B cell expansion hinders the stroma-epithelium regenerative cross talk during mucosal healing

Therapeutic promotion of intestinal regeneration holds great promise, but defining the cellular mechanisms that influence tissue regeneration remains an unmet challenge. To gain insight into the process of mucosal healing, we longitudinally examined the immune cell composition during intestinal dama...

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Published inImmunity (Cambridge, Mass.) Vol. 55; no. 12; pp. 2336 - 2351.e12
Main Authors Frede, Annika, Czarnewski, Paulo, Monasterio, Gustavo, Tripathi, Kumar P., Bejarano, David A., Ramirez Flores, Ricardo O., Sorini, Chiara, Larsson, Ludvig, Luo, Xinxin, Geerlings, Laura, Novella-Rausell, Claudio, Zagami, Chiara, Kuiper, Raoul, Morales, Rodrigo A., Castillo, Francisca, Hunt, Matthew, Mariano, Livia Lacerda, Hu, Yue O.O., Engblom, Camilla, Lennon-Duménil, Ana-Maria, Mittenzwei, Romy, Westendorf, Astrid M., Hövelmeyer, Nadine, Lundeberg, Joakim, Saez-Rodriguez, Julio, Schlitzer, Andreas, Das, Srustidhar, Villablanca, Eduardo J.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 13.12.2022
Subjects
Animals
B cell
Colitis
Disease Models, Animal
Epithelial Cells - metabolism
Epithelium
fibroblasts
inflammation
Intestinal Mucosa
mucosal healing
organoids
single cell
spatial transcriptomics
stromal cell
tissue repair
Wound Healing
stromal cell
B cell
single cell
fibroblasts
inflammation
spatial transcriptomics
organoids
epithelium
tissue repair
mucosal healing
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Abstract Therapeutic promotion of intestinal regeneration holds great promise, but defining the cellular mechanisms that influence tissue regeneration remains an unmet challenge. To gain insight into the process of mucosal healing, we longitudinally examined the immune cell composition during intestinal damage and regeneration. B cells were the dominant cell type in the healing colon, and single-cell RNA sequencing (scRNA-seq) revealed expansion of an IFN-induced B cell subset during experimental mucosal healing that predominantly located in damaged areas and associated with colitis severity. B cell depletion accelerated recovery upon injury, decreased epithelial ulceration, and enhanced gene expression programs associated with tissue remodeling. scRNA-seq from the epithelial and stromal compartments combined with spatial transcriptomics and multiplex immunostaining showed that B cells decreased interactions between stromal and epithelial cells during mucosal healing. Activated B cells disrupted the epithelial-stromal cross talk required for organoid survival. Thus, B cell expansion during injury impairs epithelial-stromal cell interactions required for mucosal healing, with implications for the treatment of IBD. [Display omitted] •B cells are the dominant immune cell type during colonic mucosal healing (MH)•IFN-induced B cells are associated with injury and expand during MH•B cell depletion results in enhanced MH following intestinal injury•B cells impair the interactions between IEC and stromal cells during MH The cellular mechanisms controlling mucosal healing (MH) following injury are largely unknown. Using unbiased multi-parameter analysis, Frede and colleagues identified that B cells accumulate in the colonic damaged areas during MH. Surprisingly, B cells played detrimental roles during MH, as their presence hindered the interaction between epithelium and stroma.
AbstractList Therapeutic promotion of intestinal regeneration holds great promise, but defining the cellular mechanisms that influence tissue regeneration remains an unmet challenge. To gain insight into the process of mucosal healing, we longitudinally examined the immune cell composition during intestinal damage and regeneration. B cells were the dominant cell type in the healing colon, and single-cell RNA sequencing (scRNA-seq) revealed expansion of an IFN-induced B cell subset during experimental mucosal healing that predominantly located in damaged areas and associated with colitis severity. B cell depletion accelerated recovery upon injury, decreased epithelial ulceration, and enhanced gene expression programs associated with tissue remodeling. scRNA-seq from the epithelial and stromal compartments combined with spatial transcriptomics and multiplex immunostaining showed that B cells decreased interactions between stromal and epithelial cells during mucosal healing. Activated B cells disrupted the epithelial-stromal cross talk required for organoid survival. Thus, B cell expansion during injury impairs epithelial-stromal cell interactions required for mucosal healing, with implications for the treatment of IBD.
Therapeutic promotion of intestinal regeneration holds great promise, but defining the cellular mechanisms that influence tissue regeneration remains an unmet challenge. To gain insight into the process of mucosal healing, we longitudinally examined the immune cell composition during intestinal damage and regeneration. B cells were the dominant cell type in the healing colon, and single-cell RNA sequencing (scRNA-seq) revealed expansion of an IFN-induced B cell subset during experimental mucosal healing that predominantly located in damaged areas and associated with colitis severity. B cell depletion accelerated recovery upon injury, decreased epithelial ulceration, and enhanced gene expression programs associated with tissue remodeling. scRNA-seq from the epithelial and stromal compartments combined with spatial transcriptomics and multiplex immunostaining showed that B cells decreased interactions between stromal and epithelial cells during mucosal healing. Activated B cells disrupted the epithelial-stromal cross talk required for organoid survival. Thus, B cell expansion during injury impairs epithelial-stromal cell interactions required for mucosal healing, with implications for the treatment of IBD. [Display omitted] •B cells are the dominant immune cell type during colonic mucosal healing (MH)•IFN-induced B cells are associated with injury and expand during MH•B cell depletion results in enhanced MH following intestinal injury•B cells impair the interactions between IEC and stromal cells during MH The cellular mechanisms controlling mucosal healing (MH) following injury are largely unknown. Using unbiased multi-parameter analysis, Frede and colleagues identified that B cells accumulate in the colonic damaged areas during MH. Surprisingly, B cells played detrimental roles during MH, as their presence hindered the interaction between epithelium and stroma.
