Tian Jin, Ning Zhang, Yu Long, Carole A. Parent, Peter N. Devreotes ^*

Gradients of chemoattractants elicit signaling events at the leading edge of a cell even though chemoattractant receptors are uniformly distributed on the cell surface. In highly polarized Dictyostelium discoideum amoebas, membrane-associated subunits of heterotrimeric guanine nucleotide-binding proteins (G proteins) were localized in a shallow anterior-posterior gradient. A uniformly applied chemoattractant generated binding sites for pleckstrin homology (PH) domains on the inner surface of the membrane in a pattern similar to that of the G subunits. Loss of cell polarity resulted in uniform distribution of both the G subunits and the sensitivity of PH domain recruitment. These observations indicate that G subunits are not sufficiently localized to restrict signaling events to the leading edge but that their distribution may determine the relative chemotactic sensitivity of polarized cells.

Department of Biological Chemistry, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
^*   To whom correspondence should be addressed. E-mail: pnd{at}welchlink.welch.jhu.edu

Dictyostelium Ric8 is a nonreceptor guanine exchange factor for heterotrimeric G proteins and is important for development and chemotaxis.

R. Kataria, X. Xu, F. Fusetti, I. Keizer-Gunnink, T. Jin, P. J. M. van Haastert, and A. Kortholt (2013)
PNAS 110, 6424-6429
 |  Abstract »  |  Full Text »  |  PDF »

Molecular Basis of Dynamic Relocalization of Dictyostelium Myosin IB.

H. Brzeska, J. Guag, G. M. Preston, M. A. Titus, and E. D. Korn (2012)
J. Biol. Chem. 287, 14923-14936
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Tyrosine Phosphorylation of the G{alpha}-Interacting Protein GIV Promotes Activation of Phosphoinositide 3-Kinase During Cell Migration.

C. Lin, J. Ear, Y. Pavlova, Y. Mittal, I. Kufareva, M. Ghassemian, R. Abagyan, M. Garcia-Marcos, and P. Ghosh (2011)
Science Signaling 4, ra64
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Coupling Mechanism of a GPCR and a Heterotrimeric G Protein During Chemoattractant Gradient Sensing in Dictyostelium.

X. Xu, T. Meckel, J. A. Brzostowski, J. Yan, M. Meier-Schellersheim, and T. Jin (2010)
Science Signaling 3, ra71
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Chemotaxis: insights from the extending pseudopod.

P. J. M. Van Haastert (2010)
J. Cell Sci. 123, 3031-3037
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Mobility of G proteins is heterogeneous and polarized during chemotaxis.

F. van Hemert, M. D. Lazova, B. E. Snaar-Jagaska, and T. Schmidt (2010)
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External and internal constraints on eukaryotic chemotaxis.

D. Fuller, W. Chen, M. Adler, A. Groisman, H. Levine, W.-J. Rappel, and W. F. Loomis (2010)
PNAS 107, 9656-9659
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Molecular regulators of leucocyte chemotaxis during inflammation.

C. H. Y. Wong, B. Heit, and P. Kubes (2010)
Cardiovasc Res 86, 183-191
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The G protein {beta}{gamma} subunit mediates reannealing of adherens junctions to reverse endothelial permeability increase by thrombin.

N. Knezevic, M. Tauseef, T. Thennes, and D. Mehta (2009)
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The Signaling Mechanisms Underlying Cell Polarity and Chemotaxis.

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A Bayesian model predicts the response of axons to molecular gradients.

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PNAS 106, 10296-10301
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RACK1 Regulates Directional Cell Migration by Acting on G{beta}{gamma} at the Interface with Its Effectors PLC{beta} and PI3K{gamma}.

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Immunostaining evidence for PI(4,5)P2 localization at the leading edge of chemoattractant-stimulated HL-60 cells.

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Activation of G{alpha}i3 triggers cell migration via regulation of GIV.

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Neurotrophin-Dependent Dendritic Filopodial Motility: A Convergence on PI3K Signaling.

B. W. Luikart, W. Zhang, G. A. Wayman, C.-H. Kwon, G. L. Westbrook, and L. F. Parada (2008)
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A spatially restricted increase in receptor mobility is involved in directional sensing during Dictyostelium discoideum chemotaxis.

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Phosducin interacts with the G-protein {beta}{gamma}-dimer of ciliate protozoan Blepharisma japonicum upon illumination.

K. Sobierajska, H. Fabczak, and S. Fabczak (2007)
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Locally controlled inhibitory mechanisms are involved in eukaryotic GPCR-mediated chemosensing.

