FBP17 and CIP4 recruit SHIP2 and lamellipodin to prime the plasma membrane for fast endophilin-mediated endocytosis

Laura Chan Wah Hak; Shaheen Khan; Ilaria Di Meglio; Ah-lai Law; Safa Lucken-ardjomande Häsler; Leonor M. Quintaneiro; Antonio P. A. Ferreira; Matthias Krause; Harvey T. Mcmahon; Emmanuel Boucrot

doi:10.1038/s41556-018-0146-8

FBP17 and CIP4 recruit SHIP2 and lamellipodin to prime the plasma membrane for fast endophilin-mediated endocytosis

Laura Chan Wah Hak, Shaheen Khan, Ilaria Di Meglio, Ah-lai Law, Safa Lucken-ardjomande Häsler, Leonor M. Quintaneiro, Antonio P. A. Ferreira, Matthias Krause, Harvey T. Mcmahon, Emmanuel Boucrot

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Abstract

Endocytosis mediates the cellular uptake of micronutrients and the turnover of plasma membrane proteins. Clathrin-mediated endocytosis is the major uptake pathway in resting cells1, but several clathrin-independent endocytic routes exist in parallel2,3. One such pathway, fast endophilin-mediated endocytosis (FEME), is not constitutive but triggered upon activation of certain receptors, including the β1 adrenergic receptor4. FEME activates promptly following stimulation as endophilin is pre-enriched by the phosphatidylinositol-3,4-bisphosphate-binding protein lamellipodin4,5. However, in the absence of stimulation, endophilin foci abort and disassemble after a few seconds. Looking for additional proteins involved in FEME, we found that 20 out of 65 BAR domain-containing proteins tested colocalized with endophilin spots. Among them, FBP17 and CIP4 prime the membrane of resting cells for FEME by recruiting the 5′-lipid phosphatase SHIP2 and lamellipodin to mediate the local production of phosphatidylinositol-3,4-bisphosphate and endophilin pre-enrichment. Membrane-bound GTP-loaded Cdc42 recruits FBP17 and CIP4, before being locally deactivated by RICH1 and SH3BP1 GTPase-activating proteins. This generates the transient assembly and disassembly of endophilin spots, which lasts 5–10 seconds. This mechanism periodically primes patches of the membrane for prompt responses upon FEME activation.

Original language	English
Pages (from-to)	1023-1031
Journal	Nature Cell Biology
Volume	20
Issue number	9
Early online date	30 Jul 2018
DOIs	https://doi.org/10.1038/s41556-018-0146-8
Publication status	Published - Sept 2018

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FBP17 and CIP4_HAK_Accepted20June2018_GREEN AAMAccepted author manuscript, 6.8 MB

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Chan Wah Hak, L., Khan, S., Di Meglio, I., Law, A., Lucken-ardjomande Häsler, S., Quintaneiro, L. M., Ferreira, A. P. A., Krause, M., Mcmahon, H. T., & Boucrot, E. (2018). FBP17 and CIP4 recruit SHIP2 and lamellipodin to prime the plasma membrane for fast endophilin-mediated endocytosis. Nature Cell Biology, 20(9), 1023-1031. https://doi.org/10.1038/s41556-018-0146-8

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title = "FBP17 and CIP4 recruit SHIP2 and lamellipodin to prime the plasma membrane for fast endophilin-mediated endocytosis",

abstract = "Endocytosis mediates the cellular uptake of micronutrients and the turnover of plasma membrane proteins. Clathrin-mediated endocytosis is the major uptake pathway in resting cells1, but several clathrin-independent endocytic routes exist in parallel2,3. One such pathway, fast endophilin-mediated endocytosis (FEME), is not constitutive but triggered upon activation of certain receptors, including the β1 adrenergic receptor4. FEME activates promptly following stimulation as endophilin is pre-enriched by the phosphatidylinositol-3,4-bisphosphate-binding protein lamellipodin4,5. However, in the absence of stimulation, endophilin foci abort and disassemble after a few seconds. Looking for additional proteins involved in FEME, we found that 20 out of 65 BAR domain-containing proteins tested colocalized with endophilin spots. Among them, FBP17 and CIP4 prime the membrane of resting cells for FEME by recruiting the 5′-lipid phosphatase SHIP2 and lamellipodin to mediate the local production of phosphatidylinositol-3,4-bisphosphate and endophilin pre-enrichment. Membrane-bound GTP-loaded Cdc42 recruits FBP17 and CIP4, before being locally deactivated by RICH1 and SH3BP1 GTPase-activating proteins. This generates the transient assembly and disassembly of endophilin spots, which lasts 5–10 seconds. This mechanism periodically primes patches of the membrane for prompt responses upon FEME activation.",

