaria in an Area of Low Malaria Endemicity
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 i...
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| Published in | PLoS pathogens Vol. 7; no. 2; p. e1001281 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.02.2011
Public Library of Science (PLoS) |
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| Online Access | Get full text |
| ISSN | 1553-7374 1553-7366 1553-7374 |
| DOI | 10.1371/journal.ppat.1001281 |
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| Abstract | 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. |
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| AbstractList | 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. 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.sup.+].sup.+]+ 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.sup.+].sup.+]+ T cell effector memory ([CD4.sup.+]5RO+) 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. 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. Despite some recent successes in reducing the burden of malaria in several African countries, malaria still causes up to 500 million cases of acute illness every year, killing over a million people. The widespread availability of a safe and effective vaccine would greatly increase our chances of controlling this disease and possibly, even, eliminating it as a major health concern. Attempts to develop a vaccine have had limited success. The fact that people can be repeatedly infected with malaria over many years has raised the concern that immunity to malaria may be short-lived, complicating the induction of long term protection by vaccination. In this study we have calculated the half-life of cellular immune responses to malaria in previously infected individuals from Thailand. We have found that, in the absence of boosting of immunity by reinfection, malaria-specific inflammatory responses are relatively short-lived, with a half life of approximately 3 years. However, malaria-specific anti-inflammatory responses (which have been linked to resistance to severe malarial disease) seem to be very long-lived (the half life being indistinguishable from infinity). Our observations have important implications for understanding the immunoepidemiology of naturally acquired malaria infections and for malaria vaccine development. 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.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. |
| Audience | Academic |
| Author | Hafalla, Julius C. R. Wipasa, Jiraprapa Liewsaree, Witaya Suphavilai, Chaisuree Sakkhachornphop, Supachai Chawansuntati, Kriangkrai Okell, Lucy Riley, Eleanor M. |
| AuthorAffiliation | Case Western Reserve University, United States of America 2 Department of Immunology and Infection, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom 3 Vector Borne Disease Section, Office of Disease Prevention and Control, Chiang Mai, Thailand 1 Research Institute for Health Sciences, Chiang Mai University, Chiang Mai, Thailand |
| AuthorAffiliation_xml | – name: 2 Department of Immunology and Infection, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom – name: 1 Research Institute for Health Sciences, Chiang Mai University, Chiang Mai, Thailand – name: 3 Vector Borne Disease Section, Office of Disease Prevention and Control, Chiang Mai, Thailand – name: Case Western Reserve University, United States of America |
| Author_xml | – sequence: 1 givenname: Jiraprapa surname: Wipasa fullname: Wipasa, Jiraprapa – sequence: 2 givenname: Lucy surname: Okell fullname: Okell, Lucy – sequence: 3 givenname: Supachai surname: Sakkhachornphop fullname: Sakkhachornphop, Supachai – sequence: 4 givenname: Chaisuree surname: Suphavilai fullname: Suphavilai, Chaisuree – sequence: 5 givenname: Kriangkrai surname: Chawansuntati fullname: Chawansuntati, Kriangkrai – sequence: 6 givenname: Witaya surname: Liewsaree fullname: Liewsaree, Witaya – sequence: 7 givenname: Julius C. R. surname: Hafalla fullname: Hafalla, Julius C. R. – sequence: 8 givenname: Eleanor M. surname: Riley fullname: Riley, Eleanor M. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21347351$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: JW EMR. Performed the experiments: JW SS CS KC. Analyzed the data: JW LO JCRH EMR. Contributed reagents/materials/analysis tools: JW WL. Wrote the paper: JW LO JCRH EMR. Organized field study and generated patient information from historical records: WL. Current address: MRC Centre for Outbreak Analysis and Modelling, Department of Infectious Disease Epidemiology, Imperial College, London. |
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| SubjectTerms | Adult CD4-Positive T-Lymphocytes - immunology CD4-Positive T-Lymphocytes - metabolism CD4-Positive T-Lymphocytes - physiology Cells, Cultured Development and progression Endemic Diseases Female Geography Humans Immunologic Memory - physiology Immunology/Immunity to Infections Infectious Diseases/Protozoal Infections Interferon gamma Interferon-gamma - secretion Interleukin-10 Interleukin-10 - secretion Malaria Malaria - epidemiology Malaria - immunology Malaria - metabolism Male Middle Aged Physiological aspects T cells Thailand - epidemiology Time Factors Young Adult |
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| Title | Short-Lived IFN-γ Effector Responses, but Long-Lived IL-10 Memory Responses, to Malaria in an Area of Low Malaria Endemicity |
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