DOI: 10.1083/jcb.137.2.359. The Apical Submembrane Cytoskeleton Participates in the Organization of the Apical Pole in Epithelial Cells

The Apical Submembrane Cytoskeleton Participates in the Organization of the Apical Pole in Epithelial Cells

10.1083/jcb.137.2.359

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

In a previous publication (Rodriguez, M.L., M. Brignoni, and P.J.I. Salas. 1994. J. Cell Sci. 107: 3145–3151), we described the existence of a terminal web-like structure in nonbrush border cells, which comprises a specifically apical cytokeratin, presumably cytokeratin 19. In the present study we confirmed the apical distribution of cytokeratin 19 and expanded that observation to other epithelial cells in tissue culture and in vivo. In tissue culture, subconfluent cell stocks under continuous treatment with two different 21-mer phosphorothioate oligodeoxy nucleotides that targeted cytokeratin 19 mRNA enabled us to obtain confluent monolayers with a partial (40–70%) and transitory reduction in this protein. The expression of other cytoskeletal proteins was undisturbed. This downregulation of cytokeratin 19 resulted in (a) decrease in the number of microvilli; (b) disorganization of the apical (but not lateral or basal) filamentous actin and abnormal apical microtubules; and (c) depletion or redistribution of apical membrane proteins as determined by differential apical–basolateral biotinylation. In fact, a subset of detergent-insoluble proteins was not expressed on the cell surface in cells with lower levels of cytokeratin 19. Apical proteins purified in the detergent phase of Triton X-114 (typically integral membrane proteins) and those differentially extracted in Triton X-100 at 37°C or in n-octyl-β-d-glycoside at 4°C (representative of GPIanchored proteins), appeared partially redistributed to the basolateral domain. A transmembrane apical protein, sucrase isomaltase, was found mispolarized in a subpopulation of the cells treated with antisense oligonucleotides, while the basolateral polarity of Na+– K+ATPase was not affected. Both sucrase isomaltase and alkaline phosphatase (a GPI-anchored protein) appeared partially depolarized in A19 treated CACO-2 monolayers as determined by differential biotinylation, affinity purification, and immunoblot. These results suggest that an apical submembrane cytoskeleton of intermediate filaments is expressed in a number of epithelia, including those without a brush border, although it may not be universal. In addition, these data indicate that this structure is involved in the organization of the apical region of the cytoplasm and the apical membrane.

Bibliography

Salas, P. J. I., Rodriguez, M. L., Viciana, A. L., Vega-Salas, D. E., & Hauri, H.-P. (1997). The Apical Submembrane Cytoskeleton Participates in the Organization of the Apical Pole in Epithelial Cells. The Journal of Cell Biology, 137(2), 359â375.

Authors 5

Pedro J.I. Salas (first)
Marcelo L. Rodriguez (additional)
Ana L. Viciana (additional)
Dora E. Vega-Salas (additional)
Hans-Peter Hauri (additional)

