Lipid polarity is maintained in absence of tight junctions

Junichi Ikenouchi, Mayu Suzuki, Kazuaki Umeda, Kazutaka Ikeda, Ryo Taguchi, Tetsuyuki Kobayashi, Satoshi B. Sato, Toshihide Kobayashi, Donna B. Stolz, Masato Umeda

Research output: Contribution to journalArticle

25 Citations (Scopus)

Abstract

The role of tight junctions (TJs) in the establishment and maintenance of lipid polarity in epithelial cells has long been a subject of controversy. We have addressed this issue using lysenin, a toxin derived from earthworms, and an influenza virus labeled with a fluorescent lipid, octadecylrhodamine B (R18). Whenepithelial cells are stained with lysenin, lysenin selectively binds to their apical membranes. Using an artificial liposome, we demonstrated that lysenin recognizes the membrane domains where sphingomyelins are clustered. Interestingly, lysenin selectively stained the apical membranes of epithelial cells depleted of zonula occludens proteins (ZO-deficient cells), which completely lack TJs. Furthermore, the fluorescent lipid inserted into the apical membrane by fusion with the influenza virus did not diffuse to the lateral membrane in ZO-deficient epithelial cells. This study revealed that sphingomyelin-cluster formation occurs only in the apical membrane and that lipid polarity is maintained even in the absence of TJs.

Original languageEnglish
Pages (from-to)9525-9533
Number of pages9
JournalJournal of Biological Chemistry
Volume287
Issue number12
DOIs
Publication statusPublished - Mar 16 2012

Fingerprint

Tight Junctions
Membranes
Lipids
Sphingomyelins
Epithelial Cells
Orthomyxoviridae
Viruses
Zonula Occludens Proteins
Oligochaeta
Membrane Fusion
Membrane Lipids
Liposomes
Fusion reactions
Maintenance
lysenin

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

Ikenouchi, J., Suzuki, M., Umeda, K., Ikeda, K., Taguchi, R., Kobayashi, T., ... Umeda, M. (2012). Lipid polarity is maintained in absence of tight junctions. Journal of Biological Chemistry, 287(12), 9525-9533. https://doi.org/10.1074/jbc.M111.327064

Lipid polarity is maintained in absence of tight junctions. / Ikenouchi, Junichi; Suzuki, Mayu; Umeda, Kazuaki; Ikeda, Kazutaka; Taguchi, Ryo; Kobayashi, Tetsuyuki; Sato, Satoshi B.; Kobayashi, Toshihide; Stolz, Donna B.; Umeda, Masato.

In: Journal of Biological Chemistry, Vol. 287, No. 12, 16.03.2012, p. 9525-9533.

Research output: Contribution to journalArticle

Ikenouchi, J, Suzuki, M, Umeda, K, Ikeda, K, Taguchi, R, Kobayashi, T, Sato, SB, Kobayashi, T, Stolz, DB & Umeda, M 2012, 'Lipid polarity is maintained in absence of tight junctions', Journal of Biological Chemistry, vol. 287, no. 12, pp. 9525-9533. https://doi.org/10.1074/jbc.M111.327064
Ikenouchi J, Suzuki M, Umeda K, Ikeda K, Taguchi R, Kobayashi T et al. Lipid polarity is maintained in absence of tight junctions. Journal of Biological Chemistry. 2012 Mar 16;287(12):9525-9533. https://doi.org/10.1074/jbc.M111.327064
Ikenouchi, Junichi ; Suzuki, Mayu ; Umeda, Kazuaki ; Ikeda, Kazutaka ; Taguchi, Ryo ; Kobayashi, Tetsuyuki ; Sato, Satoshi B. ; Kobayashi, Toshihide ; Stolz, Donna B. ; Umeda, Masato. / Lipid polarity is maintained in absence of tight junctions. In: Journal of Biological Chemistry. 2012 ; Vol. 287, No. 12. pp. 9525-9533.
@article{c88aef3532aa423a847b523a2d9dff6e,
title = "Lipid polarity is maintained in absence of tight junctions",
abstract = "The role of tight junctions (TJs) in the establishment and maintenance of lipid polarity in epithelial cells has long been a subject of controversy. We have addressed this issue using lysenin, a toxin derived from earthworms, and an influenza virus labeled with a fluorescent lipid, octadecylrhodamine B (R18). Whenepithelial cells are stained with lysenin, lysenin selectively binds to their apical membranes. Using an artificial liposome, we demonstrated that lysenin recognizes the membrane domains where sphingomyelins are clustered. Interestingly, lysenin selectively stained the apical membranes of epithelial cells depleted of zonula occludens proteins (ZO-deficient cells), which completely lack TJs. Furthermore, the fluorescent lipid inserted into the apical membrane by fusion with the influenza virus did not diffuse to the lateral membrane in ZO-deficient epithelial cells. This study revealed that sphingomyelin-cluster formation occurs only in the apical membrane and that lipid polarity is maintained even in the absence of TJs.",
author = "Junichi Ikenouchi and Mayu Suzuki and Kazuaki Umeda and Kazutaka Ikeda and Ryo Taguchi and Tetsuyuki Kobayashi and Sato, {Satoshi B.} and Toshihide Kobayashi and Stolz, {Donna B.} and Masato Umeda",
year = "2012",
month = "3",
day = "16",
doi = "10.1074/jbc.M111.327064",
language = "English",
volume = "287",
pages = "9525--9533",
journal = "Journal of Biological Chemistry",
issn = "0021-9258",
publisher = "American Society for Biochemistry and Molecular Biology Inc.",
number = "12",

