Physiological microbial exposure transiently inhibits mouse lung ILC2 responses to allergens

Katharine E. Block; Koji Iijima; Mark J. Pierson; Daniel A. Walsh; Rinna Tei; Tamara A. Kucaba; Julie Xu; Mohammad Haneef Khan; Christopher Staley; Thomas S. Griffith; Henry J. McSorley; Hirohito Kita; Stephen C. Jameson

doi:10.1038/s41590-022-01350-8

Physiological microbial exposure transiently inhibits mouse lung ILC2 responses to allergens

Katharine E. Block, Koji Iijima, Mark J. Pierson, Daniel A. Walsh, Rinna Tei, Tamara A. Kucaba, Julie Xu, Mohammad Haneef Khan, Christopher Staley, Thomas S. Griffith, Henry J. McSorley, Hirohito Kita, Stephen C. Jameson

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Abstract

Lung group 2 innate lymphoid cells (ILC2s) control the nature of immune responses to airway allergens. Some microbial products, including those that stimulate interferons, block ILC2 activation, but whether this occurs after natural infections or causes durable ILC2 inhibition is unclear. In the present study, we cohoused laboratory and pet store mice as a model of physiological microbial exposure. Laboratory mice cohoused for 2 weeks had impaired ILC2 responses and reduced lung eosinophilia to intranasal allergens, whereas these responses were restored in mice cohoused for ≥2 months. ILC2 inhibition at 2 weeks correlated with increased interferon receptor signaling, which waned by 2 months of cohousing. Reinduction of interferons in 2-month cohoused mice blocked ILC2 activation. These findings suggest that ILC2s respond dynamically to environmental cues and that microbial exposures do not control long-term desensitization of innate type 2 responses to allergens.

Original language	English (US)
Pages (from-to)	1703-1713
Number of pages	11
Journal	Nature immunology
Volume	23
Issue number	12
DOIs	https://doi.org/10.1038/s41590-022-01350-8
State	Published - Dec 2022

Bibliographical note

Funding Information:
We thank UMN Flow Cytometry Resource Facility, CFI Dirty Mouse Colony, UMN BSL-3 Program, Minnesota Supercomputing Institute, Cytokine Reference Laboratory and UMN Research Animal Resources for support. We thank Jamequist and Kita lab members for thoughtful discussion. This work was supported by the NIH (grant nos. R01HL117823 to H.K., T32HL007741 to K.E.B. and R35GM140881 to T.S.G.), Minnesota Partnership for Biotechnology and Medical Genomics (grant no. 16.48 to S.C.J. and H.K.) and UMN Medical School (grant no. AIRP-CP-21 to S.C.J.).

Funding Information:
We thank UMN Flow Cytometry Resource Facility, CFI Dirty Mouse Colony, UMN BSL-3 Program, Minnesota Supercomputing Institute, Cytokine Reference Laboratory and UMN Research Animal Resources for support. We thank Jamequist and Kita lab members for thoughtful discussion. This work was supported by the NIH (grant nos. R01HL117823 to H.K., T32HL007741 to K.E.B. and R35GM140881 to T.S.G.), Minnesota Partnership for Biotechnology and Medical Genomics (grant no. 16.48 to S.C.J. and H.K.) and UMN Medical School (grant no. AIRP-CP-21 to S.C.J.).

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© 2022, The Author(s), under exclusive licence to Springer Nature America, Inc.

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Research Support, Non-U.S. Gov't

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title = "Physiological microbial exposure transiently inhibits mouse lung ILC2 responses to allergens",

abstract = "Lung group 2 innate lymphoid cells (ILC2s) control the nature of immune responses to airway allergens. Some microbial products, including those that stimulate interferons, block ILC2 activation, but whether this occurs after natural infections or causes durable ILC2 inhibition is unclear. In the present study, we cohoused laboratory and pet store mice as a model of physiological microbial exposure. Laboratory mice cohoused for 2 weeks had impaired ILC2 responses and reduced lung eosinophilia to intranasal allergens, whereas these responses were restored in mice cohoused for ≥2 months. ILC2 inhibition at 2 weeks correlated with increased interferon receptor signaling, which waned by 2 months of cohousing. Reinduction of interferons in 2-month cohoused mice blocked ILC2 activation. These findings suggest that ILC2s respond dynamically to environmental cues and that microbial exposures do not control long-term desensitization of innate type 2 responses to allergens.",

author = "Block, {Katharine E.} and Koji Iijima and Pierson, {Mark J.} and Walsh, {Daniel A.} and Rinna Tei and Kucaba, {Tamara A.} and Julie Xu and Khan, {Mohammad Haneef} and Christopher Staley and Griffith, {Thomas S.} and McSorley, {Henry J.} and Hirohito Kita and Jameson, {Stephen C.}",

