Self‐organization of apical membrane protein sorting in epithelial cells

Polarized epithelial cells are characterized by the asymmetric distribution of proteins between apical and basolateral domains of the plasma membrane. This asymmetry is highly conserved and is fundamental to epithelial cell physiology, development, and homeostasis. How proteins are segregated for ap...

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Bibliographic Details
Published inThe FEBS journal Vol. 289; no. 3; pp. 659 - 670
Main Authors Levic, Daniel S., Bagnat, Michel
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.02.2022
Subjects
Animals
apical sorting
asymmetry
Cell Line
Cell Membrane - genetics
cell physiology
Cell Polarity - genetics
epithelial cell
Epithelial cells
Epithelial Cells - cytology
Epithelial Cells - metabolism
Epithelium
Glycan
Glycosylation
Golgi Apparatus - genetics
Homeostasis
Hydrogen-Ion Concentration
Ions
Lipids
Membrane proteins
Membrane Proteins - genetics
Membranes
Oligomerization
Phase separation
plasma membrane
Polysaccharides - genetics
Protein transport
Protein Transport - genetics
Proteins
separation
Skewed distributions
Vacuolar Proton-Translocating ATPases - genetics
V‐ATPase
zebrafish
Zebrafish - genetics
Zebrafish - growth & development
Zebrafish Proteins - genetics
V-ATPase
zebrafish
oligomerization
epithelial cell
apical sorting
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Abstract Polarized epithelial cells are characterized by the asymmetric distribution of proteins between apical and basolateral domains of the plasma membrane. This asymmetry is highly conserved and is fundamental to epithelial cell physiology, development, and homeostasis. How proteins are segregated for apical or basolateral delivery, a process known as sorting, has been the subject of considerable investigation for decades. Despite these efforts, the rules guiding apical sorting are poorly understood and remain controversial. Here, we consider mechanisms of apical membrane protein sorting and argue that they are largely driven by self‐organization and biophysical principles. The preponderance of data to date is consistent with the idea that apical sorting is not ruled by a dedicated protein‐based sorting machinery and relies instead on the concerted effects of oligomerization, phase separation of lipids and proteins in membranes, and pH‐dependent glycan interactions. Despite extensive investigation, the mechanisms targeting membrane proteins to the apical surface are not well understood. In this Viewpoint, we survey historical findings and recent advances in membrane protein sorting. We argue that apical sorting, through diverse mechanisms, is organized by biophysical phenomena of cargo segregation driven by oligomerization and phase separation. Evidence suggests that the molecular interactions underlying apical segregation of O‐glycosylated membrane proteins are regulated by luminal acidification.
AbstractList Polarized epithelial cells are characterized by the asymmetric distribution of proteins between apical and basolateral domains of the plasma membrane. This asymmetry is highly conserved and is fundamental to epithelial cell physiology, development, and homeostasis. How proteins are segregated for apical or basolateral delivery, a process known as sorting, has been the subject of considerable investigation for decades. Despite these efforts, the rules guiding apical sorting are poorly understood and remain controversial. Here, we consider mechanisms of apical membrane protein sorting and argue that they are largely driven by self-organization and biophysical principles. The preponderance of data to date is consistent with the idea that apical sorting is not ruled by a dedicated protein-based sorting machinery and relies instead on the concerted effects of oligomerization, phase separation of lipids and proteins in membranes, and pH-dependent glycan interactions.Polarized epithelial cells are characterized by the asymmetric distribution of proteins between apical and basolateral domains of the plasma membrane. This asymmetry is highly conserved and is fundamental to epithelial cell physiology, development, and homeostasis. How proteins are segregated for apical or basolateral delivery, a process known as sorting, has been the subject of considerable investigation for decades. Despite these efforts, the rules guiding apical sorting are poorly understood and remain controversial. Here, we consider mechanisms of apical membrane protein sorting and argue that they are largely driven by self-organization and biophysical principles. The preponderance of data to date is consistent with the idea that apical sorting is not ruled by a dedicated protein-based sorting machinery and relies instead on the concerted effects of oligomerization, phase separation of lipids and proteins in membranes, and pH-dependent glycan interactions.
Polarized epithelial cells are characterized by the asymmetric distribution of proteins between apical and basolateral domains of the plasma membrane. This asymmetry is highly conserved and is fundamental to epithelial cell physiology, development, and homeostasis. How proteins are segregated for apical or basolateral delivery, a process known as sorting, has been the subject of considerable investigation for decades. Despite these efforts, the rules guiding apical sorting are poorly understood and remain controversial. Here, we consider mechanisms of apical membrane protein sorting and argue that they are largely driven by self‐organization and biophysical principles. The preponderance of data to date is consistent with the idea that apical sorting is not ruled by a dedicated protein‐based sorting machinery and relies instead on the concerted effects of oligomerization, phase separation of lipids and proteins in membranes, and pH‐dependent glycan interactions.
Polarized epithelial cells are characterized by the asymmetric distribution of proteins between apical and basolateral domains of the plasma membrane. This asymmetry is highly conserved and is fundamental to epithelial cell physiology, development, and homeostasis. How proteins are segregated for apical or basolateral delivery, a process known as sorting, has been the subject of considerable investigation for decades. Despite these efforts, the rules guiding apical sorting are poorly understood and remain controversial. Here, we consider mechanisms of apical membrane protein sorting and argue that they are largely driven by self-organization and biophysical principles. The preponderance of data to date are consistent with the idea that apical sorting is not ruled by a dedicated protein-based sorting machinery and relies instead on the concerted effects of oligomerization, phase separation of lipids and proteins in membranes, and pH-dependent glycan interactions.
Polarized epithelial cells are characterized by the asymmetric distribution of proteins between apical and basolateral domains of the plasma membrane. This asymmetry is highly conserved and is fundamental to epithelial cell physiology, development, and homeostasis. How proteins are segregated for apical or basolateral delivery, a process known as sorting, has been the subject of considerable investigation for decades. Despite these efforts, the rules guiding apical sorting are poorly understood and remain controversial. Here, we consider mechanisms of apical membrane protein sorting and argue that they are largely driven by self‐organization and biophysical principles. The preponderance of data to date is consistent with the idea that apical sorting is not ruled by a dedicated protein‐based sorting machinery and relies instead on the concerted effects of oligomerization, phase separation of lipids and proteins in membranes, and pH‐dependent glycan interactions. Despite extensive investigation, the mechanisms targeting membrane proteins to the apical surface are not well understood. In this Viewpoint, we survey historical findings and recent advances in membrane protein sorting. We argue that apical sorting, through diverse mechanisms, is organized by biophysical phenomena of cargo segregation driven by oligomerization and phase separation. Evidence suggests that the molecular interactions underlying apical segregation of O‐glycosylated membrane proteins are regulated by luminal acidification.