References 94 Referenced 75

10.1016/0092-8674(94)90496-0 / Cell / Deconstructing the microtubule-organizing center by Archer (1994)
10.1016/0955-0674(94)90127-9 / Curr Opin Cell Biol / Membrane–actin microfilament connections: an increasing diversity of players related to band 4.1 by Arpin (1994)
10.1083/jcb.127.6.1995 / J Cell Biol / Functional differences betwen L- and T-plastin isoforms by Arpin (1994)
10.1083/jcb.109.6.2817 / J Cell Biol / The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium by Bacallao (1989)
10.1111/j.1432-0436.1990.tb00464.x / Differentiation / Cell-type specific and efficient synthesis of human cytokeratin 19 in transgenic mice by Bader (1990)
{'key': '2023072822492546400_B6'}
10.1242/jcs.107.10.2909 / J Cell Sci / The network organization and the phosphorylation of cytokeratins are concomitantly modified by forskolin in the enterocyte-like differentiated CACO-2 cell line by Baricault (1994)
10.1083/jcb.102.2.560 / J Cell Biol / Organization of cytokeratin bundles by desmosomes in rat mammary cells by Bologna (1986)
10.1016/S0021-9258(19)69848-0 / J Biol Chem / Phase separation of integral membrane proteins in Triton X-114 solution by Bordier (1981)
10.1242/jcs.108.5.1931 / J Cell Sci / Cyclic AMP modulates the rate of “constitutive” exocytosis of apical membrane proteins in Madin-Darby canine kidney cells by Brignoni (1995)
10.1016/0092-8674(84)90223-X / Cell / The mannose-6-phosphate receptor for lysosomal enzymes is concentrated in CisGolgi cisternae by Brown (1984)
10.1016/0092-8674(92)90189-J / Cell / Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface by Brown (1992)
10.1083/jcb.110.4.1123 / J Cell Biol / Cytoskeletal control of centrioles movement during the establishment of polarity in MDCK cells by Buendia (1990)
10.1042/bj2850939 / Biochem J / Changes in keratin expression during fetal and postnatal development of intestinal epithelial cells by Calnek (1992)
10.1111/j.1432-0436.1993.tb00649.x / Differentiation / Differential localization by in situ hybridization of distinct keratin mRNA species during intestinal epithelial cell development and differentiation by Calnek (1993)
10.1016/0165-022X(90)90084-P / J Biochem Biophys Methods / Oligodeoxynucleoside phosphorothioate stability in subcellular extracts, culture media, sera, and cerebrospinal fluid by Campbell (1990)
{'key': '2023072822492546400_B17', 'first-page': '405', 'article-title': 'Suppression of villin expression by antisense RNA impairs brush border assembly in polarized epithelial intestinal cells', 'volume': '14', 'author': 'Costa de Beauregard', 'year': '1995', 'journal-title': 'EMBO (Eur Mol Biol Organ) J'} / EMBO (Eur Mol Biol Organ) J / Suppression of villin expression by antisense RNA impairs brush border assembly in polarized epithelial intestinal cells by Costa de Beauregard (1995)
{'key': '2023072822492546400_B18', 'first-page': '462', 'article-title': 'In vitro pharmacokinetics of phosphorothioated antisense oligonucleotides', 'volume': '275', 'author': 'Crooke', 'year': '1995', 'journal-title': 'J Pharmacol Exp Ther'} / J Pharmacol Exp Ther / In vitro pharmacokinetics of phosphorothioated antisense oligonucleotides by Crooke (1995)
10.1016/0014-4827(87)90339-9 / Exp Cell Res / Turnover of cytokeratin polypeptides in mouse hepatocytes by Denk (1987)
10.1111/j.1432-0436.1987.tb00151.x / Differentiation / Patterns of expression of cytoskeletal proteins in human thyroid gland and thyroid carcinomas by Dockhorn-Dworniczak (1987)
10.1083/jcb.107.3.1037 / J Cell Biol / Organization of the actin filament cytoskeleton in the intestinal brush border: a quantitative and qualitative immunoelectron microscope study by Drenckhahn (1988)
10.1126/science.2933809 / Science (Wash DC) / Colocalization of band 3 with ankyrin and spectrin at the basal membrane of intercalated cells in the rat kidney by Drenckhahn (1985)
10.1073/pnas.85.4.1114 / Proc Natl Acad Sci USA / Sequence of the human 40-kDa keratin reveals an unusual structure with very high sequence identity to the corresponding bovine keratin by Eckert (1988)
{'key': '2023072822492546400_B24', 'first-page': '169', 'article-title': 'Alteration of intermediate filament distribution in PtK1cells by acrylamide', 'volume': '37', 'author': 'Eckert', 'year': '1985', 'journal-title': 'Eur J Cell Biol'} / Eur J Cell Biol / Alteration of intermediate filament distribution in PtK1cells by acrylamide by Eckert (1985)
10.1101/SQB.1982.046.01.039 / Cold Spring Harbor Symp Quant Biol / In vivo disruption of the cytokeratin cytoskeleton in cultured epithelial cells by microinjection of antikeratin: evidence for the presence of an intermediate-filament–organizing center by Eckert (1982)
10.1242/dev.106.2.407 / Development / Differential localization of villin and fimbrin during development of the mouse visceral endoderm and intestinal epithelium by Ezzell (1989)
10.1016/S0960-9822(95)00117-5 / Curr Biol / Microvillus assembly. Not actin alone by Fath (1995)
{'key': '2023072822492546400_B28'}
10.1083/jcb.117.3.595 / J Cell Biol / Suppression of kinesin expression in cultured hippocampal neurons using antisense oligonucleotides by Ferreira (1992)
10.1242/dev.121.1.201 / Development (Camb) / Pattern of localization and cytoskeletal association of two vegetally localized RNAs, Vg1 and Xcat-2 by Forristall (1995)
{'key': '2023072822492546400_B31', 'first-page': '255', 'article-title': 'The organization of cytokeratin filaments in the intestinal epithelium', 'volume': '19', 'author': 'Franke', 'year': '1979', 'journal-title': 'Eur J Cell Biol'} / Eur J Cell Biol / The organization of cytokeratin filaments in the intestinal epithelium by Franke (1979)
10.1242/jcs.105.3.765 / J Cell Sci / Villin-induced growth of microvilli is reversibly inhibited by cytochalasin D by Friederich (1993)
