Ebola virus enters host cells by macropinocytosis and clathrin-mediated endocytosis

Journal of Infectious Diseases

Volumn 204, Issue SUPPL. 3, 2011, Pages

  Aleksandrowicz, Paulina ^a,b   Marzi, Andrea ^c   Biedenkopf, Nadine ^d   Beimforde, Nadine ^a   Becker, Stephan ^d   Hoenen, Thomas ^d   Feldmann, Heinz ^c,e   Schnittler, Hans Joachim ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

^e PUBLIC HEALTH AGENCY OF CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

5 (N ETHYL N ISOPROPYL)AMILORIDE; ACTIN; CLATHRIN HEAVY CHAIN; DYNAMIN II; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; GLYCOPROTEIN GP1,2; LATRUNCULIN A; PROTEIN VP40; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; WORTMANNIN;

ANTIVIRAL ACTIVITY; ARTICLE; CAVEOLA; CLATHRIN MEDIATED ENDOCYTOSIS; CONTROLLED STUDY; EBOLA VIRUS; ENDOCYTOSIS; GENETIC TRANSFECTION; HOST CELL; MACROPINOCYTOSIS; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS ENTRY; VIRUS LIKE AGENT;

ACTINS; AMILORIDE; ANDROSTADIENES; ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; CAVEOLIN 1; CELL LINE; CLATHRIN; EBOLAVIRUS; ENDOCYTOSIS; EPITHELIAL CELLS; GENE SILENCING; HOST-PATHOGEN INTERACTIONS; HUMANS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; THIAZOLIDINES; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 80054774353     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jir326     Document Type: Article

References (51)