note = "Funding Information: We thank UMN Flow Cytometry Resource Facility, CFI Dirty Mouse Colony, UMN BSL-3 Program, Minnesota Supercomputing Institute, Cytokine Reference Laboratory and UMN Research Animal Resources for support. We thank Jamequist and Kita lab members for thoughtful discussion. This work was supported by the NIH (grant nos. R01HL117823 to H.K., T32HL007741 to K.E.B. and R35GM140881 to T.S.G.), Minnesota Partnership for Biotechnology and Medical Genomics (grant no. 16.48 to S.C.J. and H.K.) and UMN Medical School (grant no. AIRP-CP-21 to S.C.J.). Funding Information: We thank UMN Flow Cytometry Resource Facility, CFI Dirty Mouse Colony, UMN BSL-3 Program, Minnesota Supercomputing Institute, Cytokine Reference Laboratory and UMN Research Animal Resources for support. We thank Jamequist and Kita lab members for thoughtful discussion. This work was supported by the NIH (grant nos. R01HL117823 to H.K., T32HL007741 to K.E.B. and R35GM140881 to T.S.G.), Minnesota Partnership for Biotechnology and Medical Genomics (grant no. 16.48 to S.C.J. and H.K.) and UMN Medical School (grant no. AIRP-CP-21 to S.C.J.). Publisher Copyright: {\textcopyright} 2022, The Author(s), under exclusive licence to Springer Nature America, Inc.",

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AU - Block, Katharine E.

AU - Iijima, Koji

AU - Pierson, Mark J.

AU - Walsh, Daniel A.

AU - Tei, Rinna

AU - Kucaba, Tamara A.

AU - Xu, Julie

AU - Khan, Mohammad Haneef

AU - Staley, Christopher

AU - Griffith, Thomas S.

AU - McSorley, Henry J.

AU - Kita, Hirohito

AU - Jameson, Stephen C.

N1 - Funding Information: We thank UMN Flow Cytometry Resource Facility, CFI Dirty Mouse Colony, UMN BSL-3 Program, Minnesota Supercomputing Institute, Cytokine Reference Laboratory and UMN Research Animal Resources for support. We thank Jamequist and Kita lab members for thoughtful discussion. This work was supported by the NIH (grant nos. R01HL117823 to H.K., T32HL007741 to K.E.B. and R35GM140881 to T.S.G.), Minnesota Partnership for Biotechnology and Medical Genomics (grant no. 16.48 to S.C.J. and H.K.) and UMN Medical School (grant no. AIRP-CP-21 to S.C.J.). Funding Information: We thank UMN Flow Cytometry Resource Facility, CFI Dirty Mouse Colony, UMN BSL-3 Program, Minnesota Supercomputing Institute, Cytokine Reference Laboratory and UMN Research Animal Resources for support. We thank Jamequist and Kita lab members for thoughtful discussion. This work was supported by the NIH (grant nos. R01HL117823 to H.K., T32HL007741 to K.E.B. and R35GM140881 to T.S.G.), Minnesota Partnership for Biotechnology and Medical Genomics (grant no. 16.48 to S.C.J. and H.K.) and UMN Medical School (grant no. AIRP-CP-21 to S.C.J.). Publisher Copyright: © 2022, The Author(s), under exclusive licence to Springer Nature America, Inc.

PY - 2022/12

Y1 - 2022/12

N2 - Lung group 2 innate lymphoid cells (ILC2s) control the nature of immune responses to airway allergens. Some microbial products, including those that stimulate interferons, block ILC2 activation, but whether this occurs after natural infections or causes durable ILC2 inhibition is unclear. In the present study, we cohoused laboratory and pet store mice as a model of physiological microbial exposure. Laboratory mice cohoused for 2 weeks had impaired ILC2 responses and reduced lung eosinophilia to intranasal allergens, whereas these responses were restored in mice cohoused for ≥2 months. ILC2 inhibition at 2 weeks correlated with increased interferon receptor signaling, which waned by 2 months of cohousing. Reinduction of interferons in 2-month cohoused mice blocked ILC2 activation. These findings suggest that ILC2s respond dynamically to environmental cues and that microbial exposures do not control long-term desensitization of innate type 2 responses to allergens.

AB - Lung group 2 innate lymphoid cells (ILC2s) control the nature of immune responses to airway allergens. Some microbial products, including those that stimulate interferons, block ILC2 activation, but whether this occurs after natural infections or causes durable ILC2 inhibition is unclear. In the present study, we cohoused laboratory and pet store mice as a model of physiological microbial exposure. Laboratory mice cohoused for 2 weeks had impaired ILC2 responses and reduced lung eosinophilia to intranasal allergens, whereas these responses were restored in mice cohoused for ≥2 months. ILC2 inhibition at 2 weeks correlated with increased interferon receptor signaling, which waned by 2 months of cohousing. Reinduction of interferons in 2-month cohoused mice blocked ILC2 activation. These findings suggest that ILC2s respond dynamically to environmental cues and that microbial exposures do not control long-term desensitization of innate type 2 responses to allergens.

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JF - Nature immunology

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ER -

Physiological microbial exposure transiently inhibits mouse lung ILC2 responses to allergens

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