|
|
|
|
|
|
|
|
|||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | |||||
doi: 10.1242/10.1242/jcs.00117
Research Article |
1 Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9039, USA
2 Departments of Biology and Cell Biology, University of Virginia, Charlottesville, Virginia 22903, USA
* Author for correspondence (e-mail: dorothy.mundy{at}utsouthwestern.edu
Accepted 21 August 2002
Live cell, time-lapse microscopy was used to study trafficking of caveolin-1-GFP in stably expressing CHO cells. Multiple cytological and biochemical tests verified that caveolin-1-GFP was a reliable marker for endogenous caveolin-1. At steady state, most caveolin-1-GFP was either at the cell surface associated with invaginated caveolae or near the centrosome in caveosomes. Live cell fluorescence imaging indicated that while much of the caveolin-1-GFP in caveolae at the cell surface was relatively sessile, numerous, highly motile caveolin-1-GFP-positive vesicles were present within the cell interior. These vesicles moved at speeds ranging from 0.3-2 µm/second and movement was abolished when microtubules were depolymerized with nocodazole. In the absence of microtubules, cell surface invaginated caveolae increased more than twofold and they became organized into linear arrays. Complete depolymerization of the actin cytoskeleton with latrunculin A, by contrast, triggered rapid and massive movements of caveolin-positive structures towards the centrosomal region of the cell. The caveolar membrane system of CHO cells therefore appears to be comprised of three caveolin-1-containing compartments. These include caveolae that are confined to the cell surface by cortical actin filaments, the peri-centrosomal caveosomes and caveolar vesicles, which we call `cavicles', that move constitutively and bi-directionally along microtubules between the cell surface and caveosomes. The behavior of cavicles suggests that they function as transport intermediates between caveolae and caveosomes.
Key words: Caveolin, Recycling endosome, Caveolae, Caveosome
This article has been cited by other articles:
|
|
 |
|
  C.-K. Lai, K.-S. Jeng, K. Machida, and M. M. C. Lai Association of Hepatitis C Virus Replication Complexes with Microtubules and Actin Filaments Is Dependent on the Interaction of NS3 and NS5A J. Virol., September 1, 2008; 82(17): 8838 - 8848. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Jiao, V. Garg, B. Yang, T. S. Elton, and K. Hu Protein Kinase C-{epsilon} Induces Caveolin-Dependent Internalization of Vascular Adenosine 5'-Triphosphate-Sensitive K+ Channels Hypertension, September 1, 2008; 52(3): 499 - 506. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S.-K. Cha, T. Wu, and C.-L. Huang Protein kinase C inhibits caveolae-mediated endocytosis of TRPV5 Am J Physiol Renal Physiol, May 1, 2008; 294(5): F1212 - F1221. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. To, S. Kulkarni, T. Pawson, T. Honda, G. W. Gribble, M. B. Sporn, J. L. Wrana, and G. M. Di Guglielmo The Synthetic Triterpenoid 2-Cyano-3,12-dioxooleana-1,9-dien-28-oic Acid-Imidazolide Alters Transforming Growth Factor {beta}-dependent Signaling and Cell Migration by Affecting the Cytoskeleton and the Polarity Complex J. Biol. Chem., April 25, 2008; 283(17): 11700 - 11713. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. L. Jewell, W. Luo, E. Oh, Z. Wang, and D. C. Thurmond Filamentous Actin Regulates Insulin Exocytosis through Direct Interaction with Syntaxin 4 J. Biol. Chem., April 18, 2008; 283(16): 10716 - 10726. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Liu and P. F. Pilch A Critical Role of Cavin (Polymerase I and Transcript Release Factor) in Caveolae Formation and Organization J. Biol. Chem., February 15, 2008; 283(7): 4314 - 4322. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. D. Kojic, B. Joshi, P. Lajoie, P. U. Le, M. E. Cox, D. A. Turbin, S. M. Wiseman, and I. R. Nabi Raft-dependent Endocytosis of Autocrine Motility Factor Is Phosphatidylinositol 3-Kinase-dependent in Breast Carcinoma Cells J. Biol. Chem., October 5, 2007; 282(40): 29305 - 29313. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. F. Pilch, R. P. Souto, L. Liu, M. P. Jedrychowski, E. A. Berg, C. E. Costello, and S. P. Gygi Cellular spelunking: exploring adipocyte caveolae J. Lipid Res., October 1, 2007; 48(10): 2103 - 2111. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. A. Predescu, D. N. Predescu, and A. B. Malik Molecular determinants of endothelial transcytosis and their role in endothelial permeability Am J Physiol Lung Cell Mol Physiol, October 1, 2007; 293(4): L823 - L842. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Carlile-Klusacek and V. Rizzo Endothelial cytoskeletal reorganization in response to PAR1 stimulation is mediated by membrane rafts but not caveolae Am J Physiol Heart Circ Physiol, July 1, 2007; 293(1): H366 - H375. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Balbis, A. Parmar, Y. Wang, G. Baquiran, and B. I. Posner Compartmentalization of Signaling-Competent Epidermal Growth Factor Receptors in Endosomes Endocrinology, June 1, 2007; 148(6): 2944 - 2954. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Leyt, N. Melamed-Book, J.-P. Vaerman, S. Cohen, A. M. Weiss, and B. Aroeti Cholesterol-sensitive Modulation of Transcytosis Mol. Biol. Cell, June 1, 2007; 18(6): 2057 - 2071. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Nizzari, V. Venezia, E. Repetto, V. Caorsi, R. Magrassi, M. C. Gagliani, P. Carlo, T. Florio, G. Schettini, C. Tacchetti, et al. Amyloid Precursor Protein and Presenilin1 Interact with the Adaptor GRB2 and Modulate ERK 1,2 Signaling J. Biol. Chem., May 4, 2007; 282(18): 13833 - 13844. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
X.-H. Sun, D. C. Flynn, V. Castranova, L. L. Millecchia, A. R. Beardsley, and J. Liu Identification of a Novel Domain at the N Terminus of Caveolin-1 That Controls Rear Polarization of the Protein and Caveolae Formation J. Biol. Chem., March 9, 2007; 282(10): 7232 - 7241. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. N. Shajahan, A. Wang, M. Decker, R. D. Minshall, M. C. Liu, and R. Clarke Caveolin-1 Tyrosine Phosphorylation Enhances Paclitaxel-mediated Cytotoxicity J. Biol. Chem., February 23, 2007; 282(8): 5934 - 5943. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P.-K. Fang, K. R. Solomon, L. Zhuang, M. Qi, M. McKee, M. R. Freeman, and P. C. Yelick Caveolin-1{alpha} and -1{beta} Perform Nonredundant Roles in Early Vertebrate Development Am. J. Pathol., December 1, 2006; 169(6): 2209 - 2222. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. D. Landry, M. Denis, S. Nandi, S. Bell, A. M. Vaughan, and X. Zha ATP-binding Cassette Transporter A1 Expression Disrupts Raft Membrane Microdomains through Its ATPase-related Functions J. Biol. Chem., November 24, 2006; 281(47): 36091 - 36101. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Ushio-Fukai and R. W. Alexander Caveolin-Dependent Angiotensin II Type 1 Receptor Signaling in Vascular Smooth Muscle Hypertension, November 1, 2006; 48(5): 797 - 803. [Full Text] [PDF]
|
|
|
|
 |
|
 S. Ryoo, C. A. Lemmon, K. G. Soucy, G. Gupta, A. R. White, D. Nyhan, A. Shoukas, L. H. Romer, and D. E. Berkowitz Oxidized Low-Density Lipoprotein-Dependent Endothelial Arginase II Activation Contributes to Impaired Nitric Oxide Signaling Circ. Res., October 27, 2006; 99(9): 951 - 960. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Pellinen and J. Ivaska Integrin traffic. J. Cell Sci., September 15, 2006; 119(Pt 18): 3723 - 3731. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. P. Head, H. H. Patel, D. M. Roth, F. Murray, J. S. Swaney, I. R. Niesman, M. G. Farquhar, and P. A. Insel Microtubules and Actin Microfilaments Regulate Lipid Raft/Caveolae Localization of Adenylyl Cyclase Signaling Components J. Biol. Chem., September 8, 2006; 281(36): 26391 - 26399. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Schilling, N. Opitz, A. Wiesenthal, S. Oess, R. Tikkanen, W. Muller-Esterl, and A. Icking Translocation of Endothelial Nitric-Oxide Synthase Involves a Ternary Complex with Caveolin-1 and NOSTRIN Mol. Biol. Cell, September 1, 2006; 17(9): 3870 - 3880. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. S. Terada Specificity in reactive oxidant signaling: think globally, act locally J. Cell Biol., August 28, 2006; 174(5): 615 - 623. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Scholz, P. McDermott, M. Garnovskaya, T. N. Gallien, S. Huettelmaier, C. DeRienzo, and G. Cooper IV Microtubule-associated protein-4 (MAP-4) inhibits microtubule-dependent distribution of mRNA in isolated neonatal cardiocytes Cardiovasc Res, August 1, 2006; 71(3): 506 - 516. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Liebl, F. Difato, L. Hornikova, P. Mannova, J. Stokrova, and J. Forstova Mouse Polyomavirus Enters Early Endosomes, Requires Their Acidic pH for Productive Infection, and Meets Transferrin Cargo in Rab11-Positive Endosomes J. Virol., May 1, 2006; 80(9): 4610 - 4622. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Mehta and A. B. Malik Signaling Mechanisms Regulating Endothelial Permeability Physiol Rev, January 1, 2006; 86(1): 279 - 367. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Eash and W. J. Atwood Involvement of Cytoskeletal Components in BK Virus Infectious Entry J. Virol., September 15, 2005; 79(18): 11734 - 11741. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Veluthakal, I. Chvyrkova, M. Tannous, P. McDonald, R. Amin, T. Hadden, D. C. Thurmond, M. J. Quon, and A. Kowluru Essential Role for Membrane Lipid Rafts in Interleukin-1{beta}-Induced Nitric Oxide Release From Insulin-Secreting Cells: Potential Regulation by Caveolin-1+ Diabetes, September 1, 2005; 54(9): 2576 - 2585. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Tagawa, A. Mezzacasa, A. Hayer, A. Longatti, L. Pelkmans, and A. Helenius Assembly and trafficking of caveolar domains in the cell: caveolae as stable, cargo-triggered, vesicular transporters J. Cell Biol., August 29, 2005; 170(5): 769 - 779. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Misinzo, P. Meerts, M. Bublot, J. Mast, H. M. Weingartl, and H. J. Nauwynck Binding and entry characteristics of porcine circovirus 2 in cells of the porcine monocytic line 3D4/31 J. Gen. Virol., July 1, 2005; 86(7): 2057 - 2068. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. S. Golubkov, S. Boyd, A. Y. Savinov, A. V. Chekanov, A. L. Osterman, A. Remacle, D. V. Rozanov, S. J. Doxsey, and A. Y. Strongin Membrane Type-1 Matrix Metalloproteinase (MT1-MMP) Exhibits an Important Intracellular Cleavage Function and Causes Chromosome Instability J. Biol. Chem., July 1, 2005; 280(26): 25079 - 25086. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. M. Brainard, A. J. Miller, J. R. Martens, and S. K. England Maxi-K channels localize to caveolae in human myometrium: a role for an actin-channel-caveolin complex in the regulation of myometrial smooth muscle K+ current Am J Physiol Cell Physiol, July 1, 2005; 289(1): C49 - C57. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Pol, S. Martin, M. A. Fernandez, M. Ingelmo-Torres, C. Ferguson, C. Enrich, and R. G. Parton Cholesterol and Fatty Acids Regulate Dynamic Caveolin Trafficking through the Golgi Complex and between the Cell Surface and Lipid Bodies Mol. Biol. Cell, April 1, 2005; 16(4): 2091 - 2105. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Beardsley, K. Fang, H. Mertz, V. Castranova, S. Friend, and J. Liu Loss of Caveolin-1 Polarity Impedes Endothelial Cell Polarization and Directional Movement J. Biol. Chem., February 4, 2005; 280(5): 3541 - 3547. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Signoret, L. Hewlett, S. Wavre, A. Pelchen-Matthews, M. Oppermann, and M. Marsh Agonist-induced Endocytosis of CC Chemokine Receptor 5 Is Clathrin Dependent Mol. Biol. Cell, February 1, 2005; 16(2): 902 - 917. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Kenis, H. van Genderen, A. Bennaghmouch, H. A. Rinia, P. Frederik, J. Narula, L. Hofstra, and C. P. M. Reutelingsperger Cell Surface-expressed Phosphatidylserine and Annexin A5 Open a Novel Portal of Cell Entry J. Biol. Chem., December 10, 2004; 279(50): 52623 - 52629. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. N. Shajahan, C. Tiruppathi, A. V. Smrcka, A. B. Malik, and R. D. Minshall G{beta}{gamma} Activation of Src Induces Caveolae-mediated Endocytosis in Endothelial Cells J. Biol. Chem., November 12, 2004; 279(46): 48055 - 48062. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. W. Cohen, R. Hnasko, W. Schubert, and M. P. Lisanti Role of Caveolae and Caveolins in Health and Disease Physiol Rev, October 1, 2004; 84(4): 1341 - 1379. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. Lallemand-Breitenbach, M. Quesnoit, V. Braun, A. El Marjou, C. Pous, B. Goud, and F. Perez CLIPR-59 Is a Lipid Raft-associated Protein Containing a Cytoskeleton-associated Protein Glycine-rich Domain (CAP-Gly) That Perturbs Microtubule Dynamics J. Biol. Chem., September 24, 2004; 279(39): 41168 - 41178. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Zuo, M. Ushio-Fukai, L. L. Hilenski, and R. W. Alexander Microtubules Regulate Angiotensin II Type 1 Receptor and Rac1 Localization in Caveolae/Lipid Rafts: Role in Redox Signaling Arterioscler. Thromb. Vasc. Biol., July 1, 2004; 24(7): 1223 - 1228. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Pang, P. U. Le, and I. R. Nabi Ganglioside GM1 levels are a determinant of the extent of caveolae/raft-dependent endocytosis of cholera toxin to the Golgi apparatus J. Cell Sci., March 15, 2004; 117(8): 1421 - 1430. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Yamaga, M. Sekimata, M. Fujii, K. Kawai, H. Kamata, H. Hirata, Y. Homma, and H. Yagisawa A PLC{delta}1-binding protein, p122/RhoGAP, is localized in caveolin-enriched membrane domains and regulates caveolin internalization Genes Cells, January 1, 2004; 9(1): 25 - 37. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Hnasko and M. P. Lisanti The Biology of Caveolae: Lessons from Caveolin Knockout Mice and Implications for Human Disease Mol. Interv., December 1, 2003; 3(8): 445 - 464. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Nichols Caveosomes and endocytosis of lipid rafts J. Cell Sci., December 1, 2003; 116(23): 4707 - 4714. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. W. Hornef, B. H. Normark, A. Vandewalle, and S. Normark Intracellular Recognition of Lipopolysaccharide by Toll-like Receptor 4 in Intestinal Epithelial Cells J. Exp. Med., October 20, 2003; 198(8): 1225 - 1235. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Mani, F. Cheng, B. Havsmark, M. Jonsson, M. Belting, and L.-A. Fransson Prion, Amyloid {beta}-derived Cu(II) Ions, or Free Zn(II) Ions Support S-Nitroso-dependent Autocleavage of Glypican-1 Heparan Sulfate J. Biol. Chem., October 3, 2003; 278(40): 38956 - 38965. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-B. Manneville, S. Etienne-Manneville, P. Skehel, T. Carter, D. Ogden, and M. Ferenczi Interaction of the actin cytoskeleton with microtubules regulates secretory organelle movement near the plasma membrane in human endothelial cells J. Cell Sci., October 1, 2003; 116(19): 3927 - 3938. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. L. Boyd, H. Park, H. Yi, Y. C. Boo, G. P. Sorescu, M. Sykes, and H. Jo Chronic shear induces caveolae formation and alters ERK and Akt responses in endothelial cells Am J Physiol Heart Circ Physiol, August 7, 2003; 285(3): H1113 - H1122. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M.-O. Parat, B. Anand-Apte, and P. L. Fox Differential Caveolin-1 Polarization in Endothelial Cells during Migration in Two and Three Dimensions Mol. Biol. Cell, August 1, 2003; 14(8): 3156 - 3168. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Venkatesan, J. J. Rose, R. Lodge, P. M. Murphy, and J. F. Foley Distinct Mechanisms of Agonist-induced Endocytosis for Human Chemokine Receptors CCR5 and CXCR4 Mol. Biol. Cell, August 1, 2003; 14(8): 3305 - 3324. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. R. Nabi and P. U. Le Caveolae/raft-dependent endocytosis J. Cell Biol., May 26, 2003; 161(4): 673 - 677. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. U. Le and I. R. Nabi Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum J. Cell Sci., March 15, 2003; 116(6): 1059 - 1071. [Abstract] [Full Text] [PDF]
|
|