Therapeutic promotion of intestinal regeneration holds great promise, but defining the cellular mechanisms that influence tissue regeneration remains an unmet challenge. To gain insight into the process of mucosal healing, we longitudinally examined the immune cell composition during intestinal damage and regeneration. B cells were the dominant cell type in the healing colon, and single-cell RNA sequencing (scRNA-seq) revealed expansion of an IFN-induced B cell subset during experimental mucosal healing that predominantly located in damaged areas and associated with colitis severity. B cell depletion accelerated recovery upon injury, decreased epithelial ulceration, and enhanced gene expression programs associated with tissue remodeling. scRNA-seq from the epithelial and stromal compartments combined with spatial transcriptomics and multiplex immunostaining showed that B cells decreased interactions between stromal and epithelial cells during mucosal healing. Activated B cells disrupted the epithelial-stromal cross talk required for organoid survival. Thus, B cell expansion during injury impairs epithelial-stromal cell interactions required for mucosal healing, with implications for the treatment of IBD.Therapeutic promotion of intestinal regeneration holds great promise, but defining the cellular mechanisms that influence tissue regeneration remains an unmet challenge. To gain insight into the process of mucosal healing, we longitudinally examined the immune cell composition during intestinal damage and regeneration. B cells were the dominant cell type in the healing colon, and single-cell RNA sequencing (scRNA-seq) revealed expansion of an IFN-induced B cell subset during experimental mucosal healing that predominantly located in damaged areas and associated with colitis severity. B cell depletion accelerated recovery upon injury, decreased epithelial ulceration, and enhanced gene expression programs associated with tissue remodeling. scRNA-seq from the epithelial and stromal compartments combined with spatial transcriptomics and multiplex immunostaining showed that B cells decreased interactions between stromal and epithelial cells during mucosal healing. Activated B cells disrupted the epithelial-stromal cross talk required for organoid survival. Thus, B cell expansion during injury impairs epithelial-stromal cell interactions required for mucosal healing, with implications for the treatment of IBD.
Therapeutic promotion of intestinal regeneration holds great promise, but defining the cellular mechanisms that influence tissue regeneration remains an unmet challenge. To gain insight into the process of mucosal healing, we longitudinally examined the immune cell composition during intestinal damage and regeneration. B cells were the dominant cell type in the healing colon, and single-cell RNA sequencing (scRNA-seq) re-vealed expansion of an IFN-induced B cell subset during experimental mucosal healing that predominantly located in damaged areas and associated with colitis severity. B cell depletion accelerated recovery upon injury, decreased epithelial ulceration, and enhanced gene expression programs associated with tissue re-modeling. scRNA-seq from the epithelial and stromal compartments combined with spatial transcriptomics and multiplex immunostaining showed that B cells decreased interactions between stromal and epithelial cells during mucosal healing. Activated B cells disrupted the epithelial-stromal cross talk required for orga-noid survival. Thus, B cell expansion during injury impairs epithelial-stromal cell interactions required for mucosal healing, with implications for the treatment of IBD.
Author Hunt, Matthew
Ramirez Flores, Ricardo O.
Schlitzer, Andreas
Villablanca, Eduardo J.
Westendorf, Astrid M.
Bejarano, David A.
Morales, Rodrigo A.
Frede, Annika
Saez-Rodriguez, Julio
Engblom, Camilla
Larsson, Ludvig
Sorini, Chiara
Luo, Xinxin
Hu, Yue O.O.
Lennon-Duménil, Ana-Maria
Kuiper, Raoul
Hövelmeyer, Nadine
Das, Srustidhar
Castillo, Francisca
Mittenzwei, Romy
Mariano, Livia Lacerda
Zagami, Chiara
Geerlings, Laura
Czarnewski, Paulo
Monasterio, Gustavo
Novella-Rausell, Claudio
Tripathi, Kumar P.
Lundeberg, Joakim
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Keywords stromal cell
B cell
single cell
fibroblasts
inflammation
spatial transcriptomics
organoids
epithelium
tissue repair
mucosal healing
Language English
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36516815 - Immunity. 2022 Dec 13;55(12):2222-2224
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Snippet Therapeutic promotion of intestinal regeneration holds great promise, but defining the cellular mechanisms that influence tissue regeneration remains an unmet...
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SubjectTerms Animals
B cell
Colitis
Disease Models, Animal
Epithelial Cells - metabolism
Epithelium
fibroblasts
inflammation
Intestinal Mucosa
mucosal healing
organoids
single cell
spatial transcriptomics
stromal cell
tissue repair
Wound Healing
Title B cell expansion hinders the stroma-epithelium regenerative cross talk during mucosal healing
URI https://dx.doi.org/10.1016/j.immuni.2022.11.002
https://www.ncbi.nlm.nih.gov/pubmed/36462502
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