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PKD-dependent PARP12-catalyzed mono-ADP-ribosylation of Golgin-97 is required for E-cadherin transport from Golgi to plasma membrane

Adenosine diphosphate (ADP)-ribosylation is a posttranslational modification involved in key regulatory events catalyzed by ADP-ribosyltransferases (ARTs). Substrate identification and localization of the mono-ADP-ribosyltransferase PARP12 at the trans-Golgi network (TGN) hinted at the involvement o...

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Autores principales: Grimaldi, Giovanna, Filograna, Angela, Schembri, Laura, Lo Monte, Matteo, Di Martino, Rosaria, Pirozzi, Marinella, Spano, Daniela, Beccari, Andrea R., Parashuraman, Seetharaman, Luini, Alberto, Valente, Carmen, Corda, Daniela
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8740581/
https://www.ncbi.nlm.nih.gov/pubmed/34969853
http://dx.doi.org/10.1073/pnas.2026494119
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author Grimaldi, Giovanna
Filograna, Angela
Schembri, Laura
Lo Monte, Matteo
Di Martino, Rosaria
Pirozzi, Marinella
Spano, Daniela
Beccari, Andrea R.
Parashuraman, Seetharaman
Luini, Alberto
Valente, Carmen
Corda, Daniela
author_facet Grimaldi, Giovanna
Filograna, Angela
Schembri, Laura
Lo Monte, Matteo
Di Martino, Rosaria
Pirozzi, Marinella
Spano, Daniela
Beccari, Andrea R.
Parashuraman, Seetharaman
Luini, Alberto
Valente, Carmen
Corda, Daniela
author_sort Grimaldi, Giovanna
collection PubMed
description Adenosine diphosphate (ADP)-ribosylation is a posttranslational modification involved in key regulatory events catalyzed by ADP-ribosyltransferases (ARTs). Substrate identification and localization of the mono-ADP-ribosyltransferase PARP12 at the trans-Golgi network (TGN) hinted at the involvement of ARTs in intracellular traffic. We find that Golgin-97, a TGN protein required for the formation and transport of a specific class of basolateral cargoes (e.g., E-cadherin and vesicular stomatitis virus G protein [VSVG]), is a PARP12 substrate. PARP12 targets an acidic cluster in the Golgin-97 coiled-coil domain essential for function. Its mutation or PARP12 depletion, delays E-cadherin and VSVG export and leads to a defect in carrier fission, hence in transport, with consequent accumulation of cargoes in a trans-Golgi/Rab11–positive intermediate compartment. In contrast, PARP12 does not control the Golgin-245–dependent traffic of cargoes such as tumor necrosis factor alpha (TNFα). Thus, the transport of different basolateral proteins to the plasma membrane is differentially regulated by Golgin-97 mono-ADP-ribosylation by PARP12. This identifies a selective regulatory mechanism acting on the transport of Golgin-97– vs. Golgin-245–dependent cargoes. Of note, PARP12 enzymatic activity, and consequently Golgin-97 mono-ADP-ribosylation, depends on the activation of protein kinase D (PKD) at the TGN during traffic. PARP12 is directly phosphorylated by PKD, and this is essential to stimulate PARP12 catalytic activity. PARP12 is therefore a component of the PKD-driven regulatory cascade that selectively controls a major branch of the basolateral transport pathway. We propose that through this mechanism, PARP12 contributes to the maintenance of E-cadherin–mediated cell polarity and cell–cell junctions.
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spelling pubmed-87405812022-06-30 PKD-dependent PARP12-catalyzed mono-ADP-ribosylation of Golgin-97 is required for E-cadherin transport from Golgi to plasma membrane Grimaldi, Giovanna Filograna, Angela Schembri, Laura Lo Monte, Matteo Di Martino, Rosaria Pirozzi, Marinella Spano, Daniela Beccari, Andrea R. Parashuraman, Seetharaman Luini, Alberto Valente, Carmen Corda, Daniela Proc Natl Acad Sci U S A Biological Sciences Adenosine diphosphate (ADP)-ribosylation is a posttranslational modification involved in key regulatory events catalyzed by ADP-ribosyltransferases (ARTs). Substrate identification and localization of the mono-ADP-ribosyltransferase PARP12 at the trans-Golgi network (TGN) hinted at the involvement of ARTs in intracellular traffic. We find that Golgin-97, a TGN protein required for the formation and transport of a specific class of basolateral cargoes (e.g., E-cadherin and vesicular stomatitis virus G protein [VSVG]), is a PARP12 substrate. PARP12 targets an acidic cluster in the Golgin-97 coiled-coil domain essential for function. Its mutation or PARP12 depletion, delays E-cadherin and VSVG export and leads to a defect in carrier fission, hence in transport, with consequent accumulation of cargoes in a trans-Golgi/Rab11–positive intermediate compartment. In contrast, PARP12 does not control the Golgin-245–dependent traffic of cargoes such as tumor necrosis factor alpha (TNFα). Thus, the transport of different basolateral proteins to the plasma membrane is differentially regulated by Golgin-97 mono-ADP-ribosylation by PARP12. This identifies a selective regulatory mechanism acting on the transport of Golgin-97– vs. Golgin-245–dependent cargoes. Of note, PARP12 enzymatic activity, and consequently Golgin-97 mono-ADP-ribosylation, depends on the activation of protein kinase D (PKD) at the TGN during traffic. PARP12 is directly phosphorylated by PKD, and this is essential to stimulate PARP12 catalytic activity. PARP12 is therefore a component of the PKD-driven regulatory cascade that selectively controls a major branch of the basolateral transport pathway. We propose that through this mechanism, PARP12 contributes to the maintenance of E-cadherin–mediated cell polarity and cell–cell junctions. National Academy of Sciences 2021-12-30 2022-01-04 /pmc/articles/PMC8740581/ /pubmed/34969853 http://dx.doi.org/10.1073/pnas.2026494119 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Grimaldi, Giovanna
Filograna, Angela
Schembri, Laura
Lo Monte, Matteo
Di Martino, Rosaria
Pirozzi, Marinella
Spano, Daniela
Beccari, Andrea R.
Parashuraman, Seetharaman
Luini, Alberto
Valente, Carmen
Corda, Daniela
PKD-dependent PARP12-catalyzed mono-ADP-ribosylation of Golgin-97 is required for E-cadherin transport from Golgi to plasma membrane
title PKD-dependent PARP12-catalyzed mono-ADP-ribosylation of Golgin-97 is required for E-cadherin transport from Golgi to plasma membrane
title_full PKD-dependent PARP12-catalyzed mono-ADP-ribosylation of Golgin-97 is required for E-cadherin transport from Golgi to plasma membrane
title_fullStr PKD-dependent PARP12-catalyzed mono-ADP-ribosylation of Golgin-97 is required for E-cadherin transport from Golgi to plasma membrane
title_full_unstemmed PKD-dependent PARP12-catalyzed mono-ADP-ribosylation of Golgin-97 is required for E-cadherin transport from Golgi to plasma membrane
title_short PKD-dependent PARP12-catalyzed mono-ADP-ribosylation of Golgin-97 is required for E-cadherin transport from Golgi to plasma membrane
title_sort pkd-dependent parp12-catalyzed mono-adp-ribosylation of golgin-97 is required for e-cadherin transport from golgi to plasma membrane
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8740581/
https://www.ncbi.nlm.nih.gov/pubmed/34969853
http://dx.doi.org/10.1073/pnas.2026494119
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