10.1006/dbio.1994.1015 / Dev Biol / γ-Tubulin is asymmetrically distributed in the cortex of Xenopusoocytes by Gard (1994)
10.1083/jcb.113.2.275 / J Cell Biol / Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco-2 intestinal epithelial cells by Gilbert (1991)
10.1016/0014-4827(86)90343-5 / Exp Cell Res / Characterization of the intermediate filament proteins of murine mammary gland epithelial cells by Hall (1986)
10.1016/0955-0674(95)80017-4 / Curr Opin Cell Biol / Molecular motors, membrane movements and physiology: emerging roles for myosins by Hasson (1995)
10.1083/jcb.101.3.838 / J Cell Biol / Expression and intracellular transport of microvillus membrane hydrolases in human intestinal epithelial cells by Hauri (1985)
10.1042/bj2500865 / Biochem J / Ectoenzymes of the kidney microvillar membrane. Differential solubilization by detergents can predict a glycosylphosphatidylinositol membrane anchor by Hooper (1988)
10.1083/jcb.123.1.47 / J Cell Biol / Protein transport to the dendritic plasma membrane of cultured neurons is regulated by rab8p by Huber (1993)
10.1083/jcb.81.1.67 / J Cell Biol / The terminal web. A reevaluation of its structure and function by Hull (1979)
10.1016/0014-4827(92)90167-7 / Exp Cell Res / Cytokeratin reorganization induced by adenosine diphosphate in kidney epithelial cells by Kartha (1992)
10.1053/gast.1996.v110.pm8566599 / Gastroenterology / Cytosolic distribution of villin in M cells from mouse Peyer's patches correlates with the absence of a brush border by Kerneis (1996)
10.1242/dev.100.3.543 / Development / Polar asymmetry in the organization of the cortical cytokeratin system of Xenopus laevisoocytes and embryos by Klymkowsky (1987)
10.1126/science.6186022 / Science (Wash DC) / Drug-induced alterations of cytokeratin organization in cultured epithelial cells by Knapp (1983)
10.1038/227680a0 / Nature (Lond) / Cleavage of structural proteins during the assembly of bacteriophage T4 by Laemmli (1970)
10.1038/372801a0 / Nature (Lond) / Involvement of microtubule motors in basolateral and apical transport in kidney cells by Lafont (1994)
10.1083/jcb.111.4.1351 / J Cell Biol / Biogenetic pathways of plasma membrane proteins in CACO-2, a human intestinal epithelial cell line by Le Bivic (1990)
10.1073/pnas.85.24.9557 / Proc Natl Acad Sci USA / Polarized apical distribution of glycosyl-phosphatidylinositolanchored proteins in a renal epithelial cell line by Lisanti (1988)
10.1073/pnas.86.10.3474 / Proc Natl Acad Sci USA / Characterization of oligonucleotide transport into living cells by Loke (1989)
10.1146/annurev.cb.08.110192.001105 / Annu Rev Cell Biol / The differentiating intestinal epithelial cell: establishment and maintenance of functions through interactions between cellular structures by Louvard (1992)
10.1016/0092-8674(90)90594-5 / Cell / Sorting of endogenous plasma membrane proteins occurs from two sites in cultured human intestinal epithelial cells (Caco-2) by Matter (1990)
10.1016/0955-0674(94)90111-2 / Curr Opin Cell Biol / Organization and function of the cytoskeleton in polarized epithelial cells: a component of the protein sorting machinery by Mays (1994)
10.1083/jcb.130.5.1105 / J Cell Biol / Hierarchy of mechanisms involved in generating Na/K-ATPase polarity in MDCK epithelial cells by Mays (1995)
10.1016/0092-8674(82)90400-7 / Cell / The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors, and cultured cells by Moll (1982)
10.1146/annurev.cb.01.110185.001233 / Annu Rev Cell Biol / Organization, chemistry, and assembly of the cytoskeletal apparatus of the intestinal brush border by Mooseker (1985)
10.1085/jgp.66.1.117 / J Gen Physiol / Routes of non-electrolyte permeability in gallbladder. Effects of 2,4,6,-triaminopyrimidinium (TAP) by Moreno (1975)
10.1002/bies.950170208 / Bioessays / Regulation of protein traffic in polarized epithelial cells by Mostov (1995)
10.1126/science.1439806 / Science (Wash DC) / Regulation of cell surface polarity from bacteria to mammals by Nelson (1992)
10.1083/jcb.104.6.1527 / J Cell Biol / Modulation of fodrin (membrane skeleton) stability by cell–cell contact in Madin-Darby canine kidney epithelial cells by Nelson (1987)
10.1038/328533a0 / Nature (Lond) / Ankyrin binding to (Na+-K+)ATPase and implications for the organization of membrane domains in polarized cells by Nelson (1987)
10.1083/jcb.108.3.893 / J Cell Biol / A membrane–cytoskeletal complex containing (Na+-K+)ATPase, ankyrin, and fodrin in Madin-Darby canine kidney (MDCK) cells: implications for the biogenesis of epithelial cell polarity by Nelson (1989)
10.1111/1523-1747.ep12371683 / J Investig Dermatol / Characteristics of oligonucleotide uptake in human kertinocyte cultures by Noonberg (1993)
10.1083/jcb.107.6.2377 / J Cell Biol / The polarized distribution of an apical cell surface glycoprotein is maintained by interactions with the cytoskeleton of Madin-Darby canine kidney cells by Ojakian (1988)
10.1177/38.3.1689337 / J Histochem Cytochem / Expression of intermediate-sized filaments in developing and adult human kidney and in renal cell carcinoma by Oosterwijk (1990)
10.1007/BF00218385 / Cell Tissue Res / Characterization of intermediate filaments and their structural organization during epithelium formation in pigmented epithelial cells of the retina in vitro by Owaribe (1986)
10.1016/0014-4827(90)90174-9 / Exp Cell Res / Determination of apical membrane polarity in mammary epithelial cell cultures: the role of cell-cell, cell-substratum and membrane-cytoskeleton interactions by Parry (1990)
10.1016/0003-2697(77)90043-4 / Anal Biochem / A simplification of the protein assay method of Lowry et al., which is more generally applicable by Peterson (1977)
