Nucleoside diphosphate kinases fuel dynamin superfamily proteins with GTP for membrane remodeling

Mathieu Boissan; Guillaume Montagnac; Qinfang Shen; Lorena Griparic; Jérôme Guitton; Maryse Romao; Nathalie Sauvonnet; Thibault Lagache; Ioan Lascu; Graça Raposo; Céline Desbourdes; Uwe Schlattner; Marie Lise Lacombe; Simona Polo; Alexander M. Van Der Bliek; Aurélien Roux; Philippe Chavrier

doi:10.1126/science.1253768

Nucleoside diphosphate kinases fuel dynamin superfamily proteins with GTP for membrane remodeling

Mathieu Boissan, Guillaume Montagnac, Qinfang Shen, Lorena Griparic, Jérôme Guitton, Maryse Romao, Nathalie Sauvonnet, Thibault Lagache, Ioan Lascu, Graça Raposo, Céline Desbourdes, Uwe Schlattner, Marie Lise Lacombe, Simona Polo, Alexander M. Van Der Bliek, Aurélien Roux, Philippe Chavrier

Résultats de recherche: Contribution à un journal › Article › Revue par des pairs

124 Citations (Scopus)

Résumé

Dynamin superfamily molecular motors use guanosine triphosphate (GTP) as a source of energy for membrane-remodeling events. We found that knockdown of nucleoside diphosphate kinases (NDPKs) NM23-H1/H2, which produce GTP through adenosine triphosphate (ATP)-driven conversion of guanosine diphosphate (GDP), inhibited dynamin-mediated endocytosis. NM23-H1/H2 localized at clathrin-coated pits and interacted with the proline-rich domain of dynamin. In vitro, NM23-H1/H2 were recruited to dynamin-induced tubules, stimulated GTP-loading on dynamin, and triggered fission in the presence of ATP and GDP. NM23-H4, a mitochondria-specific NDPK, colocalized with mitochondrial dynamin-like OPA1 involved in mitochondria inner membrane fusion and increased GTP-loading on OPA1. Like OPA1 loss of function, silencing of NM23-H4 but not NM23-H1/H2 resulted in mitochondrial fragmentation, reflecting fusion defects. Thus, NDPKs interact with and provide GTP to dynamins, allowing these motor proteins to work with high thermodynamic efficiency.

langue originale	Anglais
Pages (de - à)	1510-1515
Nombre de pages	6
journal	Science
Volume	344
Numéro de publication	6191
Les DOIs	https://doi.org/10.1126/science.1253768
état	Publié - 1 janv. 2014

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10.1126/science.1253768

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Boissan, M., Montagnac, G., Shen, Q., Griparic, L., Guitton, J., Romao, M., Sauvonnet, N., Lagache, T., Lascu, I., Raposo, G., Desbourdes, C., Schlattner, U., Lacombe, M. L., Polo, S., Van Der Bliek, A. M., Roux, A., & Chavrier, P. (2014). Nucleoside diphosphate kinases fuel dynamin superfamily proteins with GTP for membrane remodeling. Science, 344(6191), 1510-1515. https://doi.org/10.1126/science.1253768

@article{c16d107fa2e642b7b62e88a888efa92c,

title = "Nucleoside diphosphate kinases fuel dynamin superfamily proteins with GTP for membrane remodeling",

abstract = "Dynamin superfamily molecular motors use guanosine triphosphate (GTP) as a source of energy for membrane-remodeling events. We found that knockdown of nucleoside diphosphate kinases (NDPKs) NM23-H1/H2, which produce GTP through adenosine triphosphate (ATP)-driven conversion of guanosine diphosphate (GDP), inhibited dynamin-mediated endocytosis. NM23-H1/H2 localized at clathrin-coated pits and interacted with the proline-rich domain of dynamin. In vitro, NM23-H1/H2 were recruited to dynamin-induced tubules, stimulated GTP-loading on dynamin, and triggered fission in the presence of ATP and GDP. NM23-H4, a mitochondria-specific NDPK, colocalized with mitochondrial dynamin-like OPA1 involved in mitochondria inner membrane fusion and increased GTP-loading on OPA1. Like OPA1 loss of function, silencing of NM23-H4 but not NM23-H1/H2 resulted in mitochondrial fragmentation, reflecting fusion defects. Thus, NDPKs interact with and provide GTP to dynamins, allowing these motor proteins to work with high thermodynamic efficiency.",

