Coxsackievirus A9 infects cells via nonacidic multivesicular bodies

Journal of Virology

Volumn 88, Issue 9, 2014, Pages 5138-5151

  Huttunen, Moona ^a   Waris, Matti ^b   Kajander, Ritva ^b   Hyypiä, Timo ^b   Marjomäki, Varpu ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; EARLY ENDOSOME ANTIGEN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PHOSPHOLIPASE C; RAB7 PROTEIN; RAC1 PROTEIN; SODIUM PROTON EXCHANGE PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; VPS4 PROTEIN;

ARTICLE; BIOACCUMULATION; BIOGENESIS; CELL ASSAY; CELL LABELING; CONTROLLED STUDY; COXSACKIE VIRUS A; COXSACKIE VIRUS INFECTION; COXSACKIEVIRUS A9; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; INTERNALIZATION; LYSOSOME; MULTIVESICULAR BODY; PH; PRIORITY JOURNAL; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS REPLICATION;

CELL LINE; ENTEROVIRUS B, HUMAN; EPITHELIAL CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; MICROSCOPY, ELECTRON; MULTIVESICULAR BODIES; VIRUS INTERNALIZATION;

EID: 84897551437     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03275-13     Document Type: Article

References (52)

1. Hyypiä T, Hovi T, Knowles NJ, Stanway G. 1997. Classification of enteroviruses based on molecular and biological properties. J. Gen. Virol. 78:1-11.
2. Chang KH, Auvinen P, Hyypiä T, Stanway G. 1989. The nucleotide sequence of coxsackievirus A9; implications for receptor binding and enterovirus classification. J. Gen. Virol. 70:3269-3280.
3. Nelsen-Salz B, Eggers HJ, Zimmermann H. 1999. Integrin αvβ3 (vitronectin receptor) is a candidate receptor for the virulent echovirus 9 strain Barty. J. Gen. Virol. 80:2311-2313.
4. Heikkilä O, Susi P, Stanway G, Hyypiä T. 2009. Integrin αVβ 6 is a high-affinity receptor for coxsackievirus A9. J. Gen. Virol. 90:197-204. http://dx.doi.org/10.1099/vir.0.004838-0.
5. Roivainen M, Piirainen L, Hovi T, Virtanen I, Riikonen T, Heino J, Hyypiä T. 1994. Entry of coxsackievirus A9 into host cells: specific interactions with alpha v beta 3 integrin, the vitronectin receptor. Virology 203:357-365. http://dx.doi.org/10.1006/viro.1994.1494.
6. Williams CH, Kajander T, Hyypiä T, Jackson T, Sheppard D, Stanway G. 2004. Integrin alpha v beta 6 is an RGD-dependent receptor for coxsackievirus A9. J. Virol. 78:6967-6973. http://dx.doi.org/10.1128/JVI.78.13.6967-6973.2004.
7. Triantafilou K, Fradelizi D, Wilson K, Triantafilou M. 2002. GRP78, a coreceptor for coxsackievirus A9, interacts with major histocompatibility complex class I molecules which mediate virus internalization. J. Virol. 76:633-643. http://dx.doi.org/10.1128/JVI.76.2.633-643.2002.
8. Triantafilou M, Triantafilou K, Wilson KM, Takada Y, Fernandez N, Stanway G. 1999. Involvement of β2-microglobulin and integrin αvβ 3 molecules in the coxsackievirus A9 infectious cycle. J. Gen. Virol. 80:2591-2600.
9. Marjomäki V, Pietiäinen V, Matilainen H, Upla P, Ivaska J, Nissinen L, Reunanen H, Huttunen P, Hyypiä T, Heino J. 2002. Internalization of echovirus 1 in caveolae. J. Virol. 76:1856-1865. http://dx.doi.org/10.1128/JVI.76.4.1856-1865.2002.
10. Mercer J, Schelhaas M, Helenius A. 2010. Virus entry by endocytosis. Annu. Rev. Biochem. 79:803-833. http://dx.doi.org/10.1146/annurev-biochem-060208-104626.
11. Fuchs R, Blaas D. 2010. Uncoating of human rhinoviruses. Rev. Med. Virol. 20:281-297. http://dx.doi.org/10.1002/rmv.654.
12. Scott CC, Gruenberg J. 2011. Ion flux and the function of endosomes and lysosomes. pH is just the start: the flux of ions across endosomal membranes influences endosome function not only through regulation of the luminal pH. Bioessays 33:103-110. http://dx.doi.org/10.1002/bies.201000108.
13. Heikkilä O, Susi P, Tevaluoto T, Härmä H, Marjomäki V, Hyypiä T, Kiljunen S. 2010. Internalization of coxsackievirus A9 is mediated by +2-microglobulin, dynamin, and Arf6 but not by caveolin-1 or clathrin. J. Virol. 84:3666-3681. http://dx.doi.org/10.1128/JVI.01340-09.