10.1242/jcs.102.3.581 / J Cell Sci / Characterization of the enterocytelike brush border cytoskeleton of the C2BBe clones of the human intestinal cell line, Caco-2 by Peterson (1992)
10.1242/jcs.105.2.461 / J Cell Sci / An in vitro model for the analysis of intestinal brush border assembly. II. Changes in expression and localization of brush border proteins during cell contact induced brush border assembly in Caco-2BBe cells by Peterson (1993)
{'key': '2023072822492546400_B70', 'first-page': '323', 'article-title': 'Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture', 'volume': '47', 'author': 'Pinto', 'year': '1983', 'journal-title': 'Biol Cell (Ivry Sur Seine)'} / Biol Cell (Ivry Sur Seine) / Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture by Pinto (1983)
10.1016/S0021-9258(18)99046-0 / J Biol Chem / Keratin expression in rat intestinal crypt and villus cells. Analysis with a panel of monoclonal antibodies by Quaroni (1990)
10.1083/jcb.126.6.1509 / J Cell Biol / Orientation of spindle axis and distribution of plasma membrane proteins during cell division in polarized MDCKII cells by Reinsch (1994)
10.1006/dbio.1993.1119 / Dev Biol / Apical orientation of the microtubule organizing center and associated γ-tubulin during the polarization of the retinal pigment epithelium in vivo by Rizzolo (1993)
10.1242/jcs.107.11.3145 / J Cell Sci / A specifically apical submembrane intermediate filament cytoskeleton in non-brush-border epithelial cells by Rodriguez (1994)
10.1126/science.2672330 / Science (Wash DC) / Morphogenesis of the polarized epithelial cell phenotype by Rodriguez-Boulan (1989)
10.1146/annurev.ph.51.030189.003521 / Annu Rev Physiol / External and internal signals for epithelial cell surface polarization by Rodriguez-Boulan (1989)
10.1083/jcb.107.6.2363 / J Cell Biol / Selective anchoring in the specific plasma membrane domain: a role in epithelial cell polarity by Salas (1988)
10.1016/S0091-679X(08)61166-8 / Methods Cell Biol / Methods to estimate the polarized distribution of surface antigens in cultured epithelial cells by Rodriguez-Boulan (1989)
10.1083/jcb.105.1.335 / J Cell Biol / Assembly of the intestinal brush border: appearance and redistribution of microvillar core proteins in developing chick enterocytes by Shibayama (1987)
10.1016/0092-8674(90)90357-K / Cell / Polarized sorting in epithelia by Simons (1990)
10.1146/annurev.cb.01.110185.001331 / Annu Rev Cell Biol / Cell surface polarity in epithelia by Simons (1985)
{'key': '2023072822492546400_B82', 'first-page': '79', 'article-title': 'Tampering with cytokeratin expression results in cell dysfunction', 'volume': '3', 'author': 'Singh', 'year': '1994', 'journal-title': 'Epithelial Cell Biol'} / Epithelial Cell Biol / Tampering with cytokeratin expression results in cell dysfunction by Singh (1994)
{'key': '2023072822492546400_B83', 'first-page': '6075', 'article-title': 'Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF–10', 'volume': '50', 'author': 'Soule', 'year': '1990', 'journal-title': 'Cancer Res'} / Cancer Res / Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF–10 by Soule (1990)
10.1093/nar/15.23.10058 / Nucleic Acids Res / Sequence of cDNA coding for human keratin 19 by Stasiak (1987)
10.1083/jcb.103.3.755 / J Cell Biol / Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonnula occludens) in a variety of epithelia by Stevenson (1986)
10.1111/j.1600-0676.1990.tb00436.x / Liver / Expression of cytokeratin 19 during human liver organogenesis by Stosiek (1990)
{'key': '2023072822492546400_B87', 'first-page': '6087', 'article-title': 'Ultrastructural and immunocytochemical characterization of an immortalized human breast epithelial cell line, MCF-10', 'volume': '50', 'author': 'Tait', 'year': '1990', 'journal-title': 'Cancer Res'} / Cancer Res / Ultrastructural and immunocytochemical characterization of an immortalized human breast epithelial cell line, MCF-10 by Tait (1990)
10.1083/jcb.125.6.1371 / J Cell Biol / Perturbation of cell adhesion and microvilli formation by antisense oligonucleotides to ERM family members by Takeuchi (1994)
10.1073/pnas.76.9.4350 / Proc Natl Acad Sci USA / Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications by Towbin (1979)
10.1083/jcb.104.4.905 / J Cell Biol / Formation of the apical pole of epithelial (Madin-Darby canine kidney) cells: polarity of an apical protein is independent of tight junctions, while segregation of a basolateral marker requires cell–cell interactions by Vega-Salas (1987)
10.1083/jcb.104.5.1249 / J Cell Biol / Modulation of the expression of an apical plasma membrane protein of Madin-Darby canine kidney epithelial cells. Cell–cell interactions control the appearance of a novel intracellular storage compartment by Vega-Salas (1987)
10.1083/jcb.107.5.1717 / J Cell Biol / Exocytosis of vacuolar apical compartment (VAC): a cell–cell contact controlled mechanism for the establishment of the apical plasma membrane domain in epithelial cells by Vega-Salas (1988)
10.1242/jcs.102.2.185 / J Cell Sci / Establishing and maintaining epithelial cell polarity. Roles of protein sorting, delivery, and retention by Wollner (1992)
10.1089/ard.1993.3.53 / Antisense Res Dev / Comparison of cellular binding and uptake of antisense phosphodiester, phosphorothioate, and mixed phosphorothioate and methylphosphorylated oligonucleotides by Zhao (1993)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:47 p.m.)
Deposited	2 years ago (July 28, 2023, 6:50 p.m.)
Indexed	1 month, 3 weeks ago (July 2, 2025, 2:31 p.m.)
Issued	28 years, 4 months ago (April 21, 1997)
Published	28 years, 4 months ago (April 21, 1997)
Published Online	28 years, 4 months ago (April 21, 1997)
Published Print	28 years, 4 months ago (April 21, 1997)

