Cited by 234Microtubule and mitosis dynamicsCellular transport and secretionDrug Transport and Resistance Mechanisms

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Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco-2 intestinal epithelial cells

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Gilbert, T, Le Bivic, A, Quaroni, A, Rodriguez-Boulan, E·1991·The Journal of Cell Biology

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Abstract

We characterized the three-dimensional organization of microtubules in the human intestinal epithelial cell line Caco-2 by laser scanning confocal microscopy. Microtubules formed a dense network approximately 4-microns thick parallel to the cell surface in the apical pole and a loose network 1-micron thick in the basal pole. Between the apical and the basal bundles, microtubules run parallel to the major cell axis, concentrated in the vicinity of the lateral membrane. Colchicine treatment for 4 h depolymerized 99.4% of microtubular tubulin. Metabolic pulse chase, in combination with domain-selective biotinylation, immune and streptavidin precipitation was used to study the role of microtubules in the sorting and targeting of four apical and one basolateral markers. Apical proteins have been recently shown to use both direct and transcytotic (via the basolateral membrane) routes to the apical surface of Caco-2 cells. Colchicine treatment slowed down the transport to the cell surface of apical and basolateral proteins, but the effect on the apical proteins was much more drastic and affected both direct and indirect pathways. The final effect of microtubular disruption on the distribution of apical proteins depended on the degree of steady-state polarization of the individual markers in control cells. Aminopeptidase N (APN) and sucrase-isomaltase (SI), which normally reach a highly polarized distribution (110 and 75 times higher on the apical than on the basolateral side) were still relatively polarized (9 times) after colchicine treatment. The decrease in the polarity of APN and SI was mostly due to an increase in the residual basolateral expression (10% of control total surface expression) since 80% of the newly synthesized APN was still transported, although at a slower rate, to the apical surface in the absence of microtubules. Alkaline phosphatase and dipeptidylpeptidase IV, which normally reach only low levels of apical polarity (four times and six times after 20 h chase, nine times and eight times at steady state) did not polarize at all in the presence of colchicine due to slower delivery to the apical surface and increased residence time in the basolateral surface. Colchicine-treated cells displayed an ectopic localization of microvilli or other apical markers in the basolateral surface and large intracellular vacuoles. Polarized secretion into apical and basolateral media was also affected by microtubular disruption. Thus, an intact microtubular network facilitates apical protein transport to the cell surface of Caco-2 cells via direct and indirect routes; this role appears to be crucial for the final polarity of some apical plasma membrane proteins but only an enhancement factor for others.

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Authors: Gilbert, T., Le Bivic, A., Quaroni, A., & Rodriguez-Boulan, E.
Affiliations: Cornell University (US)
Department of Cell Biology and Anatomy, Cornell University Medical College, New York 10021.
ORCID: Gilbert, T
Rodriguez-Boulan, E
Venue: The Journal of Cell Biology
Publisher: Rockefeller University Press
Published: 1991-04-15
Volume: 113
Issue: 2
Pages: 275-288
ISSN: 0021-9525 (ISSN-L)
1540-8140
DOI: 10.1083/jcb.113.2.275
PMC: PMC2288937
OpenAlex: W1997986612
Cited by: 234
References: 70
Citations by year: 2024: 1 · 2022: 2 · 2021: 3 · 2020: 2 · 2019: 1 · 2018: 3 · 2017: 5 · 2015: 2 · 2014: 4 · 2013: 3 · 2012: 2
FWCI: 7.10
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: The Journal of Cell Biology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion, cc-by-nc-sa)
PubMed (publishedVersion)
Funders: American Cancer Society
Association pour la Recherche sur le Cancer
Centre National de la Recherche Scientifique
National Institutes of Health (5r01hl037675-26)
National Heart, Lung, and Blood Institute (HL37675)
National Institute of General Medical Sciences (GM-34107, R01GM034107)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
Keywords: microtubules, Caco-2 cells, intestinal epithelial cells, protein targeting, colchicine, tubulin depolymerization, apical-basal polarity, transcytosis, CD13, sucrase-isomaltase, alkaline phosphatase, dipeptidyl peptidase IV, microvilli
MeSH terms: Alkaline Phosphatase, Aminopeptidases, Bacterial Proteins, Biological Transport, Colchicine, Dipeptidyl-Peptidases and Tripeptidyl-Peptidases, Epithelial Cells, Epithelium, Fluorescent Antibody Technique, Humans, Kinetics, Lasers, Membrane Proteins, Microscopy, Electron, Scanning, Microtubules, Chemical Precipitation, Proteins, Sucrase-Isomaltase Complex, Tubulin, Tumor Cells, Cultured, Dipeptidyl Peptidase 4, CD13 Antigens, Streptavidin

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Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco-2 intestinal epithelial cells

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