Dynamics of Chikungunya virus cell entry unraveled by single-virus tracking in living cells

Journal of Virology

Volumn 90, Issue 9, 2016, Pages 4745-4756

  Hoornweg, Tabitha E ^a   Van Duijl Richter, Mareike K S ^a   Ayala Nuñez, Nilda V ^a   Albulescu, Irina C ^b   Van Hemert, Martijn J ^b   Smit, Jolanda M ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

1,1' DIOCTADECYL 3,3,3',3' TETRAMETHYLINDOCARBOCYANINE; CHOLESTEROL; CLATHRIN; GLYCOPROTEIN E1; RAB PROTEIN; VALINE;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL TRACKING; CELLULAR DISTRIBUTION; CHIKUNGUNYA; CHIKUNGUNYA VIRUS; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MEMBRANE FUSION; MICROSCOPY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS INFECTIVITY; VIRUS PARTICLE; ANIMAL; CELL CULTURE; CELL LINE; CHLOROCEBUS AETHIOPS; FLUORESCENCE MICROSCOPY; METABOLISM; MOLECULAR IMAGING; PHYSIOLOGY; PROCEDURES; STAINING; VIRAL PHENOMENA AND FUNCTIONS; VIROLOGY;

ANIMALS; CELL LINE; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CHIKUNGUNYA FEVER; CHIKUNGUNYA VIRUS; CHOLESTEROL; CLATHRIN; ENDOCYTOSIS; ENDOSOMES; HUMANS; MEMBRANE FUSION; MICROSCOPY, FLUORESCENCE; MOLECULAR IMAGING; STAINING AND LABELING; VIRUS INTERNALIZATION; VIRUS PHYSIOLOGICAL PHENOMENA;

EID: 84964940282     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03184-15     Document Type: Article

References (70)

1. Schwartz O, Albert ML. 2010. Biology and pathogenesis of chikungunya virus. Nat Rev Microbiol 8:491-500. http://dx.doi.org/10.1038/nrmicro2368.
2. WHO. 2015. Chikungunya. World Health Organization, Geneva, Switzerland. http://www.who.int/mediacentre/factsheets/fs327/en/.
3. CDC. 2015. Chikungunya virus: geographic distribution. CDC, Atlanta, GA. http://www.cdc.gov/chikungunya/geo/index.html.
4. CDC. 2015. Chikungunya virus: symptoms. CDC, Atlanta, GA. http://www.cdc.gov/chikungunya/symptoms/index.html.
5. Essackjee K, Goorah S, Ramchurn SK, Cheeneebash J, Walker-Bone K. 2013. Prevalence of and risk factors for chronic arthralgia and rheumatoid-like polyarthritis more than 2 years after infection with chikungunya virus. Postgrad Med J 89:440-447. http://dx.doi.org/10.1136/postgradmedj-2012-131477.
6. Schilte C, Staikovsky F, Couderc T, Madec Y, Carpentier F, Kassab S, Albert ML, Lecuit M, Michault A. 2013. Chikungunya virus-associated long-term arthralgia: a 36-month prospective longitudinal study. PLoS Negl Trop Dis 7:e2137. http://dx.doi.org/10.1371/journal.pntd.0002137.
7. Sissoko D, Malvy D, Ezzedine K, Renault P, Moscetti F, Ledrans M, Pierre V. 2009. Post-epidemic Chikungunya disease on Reunion Island: course of rheumatic manifestations and associated factors over a 15-month period. PLoS Negl Trop Dis 3:e389. http://dx.doi.org/10.1371/journal.pntd.0000389.
8. Voss JE, Vaney M-C, Duquerroy S, Vonrhein C, Girard-Blanc C, Crublet E, Thompson A, Bricogne G, Rey FA. 2010. Glycoprotein organization of Chikungunya virus particles revealed by X-ray crystallography. Nature 468:709-712. http://dx.doi.org/10.1038/nature09555.
9. Solignat M, Gay B, Higgs S, Briant L, Devaux C. 2009. Replication cycle of chikungunya: a re-emerging arbovirus. Virology 393:183-197. http://dx.doi.org/10.1016/j.virol.2009.07.024.
10. Wang KS, Schmaljohn AL, Kuhn RJ, Strauss JH. 1991. Antiidiotypic antibodies as probes for the Sindbis virus receptor. Virology 181:694-702. http://dx.doi.org/10.1016/0042-6822(91)90903-O.