Author Levic, Daniel S.
Bagnat, Michel
AuthorAffiliation 1 Department of Cell Biology, Duke University, Durham, NC 27710, USA
AuthorAffiliation_xml – name: 1 Department of Cell Biology, Duke University, Durham, NC 27710, USA
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  givenname: Daniel S.
  orcidid: 0000-0003-0240-5178
  surname: Levic
  fullname: Levic, Daniel S.
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  givenname: Michel
  orcidid: 0000-0002-3829-0168
  surname: Bagnat
  fullname: Bagnat, Michel
  email: michel.bagnat@duke.edu
  organization: Duke University
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Cites_doi 10.1042/BJ20130933
10.1038/sj.emboj.7601813
10.1074/jbc.273.46.30263
10.1016/j.febslet.2004.11.106
10.1053/j.gastro.2013.05.013
10.1242/dev.076711
10.1073/pnas.151111298
10.1021/jp405063h
10.1089/ars.2017.7389
10.1242/jcs.036038
10.1101/cshperspect.a004697
10.1126/science.2945253
10.1073/pnas.1012424107
10.1091/mbc.e09-03-0193
10.1016/j.chemphyslip.2015.07.022
10.1038/s41589-020-0529-6
10.1016/j.molcel.2020.09.029
10.1074/jbc.274.6.3910
10.1073/pnas.1304168111
10.1083/jcb.200901145
10.1038/nrm3775
10.1016/S0092-8674(88)80026-6
10.1073/pnas.0509107102
10.1083/jcb.142.1.51
10.1038/35055042
10.1126/science.aaw9544
10.1016/j.devcel.2013.10.006
10.1083/jcb.200309005
10.1091/mbc.E16-02-0096
10.1091/mbc.E18-12-0811
10.1152/ajpcell.00514.2002
10.1073/pnas.1016184107
10.1083/jcb.146.2.313
10.1515/BC.2002.169
10.1016/j.ejcb.2010.07.001
10.1111/tra.12086
10.1016/j.tibs.2015.08.005
10.1091/mbc.E05-09-0873
10.1093/emboj/16.18.5501
10.1038/ncb2541
10.1038/378096a0
10.1074/jbc.M112.415596
10.1038/s41467-017-01328-3
10.1016/S0092-8674(00)81650-5
10.1016/j.bbamcr.2008.10.016
10.1073/pnas.97.7.3254
10.1016/S0074-7696(03)01005-2
10.1172/JCI7453
10.1016/0092-8674(91)90139-P
10.1242/jcs.032615
10.1083/jcb.201908225
10.1681/ASN.2013080883
10.1242/dev.077347
10.1083/jcb.142.6.1413
10.1083/jcb.200603132
10.1016/j.neulet.2004.04.002
10.1083/jcb.200212004
10.1016/S0021-9258(18)43616-2
10.1016/0092-8674(92)90189-J
10.1016/j.cub.2005.12.046
10.1096/fj.201601386R
10.1038/ncb1109
10.1091/mbc.E12-04-0329
10.1101/cshperspect.a027847
10.1146/annurev.iy.12.040194.000431
10.1111/j.1600-0854.2007.00539.x
10.1091/mbc.E08-05-0478
10.1039/C9SM00579J
10.1016/j.devcel.2012.02.004
10.1016/j.abb.2004.02.032
10.1016/S0021-9258(17)42002-3
10.1172/JCI35541
10.1091/mbc.e13-02-0078
10.1016/0092-8674(95)90380-1
10.1083/jcb.103.6.2565
10.1016/j.bpj.2015.07.036
10.1083/jcb.109.5.2145
10.1111/j.1600-0854.2009.00941.x
10.1016/S0021-9258(18)66848-6
10.1016/S0021-9258(19)50263-0
10.1006/excr.1994.1222
10.1016/j.cell.2020.09.021
10.1083/jcb.139.4.929
10.1021/bi992132e
10.1038/ncb2106
10.1073/pnas.74.5.2026
10.1073/pnas.1718921115
10.1083/jcb.116.3.577
10.1083/jcb.200911083
10.1083/jcb.148.3.495
10.1083/jcb.98.4.1304
10.1083/jcb.200407094
10.1006/excr.2001.5442
10.1242/jcs.020800
10.1038/cr.2012.64
10.1083/jcb.200407072
10.1016/j.febslet.2009.10.053
10.1091/mbc.E11-04-0320
10.1242/jcs.158550
10.1038/s42003-021-01693-2
10.1083/jcb.200407073
10.1172/JCI0216390
10.1091/mbc.E06-07-0629
10.1016/j.tcb.2020.01.009
10.1073/pnas.1821076116
10.1242/jcs.213199
10.1111/tra.12548
10.1091/mbc.12.12.4129
10.1038/35054500
10.1016/0092-8674(92)90551-M
10.1002/j.1460-2075.1985.tb03629.x
10.1016/0092-8674(91)90437-4
10.1038/ncb2328
10.1083/jcb.121.5.1031
10.1038/ncb1773
10.1016/0092-8674(84)90315-5
10.1126/science.2110383
10.1242/jcs.01386
10.1111/j.1600-0854.2008.00826.x
10.1073/pnas.0610700104
10.1128/jvi.70.9.6508-6515.1996
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Keywords V-ATPase
zebrafish
oligomerization
epithelial cell
apical sorting
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References 2010; 12
2004; 167
2007; 104
2004; 165
2010; 107
2002; 273
2010; 189
2019; 15
2005; 579
2006; 173
2020; 16
2004; 6
2014; 25
1995; 378
1996; 70
2012; 14
2009; 119
1993; 121
1980; 255
1998; 273
1989; 109
2014; 127
1986; 103
2009; 10
1994; 269
2005; 102
2002; 383
2000; 97
2013; 117
2007; 8
1992; 116
2003; 162
2014; 15
2009; 122
2012; 23
2012; 22
2012; 139
2009; 1793
2020; 219
2003; 284
2007; 18
1990; 248
1986; 234
2019; 30
2011; 3
1999; 104
2008; 121
2004; 426
2018; 19
2015; 192
2003; 226
1984; 37
2020; 30
1991; 66
2018; 115
1994; 12
2009; 583
2009; 185
2016; 27
1998; 142
2014; 457
2004; 363
2017; 8
1994; 213
2013; 27
2002; 110
2013; 24
2008; 9
2013; 288
2011; 13
2015; 109
2020; 367
2017; 9
2018; 131
2017; 31
2013; 14
2015; 40
1984; 98
1986; 261
2019; 116
1999; 99
2011; 22
1977; 74
1997; 16
2001; 12
2007; 26
2001; 98
1997; 139
2021; 4
2009; 21
1985; 4
2006; 16
2008; 19
2020; 80
2020; 183
2013; 145
1999; 146
2008; 10
2001; 409
1988; 52
1993; 268
2014; 111
1992; 71
2010; 89
1995; 81
2000; 39
2000; 148
2005; 168
2005; 169
1999; 274
2001; 3
1992; 68
2004; 117
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References_xml – volume: 169
  start-page: 491
  year: 2005
  end-page: 501
  article-title: Galectin‐4 and sulfatides in apical membrane trafficking in enterocyte‐like cells
  publication-title: J Cell Biol
– volume: 255
  start-page: 6633
  year: 1980
  end-page: 6639
  article-title: Biosynthetic intermediates of beta‐glucuronidase contain high mannose oligosaccharides with blocked phosphate residues
  publication-title: J Biol Chem
– volume: 145
  start-page: 625
  year: 2013
  end-page: 635
  article-title: AP‐1B‐mediated protein sorting regulates polarity and proliferation of intestinal epithelial cells in mice
