Caveolae as an additional route for influenza virus endocytosis in MDCK cells

• Autorzy: Nunes-Correia I , Eulalio A. , Nir S. , Pedroso de Lima M.C.
• Języki publikacji: EN

Abstrakty

EN

Clathrin-mediated endocytosis has been described as the primary internalization pathway for many viruses, including the influenza virus. However, caveolae, an alternative clathrin-independent endocytotic pathway, has also been described as mediating the entry of some molecules, including viruses. To address the question of pathway selection by the influenza virus, we have investigated whether the virus is internalized via clathrin-coated pits and/or caveolae in Madin Darby canine kidney (MDCK) cells. By applying pharmacological manipulations to selectively disrupt the cell internalization pathways, we found that, in MDCK cells, the influenza virus may be internalized via caveolae in addition to entry by clathrin-mediated endocytosis. However, a small contribution by another mode of entry, as recently proposed [Sieczkarski, S.B. and Whittaker, G.R., J. Virol. 76 (2002) 10455-10464], cannot be excluded.

Słowa kluczowe

EN

cell; virus; endocytosis; Madin Darby canine kidney; caveola; influenza virus; clathrin

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2004
• Tom: 09
• Numer: 1
• Opis fizyczny: p.47-60,fig.,ref.

Twórcy

autor

Nunes-Correia I

• University of Coimbra, Apartado 3126, 3000 Coimbra, Portugal

autor

Eulalio A.

autor

Nir S.

autor

Pedroso de Lima M.C.