11. Wang KS, Kuhn RJ, Strauss EG, Ou S, Strauss JH. 1992. High-affinity laminin receptor is a receptor for Sindbis virus in mammalian cells. J Virol 66:4992-5001.
12. Klimstra WB, Nangle EM, Smith MS, Yurochko AD, Ryman KD. 2003. DC-SIGN and L-SIGN can act as attachment receptors for alphaviruses and distinguish between mosquito cell-and mammalian cell-derived viruses. J Virol 77:12022-12032. http://dx.doi.org/10.1128/JVI.77.22.12022-12032.2003.
13. Smit JM, Waarts B-L, Kimata K, Klimstra WB, Bittman R, Wilschut J. 2002. Adaptation of alphaviruses to heparan sulfate: interaction of Sindbis and Semliki forest viruses with liposomes containing lipidconjugated heparin. J Virol 76:10128-10137. http://dx.doi.org/10.1128/JVI.76.20.10128-10137.2002.
14. La Linn M, Eble JA, Lübken C, Slade RW, Heino J, Davies J, Suhrbier A. 2005. An arthritogenic alphavirus uses the α1β1 integrin collagen receptor. Virology 336:229-239. http://dx.doi.org/10.1016/j.virol.2005.03.015.
15. Malygin AA, Bondarenko EI, Ivanisenko VA, Protopopova EV, Karpova GG, Loktev VB. 2009. C-terminal fragment of human lamininbinding protein contains a receptor domain for Venezuelan equine en-cephalitis and tick-borne encephalitis viruses. Biokhimiia 74:1328-1336. http://dx.doi.org/10.1134/S0006297909120050.
16. Kielian M, Chanel-Vos C, Liao M. 2010. Alphavirus entry and membrane fusion. Viruses 2:796-825. http://dx.doi.org/10.3390/v2040796.
17. Helenius A, Kartenbeck J, Simons K, Fries E. 1980. On the entry of Semliki Forest virus into BHK-21 cells. J Cell Biol 84:404-420. http://dx.doi.org/10.1083/jcb.84.2.404.
18. Kolokoltsov AA, Fleming EH, Davey RA. 2006. Venezuelan equine encephalitis virus entry mechanism requires late endosome formation and resists cell membrane cholesterol depletion. Virology 347:333-342. http://dx.doi.org/10.1016/j.virol.2005.11.051.
19. Marsh M, Bolzau E, Helenius A. 1983. Penetration of Semliki Forest virus from acidic prelysosomal vacuoles. Cell 32:931-940. http://dx.doi.org/10.1016/0092-8674(83)90078-8.
20. Yamauchi Y, Helenius A. 2013. Virus entry at a glance. J Cell Sci 126: 1289-1295. http://dx.doi.org/10.1242/jcs.119685.
21. Colpitts TM, Moore AC, Kolokoltsov AA, Davey RA. 2007. Venezuelan equine encephalitis virus infection of mosquito cells requires acidification as well as mosquito homologs of the endocytic proteins Rab5 and Rab7. Virology 369:78-91. http://dx.doi.org/10.1016/j.virol.2007.07.012.
22. White J, Helenius A. 1980. pH-dependent fusion between the Semliki Forest virus membrane and liposomes. Proc Natl Acad Sci U S A 77:3273-3277. http://dx.doi.org/10.1073/pnas.77.6.3273.
23. Nieva JL, Bron R, Corver J, Wilschut J. 1994. Membrane fusion of Semliki Forest virus requires sphingolipids in the target membrane. EMBO J 13:2797-2804.
24. Smit JM, Bittman R, Wilschut J. 1999. Low-pH-dependent fusion of Sindbis virus with receptor-free cholesterol-and sphingolipid-containing liposomes. J Virol 73:8476-8484.
25. Waarts B-L, Bittman R, Wilschut J. 2002. Sphingolipid and cholesterol dependence of alphavirus membrane fusion. Lack of correlation with lipid raft formation in target liposomes. J Biol Chem 277:38141-38147. http://dx.doi.org/10.1074/jbc.M206998200.
26. van Duijl-Richter MKS, Hoornweg TE, Rodenhuis-Zybert IA, Smit JM. 2015. Early events in chikungunya virus infection-from virus cell binding to membrane fusion. Viruses 7:3647-3674. http://dx.doi.org/10.3390/v7072792.
