The Transforming Rho Family GTPase Wrch-1 Disrupts Epithelial Cell Tight Junctions and Epithelial Morphogenesis

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Published inMolecular and Cellular Biology Vol. 29; no. 4; pp. 1035 - 1049
Main Authors Brady, Donita C., Alan, Jamie K., Madigan, James P., Fanning, Alan S., Cox, Adrienne D.
Format Journal Article
LanguageEnglish
Published United States American Society for Microbiology 01.02.2009
Taylor & Francis
American Society for Microbiology (ASM)
Subjects
Actins - metabolism
Adaptor Proteins, Signal Transducing - metabolism
Animals
Cell Adhesion - drug effects
Cell Polarity - drug effects
Cell Proliferation - drug effects
Cell Shape - drug effects
Cercopithecus aethiops
COS Cells
Dogs
Enzyme Activation - drug effects
Epithelial Cells - cytology
Epithelial Cells - drug effects
Epithelial Cells - enzymology
Epithelium - drug effects
Epithelium - embryology
Epithelium - enzymology
Guanosine Triphosphate - pharmacology
Humans
Morphogenesis - drug effects
Mutation - genetics
Protein Binding - drug effects
Protein Structure, Tertiary
Protein Transport - drug effects
rho GTP-Binding Proteins - chemistry
rho GTP-Binding Proteins - metabolism
Tight Junctions - drug effects
Tight Junctions - enzymology
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Wrch-1, an atypical and transforming Rho GTPase, regulates cellular activities including proliferation and actin organization, but its functions and effectors remain poorly characterized. We show here that Wrch-1 distributes along the apical and basolateral membranes in MDCK cells and binds the cell polarity protein Par6 in a GTP-dependent manner. Activated Wrch-1 negatively regulates the kinetics of tight junction (TJ) assembly during epithelial cell polarization but has no detectable effect on overall cell polarity in confluent monolayers. It also causes a dramatic cytoskeletal reorganization and multilayering in cells grown in two-dimensional culture and disrupts cystogenesis of cells grown in three-dimensional (3D) culture. Similarly, short hairpin RNA-mediated knockdown of Wrch-1 perturbs cystogenesis in 3D culture, suggesting that tight regulation of Wrch-1 activity is necessary for normal epithelial morphogenesis. A weakly transforming effector domain mutant of activated Wrch-1 that inhibits Par6 binding abrogates the ability of Wrch-1 to disrupt TJ formation, actin organization, and epithelial morphogenesis. We hypothesize that Wrch-1-induced morphological and growth transformation may occur in part through Par6-mediated disruption of TJs and actin organization.
Author Donita C. Brady
Adrienne D. Cox
James P. Madigan
Jamie K. Alan
Alan S. Fanning
AuthorAffiliation Department of Pharmacology, 1 Curriculum in Genetics and Molecular Biology, 2 Department of Cell and Molecular Physiology, 3 Department of Radiation Oncology, 4 Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599 5
AuthorAffiliation_xml – name: Department of Pharmacology, 1 Curriculum in Genetics and Molecular Biology, 2 Department of Cell and Molecular Physiology, 3 Department of Radiation Oncology, 4 Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599 5
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Corresponding author. Mailing address: Departments of Radiation Oncology and Pharmacology, 1028 NCCCC, 101 Manning Drive, CB # 7512, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-7512. Phone: (919) 966-7713, ext. 305. Fax: (919) 966-7681. E-mail: adrienne_cox@med.unc.edu
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Wrch-1, an atypical and transforming Rho GTPase, regulates cellular activities including proliferation and actin organization, but its functions and effectors...
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StartPage 1035
SubjectTerms Actins - metabolism
Adaptor Proteins, Signal Transducing - metabolism
Animals
Cell Adhesion - drug effects
Cell Polarity - drug effects
Cell Proliferation - drug effects
Cell Shape - drug effects
Cercopithecus aethiops
COS Cells
Dogs
Enzyme Activation - drug effects
Epithelial Cells - cytology
Epithelial Cells - drug effects
Epithelial Cells - enzymology
Epithelium - drug effects
Epithelium - embryology
Epithelium - enzymology
Guanosine Triphosphate - pharmacology
Humans
Morphogenesis - drug effects
Mutation - genetics
Protein Binding - drug effects
Protein Structure, Tertiary
Protein Transport - drug effects
rho GTP-Binding Proteins - chemistry
rho GTP-Binding Proteins - metabolism
Tight Junctions - drug effects
Tight Junctions - enzymology
Title The Transforming Rho Family GTPase Wrch-1 Disrupts Epithelial Cell Tight Junctions and Epithelial Morphogenesis
URI http://mcb.asm.org/content/29/4/1035.abstract
https://www.tandfonline.com/doi/abs/10.1128/MCB.00336-08
https://www.ncbi.nlm.nih.gov/pubmed/19064640
https://search.proquest.com/docview/66859835
https://pubmed.ncbi.nlm.nih.gov/PMC2643799
Volume 29
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