Vaccinia Virus Infection Requires Maturation of Macropinosomes

Traffic

Volumn 16, Issue 8, 2015, Pages 814-831

  Rizopoulos, Zaira ^a   Balistreri, Giuseppe ^a   Kilcher, Samuel ^b   Martin, Caroline K ^b   Syedbasha, Mohammedyaseen ^a   Helenius, Ari ^a   Mercer, Jason ^b  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Endocytosis; Macropinocytosis; Phosphoinositide exchange; PIKfyve; Poxvirus; Rab conversion; Virus entry

Indexed keywords

EARLY ENDOSOME ANTIGEN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PHOSPHATIDYLINOSITOL 3 KINASE; RAB PROTEIN; RAB7 PROTEIN; SORTING NEXIN; SORTING NEXIN 3; UNCLASSIFIED DRUG;

ARTICLE; BLUE LIGHT; CELL MATURATION; CELL VACUOLE; CONFOCAL MICROSCOPY; CYTOPLASM; ENDOSOME; FEMALE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; LYSOSOME; MACROPINOSOME; PINOCYTOSIS; PRIORITY JOURNAL; VACCINIA VIRUS INFECTION; VIRION; VIRUS CORE; VIRUS ENTRY; VIRUS INFECTION; GENETICS; HELA CELL LINE; METABOLISM; PATHOGENICITY; PHAGOCYTOSIS; PHAGOSOME; VACCINIA VIRUS; VIROLOGY;

ENDOSOMES; HELA CELLS; HUMANS; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; PHAGOCYTOSIS; PHAGOSOMES; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; SORTING NEXINS; VACCINIA VIRUS;

EID: 84937191859     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12290     Document Type: Article

References (76)