27. Gold ES, Underhill DM, Morrissette NS, Guo J, McNiven MA, Aderem A. 1999. Dynamin 2 is required for phagocytosis in macrophages. J Exp Med 190:1849-1856. http://dx.doi.org/10.1084/jem.190.12.1849.
28. Bernard E, Solignat M, Gay B, Chazal N, Higgs S, Devaux C, Briant L. 2010. Endocytosis of chikungunya virus into mammalian cells: role of clathrin and early endosomal compartments. PLoS One 5:e11479. http://dx.doi.org/10.1371/journal.pone.0011479.
29. Kirchhausen T, Owen D, Harrison SC. 2014. Molecular structure, function, and dynamics of clathrin-mediated membrane traffic. Cold Spring Harb Perspect Biol 6:a016725. http://dx.doi.org/10.1101/cshperspect.a016725.
30. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, Transidico P, Di Fiore PP, Polo S. 2005. Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci U S A 102:2760-2765. http://dx.doi.org/10.1073/pnas.0409817102.
31. Ooi YS, Stiles KM, Liu CY, Taylor GM, Kielian M. 2013. Genomewide RNAi screen identifies novel host proteins required for alphavirus entry. PLoS Pathog 9:e1003835. http://dx.doi.org/10.1371/journal.ppat.1003835.
32. Lee RCH, Hapuarachchi HC, Chen KC, Hussain KM, Chen H, Low SL, Ng LC, Lin R, Ng MM-L, Chu JJH. 2013. Mosquito cellular factors and functions in mediating the infectious entry of chikungunya virus. PLoS Negl Trop Dis 7:e2050. http://dx.doi.org/10.1371/journal.pntd.0002050.
33. Kuo S-C, Chen Y-J, Wang Y-M, Tsui P-Y, Kuo M-D, Wu T-Y, Lo SJ. 2012. Cell-based analysis of Chikungunya virus E1 protein in membrane fusion. J Biomed Sci 19:44. http://dx.doi.org/10.1186/1423-0127-19-44.
34. van Duijl-Richter M, Blijleven J, van Oijen A, Smit J. 2015. Chikungunya virus fusion properties elucidated by single-particle and bulk approaches. J Gen Virol 96:2122-2132. http://dx.doi.org/10.1099/vir.0.000144.
35. Scholte FEM, Tas A, Martina BEE, Cordioli P, Narayanan K, Makino S, Snijder EJ, van Hemert MJ. 2013. Characterization of synthetic Chikungunya viruses based on the consensus sequence of recent E1-226V isolates. PLoS One 8:e71047. http://dx.doi.org/10.1371/journal.pone.0071047.
36. van der Schaar HM, Rust MJ, Waarts B-L, van der Ende-Metselaar H, Kuhn RJ, Wilschut J, Zhuang X, Smit JM. 2007. Characterization of the early events in dengue virus cell entry by biochemical assays and singlevirus tracking. J Virol 81:12019-12028. http://dx.doi.org/10.1128/JVI.00300-07.
37. Ayala-Nuñez NV, Wilschut J, Smit JM. 2011. Monitoring virus entry into living cells using DiD-labeled dengue virus particles. Methods 55: 137-143. http://dx.doi.org/10.1016/j.ymeth.2011.07.009.
38. Thompson BS, Moesker B, Smit JM, Wilschut J, Diamond MS, Fremont DH. 2009. A therapeutic antibody against West Nile virus neutralizes infection by blocking fusion within endosomes. PLoS Pathog 5:e1000453. http://dx.doi.org/10.1371/journal.ppat.1000453.
39. Sourisseau M, Schilte C, Casartelli N, Trouillet C, Guivel-Benhassine F, Rudnicka D, Sol-Foulon N, Le Roux K, Prevost MC, Fsihi H, Frenkiel MP, Blanchet F, Afonso PV, Ceccaldi PE, Ozden S, Gessain A, Schuffenecker I, Verhasselt B, Zamborlini A, Saïb A, Rey FA, Arenzana-Seisdedos F, Desprès P, Michault A, Albert ML, Schwartz O. 2007. Characterization of reemerging chikungunya virus. PLoS Pathog 3:e89. http://dx.doi.org/10.1371/journal.ppat.0030089.
