IgM in human immunity to Plasmodium falciparum malaria

Most studies on human immunity to malaria have focused on the roles of immunoglobulin G (IgG), whereas the roles of IgM remain undefined. Analyzing multiple human cohorts to assess the dynamics of malaria-specific IgM during experimentally induced and naturally acquired malaria, we identified IgM ac...

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Published in:	Science advances Vol. 5; no. 9; p. eaax4489
Main Authors:	Boyle, M J, Chan, J A, Handayuni, I, Reiling, L, Feng, G, Hilton, A, Kurtovic, L, Oyong, D, Piera, K A, Barber, B E, William, T, Eisen, D P, Minigo, G, Langer, C, Drew, D R, de Labastida Rivera, F, Amante, F H, Williams, T N, Kinyanjui, S, Marsh, K, Doolan, D L, Engwerda, C, Fowkes, F J I, Grigg, M J, Mueller, I, McCarthy, J S, Anstey, N M, Beeson, J G
Format:	Journal Article
Language:	English
Published:	United States American Association for the Advancement of Science 01-09-2019
Subjects:	Adolescent Adult Antibodies, Protozoan - immunology Antibody Formation - immunology Antibody Specificity - immunology Antigens, Protozoan - immunology Female Host-Parasite Interactions - immunology Humans Immunity Immunoglobulin G - immunology Immunoglobulin M - immunology Immunology Malaria, Falciparum - immunology Malaria, Falciparum - parasitology Male Microbiology Middle Aged Plasmodium falciparum - immunology SciAdv r-articles Young Adult
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Abstract	Most studies on human immunity to malaria have focused on the roles of immunoglobulin G (IgG), whereas the roles of IgM remain undefined. Analyzing multiple human cohorts to assess the dynamics of malaria-specific IgM during experimentally induced and naturally acquired malaria, we identified IgM activity against blood-stage parasites. We found that merozoite-specific IgM appears rapidly in infection and is prominent during malaria in children and adults with lifetime exposure, together with IgG. Unexpectedly, IgM persisted for extended periods of time; we found no difference in decay of merozoite-specific IgM over time compared to that of IgG. IgM blocked merozoite invasion of red blood cells in a complement-dependent manner. IgM was also associated with significantly reduced risk of clinical malaria in a longitudinal cohort of children. These findings suggest that merozoite-specific IgM is an important functional and long-lived antibody response targeting blood-stage malaria parasites that contributes to malaria immunity.
AbstractList	IgM is an important and long-lived component of anti-malarial immunity in humans and blocks infection of red blood cells. Most studies on human immunity to malaria have focused on the roles of immunoglobulin G (IgG), whereas the roles of IgM remain undefined. Analyzing multiple human cohorts to assess the dynamics of malaria-specific IgM during experimentally induced and naturally acquired malaria, we identified IgM activity against blood-stage parasites. We found that merozoite-specific IgM appears rapidly in Plasmodium falciparum infection and is prominent during malaria in children and adults with lifetime exposure, together with IgG. Unexpectedly, IgM persisted for extended periods of time; we found no difference in decay of merozoite-specific IgM over time compared to that of IgG. IgM blocked merozoite invasion of red blood cells in a complement-dependent manner. IgM was also associated with significantly reduced risk of clinical malaria in a longitudinal cohort of children. These findings suggest that merozoite-specific IgM is an important functional and long-lived antibody response targeting blood-stage malaria parasites that contributes to malaria immunity. Most studies on human immunity to malaria have focused on the roles of immunoglobulin G (IgG), whereas the roles of IgM remain undefined. Analyzing multiple human cohorts to assess the dynamics of malaria-specific IgM during experimentally induced and naturally acquired malaria, we identified IgM activity against blood-stage parasites. We found that merozoite-specific IgM appears rapidly in infection and is prominent during malaria in children and adults with lifetime exposure, together with IgG. Unexpectedly, IgM persisted for extended periods of time; we found no difference in decay of merozoite-specific IgM over time compared to that of IgG. IgM blocked merozoite invasion of red blood cells in a complement-dependent manner. IgM was also associated with significantly reduced risk of clinical malaria in a longitudinal cohort of children. These findings suggest that merozoite-specific IgM is an important functional and long-lived antibody response targeting blood-stage malaria parasites that contributes to malaria immunity.
