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Targeting helminths: The expanding world of type 2 immune effector mechanisms

Maizels, Rick M., Gause, William C.·2023·Journal of Experimental Medicine
DOI 10.1084/jem.20221381PMC PMC10460967
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Abstract

In this new review, Rick Maizels and Bill Gause summarize how type 2 immune responses combat helminth parasites through novel mechanisms, coordinating multiple innate and adaptive cell and molecular players that can eliminate infection and repair-resultant tissue damage.

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Figure 1. Protective type 2 mechanisms against helminth parasites in the skin. In primary infection (left), N. brasiliensis larvae are quickly attacked by neutrophils, releasing extracellular traps (NETs); however, parasite DNases can break down the NETS, allowing helminths to continue their systemic migration. In secondary infection with the same parasite (center), IgE-armed basophils release IL-4 to activate M2 macrophages (shown in green), swarming around the larvae and upregulating Arg1, which deprives parasites of an essential amino acid. Whether Arg1 actually exits the cell is not known. In infections with S. stercoralis, basophils are not required, but a combination of eosinophils and neutrophils can trap larvae in the skin through a combination of NETs and eosinophil extracellular traps (EETs), and the release of noxious products myelin basic protein (MBP, from eosinophils) and myeloperoxidase (MPO, from neutrophils).
Figure 1. Protective type 2 mechanisms against helminth parasites in the skin. In primary infection (left), N. brasiliensis larvae are quickly attacked by neutrophils, releasing extracellular traps (NETs); however, parasite DNases can break down the NETS, allowing helminths to continue their systemic migration. In secondary infection with the same parasite (center), IgE-armed basophils release IL-4 to activate M2 macrophages (shown in green), swarming around the larvae and upregulating Arg1, which deprives parasites of an essential amino acid. Whether Arg1 actually exits the cell is not known. In infections with S. stercoralis, basophils are not required, but a combination of eosinophils and neutrophils can trap larvae in the skin through a combination of NETs and eosinophil extracellular traps (EETs), and the release of noxious products myelin basic protein (MBP, from eosinophils) and myeloperoxidase (MPO, from neutrophils).CC BY · PubMed Central
Figure 2. Immune effector mechanisms in the lung. In primary infection in the lung, an ineffective response is mobilized although it primes the immune system for effective protection to challenge infection. During N. brasiliensis infection, parasites transit from the skin to the lung as early as 12 h after infection and only remain in the lung for about 2 d. Associated tissue damage likely triggers γδT cells to produce IL-17 that recruit neutrophils, including an immature population (iNeu), which in turn drive M2 macrophage activation through IL-13 production and ingestion of apoptotic cells. Other signals including surfactant protein D (Sp-D) also help drive M2 macrophage activation. Neutrophils rapidly surround invading parasites, but they pass relatively unimpeded to the small intestine. Within several days after primary infection, macrophages have largely cleared RBCs and debris from the lung, and recruited monocytes have differentiated into monocyte-derived alveolar macrophages (Mo-AvMs), with an M2 phenotype. On secondary infection, migrating parasites that were able to exit the skin and invade the lung are surrounded by Mo-AvMs, which produce high levels of Arg1, depleting local arginine around the parasite, thereby mediating killing through a nutrient deprivation mechanism. Little tissue damage or neutrophil infiltration occurs and eosinophils, as well as Mo-AvMs, surround the parasite. Most parasites are killed, largely preventing their entry into the intestine.
Figure 2. Immune effector mechanisms in the lung. In primary infection in the lung, an ineffective response is mobilized although it primes the immune system for effective protection to challenge infection. During N. brasiliensis infection, parasites transit from the skin to the lung as early as 12 h after infection and only remain in the lung for about 2 d. Associated tissue damage likely triggers γδT cells to produce IL-17 that recruit neutrophils, including an immature population (iNeu), which in turn drive M2 macrophage activation through IL-13 production and ingestion of apoptotic cells. Other signals including surfactant protein D (Sp-D) also help drive M2 macrophage activation. Neutrophils rapidly surround invading parasites, but they pass relatively unimpeded to the small intestine. Within several days after primary infection, macrophages have largely cleared RBCs and debris from the lung, and recruited monocytes have differentiated into monocyte-derived alveolar macrophages (Mo-AvMs), with an M2 phenotype. On secondary infection, migrating parasites that were able to exit the skin and invade the lung are surrounded by Mo-AvMs, which produce high levels of Arg1, depleting local arginine around the parasite, thereby mediating killing through a nutrient deprivation mechanism. Little tissue damage or neutrophil infiltration occurs and eosinophils, as well as Mo-AvMs, surround the parasite. Most parasites are killed, largely preventing their entry into the intestine.CC BY · PubMed Central
