Distinct EH domains of the endocytic TPLATE complex confer
lipid and protein binding

J 2021

Distinct EH domains of the endocytic TPLATE complex confer lipid and protein binding

YPERMAN, K., Anna PAPAGEORGIOU, R. MERCERON, S. DE MUNCK, Y. BLOCH et. al.

Basic information

Original name

Distinct EH domains of the endocytic TPLATE complex confer lipid and protein binding

Authors

YPERMAN, K., Anna PAPAGEORGIOU (300 Greece, belonging to the institution), R. MERCERON, S. DE MUNCK, Y. BLOCH, D. EECKHOUT, Q.H. JIANG, P. TACK, R. GRIGORYAN, Thomas EVANGELIDIS (300 Greece, belonging to the institution), J. VAN LEENE, L. VINCZE, P. VANDENABEELE, F. VANHAECKE, M. POTOCKY, G. DE JAEGER, S.N. SAVVIDES, Konstantinos TRIPSIANES (300 Greece, guarantor, belonging to the institution), R. PLESKOT and D. VAN DAMME

Edition

Nature Communications, London, Nature Publishing Group, 2021, 2041-1723

Other information

Language

English

Type of outcome

Článek v odborném periodiku

Field of Study

10608 Biochemistry and molecular biology

Country of publisher

United Kingdom of Great Britain and Northern Ireland

Confidentiality degree

není předmětem státního či obchodního tajemství

References:

URL

Impact factor

Impact factor: 17.694

RIV identification code

RIV/00216224:14740/21:00122020

Organization unit

Central European Institute of Technology

DOI

http://dx.doi.org/10.1038/s41467-021-23314-6

UT WoS

000658769900002

Keywords in English

Adaptor Proteins; Signal Transducing; Calcium-Binding Proteins; Cell Membrane; X-Ray; NMR; Molecular Dynamics Simulation

Abstract

V originále

Clathrin-mediated endocytosis (CME) is the gatekeeper of the plasma membrane. In contrast to animals and yeasts, CME in plants depends on the TPLATE complex (TPC), an evolutionary ancient adaptor complex. However, the mechanistic contribution of the individual TPC subunits to plant CME remains elusive. In this study, we used a multidisciplinary approach to elucidate the structural and functional roles of the evolutionary conserved N-terminal Eps15 homology (EH) domains of the TPC subunit AtEH1/Pan1. By integrating high-resolution structural information obtained by X-ray crystallography and NMR spectroscopy with all-atom molecular dynamics simulations, we provide structural insight into the function of both EH domains. Both domains bind phosphatidic acid with a different strength, and only the second domain binds phosphatidylinositol 4,5-bisphosphate. Unbiased peptidome profiling by mass-spectrometry revealed that the first EH domain preferentially interacts with the double N-terminal NPF motif of a previously unidentified TPC interactor, the integral membrane protein Secretory Carrier Membrane Protein 5 (SCAMP5). Furthermore, we show that AtEH/Pan1 proteins control the internalization of SCAMP5 via this double NPF peptide interaction motif. Collectively, our structural and functional studies reveal distinct but complementary roles of the EH domains of AtEH/Pan1 in plant CME and connect the internalization of SCAMP5 to the TPLATE complex. AtEH/Pan1 proteins contain two N-terminal Eps15 homology (EH) domains and are subunits of the endocytic TPLATE complex present in plants. Here, the authors combine X-ray crystallography, NMR and MD simulations with biochemical and in planta analysis to characterize the two AtEH1/Pan1 EH domains and reveal their structural differences and complementary functional roles.

Links

LQ1601, research and development project

Name: CEITEC 2020 (Acronym: CEITEC2020)

Investor: Ministry of Education, Youth and Sports of the CR

MUNI/G/0739/2017, interní kód MU

Name: Pushing the limits in automated NMR structure determination using a single 4D NOESY spectrum and machine learning methods

Investor: Masaryk University, INTERDISCIPLINARY - Interdisciplinary research projects

90127, large research infrastructures

Name: CIISB II

Citovat

YPERMAN, K., Anna PAPAGEORGIOU, R. MERCERON, S. DE MUNCK, Y. BLOCH, D. EECKHOUT, Q.H. JIANG, P. TACK, R. GRIGORYAN, Thomas EVANGELIDIS, J. VAN LEENE, L. VINCZE, P. VANDENABEELE, F. VANHAECKE, M. POTOCKY, G. DE JAEGER, S.N. SAVVIDES, Konstantinos TRIPSIANES, R. PLESKOT and D. VAN DAMME. Distinct EH domains of the endocytic TPLATE complex confer lipid and protein binding. Nature Communications. London: Nature Publishing Group, 2021, vol. 12, No 1, p. "3050", 11 pp. ISSN 2041-1723. Available from: https://dx.doi.org/10.1038/s41467-021-23314-6.