  publication-title: Gastroenterology
– volume: 3
  year: 2011
  article-title: Membrane organization and lipid rafts
  publication-title: Cold Spring Harb Perspect Biol
– volume: 363
  start-page: 168
  year: 2004
  end-page: 172
  article-title: Identification of V‐ATPase as a major component in the raft fraction prepared from the synaptic plasma membrane and the synaptic vesicle of rat brain
  publication-title: Neurosci Lett
– volume: 14
  start-page: 838
  year: 2012
  end-page: 849
  article-title: Synaptotagmin‐like proteins control the formation of a single apical membrane domain in epithelial cells
  publication-title: Nat Cell Biol
– volume: 115
  start-page: E4396
  year: 2018
  end-page: E4405
  article-title: Molecular mechanism to recruit galectin‐3 into multivesicular bodies for polarized exosomal secretion
  publication-title: Proc Natl Acad Sci USA
– volume: 30
  start-page: 341
  year: 2020
  end-page: 353
  article-title: Lipid rafts: controversies resolved, mysteries remain
  publication-title: Trends Cell Biol
– volume: 107
  start-page: 17633
  year: 2010
  end-page: 17638
  article-title: Galectin‐9 trafficking regulates apical‐basal polarity in Madin‐Darby canine kidney epithelial cells
  publication-title: Proc Natl Acad Sci USA
– volume: 383
  start-page: 1475
  year: 2002
  end-page: 1480
  article-title: Lipid rafts in protein sorting and cell polarity in budding yeast
  publication-title: Biol Chem
– volume: 74
  year: 1977
  article-title: Phosphohexosyl components of a lysosomal enzyme are recognized by pinocytosis receptors on human fibroblasts
  publication-title: Proc Natl Acad Sci USA
– volume: 110
  start-page: 597
  year: 2002
  end-page: 603
  article-title: Cholesterol, lipid rafts, and disease
  publication-title: J Clin Invest
– volume: 288
  start-page: 1340
  year: 2013
  end-page: 1352
  article-title: Altering hydrophobic sequence lengths shows that hydrophobic mismatch controls affinity for ordered lipid domains (Rafts) in the multitransmembrane strand protein perfringolysin O
  publication-title: J Biol Chem
– volume: 8
  start-page: 1219
  year: 2017
  article-title: Structural determinants and functional consequences of protein affinity for membrane rafts
  publication-title: Nat Commun
– volume: 26
  start-page: 3737
  year: 2007
  end-page: 3748
  article-title: Differential involvement of endocytic compartments in the biosynthetic traffic of apical proteins
  publication-title: EMBO J
– volume: 579
  start-page: 483
  year: 2005
  end-page: 487
  article-title: PDZ‐binding motifs are unable to ensure correct polarized protein distribution in the absence of additional localization signals
  publication-title: FEBS Lett
– volume: 9
  year: 2017
  article-title: Directional fluid transport across organ‐blood barriers: physiology and cell biology
  publication-title: Cold Spring Harb Perspect Biol
– volume: 70
  start-page: 6508
  year: 1996
  end-page: 6515
  article-title: Transmembrane domain of influenza virus neuraminidase, a type II protein, possesses an apical sorting signal in polarized MDCK cells
  publication-title: J Virol
– volume: 4
  start-page: 1
  year: 2021
  end-page: 15
  article-title: Glycolipid‐dependent and lectin‐driven transcytosis in mouse enterocytes
  publication-title: Commun Biol
– volume: 583
  start-page: 3863
  year: 2009
  end-page: 3871
  article-title: The KDEL receptor: new functions for an old protein
  publication-title: FEBS Lett
– volume: 121
  start-page: 458
  year: 2008
  end-page: 465
  article-title: Loss of galectin‐3 impairs membrane polarisation of mouse enterocytes
  publication-title: J Cell Sci
– volume: 142
  start-page: 1413
  year: 1998
  end-page: 1427
  article-title: Annexin XIIIb associates with lipid microdomains to function in apical delivery
  publication-title: J Cell Biol
– volume: 97
  start-page: 3254
  year: 2000
  end-page: 3259
  article-title: Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast
  publication-title: Proc Natl Acad Sci USA
– volume: 15
  start-page: 4525
  year: 2019
  end-page: 4540
  article-title: Complex‐type N‐glycans on VSV‐G pseudotyped HIV exhibit ‘tough’ sialic and ‘brittle’ mannose self‐adhesions
  publication-title: Soft Matter
– volume: 248
  start-page: 742
  year: 1990
  end-page: 745
  article-title: Phosphorylation of the polymeric immunoglobulin receptor required for its efficient transcytosis
  publication-title: Science
– volume: 273
  start-page: 30263
  year: 1998
  end-page: 30270
  article-title: Putative O‐glycosylation sites and a membrane anchor are necessary for apical delivery of the human neurotrophin receptor in Caco‐2 cells
  publication-title: J Biol Chem
– volume: 274
  start-page: 3910
  year: 1999
  end-page: 3917
  article-title: Role of lipid modifications in targeting proteins to detergent‐resistant membrane rafts many raft proteins are acylated, while few are prenylated
  publication-title: J Biol Chem
– volume: 98
  start-page: 1304
  year: 1984
  end-page: 1319
  article-title: Viral glycoproteins destined for apical or basolateral plasma membrane domains traverse the same Golgi apparatus during their intracellular transport in doubly infected Madin‐Darby canine kidney cells
  publication-title: J Cell Biol
– volume: 367
  start-page: 301
  year: 2020
  end-page: 305
