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ADP-ribosylation factor machinery mediates endocytosis in plant cells

Satoshi Naramoto UGent, Jürgen Kleine-Vehn UGent, Stephanie Robert UGent, Masaru Fujimoto, Tomoko Dainobu, Tomasz Paciorek, Takashi Ueda, Akihiko Nakano, Marc Van Montagu UGent and Hiroo Fukuda, et al. (2010) PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 107(50). p.21890-21895
abstract
Endocytosis is crucial for various cellular functions and development of multicellular organisms. In mammals and yeast, ADP-ribosylation factor (ARF) GTPases, key components of vesicle formation, and their regulators ARF-guanine nucleotide exchange factors (GEFs) and ARF-GTPase-activating protein (GAPs) mediate endocytosis. A similar role has not been established in plants, mainly because of the lack of the canonical ARF and ARF-GEF components that are involved in endocytosis in other eukaryotes. In this study, we revealed a regulatory mechanism of endocytosis in plants based on ARF GTPase activity. We identified that ARF-GEF GNOM and ARF-GAP VASCULAR NETWORK DEFECTIVE 3 (VAN3), both of which are involved in polar auxin transport-dependent morphogenesis, localize at the plasma membranes as well as in intracellular structures. Variable angle epifluorescence microscopy revealed that GNOM and VAN3 localize to partially overlapping discrete foci at the plasma membranes that are regularly associated with the endocytic vesicle coat clathrin. Genetic studies revealed that GNOM and VAN3 activities are required for endocytosis and internalization of plasma membrane proteins, including PIN-FORMED auxin transporters. These findings identified ARF GTPase-based regulatory mechanisms for endocytosis in plants. GNOM and VAN3 previously were proposed to function solely at the recycling endosomes and trans-Golgi networks, respectively. Therefore our findings uncovered an additional cellular function of these prominent developmental regulators.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
GNOM ARF-GEF, DEPENDENT AUXIN GRADIENTS, NUCLEOTIDE-EXCHANGE FACTORS, VESICLE TRAFFICKING, MEMBRANE DYNAMICS, PROTEIN SECRETION, VASCULAR NETWORK, PLASMA-MEMBRANE, EARLY ENDOSOMES, BREFELDIN-A, vesicle trafficking, plant development, polarity
journal title
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Proc. Natl. Acad. Sci. U. S. A.
volume
107
issue
50
pages
21890 - 21895
Web of Science type
Article
Web of Science id
000285521500118
JCR category
MULTIDISCIPLINARY SCIENCES
JCR impact factor
9.771 (2010)
JCR rank
3/56 (2010)
JCR quartile
1 (2010)
ISSN
0027-8424
DOI
10.1073/pnas.1016260107
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
1242682
handle
http://hdl.handle.net/1854/LU-1242682
date created
2011-05-25 15:58:33
date last changed
2012-09-19 14:03:54
@article{1242682,
  abstract     = {Endocytosis is crucial for various cellular functions and development of multicellular organisms. In mammals and yeast, ADP-ribosylation factor (ARF) GTPases, key components of vesicle formation, and their regulators ARF-guanine nucleotide exchange factors (GEFs) and ARF-GTPase-activating protein (GAPs) mediate endocytosis. A similar role has not been established in plants, mainly because of the lack of the canonical ARF and ARF-GEF components that are involved in endocytosis in other eukaryotes. In this study, we revealed a regulatory mechanism of endocytosis in plants based on ARF GTPase activity. We identified that ARF-GEF GNOM and ARF-GAP VASCULAR NETWORK DEFECTIVE 3 (VAN3), both of which are involved in polar auxin transport-dependent morphogenesis, localize at the plasma membranes as well as in intracellular structures. Variable angle epifluorescence microscopy revealed that GNOM and VAN3 localize to partially overlapping discrete foci at the plasma membranes that are regularly associated with the endocytic vesicle coat clathrin. Genetic studies revealed that GNOM and VAN3 activities are required for endocytosis and internalization of plasma membrane proteins, including PIN-FORMED auxin transporters. These findings identified ARF GTPase-based regulatory mechanisms for endocytosis in plants. GNOM and VAN3 previously were proposed to function solely at the recycling endosomes and trans-Golgi networks, respectively. Therefore our findings uncovered an additional cellular function of these prominent developmental regulators.},
  author       = {Naramoto, Satoshi and Kleine-Vehn, J{\"u}rgen and Robert, Stephanie and Fujimoto, Masaru and Dainobu, Tomoko and Paciorek, Tomasz and Ueda, Takashi and Nakano, Akihiko and Van Montagu, Marc and Fukuda, Hiroo and Friml, Jiri},
  issn         = {0027-8424},
  journal      = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
  keyword      = {GNOM ARF-GEF,DEPENDENT AUXIN GRADIENTS,NUCLEOTIDE-EXCHANGE FACTORS,VESICLE TRAFFICKING,MEMBRANE DYNAMICS,PROTEIN SECRETION,VASCULAR NETWORK,PLASMA-MEMBRANE,EARLY ENDOSOMES,BREFELDIN-A,vesicle trafficking,plant development,polarity},
  language     = {eng},
  number       = {50},
  pages        = {21890--21895},
  title        = {ADP-ribosylation factor machinery mediates endocytosis in plant cells},
  url          = {http://dx.doi.org/10.1073/pnas.1016260107},
  volume       = {107},
  year         = {2010},
}

Chicago
Naramoto, Satoshi, Jürgen Kleine-Vehn, Stephanie Robert, Masaru Fujimoto, Tomoko Dainobu, Tomasz Paciorek, Takashi Ueda, et al. 2010. “ADP-ribosylation Factor Machinery Mediates Endocytosis in Plant Cells.” Proceedings of the National Academy of Sciences of the United States of America 107 (50): 21890–21895.
APA
Naramoto, S., Kleine-Vehn, J., Robert, S., Fujimoto, M., Dainobu, T., Paciorek, T., Ueda, T., et al. (2010). ADP-ribosylation factor machinery mediates endocytosis in plant cells. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 107(50), 21890–21895.
Vancouver
1.
Naramoto S, Kleine-Vehn J, Robert S, Fujimoto M, Dainobu T, Paciorek T, et al. ADP-ribosylation factor machinery mediates endocytosis in plant cells. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2010;107(50):21890–5.
MLA
Naramoto, Satoshi, Jürgen Kleine-Vehn, Stephanie Robert, et al. “ADP-ribosylation Factor Machinery Mediates Endocytosis in Plant Cells.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 107.50 (2010): 21890–21895. Print.