Membrane localization is critical for activation of the PICK1 BAR domain

Kenneth L Madsen; Jacob Eriksen; Laura Milan-Lobo; Daniel S Han; Masha Y Niv; Ina Ammendrup-Johnsen; Ulla Henriksen; Vikram K Bhatia; Dimitrios Stamou; Harald H Sitte; Harvey T McMahon; Harel Weinstein; Ulrik Gether

doi:10.1111/j.1600-0854.2008.00761.x

Membrane localization is critical for activation of the PICK1 BAR domain

Kenneth L Madsen, Jacob Eriksen, Laura Milan-Lobo, Daniel S Han, Masha Y Niv, Ina Ammendrup-Johnsen, Ulla Henriksen, Vikram K Bhatia, Dimitrios Stamou, Harald H Sitte, Harvey T McMahon, Harel Weinstein, Ulrik Gether

40 Citations (Scopus)

Abstract

The PSD-95/Discs-large/ZO-1 homology (PDZ) domain protein, protein interacting with C kinase 1 (PICK1) contains a C-terminal Bin/amphiphysin/Rvs (BAR) domain mediating recognition of curved membranes; however, the molecular mechanisms controlling the activity of this domain are poorly understood. In agreement with negative regulation of the BAR domain by the N-terminal PDZ domain, PICK1 distributed evenly in the cytoplasm, whereas truncation of the PDZ domain caused BAR domain-dependent redistribution to clusters colocalizing with markers of recycling endosomal compartments. A similar clustering was observed both upon truncation of a short putative alpha-helical segment in the linker between the PDZ and the BAR domains and upon coexpression of PICK1 with a transmembrane PDZ ligand, including the alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor GluR2 subunit, the GluR2 C-terminus transferred to the single transmembrane protein Tac or the dopamine transporter C-terminus transferred to Tac. In contrast, transfer of the GluR2 C-terminus to cyan fluorescent protein, a cytosolic protein, did not elicit BAR domain-dependent clustering. Instead, localizing PICK1 to the membrane by introducing an N-terminal myristoylation site produced BAR domain-dependent, but ligand-independent, PICK1 clustering. The data support that in the absence of PDZ ligand, the PICK1 BAR domain is inhibited through a PDZ domain-dependent and linker-dependent mechanism. Moreover, they suggest that unmasking of the BAR domain's membrane-binding capacity is not a consequence of ligand binding to the PDZ domain per se but results from, and coincides with, recruitment of PICK1 to a membrane compartment.

Original language	English
Journal	Traffic - International Journal of Intracellular Transport
Volume	9
Issue number	8
Pages (from-to)	1327-43
Number of pages	16
ISSN	1398-9219
DOIs	https://doi.org/10.1111/j.1600-0854.2008.00761.x
Publication status	Published - 2008

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Madsen, K. L., Eriksen, J., Milan-Lobo, L., Han, D. S., Niv, M. Y., Ammendrup-Johnsen, I., Henriksen, U., Bhatia, V. K., Stamou, D., Sitte, H. H., McMahon, H. T., Weinstein, H., & Gether, U. (2008). Membrane localization is critical for activation of the PICK1 BAR domain. Traffic - International Journal of Intracellular Transport, 9(8), 1327-43. https://doi.org/10.1111/j.1600-0854.2008.00761.x

Madsen, KL, Eriksen, J, Milan-Lobo, L, Han, DS, Niv, MY, Ammendrup-Johnsen, I, Henriksen, U, Bhatia, VK, Stamou, D, Sitte, HH, McMahon, HT, Weinstein, H & Gether, U 2008, 'Membrane localization is critical for activation of the PICK1 BAR domain', Traffic - International Journal of Intracellular Transport, vol. 9, no. 8, pp. 1327-43. https://doi.org/10.1111/j.1600-0854.2008.00761.x

@article{c81745c0c79011debda0000ea68e967b,

title = "Membrane localization is critical for activation of the PICK1 BAR domain",

abstract = "The PSD-95/Discs-large/ZO-1 homology (PDZ) domain protein, protein interacting with C kinase 1 (PICK1) contains a C-terminal Bin/amphiphysin/Rvs (BAR) domain mediating recognition of curved membranes; however, the molecular mechanisms controlling the activity of this domain are poorly understood. In agreement with negative regulation of the BAR domain by the N-terminal PDZ domain, PICK1 distributed evenly in the cytoplasm, whereas truncation of the PDZ domain caused BAR domain-dependent redistribution to clusters colocalizing with markers of recycling endosomal compartments. A similar clustering was observed both upon truncation of a short putative alpha-helical segment in the linker between the PDZ and the BAR domains and upon coexpression of PICK1 with a transmembrane PDZ ligand, including the alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor GluR2 subunit, the GluR2 C-terminus transferred to the single transmembrane protein Tac or the dopamine transporter C-terminus transferred to Tac. In contrast, transfer of the GluR2 C-terminus to cyan fluorescent protein, a cytosolic protein, did not elicit BAR domain-dependent clustering. Instead, localizing PICK1 to the membrane by introducing an N-terminal myristoylation site produced BAR domain-dependent, but ligand-independent, PICK1 clustering. The data support that in the absence of PDZ ligand, the PICK1 BAR domain is inhibited through a PDZ domain-dependent and linker-dependent mechanism. Moreover, they suggest that unmasking of the BAR domain's membrane-binding capacity is not a consequence of ligand binding to the PDZ domain per se but results from, and coincides with, recruitment of PICK1 to a membrane compartment.",