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Isoprenylcysteine Carboxy Methylation Is Essential for Development in Dictyostelium discoideum.

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A Cell Number-Counting Factor Regulates Levels of a Novel Protein, SslA, as Part of a Group Size Regulation Mechanism in Dictyostelium.

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Attenuation of Phospholipid Signaling Provides a Novel Mechanism for the Action of Valproic Acid.

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Directional sensing in eukaryotic chemotaxis: A balanced inactivation model.

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The Phosducin-Like Protein PhLP1 Is Essential for G{beta}{gamma} Dimer Formation in Dictyostelium discoideum.

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Neutrophils Lacking Platelet-Endothelial Cell Adhesion Molecule-1 Exhibit Loss of Directionality and Motility in CXCR2-Mediated Chemotaxis.

Y. Wu, P. Stabach, M. Michaud, and J. A. Madri (2005)
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Controlling Cell Behavior Electrically: Current Views and Future Potential.

C. D. McCaig, A. M. Rajnicek, B. Song, and M. Zhao (2005)
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G protein {beta} interacts with the glucocorticoid receptor and suppresses its transcriptional activity in the nucleus.

T. Kino, A. Tiulpakov, T. Ichijo, L. Chheng, T. Kozasa, and G. P. Chrousos (2005)
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The Macrophage-derived Lectin, MNCF, Activates Neutrophil Migration through a Pertussis Toxin-sensitive Pathway.

A. N. Moreno, G. Pereira-da-Silva, C. Oliver, M. C. Jamur, A. Panunto-Castelo, and M. C. Roque-Barreira (2005)
Journal of Histochemistry & Cytochemistry 53, 715-723
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Cyclic AMP mediates keratinocyte directional migration in an electric field.

C. E. Pullar and R. R. Isseroff (2005)
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PldB, a Putative Phospholipase D Homologue in Dictyostelium discoideum Mediates Quorum Sensing during Development.

Y. Chen, V. Rodrick, Y. Yan, and D. Brazill (2005)
Eukaryot. Cell 4, 694-702
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Quantitative Imaging of Single Live Cells Reveals Spatiotemporal Dynamics of Multistep Signaling Events of Chemoattractant Gradient Sensing in Dictyostelium.

X. Xu, M. Meier-Schellersheim, X. Jiao, L. E. Nelson, and T. Jin (2005)
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A Quantitative High-Throughput Endothelial Cell Migration Assay.

V. Mastyugin, E. McWhinnie, M. Labow, and F. Buxton (2004)
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Dictyostelium PAKc Is Required for Proper Chemotaxis.

S. Lee, F. Rivero, K. C. Park, E. Huang, S. Funamoto, and R. A. Firtel (2004)
Mol. Biol. Cell 15, 5456-5469
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Localized Ras signaling at the leading edge regulates PI3K, cell polarity, and directional cell movement.

A. T. Sasaki, C. Chun, K. Takeda, and R. A. Firtel (2004)
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The C-terminal domain LLKIL motif of CXCR2 is required for ligand-mediated polarization of early signals during chemotaxis.

J. Sai, G.-H. Fan, D. Wang, and A. Richmond (2004)
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Moving Forward: Mechanisms of Chemoattractant Gradient Sensing.

J. Franca-Koh and P. N. Devreotes (2004)
Physiology 19, 300-308
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Chemoattractant-induced phosphatidylinositol 3,4,5-trisphosphate accumulation is spatially amplified and adapts, independent of the actin cytoskeleton.

C. Janetopoulos, L. Ma, P. N. Devreotes, and P. A. Iglesias (2004)
PNAS 101, 8951-8956
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Sensitization of Dictyostelium chemotaxis by phosphoinositide-3-kinase-mediated self-organizing signalling patches.

M. Postma, J. Roelofs, J. Goedhart, H. M. Loovers, A. J. W. G. Visser, and P. J. M. Van Haastert (2004)
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Signaling in Leukocyte Transendothelial Migration.

J. D. van Buul and P. L. Hordijk (2004)
Arterioscler Thromb Vasc Biol 24, 824-833
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Novel Mechanism of PTEN Regulation by Its Phosphatidylinositol 4,5-Bisphosphate Binding Motif Is Critical for Chemotaxis.

M. Iijima, Y. E. Huang, H. R. Luo, F. Vazquez, and P. N. Devreotes (2004)
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A G{alpha}-dependent pathway that antagonizes multiple chemoattractant responses that regulate directional cell movement.

