Advertisement

Virologica Sinica

, Volume 34, Issue 1, pp 30–41 | Cite as

The Role of Host Cytoskeleton in Flavivirus Infection

  • Yue Zhang
  • Wei Gao
  • Jian Li
  • Weihua Wu
  • Yaming JiuEmail author
Review

Abstract

The family of flaviviruses is one of the most medically important groups of emerging arthropod-borne viruses. Host cell cytoskeletons have been reported to have close contact with flaviviruses during virus entry, intracellular transport, replication, and egress process, although many detailed mechanisms are still unclear. This article provides a brief overview of the function of the most prominent flaviviruses-induced or -hijacked cytoskeletal structures including actin, microtubules and intermediate filaments, mainly focus on infection by dengue virus, Zika virus and West Nile virus. We suggest that virus interaction with host cytoskeleton to be an interesting area of future research.

Keywords

Flavivirus Host cytoskeleton Actin filaments Intermediate filaments Microtubules 

Notes

Acknowledgements

We thank Xia Jin (Institut Pasteur of Shanghai, Chinese Academy of Science) for discussions and critical reading of the manuscript. This work was supported by Collaborative Research Grant (KLMVI-OP-201904) of CAS Key Laboratory of Molecular Virology and Immunology, Institut Pasteur of Shanghai, Chinese Academy of Sciences, and the starting Grant of Institut Pasteur of Shanghai (1185170000), Chinese Academy of Sciences.

Compliance with Ethical Standards

Conflict of interest

All the authors declare that they have no conflict of interest.

