Japanese encephalitis virus enters rat neuroblastoma cells via a pH dependent, dynamin and caveola-mediated endocytosis pathway

Journal of Virology

Volumn 86, Issue 24, 2012, Pages 13407-13422

  Zhu, Yong Zhe ^a   Xu, Qing Qiang ^a   Wu, Da Ge ^a   Ren, Hao ^a   Zhao, Ping ^a   Lao, Wen Guang ^a   Wang, Yan ^a   Tao, Qing Yuan ^a   Qian, Xi Jing ^a   Wei, You Heng ^b   Cao, Ming Mei ^a   Qi, Zhong Tian ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIUM CHLORIDE; CAVEOLIN; CHLOROQUINE; DYNAMIN; PROTEINASE K; TRANSFERRIN;

ADSORPTION; ANIMAL CELL; ARTICLE; CAVEOLA; CELL VIABILITY; CONTROLLED STUDY; ENDOCYTOSIS; GENE DOSAGE; GENE SILENCING; HUMAN; HUMAN CELL; INTERNALIZATION; JAPANESE ENCEPHALITIS VIRUS; NEUROBLASTOMA CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PHAGOCYTOSIS; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; VIRUS ENTRY; VIRUS PARTICLE; WESTERN BLOTTING;

ANIMALS; BASE SEQUENCE; CELL LINE, TUMOR; CLATHRIN; DNA PRIMERS; DYNAMINS; ENCEPHALITIS VIRUS, JAPANESE; ENDOCYTOSIS; HYDROGEN-ION CONCENTRATION; NEUROBLASTOMA; RATS; RNA, SMALL INTERFERING; VACUOLAR PROTON-TRANSLOCATING ATPASES;

FLAVIVIRUS; JAPANESE ENCEPHALITIS VIRUS; RATTUS;

EID: 84870664901     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00903-12     Document Type: Article

References (87)