Funders 0

None

BibTeX

@article{Salas_1997, title={The Apical Submembrane Cytoskeleton Participates in the Organization of the Apical Pole in Epithelial Cells}, volume={137}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.137.2.359}, DOI={10.1083/jcb.137.2.359}, number={2}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Salas, Pedro J.I. and Rodriguez, Marcelo L. and Viciana, Ana L. and Vega-Salas, Dora E. and Hauri, Hans-Peter}, year={1997}, month=apr, pages={359–375} }

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  "abstract": "<jats:p>In a previous publication (Rodriguez, M.L., M. Brignoni, and P.J.I. Salas. 1994. J. Cell Sci. 107: 3145\u20133151), we described the existence of a terminal web-like structure in nonbrush border cells, which comprises a specifically apical cytokeratin, presumably cytokeratin 19. In the present study we confirmed the apical distribution of cytokeratin 19 and expanded that observation to other epithelial cells in tissue culture and in vivo. In tissue culture, subconfluent cell stocks under continuous treatment with two different 21-mer phosphorothioate oligodeoxy nucleotides that targeted cytokeratin 19 mRNA enabled us to obtain confluent monolayers with a partial (40\u201370%) and transitory reduction in this protein. The expression of other cytoskeletal proteins was undisturbed. This downregulation of cytokeratin 19 resulted in (a) decrease in the number of microvilli; (b) disorganization of the apical (but not lateral or basal) filamentous actin and abnormal apical microtubules; and (c) depletion or redistribution of apical membrane proteins as determined by differential apical\u2013basolateral biotinylation. In fact, a subset of detergent-insoluble proteins was not expressed on the cell surface in cells with lower levels of cytokeratin 19. Apical proteins purified in the detergent phase of Triton X-114 (typically integral membrane proteins) and those differentially extracted in Triton X-100 at 37\u00b0C or in n-octyl-\u03b2-d-glycoside at 4\u00b0C (representative of GPIanchored proteins), appeared partially redistributed to the basolateral domain. A transmembrane apical protein, sucrase isomaltase, was found mispolarized in a subpopulation of the cells treated with antisense oligonucleotides, while the basolateral polarity of Na+\u2013 K+ATPase was not affected. Both sucrase isomaltase and alkaline phosphatase (a GPI-anchored protein) appeared partially depolarized in A19 treated CACO-2 monolayers as determined by differential biotinylation, affinity purification, and immunoblot. These results suggest that an apical submembrane cytoskeleton of intermediate filaments is expressed in a number of epithelia, including those without a brush border, although it may not be universal. In addition, these data indicate that this structure is involved in the organization of the apical region of the cytoplasm and the apical membrane.</jats:p>",
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      "first-page": "589",
      "DOI": "10.1016/0092-8674(94)90496-0",
      "article-title": "Deconstructing the microtubule-organizing center",
      "volume": "76",
      "author": "Archer",
      "year": "1994",
      "journal-title": "Cell"
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      "first-page": "136",
      "DOI": "10.1016/0955-0674(94)90127-9",
      "article-title": "Membrane\u2013actin microfilament connections: an increasing diversity of players related to band 4.1",
      "volume": "6",
      "author": "Arpin",
      "year": "1994",
      "journal-title": "Curr Opin Cell Biol"
    },
    {
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      "DOI": "10.1083/jcb.127.6.1995",
      "article-title": "Functional differences betwen L- and T-plastin isoforms",
      "volume": "127",
      "author": "Arpin",
      "year": "1994",
      "journal-title": "J Cell Biol"
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      "first-page": "2817",
      "DOI": "10.1083/jcb.109.6.2817",
      "article-title": "The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium",
      "volume": "109",
      "author": "Bacallao",
      "year": "1989",
      "journal-title": "J Cell Biol"
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      "key": "2023072822492546400_B5",
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      "first-page": "109",
      "DOI": "10.1111/j.1432-0436.1990.tb00464.x",
      "article-title": "Cell-type specific and efficient synthesis of human cytokeratin 19 in transgenic mice",
      "volume": "45",
      "author": "Bader",
      "year": "1990",
      "journal-title": "Differentiation"
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      "key": "2023072822492546400_B7",
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      "first-page": "2909",
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      "article-title": "The network organization and the phosphorylation of cytokeratins are concomitantly modified by forskolin in the enterocyte-like differentiated CACO-2 cell line",
      "volume": "107",
      "author": "Baricault",
      "year": "1994",
      "journal-title": "J Cell Sci"
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      "key": "2023072822492546400_B8",
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      "first-page": "560",
      "DOI": "10.1083/jcb.102.2.560",
      "article-title": "Organization of cytokeratin bundles by desmosomes in rat mammary cells",
      "volume": "102",
      "author": "Bologna",
      "year": "1986",
      "journal-title": "J Cell Biol"
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      "key": "2023072822492546400_B9",
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      "first-page": "1604",
      "DOI": "10.1016/S0021-9258(19)69848-0",
      "article-title": "Phase separation of integral membrane proteins in Triton X-114 solution",
      "volume": "256",
      "author": "Bordier",
      "year": "1981",
      "journal-title": "J Biol Chem"
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    {
      "key": "2023072822492546400_B10",
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      "first-page": "1931",
      "DOI": "10.1242/jcs.108.5.1931",
      "article-title": "Cyclic AMP modulates the rate of \u201cconstitutive\u201d exocytosis of apical membrane proteins in Madin-Darby canine kidney cells",
      "volume": "108",
      "author": "Brignoni",
      "year": "1995",
      "journal-title": "J Cell Sci"
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      "first-page": "295",
      "DOI": "10.1016/0092-8674(84)90223-X",
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      "volume": "36",
      "author": "Brown",
      "year": "1984",
      "journal-title": "Cell"
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      "first-page": "533",
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      "volume": "68",