Figure 3. Multiple mechanisms drive host protection to helminths in intestinal tissue. The type 2 response is likely initiated by tuft cell sensing of helminth excretory/secretory (ES) products in the lumen. This triggers tuft cell production of leukotrienes, which, combined with constitutive tuft cell IL-25 production, and also production of macrophage migration inhibitory factor (MIF) by unknown sources and neuromedin U (NMU), induces type 2 responses. Helminths that actually invade the epithelial barrier damage intestinal epithelial cells (IECs), which release ATP. Extracellular ATP, when degraded to ADP, can bind A2BAR, which activate IECs contributing to tuft cell hyperplasia and IL-33 production. ATP may also bind P2X7 on mast cells. Myeloid cells and ILC2s produce type 2 cytokines driving the response. As parasites cross the intestinal barrier, group 1b phospholipase A2 (Pla2g1b) binds the parasites, impairing their development. H. polygyrus larvae dwell in the submucosa as they develop into adults. After secondary inoculation, a rapidly developing granuloma, composed primarily of M2 macrophages, and also eosinophils, surrounds the parasite and impairs its development through Arg1-dependent mechanisms. Type 2 cytokines drive the type 2 granulomas while IFN-γ suppresses it. Helminths in the lumen may be expulsed through a combination of fluids flowing into the lumen, enhanced by activated mast cells, production of mucins (muc), and increased muscle contractility (weep-and-sweep response). Also, parasites, such as Trichuris, residing in the epithelial layer may be expulsed through upward IEC proliferation. M2 macrophages also mediate enteric disease tolerance mechanisms including neuronal protection.
Figure 3. Multiple mechanisms drive host protection to helminths in intestinal tissue. The type 2 response is likely initiated by tuft cell sensing of helminth excretory/secretory (ES) products in the lumen. This triggers tuft cell production of leukotrienes, which, combined with constitutive tuft cell IL-25 production, and also production of macrophage migration inhibitory factor (MIF) by unknown sources and neuromedin U (NMU), induces type 2 responses. Helminths that actually invade the epithelial barrier damage intestinal epithelial cells (IECs), which release ATP. Extracellular ATP, when degraded to ADP, can bind A2BAR, which activate IECs contributing to tuft cell hyperplasia and IL-33 production. ATP may also bind P2X7 on mast cells. Myeloid cells and ILC2s produce type 2 cytokines driving the response. As parasites cross the intestinal barrier, group 1b phospholipase A2 (Pla2g1b) binds the parasites, impairing their development. H. polygyrus larvae dwell in the submucosa as they develop into adults. After secondary inoculation, a rapidly developing granuloma, composed primarily of M2 macrophages, and also eosinophils, surrounds the parasite and impairs its development through Arg1-dependent mechanisms. Type 2 cytokines drive the type 2 granulomas while IFN-γ suppresses it. Helminths in the lumen may be expulsed through a combination of fluids flowing into the lumen, enhanced by activated mast cells, production of mucins (muc), and increased muscle contractility (weep-and-sweep response). Also, parasites, such as Trichuris, residing in the epithelial layer may be expulsed through upward IEC proliferation. M2 macrophages also mediate enteric disease tolerance mechanisms including neuronal protection.CC BY · PubMed Central

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Metadata

Authors
Maizels, R. M., & Gause, W. C.
Venue
Journal of Experimental Medicine
Publisher
Rockefeller University Press
Published
2023-08-28
Volume
220
Issue
10
ISSN
  • 0022-1007
  • 1540-9538
DOI
10.1084/jem.20221381
PMC
PMC10460967
Cited by
45
References
5
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
  • Wellcome Trust (219530, 104111)
  • Netherlands Lung Foundation (AWWA)
  • National Institutes of Health (R01DK113790, R01AI131634)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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