1. Acosta EG, Castilla V, Damonte EB. 2008. Functional entry of dengue virus into Aedes albopictus mosquito cells is dependent on clathrinmediated endocytosis. J. Gen. Virol. 89:474-484.
2. Acosta EG, Castilla V, Damonte EB. 2009. Alternative infectious entry pathways for dengue virus serotypes into mammalian cells. Cell. Microbiol. 11:1533-1549.
3. Amstutz B, et al. 2008. Subversion of CtBP1-controlled macropinocytosis by human adenovirus serotype 3. EMBO J. 27:956-969.
4. Ashok A, Atwood WJ. 2003. Contrasting roles of endosomal pH and the cytoskeleton in infection of human glial cells by JC virus and simian virus 40. J. Virol. 77:1347-1356.
5. Benmerah A, Bayrou M, Cerf-Bensussan N, Dautry-Varsat A. 1999. Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J. Cell Sci. 112:1303-1311.
6. Boonsanay V, Smith DR. 2007. Entry into and production of the Japanese encephalitis virus from C6/36 Cells. Intervirology 50:85-92.
7. Cantín C, Holguera J, Ferreira L, Villar E, Muñoz-Barroso I. 2007. Newcastle disease virus may enter cells by caveolae-mediated endocytosis. J. Gen. Virol. 88:559-569.
8. Cao H, Thompson HM, Krueger EW, McNiven MA. 2000. Disruption of Golgi structure and function in mammalian cells expressing a mutant dynamin. J. Cell Sci. 113:1993-2002.
9. Chien YJ, Chen WJ, Hsu WL, Chiou SS. 2008. Bovine lactoferrin inhibits Japanese encephalitis virus by binding to heparan sulfate and receptor for low density lipoprotein. Virology 379:143-151.
10. Chu JJ, Ng ML. 2004. Infectious entry of West Nile virus occurs through a clathrin-mediated endocytic pathway. J. Virol. 78:10543-10555.
11. Chu JJ, Ng ML. 2004. Interaction of West Nile virus with alpha v beta 3 integrin mediates virus entry into cells. J. Biol. Chem. 279:54533-54541.
12. 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 349:463-475.
13. Clement C, et al. 2006. A novel role for phagocytosis-like uptake in herpes simplex virus entry. J. Cell Biol. 174:1009-1021.
14. Coyne CB, Bergelson JM. 2006. Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 124: 119-131.
15. Damke H, Baba T, Warnock DE, Schmid SL. 1994. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127:915-934.
16. Das S, Laxminarayana SV, Chandra N, Ravi V, Desai A. 2009. Heatshock protein 70 on Neuro2a cells is a putative receptor for Japanese encephalitis virus. Virology 385:47-57.
17. Das S, Chakraborty S, Basu A. 2010. Critical role of lipid rafts in virus entry and activation of phosphoinositide 3= kinase/Akt signaling during early stages of Japanese encephalitis virus infection in neural stem/progenitor cells. J. Neurochem. 115:537-549.
18. Doherty GJ, McMahon HT. 2009. Mechanisms of endocytosis. Annu. Rev. Biochem. 78:857-902.
19. Eash S, Querbes W, Atwood WJ. 2004. Infection of Vero cells by BK virus is dependent on caveolae. J. Virol. 78:11583-11590.
20. Feng X, et al. 2001. Caveolin-1 associates with TRAF2 to form a complex that is recruited to tumor necrosis factor receptors. J. Biol. Chem. 276: 8341-8349.
21. Fra AM, Williamson E, Simons K, Parton RG. 1995. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc. Natl. Acad. Sci. U. S. A. 92:8655-8659.
22. Fujinaga Y, et al. 2003. Gangliosides that associate with lipid rafts mediate transport of cholera and related toxins from the plasma membrane to endoplasmic reticulum. Mol. Biol. Cell 14:4783-4793.
23. Garuti R, et al. 2005. The modular adaptor protein autosomal recessive hypercholesterolemia (ARH) promotes low density lipoprotein receptor clustering into clathrin-coated pits. J. Biol. Chem. 280:40996-41004.
24. Ghosh D, Basu A. 2009. Japanese encephalitis-a pathological and clinical perspective. PLoS Negl. Trop. Dis. 3:e437. doi:10.1371/journal.pntd.0000437.
25. Ghoshal A, et al. 2007. Proinflammatory mediators released by activated microglia induce neuronal death in Japanese encephalitis. Glia 55:483-496.
26. Gubler D, Kuno G, Markoff L. 2007. Flaviviruses, p 1153-1252. In Knipe DM, Howley PM (ed), Fields virology, 5th ed, vol 1. Lippincott-Williams & Wilkins, Philadelphia, PA.
27. Guo CJ, et al. 2011. Entry of tiger frog virus (an Iridovirus) into HepG2 cells via a pH-dependent, atypical, caveolae-mediated endocytosis pathway. J. Virol. 85:6416-6426.