Animal and Human Rights Statement

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

  1. Acosta EG, Castilla V, Damonte EB (2008) Functional entry of dengue virus into Aedes albopictus mosquito cells is dependent on clathrin-mediated endocytosis. J Gen Virol 89:474–484CrossRefGoogle Scholar
  2. Alcantara D, O’Driscoll M (2014) Congenital microcephaly. Am J Med Genet C Semin Med Genet 166C:124–139CrossRefGoogle Scholar
  3. Al-Obaidi MMJ, Bahadoran A, Wang SM, Manikam R, Raju CS, Sekaran SD (2018) Disruption of the blood brain barrier is vital property of neurotropic viral infection of the central nervous system. Acta Virol 62:16–27CrossRefGoogle Scholar
  4. Ayala-Nunez NV, Hoornweg TE, van de Pol DP, Sjollema KA, Flipse J, van der Schaar HM, Smit JM (2016) How antibodies alter the cell entry pathway of dengue virus particles in macrophages. Sci Rep 6:28768CrossRefGoogle Scholar
  5. Barreto-Vieira DF, Jácome FC, da Silva MAN, Caldas GC, de Filippis AMB, de Sequeira PC, de Souza EM, Andrade AA, Manso PPA, Trindade GF, Lima SMB, Barth OM (2017) Structural investigation of C6/36 and Vero cell cultures infected with a Brazilian Zika virus. PLoS ONE 12:e0184397CrossRefGoogle Scholar
  6. Bekerman E, Einav S (2015) Infectious disease. Combating emerging viral threats. Science 348:282–283CrossRefGoogle Scholar
  7. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, Wint GR, Simmons CP, Scott TW, Farrar JJ, Hay SI (2013) The global distribution and burden of dengue. Nature 496:504–507CrossRefGoogle Scholar
  8. Bily T, Palus M, Eyer L, Elsterova J, Vancova M, Ruzek D (2015) Electron tomography analysis of tick-borne encephalitis virus infection in human neurons. Sci Rep 5:10745CrossRefGoogle Scholar
  9. Blazquez AB, Escribano-Romero E, Merino-Ramos T, Saiz JC, Martin-Acebes MA (2013) Infection with Usutu virus induces an autophagic response in mammalian cells. PLoS Negl Trop Dis 7:e2509CrossRefGoogle Scholar
  10. Brault JB, Kudelko M, Vidalain PO, Tangy F, Despres P, Pardigon N (2011) The interaction of flavivirus M protein with light chain Tctex-1 of human dynein plays a role in late stages of virus replication. Virology 417:369–378CrossRefGoogle Scholar
  11. Chee HY, AbuBakar S (2004) Identification of a 48 kDa tubulin or tubulin-like C6/36 mosquito cells protein that binds dengue virus 2 using mass spectrometry. Biochem Biophys Res Commun 320:11–17CrossRefGoogle Scholar
  12. Chen W, Gao N, Wang JL, Tian YP, Chen ZT, An J (2008) Vimentin is required for dengue virus serotype 2 infection but microtubules are not necessary for this process. Arch Virol 153:1777–1781CrossRefGoogle Scholar
  13. Chiou CT, Hu CC, Chen PH, Liao CL, Lin YL, Wang JJ (2003) Association of Japanese encephalitis virus NS3 protein with microtubules and tumour susceptibility gene 101 (TSG101) protein. J Gen Virol 84:2795–2805CrossRefGoogle Scholar
  14. Chu JJ, Ng ML (2002) Trafficking mechanism of West Nile (Sarafend) virus structural proteins. J Med Virol 67:127–136Google Scholar
  15. Chu JJ, Ng ML (2004) Infectious entry of West Nile virus occurs through a clathrin-mediated endocytic pathway. J Virol 78:10543–10555CrossRefGoogle Scholar
  16. Chu JJ, Choo BG, Lee JW, Ng ML (2003) Actin filaments participate in West Nile (Sarafend) virus maturation process. J Med Virol 71:463–472CrossRefGoogle Scholar
  17. Chu JJ, Leong PW, Ng ML (2006) Analysis of the endocytic pathway mediating the infectious entry of mosquito-borne flavivirus West Nile into Aedes albopictus mosquito (C6/36) cells. Virology 349:463–475CrossRefGoogle Scholar
  18. Chuang CK, Yang TH, Chen TH, Yang CF, Chen WJ (2015) Heat shock cognate protein 70 isoform D is required for clathrin-dependent endocytosis of Japanese encephalitis virus in C6/36 cells. J Gen Virol 96:793–803CrossRefGoogle Scholar
  19. Cortese M, Goellner S, Acosta EG, Neufeldt CJ, Oleksiuk O, Lampe M, Haselmann U, Funaya C, Schieber N, Ronchi P, Schorb M, Pruunsild P, Schwab Y, Chatel-Chaix L, Ruggieri A, Bartenschlager R (2017) Ultrastructural characterization of Zika virus replication factories. Cell Rep 18:2113–2123CrossRefGoogle Scholar