1. Marsh M, Helenius A. Virus entry: open sesame. Cell 2006;124:729-740.
2. Mercer J, Schelhaas M, Helenius A. Virus entry by endocytosis. Annu Rev Biochem 2010;79:803-833.
3. Huotari J, Helenius A. Endosome maturation. EMBO J 2011;30:3481-3500.
4. Scott CC, Vacca F, Gruenberg J. Endosome maturation, transport and functions. Semin Cell Dev Biol 2014;31:2-10.
5. Poteryaev D, Datta S, Ackema K, Zerial M, Spang A. Identification of the switch in early-to-late endosome transition. Cell 2010;141:497-508.
6. Solinger JA, Spang A. Tethering complexes in the endocytic pathway: CORVET and HOPS. FEBS J 2013;280:2743-2757.
7. Woodman PG. Biogenesis of the sorting endosome: the role of Rab5. Traffic 2000;1:695-701.
8. Jovic M, Sharma M, Rahajeng J, Caplan S. The early endosome: a busy sorting station for proteins at the crossroads. Histol Histopathol 2010;25:99-112.
9. Gillooly DJ, Morrow IC, Lindsay M, Gould R, Bryant NJ, Gaullier JM, Parton RG, Stenmark H. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J 2000;19:4577-4588.
10. Odorizzi G, Babst M, Emr SD. Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 1998;95:847-858.
11. Maxfield FR, Yamashiro DJ. Endosome acidification and the pathways of receptor-mediated endocytosis. Adv Exp Med Biol 1987;225:189-198.
12. Pasqual G, Rojek JM, Masin M, Chatton JY, Kunz S. Old world arenaviruses enter the host cell via the multivesicular body and depend on the endosomal sorting complex required for transport. PLoS Pathog 2011;7:e1002232.
13. Lozach PY, Mancini R, Bitto D, Meier R, Oestereich L, Overby AK, Pettersson RF, Helenius A. Entry of bunyaviruses into mammalian cells. Cell Host Microbe 2010;7:488-499.
14. Lozach PY, Huotari J, Helenius A. Late-penetrating viruses. Curr Opin Virol 2011;1:35-43.
15. Mercer J, Helenius A. Virus entry by macropinocytosis. Nat Cell Biol 2009;11:510-520.
16. Swanson JA. Shaping cups into phagosomes and macropinosomes. Nat Rev Mol Cell Biol 2008;9:639-649.
17. Feliciano WD, Yoshida S, Straight SW, Swanson JA. Coordination of the Rab5 cycle on macropinosomes. Traffic 2011;12:1911-1922.
18. Schnatwinkel C, Christoforidis S, Lindsay MR, Uttenweiler-Joseph S, Wilm M, Parton RG, Zerial M. The Rab5 effector Rabankyrin-5 regulates and coordinates different endocytic mechanisms. PLoS Biol 2004;2:E261.
19. Sun P, Yamamoto H, Suetsugu S, Miki H, Takenawa T, Endo T. Small GTPase Rah/Rab34 is associated with membrane ruffles and macropinosomes and promotes macropinosome formation. J Biol Chem 2003;278:4063-4071.
20. Hamasaki M, Araki N, Hatae T. Association of early endosomal autoantigen 1 with macropinocytosis in EGF-stimulated A431 cells. Anat Rec 2004;277:298-306.
21. Bryant DM, Kerr MC, Hammond LA, Joseph SR, Mostov KE, Teasdale RD, Stow JL. EGF induces macropinocytosis and SNX1-modulated recycling of E-cadherin. J Cell Sci 2007;120:1818-1828.
22. Kerr MC, Lindsay MR, Luetterforst R, Hamilton N, Simpson F, Parton RG, Gleeson PA, Teasdale RD. Visualisation of macropinosome maturation by the recruitment of sorting nexins. J Cell Sci 2006;119:3967-3980.
23. Lim JP, Wang JT, Kerr MC, Teasdale RD, Gleeson PA. A role for SNX5 in the regulation of macropinocytosis. BMC Cell Biol 2008;9:58.
24. Merino-Trigo A, Kerr MC, Houghton F, Lindberg A, Mitchell C, Teasdale RD, Gleeson PA. Sorting nexin 5 is localized to a subdomain of the early endosomes and is recruited to the plasma membrane following EGF stimulation. J Cell Sci 2004;117:6413-6424.
25. Braun V, Wong A, Landekic M, Hong WJ, Grinstein S, Brumell JH. Sorting nexin 3 (SNX3) is a component of a tubular endosomal network induced by Salmonella and involved in maturation of the Salmonella-containing vacuole. Cell Microbiol 2010;12:1352-1367.
26. Racoosin EL, Swanson JA. Macropinosome maturation and fusion with tubular lysosomes in macrophages. J Cell Biol 1993;121:1011-1020.
27. Egami Y, Araki N. Dynamic changes in the spatiotemporal localization of Rab21 in live RAW264 cells during macropinocytosis. PLoS One 2009;4:e6689.
28. Hewlett LJ, Prescott AR, Watts C. The coated pit and macropinocytic pathways serve distinct endosome populations. J Cell Biol 1994;124:689-703.
