Lowering the cholesterol content of MA104 cells inhibits receptor- mediated transport of folate

doi:10.1083/jcb.118.1.63

This Article

	Full Text (PDF, 1081K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Chang, W. J.
	Articles by Anderson, R. G.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Chang, W. J.
	Articles by Anderson, R. G.


Social Bookmarking

	What's this?

ARTICLES

Lowering the cholesterol content of MA104 cells inhibits receptor- mediated transport of folate

WJ Chang, KG Rothberg, BA Kamen and RG Anderson
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas 75235.

The folate receptor is clustered on the surface of MA104 cells in association with caveolae. This relationship is thought to be essential for the proper internalization and recycling of the receptor during the delivery of 5-methyltetrahydrofolate to the cytoplasm of folate- depleted cells. Both the clustered organization of the receptor and the integrity of caveolae are disrupted when cells are deprived of cholesterol. We now show that cholesterol depletion of MA104 cells markedly reduces the rate of 5-methyltetrahydrofolate internalization and causes a 70% decline in the number of receptors present in the internal, recycling compartment. This effect is consistent with morphologic data showing that cholesterol-depleted MA104 cells have a reduced number of caveolae as well as fewer receptors per caveolae.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Stirling, L., Williams, M. R., Morielli, A. D. (2009). Dual Roles for RHOA/RHO-Kinase In the Regulated Trafficking of a Voltage-sensitive Potassium Channel. Mol. Biol. Cell 20: 2991-3002 [Abstract] [Full Text]
Kitami, T., Rubio, R., O'Brien, W., Quackenbush, J., Nadeau, J. H. (2008). Gene-environment interactions reveal a homeostatic role for cholesterol metabolism during dietary folate perturbation in mice. Physiol. Genomics 35: 182-190 [Abstract] [Full Text]
Abdel Nour, A. M., Ringot, D., Gueant, J.-L., Chango, A. (2007). Folate receptor and human reduced folate carrier expression in HepG2 cell line exposed to fumonisin B1 and folate deficiency. Carcinogenesis 28: 2291-2297 [Abstract] [Full Text]
Landry, Y. D., Denis, M., Nandi, S., Bell, S., Vaughan, A. M., Zha, X. (2006). ATP-binding Cassette Transporter A1 Expression Disrupts Raft Membrane Microdomains through Its ATPase-related Functions. J. Biol. Chem. 281: 36091-36101 [Abstract] [Full Text]
Reversi, A., Rimoldi, V., Brambillasca, S., Chini, B. (2006). Effects of cholesterol manipulation on the signaling of the human oxytocin receptor. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291: R861-R869 [Abstract] [Full Text]
Mineo, C., Deguchi, H., Griffin, J. H., Shaul, P. W. (2006). Endothelial and Antithrombotic Actions of HDL. Circ. Res. 98: 1352-1364 [Abstract] [Full Text]
Vihanto, M. M., Vindis, C., Djonov, V., Cerretti, D. P., Huynh-Do, U. (2006). Caveolin-1 is required for signaling and membrane targeting of EphB1 receptor tyrosine kinase. J. Cell Sci. 119: 2299-2309 [Abstract] [Full Text]
Zaas, D. W., Duncan, M. J., Li, G., Wright, J. R., Abraham, S. N. (2005). Pseudomonas Invasion of Type I Pneumocytes Is Dependent on the Expression and Phosphorylation of Caveolin-2. J. Biol. Chem. 280: 4864-4872 [Abstract] [Full Text]
Paulos, C. M., Reddy, J. A., Leamon, C. P., Turk, M. J., Low, P. S. (2004). Ligand Binding and Kinetics of Folate Receptor Recycling in Vivo: Impact on Receptor-Mediated Drug Delivery. Mol. Pharmacol. 66: 1406-1414 [Abstract] [Full Text]