  20. Coyaud E, Ranadheera C, Cheng D, Gonçalves J, Dyakov BJA, Laurent EMN, St-Germain J, Pelletier L, Gingras AC, Brumell JH, Kim PK, Safronetz D, Raught B (2018) Global interactomics uncovers extensive organellar targeting by Zika virus. Mol Cell Proteom 17:2242–2255CrossRefGoogle Scholar
  21. Cuartas-Lopez AM, Hernandez-Cuellar CE, Gallego-Gomez JC (2018) Disentangling the role of PI3 K/Akt, Rho GTPase and the actin cytoskeleton on dengue virus infection. Virus Res 256:153–165CrossRefGoogle Scholar
  22. Cudmore S, Reckmann I, Way M (1997) Viral manipulations of the actin cytoskeleton. Trends Microbiol 5:142–148CrossRefGoogle Scholar
  23. Cureton DK, Massol RH, Saffarian S, Kirchhausen TL, Whelan SP (2009) Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog 5:e1000394CrossRefGoogle Scholar
  24. Decembre E, Assil S, Hillaire ML, Dejnirattisai W, Mongkolsapaya J, Screaton GR, Davidson AD, Dreux M (2014) Sensing of immature particles produced by dengue virus infected cells induces an antiviral response by plasmacytoid dendritic cells. PLoS Pathog 10:e1004434CrossRefGoogle Scholar
  25. El Costa H, Gouilly J, Mansuy JM, Chen Q, Levy C, Cartron G, Veas F, Al-Daccak R, Izopet J, Jabrane-Ferrat N (2016) ZIKA virus reveals broad tissue and cell tropism during the first trimester of pregnancy. Sci Rep 6:35296CrossRefGoogle Scholar
  26. Foo KY, Chee HY (2015) Interaction between flavivirus and cytoskeleton during. Virus Replication Biomed Res Int 2015:427814Google Scholar
  27. Foster LJ, De Hoog CL, Mann M (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci USA 100:5813–5818CrossRefGoogle Scholar
  28. Fraisier C et al (2013) Altered protein networks and cellular pathways in severe west nile disease in mice. PLoS ONE 8:e68318CrossRefGoogle Scholar
  29. Ganapathiraju MK, Karunakaran KB, Correa-Menendez J (2016) Predicted protein interactions of IFITMs may shed light on mechanisms of Zika virus-induced microcephaly and host invasion. F1000Res 5:1919CrossRefGoogle Scholar
  30. Gerold G, Bruening J, Weigel B, Pietschmann T (2017) Protein Interactions during the flavivirus and hepacivirus life cycle. Mol Cell Proteom 16:S75–S91CrossRefGoogle Scholar
  31. Greber UF, Way M (2006) A superhighway to virus infection. Cell 124:741–754CrossRefGoogle Scholar
  32. Guzman MG, Kouri G (2003) Dengue and dengue hemorrhagic fever in the Americas: lessons and challenges. J Clin Virol 27:1–13CrossRefGoogle Scholar
  33. Hackett BA, Cherry S (2018) Flavivirus internalization is regulated by a size-dependent endocytic pathway. Proc Natl Acad Sci USA 115:4246–4251CrossRefGoogle Scholar
  34. Henry Sum MS (2015) The involvement of microtubules and actin during the infection of Japanese encephalitis virus in neuroblastoma cell line, IMR32. Biomed Res Int 2015:695283CrossRefGoogle Scholar
  35. Hou S, Kumar A, Xu ZM, Airo AM, Stryapunina I, Wong CP, Branton W, Tchesnokov E, Götte M, Power C, Hobman TC (2017) Zika virus hijacks stress granule proteins and modulates the host stress response. J Virol pii: JVI.00474-17Google Scholar
  36. Jhan MK, Tsai TT, Chen CL, Tsai CC, Cheng YL, Lee YC, Ko CY, Lin YS, Chang CP, Lin LT, Lin CF (2017) Dengue virus infection increases microglial cell migration. Sci Rep 7:91CrossRefGoogle Scholar
  37. Kalia M, Khasa R, Sharma M, Nain M, Vrati S (2013) Japanese encephalitis virus infects neuronal cells through a clathrin-independent endocytic mechanism. J Virol 87:148–162CrossRefGoogle Scholar
  38. Kanlaya R, Pattanakitsakul SN, Sinchaikul S, Chen ST, Thongboonkerd V (2009) Alterations in actin cytoskeletal assembly and junctional protein complexes in human endothelial cells induced by dengue virus infection and mimicry of leukocyte transendothelial migration. J Proteome Res 8:2551–2562CrossRefGoogle Scholar
  39. Kanlaya R, Pattanakitsakul SN, Sinchaikul S, Chen ST, Thongboonkerd V (2010a) The ubiquitin-proteasome pathway is important for dengue virus infection in primary human endothelial cells. J Proteome Res 9:4960–4971CrossRefGoogle Scholar
  40. Kanlaya R, Pattanakitsakul SN, Sinchaikul S, Chen ST, Thongboonkerd V (2010b) Vimentin interacts with heterogeneous nuclear ribonucleoproteins and dengue nonstructural protein 1 and is important for viral replication and release. Mol BioSyst 6:795–806CrossRefGoogle Scholar