Bibliografia

• 1. Cox, N.J. and Fukuda, K. Influenza. Infect. Dis. Clin. North Am. 12 (1998) 27-38.
• 2. Hernandez, L.D., Hoffman, L.R., Wolfsberg, T.G. and White, J.M. Virus-cell and cell-cell fusion. Annu. Rev. Cell Dev. Biol. 12 (1996) 627-661.
• 3. Hoekstra, D. and Pedroso de Lima, M.C. Membrane interactions of HIV: Implications for pathogenesis and theraphy in AIDS, in: Advances in membrane fluidity (Aloia, R.C. and Curtain, C.C., Eds.), Wiley-Liss, New York, 1992, 71-97.
• 4. Wiley, D.C. and Skehel, J.J. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochem. 56 (1987) 365-394.
• 5. Bergelson, L.D., Bukrinskaya, A.G., Prokazova, N.V., Shaposhnikova, G.I., Kocharov, S.L., Shevchenko, V.P., Kornilaeva, G.V. and Fomina-Ageeva, E.V. Role of gangliosides in reception of influenza virus. Eur. J. Biochem. 128 (1982) 467-474.
• 6. Paulson, J.C., Rogers, G.N., Murayama, J.I., Sze, G. and Martin, E. Biological implications of influenza virus receptor specificity, in: Virus attachment and entry into cells. (Crowell, R.L. and Lonberg-Holm, K., Eds.) American Society for Microbiology, Washington, DC, 1986, 144-151.
• 7. Pedroso de Lima, M.C., Ramalho-Santos, J., Flasher, D., Slepushkin, V.A., Nir, S. and Düzgünes, N. Target cell membrane sialic acid modulates both binding and fusion activity of influenza virus. Biochim. Biophys. Acta 1236 (1995) 323-330.
• 8. Mellman, I. Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol. 12 (1996) 575-625.
• 9. Gaudin, Y., Ruigrok, R.W.H. and Brunner, J. Low-pH induced conformational changes in viral fusion proteins: implications for the fusion mechanism. J. Gen. Virol. 76 (1995) 1541-1556.
• 10. Ramalho-Santos, J. and Pedroso de Lima, M.C. The influenza virus hemagglutinin: a model protein in the study of membrane fusion. Biochim. Biophys. Acta 1376 (1998) 147-154.
• 11. Marsh, M. and Helenius, A. Adsorptive endocytosis of Semliki Forest virus. J. Mol. Biol. 142 (1980) 439-454.
• 12. Matlin, K.S., Reggio, H., Helenius, A. and Simons, K. Infectious entry pathway of influenza virus in a canine kidney cell line. J. Cell Biol. 91 (1981) 601-613.
• 13. Matlin, K.S., Reggio, H., Helenius, A. and Simons, K. Pathway of vesicular stomatitis virus entry leading to infection. J. Mol. Biol. 156 (1982) 609-631.
• 14. Anderson, R.G. The caveolae membrane system. Annu. Rev. Biochem. 67 (1998) 199-225.
• 15. Kartenbeck, J., Stukenbrok, H. and Helenius, A. Endocytosis of simian virus 40 into the endoplasmic reticulum. J. Cell Biol. 109 (1989) 2721-2729.
• 16. Orlandi, P.A. and Fishman, P.H. Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J. Cell Biol. 141 (1998) 905-915.
• 17. Pelkmans, L., Kartenbeck, J. and Helenius, A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3 (2001) 473-483.
• 18. Ros-Baró, A., López-Iglesias, C., Peiró, S., Bellido, D., Palacín, M., Zorzano, A. and Camps, M. Lipid rafts are required for GLUT4 internalization in adipose cells. Proc. Natl. Acad. Sci. USA 98 (2001) 12050-12055.
• 19. Lefkowitz, R.J. G protein-coupled receptors. III. New roles for receptor kinases and beta-arrestins in receptor signaling and desensitization. J. Biol. Chem. 273 (1998) 18677-18680.
• 20. Schnitzer, J.E., Oh, P., Pinney, E. and Allard, J. Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of selected macromolecules. J. Cell Biol. 127 (1994) 1217-1232.
• 21. Brown, D.A. and London, E. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14 (1998) 111-136.
• 22. Brown, D.A. and London, E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275 (2000) 17221-17224.
• 23. Simons, K. and Ikonen, E. Functional rafts in cell membranes. Nature 387 (1997) 569-572.
• 24. Rothberg, K.G., Ying, Y.S., Kamen, B.A. and Anderson, R.G. Cholesterol controls the clustering of the glycophospholipid-anchored membrane receptor for 5-methyltetrahydrofolate. J. Cell Biol. 111 (1990) 2931-2938.
• 25. Rothberg, K.G., Heuser, J.E., Donzell, W.C., Ying, Y.S., Glenney, J.R. and Anderson, R.G. Caveolin, a protein component of caveolae membrane coats. Cell 68 (1992) 673-682.
• 26. Neufeld, E.B., Cooney, A.M., Pitha, J., Dawidowicz, E.A., Dwyer, N.K., Pentchev, P.G. and Blanchette-Mackie, E.J. Intracellular trafficking of cholesterol monitored with a cyclodextrin. J. Biol. Chem. 271 (1996) 21604-21613.
• 27. Hoekstra, D. and Kok, J.W. Entry mechanisms of enveloped viruses. Implications for fusion of intracellular membranes. Biosci. Rep. 9 (1989) 273-305.
• 28. Thomsen, P., Roepstorff, K., Stahlhut, M. and van Deurs, B. Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol. Biol. Cell 13 (2002) 238-250.
• 29. Nunes-Correia, I., Ramalho-Santos, J., Nir, S. and Pedroso de Lima., M.C. Interactions of influenza virus with cultured cells: detailed kinetic modeling of binding and endocytosis. Biochemistry 38 (1999) 1095-1101.
• 30. Nunes-Correia, I., Nir, S. and Pedroso de Lima, M.C. Kinetics of influenza virus fusion with the endosomal and plasma membranes of cultured cells: effect of temperature. J. Memb. Biol. 195 (2003) 21-26.
• 31. Nunes-Correia, I., Eulálio, A., Nir, S., Düzgünes, N., Ramalho-Santos, J. and Pedroso de Lima, M.C. Fluorescent probes for monitoring virus fusion kinetics: comparative evaluation of reliability. Biochim. Biophys. Acta 1561 (2002) 65-75.
• 32. Sieczkarski S.B. and Whittaker, G.R. Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J. Virol. 76 (2002) 10455-10464.
• 33. Hoekstra, D., de Boer, T., Klappe, K. and Wilschut, J. Fluorescent method for measuring the kinetics of fusion between biological membranes. Biochemistry 23 (1984) 5675-5681.
• 34. Ramalho-Santos, J., Pedroso de Lima, M.C. and Nir, S. Partial fusion activity of influenza virus towards liposomes and erythrocyte ghosts is distinct from viral inactivation. J. Biol. Chem. 271 (1996) 23902-23906.
• 35. Sedmak, J.J. and Grossero, F.E. A rapid sensitive and versatile assay for protein using coomassie brilliant Blue G250. Anal. Biochem. 79 (1977) 544-552.
• 36. Lee, K.-D., Nir, S. and Papahadjopoulos, D. Quantitative analysis of liposome-cell interactions in vitro: rate constants of binding and endocytosis with suspension and adherent J774 cells and human monocytes. Biochemistry 32 (1993) 889-899.
• 37. Wang, L.H., Rothberg, K.G. and Anderson, R.G. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J. Cell Biol. 123 (1993) 1107-1117.
• 38. Larkin, J.M., Brown M.S., Goldstein J.L. and Anderson R.G. Depletion of intracellular potassium arrests coated pit formation and receptor-mediated endocytosis in fibroblasts. Cell 33 (1983) 273-285.
• 39. Okamoto, Y., Ninomiya H., Miwa, S. and Masaki, T. Cholesterol oxidation switches the internalization pathway of endothelin receptor type A from caveolae to clathrin-coated pits in Chinese hamster ovary cells. J. Biol. Chem. 275 (2000) 6439-6446.
• 40. Pitha, J., Irie, T., Sklar, P.B. and Nye, J.S. Drug solubilizers to aid pharmacologists: amorphous cyclodextrin derivatives. Life Sci. 43 (1988) 493-502.
• 41. Chen, X. and Resh, M D. Cholesterol depletion from the plasma membrane triggers ligand-independent activation of the epidermal growth factor receptor. J. Biol. Chem. 277 (2002) 49631-49637.
• 42. Hooper, N.M. Detergent-insoluble glycosphingolipid/cholesterol-rich membrane domains, lipid rafts and caveolae (review). Mol. Membr. Biol. 16 (1999) 145-156.
• 43. Ostermeyer, A.G., Beckrich, B.T., Ivarson, K.A., Grove, K.E. and Brown, D.A. Glycosphingolipids are not essential for formation of detergent-resistant membrane rafts in melanoma cells. J. Biol. Chem. 274 (1999) 34459-34466.
• 44. Zuhorn, I.S., Kalicharan, R. and Hoekstra, D. Lipoplex-mediated transfection of mammalian cells occurs through the cholesterol-dependent clathrin-mediated pathway of endocytosis. J. Biol. Chem. 277 (2002) 18021-18028.
• 45. Schnitzer, J.E., Allard, J. and Oh, P. NEM inhibits transcytosis, endocytosis, and capillary permeability: implication of caveolae fusion in endothelia. Am. J. Physiol.. 268 (1995) H48-H55.