1. Sanchez A, Geisbert TW, Feldmann H. Marburg and Ebola viruses. In: Fields BN, Knipe DM, Howley PM, eds. Fields virology. 5th ed. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins, 2007.
2. Feldmann H, Jones S, Klenk HD, Schnittler HJ. Ebola virus: from discovery to vaccine. Nat Rev Immunol 2003; 3:677-85. (Pubitemid 37328670)
3. Geisbert TW, Jahrling PB. Exotic emerging viral diseases: progress and challenges. Nat Med 2004; 10:S110-21. (Pubitemid 40018234)
4. Schnittler HJ, Feldmann H. Marburg and Ebola hemorrhagic fevers: does the primary course of infection depend on the accessibility of organ-specific macrophages? Clin Infect Dis 1998; 27:404-6. (Pubitemid 28365774)
5. Feldmann H, Volchkov VE, Volchkova VA, Stroher U, Klenk HD. Biosynthesis and role of filoviral glycoproteins. J Gen Virol 2001; 82:2839-48. (Pubitemid 33107496)
6. Takada A, Watanabe S, Ito H, Okazaki K, Kida H, Kawaoka Y. Downregulation of beta1 integrins by Ebola virus glycoprotein: implication for virus entry. Virology 2000; 278:20-6. (Pubitemid 32002589)
7. Alvarez CP, Lasala F, Carrillo J, Muniz O, Corbi AL, Delgado R. C-type lectins DC-SIGN and L-SIGN mediate cellular entry by Ebola virus in cis and in trans. J Virol 2002; 76:6841-4. (Pubitemid 34633551)
8. Shimojima M, Ikeda Y, Kawaoka Y. The mechanism of Axl-mediated Ebola virus infection. J Infect Dis 2007; 196(Suppl 2):S259-63. (Pubitemid 351417269)
9. Becker S, Spiess M, Klenk HD. The asialoglycoprotein receptor is a potential liver-specific receptor for Marburg virus. J Gen Virol 1995; 76:393-9.
10. Mercer J, Helenius A. Virus entry by macropinocytosis. Nat Cell Biol 2009; 11:510-20.
11. Swanson JA. Shaping cups into phagosomes and macropinosomes. Nat Rev Mol Cell Biol 2008; 9:639-49.
12. Empig CJ, Goldsmith MA. Association of the caveola vesicular system with cellular entry by filoviruses. J Virol 2002; 76:5266-70. (Pubitemid 34441729)
13. Yonezawa A, Cavrois M, Greene WC. Studies of Ebola virus glycoprotein- mediated entry and fusion by using pseudotyped human immunodeficiency virus type 1 virions: involvement of cytoskeletal proteins and enhancement by tumor necrosis factor alpha. J Virol 2005; 79:918-26. (Pubitemid 40053875)
14. Bhattacharyya S, Warfield KL, Ruthel G, Bavari S, Aman MJ, Hope TJ. Ebola virus uses clathrin-mediated endocytosis as an entry pathway. Virology 2010; 401:18-28.
15. Sanchez A. Analysis of filovirus entry into vero e6 cells, using inhibitors of endocytosis, endosomal acidification, structural integrity, and cathepsin (B and L) activity. J Infect Dis 2007; 196(Suppl 2):S251-8. (Pubitemid 351417268)
16. Saeed MF, Kolokoltsov AA, Freiberg AN, Holbrook MR, Davey RA. Phosphoinositide-3 kinase-Akt pathway controls cellular entry of Ebola virus. PLoS Pathog 2008; 4:e1000141.
17. Feldmann H, Geisbert TW, Jahrling PB, et al. Filoviridae. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA, eds. Virus taxonomy: VIIIth report of the International Committee on Taxonomy of Viruses. London: Elsevier Academic Press, 2005; 645-53.
18. Richter T, Floetenmeyer M, Ferguson C, et al. High-resolution 3D quantitative analysis of caveolar ultrastructure and caveola-cytoskeleton interactions. Traffic 2008; 9:893-909. (Pubitemid 351639495)
19. Traub LM. Clathrin couture: fashioning distinctive membrane coats at the cell surface. PLoS Biol 2009; 7:e1000192.
20. Noda T, Sagara H, Suzuki E, Takada A, Kida H, Kawaoka Y. Ebola virus VP40 drives the formation of virus-like filamentous particles along with GP. J Virol 2002; 76:4855-65. (Pubitemid 34441691)
21. Wahl-Jensen VM, Afanasieva TA, Seebach J, Stroher U, Feldmann H, Schnittler HJ. Effects of Ebola virus glycoproteins on endothelial cell activation and barrier function. J Virol 2005; 79:10442-50. (Pubitemid 41098584)
22. Hoenen T, Groseth A, Kolesnikova L, et al. Infection of naive target cells with virus-like particles: implications for the function of Ebola virus VP24. J Virol 2006; 80:7260-4. (Pubitemid 44025222)
23. Seebach J, Donnert G, Kronstein R, et al. Regulation of endothelial barrier function during flow-induced conversion to an arterial phenotype. Cardiovasc Res 2007; 75:596-607. (Pubitemid 47080968)
24. Ebihara H, Theriault S, Neumann G, et al. In vitro and in vivo characterization of recombinant Ebola viruses expressing enhanced green fluorescent protein. J Infect Dis 2007; 196(Suppl 2):S313-22. (Pubitemid 351417277)
