Proximal colon-derived O-glycosylated mucus encapsulates and modulates the microbiota

Kirk Bergstrom; Xindi Shan; David Casero; Albert Batushansky; Venu Lagishetty; Jonathan P. Jacobs; Christopher Hoover; Yuji Kondo; Bojing Shao; Liang Gao; Wesley Zandberg; Benjamin Noyovitz; J. Michael McDaniel; Deanna L. Gibson; Sepideh Pakpour; Negin Kazemian; Samuel McGee; Courtney W. Houchen; Chinthalapally V. Rao; Timothy M. Griffin; Justin L. Sonnenburg; Rodger P. McEver; Jonathan Braun; Lijun Xia

doi:10.1126/science.aay7367

Proximal colon-derived O-glycosylated mucus encapsulates and modulates the microbiota

Kirk Bergstrom, Xindi Shan, David Casero, Albert Batushansky, Venu Lagishetty, Jonathan P. Jacobs, Christopher Hoover, Yuji Kondo, Bojing Shao, Liang Gao, Wesley Zandberg, Benjamin Noyovitz, J. Michael McDaniel, Deanna L. Gibson, Sepideh Pakpour, Negin Kazemian, Samuel McGee, Courtney W. Houchen, Chinthalapally V. Rao, Timothy M. GriffinJustin L. Sonnenburg, Rodger P. McEver, Jonathan Braun, Lijun Xia

Research output: Contribution to journal › Article › peer-review

133 Scopus citations

Abstract

Colon mucus segregates the intestinal microbiota from host tissues, but how it organizes to function throughout the colon is unclear. In mice, we found that colon mucus consists of two distinct O-glycosylated entities of Muc2: A major form produced by the proximal colon, which encapsulates the fecal material including the microbiota, and a minor form derived from the distal colon, which adheres to the major form. The microbiota directs its own encapsulation by inducing Muc2 production from proximal colon goblet cells. In turn, O-glycans on proximal colon-derived Muc2 modulate the structure and function of the microbiota as well as transcription in the colon mucosa. Our work shows how proximal colon control of mucin production is an important element in the regulation of host-microbiota symbiosis.

Original language	English
Article number	aay7367
Journal	Science
Volume	370
Issue number	6515
DOIs	https://doi.org/10.1126/science.aay7367
State	Published - 23 Oct 2020
Externally published	Yes

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Bergstrom, K., Shan, X., Casero, D., Batushansky, A., Lagishetty, V., Jacobs, J. P., Hoover, C., Kondo, Y., Shao, B., Gao, L., Zandberg, W., Noyovitz, B., Michael McDaniel, J., Gibson, D. L., Pakpour, S., Kazemian, N., McGee, S., Houchen, C. W., Rao, C. V., ... Xia, L. (2020). Proximal colon-derived O-glycosylated mucus encapsulates and modulates the microbiota. Science, 370(6515), Article aay7367. https://doi.org/10.1126/science.aay7367

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title = "Proximal colon-derived O-glycosylated mucus encapsulates and modulates the microbiota",

abstract = "Colon mucus segregates the intestinal microbiota from host tissues, but how it organizes to function throughout the colon is unclear. In mice, we found that colon mucus consists of two distinct O-glycosylated entities of Muc2: A major form produced by the proximal colon, which encapsulates the fecal material including the microbiota, and a minor form derived from the distal colon, which adheres to the major form. The microbiota directs its own encapsulation by inducing Muc2 production from proximal colon goblet cells. In turn, O-glycans on proximal colon-derived Muc2 modulate the structure and function of the microbiota as well as transcription in the colon mucosa. Our work shows how proximal colon control of mucin production is an important element in the regulation of host-microbiota symbiosis.",

author = "Kirk Bergstrom and Xindi Shan and David Casero and Albert Batushansky and Venu Lagishetty and Jacobs, {Jonathan P.} and Christopher Hoover and Yuji Kondo and Bojing Shao and Liang Gao and Wesley Zandberg and Benjamin Noyovitz and {Michael McDaniel}, J. and Gibson, {Deanna L.} and Sepideh Pakpour and Negin Kazemian and Samuel McGee and Houchen, {Courtney W.} and Rao, {Chinthalapally V.} and Griffin, {Timothy M.} and Sonnenburg, {Justin L.} and McEver, {Rodger P.} and Jonathan Braun and Lijun Xia",

year = "2020",

month = oct,

day = "23",

doi = "10.1126/science.aay7367",

language = "English",

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Bergstrom, K, Shan, X, Casero, D, Batushansky, A, Lagishetty, V, Jacobs, JP, Hoover, C, Kondo, Y, Shao, B, Gao, L, Zandberg, W, Noyovitz, B, Michael McDaniel, J, Gibson, DL, Pakpour, S, Kazemian, N, McGee, S, Houchen, CW, Rao, CV, Griffin, TM, Sonnenburg, JL, McEver, RP, Braun, J & Xia, L 2020, 'Proximal colon-derived O-glycosylated mucus encapsulates and modulates the microbiota', Science, vol. 370, no. 6515, aay7367. https://doi.org/10.1126/science.aay7367

TY - JOUR

T1 - Proximal colon-derived O-glycosylated mucus encapsulates and modulates the microbiota

AU - Bergstrom, Kirk

AU - Shan, Xindi

AU - Casero, David

AU - Batushansky, Albert

AU - Lagishetty, Venu

AU - Jacobs, Jonathan P.

AU - Hoover, Christopher

AU - Kondo, Yuji

AU - Shao, Bojing

AU - Gao, Liang

AU - Zandberg, Wesley

AU - Noyovitz, Benjamin

AU - Michael McDaniel, J.

AU - Gibson, Deanna L.

AU - Pakpour, Sepideh

AU - Kazemian, Negin

AU - McGee, Samuel

AU - Houchen, Courtney W.

AU - Rao, Chinthalapally V.

AU - Griffin, Timothy M.

AU - Sonnenburg, Justin L.

AU - McEver, Rodger P.

AU - Braun, Jonathan

AU - Xia, Lijun

PY - 2020/10/23

Y1 - 2020/10/23

N2 - Colon mucus segregates the intestinal microbiota from host tissues, but how it organizes to function throughout the colon is unclear. In mice, we found that colon mucus consists of two distinct O-glycosylated entities of Muc2: A major form produced by the proximal colon, which encapsulates the fecal material including the microbiota, and a minor form derived from the distal colon, which adheres to the major form. The microbiota directs its own encapsulation by inducing Muc2 production from proximal colon goblet cells. In turn, O-glycans on proximal colon-derived Muc2 modulate the structure and function of the microbiota as well as transcription in the colon mucosa. Our work shows how proximal colon control of mucin production is an important element in the regulation of host-microbiota symbiosis.

AB - Colon mucus segregates the intestinal microbiota from host tissues, but how it organizes to function throughout the colon is unclear. In mice, we found that colon mucus consists of two distinct O-glycosylated entities of Muc2: A major form produced by the proximal colon, which encapsulates the fecal material including the microbiota, and a minor form derived from the distal colon, which adheres to the major form. The microbiota directs its own encapsulation by inducing Muc2 production from proximal colon goblet cells. In turn, O-glycans on proximal colon-derived Muc2 modulate the structure and function of the microbiota as well as transcription in the colon mucosa. Our work shows how proximal colon control of mucin production is an important element in the regulation of host-microbiota symbiosis.

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VL - 370

JO - Science

JF - Science

IS - 6515

M1 - aay7367

ER -

Proximal colon-derived O-glycosylated mucus encapsulates and modulates the microbiota

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