28. Harrison SC. 2008. The pH sensor for flavivirus membrane fusion. J. Cell Biol. 183:177-179.
29. Hashimoto M, Takenouchi T, Rockenstein E, Masliah E. 2003. Alphasynuclein up-regulates expression of caveolin-1 and down-regulates extracellular signal-regulated kinase activity in B103 neuroblastoma cells: role in the pathogenesis of Parkinson's disease. J. Neurochem. 85:1468-1479.
30. Johannsdottir HK, Mancini R, Kartenbeck J, Amato L, Helenius A. 2009. Host cell factors and functions involved in vesicular stomatitis virus entry. J. Virol. 83:440-453.
31. Krishnan MN, et al. 2007. Rab 5 is required for the cellular entry of dengue and West Nile viruses. J. Virol. 81:4881-4885.
32. Lau AW, Chou MM. 2008. The adaptor complex AP-2 regulates postendocytic trafficking through the non-clathrin Arf6-dependent endocytic pathway. J. Cell Sci. 121:4008-4017.
33. Le PU, Nabi IR. 2003. Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum. J. Cell Sci. 116:1059-1071.
34. Lee CJ, Lin HR, Liao CL, Lin YL. 2008. Cholesterol effectively blocks entry of flavivirus. J. Virol. 82:6470-6480.
35. Lee CJ, Liao CL, Lin YL. 2005. Flavivirus activates phosphatidylinositol 3-kinase signaling to block caspase-dependent apoptotic cell death at the early stage of virus infection. J. Virol. 79:8388-8399.
36. Macia E, et al. 2006. Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10:839-850.
37. Marechal V, et al. 2001. Human immunodeficiency virus type 1 entry into macrophages mediated by macropinocytosis. J. Virol. 75:11166-11177.
38. Marjomaki V, et al. 2002. Internalization of echovirus 1 in caveolae. J. Virol. 76:1856-1865.
39. Marsh M, Helenius A. 2006. Virus entry: open sesame. Cell 124:729-740.
40. Mayor S, Pagano RE. 2007. Pathways of clathrin-independent endocytosis. Nat. Rev. Mol. Cell Biol. 8:603-612.
41. McMinn PC. 1997. The molecular basis of virulence of the encephalitogenic flaviviruses. J. Gen. Virol. 78:2711-2722.
42. 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. 82:5212-5219.
43. Mineo C, Ying YS, Chapline C, Jaken S, Anderson RG. 1998. Targeting of protein kinase Calpha to caveolae. J. Cell Biol. 141:601-610.
44. Misra UK, Kalita J. 2010. Overview: Japanese encephalitis. Prog. Neurobiol. 91:108-120.
45. Mizzen L, Hilton A, Cheley S, Anderson R. 1985. Attenuation of murine coronavirus infection by ammonium chloride. Virology 142:378-388.
46. Mosso C, Galván-Mendoza IJ, Ludert JE, del Angel RM. 2008. Endocytic pathway followed by dengue virus to infect the mosquito cell line C6/36 HT. Virology 378:193-199.
47. Mukhopadhyay S, Kuhn RJ, Rossmann MG. 2005. A structural perspective of the flavivirus life cycle. Nat. Rev. Microbiol. 3:13-22.
48. Nawa M, Machida S, Takasaki T, Kurane I. 2007. Plaque formation by Japanese encephalitis virus bound to mosquito C6/36 cells after low pH exposure on the cell surface. Jpn. J. Infect. Dis. 60:118-120.
49. 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. 84:1737-1741.
50. Nelson N. 2003. A journey from mammals to yeast with vacuolar H-ATPase (V-ATPase). J. Bioenerg. Biomembr. 35:281-289.
51. Nomura R, Fujimoto T. 1999. Tyrosine-phosphorylated caveolin-1: immunolocalization and molecular characterization. Mol. Biol. Cell 10:975-986.
52. Nunes-Correia I, Eulálio A, Nir S, Pedroso de Lima MC. 2004. Caveolae as an additional route for influenza virus endocytosis inMDCKcells. Cell. Mol. Biol. Lett. 9:47-60.
53. Oh P, McIntosh DP, Schnitzer JE. 1998. Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J. Cell Biol. 141:101-114.
54. Parton RG, Joggerst B, Simons K. 1994. Regulated internalization of caveolae. J. Cell Biol. 127:1199-1215.
55. 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.
56. Pelkmans L, Helenius A. 2003. Insider information: what viruses tell us about endocytosis. Curr. Opin. Cell Biol. 15:414-422.
57. Pelkmans L, Püntener D, Helenius A. 2002. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296:535-539.
58. Pelkmans L, et al. 2005. Genome-wide analysis of human kinases in clathrin-and caveolae/raft-mediated endocytosis. Nature 436:78-86.
59. Pelkmans L, Kartenbeck J, Helenius A. 2001. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3:473-483.
60. Perry JW, Wobus CE. 2010. Endocytosis of murine norovirus 1 into murine macrophages is dependent on dynamin II and cholesterol. J. Virol. 84:6163-6176.