Sandoval, R. M., Kennedy, M. D., Low, P. S., Molitoris, B. A. (2004). Uptake and trafficking of fluorescent conjugates of folic acid in intact kidney determined using intravital two-photon microscopy. Am. J. Physiol. Cell Physiol. 287: C517-C526 [Abstract] [Full Text]
Cho, C.-H., Lee, C. S., Chang, M., Jang, I.-H., Kim, S. J., Hwang, I., Ryu, S. H., Lee, C. O., Koh, G. Y. (2004). Localization of VEGFR-2 and PLD2 in endothelial caveolae is involved in VEGF-induced phosphorylation of MEK and ERK. Am. J. Physiol. Heart Circ. Physiol. 286: H1881-H1888 [Abstract] [Full Text]
Pouvreau, S., Berthier, C., Blaineau, S., Amsellem, J., Coronado, R., Strube, C. (2004). Membrane cholesterol modulates dihydropyridine receptor function in mice fetal skeletal muscle cells. J. Physiol. 555: 365-381 [Abstract] [Full Text]
Thorn, H., Stenkula, K. G., Karlsson, M., Ortegren, U., Nystrom, F. H., Gustavsson, J., Stralfors, P. (2003). Cell Surface Orifices of Caveolae and Localization of Caveolin to the Necks of Caveolae in Adipocytes. Mol. Biol. Cell 14: 3967-3976 [Abstract] [Full Text]
Coppens, I., Joiner, K. A. (2003). Host but Not Parasite Cholesterol Controls Toxoplasma Cell Entry by Modulating Organelle Discharge. Mol. Biol. Cell 14: 3804-3820 [Abstract] [Full Text]
Chao, W. T., Fan, S. S., Chen, J. K., Yang, V. C. (2003). Visualizing caveolin-1 and HDL in cholesterol-loaded aortic endothelial cells. J. Lipid Res. 44: 1094-1099 [Abstract] [Full Text]
Huo, H., Guo, X., Hong, S., Jiang, M., Liu, X., Liao, K. (2003). Lipid Rafts/Caveolae Are Essential for Insulin-like Growth Factor-1 Receptor Signaling during 3T3-L1 Preadipocyte Differentiation Induction. J. Biol. Chem. 278: 11561-11569 [Abstract] [Full Text]
Sato, K.-i., Iwasaki, T., Ogawa, K., Konishi, M., Tokmakov, A. A., Fukami, Y. (2003). Low density detergent-insoluble membrane of Xenopus eggs: subcellular microdomain for tyrosine kinase signaling in fertilization. Development 129: 885-896 [Abstract] [Full Text]
Shaul, P. W (2003). Endothelial nitric oxide synthase, caveolae and the development of atherosclerosis. J. Physiol. 547: 21-33 [Abstract] [Full Text]
Hua, H., Munk, S., Whiteside, C. I. (2003). Endothelin-1 activates mesangial cell ERK1/2 via EGF-receptor transactivation and caveolin-1 interaction. Am. J. Physiol. Renal Physiol. 284: F303-F312 [Abstract] [Full Text]
Labrecque, L., Royal, I., Surprenant, D. S., Patterson, C., Gingras, D., Beliveau, R. (2003). Regulation of Vascular Endothelial Growth Factor Receptor-2 Activity by Caveolin-1 and Plasma Membrane Cholesterol. Mol. Biol. Cell 14: 334-347 [Abstract] [Full Text]
Isshiki, M., Ying, Y.-s., Fujita, T., Anderson, R. G. W. (2002). A Molecular Sensor Detects Signal Transduction from Caveolae in Living Cells. J. Biol. Chem. 277: 43389-43398 [Abstract] [Full Text]
Liu, P., Rudick, M., Anderson, R. G. W. (2002). Multiple Functions of Caveolin-1. J. Biol. Chem. 277: 41295-41298 [Full Text]
Heese-Peck, A., Pichler, H., Zanolari, B., Watanabe, R., Daum, G., Riezman, H. (2002). Multiple Functions of Sterols in Yeast Endocytosis. Mol. Biol. Cell 13: 2664-2680 [Abstract] [Full Text]
Anderson, R. G. W., Jacobson, K. (2002). A Role for Lipid Shells in Targeting Proteins to Caveolae, Rafts, and Other Lipid Domains. Science 296: 1821-1825 [Abstract] [Full Text]