40. Dean RT, Jessup W, Roberts CR. 1984. Effects of exogenous amines on mammalian cells, with particular reference to membrane flow. Biochem J 217:27-40. http://dx.doi.org/10.1042/bj2170027.
41. Axelsson MAB, Karlsson NG, Steel DM, Ouwendijk J, Nilsson T, Hansson GC. 2001. Neutralization of pH in the Golgi apparatus causes redistribution of glycosyltransferases and changes in the O-glycosylation of mucins. Glycobiology 11:633-644. http://dx.doi.org/10.1093/glycob/11.8.633.
42. Stauffer F, De Miranda J, Schechter MC, Carneiro FA, Salgado LT, Machado GF, Da Poian AT. 2007. Inactivation of vesicular stomatitis virus through inhibition of membrane fusion by chemical modification of the viral glycoprotein. Antiviral Res 73:31-39. http://dx.doi.org/10.1016/j.antiviral.2006.07.007.
43. Stauffer F, De Miranda J, Schechter MC, Queiroz FA, Santos NO, Alves AMB, Da Poian AT. 2007. New chemical method of viral inactivation for vaccine development based on membrane fusion inhibition. Vaccine 25: 7885-7892. http://dx.doi.org/10.1016/j.vaccine.2007.09.025.
44. Le Roy C, Wrana JL. 2005. Clathrin-and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 6:112-126. http://dx.doi.org/10.1038/nrm1571.
45. Liu AP, Aguet F, Danuser G, Schmid SL. 2010. Local clustering of transferrin receptors promotes clathrin-coated pit initiation. J Cell Biol 191:1381-1393. http://dx.doi.org/10.1083/jcb.201008117.
46. Schelhaas M, Shah B, Holzer M, Blattmann P, Kühling L, Day PM, Schiller JT, Helenius A. 2012. Entry of human papillomavirus type 16 by actin-dependent, clathrin-and lipid raft-independent endocytosis. PLoS Pathog 8:e1002657. http://dx.doi.org/10.1371/journal.ppat.1002657.
47. Cuesta-Geijo MA, Galindo I, Hernáez B, Quetglas JI, Dalmau-Mena I, Alonso C. 2012. Endosomal maturation, Rab7 GTPase and phosphoinositides in African swine fever virus entry. PLoS One 7:e48853. http://dx.doi.org/10.1371/journal.pone.0048853.
48. Huotari J, Helenius A. 2011. Endosome maturation. EMBO J 30:3481-3500. http://dx.doi.org/10.1038/emboj.2011.286.
49. Schnatwinkel C, Christoforidis S, Lindsay MR, Uttenweiler-Joseph S, Wilm M, Parton RG, Zerial M. 2004. The Rab5 effector Rabankyrin-5 regulates and coordinates different endocytic mechanisms. PLoS Biol 2:E261. http://dx.doi.org/10.1371/journal.pbio.0020261.
50. Coyne CB, Shen L, Turner JR, Bergelson JM. 2007. Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell Host Microbe 2:181-192. http://dx.doi.org/10.1016/j.chom.2007.07.003.
51. Mellman I. 1992. The importance of being acid: the role of acidification in intracellular membrane traffic. J Exp Biol 172:39-45.
52. Kielian MC, Helenius A. 1984. Role of cholesterol in fusion of Semliki Forest virus with membranes. J Virol 52:281-283.
53. Phalen T, Kielian M. 1991. Cholesterol is required for infection by Semliki Forest virus. J Cell Biol 112:615-623. http://dx.doi.org/10.1083/jcb.112.4.615.
54. Chatterjee PK, Vashishtha M, Kielian M. 2000. Biochemical consequences of a mutation that controls the cholesterol dependence of Semliki Forest virus fusion. J Virol 74:1623-1631. http://dx.doi.org/10.1128/JVI.74.4.1623-1631.2000.
55. Lu YE, Cassese T, Kielian M. 1999. The cholesterol requirement for Sindbis virus entry and exit and characterization of a spike protein region involved in cholesterol dependence. J Virol 73:4272-4278.
56. Tsetsarkin KA, Vanlandingham DL, McGee CE, Higgs S. 2007. A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog 3:e201. http://dx.doi.org/10.1371/journal.ppat.0030201.