  article-title: Lipid‐gated monovalent ion fluxes regulate endocytic traffic and support immune surveillance
  publication-title: Science
– volume: 107
  start-page: 22050
  year: 2010
  end-page: 22054
  article-title: Palmitoylation regulates raft affinity for the majority of integral raft proteins
  publication-title: Proc Natl Acad Sci USA
– volume: 226
  start-page: 259
  year: 2003
  end-page: 319
  article-title: Acidification and protein traffic
  publication-title: Int Rev Cytol
– volume: 1793
  start-page: 605
  year: 2009
  end-page: 614
  article-title: Sorting of lysosomal proteins
  publication-title: Biochim Biophys Acta BBA Mol Cell Res
– volume: 16
  start-page: 5501
  year: 1997
  end-page: 5508
  article-title: Interaction of influenza virus haemagglutinin with sphingolipid‐cholesterol membrane domains via its transmembrane domain
  publication-title: EMBO J
– volume: 139
  start-page: 2061
  year: 2012
  end-page: 2070
  article-title: AP‐1 is required for the maintenance of apico‐basal polarity in the intestine
  publication-title: Development
– volume: 40
  start-page: 611
  year: 2015
  end-page: 622
  article-title: Recent insights into the structure, regulation, and function of the V‐ATPases
  publication-title: Trends Biochem Sci
– volume: 284
  start-page: C1105
  year: 2003
  end-page: C1113
  article-title: Identification of an apical sorting determinant in the cytoplasmic tail of megalin
  publication-title: Am J Physiol Cell Physiol
– volume: 52
  start-page: 329
  year: 1988
  end-page: 341
  article-title: The mannose 6‐phosphate receptor and the biogenesis of lysosomes
  publication-title: Cell
– volume: 189
  start-page: 1171
  year: 2010
  end-page: 1186
  article-title: A cation counterflux supports lysosomal acidification
  publication-title: J Cell Biol
– volume: 183
  start-page: 717
  year: 2020
  end-page: 729
  article-title: Assembly mechanism of mucin and von Willebrand factor polymers
  publication-title: Cell
– volume: 80
  start-page: 501
  year: 2020
  end-page: 511
  article-title: Structures of a complete human V‐ATPase reveal mechanisms of its assembly
  publication-title: Mol Cell
– volume: 12
  start-page: 63
  year: 1994
  end-page: 84
  article-title: Transepithelial transport of immunoglobulins
  publication-title: Annu Rev Immunol
– volume: 261
  start-page: 15172
  year: 1986
  end-page: 15178
  article-title: Ammonium chloride slows transport of the influenza virus hemagglutinin but does not cause mis‐sorting in a polarized epithelial cell line
  publication-title: J Biol Chem
– volume: 39
  start-page: 1083
  year: 2000
  end-page: 1090
  article-title: The amino‐terminal nine amino acid sequence of poliovirus capsid VP4 protein is sufficient to confer N‐myristoylation and targeting to detergent‐insoluble membranes
  publication-title: Biochemistry
– volume: 273
  start-page: 178
  year: 2002
  end-page: 186
  article-title: Role of the membrane‐proximal O‐glycosylation site in sorting of the human receptor for neurotrophins to the apical membrane of MDCK cells
  publication-title: Exp Cell Res
– volume: 117
  start-page: 5079
  year: 2004
  end-page: 5086
  article-title: N‐glycans, not the GPI anchor, mediate the apical targeting of a naturally glycosylated, GPI‐anchored protein in polarised epithelial cells
  publication-title: J Cell Sci
– volume: 98
  start-page: 9419
  year: 2001
  end-page: 9424
  article-title: Carbohydrate self‐recognition mediates marine sponge cellular adhesion
  publication-title: Proc Natl Acad Sci USA
– volume: 102
  start-page: 17981
  year: 2005
  end-page: 17986
  article-title: A genome‐wide visual screen reveals a role for sphingolipids and ergosterol in cell surface delivery in yeast
  publication-title: Proc Natl Acad Sci USA
– volume: 89
  start-page: 788
  year: 2010
  end-page: 798
  article-title: Trafficking of galectin‐3 through endosomal organelles of polarized and non‐polarized cells
  publication-title: Eur J Cell Biol
– volume: 4
  start-page: 297
  year: 1985
  end-page: 307
  article-title: An enzymatic assay reveals that proteins destined for the apical or basolateral domains of an epithelial cell line share the same late Golgi compartments
  publication-title: EMBO J
– volume: 148
  start-page: 495
  year: 2000
  end-page: 504
  article-title: Influenza M2 proton channel activity selectively inhibits trans‐golgi network release of apical membrane and secreted proteins in polarized Madin‐Darby canine kidney cells
  publication-title: J Cell Biol
– volume: 457
  start-page: 107
  year: 2014
  end-page: 115
  article-title: Ligand binding and complex formation of galectin‐3 is modulated by pH variations
  publication-title: Biochem J
– volume: 16
  start-page: 644
  year: 2020
  end-page: 652
  article-title: Plasma membranes are asymmetric in lipid unsaturation, packing and protein shape
  publication-title: Nat Chem Biol
– volume: 185
  start-page: 601
  year: 2009
  end-page: 612
  article-title: Segregation of sphingolipids and sterols during formation of secretory vesicles at the trans‐Golgi network
  publication-title: J Cell Biol
– volume: 213
  start-page: 449
  year: 1994
  end-page: 457
  article-title: N‐glycosylation of erythropoietin is critical for apical secretion by Madin‐Darby canine kidney cells
  publication-title: Exp Cell Res
– volume: 8
  start-page: 379
  year: 2007
  end-page: 388
  article-title: Apical sorting by galectin‐3‐dependent glycoprotein clustering