      "author": "Brown",
      "year": "1992",
      "journal-title": "Cell"
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      "first-page": "1123",
      "DOI": "10.1083/jcb.110.4.1123",
      "article-title": "Cytoskeletal control of centrioles movement during the establishment of polarity in MDCK cells",
      "volume": "110",
      "author": "Buendia",
      "year": "1990",
      "journal-title": "J Cell Biol"
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      "key": "2023072822492546400_B14",
      "doi-asserted-by": "crossref",
      "first-page": "939",
      "DOI": "10.1042/bj2850939",
      "article-title": "Changes in keratin expression during fetal and postnatal development of intestinal epithelial cells",
      "volume": "285",
      "author": "Calnek",
      "year": "1992",
      "journal-title": "Biochem J"
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      "key": "2023072822492546400_B15",
      "doi-asserted-by": "crossref",
      "first-page": "95",
      "DOI": "10.1111/j.1432-0436.1993.tb00649.x",
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      "volume": "53",
      "author": "Calnek",
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      "first-page": "259",
      "DOI": "10.1016/0165-022X(90)90084-P",
      "article-title": "Oligodeoxynucleoside phosphorothioate stability in subcellular extracts, culture media, sera, and cerebrospinal fluid",
      "volume": "20",
      "author": "Campbell",
      "year": "1990",
      "journal-title": "J Biochem Biophys Methods"
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    {
      "key": "2023072822492546400_B17",
      "first-page": "405",
      "article-title": "Suppression of villin expression by antisense RNA impairs brush border assembly in polarized epithelial intestinal cells",
      "volume": "14",
      "author": "Costa de Beauregard",
      "year": "1995",
      "journal-title": "EMBO (Eur Mol Biol Organ) J"
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    {
      "key": "2023072822492546400_B18",
      "first-page": "462",
      "article-title": "In vitro pharmacokinetics of phosphorothioated antisense oligonucleotides",
      "volume": "275",
      "author": "Crooke",
      "year": "1995",
      "journal-title": "J Pharmacol Exp Ther"
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      "key": "2023072822492546400_B19",
      "doi-asserted-by": "crossref",
      "first-page": "137",
      "DOI": "10.1016/0014-4827(87)90339-9",
      "article-title": "Turnover of cytokeratin polypeptides in mouse hepatocytes",
      "volume": "173",
      "author": "Denk",
      "year": "1987",
      "journal-title": "Exp Cell Res"
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      "key": "2023072822492546400_B20",
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      "first-page": "53",
      "DOI": "10.1111/j.1432-0436.1987.tb00151.x",
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      "volume": "35",
      "author": "Dockhorn-Dworniczak",
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      "first-page": "1038",
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      "volume": "107",
      "author": "Drenckhahn",
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      "journal-title": "J Cell Biol"
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      "first-page": "1287",
      "DOI": "10.1126/science.2933809",
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      "volume": "230",
      "author": "Drenckhahn",
      "year": "1985",
      "journal-title": "Science (Wash DC)"
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      "first-page": "1114",
      "DOI": "10.1073/pnas.85.4.1114",
      "article-title": "Sequence of the human 40-kDa keratin reveals an unusual structure with very high sequence identity to the corresponding bovine keratin",
      "volume": "85",
      "author": "Eckert",
      "year": "1988",
      "journal-title": "Proc Natl Acad Sci USA"
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    {
      "key": "2023072822492546400_B24",
      "first-page": "169",
      "article-title": "Alteration of intermediate filament distribution in PtK1cells by acrylamide",
      "volume": "37",
      "author": "Eckert",
      "year": "1985",
      "journal-title": "Eur J Cell Biol"
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    {
      "key": "2023072822492546400_B25",
      "doi-asserted-by": "crossref",
      "first-page": "403",
      "DOI": "10.1101/SQB.1982.046.01.039",
      "article-title": "In vivo disruption of the cytokeratin cytoskeleton in cultured epithelial cells by microinjection of antikeratin: evidence for the presence of an intermediate-filament\u2013organizing center",
      "volume": "46",
      "author": "Eckert",
      "year": "1982",
      "journal-title": "Cold Spring Harbor Symp Quant Biol"
    },
    {
      "key": "2023072822492546400_B26",
      "doi-asserted-by": "crossref",
      "first-page": "407",
      "DOI": "10.1242/dev.106.2.407",
      "article-title": "Differential localization of villin and fimbrin during development of the mouse visceral endoderm and intestinal epithelium",
      "volume": "106",
      "author": "Ezzell",
      "year": "1989",
      "journal-title": "Development"
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    {
      "key": "2023072822492546400_B27",
      "doi-asserted-by": "crossref",
      "first-page": "591",
      "DOI": "10.1016/S0960-9822(95)00117-5",
      "article-title": "Microvillus assembly. Not actin alone",
      "volume": "5",
      "author": "Fath",
      "year": "1995",
      "journal-title": "Curr Biol"
    },
    {
      "key": "2023072822492546400_B28"
    },
    {
      "key": "2023072822492546400_B29",
      "doi-asserted-by": "crossref",
      "first-page": "595",
      "DOI": "10.1083/jcb.117.3.595",
      "article-title": "Suppression of kinesin expression in cultured hippocampal neurons using antisense oligonucleotides",
      "volume": "117",
      "author": "Ferreira",
      "year": "1992",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822492546400_B30",
      "doi-asserted-by": "crossref",
      "first-page": "201",
      "DOI": "10.1242/dev.121.1.201",
      "article-title": "Pattern of localization and cytoskeletal association of two vegetally localized RNAs, Vg1 and Xcat-2",
      "volume": "121",
      "author": "Forristall",
      "year": "1995",
      "journal-title": "Development (Camb)"
    },
    {
      "key": "2023072822492546400_B31",
      "first-page": "255",
      "article-title": "The organization of cytokeratin filaments in the intestinal epithelium",
      "volume": "19",
      "author": "Franke",
      "year": "1979",
      "journal-title": "Eur J Cell Biol"
    },
    {
      "key": "2023072822492546400_B32",
      "doi-asserted-by": "crossref",
      "first-page": "765",