Garver, W. S., Krishnan, K., Gallagos, J. R., Michikawa, M., Francis, G. A., Heidenreich, R. A. (2002). Niemann-Pick C1 protein regulates cholesterol transport to the trans-Golgi network and plasma membrane caveolae. J. Lipid Res. 43: 579-589 [Abstract] [Full Text]
Kovbasnjuk, O., Edidin, M., Donowitz, M. (2002). Role of lipid rafts in Shiga toxin 1 interaction with the apical surface of Caco-2 cells. J. Cell Sci. 114: 4025-4031 [Abstract] [Full Text]
MINEO, C., SHAUL, P.W. (2002). Modulation of Endothelial NO Production by High-density Lipoprotein. Cold Spring Harb Symp Quant Biol 67: 459-470 [Abstract]
Bickel, P. E. (2002). Lipid rafts and insulin signaling. Am. J. Physiol. Endocrinol. Metab. 282: E1-E10 [Abstract] [Full Text]
Thomsen, P., Roepstorff, K., Stahlhut, M., van Deurs, B. (2002). Caveolae Are Highly Immobile Plasma Membrane Microdomains, Which Are not Involved in Constitutive Endocytic Trafficking. Mol. Biol. Cell 13: 238-250 [Abstract] [Full Text]
Ushio-Fukai, M., Hilenski, L., Santanam, N., Becker, P. L., Ma, Y., Griendling, K. K., Alexander, R. W. (2001). Cholesterol Depletion Inhibits Epidermal Growth Factor Receptor Transactivation by Angiotensin II in Vascular Smooth Muscle Cells. ROLE OF CHOLESTEROL-RICH MICRODOMAINS AND FOCAL ADHESIONS IN ANGIOTENSIN II SIGNALING. J. Biol. Chem. 276: 48269-48275 [Abstract] [Full Text]
Mangé, A., Nishida, N., Milhavet, O., McMahon, H. E. M., Casanova, D., Lehmann, S. (2000). Amphotericin B Inhibits the Generation of the Scrapie Isoform of the Prion Protein in Infected Cultures. J. Virol. 74: 3135-3140 [Abstract] [Full Text]
Koziak, K., Kaczmarek, E., Kittel, A., Sevigny, J., Blusztajn, J. K., Schulte am Esch, J. II, Imai, M., Guckelberger, O., Goepfert, C., Qawi, I., Robson, S. C. (2000). Palmitoylation Targets CD39/Endothelial ATP Diphosphohydrolase to Caveolae. J. Biol. Chem. 275: 2057-2062 [Abstract] [Full Text]
Blair, A., Shaul, P. W., Yuhanna, I. S., Conrad, P. A., Smart, E. J. (1999). Oxidized Low Density Lipoprotein Displaces Endothelial Nitric-oxide Synthase (eNOS) from Plasmalemmal Caveolae and Impairs eNOS Activation. J. Biol. Chem. 274: 32512-32519 [Abstract] [Full Text]
GUSTAVSSON, J., PARPAL, S., KARLSSON, M., RAMSING, C., THORN, H., BORG, M., LINDROTH, M., PETERSON, K. H., MAGNUSSON, K.-E., STRåLFORS, P. (1999). Localization of the insulin receptor in caveolae of adipocyte plasma membrane. FASEB J. 13: 1961-1971 [Abstract] [Full Text]
Munn, A. L., Heese-Peck, A., Stevenson, B. J., Pichler, H., Riezman, H. (1999). Specific Sterols Required for the Internalization Step of Endocytosis in Yeast. Mol. Biol. Cell 10: 3943-3957 [Abstract] [Full Text]
Christian, A. E., Byun, H.-S., Zhong, N., Wanunu, M., Marti, T., Fürer, A., Diederich, F., Bittman, R., Rothblat, G. H. (1999). Comparison of the capacity of {beta}-cyclodextrin derivatives and cyclophanes to shuttle cholesterol between cells and serum lipoproteins. J. Lipid Res. 40: 1475-1482 [Abstract] [Full Text]
Naslavsky, N., Shmeeda, H., Friedlander, G., Yanai, A., Futerman, A. H., Barenholz, Y., Taraboulos, A. (1999). Sphingolipid Depletion Increases Formation of the Scrapie Prion Protein in Neuroblastoma Cells Infected with Prions. J. Biol. Chem. 274: 20763-20771 [Abstract] [Full Text]
Peterson, T. E., Poppa, V., Ueba, H., Wu, A., Yan, C., Berk, B. C. (1999). Opposing Effects of Reactive Oxygen Species and Cholesterol on Endothelial Nitric Oxide Synthase and Endothelial Cell Caveolae. Circ. Res. 85: 29-37 [Abstract] [Full Text]