}

TY - JOUR

T1 - Lipid polarity is maintained in absence of tight junctions

AU - Ikenouchi, Junichi

AU - Suzuki, Mayu

AU - Umeda, Kazuaki

AU - Ikeda, Kazutaka

AU - Taguchi, Ryo

AU - Kobayashi, Tetsuyuki

AU - Sato, Satoshi B.

AU - Kobayashi, Toshihide

AU - Stolz, Donna B.

AU - Umeda, Masato

PY - 2012/3/16

Y1 - 2012/3/16

N2 - The role of tight junctions (TJs) in the establishment and maintenance of lipid polarity in epithelial cells has long been a subject of controversy. We have addressed this issue using lysenin, a toxin derived from earthworms, and an influenza virus labeled with a fluorescent lipid, octadecylrhodamine B (R18). Whenepithelial cells are stained with lysenin, lysenin selectively binds to their apical membranes. Using an artificial liposome, we demonstrated that lysenin recognizes the membrane domains where sphingomyelins are clustered. Interestingly, lysenin selectively stained the apical membranes of epithelial cells depleted of zonula occludens proteins (ZO-deficient cells), which completely lack TJs. Furthermore, the fluorescent lipid inserted into the apical membrane by fusion with the influenza virus did not diffuse to the lateral membrane in ZO-deficient epithelial cells. This study revealed that sphingomyelin-cluster formation occurs only in the apical membrane and that lipid polarity is maintained even in the absence of TJs.

AB - The role of tight junctions (TJs) in the establishment and maintenance of lipid polarity in epithelial cells has long been a subject of controversy. We have addressed this issue using lysenin, a toxin derived from earthworms, and an influenza virus labeled with a fluorescent lipid, octadecylrhodamine B (R18). Whenepithelial cells are stained with lysenin, lysenin selectively binds to their apical membranes. Using an artificial liposome, we demonstrated that lysenin recognizes the membrane domains where sphingomyelins are clustered. Interestingly, lysenin selectively stained the apical membranes of epithelial cells depleted of zonula occludens proteins (ZO-deficient cells), which completely lack TJs. Furthermore, the fluorescent lipid inserted into the apical membrane by fusion with the influenza virus did not diffuse to the lateral membrane in ZO-deficient epithelial cells. This study revealed that sphingomyelin-cluster formation occurs only in the apical membrane and that lipid polarity is maintained even in the absence of TJs.

UR - http://www.scopus.com/inward/record.url?scp=84863353883&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84863353883&partnerID=8YFLogxK

U2 - 10.1074/jbc.M111.327064

DO - 10.1074/jbc.M111.327064

M3 - Article

C2 - 22294698

AN - SCOPUS:84863353883

VL - 287

SP - 9525

EP - 9533

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 0021-9258

IS - 12

ER -