NLRP6 Inflammasome Orchestrates the Colonic Host-Microbial Interface by Regulating Goblet Cell Mucus Secretion

Mucus production by goblet cells of the large intestine serves as a crucial antimicrobial protective mechanism at the interface between the eukaryotic and prokaryotic cells of the mammalian intestinal ecosystem. However, the regulatory pathways involved in goblet cell-induced mucus secretion remain...

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Published in	Cell Vol. 156; no. 5; pp. 1045 - 1059
Main Authors	Wlodarska, Marta, Thaiss, Christoph A., Nowarski, Roni, Henao-Mejia, Jorge, Zhang, Jian-Ping, Brown, Eric M., Frankel, Gad, Levy, Maayan, Katz, Meirav N., Philbrick, William M., Elinav, Eran, Finlay, B. Brett, Flavell, Richard A.
Format	Journal Article
Language	English
Published	United States Elsevier Inc 27.02.2014
Subjects	Animals Autophagy biogeography chronic diseases Colitis - immunology Colitis - microbiology Colon - immunology Colon - microbiology ecosystems enteropathogens Epithelial Cells - immunology Epithelial Cells - metabolism exocytosis goblet cells Goblet Cells - cytology Goblet Cells - immunology Inflammasomes - immunology intestinal microorganisms Intestinal Mucosa - cytology Intestinal Mucosa - immunology Intestinal Mucosa - metabolism large intestine Mice mucins mucus Mucus - metabolism mutualism prokaryotic cells Receptors, Cell Surface - immunology secretion
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Abstract	Mucus production by goblet cells of the large intestine serves as a crucial antimicrobial protective mechanism at the interface between the eukaryotic and prokaryotic cells of the mammalian intestinal ecosystem. However, the regulatory pathways involved in goblet cell-induced mucus secretion remain largely unknown. Here, we demonstrate that the NLRP6 inflammasome, a recently described regulator of colonic microbiota composition and biogeographical distribution, is a critical orchestrator of goblet cell mucin granule exocytosis. NLRP6 deficiency leads to defective autophagy in goblet cells and abrogated mucus secretion into the large intestinal lumen. Consequently, NLRP6 inflammasome-deficient mice are unable to clear enteric pathogens from the mucosal surface, rendering them highly susceptible to persistent infection. This study identifies an innate immune regulatory pathway governing goblet cell mucus secretion, linking nonhematopoietic inflammasome signaling to autophagy and highlighting the goblet cell as a critical innate immune player in the control of intestinal host-microbial mutualism. [Display omitted] [Display omitted] •The NLRP6 inflammasome is highly expressed in intestinal goblet cells•NLRP6 inflammasome regulates goblet cell mucus secretion•NLRP6 regulation of goblet cells is mediated through induction of autophagy•Altered NLRP6 signaling induces impaired mucus layer and susceptibility to infection Intestinal goblet cells secrete mucus and antimicrobial peptides to ward off pathogens, with the NLRP6 inflammasome, an immune sensor, being central to regulating mucus granule secretion.