57. Wintachai P, Wikan N, Kuadkitkan A, Jaimipuk T, Ubol S, Pulmanausahakul R, Auewarakul P, Kasinrerk W, Weng W-Y, Panyasrivanit M, Paemanee A, Kittisenachai S, Roytrakul S, Smith DR. 2012. Identification of prohibitin as a Chikungunya virus receptor protein. J Med Virol 84:1757-1770. http://dx.doi.org/10.1002/jmv.23403.
58. Moller-Tank S, Kondratowicz AS, Davey RA, Rennert PD, Maury W. 2013. Role of the phosphatidylserine receptor TIM-1 in enveloped-virus entry. J Virol 87:8327-8341. http://dx.doi.org/10.1128/JVI.01025-13.
59. Silva LA, Khomandiak S, Ashbrook AW, Weller R, Heise MT, Morrison TE, Dermody TS. 2014. A single-amino-acid polymorphism in Chikungunya virus E2 glycoprotein influences glycosaminoglycan utilization. J Virol 88:2385-2397. http://dx.doi.org/10.1128/JVI.03116-13.
60. Fongsaran C, Jirakanwisal K, Kuadkitkan A, Wikan N, Wintachai P, Thepparit C, Ubol S, Phaonakrop N, Roytrakul S, Smith DR. 2014. Involvement of ATP synthase-subunit in chikungunya virus entry into insect cells. Arch Virol 159:3353-3364. http://dx.doi.org/10.1007/s00705-014-2210-4.
61. Sieczkarski SB, Whittaker GR. 2003. Differential requirements of Rab5 and Rab7 for endocytosis of influenza and other enveloped viruses. Traffic 4:333-343. http://dx.doi.org/10.1034/j.1600-0854.2003.00090.x.
62. Leung JY-S, Ng MM-L, Chu JJH. 2011. Replication of alphaviruses: a review on the entry process of alphaviruses into cells. Adv Virol 2011:249640 http://dx.doi.org/10.1155/2011/249640.
63. Zaitseva E, Yang S-T, Melikov K, Pourmal S, Chernomordik LV. 2010. Dengue virus ensures its fusion in late endosomes using compartment-specific lipids. PLoS Pathog 6:e1001131. http://dx.doi.org/10.1371/journal.ppat.1001131.
64. +-ATPase regulation of endosomal acidification in K562 erythroleukemia cells. Analysis via inhibition of transferrin recycling by low temperatures. J Biol Chem 266:3469-3474.
65. Vonderheit A, Helenius A. 2005. Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 3:e233. http://dx.doi.org/10.1371/journal.pbio.0030233.
66. Vazeille M, Moutailler S, Coudrier D, Rousseaux C, Khun H, Huerre M, Thiria J, Dehecq J-S, Fontenille D, Schuffenecker I, Despres P, Failloux A-B. 2007. Two Chikungunya isolates from the outbreak of La Reunion (Indian Ocean) exhibit different patterns of infection in the mosquito, Aedes albopictus. PLoS One 2:e1168. http://dx.doi.org/10.1371/journal.pone.0001168.
67. Tsetsarkin KA, McGee CE, Higgs S. 2011. Chikungunya virus adaptation to Aedes albopictus mosquitoes does not correlate with acquisition of cholesterol dependence or decreased pH threshold for fusion reaction. Virol J 8:376. http://dx.doi.org/10.1186/1743-422X-8-376.
68. Gay B, Bernard E, Solignat M, Chazal N, Devaux C, Briant L. 2012. pH-dependent entry of chikungunya virus into Aedes albopictus cells. Infect Genet Evol 12:1275-1281. http://dx.doi.org/10.1016/j.meegid.2012.02.003.
69. Bordi L, Meschi S, Selleri M, Lalle E, Castilletti C, Carletti F, Chiappini R, Di Caro A, Capobianchi MR. 2011. Chikungunya virus isolates with/without A226V mutation show different sensitivity to IFN-α, but similar replication kinetics in non human primate cells. New Microbiol 34:87-91.
70. Priya R, Dhanwani R, Patro IK, Rao PVL, Parida MM. 2013. Differential regulation of TLR mediated innate immune response of mouse neuronal cells following infection with novel ECSA genotype of Chikungunya virus with and without E1:A226V mutation. Infect Genet Evol 20:396-406. http://dx.doi.org/10.1016/j.meegid.2013.09.030.