The Ebola virus glycoprotein mediates entry via a non-classical dynamin-dependent macropinocytic pathway

Virology

Volumn 419, Issue 2, 2011, Pages 72-83

  Mulherkar, Nirupama ^a   Raaben, Matthijs ^b   de la Torre, Juan Carlos ^c   Whelan, Sean P ^b   Chandran, Kartik ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Antigen presenting cells; Dendritic cells; Dynamin; Ebola virus; Endocytosis; Filovirus; Glycoprotein; Macropinocytosis; Monocytes; Pak 1; Vesicular stomatitis virus; Viral entry; Viral infection; Virus like particles

Indexed keywords

DYNAMIN II; MUCIN; VIRUS GLYCOPROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL SURFACE; CONTROLLED STUDY; DENDRITIC CELL; EBOLA VIRUS; ELECTRON MICROSCOPY; GENETIC SCREENING; HOST CELL; HUMAN; HUMAN CELL; MONOCYTE; MOUSE; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION; PROTEIN INTERACTION; VERO CELL; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS PARTICLE;

ACTINS; AMILORIDE; ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; DENDRITIC CELLS; DYNAMIN II; EBOLAVIRUS; HUMANS; HYDRAZONES; MICE; MICROSCOPY, ELECTRON; PINOCYTOSIS; VERO CELLS; VESICULOVIRUS; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

EBOLA VIRUS; MARBURGVIRUS; VESICULAR STOMATITIS VIRUS;

EID: 80052942161     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.08.009     Document Type: Article

References (49)