AbstractList	Mucus production by goblet cells of the large intestine serves as a crucial anti microbial protective mechanism at the interface between the eukaryotic and prokaryotic cells of the mammalian intestinal ecosystem. However, the regulatory pathways involved in goblet cell-induced mucus secretion remain largely unknown. Here we demonstrate that the NLRP6 inflammasome, a recently described regulator of colonic microbiota composition and bio-geographical distribution, is a critical orchestrator of goblet cell mucin granule exocytosis. NLRP6 deficiency leads to defective autophagy in goblet cells and abrogated mucin secretion into the large intestinal lumen. Consequently, NLRP6 inflammasome-deficient mice are unable to clear enteric pathogens from the mucosal surface, rendering them highly susceptible to persistent infection. This study identifies the first innate immune regulatory pathway governing goblet cell mucus secretion, linking non-hematopoietic inflammasome signaling to autophagy and highlighting the goblet cell as a critical innate immune player in the control of intestinal host-microbial mutualism. Mucus production by goblet cells of the large intestine serves as a crucial antimicrobial protective mechanism at the interface between the eukaryotic and prokaryotic cells of the mammalian intestinal ecosystem. However, the regulatory pathways involved in goblet cell-induced mucus secretion remain largely unknown. Here, we demonstrate that the NLRP6 inflammasome, a recently described regulator of colonic microbiota composition and biogeographical distribution, is a critical orchestrator of goblet cell mucin granule exocytosis. NLRP6 deficiency leads to defective autophagy in goblet cells and abrogated mucus secretion into the large intestinal lumen. Consequently, NLRP6 inflammasome-deficient mice are unable to clear enteric pathogens from the mucosal surface, rendering them highly susceptible to persistent infection. This study identifies an innate immune regulatory pathway governing goblet cell mucus secretion, linking nonhematopoietic inflammasome signaling to autophagy and highlighting the goblet cell as a critical innate immune player in the control of intestinal host-microbial mutualism.[Display omitted] Mucus production by goblet cells of the large intestine serves as a crucial antimicrobial protective mechanism at the interface between the eukaryotic and prokaryotic cells of the mammalian intestinal ecosystem. However, the regulatory pathways involved in goblet cell-induced mucus secretion remain largely unknown. Here, we demonstrate that the NLRP6 inflammasome, a recently described regulator of colonic microbiota composition and biogeographical distribution, is a critical orchestrator of goblet cell mucin granule exocytosis. NLRP6 deficiency leads to defective autophagy in goblet cells and abrogated mucus secretion into the large intestinal lumen. Consequently, NLRP6 inflammasome-deficient mice are unable to clear enteric pathogens from the mucosal surface, rendering them highly susceptible to persistent infection. This study identifies an innate immune regulatory pathway governing goblet cell mucus secretion, linking nonhematopoietic inflammasome signaling to autophagy and highlighting the goblet cell as a critical innate immune player in the control of intestinal host-microbial mutualism. [Display omitted] [Display omitted] •The NLRP6 inflammasome is highly expressed in intestinal goblet cells•NLRP6 inflammasome regulates goblet cell mucus secretion•NLRP6 regulation of goblet cells is mediated through induction of autophagy•Altered NLRP6 signaling induces impaired mucus layer and susceptibility to infection Intestinal goblet cells secrete mucus and antimicrobial peptides to ward off pathogens, with the NLRP6 inflammasome, an immune sensor, being central to regulating mucus granule secretion. Mucus production by goblet cells of the large intestine serves as a crucial antimicrobial protective mechanism at the interface between the eukaryotic and prokaryotic cells of the mammalian intestinal ecosystem. However, the regulatory pathways involved in goblet cell-induced mucus secretion remain largely unknown. Here, we demonstrate that the NLRP6 inflammasome, a recently described regulator of colonic microbiota composition and biogeographical distribution, is a critical orchestrator of goblet cell mucin granule exocytosis. NLRP6 deficiency leads to defective autophagy in goblet cells and abrogated mucus secretion into the large intestinal lumen. Consequently, NLRP6 inflammasome-deficient mice are unable to clear enteric pathogens from the mucosal surface, rendering them highly susceptible to persistent infection. This study identifies an innate immune regulatory pathway governing goblet cell mucus secretion, linking nonhematopoietic inflammasome signaling to