Rothblat, G. H., de la Llera-Moya, M., Atger, V., Kellner-Weibel, G., Williams, D. L., Phillips, M. C. (1999). Cell cholesterol efflux: integration of old and new observations provides new insights. J. Lipid Res. 40: 781-796 [Abstract] [Full Text]
Rodal, S. K., Skretting, G., Garred, O., Vilhardt, F., van Deurs, B., Sandvig, K. (1999). Extraction of Cholesterol with Methyl-beta -Cyclodextrin Perturbs Formation of Clathrin-coated Endocytic Vesicles. Mol. Biol. Cell 10: 961-974 [Abstract] [Full Text]
Gilbert, A, Paccaud, J., Foti, M, Porcheron, G, Balz, J, Carpentier, J. (1999). Direct demonstration of the endocytic function of caveolae by a cell-free assay. J. Cell Sci. 112: 1101-1110 [Abstract]
Shaul, P. W., Anderson, R. G.�W. (1998). Role of plasmalemmal caveolae in signal transduction. Am. J. Physiol. Lung Cell. Mol. Physiol. 275: L843-L851 [Abstract] [Full Text]
Field, F. J., Born, E., Murthy, S., Mathur, S. N. (1998). Caveolin is present in intestinal cells: role in cholesterol trafficking?. J. Lipid Res. 39: 1938-1950 [Abstract] [Full Text]
Furuchi, T., Anderson, R. G.�W. (1998). Cholesterol Depletion of Caveolae Causes Hyperactivation of Extracellular Signal-related Kinase (ERK). J. Biol. Chem. 273: 21099-21104 [Abstract] [Full Text]
Deckert, V., Brunet, A., Lantoine, F., Lizard, G., Brussel, E. M.-v., Monier, S., Lagrost, L., David-Dufilho, M., Gambert, P., Devynck, M.-A. (1998). Inhibition by Cholesterol Oxides of NO Release From Human Vascular Endothelial Cells. Arterioscler. Thromb. Vasc. Bio. 18: 1054-1060 [Abstract] [Full Text]
Orlandi, P. A., Fishman, P. H. (1998). Filipin-dependent Inhibition of Cholera Toxin: Evidence for Toxin Internalization and Activation through Caveolae-like Domains. JCB 141: 905-915 [Abstract] [Full Text]
Uittenbogaard, A., Ying, Y.-s., Smart, E. J. (1998). Characterization of a Cytosolic Heat-shock Protein-Caveolin Chaperone Complex. INVOLVEMENT IN CHOLESTEROL TRAFFICKING. J. Biol. Chem. 273: 6525-6532 [Abstract] [Full Text]
Lupu, C., Goodwin, C. A., Westmuckett, A. D., Emeis, J. J., Scully, M. F., Kakkar, V. V., Lupu, F. (1997). Tissue Factor Pathway Inhibitor in Endothelial Cells Colocalizes With Glycolipid Microdomains/Caveolae : Regulatory Mechanism(s) of the Anticoagulant Properties of the Endothelium. Arterioscler. Thromb. Vasc. Bio. 17: 2964-2974 [Abstract] [Full Text]
Stulnig, T. M., Berger, M., Sigmund, T., Stockinger, H., Horejsi, V., Waldhausl, W. (1997). Signal Transduction via Glycosyl Phosphatidylinositol-anchored Proteins in T Cells Is Inhibited by Lowering Cellular Cholesterol. J. Biol. Chem. 272: 19242-19247 [Abstract] [Full Text]
Stevens, V. L., Tang, J. (1997). Fumonisin B1-induced Sphingolipid Depletion Inhibits Vitamin Uptake via the Glycosylphosphatidylinositol-anchored Folate Receptor. J. Biol. Chem. 272: 18020-18025 [Abstract] [Full Text]
Babitt, J., Trigatti, B., Rigotti, A., Smart, E. J., Anderson, R. G.�W., Xu, S., Krieger, M. (1997). Murine SR-BI, a High Density Lipoprotein Receptor That Mediates Selective Lipid Uptake, Is N-Glycosylated and Fatty Acylated and Colocalizes with Plasma Membrane Caveolae. J. Biol. Chem. 272: 13242-13249 [Abstract] [Full Text]
Rehm, A., Ploegh, H. L. (1997). Assembly and Intracellular Targeting of the {beta}{gamma} Subunits of Heterotrimeric G Proteins. JCB 137: 305-317 [Abstract] [Full Text]