author = "Mathieu Boissan and Guillaume Montagnac and Qinfang Shen and Lorena Griparic and J{\'e}r{\^o}me Guitton and Maryse Romao and Nathalie Sauvonnet and Thibault Lagache and Ioan Lascu and Gra{\c c}a Raposo and C{\'e}line Desbourdes and Uwe Schlattner and Lacombe, {Marie Lise} and Simona Polo and {Van Der Bliek}, {Alexander M.} and Aur{\'e}lien Roux and Philippe Chavrier",

year = "2014",

month = jan,

day = "1",

doi = "10.1126/science.1253768",

language = "English",

volume = "344",

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Boissan, M, Montagnac, G, Shen, Q, Griparic, L, Guitton, J, Romao, M, Sauvonnet, N, Lagache, T, Lascu, I, Raposo, G, Desbourdes, C, Schlattner, U, Lacombe, ML, Polo, S, Van Der Bliek, AM, Roux, A & Chavrier, P 2014, 'Nucleoside diphosphate kinases fuel dynamin superfamily proteins with GTP for membrane remodeling', Science, VOL. 344, Numéro 6191, p. 1510-1515. https://doi.org/10.1126/science.1253768

TY - JOUR

T1 - Nucleoside diphosphate kinases fuel dynamin superfamily proteins with GTP for membrane remodeling

AU - Boissan, Mathieu

AU - Montagnac, Guillaume

AU - Shen, Qinfang

AU - Griparic, Lorena

AU - Guitton, Jérôme

AU - Romao, Maryse

AU - Sauvonnet, Nathalie

AU - Lagache, Thibault

AU - Lascu, Ioan

AU - Raposo, Graça

AU - Desbourdes, Céline

AU - Schlattner, Uwe

AU - Lacombe, Marie Lise

AU - Polo, Simona

AU - Van Der Bliek, Alexander M.

AU - Roux, Aurélien

AU - Chavrier, Philippe

PY - 2014/1/1

Y1 - 2014/1/1

N2 - Dynamin superfamily molecular motors use guanosine triphosphate (GTP) as a source of energy for membrane-remodeling events. We found that knockdown of nucleoside diphosphate kinases (NDPKs) NM23-H1/H2, which produce GTP through adenosine triphosphate (ATP)-driven conversion of guanosine diphosphate (GDP), inhibited dynamin-mediated endocytosis. NM23-H1/H2 localized at clathrin-coated pits and interacted with the proline-rich domain of dynamin. In vitro, NM23-H1/H2 were recruited to dynamin-induced tubules, stimulated GTP-loading on dynamin, and triggered fission in the presence of ATP and GDP. NM23-H4, a mitochondria-specific NDPK, colocalized with mitochondrial dynamin-like OPA1 involved in mitochondria inner membrane fusion and increased GTP-loading on OPA1. Like OPA1 loss of function, silencing of NM23-H4 but not NM23-H1/H2 resulted in mitochondrial fragmentation, reflecting fusion defects. Thus, NDPKs interact with and provide GTP to dynamins, allowing these motor proteins to work with high thermodynamic efficiency.

AB - Dynamin superfamily molecular motors use guanosine triphosphate (GTP) as a source of energy for membrane-remodeling events. We found that knockdown of nucleoside diphosphate kinases (NDPKs) NM23-H1/H2, which produce GTP through adenosine triphosphate (ATP)-driven conversion of guanosine diphosphate (GDP), inhibited dynamin-mediated endocytosis. NM23-H1/H2 localized at clathrin-coated pits and interacted with the proline-rich domain of dynamin. In vitro, NM23-H1/H2 were recruited to dynamin-induced tubules, stimulated GTP-loading on dynamin, and triggered fission in the presence of ATP and GDP. NM23-H4, a mitochondria-specific NDPK, colocalized with mitochondrial dynamin-like OPA1 involved in mitochondria inner membrane fusion and increased GTP-loading on OPA1. Like OPA1 loss of function, silencing of NM23-H4 but not NM23-H1/H2 resulted in mitochondrial fragmentation, reflecting fusion defects. Thus, NDPKs interact with and provide GTP to dynamins, allowing these motor proteins to work with high thermodynamic efficiency.

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DO - 10.1126/science.1253768

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EP - 1515

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JF - Science

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