Antecedent Nippostrongylus infection alters the lung immune response to Plasmodium berghei

J. M. Craig, A. L. Scott

Research output: Research - peer-reviewArticle

Abstract

In endemic regions, it is not uncommon for patients to be co-infected with soil-transmitted helminths and malaria. Although both malaria and many helminth species use the lungs as a site of development, little attention has been paid to the impact that pulmonary immunity induced by one parasite has on the lung response to the other. To model the consequences of a prior hookworm exposure on the development of immunity to malaria in the lungs, mice were infected with Nippostrongylus brasiliensis and 2 weeks later challenged with Plasmodium berghei. We found that a pre-existing hookworm-induced type 2 immune environment had a measurable but modest impact on the nature of the malaria-driven type 1 cytokine response in the lungs that was associated with a transient effect on parasite development and no significant changes in morbidity and mortality after malaria infection. However, prior hookworm infection did have a lasting effect on lung macrophages, where the malaria-induced M1-like response was blunted by previous M2 polarization. These results demonstrate that, although helminth parasites confer robust changes to the immunological status of the pulmonary microenvironment, lung immunity is plastic and capable of rapidly adapting to consecutive heterologous infections.

LanguageEnglish (US)
Article numbere12441
JournalParasite Immunology
Volume39
Issue number8
DOIs
StatePublished - Aug 1 2017

Fingerprint

Nippostrongylus
Plasmodium berghei
Lung
Infection
Malaria
Helminths
Immunity
Parasites
Ancylostomatoidea
Hookworm Infections
Plastics
Soil
Macrophages
Cytokines
Morbidity
Mortality

Keywords

  • alveolar macrophage
  • emphysema
  • lung
  • M2
  • malaria

ASJC Scopus subject areas

  • Parasitology
  • Immunology

Cite this

Antecedent Nippostrongylus infection alters the lung immune response to Plasmodium berghei. / Craig, J. M.; Scott, A. L.

In: Parasite Immunology, Vol. 39, No. 8, e12441, 01.08.2017.

Research output: Research - peer-reviewArticle

@article{3a0c0d89a7a047a3bc57e7bf7ef17566,
title = "Antecedent Nippostrongylus infection alters the lung immune response to Plasmodium berghei",
abstract = "In endemic regions, it is not uncommon for patients to be co-infected with soil-transmitted helminths and malaria. Although both malaria and many helminth species use the lungs as a site of development, little attention has been paid to the impact that pulmonary immunity induced by one parasite has on the lung response to the other. To model the consequences of a prior hookworm exposure on the development of immunity to malaria in the lungs, mice were infected with Nippostrongylus brasiliensis and 2 weeks later challenged with Plasmodium berghei. We found that a pre-existing hookworm-induced type 2 immune environment had a measurable but modest impact on the nature of the malaria-driven type 1 cytokine response in the lungs that was associated with a transient effect on parasite development and no significant changes in morbidity and mortality after malaria infection. However, prior hookworm infection did have a lasting effect on lung macrophages, where the malaria-induced M1-like response was blunted by previous M2 polarization. These results demonstrate that, although helminth parasites confer robust changes to the immunological status of the pulmonary microenvironment, lung immunity is plastic and capable of rapidly adapting to consecutive heterologous infections.",
keywords = "alveolar macrophage, emphysema, lung, M2, malaria",
author = "Craig, {J. M.} and Scott, {A. L.}",
year = "2017",
month = "8",
doi = "10.1111/pim.12441",
volume = "39",
journal = "Parasite Immunology",
issn = "0141-9838",
publisher = "Wiley-Blackwell",
number = "8",

}

TY - JOUR

T1 - Antecedent Nippostrongylus infection alters the lung immune response to Plasmodium berghei

AU - Craig,J. M.

AU - Scott,A. L.

PY - 2017/8/1

Y1 - 2017/8/1

N2 - In endemic regions, it is not uncommon for patients to be co-infected with soil-transmitted helminths and malaria. Although both malaria and many helminth species use the lungs as a site of development, little attention has been paid to the impact that pulmonary immunity induced by one parasite has on the lung response to the other. To model the consequences of a prior hookworm exposure on the development of immunity to malaria in the lungs, mice were infected with Nippostrongylus brasiliensis and 2 weeks later challenged with Plasmodium berghei. We found that a pre-existing hookworm-induced type 2 immune environment had a measurable but modest impact on the nature of the malaria-driven type 1 cytokine response in the lungs that was associated with a transient effect on parasite development and no significant changes in morbidity and mortality after malaria infection. However, prior hookworm infection did have a lasting effect on lung macrophages, where the malaria-induced M1-like response was blunted by previous M2 polarization. These results demonstrate that, although helminth parasites confer robust changes to the immunological status of the pulmonary microenvironment, lung immunity is plastic and capable of rapidly adapting to consecutive heterologous infections.

AB - In endemic regions, it is not uncommon for patients to be co-infected with soil-transmitted helminths and malaria. Although both malaria and many helminth species use the lungs as a site of development, little attention has been paid to the impact that pulmonary immunity induced by one parasite has on the lung response to the other. To model the consequences of a prior hookworm exposure on the development of immunity to malaria in the lungs, mice were infected with Nippostrongylus brasiliensis and 2 weeks later challenged with Plasmodium berghei. We found that a pre-existing hookworm-induced type 2 immune environment had a measurable but modest impact on the nature of the malaria-driven type 1 cytokine response in the lungs that was associated with a transient effect on parasite development and no significant changes in morbidity and mortality after malaria infection. However, prior hookworm infection did have a lasting effect on lung macrophages, where the malaria-induced M1-like response was blunted by previous M2 polarization. These results demonstrate that, although helminth parasites confer robust changes to the immunological status of the pulmonary microenvironment, lung immunity is plastic and capable of rapidly adapting to consecutive heterologous infections.

KW - alveolar macrophage

KW - emphysema

KW - lung

KW - M2

KW - malaria

UR - http://www.scopus.com/inward/record.url?scp=85020060156&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85020060156&partnerID=8YFLogxK

U2 - 10.1111/pim.12441

DO - 10.1111/pim.12441

M3 - Article

VL - 39

JO - Parasite Immunology

T2 - Parasite Immunology

JF - Parasite Immunology

SN - 0141-9838

IS - 8

M1 - e12441

ER -