Author	Reiling, L Fowkes, F J I Boyle, M J William, T Oyong, D Doolan, D L Anstey, N M Chan, J A Kinyanjui, S Beeson, J G Kurtovic, L Handayuni, I Piera, K A Williams, T N Eisen, D P Langer, C Marsh, K McCarthy, J S Mueller, I Feng, G Grigg, M J Drew, D R Barber, B E Hilton, A de Labastida Rivera, F Minigo, G Amante, F H Engwerda, C
Author_xml	– sequence: 1 givenname: M J orcidid: 0000-0002-0268-232X surname: Boyle fullname: Boyle, M J organization: QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia – sequence: 2 givenname: J A orcidid: 0000-0003-0708-8263 surname: Chan fullname: Chan, J A organization: Burnet Institute for Medical Research and Public Health, Melbourne, Victoria, Australia – sequence: 3 givenname: I surname: Handayuni fullname: Handayuni, I organization: Global and Tropical Health Division, Menzies School of Health Research, Darwin, Northern Territory, Australia – sequence: 4 givenname: L surname: Reiling fullname: Reiling, L organization: Burnet Institute for Medical Research and Public Health, Melbourne, Victoria, Australia – sequence: 5 givenname: G surname: Feng fullname: Feng, G organization: Department of Medicine, University of Melbourne, Melbourne, Victoria, Australia – sequence: 6 givenname: A orcidid: 0000-0001-8739-1830 surname: Hilton fullname: Hilton, A organization: Burnet Institute for Medical Research and Public Health, Melbourne, Victoria, Australia – sequence: 7 givenname: L orcidid: 0000-0001-8594-0031 surname: Kurtovic fullname: Kurtovic, L organization: Department of Immunology and Pathology, Monash University, Melbourne, Victoria, Australia – sequence: 8 givenname: D surname: Oyong fullname: Oyong, D organization: Charles Darwin University, Darwin, Northern Territory, Australia – sequence: 9 givenname: K A orcidid: 0000-0002-7414-9604 surname: Piera fullname: Piera, K A organization: Global and Tropical Health Division, Menzies School of Health Research, Darwin, Northern Territory, Australia – sequence: 10 givenname: B E orcidid: 0000-0003-1066-7960 surname: Barber fullname: Barber, B E organization: Infectious Diseases Society Sabah-Menzies School of Health Research Clinical Research Unit, Queen Elizabeth Hospital, Kota Kinabalu, Sabah, Malaysia – sequence: 11 givenname: T orcidid: 0000-0002-2195-6736 surname: William fullname: William, T organization: Gleneagles Hospital Kota Kinabalu Sabah, Malaysia – sequence: 12 givenname: D P surname: Eisen fullname: Eisen, D P organization: Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, Queensland, Australia – sequence: 13 givenname: G orcidid: 0000-0001-5158-7700 surname: Minigo fullname: Minigo, G organization: Charles Darwin University, Darwin, Northern Territory, Australia – sequence: 14 givenname: C surname: Langer fullname: Langer, C organization: Burnet Institute for Medical Research and Public Health, Melbourne, Victoria, Australia – sequence: 15 givenname: D R surname: Drew fullname: Drew, D R organization: Burnet Institute for Medical Research and Public Health, Melbourne, Victoria, Australia – sequence: 16 givenname: F orcidid: 0000-0001-5241-2339 surname: de Labastida Rivera fullname: de Labastida Rivera, F organization: QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia – sequence: 17 givenname: F H surname: Amante fullname: Amante, F H organization: QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia – sequence: 18 givenname: T N surname: Williams fullname: Williams, T N organization: Imperial College, London, UK – sequence: 19 givenname: S orcidid: 0000-0002-3910-0450 surname: Kinyanjui fullname: Kinyanjui, S organization: Nuffield Department of Medicine, University of Oxford, Oxford, UK – sequence: 20 givenname: K orcidid: 0000-0001-8377-5466 surname: Marsh fullname: Marsh, K organization: Nuffield Department of Medicine, University of Oxford, Oxford, UK – sequence: 21 givenname: D L surname: Doolan fullname: Doolan, D L organization: Australian Institute of Tropical Health and Medicine, James Cook University, Cairns, Queensland, Australia – sequence: 22 givenname: C orcidid: 0000-0003-2813-4804 surname: Engwerda fullname: Engwerda, C organization: QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia – sequence: 23 givenname: F J I surname: Fowkes fullname: Fowkes, F J I organization: Department of Epidemiology and Preventive Medicine, Department of Infectious Diseases, Monash University, Melbourne, Victoria, Australia – sequence: 24 givenname: M J orcidid: 0000-0001-9914-8352 surname: Grigg fullname: Grigg, M J organization: Infectious Diseases Society Sabah-Menzies School of Health Research Clinical Research Unit, Queen Elizabeth Hospital, Kota Kinabalu, Sabah, Malaysia – sequence: 25 givenname: I surname: Mueller fullname: Mueller, I organization: Department of Parasites and Insect Vectors, Institute Pasteur, Paris, France – sequence: 26 givenname: J S orcidid: 0000-0001-6596-9718 surname: McCarthy fullname: McCarthy, J S organization: The University of Queensland, Brisbane, Queensland, Australia – sequence: 27 givenname: N M surname: Anstey fullname: Anstey, N M organization: Charles Darwin University, Darwin, Northern Territory, Australia – sequence: 28 givenname: J G orcidid: 0000-0002-1018-7898 surname: Beeson fullname: Beeson, J G organization: Department of Microbiology and Central Clinical School, Monash University, Melbourne, Victoria, Australia
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Snippet	Most studies on human immunity to malaria have focused on the roles of immunoglobulin G (IgG), whereas the roles of IgM remain undefined. Analyzing multiple... IgM is an important and long-lived component of anti-malarial immunity in humans and blocks infection of red blood cells. Most studies on human immunity to...
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SubjectTerms	Adolescent Adult Antibodies, Protozoan - immunology Antibody Formation - immunology Antibody Specificity - immunology Antigens, Protozoan - immunology Female Host-Parasite Interactions - immunology Humans Immunity Immunoglobulin G - immunology Immunoglobulin M - immunology Immunology Malaria, Falciparum - immunology Malaria, Falciparum - parasitology Male Microbiology Middle Aged Plasmodium falciparum - immunology SciAdv r-articles Young Adult
Title	IgM in human immunity to Plasmodium falciparum malaria
URI	https://www.ncbi.nlm.nih.gov/pubmed/31579826 https://search.proquest.com/docview/2300596437 https://pubmed.ncbi.nlm.nih.gov/PMC6760923
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