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© The Rockefeller University Press, 0021-9525/1998//85 $5.00
The Journal of Cell Biology, Volume 141, Number 1, , 1998 85-99

Dynamin-mediated Internalization of Caveolae

John R. Henley^*, Eugene W.A. Krueger, Barbara J. Oswald, and Mark A. McNiven^*,,

^* Department of Molecular Neuroscience, Department of Biochemistry and Molecular Biology, and Center for Basic Research in Digestive Diseases, Mayo Clinic, Rochester, Minnesota 55905

The dynamins comprise an expanding family of ubiquitously expressed 100-kD GTPases that have been implicated in severing clathrin-coated pits during receptor-mediated endocytosis. Currently, it is unclear whether the different dynamin isoforms perform redundant functions or participate in distinct endocytic processes. To define the function of dynamin II in mammalian epithelial cells, we have generated and characterized peptide-specific antibodies to domains that either are unique to this isoform or conserved within the dynamin family. When microinjected into cultured hepatocytes these affinity-purified antibodies inhibited clathrin-mediated endocytosis and induced the formation of long plasmalemmal invaginations with attached clathrin-coated pits. In addition, clusters of distinct, nonclathrin-coated, flask-shaped invaginations resembling caveolae accumulated at the plasma membrane of antibody-injected cells. In support of this, caveola-mediated endocytosis of labeled cholera toxin B was inhibited in antibody-injected hepatocytes. Using immunoisolation techniques an anti-dynamin antibody isolated caveolar membranes directly from a hepatocyte postnuclear membrane fraction. Finally, double label immunofluorescence microscopy revealed a striking colocalization between dynamin and the caveolar coat protein caveolin. Thus, functional in vivo studies as well as ultrastructural and biochemical analyses indicate that dynamin mediates both clathrin-dependent endocytosis and the internalization of caveolae in mammalian cells.

Abbreviations used in this paper: Dyn1/2/3, dynamin I/II/III; GPI, glycosylphosphatidylinositol; HLA, human leukocyte antigen; pIgA-R, polymeric IgA receptor.

Please address all correspondence to Mark A. McNiven, Center for Basic Research in Digestive Diseases, Mayo Clinic, Rochester, MN 55905. Tel.: (507) 284-0683. Fax: (507) 284-0762. E-mail: mcniven.mark{at}mayo.edu

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• Krueger, E. W., Orth, J. D., Cao, H., McNiven, M. A. (2003). A Dynamin-Cortactin-Arp2/3 Complex Mediates Actin Reorganization in Growth Factor-stimulated Cells. Mol. Biol. Cell 14: 1085-1096 [Abstract] [Full Text]  
• Ashbourne Excoffon, K. J. D., Moninger, T., Zabner, J. (2003). The Coxsackie B Virus and Adenovirus Receptor Resides in a Distinct Membrane Microdomain. J. Virol. 77: 2559-2567 [Abstract] [Full Text]  
• Fishman, P. H., Orlandi, P. A. (2003). Cholera toxin internalization and intoxication. J. Cell Sci. 116: 431-432 [Full Text]  
• Tse, S. M. L., Furuya, W., Gold, E., Schreiber, A. D., Sandvig, K., Inman, R. D., Grinstein, S. (2003). Differential Role of Actin, Clathrin, and Dynamin in Fcgamma Receptor-mediated Endocytosis and Phagocytosis. J. Biol. Chem. 278: 3331-3338 [Abstract] [Full Text]  
• Haigis, M. C., Raines, R. T. (2003). Secretory ribonucleases are internalized by a dynamin-independent endocytic pathway. J. Cell Sci. 116: 313-324 [Abstract] [Full Text]  
• Ehehalt, R., Keller, P., Haass, C., Thiele, C., Simons, K. (2003). Amyloidogenic processing of the Alzheimer {beta}-amyloid precursor protein depends on lipid rafts. JCB 160: 113-123 [Abstract] [Full Text]  
• Holroyd, P., Lang, T., Wenzel, D., De Camilli, P., Jahn, R. (2002). Imaging direct, dynamin-dependent recapture of fusing secretory granules on plasma membrane lawns from PC12 cells. Proc. Natl. Acad. Sci. USA 99: 16806-16811 [Abstract] [Full Text]  
• Lu, J.-C., Scott, P., Strous, G. J., Schuler, L. A. (2002). Multiple Internalization Motifs Differentially Used by Prolactin Receptor Isoforms Mediate Similar Endocytic Pathways. Mol. Endocrinol. 16: 2515-2527 [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]  

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