25. Helenius A, Kartenbeck J, Simons K, Fries E. On the entry of Semliki forest virus into BHK-21 cells. J Cell Biol 1980; 84:404-20. (Pubitemid 10147875)
26. Pelkmans L, Kartenbeck J, Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 2001; 3:473-83. (Pubitemid 32422083)
27. Altschuler Y, Barbas SM, Terlecky LJ, et al. Redundant and distinct functions for dynamin-1 and dynamin-2 isoforms. J Cell Biol 1998; 143:1871-81. (Pubitemid 29022610)
28. Kostic C, Chiodini F, Salmon P, et al. Activity analysis of housekeeping promoters using self-inactivating lentiviral vector delivery into the mouse retina. Gene Ther 2003; 10:818-21. (Pubitemid 36621827)
29. Soulet F, Schmid SL, Damke H. Domain requirements for an endocytosis-independent, isoform-specific function of dynamin-2. Exp Cell Res 2006; 312:3539-45. (Pubitemid 44470774)
30. Schindelin J. Fiji Is Just ImageJ-batteries included. Luxembourg: ImageJ User and Developer Conference, 2008.
31. Kalaidzidis Y. Intracellular objects tracking. Eur J Cell Biol 2007; 86:569-78. (Pubitemid 47233378)
32. Afanasieva TA, Wahl-Jensen V, Seebach J, et al. Hemorrhagic fevers: endothelial cells and Ebola-virus hemorrhagic fever. In: Aird WC, ed. Endothelial biomedicine. New York: Cambridge University Press, 2007; 1311-9.
33. Spector I, Shochet NR, Kashman Y, Groweiss A. Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science 1983; 219:493-5. (Pubitemid 13189272)
34. Vigne P, Frelin C, Cragoe EJ Jr, Lazdunski M. Ethylisopropylamiloride: a new and highly potent derivative of amiloride for the inhibition of the Na1/H1 exchange system in various cell types. Biochem Biophys Res Commun 1983; 116:86-90. (Pubitemid 13023866)
35. Wymann MP, Bulgarelli-Leva G, Zvelebil MJ, et al. Wortmannin inactivates phosphoinositide 3-kinase by covalent modification of Lys- 802, a residue involved in the phosphate transfer reaction. Mol Cell Biol 1996; 16:1722-33. (Pubitemid 26095645)
36. Parton RG. Caveolae meet endosomes: a stable relationship? Dev Cell 2004; 7:458-60. (Pubitemid 39341830)
37. Bavari S, Bosio CM, Wiegand E, et al. Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg viruses. J Exp Med 2002; 195:593-602. (Pubitemid 34461504)
38. Praefcke GJ, McMahon HT. The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 2004; 5:133-47. (Pubitemid 38160256)
39. Schlunck G, Damke H, Kiosses WB, et al. Modulation of Rac localization and function by dynamin. Mol Biol Cell 2004; 15:256-67. (Pubitemid 38044961)
40. Bonazzi M, Spano S, Turacchio G, et al. CtBP3/BARS drives membrane fission in dynamin-independent transport pathways. Nat Cell Biol 2005; 7:570-80. (Pubitemid 40796980)
41. Lindemann D, Schnittler H. Genetic manipulation of endothelial cells by viral vectors. Thromb Haemost 2009; 102:1135-43.
42. Le Roy C, Wrana JL. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 2005; 6:112-26. (Pubitemid 40215807)
43. Marsh M, Helenius A. Virus entry: open sesame. Cell 2006; 124:729-40. (Pubitemid 43261448)
44. Nanbo A, Imai M,Watanabe S, et al. Ebolavirus is internalized into host cells via macropinocytosis in a viral glycoprotein-dependent manner. PLoS Pathog 2010; 6:e1001121.
45. Saeed MF, Kolokoltsov AA, Albrecht T, Davey RA. Cellular entry of Ebola virus involves uptake by a macropinocytosis-like mechanism and subsequent trafficking through early and late endosomes. PLoS Pathog 2010; 6:e1001110.
46. Schnittler HJ, Schneider SW, Raifer H, et al. Role of actin filaments in endothelial cell-cell adhesion and membrane stability under fluid shear stress. Pflugers Arch 2001; 442:675-87. (Pubitemid 32783676)
47. Wahl-Jensen V, Kurz SK, Hazelton PR, et al. Role of Ebola virus secreted glycoproteins and virus-like particles in activation of human macrophages. J Virol 2005; 79:2413-9. (Pubitemid 40204596)
48. Saffarian S, Cocucci E, Kirchhausen T. Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol 2009; 7:e1000191.
49. Cossart P, Veiga E. Non-classical use of clathrin during bacterial infections. J Microsc 2008; 231:524-8.
50. Sieczkarski SB, Whittaker GR. Dissecting virus entry via endocytosis. J Gen Virol 2002; 83:1535-45. (Pubitemid 34721298)
51. Vercauteren D, Vandenbroucke RE, Jones AT, et al. The use of inhibitors to study endocytic pathways of gene carriers: optimization and pitfalls. Mol Ther 2010; 18:561-9. Ebola