Cell injury triggers actin polymerization to initiate epithelial restitution

The role of the actin cytoskeleton in the sequence of physiological epithelial repair in the intact epithelium has yet to be elucidated. Here, we explore the role of actin in gastric repair and gastric organoids (gastroids). In response to two-photon-induced cellular damage of either an gastric or g...

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Published inJournal of cell science Vol. 131; no. 16
Main Authors Aihara, Eitaro, Medina-Candelaria, Neisha M, Hanyu, Hikaru, Matthis, Andrea L, Engevik, Kristen A, Gurniak, Christine B, Witke, Walter, Turner, Jerrold R, Zhang, Tongli, Montrose, Marshall H
Format Journal Article
LanguageEnglish
Published England The Company of Biologists Ltd 15.08.2018
Subjects
Actins - metabolism
Animals
Cell Movement
Cells, Cultured
Epithelial Cells - physiology
Female
Gastric Mucosa - injuries
Gastric Mucosa - metabolism
Gastric Mucosa - physiology
Male
Mice
Mice, Transgenic
Organoids - cytology
Organoids - injuries
Organoids - physiology
Polymerization
Protein Multimerization - physiology
Re-Epithelialization - physiology
Regeneration - physiology
Stomach - cytology
Stomach - injuries
Epithelial cell
Gastric organoid
Repair
Actin
Cell migration
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Abstract The role of the actin cytoskeleton in the sequence of physiological epithelial repair in the intact epithelium has yet to be elucidated. Here, we explore the role of actin in gastric repair and gastric organoids (gastroids). In response to two-photon-induced cellular damage of either an gastric or gastroid epithelium, actin redistribution specifically occurred in the lateral membranes of cells neighboring the damaged cell. This was followed by their migration inward to close the gap at the basal pole of the dead cell, in parallel with exfoliation of the dead cell into the lumen. The repair and focal increase of actin was significantly blocked by treatment with EDTA or the inhibition of actin polymerization. Treatment with inhibitors of myosin light chain kinase, myosin II, trefoil factor 2 signaling or phospholipase C slowed both the initial actin redistribution and the repair. While Rac1 inhibition facilitated repair, inhibition of RhoA/Rho-associated protein kinase inhibited it. Inhibitors of focal adhesion kinase and Cdc42 had negligible effects. Hence, initial actin polymerization occurs in the lateral membrane, and is primarily important to initiate dead cell exfoliation and cell migration to close the gap.
AbstractList The role of the actin cytoskeleton in the sequence of physiological epithelial repair in the intact epithelium has yet to be elucidated. Here, we explore the role of actin in gastric repair and gastric organoids (gastroids). In response to two-photon-induced cellular damage of either an gastric or gastroid epithelium, actin redistribution specifically occurred in the lateral membranes of cells neighboring the damaged cell. This was followed by their migration inward to close the gap at the basal pole of the dead cell, in parallel with exfoliation of the dead cell into the lumen. The repair and focal increase of actin was significantly blocked by treatment with EDTA or the inhibition of actin polymerization. Treatment with inhibitors of myosin light chain kinase, myosin II, trefoil factor 2 signaling or phospholipase C slowed both the initial actin redistribution and the repair. While Rac1 inhibition facilitated repair, inhibition of RhoA/Rho-associated protein kinase inhibited it. Inhibitors of focal adhesion kinase and Cdc42 had negligible effects. Hence, initial actin polymerization occurs in the lateral membrane, and is primarily important to initiate dead cell exfoliation and cell migration to close the gap.