14. Shakeel S, Seitsonen JJ, Kajander T, Laurinmäki P, Hyypiä T, Susi P, Butcher SJ. 2013. Structural and functional analysis of coxsackievirus A9 integrin αvβ 6 binding and uncoating. J. Virol. 87:3943-3951. http://dx.doi.org/10.1128/JVI.02989-12.
15. Karjalainen M, Rintanen N, Lehkonen M, Kallio K, Mäki A, Hellström K, Siljamäki V, Upla P, Marjomäki V. 2011. Echovirus 1 infection depends on biogenesis of novel multivesicular bodies. Cell. Microbiol. 13:1975-1995. http://dx.doi.org/10.1111/j.1462-5822.2011.01685.x.
16. Rintanen N, Karjalainen M, Alanko J, Paavolainen L, Mäki A, Nissinen L, Lehkonen M, Kallio K, Cheng RH, Upla P, Ivaska J, Marjomäki V. 2012. Calpains promote α2β1 integrin turnover in nonrecycling integrin pathway. Mol. Biol. Cell 23:448-463. http://dx.doi.org/10.1091/mbc.E11-06-0548.
17. Hanson PI, Cashikar A. 2012. Multivesicular body morphogenesis. Annu. Rev. Cell Dev. Biol. 28:337-362. http://dx.doi.org/10.1146/annurev-cellbio-092910-154152.
18. Matsuo H, Chevallier J, Mayran N, Le Blanc I, Ferguson C, Faure J, Blanc NS, Matile S, Dubochet J, Sadoul R, Parton RG, Vilbois F, Gruenberg J. 2004. Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science 303:531-534. http://dx.doi.org/10.1126/science.1092425.
19. Hendry E, Hatanaka H, Fry E, Smyth M, Tate J, Stanway G, Santti J, Maaronen M, Hyypiä T, Stuart D. 1999. The crystal structure of coxsackievirus A9: new insights into the uncoating mechanisms of enteroviruses. Structure. 7:1527-1538.
20. Abraham G, Colonno RJ. 1984. Many rhinovirus serotypes share the same cellular receptor. J. Virol. 51:340-345.
21. Pulli T, Roivainen M, Hovi T, Hyypiä T. 1998. Induction of neutralizing antibodies by synthetic peptides representing the C terminus of coxsackievirus A9 capsid protein VP1. J. Gen. Virol. 79:2249-2253.
22. Buttinelli G, Donati V, Ruggeri FM, Joki-Korpela P, Hyypiä T, Fiore L. 2003. Antigenic sites of coxsackie A9 virus inducing neutralizing monoclonal antibodies protective in mice. Virology 312:74-83. http://dx.doi.org/10.1016/S0042-6822(03)00182-X.
23. Upla P, Marjomäki V, Nissinen L, Nylund C, Waris M, Hyypiä T, Heino J. 2008. Calpain 1 and 2 are required for RNA replication of echovirus 1. J. Virol. 82:1581-1590. http://dx.doi.org/10.1128/JVI.01375-07.
24. Upla P, Marjomäki V, Kankaanpää P, Ivaska J, Hyypiä T, Van Der Goot FG, Heino J. 2004. Clustering induces a lateral redistribution of alpha 2 beta 1 integrin from membrane rafts to caveolae and subsequent protein kinase C-dependent internalization. Mol. Biol. Cell 15:625-636. http://dx.doi.org/10.1091/mbc.E03-08-0588.
25. Slot JW, Geuze HJ. 2007. Cryosectioning and immunolabeling. Nat. Protoc. 2:2480-2491. http://dx.doi.org/10.1038/nprot.2007.365.
26. Kankaanpää P, Paavolainen L, Tiitta S, Karjalainen M, Päivärinne J, Nieminen J, Marjomäki V, Heino J, White DJ. 2012. BioImageXD: an open, general-purpose and high-throughput image-processing platform. Nat. Methods 9:683-689. http://dx.doi.org/10.1038/nmeth.2047.
27. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, Lockett S. 2004. Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys. J. 86:3993-4003. http://dx.doi.org/10.1529/biophysj.103.038422.
28. Brandenburg B, Lee LY, Lakadamyali M, Rust MJ, Zhuang X, Hogle JM. 2007. Imaging poliovirus entry in live cells. PLoS Biol. 5(7):e183. http://dx.doi.org/10.1371/journal.pbio.0050183.
29. Karjalainen M, Kakkonen E, Upla P, Paloranta H, Kankaanpää P, Liberali P, Renkema GH, Hyypiä T, Heino J, Marjomäki V. 2008. A Raft-derived, Pak1-regulated entry participates in α2β1 integrindependent sorting to caveosomes. Mol. Biol. Cell 19:2857-2869. http://dx.doi.org/10.1091/mbc.E07-10-1094.
30. Gruenberg J, Griffiths G, Howell KE. 1989. Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J. Cell Biol. 108:1301-1316.
31. Gruenberg J, Stenmark H. 2004. The biogenesis of multivesicular endosomes. Nat. Rev. Mol. Cell Biol. 5:317-323. http://dx.doi.org/10.1038/nrm1360.
32. Hirsch JG, Fedorko ME, Cohn ZA. 1968. Vesicle fusion and formation at the surface of pinocytic vacuoles in macrophages. J. Cell Biol. 38:629-632.