61. Pitha J, Irie T, Sklar PB, Nye JS. 1988. Drug solubilizers to aid pharmacologists: amorphous cyclodextrin derivatives. Life Sci. 43:493-502.
62. Rahn E, Petermann P, Hsu MJ, Rixon FJ, Knebel-Mörsdorf D. 2011. Entry pathways of herpes simplex virus type 1 into human keratinocytes are dynamin-and cholesterol-dependent. PLoS One 6:e25464. doi: 10.1371/journal.pone.0025464.
63. Raung SL, Kuo MD, Wang YM, Chen CJ. 2001. Role of reactive oxygen intermediates in Japanese encephalitis virus infection in murine neuroblastoma cells. Neurosci. Lett. 315:9-12.
64. Raung SL, Chen SY, Liao SL, Chen JH, Chen CJ. 2007. Japanese encephalitis virus infection stimulates Src tyrosine kinase in neuron/glia. Neurosci. Lett. 419:263-268.
65. Sancey L, et al. 2009. Clustering and internalization of integrin alphavbeta3 with a tetrameric RGD-synthetic peptide. Mol. Ther. 17:837-843.
66. Sanchez A. 2007. Analysis of filovirus entry into Vero e6 cells, usinginhibitors of endocytosis, endosomal acidification, structural integrity, and cathepsin (B and L) activity. J. Infect. Dis. 196:S251-S258.
67. Sánchez-San Martín C, López T, Arias CF, López S. 2004. Characterization of rotavirus cell entry. J. Virol. 78:2310-2318.
68. Sandvig K, Torgersen ML, Raa HA, van Deurs B. 2008. Clathrinindependent endocytosis: from nonexisting to an extreme degree of complexity. Histochem. Cell Biol. 129:267-276.
69. Schelhaas M. 2010. Come in and take your coat off-how host cells provide endocytosis for virus entry. Cell. Microbiol. 12:1378-1388.
70. Sieczkarski SB, Whittaker GR. 2002. Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J. Virol. 76:10455-10464.
71. Sieczkarski SB, Whittaker GR. 2002. Dissecting virus entry via endocytosis. J. Gen. Virol. 83:1535-1545.
72. Silva MC, Guerrero-Plata A, Gilfoy FD, Garofalo RP, Mason PW. 2007. Differential activation of human monocyte-derived and plasmacytoid dendritic cells by West Nile virus generated in different host cells. J. Virol. 81:13640-13648.
73. Simons K, Toomre D. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31-39.
74. Sorkin A, von Zastrow M. 2009. Endocytosis and signalling: intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 10:609-622.
75. Suksanpaisan L, Susantad T, Smith DR. 2009. Characterization of dengue virus entry into HepG2 cells. J. Biomed. Sci. 16:17. doi:10.1186/1423-0127-16-17.
76. Sun X, Yau VK, Briggs BJ, Whittaker GR. 2005. Role of clathrinmediated endocytosis during vesicular stomatitis virus entry into host cells. Virology 338:53-60.
77. Superti F, et al. 1987. Entry pathway of vesicular stomatitis virus into different host cells. J. Gen. Virol. 68:387-399.
78. Swarup V, Ghosh J, Das S, Basu A. 2008. Tumor necrosis factor receptor-associated death domain mediated neuronal death contributes to the glial activation and subsequent neuroinflammation in Japanese encephalitis. Neurochem Int. 52:1310-1321.
79. Tani H, et al. 2010. Involvement of ceramide in the propagation of Japanese encephalitis virus, J. Virol. 84:2798-2807.
80. Tani H, et al. 2007. Replication-competent recombinant vesicular stomatitis virus encoding hepatitis C virus envelope proteins. J. Virol. 81: 8601-8612.
81. Thomsen P, Roepstorff K, Stahlhut M, van Deurs B. 2002. Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol. Biol. Cell 13:238-250.
82. Urs NM, et al. 2005. A requirement for membrane cholesterol in the beta-arrestin-and clathrin-dependent endocytosis of LPA1 lysophosphatidic acid receptors. J. Cell Sci. 118:5291-5304.
83. van der Schaar HM, et al. 2008. Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog. 4:e1000244. doi:10.1371/journal.ppat.1000244.
84. Wang LH, Rothberg KG, Anderson RG. 1993. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J. Cell Biol. 123:1107-1117.
85. West MA, Bretscher MS, Watts C. 1989. Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J. Cell Biol. 109:2731-2739.
86. Wu SC, Chiang JR, Lin CW. 2004. Novel cell adhesive glycosaminoglycan-binding proteins of Japanese encephalitis virus. Biomacromolecules 5:2160-2164.
87. Zhu YZ, et al. 2012. Association of heat-shock protein 70 with lipid rafts is required for Japanese encephalitis virus infection in Huh7 cells. J. Gen. Virol. 93:61-71.