      "DOI": "10.1242/jcs.105.3.765",
      "article-title": "Villin-induced growth of microvilli is reversibly inhibited by cytochalasin D",
      "volume": "105",
      "author": "Friederich",
      "year": "1993",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "2023072822492546400_B33",
      "doi-asserted-by": "crossref",
      "first-page": "131",
      "DOI": "10.1006/dbio.1994.1015",
      "article-title": "\u03b3-Tubulin is asymmetrically distributed in the cortex of Xenopusoocytes",
      "volume": "161",
      "author": "Gard",
      "year": "1994",
      "journal-title": "Dev Biol"
    },
    {
      "key": "2023072822492546400_B34",
      "doi-asserted-by": "crossref",
      "first-page": "275",
      "DOI": "10.1083/jcb.113.2.275",
      "article-title": "Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco-2 intestinal epithelial cells",
      "volume": "113",
      "author": "Gilbert",
      "year": "1991",
      "journal-title": "J Cell Biol"
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    {
      "key": "2023072822492546400_B35",
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      "first-page": "379",
      "DOI": "10.1016/0014-4827(86)90343-5",
      "article-title": "Characterization of the intermediate filament proteins of murine mammary gland epithelial cells",
      "volume": "162",
      "author": "Hall",
      "year": "1986",
      "journal-title": "Exp Cell Res"
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    {
      "key": "2023072822492546400_B36",
      "doi-asserted-by": "crossref",
      "first-page": "587",
      "DOI": "10.1016/0955-0674(95)80017-4",
      "article-title": "Molecular motors, membrane movements and physiology: emerging roles for myosins",
      "volume": "7",
      "author": "Hasson",
      "year": "1995",
      "journal-title": "Curr Opin Cell Biol"
    },
    {
      "key": "2023072822492546400_B37",
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      "first-page": "838",
      "DOI": "10.1083/jcb.101.3.838",
      "article-title": "Expression and intracellular transport of microvillus membrane hydrolases in human intestinal epithelial cells",
      "volume": "101",
      "author": "Hauri",
      "year": "1985",
      "journal-title": "J Cell Biol"
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    {
      "key": "2023072822492546400_B38",
      "doi-asserted-by": "crossref",
      "first-page": "865",
      "DOI": "10.1042/bj2500865",
      "article-title": "Ectoenzymes of the kidney microvillar membrane. Differential solubilization by detergents can predict a glycosylphosphatidylinositol membrane anchor",
      "volume": "250",
      "author": "Hooper",
      "year": "1988",
      "journal-title": "Biochem J"
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    {
      "key": "2023072822492546400_B39",
      "doi-asserted-by": "crossref",
      "first-page": "47",
      "DOI": "10.1083/jcb.123.1.47",
      "article-title": "Protein transport to the dendritic plasma membrane of cultured neurons is regulated by rab8p",
      "volume": "123",
      "author": "Huber",
      "year": "1993",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822492546400_B40",
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      "first-page": "67",
      "DOI": "10.1083/jcb.81.1.67",
      "article-title": "The terminal web. A reevaluation of its structure and function",
      "volume": "81",
      "author": "Hull",
      "year": "1979",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822492546400_B41",
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      "first-page": "219",
      "DOI": "10.1016/0014-4827(92)90167-7",
      "article-title": "Cytokeratin reorganization induced by adenosine diphosphate in kidney epithelial cells",
      "volume": "200",
      "author": "Kartha",
      "year": "1992",
      "journal-title": "Exp Cell Res"
    },
    {
      "key": "2023072822492546400_B42",
      "doi-asserted-by": "crossref",
      "first-page": "515",
      "DOI": "10.1053/gast.1996.v110.pm8566599",
      "article-title": "Cytosolic distribution of villin in M cells from mouse Peyer's patches correlates with the absence of a brush border",
      "volume": "110",
      "author": "Kerneis",
      "year": "1996",
      "journal-title": "Gastroenterology"
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    {
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      "first-page": "543",
      "DOI": "10.1242/dev.100.3.543",
      "article-title": "Polar asymmetry in the organization of the cortical cytokeratin system of Xenopus laevisoocytes and embryos",
      "volume": "100",
      "author": "Klymkowsky",
      "year": "1987",
      "journal-title": "Development"
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    {
      "key": "2023072822492546400_B44",
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      "first-page": "501",
      "DOI": "10.1126/science.6186022",
      "article-title": "Drug-induced alterations of cytokeratin organization in cultured epithelial cells",
      "volume": "219",
      "author": "Knapp",
      "year": "1983",
      "journal-title": "Science (Wash DC)"
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    {
      "key": "2023072822492546400_B45",
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      "first-page": "680",
      "DOI": "10.1038/227680a0",
      "article-title": "Cleavage of structural proteins during the assembly of bacteriophage T4",
      "volume": "227",
      "author": "Laemmli",
      "year": "1970",
      "journal-title": "Nature (Lond)"
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    {
      "key": "2023072822492546400_B46",
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      "first-page": "801",
      "DOI": "10.1038/372801a0",
      "article-title": "Involvement of microtubule motors in basolateral and apical transport in kidney cells",
      "volume": "372",
      "author": "Lafont",
      "year": "1994",
      "journal-title": "Nature (Lond)"
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    {
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      "first-page": "1351",
      "DOI": "10.1083/jcb.111.4.1351",
      "article-title": "Biogenetic pathways of plasma membrane proteins in CACO-2, a human intestinal epithelial cell line",
      "volume": "111",
      "author": "Le Bivic",
      "year": "1990",
      "journal-title": "J Cell Biol"
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    {
      "key": "2023072822492546400_B48",
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      "first-page": "9557",
      "DOI": "10.1073/pnas.85.24.9557",
      "article-title": "Polarized apical distribution of glycosyl-phosphatidylinositolanchored proteins in a renal epithelial cell line",
      "volume": "85",
      "author": "Lisanti",
      "year": "1988",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2023072822492546400_B49",