1. Alvarez C.P., Lasala F., Carrillo J., Muniz O., Corbi A.L., Delgado R. C-type lectins DC-SIGN and L-SIGN mediate cellular entry by Ebola virus in cis and in trans. J. Virol. 2002, 76:6841-6844.
2. Arii J., Goto H., Suenaga T., Oyama M., Kozuka-Hata H., Imai T., Minowa A., Akashi H., Arase H., Kawaoka Y., Kawaguchi Y. Non-muscle myosin IIA is a functional entry receptor for herpes simplex virus-1. Nature 2010, 467:859-862.
3. Ascenzi P., Bocedi A., Heptonstall J., Capobianchi M.R., Di Caro A., Mastrangelo E., Bolognesi M., Ippolito G. Ebolavirus and Marburgvirus: insight the Filoviridae family. Mol. Aspects Med. 2008, 29:151-185.
4. Bhattacharyya S., Warfield K.L., Ruthel G., Bavari S., Aman M.J., Hope T.J. Ebola virus uses clathrin-mediated endocytosis as an entry pathway. Virology 2010, 401:18-28.
5. Bray M., Geisbert T.W. Ebola virus: the role of macrophages and dendritic cells in the pathogenesis of Ebola hemorrhagic fever. Int. J. Biochem. Cell Biol. 2005, 37:1560-1566.
6. Brindley M.A., Hunt C.L., Kondratowicz A.S., Bowman J., Sinn P.L., McCray P.B., Quinn K., Weller M.L., Chiorini J.A., Maury W. Tyrosine kinase receptor Axl enhances entry of Zaire ebolavirus without direct interactions with the viral glycoprotein. Virology 2011, 415:83-94.
7. Carter G.C., Bernstone L., Baskaran D., James W. HIV-1 infects macrophages by exploiting an endocytic route dependent on dynamin, Rac1 and Pak1. Virology 2011, 409:234-250.
8. Chan S.Y., Empig C.J., Welte F.J., Speck R.F., Schmaljohn A., Kreisberg J.F., Goldsmith M.A. Folate receptor-alpha is a cofactor for cellular entry by Marburg and Ebola viruses. Cell 2001, 106:117-126.
9. Chandran K., Sullivan N.J., Felbor U., Whelan S.P., Cunningham J.M. Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 2005, 308:1643-1645.
10. Conner S.D., Schmid S.L. Regulated portals of entry into the cell. Nature 2003, 422:37-44.
11. Donaldson J.G. Multiple roles for Arf6: sorting, structuring, and signaling at the plasma membrane. J. Biol. Chem. 2003, 278:41573-41576.
12. Feldmann H., Geisbert T., Kawaoka Y. Filoviruses: recent advances and future challenges. J. Infect. Dis. 2007, 196(Suppl. 2):S129-S130.
13. Geisbert T.W., Hensley L.E., Larsen T., Young H.A., Reed D.S., Geisbert J.B., Scott D.P., Kagan E., Jahrling P.B., Davis K.J. Pathogenesis of Ebola hemorrhagic fever in cynomolgus macaques: evidence that dendritic cells are early and sustained targets of infection. Am. J. Pathol. 2003, 163:2347-2370.
14. Heinrich B.S., Cureton D.K., Rahmeh A.A., Whelan S.P. Protein expression redirects vesicular stomatitis virus RNA synthesis to cytoplasmic inclusions. PLoS Pathog. 2010, 6:e1000958.
15. Hewlett L.J., Prescott A.R., Watts C. The coated pit and macropinocytic pathways serve distinct endosome populations. J. Cell Biol. 1994, 124:689-703.
16. Hunt C.L., Kolokoltsov A.A., Davey R.A., Maury W. The Tyro3 receptor kinase Axl enhances macropinocytosis of Zaire ebolavirus. J. Virol. 2011, 85:334-347.
17. Ji X., Olinger G.G., Aris S., Chen Y., Gewurz H., Spear G.T. Mannose-binding lectin binds to Ebola and Marburg envelope glycoproteins, resulting in blocking of virus interaction with DC-SIGN and complement-mediated virus neutralization. J. Gen. Virol. 2005, 86:2535-2542.
18. Kirchhausen T., Macia E., Pelish H.E. Use of dynasore, the small molecule inhibitor of dynamin, in the regulation of endocytosis. Methods Enzymol. 2008, 438:77-93.
19. Koivusalo M., Welch C., Hayashi H., Scott C.C., Kim M., Alexander T., Touret N., Hahn K.M., Grinstein S. Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J. Cell Biol. 2010, 188:547-563.
20. Kondratowicz A.S., Lennemann N.J., Sinn P.L., Davey R.A., Hunt C.L., Moller-Tank S., Meyerholz D.K., Rennert P., Mullins R.F., Brindley M., Sandersfeld L.M., Quinn K., Weller M., McCray P.B., Chiorini J., Maury W. T-cell immunoglobulin and mucin domain 1 (TIM-1) is a receptor for Zaire Ebolavirus and Lake Victoria Marburgvirus. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:8426-8431.
21. Kuhn J.H. Filoviruses. A compendium of 40years of epidemiological, clinical, and laboratory studies. Arch. Virol. Suppl. 2008, 20:13-360.
22. Kuhn J.H., Becker S., Ebihara H., Geisbert T.W., Johnson K.M., Kawaoka Y., Lipkin W.I., Negredo A.I., Netesov S.V., Nichol S.T., Palacios G., Peters C.J., Tenorio A., Volchkov V.E., Jahrling P.B. Proposal for a revised taxonomy of the family Filoviridae: classification, names of taxa and viruses, and virus abbreviations. Arch. Virol. 2010, 155:2083-2103.
23. Lee J.E., Saphire E.O. Neutralizing ebolavirus: structural insights into the envelope glycoprotein and antibodies targeted against it. Curr. Opin. Struct. Biol. 2009, 19:408-417.
24. Lee J.E., Fusco M.L., Hessell A.J., Oswald W.B., Burton D.R., Saphire E.O. Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 2008, 454:177-182.