  41. Khadka S, Vangeloff AD, Zhang C, Siddavatam P, Heaton NS, Wang L, Sengupta R, Sahasrabudhe S, Randall G, Gribskov M, Kuhn RJ, Perera R, LaCount DJ (2011) A physical interaction network of dengue virus and human proteins. Mol Cell Proteom 10(M111):012187Google Scholar
  42. Le Breton M, Meyniel-Schicklin L, Deloire A, Coutard B, Canard B, de Lamballerie X, Andre P, Rabourdin-Combe C, Lotteau V, Davoust N (2011) Flavivirus NS3 and NS5 proteins interaction network: a high-throughput yeast two-hybrid screen. BMC Microbiol 11:234CrossRefGoogle Scholar
  43. Lee JW, Ng ML (2004) A nano-view of West Nile virus-induced cellular changes during infection. J Nanobiotechnol 2:6CrossRefGoogle Scholar
  44. Lei S et al (2013) ROCK is involved in vimentin phosphorylation and rearrangement induced by dengue virus. Cell Biochem Biophys 67:1333–1342CrossRefGoogle Scholar
  45. Liu CC, Zhang YN, Li ZY, Hou JX, Zhou J, Kan L, Zhou B, Chen PY (2017) Rab5 and Rab11 are required for clathrin-dependent endocytosis of Japanese encephalitis virus in BHK-21 cells. J Virol 91.pii:e01113-17Google Scholar
  46. Makino Y, Suzuki T, Hasebe R, Kimura T, Maeda A, Takahashi H, Sawa H (2014) Establishment of tracking system for West Nile virus entry and evidence of microtubule involvement in particle transport. J Virol Methods 195:250–257CrossRefGoogle Scholar
  47. Medigeshi GR, Hirsch AJ, Streblow DN, Nikolich-Zugich J, Nelson JA (2008) West Nile virus entry requires cholesterol-rich membrane microdomains and is independent of alphavbeta3 integrin. J Virol 82:5212–5219CrossRefGoogle Scholar
  48. Merino-Gracia J, Garcia-Mayoral MF, Rodriguez-Crespo I (2011) The association of viral proteins with host cell dynein components during virus infection. FEBS J 278:2997–3011CrossRefGoogle Scholar
  49. Mooren OL, Galletta BJ, Cooper JA (2012) Roles for actin assembly in endocytosis. Annu Rev Biochem 81:661–686CrossRefGoogle Scholar
  50. Nawa M, Takasaki T, Yamada K, Kurane I, Akatsuka T (2003) Interference in Japanese encephalitis virus infection of Vero cells by a cationic amphiphilic drug, chlorpromazine. J Gen Virol 84:1737–1741CrossRefGoogle Scholar
  51. Ng ML (1987) Ultrastructural studies of Kunjin virus-infected Aedes albopictus cells. J Gen Virol 68(Pt 2):577–582Google Scholar
  52. Ng ML, Hong SS (1989) Flavivirus infection: essential ultrastructural changes and association of Kunjin virus NS3 protein with microtubules. Arch Virol 106:103–120CrossRefGoogle Scholar
  53. Ng ML, Pedersen JS, Toh BH, Westaway EG (1983) Immunofluorescent sites in vero cells infected with the flavivirus Kunjin. Arch Virol 78:177–190CrossRefGoogle Scholar
  54. Ng ML, Howe J, Sreenivasan V, Mulders JJ (1994) Flavivirus West Nile (Sarafend) egress at the plasma membrane. Arch Virol 137:303–313CrossRefGoogle Scholar
  55. Nikolay B, Diallo M, Boye CS, Sall AA (2011) Usutu virus in Africa. Vector Borne Zoonotic Dis 11:1417–1423CrossRefGoogle Scholar
  56. Ploubidou A, Way M (2001) Viral transport and the cytoskeleton. Curr Opin Cell Biol 13:97–105CrossRefGoogle Scholar
  57. Potokar M, Korva M, Jorgacevski J, Avsic-Zupanc T, Zorec R (2014) Tick-borne encephalitis virus infects rat astrocytes but does not affect their viability. PLoS ONE 9:e86219CrossRefGoogle Scholar
  58. Rasmussen SA, Jamieson DJ, Honein MA, Petersen LR (2016) Zika virus and birth defects-reviewing the evidence for causality. N Engl J Med 374:1981–1987CrossRefGoogle Scholar
  59. Reyes-Del Valle J, Chavez-Salinas S, Medina F, Del Angel RM (2005) Heat shock protein 90 and heat shock protein 70 are components of dengue virus receptor complex in human cells. J Virol 79:4557–4567CrossRefGoogle Scholar
  60. Rossignol ED, Peters KN, Connor JH, Bullitt E (2017) Zika virus induced cellular remodelling. Cell Microbiol.  https://doi.org/10.1111/cmi.12740 Google Scholar
  61. Ruzek D, Vancova M, Tesarova M, Ahantarig A, Kopecky J, Grubhoffer L (2009) Morphological changes in human neural cells following tick-borne encephalitis virus infection. J Gen Virol 90:1649–1658CrossRefGoogle Scholar