autophagy and highlighting the goblet cell as a critical innate immune player in the control of intestinal host-microbial mutualism. PAPERCLIP: Summary Mucus production by goblet cells of the large intestine serves as a crucial antimicrobial protective mechanism at the interface between the eukaryotic and prokaryotic cells of the mammalian intestinal ecosystem. However, the regulatory pathways involved in goblet cell-induced mucus secretion remain largely unknown. Here, we demonstrate that the NLRP6 inflammasome, a recently described regulator of colonic microbiota composition and biogeographical distribution, is a critical orchestrator of goblet cell mucin granule exocytosis. NLRP6 deficiency leads to defective autophagy in goblet cells and abrogated mucus secretion into the large intestinal lumen. Consequently, NLRP6 inflammasome-deficient mice are unable to clear enteric pathogens from the mucosal surface, rendering them highly susceptible to persistent infection. This study identifies an innate immune regulatory pathway governing goblet cell mucus secretion, linking nonhematopoietic inflammasome signaling to autophagy and highlighting the goblet cell as a critical innate immune player in the control of intestinal host-microbial mutualism. PaperClip Help with MP3 files Options Mucus production by goblet cells of the large intestine serves as a crucial antimicrobial protective mechanism at the interface between the eukaryotic and prokaryotic cells of the mammalian intestinal ecosystem. However, the regulatory pathways involved in goblet cell-induced mucus secretion remain largely unknown. Here, we demonstrate that the NLRP6 inflammasome, a recently described regulator of colonic microbiota composition and biogeographical distribution, is a critical orchestrator of goblet cell mucin granule exocytosis. NLRP6 deficiency leads to defective autophagy in goblet cells and abrogated mucus secretion into the large intestinal lumen. Consequently, NLRP6 inflammasome-deficient mice are unable to clear enteric pathogens from the mucosal surface, rendering them highly susceptible to persistent infection. This study identifies an innate immune regulatory pathway governing goblet cell mucus secretion, linking nonhematopoietic inflammasome signaling to autophagy and highlighting the goblet cell as a critical innate immune player in the control of intestinal host-microbial mutualism. PAPERCLIP:Mucus production by goblet cells of the large intestine serves as a crucial antimicrobial protective mechanism at the interface between the eukaryotic and prokaryotic cells of the mammalian intestinal ecosystem. However, the regulatory pathways involved in goblet cell-induced mucus secretion remain largely unknown. Here, we demonstrate that the NLRP6 inflammasome, a recently described regulator of colonic microbiota composition and biogeographical distribution, is a critical orchestrator of goblet cell mucin granule exocytosis. NLRP6 deficiency leads to defective autophagy in goblet cells and abrogated mucus secretion into the large intestinal lumen. Consequently, NLRP6 inflammasome-deficient mice are unable to clear enteric pathogens from the mucosal surface, rendering them highly susceptible to persistent infection. This study identifies an innate immune regulatory pathway governing goblet cell mucus secretion, linking nonhematopoietic inflammasome signaling to autophagy and highlighting the goblet cell as a critical innate immune player in the control of intestinal host-microbial mutualism. PAPERCLIP:
Author	Philbrick, William M. Elinav, Eran Henao-Mejia, Jorge Levy, Maayan Flavell, Richard A. Nowarski, Roni Wlodarska, Marta Brown, Eric M. Thaiss, Christoph A. Finlay, B. Brett Frankel, Gad Katz, Meirav N. Zhang, Jian-Ping
AuthorAffiliation	8 Department of Biochemistry and Molecular Biology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada 1 Michael Smith Laboratories, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada 4 Department of Immunobiology, Yale University School of Medicine, New Haven, CT 06520, USA 7 Research Center for digestive tract and liver diseases, Tel Aviv Sourasky Medical Center, Sackler faculty of Medicine, Tel Aviv University, Tel Aviv, 64239, Israel 9 Howard Hughes Medical Institute 3 Immunology Department, Weizmann Institute of Science, Rehovot 76100, Israel 6 MRC Center for Molecular Bacteriology and Infection, Department of Life Sciences, Flowers Building, Imperial College, London, SW7 2AZ, UK 5 Center on Endocrinology and Metabolism, Yale University School of Medicine, New Haven, CT 06520, USA 2 Department of Microbiology and Immunology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada
AuthorAffiliation_xml	– name: 1 Michael Smith Laboratories, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada – name: 2 Department of Microbiology and Immunology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada – name: 3 Immunology Department, Weizmann Institute of Science, Rehovot 76100, Israel – name: 7 Research Center for digestive tract and liver diseases, Tel Aviv Sourasky Medical Center, Sackler faculty of Medicine, Tel Aviv University, Tel Aviv, 64239, Israel – name: 9 Howard Hughes Medical Institute – name: 5 Center on Endocrinology and Metabolism, Yale University School of Medicine, New Haven, CT 06520, USA – name: 6 MRC Center for Molecular Bacteriology and Infection, Department of Life Sciences, Flowers Building, Imperial College, London, SW7 2AZ, UK – name: 8 Department of Biochemistry and Molecular Biology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada – name: 4 Department of Immunobiology, Yale University School of Medicine, New Haven, CT 06520, USA
Author_xml	– sequence: 1 givenname: Marta surname: Wlodarska fullname: Wlodarska, Marta organization: Michael Smith Laboratories, The University of British Columbia, Vancouver, BC V6T 1Z4, Canada – sequence: 2 givenname: Christoph A. surname: Thaiss fullname: Thaiss, Christoph A. organization: Immunology Department, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 3 givenname: Roni surname: Nowarski fullname: Nowarski, Roni organization: Department of Immunobiology, Yale University School of Medicine, New Haven, CT 06520, USA – sequence: 4 givenname: Jorge surname: Henao-Mejia fullname: Henao-Mejia, Jorge organization: Department of Immunobiology, Yale University School of Medicine, New Haven, CT 06520, USA – sequence: 5 givenname: Jian-Ping surname: Zhang fullname: Zhang, Jian-Ping organization: Center on Endocrinology and Metabolism, Yale University School of Medicine, New Haven, CT 06520, USA – sequence: 6 givenname: Eric M. surname: Brown fullname: Brown, Eric M. organization: Michael Smith Laboratories, The University of British Columbia, Vancouver, BC V6T 1Z4, Canada – sequence: 7 givenname: Gad surname: Frankel fullname: Frankel, Gad organization: MRC Center for Molecular Bacteriology and Infection, Department of Life Sciences, Flowers Building, Imperial College, London SW7 2AZ, UK – sequence: 8 givenname: Maayan surname: Levy fullname: Levy, Maayan organization: Immunology Department, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 9 givenname: Meirav N. surname: Katz fullname: Katz, Meirav N. organization: Immunology Department, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 10 givenname: William M. surname: Philbrick fullname: Philbrick, William M. organization: Center on Endocrinology and Metabolism, Yale University School of Medicine, New Haven, CT 06520, USA – sequence: 11 givenname: Eran surname: Elinav fullname: Elinav, Eran email: eran.elinav@weizmann.ac.il organization: Immunology Department, Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 12 givenname: B. Brett surname: Finlay fullname: Finlay, B. Brett email: bfinlay@interchange.ubc.ca organization: Michael Smith Laboratories, The University of British Columbia, Vancouver, BC V6T 1Z4, Canada – sequence: 13 givenname: Richard A. surname: Flavell fullname: Flavell, Richard A. email: richard.flavell@yale.edu organization: Department of Immunobiology, Yale University School of Medicine, New Haven, CT 06520, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/24581500$$D View this record in MEDLINE/PubMed
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Snippet	Mucus production by goblet cells of the large intestine serves as a crucial antimicrobial protective mechanism at the interface between the eukaryotic and... Mucus production by goblet cells of the large intestine serves as a crucial antimicrobial protective mechanism at the interface between the eukaryotic and... Summary Mucus production by goblet cells of the large intestine serves as a crucial antimicrobial protective mechanism at the interface between the eukaryotic... Mucus production by goblet cells of the large intestine serves as a crucial anti microbial protective mechanism at the interface between the eukaryotic and...
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SubjectTerms	Animals Autophagy biogeography chronic diseases Colitis - immunology Colitis - microbiology Colon - immunology Colon - microbiology ecosystems enteropathogens Epithelial Cells - immunology Epithelial Cells - metabolism exocytosis goblet cells Goblet Cells - cytology Goblet Cells - immunology Inflammasomes - immunology intestinal microorganisms Intestinal Mucosa - cytology Intestinal Mucosa - immunology Intestinal Mucosa - metabolism large intestine Mice mucins mucus Mucus - metabolism mutualism prokaryotic cells Receptors, Cell Surface - immunology secretion
Title	NLRP6 Inflammasome Orchestrates the Colonic Host-Microbial Interface by Regulating Goblet Cell Mucus Secretion
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