J. A. Brzostowski, C. A. Parent, and A. R. Kimmel (2004)
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G{beta}{gamma} Mediates the Interplay between Tubulin Dimers and Microtubules in the Modulation of Gq Signaling.

J. S. Popova and M. M. Rasenick (2003)
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Leading the way: directional sensing through phosphatidylinositol 3-kinase and other signaling pathways.

S. Merlot and R. A. Firtel (2003)
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Leukocyte-Endothelium Interaction Promotes SDF-1-dependent Polarization of CXCR4.

J. D. van Buul, C. Voermans, J. van Gelderen, E. C. Anthony, C. E. van der Schoot, and P. L. Hordijk (2003)
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Eukaryotic Chemotaxis: Distinctions between Directional Sensing and Polarization.

P. Devreotes and C. Janetopoulos (2003)
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Receptor-mediated Regulation of PI3Ks Confines PI(3,4,5)P3 to the Leading Edge of Chemotaxing Cells.

Y. E. Huang, M. Iijima, C. A. Parent, S. Funamoto, R. A. Firtel, and P. Devreotes (2003)
Mol. Biol. Cell 14, 1913-1922
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ERK and RhoA Differentially Regulate Pseudopodia Growth and Retraction during Chemotaxis.

A. A. Brahmbhatt and R. L. Klemke (2003)
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Membrane Lipid Organization Is Critical for Human Neutrophil Polarization.

L. M. Pierini, R. J. Eddy, M. Fuortes, S. Seveau, C. Casulo, and F. R. Maxfield (2003)
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Gradient Steepness Influences the Pathfinding Decisions of Neuronal Growth Cones In Vivo.

C. M. Isbister, P. J. Mackenzie, K. C. W. To, and T. P. O'Connor (2003)
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Electrical cues regulate the orientation and frequency of cell division and the rate of wound healing in vivo.

B. Song, M. Zhao, J. V. Forrester, and C. D. McCaig (2002)
PNAS 99, 13577-13582
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Polarization of Myosin II Heavy Chain-Protein Kinase C in Chemotaxing Dictyostelium Cells.

H. Rubin and S. Ravid (2002)
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Cells Respond to and Bind Countin, a Component of a Multisubunit Cell Number Counting Factor.

T. Gao, K. Ehrenman, L. Tang, M. Leippe, D. A. Brock, and R. H. Gomer (2002)
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A Single Cell Density-sensing Factor Stimulates Distinct Signal Transduction Pathways through Two Different Receptors.

W. J. Deery, T. Gao, R. Ammann, and R. H. Gomer (2002)
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Genetic analysis of the role of G protein-coupled receptor signaling in electrotaxis.

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Increased responsiveness of murine eosinophils to MIP-1{beta} (CCL4) and TCA-3 (CCL1) is mediated by their specific receptors, CCR5 and CCR8.

S. H. P. Oliveira, S. Lira, C. Martinez-A, M. Wiekowski, L. Sullivan, and N. W. Lukacs (2002)
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Asymmetric cell division: microtubule dynamics and spindle asymmetry.

J. A. Kaltschmidt and A. H. Brand (2002)
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A Highly Effective Dominant Negative alpha s Construct Containing Mutations That Affect Distinct Functions Inhibits Multiple Gs-coupled Receptor Signaling Pathways.

C. H. Berlot (2002)
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CHEMOTACTIC SIGNALING PATHWAYS IN NEUTROPHILS: FROM RECEPTOR TO ACTIN ASSEMBLY.

G. Cicchetti, P. G. Allen, and M. Glogauer (2002)
Critical Reviews in Oral Biology & Medicine 13, 220-228
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Regulation of endothelial cell branching morphogenesis by endogenous chemokine stromal-derived factor-1.

O. Salvucci, L. Yao, S. Villalba, A. Sajewicz, S. Pittaluga, and G. Tosato (2002)
Blood 99, 2703-2711
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Purification of pseudopodia from polarized cells reveals redistribution and activation of Rac through assembly of a CAS/Crk scaffold.

S. Y. Cho and R. L. Klemke (2002)
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Functional expression and FRET analysis of green fluorescent proteins fused to G-protein subunits in rat sympathetic neurons.

V. Ruiz-Velasco and S. R Ikeda (2001)
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EDG-1 links the PDGF receptor to Src and focal adhesion kinase activation leading to lamellipodia formation and cell migration.

H. M. ROSENFELDT, J. P. HOBSON, M. MACEYKA, A. OLIVERA, V. E. NAVA, S. MILSTIEN, and S. SPIEGEL (2001)
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Single Nucleotide Polymorphism of Human Platelet-activating Factor Receptor Impairs G-protein Activation.