  62. Shrivastava N, Sripada S, Kaur J, Shah PS, Cecilia D (2011) Insights into the internalization and retrograde trafficking of Dengue 2 virus in BHK-21 cells. PLoS ONE 6:e25229CrossRefGoogle Scholar
  63. Skruzny M, Brach T, Ciuffa R, Rybina S, Wachsmuth M, Kaksonen M (2012) Molecular basis for coupling the plasma membrane to the actin cytoskeleton during clathrin-mediated endocytosis. Proc Natl Acad Sci USA 109:E2533–E2542CrossRefGoogle Scholar
  64. Soe HJ, Yong YK, Al-Obaidi MMJ, Raju CS, Gudimella R, Manikam R, Sekaran SD (2018) Identifying protein biomarkers in predicting disease severity of dengue virus infection using immune-related protein microarray. Medicine (Baltimore) 97:e9713CrossRefGoogle Scholar
  65. Taylor MP, Koyuncu OO, Enquist LW (2011) Subversion of the actin cytoskeleton during viral infection. Nat Rev Microbiol 9:427–439CrossRefGoogle Scholar
  66. Teo CS, Chu JJ (2014) Cellular vimentin regulates construction of dengue virus replication complexes through interaction with NS4A protein. J Virol 88:1897–1913CrossRefGoogle Scholar
  67. Wang JL, Zhang JL, Chen W, Xu XF, Gao N, Fan DY, An J (2010) Roles of small GTPase Rac1 in the regulation of actin cytoskeleton during dengue virus infection. PLoS Negl Trop Dis 4:e809CrossRefGoogle Scholar
  68. Wang XJ, Jiang SC, Wei HX, Deng SQ, He C, Peng HJ (2017) The differential expression and possible function of long noncoding RNAs in liver cells infected by dengue virus. Am J Trop Med Hyg 97:1904–1912CrossRefGoogle Scholar
  69. Wolf B, Diop F, Ferraris P, Wichit S, Busso C, Misse D, Gonczy P (2017) Zika virus causes supernumerary foci with centriolar proteins and impaired spindle positioning. Open Biol 7:160231CrossRefGoogle Scholar
  70. Wu N, Gao N, Fan D, Wei J, Zhang J, An J (2014) miR-223 inhibits dengue virus replication by negatively regulating the microtubule-destabilizing protein STMN1 in EAhy926 cells. Microbes Infect 16:911–922CrossRefGoogle Scholar
  71. Xu XF, Chen ZT, Gao N, Zhang JL, An J (2009) Myosin Vc, a member of the actin motor family associated with Rab8, is involved in the release of DV2 from HepG2 cells. Intervirology 52:258–265CrossRefGoogle Scholar
  72. Xu Z, Waeckerlin R, Urbanowski MD, van Marle G, Hobman TC (2012) West Nile virus infection causes endocytosis of a specific subset of tight junction membrane proteins. PLoS ONE 7:e37886CrossRefGoogle Scholar
  73. Xu Q, Cao M, Song H, Chen S, Qian X, Zhao P, Ren H, Tang H, Wang Y, Wei Y, Zhu Y, Qi Z (2016) Caveolin-1-mediated Japanese encephalitis virus entry requires a two-step regulation of actin reorganization. Future Microbiol 11:1227–1248CrossRefGoogle Scholar
  74. Yang J, Zou L, Hu Z, Chen W, Zhang J, Zhu J, Fang X, Yuan W, Hu X, Hu F, Rao X (2013) Identification and characterization of a 43 kDa actin protein involved in the DENV-2 binding and infection of ECV304 cells. Microbes Infect 15:310–318CrossRefGoogle Scholar
  75. Zamudio-Meza H, Castillo-Alvarez A, Gonzalez-Bonilla C, Meza I (2009) Cross-talk between Rac1 and Cdc42 GTPases regulates formation of filopodia required for dengue virus type-2 entry into HMEC-1 cells. J Gen Virol 90:2902–2911CrossRefGoogle Scholar
  76. Zanini F, Pu SY, Bekerman E, Einav S, Quake SR (2018) Single-cell transcriptional dynamics of flavivirus infection. Elife 7:e32942CrossRefGoogle Scholar
  77. Zhang M, Zheng X, Wu Y, Gan M, He A, Li Z, Zhang D, Wu X, Zhan X (2013) Differential proteomics of Aedes albopictus salivary gland, midgut and C6/36 cell induced by dengue virus infection. Virology 444:109–118CrossRefGoogle Scholar
  78. Zhang J, Wu N, Gao N, Yan W, Sheng Z, Fan D, An J (2016) Small G Rac1 is involved in replication cycle of dengue serotype 2 virus in EAhy926 cells via the regulation of actin cytoskeleton. Sci China Life Sci 59:487–494CrossRefGoogle Scholar

Copyright information

© Wuhan Institute of Virology, CAS 2019

Authors and Affiliations

  1. 1.CAS Key Laboratory of Molecular Virology and Immunology, Institut Pasteur of ShanghaiChinese Academy of SciencesShanghaiChina
  2. 2.University of Chinese Academy of SciencesBeijingChina

Personalised recommendations