  publication-title: Traffic
– volume: 121
  start-page: 1031
  year: 1993
  end-page: 1039
  article-title: Glycosylphosphatidylinositol‐anchored proteins are preferentially targeted to the basolateral surface in Fischer rat thyroid epithelial cells
  publication-title: J Cell Biol
– volume: 109
  start-page: 2145
  year: 1989
  end-page: 2156
  article-title: A glycophospholipid membrane anchor acts as an apical targeting signal in polarized epithelial cells
  publication-title: J Cell Biol
– volume: 18
  start-page: 1710
  year: 2007
  end-page: 1722
  article-title: A bipartite signal regulates the faithful delivery of apical domain marker podocalyxin/Gp135
  publication-title: Mol Biol Cell
– volume: 37
  start-page: 195
  year: 1984
  end-page: 204
  article-title: Intracellular receptor sorting during endocytosis: Comparative immunoelectron microscopy of multiple receptors in rat liver
  publication-title: Cell
– volume: 378
  start-page: 96
  year: 1995
  article-title: N ‐glycans as apical sorting signals in epithelial cells
  publication-title: Nature
– volume: 103
  start-page: 2565
  year: 1986
  end-page: 2568
  article-title: The sorting of proteins to the plasma membrane in epithelial cells
  publication-title: J Cell Biol
– volume: 13
  start-page: 1189
  year: 2011
  end-page: 1201
  article-title: Apicobasal domain identities of expanding tubular membranes depend on glycosphingolipid biosynthesis
  publication-title: Nat Cell Biol
– volume: 146
  start-page: 313
  year: 1999
  end-page: 320
  article-title: N‐glycans mediate the apical sorting of a Gpi‐anchored, raft‐associated protein in Madin‐Darby canine kidney cells
  publication-title: J Cell Biol
– volume: 122
  start-page: 4253
  year: 2009
  end-page: 4266
  article-title: Apical trafficking in epithelial cells: signals, clusters and motors
  publication-title: J Cell Sci
– volume: 23
  start-page: 3636
  year: 2012
  end-page: 3646
  article-title: Sialylation of N‐linked glycans mediates apical delivery of endolyn in MDCK cells via a galectin‐9‐dependent mechanism
  publication-title: Mol Biol Cell
– volume: 167
  start-page: 699
  year: 2004
  end-page: 709
  article-title: Protein oligomerization modulates raft partitioning and apical sorting of GPI‐anchored proteins
  publication-title: J Cell Biol
– volume: 10
  start-page: 1128
  year: 2009
  end-page: 1142
  article-title: Identification of a cytoplasmic signal for apical transcytosis
  publication-title: Traffic Cph Den
– volume: 22
  start-page: 793
  year: 2012
  end-page: 805
  article-title: Polarized sorting and trafficking in epithelial cells
  publication-title: Cell Res
– volume: 426
  start-page: 173
  year: 2004
  end-page: 181
  article-title: Carbohydrate‐to‐carbohydrate interaction in basic cell biology: a brief overview
  publication-title: Arch Biochem Biophys
– volume: 12
  start-page: 4129
  year: 2001
  end-page: 4138
  article-title: Plasma membrane proton ATPase Pma1p requires raft association for surface delivery in yeast
  publication-title: Mol Biol Cell
– volume: 173
  start-page: 937
  year: 2006
  end-page: 948
  article-title: Apical targeting of syntaxin 3 is essential for epithelial cell polarity
  publication-title: J Cell Biol
– volume: 14
  start-page: 1014
  year: 2013
  end-page: 1027
  article-title: pH‐dependent recycling of galectin‐3 at the apical membrane of epithelial cells
  publication-title: Traffic
– volume: 6
  start-page: 297
  year: 2004
  end-page: 307
  article-title: Delivery of raft‐associated, GPI‐anchored proteins to the apical surface of polarized MDCK cells by a transcytotic pathway
  publication-title: Nat Cell Biol
– volume: 27
  start-page: 353
  year: 2013
  end-page: 366
  article-title: The adaptor protein‐1 μ1B subunit expands the repertoire of basolateral sorting signal recognition in epithelial cells
  publication-title: Dev Cell
– volume: 66
  start-page: 907
  year: 1991
  end-page: 920
  article-title: Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant
  publication-title: Cell
– volume: 117
  start-page: 9252
  year: 2013
  end-page: 9258
  article-title: Electrostatically defying cation‐cation clusters: can likes attract in a low‐polarity environment?
  publication-title: J Phys Chem A
– volume: 25
  start-page: 1375
  year: 2014
  end-page: 1386
  article-title: Trafficking to the apical and basolateral membranes in polarized epithelial cells
  publication-title: J Am Soc Nephrol
– volume: 111
  start-page: 4127
  year: 2014
  end-page: 4132
  article-title: Four‐dimensional live imaging of apical biosynthetic trafficking reveals a post‐Golgi sorting role of apical endosomal intermediates
  publication-title: Proc Natl Acad Sci USA
– volume: 116
  start-page: 11796
  year: 2019
  end-page: 11805
  article-title: Quantitative proteomics of MDCK cells identify unrecognized roles of clathrin adaptor AP‐1 in polarized distribution of surface proteins
  publication-title: Proc Natl Acad Sci USA
– volume: 116
  start-page: 577
  year: 1992
  end-page: 583
  article-title: Plasma membrane protein sorting in polarized epithelial cells
  publication-title: J Cell Biol
– volume: 104
  start-page: 1564
  year: 2007
  end-page: 1569
  article-title: AP1B sorts basolateral proteins in recycling and biosynthetic routes of MDCK cells
  publication-title: Proc Natl Acad Sci USA
– volume: 269
  start-page: 2712
  year: 1994
  end-page: 2721
