Serum amyloid A is a soluble pattern recognition receptor that drives type 2 immunity

Ursula Smole; Naina Gour; Jordan Phelan; Gerhard Hofer; Cordula Köhler; Bernhard Kratzer; Peter A. Tauber; Xiao Xiao; Nu Yao; Jan Dvorak; Luis Caraballo; Leonardo Puerta; Sandra Rosskopf; Jamila Chakir; Ernst Malle; Andrew P. Lane; Winfried F. Pickl; Stephane Lajoie; Marsha Wills-Karp

doi:10.1038/s41590-020-0698-1

Serum amyloid A is a soluble pattern recognition receptor that drives type 2 immunity

Ursula Smole, Naina Gour, Jordan Phelan, Gerhard Hofer, Cordula Köhler, Bernhard Kratzer, Peter A. Tauber, Xiao Xiao, Nu Yao, Jan Dvorak, Luis Caraballo, Leonardo Puerta, Sandra Rosskopf, Jamila Chakir, Ernst Malle, Andrew P. Lane, Winfried F. Pickl, Stephane Lajoie, Marsha Wills-Karp

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14 Scopus citations

Abstract

The molecular basis for the propensity of a small number of environmental proteins to provoke allergic responses is largely unknown. Herein, we report that mite group 13 allergens of the fatty acid-binding protein (FABP) family are sensed by an evolutionarily conserved acute-phase protein, serum amyloid A1 (SAA1), that promotes pulmonary type 2 immunity. Mechanistically, SAA1 interacted directly with allergenic mite FABPs (Der p 13 and Blo t 13). The interaction between mite FABPs and SAA1 activated the SAA1-binding receptor, formyl peptide receptor 2 (FPR2), which drove the epithelial release of the type-2-promoting cytokine interleukin (IL)-33 in a SAA1-dependent manner. Importantly, the SAA1–FPR2–IL-33 axis was upregulated in nasal epithelial cells from patients with chronic rhinosinusitis. These findings identify an unrecognized role for SAA1 as a soluble pattern recognition receptor for conserved FABPs found in common mite allergens that initiate type 2 immunity at mucosal surfaces.

Original language	English (US)
Pages (from-to)	756-765
Number of pages	10
Journal	Nature Immunology
Volume	21
Issue number	7
DOIs	https://doi.org/10.1038/s41590-020-0698-1
State	Published - Jul 1 2020

ASJC Scopus subject areas

Immunology and Allergy
Immunology

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Smole, U., Gour, N., Phelan, J., Hofer, G., Köhler, C., Kratzer, B., Tauber, P. A., Xiao, X., Yao, N., Dvorak, J., Caraballo, L., Puerta, L., Rosskopf, S., Chakir, J., Malle, E., Lane, A. P., Pickl, W. F., Lajoie, S., & Wills-Karp, M. (2020). Serum amyloid A is a soluble pattern recognition receptor that drives type 2 immunity. Nature Immunology, 21(7), 756-765. https://doi.org/10.1038/s41590-020-0698-1

Smole, U, Gour, N, Phelan, J, Hofer, G, Köhler, C, Kratzer, B, Tauber, PA, Xiao, X, Yao, N, Dvorak, J, Caraballo, L, Puerta, L, Rosskopf, S, Chakir, J, Malle, E, Lane, AP, Pickl, WF, Lajoie, S & Wills-Karp, M 2020, 'Serum amyloid A is a soluble pattern recognition receptor that drives type 2 immunity', Nature Immunology, vol. 21, no. 7, pp. 756-765. https://doi.org/10.1038/s41590-020-0698-1

