Retnla (Relmα/Fizz1) Suppresses Helminth-Induced Th2-Type Immunity

Pesce, John T.; Ramalingam, Thirumalai R.; Wilson, Mark S.; Mentink-Kane, Margaret M.; Thompson, Robert W.; Cheever, Allen W.; Urban, Joseph F.; Wynn, Thomas A.

doi:10.1371/journal.ppat.1000393

Cited by 213Parasites and Host InteractionsIL-33, ST2, and ILC PathwaysParasitic Diseases Research and Treatment

Retnla (Relmα/Fizz1) Suppresses Helminth-Induced Th2-Type Immunity

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Pesce, John T., Ramalingam, Thirumalai R., Wilson, Mark S., Mentink-Kane, Margaret M., Thompson, Robert W., Cheever, Allen W., Urban, Joseph F., Wynn, Thomas A.·2009·PLoS Pathogens

DOI 10.1371/journal.ppat.1000393PMC PMC2663845

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Abstract

Retnla (Resistin-like molecule alpha/FIZZ1) is induced during Th2 cytokine immune responses. However, the role of Retnla in Th2-type immunity is unknown. Here, using Retnla(-/-) mice and three distinct helminth models, we show that Retnla functions as a negative regulator of Th2 responses. Pulmonary granuloma formation induced by the eggs of the helminth parasite Schistosoma mansoni is dependent on IL-4 and IL-13 and associated with marked increases in Retnla expression. We found that both primary and secondary pulmonary granuloma formation were exacerbated in the absence of Retlna. The number of granuloma-associated eosinophils and serum IgE titers were also enhanced. Moreover, when chronically infected with S. mansoni cercariae, Retnla(-/-) mice displayed significant increases in granulomatous inflammation in the liver and the development of fibrosis and progression to hepatosplenic disease was markedly augmented. Finally, Retnla(-/-) mice infected with the gastrointestinal (GI) parasite Nippostrongylus brasiliensis had intensified lung pathology to migrating larvae, reduced fecundity, and accelerated expulsion of adult worms from the intestine, suggesting Th2 immunity was enhanced. When their immune responses were compared, helminth infected Retnla(-/-) mice developed stronger Th2 responses, which could be reversed by exogenous rRelmalpha treatment. Studies with several cytokine knockout mice showed that expression of Retnla was dependent on IL-4 and IL-13 and inhibited by IFN-gamma, while tissue localization and cell isolation experiments indicated that eosinophils and epithelial cells were the primary producers of Retnla in the liver and lung, respectively. Thus, the Th2-inducible gene Retnla suppresses resistance to GI nematode infection, pulmonary granulomatous inflammation, and fibrosis by negatively regulating Th2-dependent responses.

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Macrophages can also regulate or reverse fibrosis through secretion of matrix degrading MMPs and M2 factors (IL-10, RELMα, Arg-1) that suppress fibrosis.
“Macrophages, however, can also regulate or reverse fibrosis through the secretion of matrix degrading MMPs and other M2 factors that have been shown to suppress fibrosis (IL-10, RELMα, Arg-1) [102,138–140].”
From Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine (2012) · cites this paper as [139]

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[14]Sandler NG Mentink-Kane MM Cheever AW Wynn TA 2003 Global gene expression profiles during acute pathogen-induced pulmonary inflammation reveal divergent roles for Th1 and Th2 responses in tissue repair. J Immunol 171 3655 3667 14500663
[50]Mora AL Torres-Gonzalez E Rojas M Corredor C Ritzenthaler J 2006 Activation of alveolar macrophages via the alternative pathway in herpesvirus-induced lung fibrosis. Am J Respir Cell Mol Biol 35 466 473 16709958 PMC2643265
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Authors: Pesce, J. T., Ramalingam, T. R., Wilson, M. S., Mentink-Kane, M. M., Thompson, R. W., Cheever, A. W., Urban, J. F., & Wynn, T. A.
Affiliations: National Institutes of Health (US)
Biomedical Research Institute (US)
Agricultural Research Service (US)
Corresponding author: Wynn, Thomas A.
ORCID: Ramalingam, Thirumalai R.
Wilson, Mark S.
Urban, Joseph F.
Wynn, Thomas A.
Venue: PLoS Pathogens
Publisher: Public Library of Science (PLoS)
Published: 2009-04-17
Volume: 5
Issue: 4
Pages: e1000393
ISSN: 1553-7366 (ISSN-L)
1553-7374
DOI: 10.1371/journal.ppat.1000393
PMC: PMC2663845
OpenAlex: W2087869886
Cited by: 213
References: 53
Citations by year: 2026: 4 · 2025: 1 · 2024: 5 · 2023: 10 · 2022: 6 · 2021: 11 · 2020: 11 · 2019: 10 · 2018: 14 · 2017: 11 · 2016: 15 · 2015: 21 · 2014: 21 · 2013: 10 · 2012: 20
FWCI: 14.83
Type: journal article
Language: en
Open access: gold
doi.org
Licence: public-domain
creativecommons.org/publicdomain/zero/1.0/ (unspecified)
Locations: PLoS Pathogens (publishedVersion, public-domain)
PubMed Central (publishedVersion, public-domain)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: Regeneron Pharmaceuticals
National Institutes of Health
National Institute of Allergy and Infectious Diseases
Topics: Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
Keywords: Fizz1, Th2 immune response, helminthiasis, Schistosoma mansoni, Nippostrongylus brasiliensis, pulmonary granuloma, IL-4, IL-13, interferon-gamma, eosinophils, IgE, liver fibrosis, hepatosplenic schistosomiasis, intestinal nematode infection, granulomatous inflammation
MeSH terms: Animals, Eosinophils, Granuloma, Immunity, Innate, Interferon-gamma, Lung Diseases, Parasitic, Mice, Inbred C57BL, Nippostrongylus, Pulmonary Fibrosis, Schistosoma mansoni, Schistosomiasis mansoni, Interleukin-4, Strongylida Infections, Th2 Cells, Interleukin-13, Intercellular Signaling Peptides and Proteins, Mice

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Retnla (Relmα/Fizz1) Suppresses Helminth-Induced Th2-Type Immunity

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