33. Raiborg C, Malerod L, Pedersen NM, Stenmark H. 2008. Differential functions of Hrs and ESCRT proteins in endocytic membrane trafficking. Exp. Cell Res. 314:801-813. http://dx.doi.org/10.1016/j.yexcr.2007.10.014.
34. Urbe S, Sachse M, Row PE, Preisinger C, Barr FA, Strous G, Klumperman J, Clague MJ. 2003. The UIM domain of Hrs couples receptor sorting to vesicle formation. J. Cell Sci. 116:4169-4179. http://dx.doi.org/10.1242/jcs.00723.
35. Katzmann DJ, Odorizzi G, Emr SD. 2002. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3:893-905. http://dx.doi.org/10.1038/nrm973.
36. Futai M, Oka T, Sun-Wada G, Moriyama Y, Kanazawa H, Wada Y. 2000. Luminal acidification of diverse organelles by v-ATPase in animal cells. J. Exp. Biol. 203:107-116.
37. Clague MJ, Urbe S, Aniento F, Gruenberg J. 1994. Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J. Biol. Chem. 269:21-24.
38. van Deurs B, Holm PK, Kayser L, Sandvig K. 1995. Delivery to lysosomes in the human carcinoma cell line HEp-2 involves an actin filamentfacilitated fusion between mature endosomes and preexisting lysosomes. Eur. J. Cell Biol. 66:309-323.
39. Bayer N, Schober D, Prchla E, Murphy RF, Blaas D, Fuchs R. 1998. Effect of bafilomycin A1 and nocodazole on endocytic transport in HeLa cells: implications for viral uncoating and infection. J. Virol. 72:9645-9655.
40. Siljamäki E, Rintanen N, Kirsi M, Upla P, Wang W, Karjalainen M, Ikonen E, Marjomäki V. 2013. Cholesterol dependence of collagenandechovirus 1 trafficking along the novel α2β1 integrin internalization pathway. PLoS One 8(2): e55465. http://dx.doi.org/10.1371/journal.pone.0055465.
41. Pietiäinen V, Marjomäki V, Upla P, Pelkmans L, Helenius A, Hyypiä T. 2004. Echovirus 1 endocytosis into caveosomes requires lipid rafts, dynamin II, and signaling events. Mol. Biol. Cell 15:4911-4925. http://dx.doi.org/10.1091/mbc.E04-01-0070.
42. Coyne CB, Kim KS, Bergelson JM. 2007. Poliovirus entry into human brain microvascular cells requires receptor-induced activation of SHP-2. EMBO J. 26:4016-4028. http://dx.doi.org/10.1038/sj.emboj.7601831.
43. Gazina EV, Harrison DN, Jefferies M, Tan H, Williams D, Anderson DA, Petrou S. 2005. Ion transport blockers inhibit human rhinovirus 2 release. Antiviral Res. 67:98-106. http://dx.doi.org/10.1016/j.antiviral.2005.05.003.
44. Harrison DN, Gazina EV, Purcell DF, Anderson DA, Petrou S. 2008. Amiloride derivatives inhibit coxsackievirus B3 RNA replication. J. Virol. 82:1465-1473. http://dx.doi.org/10.1128/JVI.01374-07.
45. Koivusalo M, Welch C, Hayashi H, Scott CC, Kim M, Alexander T, Touret N, Hahn KM, Grinstein S. 2010. Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J. Cell Biol. 188:547-563. http://dx.doi.org/10.1083/jcb.200908086.
46. Liberali P, Kakkonen E, Turacchio G, Valente C, Spaar A, Perinetti G, Bockmann RA, Corda D, Colanzi A, Marjomäki V, Luini A. 2008. The closure of Pak1-dependent macropinosomes requires the phosphorylation of CtBP1/BARS. EMBO J. 27:970-981. http://dx.doi.org/10.1038/emboj.2008.59.
47. Bosco EE, Mulloy JC, Zheng Y. 2009. Rac1 GTPase: a "Rac" of all trades. Cell. Mol. Life Sci. 66:370-374. http://dx.doi.org/10.1007/s00018-008-8552-x.
48. Morel E, Parton RG, Gruenberg J. 2009. Annexin A2-dependent polymerization of actin mediates endosome biogenesis. Dev. Cell 16:445-457. http://dx.doi.org/10.1016/j.devcel.2009.01.007.
49. Doedens J, Maynell LA, Klymkowsky MW, Kirkegaard K. 1994. Secretory pathway function, but not cytoskeletal integrity, is required in poliovirus infection. Arch. Virol. Suppl. 9:159-172.
50. Gromeier M, Wetz K. 1990. Kinetics of poliovirus uncoating in HeLa cells in a nonacidic environment. J. Virol. 64:3590-3597.
51. Perez L, Carrasco L. 1993. Entry of poliovirus into cells does not require a low-pH step. J. Virol. 67:4543-4548.
52. Patel KP, Coyne CB, Bergelson JM. 2009. Dynamin-and lipid raftdependent entry of decay-accelerating factor (DAF)-binding and non-DAF-binding coxsackieviruses into nonpolarized cells. J. Virol. 83:11064-11077. http://dx.doi.org/10.1128/JVI.01016-09.