Transmembrane domains control exclusion of membrane proteins from clathrin-coated pits

Efficient sorting of proteins is essential to allow transport between intracellular compartments while maintaining their specific composition. During endocytosis, membrane proteins can be concentrated in endocytic vesicles by specific interactions between their cytoplasmic domains and cytosolic coat proteins. It is, however, unclear whether they can be excluded from transport vesicles and what the determinants for this sorting could be. Here, we show that in the absence of cytosolic sorting signals, transmembrane domains control the access of surface proteins to endosomal compartments. They act in particular by determining the degree of exclusion of membrane proteins from endocytic clathrin-coated vesicles. When cytosolic endocytosis signals are present, it is the combination of cytosolic and transmembrane determinants that ultimately controls the efficiency with which a given transmembrane protein is endocytosed.

• Publication year

  2010

• Venue

  Journal of Cell Science

• Publication date

  2010-10-01

• Fields of study

  Biology, Medicine, Chemistry

• Identifiers
  DOI 10.1242/jcs.073031PMID 20826467
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Transmembrane domain–dependent partitioning of membrane proteins within the endoplasmic reticulum

  2008influential reference
• Identification of a Signal Peptide for Unconventional Secretion*

  2007cited by this paper
• Intracellular trafficking of the HCMV immunoevasin UL16 depends on elements present in both its cytoplasmic and transmembrane domains.

  2006cited by this paper
• Selective membrane exclusion in phagocytic and macropinocytic cups

  2006cited by this paper
• Dynamic transport of SNARE proteins in the Golgi apparatus.

  2005cited by this paper
• Two distinct TL-like molecular subsets defined by monoclonal antibodies on the surface of human thymocytes with different expression on leukemia lines

  2004cited by this paper
• Cargo recognition during clathrin-mediated endocytosis: a team effort.

  2004cited by this paper
• Direct Measurement of Antigen Binding Properties of CD1 Proteins Using Fluorescent Lipid Probes*

  2004cited by this paper
• GM1-containing lipid rafts are depleted within clathrin-coated pits.

  2003cited by this paper
• Signals for sorting of transmembrane proteins to endosomes and lysosomes.

  2003cited by this paper
• A resident Golgi protein is excluded from peri-Golgi vesicles in NRK cells

  2002cited by this paper
• The ubiquitin-dependent endocytosis motif is required for efficient incorporation of growth hormone receptor in clathrin-coated pits, but not clathrin-coated lattices.

  2001cited by this paper
• Cross-talk between Caveolae and Glycosylphosphatidylinositol-rich Domains*

  2001cited by this paper
• Down-regulation of cell surface receptors is modulated by polar residues within the transmembrane domain.

  2000cited by this paper
• Exclusion of Golgi Residents from Transport Vesicles Budding from Golgi Cisternae in Intact Cells

  2000cited by this paper
• Inhibition of clathrin-coated pit assembly by an Eps15 mutant.

  1999cited by this paper
• Cholesterol‐dependent retention of GPI‐anchored proteins in endosomes

  1998cited by this paper
• The tyrosine-containing cytoplasmic tail of CD1b is essential for its efficient presentation of bacterial lipid antigens.

  1998cited by this paper
• Transmembrane domain‐dependent sorting of proteins to the ER and plasma membrane in yeast

  1997cited by this paper
• The Transmembrane Domain of a Carboxyl-terminal Anchored Protein Determines Localization to the Endoplasmic Reticulum*

  1997cited by this paper
• Rab11 regulates recycling through the pericentriolar recycling endosome

  1996cited by this paper
• Insolubility and redistribution of GPI-anchored proteins at the cell surface after detergent treatment.

  1995cited by this paper
• An investigation of the role of transmembrane domains in Golgi protein retention.

  1995cited by this paper
• Retention of a cis Golgi protein requires polar residues on one face of a predicted alpha-helix in the transmembrane domain.

  1993cited by this paper
• Transmembrane domain length affects charge-mediated retention and degradation of proteins within the endoplasmic reticulum.

  1993cited by this paper
• Non-random distribution of amino acids in the transmembrane segments of human type I single span membrane proteins.

  1993cited by this paper
• Membrane protein sorting in the yeast secretory pathway: evidence that the vacuole may be the default compartment

  1992cited by this paper
• The protein tyrosine kinase p56lck inhibits CD4 endocytosis by preventing entry of CD4 into coated pits

  1992cited by this paper
• Sequences within and adjacent to the transmembrane segment of alpha-2,6-sialyltransferase specify Golgi retention.