@article{1784537,
   author = {Yperman, K. and Papageorgiou, Anna and Merceron, R. and De Munck, S. and Bloch, Y. and Eeckhout, D. and Jiang, Q.H. and Tack, P. and Grigoryan, R. and Evangelidis, Thomas and Van Leene, J. and Vincze, L. and Vandenabeele, P. and Vanhaecke, F. and Potocky, M. and De Jaeger, G. and Savvides, S.N. and Tripsianes, Konstantinos and Pleskot, R. and Van Damme, D.},
   article_location = {London},
   article_number = {1},
   doi = {http://dx.doi.org/10.1038/s41467-021-23314-6},
   keywords = {Adaptor Proteins; Signal Transducing; Calcium-Binding Proteins; Cell Membrane; X-Ray; NMR; Molecular Dynamics Simulation},
   language = {eng},
   issn = {2041-1723},
   journal = {Nature Communications},
   title = {Distinct EH domains of the endocytic TPLATE complex confer lipid and protein binding},
   url = {https://www.ncbi.nlm.nih.gov/pubmed/34031427},
   volume = {12},
   year = {2021}
}

TY  - JOUR
ID  - 1784537
AU  - Yperman, K. - Papageorgiou, Anna - Merceron, R. - De Munck, S. - Bloch, Y. - Eeckhout, D. - Jiang, Q.H. - Tack, P. - Grigoryan, R. - Evangelidis, Thomas - Van Leene, J. - Vincze, L. - Vandenabeele, P. - Vanhaecke, F. - Potocky, M. - De Jaeger, G. - Savvides, S.N. - Tripsianes, Konstantinos - Pleskot, R. - Van Damme, D.
PY  - 2021
TI  - Distinct EH domains of the endocytic TPLATE complex confer lipid and protein binding
JF  - Nature Communications
VL  - 12
IS  - 1
SP  - "3050"
EP  - "3050"
PB  - Nature Publishing Group
SN  - 20411723
KW  - Adaptor Proteins
KW  - Signal Transducing
KW  - Calcium-Binding Proteins
KW  - Cell Membrane
KW  - X-Ray
KW  - NMR
KW  - Molecular Dynamics Simulation
UR  - https://www.ncbi.nlm.nih.gov/pubmed/34031427
N2  - Clathrin-mediated endocytosis (CME) is the gatekeeper of the plasma membrane. In contrast to animals and yeasts, CME in plants depends on the TPLATE complex (TPC), an evolutionary ancient adaptor complex. However, the mechanistic contribution of the individual TPC subunits to plant CME remains elusive. In this study, we used a multidisciplinary approach to elucidate the structural and functional roles of the evolutionary conserved N-terminal Eps15 homology (EH) domains of the TPC subunit AtEH1/Pan1. By integrating high-resolution structural information obtained by X-ray crystallography and NMR spectroscopy with all-atom molecular dynamics simulations, we provide structural insight into the function of both EH domains. Both domains bind phosphatidic acid with a different strength, and only the second domain binds phosphatidylinositol 4,5-bisphosphate. Unbiased peptidome profiling by mass-spectrometry revealed that the first EH domain preferentially interacts with the double N-terminal NPF motif of a previously unidentified TPC interactor, the integral membrane protein Secretory Carrier Membrane Protein 5 (SCAMP5). Furthermore, we show that AtEH/Pan1 proteins control the internalization of SCAMP5 via this double NPF peptide interaction motif. Collectively, our structural and functional studies reveal distinct but complementary roles of the EH domains of AtEH/Pan1 in plant CME and connect the internalization of SCAMP5 to the TPLATE complex. AtEH/Pan1 proteins contain two N-terminal Eps15 homology (EH) domains and are subunits of the endocytic TPLATE complex present in plants. Here, the authors combine X-ray crystallography, NMR and MD simulations with biochemical and in planta analysis to characterize the two AtEH1/Pan1 EH domains and reveal their structural differences and complementary functional roles.
ER  -

YPERMAN, K., Anna PAPAGEORGIOU, R. MERCERON, S. DE MUNCK, Y. BLOCH, D. EECKHOUT, Q.H. JIANG, P. TACK, R. GRIGORYAN, Thomas EVANGELIDIS, J. VAN LEENE, L. VINCZE, P. VANDENABEELE, F. VANHAECKE, M. POTOCKY, G. DE JAEGER, S.N. SAVVIDES, Konstantinos TRIPSIANES, R. PLESKOT and D. VAN DAMME. Distinct EH domains of the endocytic TPLATE complex confer lipid and protein binding. \textit{Nature Communications}. London: Nature Publishing Group, 2021, vol.~12, No~1, p.~''3050'', 11 pp. ISSN~2041-1723. Available from: https://dx.doi.org/10.1038/s41467-021-23314-6.

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