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      "first-page": "3474",
      "DOI": "10.1073/pnas.86.10.3474",
      "article-title": "Characterization of oligonucleotide transport into living cells",
      "volume": "86",
      "author": "Loke",
      "year": "1989",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2023072822492546400_B50",
      "doi-asserted-by": "crossref",
      "first-page": "157",
      "DOI": "10.1146/annurev.cb.08.110192.001105",
      "article-title": "The differentiating intestinal epithelial cell: establishment and maintenance of functions through interactions between cellular structures",
      "volume": "8",
      "author": "Louvard",
      "year": "1992",
      "journal-title": "Annu Rev Cell Biol"
    },
    {
      "key": "2023072822492546400_B51",
      "doi-asserted-by": "crossref",
      "first-page": "429",
      "DOI": "10.1016/0092-8674(90)90594-5",
      "article-title": "Sorting of endogenous plasma membrane proteins occurs from two sites in cultured human intestinal epithelial cells (Caco-2)",
      "volume": "60",
      "author": "Matter",
      "year": "1990",
      "journal-title": "Cell"
    },
    {
      "key": "2023072822492546400_B52",
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      "first-page": "16",
      "DOI": "10.1016/0955-0674(94)90111-2",
      "article-title": "Organization and function of the cytoskeleton in polarized epithelial cells: a component of the protein sorting machinery",
      "volume": "6",
      "author": "Mays",
      "year": "1994",
      "journal-title": "Curr Opin Cell Biol"
    },
    {
      "key": "2023072822492546400_B53",
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      "first-page": "1105",
      "DOI": "10.1083/jcb.130.5.1105",
      "article-title": "Hierarchy of mechanisms involved in generating Na/K-ATPase polarity in MDCK epithelial cells",
      "volume": "130",
      "author": "Mays",
      "year": "1995",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822492546400_B54",
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      "first-page": "11",
      "DOI": "10.1016/0092-8674(82)90400-7",
      "article-title": "The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors, and cultured cells",
      "volume": "31",
      "author": "Moll",
      "year": "1982",
      "journal-title": "Cell"
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    {
      "key": "2023072822492546400_B55",
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      "first-page": "209",
      "DOI": "10.1146/annurev.cb.01.110185.001233",
      "article-title": "Organization, chemistry, and assembly of the cytoskeletal apparatus of the intestinal brush border",
      "volume": "1",
      "author": "Mooseker",
      "year": "1985",
      "journal-title": "Annu Rev Cell Biol"
    },
    {
      "key": "2023072822492546400_B56",
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      "first-page": "117",
      "DOI": "10.1085/jgp.66.1.117",
      "article-title": "Routes of non-electrolyte permeability in gallbladder. Effects of 2,4,6,-triaminopyrimidinium (TAP)",
      "volume": "66",
      "author": "Moreno",
      "year": "1975",
      "journal-title": "J Gen Physiol"
    },
    {
      "key": "2023072822492546400_B57",
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      "first-page": "129",
      "DOI": "10.1002/bies.950170208",
      "article-title": "Regulation of protein traffic in polarized epithelial cells",
      "volume": "17",
      "author": "Mostov",
      "year": "1995",
      "journal-title": "Bioessays"
    },
    {
      "key": "2023072822492546400_B58",
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      "first-page": "948",
      "DOI": "10.1126/science.1439806",
      "article-title": "Regulation of cell surface polarity from bacteria to mammals",
      "volume": "258",
      "author": "Nelson",
      "year": "1992",
      "journal-title": "Science (Wash DC)"
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    {
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      "first-page": "1527",
      "DOI": "10.1083/jcb.104.6.1527",
      "article-title": "Modulation of fodrin (membrane skeleton) stability by cell\u2013cell contact in Madin-Darby canine kidney epithelial cells",
      "volume": "104",
      "author": "Nelson",
      "year": "1987",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2023072822492546400_B60",
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      "first-page": "533",
      "DOI": "10.1038/328533a0",
      "article-title": "Ankyrin binding to (Na+-K+)ATPase and implications for the organization of membrane domains in polarized cells",
      "volume": "328",
      "author": "Nelson",
      "year": "1987",
      "journal-title": "Nature (Lond)"
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      "volume": "108",
      "author": "Nelson",
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      "DOI": "10.1111/1523-1747.ep12371683",
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      "volume": "101",
      "author": "Noonberg",
      "year": "1993",
      "journal-title": "J Investig Dermatol"
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      "first-page": "2377",
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      "author": "Ojakian",
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      "author": "Oosterwijk",
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      "author": "Owaribe",
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      "author": "Parry",
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      "author": "Peterson",
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      "author": "Peterson",
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      "author": "Peterson",
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      "article-title": "Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture",
      "volume": "47",
      "author": "Pinto",
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      "journal-title": "Biol Cell (Ivry Sur Seine)"
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      "volume": "266",
      "author": "Quaroni",
      "year": "1990",
      "journal-title": "J Biol Chem"
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      "first-page": "1509",
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      "author": "Reinsch",
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      "author": "Rizzolo",
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      "author": "Rodriguez",
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      "author": "Shibayama",
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      "article-title": "Tampering with cytokeratin expression results in cell dysfunction",
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