29. West MA, Bretscher MS, Watts C. Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J Cell Biol 1989;109:2731-2739.
30. Kerr MC, Wang JT, Castro NA, Hamilton NA, Town L, Brown DL, Meunier FA, Brown NF, Stow JL, Teasdale RD. Inhibition of the PtdIns(5) kinase PIKfyve disrupts intracellular replication of Salmonella. EMBO J 2010;29:1331-1347.
31. Mercer J, Helenius A. Gulping rather than sipping: macropinocytosis as a way of virus entry. Curr Opin Microbiol 2012;15:490-499.
32. Moss B. Poxviridae: the viruses and their replication. In: Knipe DM, Howley PM, editors. Fields Virology. Philadelphia: Lippincott-Raven; 2013, pp. 2129-2159.
33. Mercer J, Knebel S, Schmidt FI, Crouse J, Burkard C, Helenius A. Vaccinia virus strains use distinct forms of macropinocytosis for host-cell entry. Proc Natl Acad Sci U S A 2010;107:9346-9351.
34. Mercer J, Helenius A. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 2008;320:531-535.
35. Schmidt FI, Bleck CK, Helenius A, Mercer J. Vaccinia extracellular virions enter cells by macropinocytosis and acid-activated membrane rupture. EMBO J 2011;30:3647-3661.
36. Schmidt FI, Bleck CK, Mercer J. Poxvirus host cell entry. Curr Opin Virol 2012;2:20-27.
37. Sandgren KJ, Wilkinson J, Miranda-Saksena M, McInerney GM, Byth-Wilson K, Robinson PJ, Cunningham AL. A differential role for macropinocytosis in mediating entry of the two forms of vaccinia virus into dendritic cells. PLoS Pathog 2010;6:e1000866.
38. Huang CY, Lu TY, Bair CH, Chang YS, Jwo JK, Chang W. A novel cellular protein, VPEF, facilitates vaccinia virus penetration into HeLa cells through fluid phase endocytosis. J Virol 2008;82:7988-7999.
39. Locker JK, Kuehn A, Schleich S, Rutter G, Hohenberg H, Wepf R, Griffiths G. Entry of the two infectious forms of vaccinia virus at the plasma membrane is signaling-dependent for the IMV but not the EEV. Mol Biol Cell 2000;11:2497-2511.
40. Kilcher S, Schmidt FI, Schneider C, Kopf M, Helenius A, Mercer J. siRNA screen of early poxvirus genes identifies the AAA+ ATPase D5 as the virus genome-uncoating factor. Cell Host Microbe 2014;15:103-112.
41. Dales S. The uptake and development of vaccinia virus in strain L cells followed with labeled viral deoxyribonucleic acid. J Cell Biol 1963;18:51-72.
42. Mercer J, Snijder B, Sacher R, Burkard C, Bleck CK, Stahlberg H, Pelkmans L, Helenius A. RNAi screening reveals proteasome- and Cullin3-dependent stages in vaccinia virus infection. Cell Rep 2012;2:1036-1047.
43. Miaczynska M, Christoforidis S, Giner A, Shevchenko A, Uttenweiler-Joseph S, Habermann B, Wilm M, Parton RG, Zerial M. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 2004;116:445-456.
44. Bengali Z, Townsley AC, Moss B. Vaccinia virus strain differences in cell attachment and entry. Virology 2009;389:132-140.
45. Townsley AC, Moss B. Two distinct low-pH steps promote entry of vaccinia virus. J Virol 2007;81:8613-8620.
46. Townsley AC, Weisberg AS, Wagenaar TR, Moss B. Vaccinia virus entry into cells via a low-pH-dependent endosomal pathway. J Virol 2006;80:8899-8908.
47. Whitbeck JC, Foo CH, Ponce de Leon M, Eisenberg RJ, Cohen GH. Vaccinia virus exhibits cell-type-dependent entry characteristics. Virology 2009;385:383-391.
48. Engel S, Heger T, Mancini R, Herzog F, Kartenbeck J, Hayer A, Helenius A. Role of endosomes in simian virus 40 entry and infection. J Virol 2011;85:4198-4211.
49. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, Doerks T, Stark M, Muller J, Bork P, Jensen LJ, von Mering C. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 2011;39:D561-D568.
50. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009;4:44-57.
51. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Baseler MW, Lane HC, Lempicki RA. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 2003;4:3.
52. Yoshida S, Hoppe AD, Araki N, Swanson JA. Sequential signaling in plasma-membrane domains during macropinosome formation in macrophages. J Cell Sci 2009;122:3250-3261.
53. Zoncu R, Perera RM, Balkin DM, Pirruccello M, Toomre D, De Camilli P. A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 2009;136:1110-1121.