author = "{Chan Wah Hak}, Laura and Shaheen Khan and {Di Meglio}, Ilaria and Ah-lai Law and {Lucken-ardjomande H{\"a}sler}, Safa and Quintaneiro, {Leonor M.} and Ferreira, {Antonio P. A.} and Matthias Krause and Mcmahon, {Harvey T.} and Emmanuel Boucrot",

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AU - Chan Wah Hak, Laura

AU - Khan, Shaheen

AU - Di Meglio, Ilaria

AU - Law, Ah-lai

AU - Lucken-ardjomande Häsler, Safa

AU - Quintaneiro, Leonor M.

AU - Ferreira, Antonio P. A.

AU - Krause, Matthias

AU - Mcmahon, Harvey T.

AU - Boucrot, Emmanuel

PY - 2018/9

Y1 - 2018/9

N2 - Endocytosis mediates the cellular uptake of micronutrients and the turnover of plasma membrane proteins. Clathrin-mediated endocytosis is the major uptake pathway in resting cells1, but several clathrin-independent endocytic routes exist in parallel2,3. One such pathway, fast endophilin-mediated endocytosis (FEME), is not constitutive but triggered upon activation of certain receptors, including the β1 adrenergic receptor4. FEME activates promptly following stimulation as endophilin is pre-enriched by the phosphatidylinositol-3,4-bisphosphate-binding protein lamellipodin4,5. However, in the absence of stimulation, endophilin foci abort and disassemble after a few seconds. Looking for additional proteins involved in FEME, we found that 20 out of 65 BAR domain-containing proteins tested colocalized with endophilin spots. Among them, FBP17 and CIP4 prime the membrane of resting cells for FEME by recruiting the 5′-lipid phosphatase SHIP2 and lamellipodin to mediate the local production of phosphatidylinositol-3,4-bisphosphate and endophilin pre-enrichment. Membrane-bound GTP-loaded Cdc42 recruits FBP17 and CIP4, before being locally deactivated by RICH1 and SH3BP1 GTPase-activating proteins. This generates the transient assembly and disassembly of endophilin spots, which lasts 5–10 seconds. This mechanism periodically primes patches of the membrane for prompt responses upon FEME activation.

AB - Endocytosis mediates the cellular uptake of micronutrients and the turnover of plasma membrane proteins. Clathrin-mediated endocytosis is the major uptake pathway in resting cells1, but several clathrin-independent endocytic routes exist in parallel2,3. One such pathway, fast endophilin-mediated endocytosis (FEME), is not constitutive but triggered upon activation of certain receptors, including the β1 adrenergic receptor4. FEME activates promptly following stimulation as endophilin is pre-enriched by the phosphatidylinositol-3,4-bisphosphate-binding protein lamellipodin4,5. However, in the absence of stimulation, endophilin foci abort and disassemble after a few seconds. Looking for additional proteins involved in FEME, we found that 20 out of 65 BAR domain-containing proteins tested colocalized with endophilin spots. Among them, FBP17 and CIP4 prime the membrane of resting cells for FEME by recruiting the 5′-lipid phosphatase SHIP2 and lamellipodin to mediate the local production of phosphatidylinositol-3,4-bisphosphate and endophilin pre-enrichment. Membrane-bound GTP-loaded Cdc42 recruits FBP17 and CIP4, before being locally deactivated by RICH1 and SH3BP1 GTPase-activating proteins. This generates the transient assembly and disassembly of endophilin spots, which lasts 5–10 seconds. This mechanism periodically primes patches of the membrane for prompt responses upon FEME activation.

U2 - 10.1038/s41556-018-0146-8

DO - 10.1038/s41556-018-0146-8

M3 - Article

SN - 1465-7392

VL - 20

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EP - 1031

JO - Nature Cell Biology

JF - Nature Cell Biology

IS - 9

ER -

FBP17 and CIP4 recruit SHIP2 and lamellipodin to prime the plasma membrane for fast endophilin-mediated endocytosis

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