  article-title: Transport, function, and sorting of lactase‐phlorizin hydrolase in Madin‐Darby canine kidney cells
  publication-title: J Biol Chem
– volume: 121
  start-page: 4001
  year: 2008
  end-page: 4007
  article-title: Different GPI‐attachment signals affect the oligomerisation of GPI‐anchored proteins and their apical sorting
  publication-title: J Cell Sci
– volume: 109
  start-page: 948
  year: 2015
  end-page: 955
  article-title: Hexagonal substructure and hydrogen bonding in liquid‐ordered phases containing palmitoyl sphingomyelin
  publication-title: Biophys J
– volume: 15
  start-page: 225
  year: 2014
  end-page: 242
  article-title: Organization and execution of the epithelial polarity programme
  publication-title: Nat Rev Mol Cell Biol
– volume: 22
  start-page: 4621
  year: 2011
  end-page: 4634
  article-title: N‐Glycosylation instead of cholesterol mediates oligomerization and apical sorting of GPI‐APs in FRT cells
  publication-title: Mol Biol Cell
– volume: 30
  start-page: 1716
  year: 2019
  end-page: 1728
  article-title: Clathrin and clathrin adaptor AP‐1 control apical trafficking of megalin in the biosynthetic and recycling routes
  publication-title: Mol Biol Cell
– volume: 234
  start-page: 438
  year: 1986
  end-page: 443
  article-title: The trans Golgi network: sorting at the exit site of the Golgi complex
  publication-title: Science
– volume: 71
  start-page: 741
  year: 1992
  end-page: 753
  article-title: Basolateral sorting of LDL receptor in MDCK cells: the cytoplasmic domain contains two tyrosine‐dependent targeting determinants
  publication-title: Cell
– volume: 21
  start-page: 219
  year: 2009
  end-page: 231
  article-title: Galectin‐3, a novel centrosome‐associated protein, required for epithelial morphogenesis
  publication-title: Mol Biol Cell
– volume: 142
  start-page: 51
  year: 1998
  end-page: 57
  article-title: Mutations in the middle of the transmembrane domain reverse the polarity of transport of the influenza virus hemagglutinin in MDCK epithelial cells
  publication-title: J Cell Biol
– volume: 131
  year: 2018
  article-title: Galectin‐3 modulates the polarized surface delivery of β1‐integrin in epithelial cells
  publication-title: J Cell Sci
– volume: 22
  start-page: 811
  year: 2012
  end-page: 823
  article-title: The clathrin adaptor AP‐1A mediates basolateral polarity
  publication-title: Dev Cell
– volume: 24
  start-page: 1996
  year: 2013
  end-page: 2007
  article-title: Multiple motifs regulate apical sorting of p75 via a mechanism that involves dimerization and higher‐order oligomerization
  publication-title: Mol Biol Cell
– volume: 165
  start-page: 529
  year: 2004
  end-page: 537
  article-title: Carbohydrate–carbohydrate interaction provides adhesion force and specificity for cellular recognition
  publication-title: J Cell Biol
– volume: 99
  start-page: 189
  year: 1999
  end-page: 198
  article-title: A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells
  publication-title: Cell
– volume: 168
  start-page: 303
  year: 2005
  end-page: 313
  article-title: Gp135/podocalyxin and NHERF‐2 participate in the formation of a preapical domain during polarization of MDCK cells
  publication-title: J Cell Biol
– volume: 10
  start-page: 1135
  year: 2008
  end-page: 1145
  article-title: GPHR is a novel anion channel critical for acidification and functions of the Golgi apparatus
  publication-title: Nat Cell Biol
– volume: 30
  start-page: 5
  year: 2019
  end-page: 21
  article-title: Abnormal Golgi pH homeostasis in cancer cells impairs apical targeting of carcinoembryonic antigen by inhibiting its glycosyl‐phosphatidylinositol anchor‐mediated association with lipid rafts
  publication-title: Antioxid Redox Signal
– volume: 268
  start-page: 11750
  year: 1993
  end-page: 11757
  article-title: Apical secretion of a cytosolic protein by Madin‐Darby canine kidney cells. Evidence for polarized release of an endogenous lectin by a nonclassical secretory pathway
  publication-title: J Biol Chem
– volume: 16
  start-page: 408
  year: 2006
  end-page: 414
  article-title: Requirement for galectin‐3 in apical protein sorting
  publication-title: Curr Biol
– volume: 192
  start-page: 23
  year: 2015
  end-page: 32
  article-title: Structural determinants of protein partitioning into ordered membrane domains and lipid rafts
  publication-title: Chem Phys Lipids
– volume: 31
  start-page: 4917
  year: 2017
  end-page: 4927
  article-title: Galectin‐8 regulates targeting of Gp135/podocalyxin and lumen formation at the apical surface of renal epithelial cells
  publication-title: FASEB J
– volume: 27
  start-page: 2259
  year: 2016
  end-page: 2271
  article-title: Iterative sorting of apical and basolateral cargo in Madin‐Darby canine kidney cells
  publication-title: Mol Biol Cell
– volume: 19
  start-page: 4341
  year: 2008
  end-page: 4351
  article-title: Exon loss accounts for differential sorting of Na‐K‐Cl cotransporters in polarized epithelial cells
  publication-title: Mol Biol Cell
– volume: 9
  start-page: 2141
  year: 2008
  end-page: 2150
  article-title: N‐ and O‐glycans are not directly involved in the oligomerization and apical sorting of GPI proteins
  publication-title: Traffic Cph Den
– volume: 127
  start-page: 4987
  year: 2014
  end-page: 4993
  article-title: The vacuolar‐type H+‐ATPase at a glance – more than a proton pump
  publication-title: J Cell Sci