The role of the actin cytoskeleton in the sequence of physiological epithelial repair in the intact epithelium has yet to be elucidated. Here, we explore the role of actin in gastric repair in vivo and in vitro gastric organoids (gastroids). In response to two-photon-induced cellular damage of either an in vivo gastric or in vitro gastroid epithelium, actin redistribution specifically occurred in the lateral membranes of cells neighboring the damaged cell. This was followed by their migration inward to close the gap at the basal pole of the dead cell, in parallel with exfoliation of the dead cell into the lumen. The repair and focal increase of actin was significantly blocked by treatment with EDTA or the inhibition of actin polymerization. Treatment with inhibitors of myosin light chain kinase, myosin II, trefoil factor 2 signaling or phospholipase C slowed both the initial actin redistribution and the repair. While Rac1 inhibition facilitated repair, inhibition of RhoA/Rho-associated protein kinase inhibited it. Inhibitors of focal adhesion kinase and Cdc42 had negligible effects. Hence, initial actin polymerization occurs in the lateral membrane, and is primarily important to initiate dead cell exfoliation and cell migration to close the gap.
The role of the actin cytoskeleton in the sequence of physiological epithelial repair in the intact epithelium has yet to be elucidated. Here, we explore the role of actin in gastric repair in vivo and in vitro gastric organoids (gastroids). In response to two-photon-induced cellular damage of either an in vivo gastric or in vitro gastroid epithelium, actin redistribution specifically occurred in the lateral membranes of cells neighboring the damaged cell. This was followed by their migration inward to close the gap at the basal pole of the dead cell, in parallel with exfoliation of the dead cell into the lumen. The repair and focal increase of actin was significantly blocked by treatment with EDTA or the inhibition of actin polymerization. Treatment with inhibitors of myosin light chain kinase, myosin II, trefoil factor 2 signaling or phospholipase C slowed both the initial actin redistribution and the repair. While Rac1 inhibition facilitated repair, inhibition of RhoA/Rho-associated protein kinase inhibited it. Inhibitors of focal adhesion kinase and Cdc42 had negligible effects. Hence, initial actin polymerization occurs in the lateral membrane, and is primarily important to initiate dead cell exfoliation and cell migration to close the gap. Summary: The role of actin in epithelial repair is explored in experiments using gastric organoids, demonstrating that initial actin polymerization in the lateral membrane is of primary importance for initiation of repair.
Author Gurniak, Christine B
Hanyu, Hikaru
Medina-Candelaria, Neisha M
Aihara, Eitaro
Matthis, Andrea L
Montrose, Marshall H
Zhang, Tongli
Engevik, Kristen A
Witke, Walter
Turner, Jerrold R
AuthorAffiliation 1 Department of Pharmacology and Systems Physiology , University of Cincinnati , Cincinnati, OH 45267, USA
2 Institute of Genetics, University of Bonn , Bonn , Germany
3 Departments of Pathology and Medicine , Brigham and Women's Hospital and Harvard Medical School , Boston, MA 02115, USA
AuthorAffiliation_xml – name: 3 Departments of Pathology and Medicine , Brigham and Women's Hospital and Harvard Medical School , Boston, MA 02115, USA
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  organization: Department of Pharmacology and Systems Physiology, University of Cincinnati, Cincinnati, OH 45267, USA aiharaeo@uc.edu mhm@uc.edu
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Issue 16
Keywords Epithelial cell
Gastric organoid
Repair
Actin
Cell migration
Language English
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SSID ssj0007297
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Snippet The role of the actin cytoskeleton in the sequence of physiological epithelial repair in the intact epithelium has yet to be elucidated. Here, we explore the...
SourceID pubmedcentral
proquest
crossref
pubmed
SourceType Open Access Repository
Aggregation Database
Index Database
SubjectTerms Actins - metabolism
Animals
Cell Movement
Cells, Cultured
Epithelial Cells - physiology
Female
Gastric Mucosa - injuries
Gastric Mucosa - metabolism
Gastric Mucosa - physiology
Male
Mice
Mice, Transgenic
Organoids - cytology
Organoids - injuries
Organoids - physiology
Polymerization
Protein Multimerization - physiology
Re-Epithelialization - physiology
Regeneration - physiology
Stomach - cytology
Stomach - injuries
Title Cell injury triggers actin polymerization to initiate epithelial restitution
URI https://www.ncbi.nlm.nih.gov/pubmed/30072444
https://search.proquest.com/docview/2083718126
https://pubmed.ncbi.nlm.nih.gov/PMC6127731
Volume 131
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