25. Liberali P., Kakkonen E., Turacchio G., Valente C., Spaar A., Perinetti G., Bockmann R.A., Corda D., Colanzi A., Marjomaki V., Luini A. The closure of Pak1-dependent macropinosomes requires the phosphorylation of CtBP1/BARS. EMBO J. 2008, 27:970-981.
26. Lin G., Simmons G., Pohlmann S., Baribaud F., Ni H., Leslie G.J., Haggarty B.S., Bates P., Weissman D., Hoxie J.A., Doms R.W. Differential N-linked glycosylation of human immunodeficiency virus and Ebola virus envelope glycoproteins modulates interactions with DC-SIGN and DC-SIGNR. J. Virol. 2003, 77:1337-1346.
27. Liu Y.W., Surka M.C., Schroeter T., Lukiyanchuk V., Schmid S.L. Isoform and splice-variant specific functions of dynamin-2 revealed by analysis of conditional knock-out cells. Mol. Biol. Cell 2008, 19:5347-5359.
28. Martinez O., Johnson J., Manicassamy B., Rong L., Olinger G.G., Hensley L.E., Basler C.F. Zaire Ebola virus entry into human dendritic cells is insensitive to cathepsin L inhibition. Cell. Microbiol. 2010, 12:148-157.
29. Martin-Serrano J., Perez-Caballero D., Bieniasz P.D. Context-dependent effects of L domains and ubiquitination on viral budding. J. Virol. 2004, 78:5554-5563.
30. Mercer J., Helenius A. Virus entry by macropinocytosis. Nat. Cell Biol. 2009, 11:510-520.
31. Mercer J., Schelhaas M., Helenius A. Virus entry by endocytosis. Annu. Rev. Biochem. 2010, 79:803-833.
32. Nanbo A., Imai M., Watanabe S., Noda T., Takahashi K., Neumann G., Halfmann P., Kawaoka Y. Ebolavirus is internalized into host cells via macropinocytosis in a viral glycoprotein-dependent manner. PLoS Pathog. 2010, 6.
33. Ohtsubo K., Marth J.D. Glycosylation in cellular mechanisms of health and disease. Cell 2006, 126:855-867.
34. Quinn K., Brindley M.A., Weller M.L., Kaludov N., Kondratowicz A., Hunt C.L., Sinn P.L., McCray P.B., Stein C.S., Davidson B.L., Flick R., Mandell R., Staplin W., Maury W., Chiorini J.A. Rho GTPases modulate entry of Ebola virus and vesicular stomatitis virus pseudotyped vectors. J. Virol. 2009, 83:10176-10186.
35. Quirin K., Eschli B., Scheu I., Poort L., Kartenbeck J., Helenius A. Lymphocytic choriomeningitis virus uses a novel endocytic pathway for infectious entry via late endosomes. Virology 2008, 378:21-33.
36. Saeed M.F., Kolokoltsov A.A., Albrecht T., Davey R.A. Cellular entry of Ebola virus involves uptake by a macropinocytosis-like mechanism and subsequent trafficking through early and late endosomes. PLoS Pathog. 2010, 6.
37. 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-S258.
38. Schlunck G., Damke H., Kiosses W.B., Rusk N., Symons M.H., Waterman-Storer C.M., Schmid S.L., Schwartz M.A. Modulation of Rac localization and function by dynamin. Mol. Biol. Cell 2004, 15:256-267.
39. Schornberg K., Matsuyama S., Kabsch K., Delos S., Bouton A., White J. Role of endosomal cathepsins in entry mediated by the Ebola virus glycoprotein. J. Virol. 2006, 80:4174-4178.
40. Simmons G., Wool-Lewis R.J., Baribaud F., Netter R.C., Bates P. Ebola virus glycoproteins induce global surface protein down-modulation and loss of cell adherence. J. Virol. 2002, 76:2518-2528.
41. Simmons G., Reeves J.D., Grogan C.C., Vandenberghe L.H., Baribaud F., Whitbeck J.C., Burke E., Buchmeier M.J., Soilleux E.J., Riley J.L., Doms R.W., Bates P., Pohlmann S. DC-SIGN and DC-SIGNR bind ebola glycoproteins and enhance infection of macrophages and endothelial cells. Virology 2003, 305:115-123.
42. Simmons G., Rennekamp A.J., Chai N., Vandenberghe L.H., Riley J.L., Bates P. Folate receptor alpha and caveolae are not required for Ebola virus glycoprotein-mediated viral infection. J. Virol. 2003, 77:13433-13438.
43. Takada A., Robison C., Goto H., Sanchez A., Murti K.G., Whitt M.A., Kawaoka Y. A system for functional analysis of Ebola virus glycoprotein. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:14764-14769.
44. 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, 278:20-26.
45. Takada A., Fujioka K., Tsuiji M., Morikawa A., Higashi N., Ebihara H., Kobasa D., Feldmann H., Irimura T., Kawaoka Y. Human macrophage C-type lectin specific for galactose and N-acetylgalactosamine promotes filovirus entry. J. Virol. 2004, 78:2943-2947.
46. Wilson J.A., Hevey M., Bakken R., Guest S., Bray M., Schmaljohn A.L., Hart M.K. Epitopes involved in antibody-mediated protection from Ebola virus. Science 2000, 287:1664-1666.
47. Wong A.C., Sandesara R.G., Mulherkar N., Whelan S.P., Chandran K. A forward genetic strategy reveals destabilizing mutations in the Ebolavirus glycoprotein that alter its protease dependence during cell entry. J. Virol. 2010, 84:163-175.
48. Wool-Lewis R.J., Bates P. Characterization of Ebola virus entry by using pseudotyped viruses: identification of receptor-deficient cell lines. J. Virol. 1998, 72:3155-3160.
49. Yonezawa A., Cavrois M., Greene W.C. 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, 79:918-926.