K. Fukunaga, S. Ishii, K. Asano, T. Yokomizo, T. Shiomi, T. Shimizu, and K. Yamaguchi (2001)
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Cytoskeleton-dependent Membrane Domain Segregation during Neutrophil Polarization.

S. Seveau, R. J. Eddy, F. R. Maxfield, and L. M. Pierini (2001)
Mol. Biol. Cell 12, 3550-3562
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Single-Molecule Analysis of Chemotactic Signaling in Dictyostelium Cells.

M. Ueda, Y. Sako, T. Tanaka, P. Devreotes, and T. Yanagida (2001)
Science 294, 864-867
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Amoeboid leukocyte crawling through extracellular matrix: lessons from the Dictyostelium paradigm of cell movement.

P. Friedl, S. Borgmann, and E.-B. Brocker (2001)
J. Leukoc. Biol. 70, 491-509
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Abnormal Migration Phenotype of Mitogen-Activated Protein Kinase-Activated Protein Kinase 2-/- Neutrophils in Zigmond Chambers Containing Formyl-Methionyl-Leucyl-Phenylalanine Gradients.

M. O. Hannigan, L. Zhan, Y. Ai, A. Kotlyarov, M. Gaestel, and C.-K. Huang (2001)
J. Immunol. 167, 3953-3961
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Ggamma in Dictyostelium: Its Role in Localization of Gbeta gamma to the Membrane Is Required for Chemotaxis in Shallow Gradients.

N. Zhang, Y. Long, and P. N. Devreotes (2001)
Mol. Biol. Cell 12, 3204-3213
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Receptor-Mediated Activation of Heterotrimeric G-Proteins in Living Cells.

C. Janetopoulos, T. Jin, and P. Devreotes (2001)
Science 291, 2408-2411
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High-efficiency transient transfection of endothelial cells for functional analysis.

A. T. KOVALA, K. A. HARVEY, P. McGLYNN, G. BOGUSLAWSKI, J. G. N. GARCIA, and D. ENGLISH (2000)
FASEB J 14, 2486-2494
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Cellular signaling in macrophage migration and chemotaxis.

G. E. Jones (2000)
J. Leukoc. Biol. 68, 593-602
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Roles of phospholipid signaling in chemoattractant-induced responses.

D. Wu, C. K. Huang, and H. Jiang (2000)
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The Internal Phosphodiesterase RegA Is Essential for the Suppression of Lateral Pseudopods during Dictyostelium Chemotaxis.

D. J. Wessels, H. Zhang, J. Reynolds, K. Daniels, P. Heid, S. Lu, A. Kuspa, G. Shaulsky, W. F. Loomis, and D. R. Soll (2000)
Mol. Biol. Cell 11, 2803-2820
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SIGNAL TRANSDUCTION:Signals to Move Cells.

L. V. Dekker and A. W. Segal (2000)
Science 287, 982-985
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Visualization of a Functional Galpha q-Green Fluorescent Protein Fusion in Living Cells. ASSOCIATION WITH THE PLASMA MEMBRANE IS DISRUPTED BY MUTATIONAL ACTIVATION AND BY ELIMINATION OF PALMITOYLATION SITES, BUT NOT BY ACTIVATION MEDIATED BY RECEPTORS OR AlF4-.

T. E. Hughes, H. Zhang, D. E. Logothetis, and C. H. Berlot (2001)
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Nuclear Localization of G Protein beta 5 and Regulator of G Protein Signaling 7 in Neurons and Brain.

J.-H. Zhang, V. A. Barr, Y. Mo, A. M. Rojkova, S. Liu, and W. F. Simonds (2001)
J. Biol. Chem. 276, 10284-10289
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Role of Phosphoinositide 3-Kinase in Monocyte Recruitment under Flow Conditions.

R. E. Gerszten, E. B. Friedrich, T. Matsui, R. R. Hung, L. Li, T. Force, and A. Rosenzweig (2001)
J. Biol. Chem. 276, 26846-26851
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A Cell Number-counting Factor Regulates Group Size in Dictyostelium by Differentially Modulating cAMP-induced cAMP and cGMP Pulse Sizes.

L. Tang, R. Ammann, T. Gao, and R. H. Gomer (2001)
J. Biol. Chem. 276, 27663-27669
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Purification of pseudopodia from polarized cells reveals redistribution and activation of Rac through assembly of a CAS/Crk scaffold.

S. Y. Cho and R. L. Klemke (2002)
J. Cell Biol. 156, 725-736
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