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Cell wall constrains lateral diffusion of plant plasma-membrane proteins

Alexandre Martinière, Irene Lavagi, Gayathri Nageswaran, Daniel J Rolfe, Lilly Maneta-Peyret, Doan-Trung Luu, Stanley W Botchway, Stephen ED Webb, Sebastien Mongrand and Christophe Maurel, et al. (2012) PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 109(31). p.12805-12810
abstract
A cell membrane can be considered a liquid-phase plane in which lipids and proteins theoretically are free to diffuse. Numerous reports, however, describe retarded diffusion of membrane proteins in animal cells. This anomalous diffusion results from a combination of structuring factors including protein-protein interactions, cytoskeleton corralling, and lipid organization into microdomains. In plant cells, plasma-membrane (PM) proteins have been described as relatively immobile, but the control mechanisms that structure the PM have not been studied. Here, we use fluorescence recovery after photobleaching to estimate mobility of a set of minimal PM proteins. These proteins consist only of a PM-anchoring domain fused to a fluorescent protein, but their mobilities remained limited, as is the case for many full-length proteins. Neither the cytoskeleton nor membrane microdomain structure was involved in constraining the diffusion of these proteins. The cell wall, however, was shown to have a crucial role in immobilizing PM proteins. In addition, by single-molecule fluorescence imaging we confirmed that the pattern of cellulose deposition in the cell wall affects the trajectory and speed of PM protein diffusion. Regulation of PM protein dynamics by the plant cell wall can be interpreted as a mechanism for regulating protein interactions in processes such as trafficking and signal transduction.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
ENDOCYTOSIS, CELLULOSE, REVEALS, DYNAMICS, ARABIDOPSIS, LIPID RAFTS, CARRIER POLARITY, DETERGENT-RESISTANT MEMBRANES, ENDOPLASMIC-RETICULUM, MOBILITY
journal title
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Proc. Natl. Acad. Sci. USA
volume
109
issue
31
pages
12805 - 12810
Web of Science type
Article
Web of Science id
000307538200102
JCR category
MULTIDISCIPLINARY SCIENCES
JCR impact factor
9.737 (2012)
JCR rank
4/56 (2012)
JCR quartile
1 (2012)
ISSN
0027-8424
DOI
10.1073/pnas.1202040109
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
2997464
handle
http://hdl.handle.net/1854/LU-2997464
date created
2012-09-21 15:48:28
date last changed
2012-09-24 09:45:14
@article{2997464,
  abstract     = {A cell membrane can be considered a liquid-phase plane in which lipids and proteins theoretically are free to diffuse. Numerous reports, however, describe retarded diffusion of membrane proteins in animal cells. This anomalous diffusion results from a combination of structuring factors including protein-protein interactions, cytoskeleton corralling, and lipid organization into microdomains. In plant cells, plasma-membrane (PM) proteins have been described as relatively immobile, but the control mechanisms that structure the PM have not been studied. Here, we use fluorescence recovery after photobleaching to estimate mobility of a set of minimal PM proteins. These proteins consist only of a PM-anchoring domain fused to a fluorescent protein, but their mobilities remained limited, as is the case for many full-length proteins. Neither the cytoskeleton nor membrane microdomain structure was involved in constraining the diffusion of these proteins. The cell wall, however, was shown to have a crucial role in immobilizing PM proteins. In addition, by single-molecule fluorescence imaging we confirmed that the pattern of cellulose deposition in the cell wall affects the trajectory and speed of PM protein diffusion. Regulation of PM protein dynamics by the plant cell wall can be interpreted as a mechanism for regulating protein interactions in processes such as trafficking and signal transduction.},
  author       = {Martini{\`e}re, Alexandre and Lavagi, Irene and Nageswaran, Gayathri and Rolfe, Daniel J and Maneta-Peyret, Lilly and Luu, Doan-Trung and Botchway, Stanley W and Webb, Stephen ED and Mongrand, Sebastien and Maurel, Christophe and Martin-Fernandez, Marisa L and Kleine-Vehn, J{\"u}rgen and Friml, Jiri and Moreau, Patrick and Runions, John},
  issn         = {0027-8424},
  journal      = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  keyword      = {ENDOCYTOSIS,CELLULOSE,REVEALS,DYNAMICS,ARABIDOPSIS,LIPID RAFTS,CARRIER POLARITY,DETERGENT-RESISTANT MEMBRANES,ENDOPLASMIC-RETICULUM,MOBILITY},
  language     = {eng},
  number       = {31},
  pages        = {12805--12810},
  title        = {Cell wall constrains lateral diffusion of plant plasma-membrane proteins},
  url          = {http://dx.doi.org/10.1073/pnas.1202040109},
  volume       = {109},
  year         = {2012},
}

Chicago
Martinière, Alexandre, Irene Lavagi, Gayathri Nageswaran, Daniel J Rolfe, Lilly Maneta-Peyret, Doan-Trung Luu, Stanley W Botchway, et al. 2012. “Cell Wall Constrains Lateral Diffusion of Plant Plasma-membrane Proteins.” Proceedings of the National Academy of Sciences of the United States of America 109 (31): 12805–12810.
APA
Martinière, A., Lavagi, I., Nageswaran, G., Rolfe, D. J., Maneta-Peyret, L., Luu, D.-T., Botchway, S. W., et al. (2012). Cell wall constrains lateral diffusion of plant plasma-membrane proteins. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 109(31), 12805–12810.
Vancouver
1.
Martinière A, Lavagi I, Nageswaran G, Rolfe DJ, Maneta-Peyret L, Luu D-T, et al. Cell wall constrains lateral diffusion of plant plasma-membrane proteins. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2012;109(31):12805–10.
MLA
Martinière, Alexandre, Irene Lavagi, Gayathri Nageswaran, et al. “Cell Wall Constrains Lateral Diffusion of Plant Plasma-membrane Proteins.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 109.31 (2012): 12805–12810. Print.