author = "Madsen, {Kenneth L} and Jacob Eriksen and Laura Milan-Lobo and Han, {Daniel S} and Niv, {Masha Y} and Ina Ammendrup-Johnsen and Ulla Henriksen and Bhatia, {Vikram K} and Dimitrios Stamou and Sitte, {Harald H} and McMahon, {Harvey T} and Harel Weinstein and Ulrik Gether",

note = "Keywords: Animals; Biological Transport; COS Cells; Carrier Proteins; Cell Membrane; Cercopithecus aethiops; Gene Expression Regulation; Hippocampus; Ligands; Lipids; Models, Biological; Nuclear Proteins; Protein Conformation; Protein Structure, Secondary; Protein Structure, Tertiary; Rats",

year = "2008",

doi = "10.1111/j.1600-0854.2008.00761.x",

language = "English",

volume = "9",

pages = "1327--43",

journal = "Traffic - International Journal of Intracellular Transport",

issn = "1398-9219",

publisher = "Wiley-Blackwell",

number = "8",

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TY - JOUR

T1 - Membrane localization is critical for activation of the PICK1 BAR domain

AU - Madsen, Kenneth L

AU - Eriksen, Jacob

AU - Milan-Lobo, Laura

AU - Han, Daniel S

AU - Niv, Masha Y

AU - Ammendrup-Johnsen, Ina

AU - Henriksen, Ulla

AU - Bhatia, Vikram K

AU - Stamou, Dimitrios

AU - Sitte, Harald H

AU - McMahon, Harvey T

AU - Weinstein, Harel

AU - Gether, Ulrik

N1 - Keywords: Animals; Biological Transport; COS Cells; Carrier Proteins; Cell Membrane; Cercopithecus aethiops; Gene Expression Regulation; Hippocampus; Ligands; Lipids; Models, Biological; Nuclear Proteins; Protein Conformation; Protein Structure, Secondary; Protein Structure, Tertiary; Rats

PY - 2008

Y1 - 2008

N2 - The PSD-95/Discs-large/ZO-1 homology (PDZ) domain protein, protein interacting with C kinase 1 (PICK1) contains a C-terminal Bin/amphiphysin/Rvs (BAR) domain mediating recognition of curved membranes; however, the molecular mechanisms controlling the activity of this domain are poorly understood. In agreement with negative regulation of the BAR domain by the N-terminal PDZ domain, PICK1 distributed evenly in the cytoplasm, whereas truncation of the PDZ domain caused BAR domain-dependent redistribution to clusters colocalizing with markers of recycling endosomal compartments. A similar clustering was observed both upon truncation of a short putative alpha-helical segment in the linker between the PDZ and the BAR domains and upon coexpression of PICK1 with a transmembrane PDZ ligand, including the alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor GluR2 subunit, the GluR2 C-terminus transferred to the single transmembrane protein Tac or the dopamine transporter C-terminus transferred to Tac. In contrast, transfer of the GluR2 C-terminus to cyan fluorescent protein, a cytosolic protein, did not elicit BAR domain-dependent clustering. Instead, localizing PICK1 to the membrane by introducing an N-terminal myristoylation site produced BAR domain-dependent, but ligand-independent, PICK1 clustering. The data support that in the absence of PDZ ligand, the PICK1 BAR domain is inhibited through a PDZ domain-dependent and linker-dependent mechanism. Moreover, they suggest that unmasking of the BAR domain's membrane-binding capacity is not a consequence of ligand binding to the PDZ domain per se but results from, and coincides with, recruitment of PICK1 to a membrane compartment.

AB - The PSD-95/Discs-large/ZO-1 homology (PDZ) domain protein, protein interacting with C kinase 1 (PICK1) contains a C-terminal Bin/amphiphysin/Rvs (BAR) domain mediating recognition of curved membranes; however, the molecular mechanisms controlling the activity of this domain are poorly understood. In agreement with negative regulation of the BAR domain by the N-terminal PDZ domain, PICK1 distributed evenly in the cytoplasm, whereas truncation of the PDZ domain caused BAR domain-dependent redistribution to clusters colocalizing with markers of recycling endosomal compartments. A similar clustering was observed both upon truncation of a short putative alpha-helical segment in the linker between the PDZ and the BAR domains and upon coexpression of PICK1 with a transmembrane PDZ ligand, including the alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor GluR2 subunit, the GluR2 C-terminus transferred to the single transmembrane protein Tac or the dopamine transporter C-terminus transferred to Tac. In contrast, transfer of the GluR2 C-terminus to cyan fluorescent protein, a cytosolic protein, did not elicit BAR domain-dependent clustering. Instead, localizing PICK1 to the membrane by introducing an N-terminal myristoylation site produced BAR domain-dependent, but ligand-independent, PICK1 clustering. The data support that in the absence of PDZ ligand, the PICK1 BAR domain is inhibited through a PDZ domain-dependent and linker-dependent mechanism. Moreover, they suggest that unmasking of the BAR domain's membrane-binding capacity is not a consequence of ligand binding to the PDZ domain per se but results from, and coincides with, recruitment of PICK1 to a membrane compartment.

U2 - 10.1111/j.1600-0854.2008.00761.x

DO - 10.1111/j.1600-0854.2008.00761.x

M3 - Journal article

C2 - 18466293

SN - 1398-9219

VL - 9

SP - 1327

EP - 1343

JO - Traffic - International Journal of Intracellular Transport

JF - Traffic - International Journal of Intracellular Transport

IS - 8

ER -

Membrane localization is critical for activation of the PICK1 BAR domain

Abstract

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