– volume: 3
  start-page: 140
  year: 2001
  article-title: Multicolour imaging of post‐Golgi sorting and trafficking in live cells
  publication-title: Nat Cell Biol
– volume: 68
  start-page: 533
  year: 1992
  end-page: 544
  article-title: Sorting of GPI‐anchored proteins to glycolipid‐enriched membrane subdomains during transport to the apical cell surface
  publication-title: Cell
– volume: 18
  start-page: 2687
  year: 2007
  article-title: Recycling endosomes of polarized epithelial cells actively sort apical and basolateral cargos into separate subdomains
  publication-title: Mol Biol Cell
– volume: 66
  start-page: 65
  year: 1991
  end-page: 75
  article-title: An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor
  publication-title: Cell
– volume: 104
  start-page: 1353
  year: 1999
  end-page: 1361
  article-title: A PDZ‐interacting domain in CFTR is an apical membrane polarization signal
  publication-title: J Clin Invest
– volume: 81
  start-page: 309
  year: 1995
  end-page: 312
  article-title: The role of N‐glycans in the secretory pathway
  publication-title: Cell
– volume: 162
  start-page: 211
  year: 2003
  end-page: 222
  article-title: Vacuole membrane fusion : V0 functions after trans‐SNARE pairing and is coupled to the Ca2+‐releasing channel
  publication-title: J Cell Biol
– volume: 119
  start-page: 540
  year: 2009
  end-page: 550
  article-title: Differential roles of NHERF1, NHERF2, and PDZK1 in regulating CFTR‐mediated intestinal anion secretion in mice
  publication-title: J Clin Invest
– volume: 219
  year: 2020
  article-title: Distinct roles for luminal acidification in apical protein sorting and trafficking in zebrafish
  publication-title: J Cell Biol
– volume: 409
  start-page: 581
  year: 2001
  end-page: 588
  article-title: Trans‐complex formation by proteolipid channels in the terminal phase of membrane fusion
  publication-title: Nature
– volume: 19
  start-page: 215
  year: 2018
  end-page: 228
  article-title: Clathrin and AP1 are required for apical sorting of glycosyl phosphatidyl inositol‐anchored proteins in biosynthetic and recycling routes in Madin‐Darby canine kidney cells
  publication-title: Traffic
– volume: 139
  start-page: 2071
  year: 2012
  end-page: 2083
  article-title: Clathrin and AP‐1 regulate apical polarity and lumen formation during tubulogenesis
  publication-title: Development
– volume: 12
  start-page: 1035
  year: 2010
  end-page: 1045
  article-title: A molecular network for generation of the apical surface and lumen
  publication-title: Nat Cell Biol
– volume: 139
  start-page: 929
  year: 1997
  end-page: 940
  article-title: The O‐glycosylated stalk domain is required for apical sorting of neurotrophin receptors in polarized MDCK cells
  publication-title: J Cell Biol
– ident: e_1_2_12_74_1
  doi: 10.1042/BJ20130933
– ident: e_1_2_12_22_1
  doi: 10.1038/sj.emboj.7601813
– ident: e_1_2_12_98_1
  doi: 10.1074/jbc.273.46.30263
– ident: e_1_2_12_47_1
  doi: 10.1016/j.febslet.2004.11.106
– ident: e_1_2_12_52_1
  doi: 10.1053/j.gastro.2013.05.013
– ident: e_1_2_12_51_1
  doi: 10.1242/dev.076711
– ident: e_1_2_12_114_1
  doi: 10.1073/pnas.151111298
– ident: e_1_2_12_117_1
  doi: 10.1021/jp405063h
– ident: e_1_2_12_72_1
  doi: 10.1089/ars.2017.7389
– ident: e_1_2_12_78_1
  doi: 10.1242/jcs.036038
– ident: e_1_2_12_82_1
  doi: 10.1101/cshperspect.a004697
– ident: e_1_2_12_12_1
  doi: 10.1126/science.2945253
– ident: e_1_2_12_62_1
  doi: 10.1073/pnas.1012424107
– ident: e_1_2_12_64_1
  doi: 10.1091/mbc.e09-03-0193
– ident: e_1_2_12_84_1
  doi: 10.1016/j.chemphyslip.2015.07.022
– ident: e_1_2_12_101_1
  doi: 10.1038/s41589-020-0529-6
– ident: e_1_2_12_121_1
  doi: 10.1016/j.molcel.2020.09.029
– ident: e_1_2_12_89_1
  doi: 10.1074/jbc.274.6.3910
– ident: e_1_2_12_23_1
  doi: 10.1073/pnas.1304168111
– ident: e_1_2_12_83_1
  doi: 10.1083/jcb.200901145
– ident: e_1_2_12_2_1
  doi: 10.1038/nrm3775
– ident: e_1_2_12_41_1
  doi: 10.1016/S0092-8674(88)80026-6
– ident: e_1_2_12_94_1
  doi: 10.1073/pnas.0509107102
– ident: e_1_2_12_34_1
  doi: 10.1083/jcb.142.1.51
– ident: e_1_2_12_13_1
  doi: 10.1038/35055042
– ident: e_1_2_12_120_1
  doi: 10.1126/science.aaw9544
– ident: e_1_2_12_4_1
  doi: 10.1016/j.devcel.2013.10.006
– ident: e_1_2_12_112_1
  doi: 10.1083/jcb.200309005
– ident: e_1_2_12_24_1
  doi: 10.1091/mbc.E16-02-0096
– ident: e_1_2_12_57_1
  doi: 10.1091/mbc.E18-12-0811
– ident: e_1_2_12_36_1
  doi: 10.1152/ajpcell.00514.2002
– ident: e_1_2_12_90_1
  doi: 10.1073/pnas.1016184107
– ident: e_1_2_12_26_1
  doi: 10.1083/jcb.146.2.313
– ident: e_1_2_12_97_1
  doi: 10.1515/BC.2002.169
– ident: e_1_2_12_67_1
  doi: 10.1016/j.ejcb.2010.07.001
– ident: e_1_2_12_68_1
  doi: 10.1111/tra.12086
– ident: e_1_2_12_107_1
  doi: 10.1016/j.tibs.2015.08.005
– ident: e_1_2_12_21_1
  doi: 10.1091/mbc.E05-09-0873
– ident: e_1_2_12_79_1
  doi: 10.1093/emboj/16.18.5501
– ident: e_1_2_12_55_1
  doi: 10.1038/ncb2541
– ident: e_1_2_12_30_1
  doi: 10.1038/378096a0
– ident: e_1_2_12_100_1
  doi: 10.1074/jbc.M112.415596
– ident: e_1_2_12_87_1
  doi: 10.1038/s41467-017-01328-3
– ident: e_1_2_12_5_1
  doi: 10.1016/S0092-8674(00)81650-5
– ident: e_1_2_12_42_1
  doi: 10.1016/j.bbamcr.2008.10.016
– ident: e_1_2_12_95_1
  doi: 10.1073/pnas.97.7.3254
– ident: e_1_2_12_104_1
  doi: 10.1016/S0074-7696(03)01005-2
– ident: e_1_2_12_35_1
  doi: 10.1172/JCI7453
– ident: e_1_2_12_44_1
  doi: 10.1016/0092-8674(91)90139-P