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abstract = "The molecular basis for the propensity of a small number of environmental proteins to provoke allergic responses is largely unknown. Herein, we report that mite group 13 allergens of the fatty acid-binding protein (FABP) family are sensed by an evolutionarily conserved acute-phase protein, serum amyloid A1 (SAA1), that promotes pulmonary type 2 immunity. Mechanistically, SAA1 interacted directly with allergenic mite FABPs (Der p 13 and Blo t 13). The interaction between mite FABPs and SAA1 activated the SAA1-binding receptor, formyl peptide receptor 2 (FPR2), which drove the epithelial release of the type-2-promoting cytokine interleukin (IL)-33 in a SAA1-dependent manner. Importantly, the SAA1–FPR2–IL-33 axis was upregulated in nasal epithelial cells from patients with chronic rhinosinusitis. These findings identify an unrecognized role for SAA1 as a soluble pattern recognition receptor for conserved FABPs found in common mite allergens that initiate type 2 immunity at mucosal surfaces.",

author = "Ursula Smole and Naina Gour and Jordan Phelan and Gerhard Hofer and Cordula K{\"o}hler and Bernhard Kratzer and Tauber, {Peter A.} and Xiao Xiao and Nu Yao and Jan Dvorak and Luis Caraballo and Leonardo Puerta and Sandra Rosskopf and Jamila Chakir and Ernst Malle and Lane, {Andrew P.} and Pickl, {Winfried F.} and Stephane Lajoie and Marsha Wills-Karp",

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AU - Smole, Ursula

AU - Gour, Naina

AU - Phelan, Jordan

AU - Hofer, Gerhard

AU - Köhler, Cordula

AU - Kratzer, Bernhard

AU - Tauber, Peter A.

AU - Xiao, Xiao

AU - Yao, Nu

AU - Dvorak, Jan

AU - Caraballo, Luis

AU - Puerta, Leonardo

AU - Rosskopf, Sandra

AU - Chakir, Jamila

AU - Malle, Ernst

AU - Lane, Andrew P.

AU - Pickl, Winfried F.

AU - Lajoie, Stephane

AU - Wills-Karp, Marsha

PY - 2020/7/1

Y1 - 2020/7/1

N2 - The molecular basis for the propensity of a small number of environmental proteins to provoke allergic responses is largely unknown. Herein, we report that mite group 13 allergens of the fatty acid-binding protein (FABP) family are sensed by an evolutionarily conserved acute-phase protein, serum amyloid A1 (SAA1), that promotes pulmonary type 2 immunity. Mechanistically, SAA1 interacted directly with allergenic mite FABPs (Der p 13 and Blo t 13). The interaction between mite FABPs and SAA1 activated the SAA1-binding receptor, formyl peptide receptor 2 (FPR2), which drove the epithelial release of the type-2-promoting cytokine interleukin (IL)-33 in a SAA1-dependent manner. Importantly, the SAA1–FPR2–IL-33 axis was upregulated in nasal epithelial cells from patients with chronic rhinosinusitis. These findings identify an unrecognized role for SAA1 as a soluble pattern recognition receptor for conserved FABPs found in common mite allergens that initiate type 2 immunity at mucosal surfaces.

AB - The molecular basis for the propensity of a small number of environmental proteins to provoke allergic responses is largely unknown. Herein, we report that mite group 13 allergens of the fatty acid-binding protein (FABP) family are sensed by an evolutionarily conserved acute-phase protein, serum amyloid A1 (SAA1), that promotes pulmonary type 2 immunity. Mechanistically, SAA1 interacted directly with allergenic mite FABPs (Der p 13 and Blo t 13). The interaction between mite FABPs and SAA1 activated the SAA1-binding receptor, formyl peptide receptor 2 (FPR2), which drove the epithelial release of the type-2-promoting cytokine interleukin (IL)-33 in a SAA1-dependent manner. Importantly, the SAA1–FPR2–IL-33 axis was upregulated in nasal epithelial cells from patients with chronic rhinosinusitis. These findings identify an unrecognized role for SAA1 as a soluble pattern recognition receptor for conserved FABPs found in common mite allergens that initiate type 2 immunity at mucosal surfaces.

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Serum amyloid A is a soluble pattern recognition receptor that drives type 2 immunity

Abstract

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