  1991cited by this paper
• Differential endocytosis of CD4 in lymphocytic and nonlymphocytic cells

  1991cited by this paper
• Role of potentially charged transmembrane residues in targeting proteins for retention and degradation within the endoplasmic reticulum.

  1991cited by this paper
• Coated pits act as molecular filters.

  1980cited by this paper
• Improved mountant for immunofluorescence preparations.

  1974influential reference
• Monolayer cell culture of neonatal rat pancreas: an ultrastructural and biochemical study of functioning endocrine cells.

  1973cited by this paper
• A new technique for the assay of infectivity of human adenovirus 5 DNA.

  1973cited by this paper

• Improved CAR internalization and recycling through transmembrane domain optimization reduces CAR-T cytokine release and exhaustion

  2025cites this paper
• Short transmembrane domains target type II proteins to the Golgi apparatus and type I to the endoplasmic reticulum.

  2024cites this paper
• cis-B7:CD28 interactions at invaginated synaptic membranes provide CD28 co-stimulation and promote CD8+ T cell function and anti-tumor immunity.

  2023cites this paper
• Transcytosis and trans-synaptic retention by postsynaptic ErbB4 underlie axonal accumulation of NRG3

  2022cites this paper
• Should I stay or should I go? Golgi membrane spatial organization for protein sorting and retention.

  2021cites this paper
• Quality control of mislocalized and orphan proteins.

  2021cites this paper
• The AJ521 antibody detects the human CD1b protein by western blot

  2020cites this paper
• Biomimetic Magnetoliposomes as Oxaliplatin Nanocarriers: In Vitro Study for Potential Application in Colon Cancer

  2020cites this paper
• The AL626 antibody recognizes an ALFA-tagged recombinant protein by immuno-electron microscopy

  2020cites this paper
• The AJ521 antibody detects the human CD1b protein by flow cytometry

  2020cites this paper
• The AJ521 antibody labels the human CD1b protein by immunofluorescence

  2020cites this paper
• Ent3 and GGA adaptors facilitate diverse anterograde and retrograde trafficking events to and from the prevacuolar endosome

  2019cites this paper
• Oxaliplatin–Biomimetic Magnetic Nanoparticle Assemblies for Colon Cancer-Targeted Chemotherapy: An In Vitro Study

  2019cites this paper
• Mucin‐coating technologies for protection and reduced aggregation of cellular production systems

  2019cites this paper
• Sequence-specific Mucins for Glycocalyx Engineering.

  2019cites this paper
• TM9SF4 levels determine sorting of transmembrane domains in the early secretory pathway

  2018cites this paper
• Signal-anchor sequences are an essential factor for the Golgi-plasma membrane localization of type II membrane proteins

  2018cites this paper
• The shape of the transmembrane domain is a novel endocytosis signal for single-spanning membrane proteins

  2017influential citation
• Genetically Encoded Toolbox for Glycocalyx Engineering: Tunable Control of Cell Adhesion, Survival, and Cancer Cell Behaviors.

  2017cites this paper
• Transmembrane Domain Lengths Serve as Signatures of Organismal Complexity and Viral Transport Mechanisms

  2016cites this paper
• Modulation of Intracellular Quantum Dot to Fluorescent Protein Förster Resonance Energy Transfer via Customized Ligands and Spatial Control of Donor–Acceptor Assembly

  2015cites this paper
• TM9 family proteins control surface targeting of glycine-rich transmembrane domains

  2015cites this paper
• An investigation of the effect of membrane curvature on transmembrane-domain dependent protein sorting in lipid bilayers

  2014cites this paper
• Golgi-Dependent Transport of Vacuolar Sorting Receptors Is Regulated by COPII, AP1, and AP4 Protein Complexes in Tobacco[W][OPEN]

  2014cites this paper
• Routes to and from the plasma membrane: bulk flow versus signal mediated endocytosis

  2014cites this paper
• Anchors aweigh: protein localization and transport mediated by transmembrane domains

  2013cites this paper
• Organelles and signals controlling vacuolar sortingreceptor trafficking in plants

  2013cites this paper
• Host-pathogen interactions: from bacterial virulence to host defense

  2012cites this paper
• TM9/Phg1 and SadA proteins control surface expression and stability of SibA adhesion molecules in Dictyostelium

  2012cites this paper
• A Systematic Approach to Pair Secretory Cargo Receptors with Their Cargo Suggests a Mechanism for Cargo Selection by Erv14

  2012cites this paper
• A new approach to improve the quality of ultrathin cryo-sections; its use for immunogold EM and correlative electron cryo-tomography.

  2011cites this paper