– ident: e_1_2_12_8_1
  doi: 10.1242/jcs.032615
– ident: e_1_2_12_105_1
  doi: 10.1083/jcb.201908225
– ident: e_1_2_12_80_1
  doi: 10.1681/ASN.2013080883
– ident: e_1_2_12_50_1
  doi: 10.1242/dev.077347
– ident: e_1_2_12_37_1
  doi: 10.1083/jcb.142.6.1413
– ident: e_1_2_12_54_1
  doi: 10.1083/jcb.200603132
– ident: e_1_2_12_122_1
  doi: 10.1016/j.neulet.2004.04.002
– ident: e_1_2_12_119_1
  doi: 10.1083/jcb.200212004
– ident: e_1_2_12_40_1
  doi: 10.1016/S0021-9258(18)43616-2
– ident: e_1_2_12_86_1
  doi: 10.1016/0092-8674(92)90189-J
– ident: e_1_2_12_60_1
  doi: 10.1016/j.cub.2005.12.046
– ident: e_1_2_12_69_1
  doi: 10.1096/fj.201601386R
– ident: e_1_2_12_20_1
  doi: 10.1038/ncb1109
– ident: e_1_2_12_63_1
  doi: 10.1091/mbc.E12-04-0329
– ident: e_1_2_12_3_1
  doi: 10.1101/cshperspect.a027847
– ident: e_1_2_12_16_1
  doi: 10.1146/annurev.iy.12.040194.000431
– ident: e_1_2_12_73_1
  doi: 10.1111/j.1600-0854.2007.00539.x
– ident: e_1_2_12_111_1
  doi: 10.1091/mbc.E08-05-0478
– ident: e_1_2_12_115_1
  doi: 10.1039/C9SM00579J
– ident: e_1_2_12_6_1
  doi: 10.1016/j.devcel.2012.02.004
– ident: e_1_2_12_113_1
  doi: 10.1016/j.abb.2004.02.032
– ident: e_1_2_12_71_1
  doi: 10.1016/S0021-9258(17)42002-3
– ident: e_1_2_12_48_1
  doi: 10.1172/JCI35541
– ident: e_1_2_12_70_1
  doi: 10.1091/mbc.e13-02-0078
– ident: e_1_2_12_58_1
  doi: 10.1016/0092-8674(95)90380-1
– ident: e_1_2_12_7_1
  doi: 10.1083/jcb.103.6.2565
– ident: e_1_2_12_92_1
  doi: 10.1016/j.bpj.2015.07.036
– ident: e_1_2_12_25_1
  doi: 10.1083/jcb.109.5.2145
– ident: e_1_2_12_17_1
  doi: 10.1111/j.1600-0854.2009.00941.x
– ident: e_1_2_12_102_1
  doi: 10.1016/S0021-9258(18)66848-6
– ident: e_1_2_12_65_1
  doi: 10.1016/S0021-9258(19)50263-0
– ident: e_1_2_12_29_1
  doi: 10.1006/excr.1994.1222
– ident: e_1_2_12_116_1
  doi: 10.1016/j.cell.2020.09.021
– ident: e_1_2_12_31_1
  doi: 10.1083/jcb.139.4.929
– ident: e_1_2_12_91_1
  doi: 10.1021/bi992132e
– ident: e_1_2_12_19_1
  doi: 10.1038/ncb2106
– ident: e_1_2_12_39_1
  doi: 10.1073/pnas.74.5.2026
– ident: e_1_2_12_66_1
  doi: 10.1073/pnas.1718921115
– ident: e_1_2_12_81_1
  doi: 10.1083/jcb.116.3.577
– ident: e_1_2_12_109_1
  doi: 10.1083/jcb.200911083
– ident: e_1_2_12_103_1
  doi: 10.1083/jcb.148.3.495
– ident: e_1_2_12_10_1
  doi: 10.1083/jcb.98.4.1304
– ident: e_1_2_12_77_1
  doi: 10.1083/jcb.200407094
– ident: e_1_2_12_32_1
  doi: 10.1006/excr.2001.5442
– ident: e_1_2_12_61_1
  doi: 10.1242/jcs.020800
– ident: e_1_2_12_9_1
  doi: 10.1038/cr.2012.64
– ident: e_1_2_12_18_1
  doi: 10.1083/jcb.200407072
– ident: e_1_2_12_38_1
  doi: 10.1016/j.febslet.2009.10.053
– ident: e_1_2_12_28_1
  doi: 10.1091/mbc.E11-04-0320
– ident: e_1_2_12_106_1
  doi: 10.1242/jcs.158550
– ident: e_1_2_12_76_1
  doi: 10.1038/s42003-021-01693-2
– ident: e_1_2_12_59_1
  doi: 10.1083/jcb.200407073
– ident: e_1_2_12_99_1
  doi: 10.1172/JCI0216390
– ident: e_1_2_12_49_1
  doi: 10.1091/mbc.E06-07-0629
– ident: e_1_2_12_85_1
  doi: 10.1016/j.tcb.2020.01.009
– ident: e_1_2_12_56_1
  doi: 10.1073/pnas.1821076116
– ident: e_1_2_12_75_1
  doi: 10.1242/jcs.213199
– ident: e_1_2_12_53_1
  doi: 10.1111/tra.12548
– ident: e_1_2_12_96_1
  doi: 10.1091/mbc.12.12.4129
– ident: e_1_2_12_118_1
  doi: 10.1038/35054500
– ident: e_1_2_12_45_1
  doi: 10.1016/0092-8674(92)90551-M
– ident: e_1_2_12_11_1
  doi: 10.1002/j.1460-2075.1985.tb03629.x
– ident: e_1_2_12_43_1
  doi: 10.1016/0092-8674(91)90437-4
– ident: e_1_2_12_93_1
  doi: 10.1038/ncb2328
– ident: e_1_2_12_110_1
  doi: 10.1083/jcb.121.5.1031
– ident: e_1_2_12_108_1
  doi: 10.1038/ncb1773
– ident: e_1_2_12_14_1
  doi: 10.1016/0092-8674(84)90315-5
– ident: e_1_2_12_15_1
  doi: 10.1126/science.2110383
– ident: e_1_2_12_27_1
  doi: 10.1242/jcs.01386
– ident: e_1_2_12_88_1
  doi: 10.1111/j.1600-0854.2008.00826.x
– ident: e_1_2_12_46_1
  doi: 10.1073/pnas.0610700104
– ident: e_1_2_12_33_1
  doi: 10.1128/jvi.70.9.6508-6515.1996
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Snippet Polarized epithelial cells are characterized by the asymmetric distribution of proteins between apical and basolateral domains of the plasma membrane. This...
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pubmed
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wiley
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StartPage 659
SubjectTerms Animals
apical sorting
asymmetry
Cell Line
Cell Membrane - genetics
cell physiology
Cell Polarity - genetics
epithelial cell
Epithelial cells
Epithelial Cells - cytology
Epithelial Cells - metabolism
Epithelium
Glycan
Glycosylation
Golgi Apparatus - genetics
Homeostasis
Hydrogen-Ion Concentration
Ions
Lipids
Membrane proteins
Membrane Proteins - genetics
Membranes
Oligomerization
Phase separation
plasma membrane
Polysaccharides - genetics
Protein transport
Protein Transport - genetics
Proteins
separation
Skewed distributions
Vacuolar Proton-Translocating ATPases - genetics
V‐ATPase
zebrafish
Zebrafish - genetics
Zebrafish - growth & development
Zebrafish Proteins - genetics
Title Self‐organization of apical membrane protein sorting in epithelial cells
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Ffebs.15882
https://www.ncbi.nlm.nih.gov/pubmed/33864720
https://www.proquest.com/docview/2624153817
https://www.proquest.com/docview/2514604941
https://www.proquest.com/docview/2648863627
https://pubmed.ncbi.nlm.nih.gov/PMC8522177
Volume 289
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