Fielding, C. J., Bist, A., Fielding, P. E. (1997). Caveolin mRNA levels are up-regulated by free cholesterol and down-regulated by oxysterols in fibroblast monolayers. Proc. Natl. Acad. Sci. USA 94: 3753-3758 [Abstract] [Full Text]
Baum, C. L., Reschly, E. J., Gayen, A. K., Groh, M. E., Schadick, K. (1997). Sterol Carrier Protein-2 Overexpression Enhances Sterol Cycling and Inhibits Cholesterol Ester Synthesis and High Density Lipoprotein Cholesterol Secretion. J. Biol. Chem. 272: 6490-6498 [Abstract] [Full Text]
Smart, E. J., Ying, Y.-s., Donzell, W. C., Anderson, R. G.W. (1996). A Role for Caveolin in Transport of Cholesterol from Endoplasmic Reticulum to Plasma Membrane. J. Biol. Chem. 271: 29427-29435 [Abstract] [Full Text]
Yancey, P. G., Rodrigueza, W. V., Kilsdonk, E. P.C., Stoudt, G. W., Johnson, W. J., Phillips, M. C., Rothblat, G. H. (1996). Cellular Cholesterol Efflux Mediated by Cyclodextrins. DEMONSTRATION OF KINETIC POOLS AND MECHANISM OF EFFLUX. J. Biol. Chem. 271: 16026-16034 [Abstract] [Full Text]
Mineo, C., James, G. L., Smart, E. J., Anderson, R. G. W. (1996). Localization of Epidermal Growth Factor-stimulated Ras/Raf-1 Interaction to Caveolae Membrane. J. Biol. Chem. 271: 11930-11935 [Abstract] [Full Text]
Shaul, P. W., Smart, E. J., Robinson, L. J., German, Z., Yuhanna, I. S., Ying, Y., Anderson, R. G. W., Michel, T. (1996). Acylation Targets Endothelial Nitric-oxide Synthase to Plasmalemmal Caveolae. J. Biol. Chem. 271: 6518-6522 [Abstract] [Full Text]
Liu, P., Anderson, R. G. W. (1995). Compartmentalized Production of Ceramide at the Cell Surface. J. Biol. Chem. 270: 27179-27185 [Abstract] [Full Text]
Liscum, L., Underwood, K. W. (1995). Intracellular Cholesterol Transport and Compartmentation. J. Biol. Chem. 270: 15443-15446 [Full Text]
Smart, E.J., Estes, K., Anderson, R.G.W. (1995). Inhibitors That Block Both the Internalization of Caveolae and the Return of Plasmalemmal Vesicles. Cold Spring Harb Symp Quant Biol 60: 243-248 [Abstract]
Peiro, S., Comella, J. X., Enrich, C., Martin-Zanca, D., Rocamora, N. (2000). PC12 Cells Have Caveolae That Contain TrkA. CAVEOLAE-DISRUPTING DRUGS INHIBIT NERVE GROWTH FACTOR-INDUCED, BUT NOT EPIDERMAL GROWTH FACTOR-INDUCED, MAPK PHOSPHORYLATION. J. Biol. Chem. 275: 37846-37852 [Abstract] [Full Text]
Uittenbogaard, A., Smart, E. J. (2000). Palmitoylation of Caveolin-1 Is Required for Cholesterol Binding, Chaperone Complex Formation, and Rapid Transport of Cholesterol to Caveolae. J. Biol. Chem. 275: 25595-25599 [Abstract] [Full Text]
Liu, P., Wang, P.-y., Michaely, P., Zhu, M., Anderson, R. G. W. (2000). Presence of Oxidized Cholesterol in Caveolae Uncouples Active Platelet-derived Growth Factor Receptors from Tyrosine Kinase Substrates. J. Biol. Chem. 275: 31648-31654 [Abstract] [Full Text]
Parpal, S., Karlsson, M., Thorn, H., Stralfors, P. (2001). Cholesterol Depletion Disrupts Caveolae and Insulin Receptor Signaling for Metabolic Control via Insulin Receptor Substrate-1, but Not for Mitogen-activated Protein Kinase Control. J. Biol. Chem. 276: 9670-9678 [Abstract] [Full Text]
Watson, R. T., Shigematsu, S., Chiang, S.-H., Mora, S., Kanzaki, M., Macara, I. G., Saltiel, A. R., Pessin, J. E. (2001). Lipid raft microdomain compartmentalization of TC10 is required for insulin signaling and GLUT4 translocation. JCB 154: 829-840 [Abstract] [Full Text]
Matveev, S. V., Smart, E. J. (2002). Heterologous desensitization of EGF receptors and PDGF receptors by sequestration in caveolae. Am. J. Physiol. Cell Physiol. 282: C935-C946 [Abstract] [Full Text]