54. de Lartigue J, Polson H, Feldman M, Shokat K, Tooze SA, Urbe S, Clague MJ. PIKfyve regulation of endosome-linked pathways. Traffic 2009;10:883-893.
55. Schmidt FI, Bleck CK, Reh L, Novy K, Wollscheid B, Helenius A, Stahlberg H, Mercer J. Vaccinia virus entry is followed by core activation and proteasome-mediated release of the immunomodulatory effector VH1 from lateral bodies. Cell Rep 2013;4:464-476.
56. Smith GL, Vanderplasschen A, Law M. The formation and function of extracellular enveloped vaccinia virus. J Gen Virol 2002;83:2915-2931.
57. Perini ED, Schaefer R, Stoter M, Kalaidzidis Y, Zerial M. Mammalian CORVET is required for fusion and conversion of distinct early endosome subpopulations. Traffic 2014;15:1366-1389.
58. Bogdanovic A, Bennett N, Kieffer S, Louwagie M, Morio T, Garin J, Satre M, Bruckert F. Syntaxin 7, syntaxin 8, Vti1 and VAMP7 (vesicle-associated membrane protein 7) form an active SNARE complex for early macropinocytic compartment fusion in Dictyostelium discoideum. Biochem J 2002;368:29-39.
59. Xu Y, Hortsman H, Seet L, Wong SH, Hong W. SNX3 regulates endosomal function through its PX-domain-mediated interaction with PtdIns(3)P. Nat Cell Biol 2001;3:658-666.
60. Humphries WHt, Szymanski CJ, Payne CK. Endo-lysosomal vesicles positive for Rab7 and LAMP1 are terminal vesicles for the transport of dextran. PLoS One 2011;6:e26626.
61. Schmidt FI, Kuhn P, Robinson T, Mercer J, Dittrich PS. Single-virus fusion experiments reveal proton influx into vaccinia virions and hemifusion lag times. Biophys J 2013;105:420-431.
62. Laliberte JP, Weisberg AS, Moss B. The membrane fusion step of vaccinia virus entry is cooperatively mediated by multiple viral proteins and host cell components. PLoS Pathog 2011;7:e1002446.
63. Pankiv S, Alemu EA, Brech A, Bruun JA, Lamark T, Overvatn A, Bjorkoy G, Johansen T. FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J Cell Biol 2010;188:253-269.
64. Wang T, Ming Z, Xiaochun W, Hong W. Rab7: role of its protein interaction cascades in endo-lysosomal traffic. Cell Signal 2011;23:516-521.
65. Wang T, Hong W. Interorganellar regulation of lysosome positioning by the Golgi apparatus through Rab34 interaction with Rab-interacting lysosomal protein. Mol Biol Cell 2002;13:4317-4332.
66. Kruth HS, Jones NL, Huang W, Zhao B, Ishii I, Chang J, Combs CA, Malide D, Zhang WY. Macropinocytosis is the endocytic pathway that mediates macrophage foam cell formation with native low density lipoprotein. J Biol Chem 2005;280:2352-2360.
67. Levin R, Grinstein S, Schlam D. Phosphoinositides in phagocytosis and macropinocytosis. Biochim Biophys Acta 2015;1851:805-823.
68. Soares JA, Leite FG, Andrade LG, Torres AA, De Sousa LP, Barcelos LS, Teixeira MM, Ferreira PC, Kroon EG, Souto-Padron T, Bonjardim CA. Activation of the PI3K/Akt pathway early during vaccinia and cowpox virus infections is required for both host survival and viral replication. J Virol 2009;83:6883-6899.
69. McNulty S, Bornmann W, Schriewer J, Werner C, Smith SK, Olson VA, Damon IK, Buller RM, Heuser J, Kalman D. Multiple phosphatidylinositol 3-kinases regulate vaccinia virus morphogenesis. PLoS One 2010;5:e10884.
70. Izmailyan R, Hsao JC, Chung CS, Chen CH, Hsu PW, Liao CL, Chang W. Integrin beta1 mediates vaccinia virus entry through activation of PI3K/Akt signaling. J Virol 2012;86:6677-6687.
71. Hiley CT, Chard LS, Gangeswaran R, Tysome JR, Briat A, Lemoine NR, Wang Y. Vascular endothelial growth factor A promotes vaccinia virus entry into host cells via activation of the Akt pathway. J Virol 2013;87:2781-2790.
72. Er EE, Mendoza MC, Mackey AM, Rameh LE, Blenis J. AKT facilitates EGFR trafficking and degradation by phosphorylating and activating PIKfyve. Sci Signal 2013;6:ra45.
73. Moss B. Poxvirus cell entry: how many proteins does it take? Viruses 2012;4:688-707.
74. Fairn GD, Grinstein S. How nascent phagosomes mature to become phagolysosomes. Trends Immunol 2012;33:397-405.
75. Hyttinen JM, Niittykoski M, Salminen A, Kaarniranta K. Maturation of autophagosomes and endosomes: a key role for Rab7. Biochim Biophys Acta 2013;1833:503-510.
76. Pelkmans L, Burli T, Zerial M, Helenius A. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 2004;118:767-780.