Entry of tiger frog virus (an iridovirus) into HepG2 cells via a pH-dependent, atypical, caveola-mediated endocytosis pathway

Journal of Virology

Volumn 85, Issue 13, 2011, Pages 6416-6426

  Guo, Chang Jun ^a   Liu, Dong ^a   Wu, Yan Yan ^a   Yang, Xiao Bo ^a   Yang, Li Shi ^a   Mi, Shu ^a   Huang, Yu Xin ^a   Luo, Yong Wen ^a   Jia, Kun Tong ^a   Liu, Zhao Yu ^a   Chen, Wei Jian ^a   Weng, Shao Ping ^a   Yu, Xiao Qiang ^b   He, Jian Guo ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; AMMONIUM CHLORIDE; BAFILOMYCIN; CAVEOLIN 1; CHLOROQUINE; CHLORPROMAZINE; CHOLERA TOXIN B SUBUNIT; CHOLESTEROL; CLATHRIN; DYNAMIN; ESP15 PROTEIN; MEMBRANE LIPID; UNCLASSIFIED DRUG;

ARTICLE; CAVEOLA; CELL ORGANELLE; CELL STRAIN BHK; CELL STRAIN HEPG2; COATED VESICLE; CONTROLLED STUDY; ENDOCYTOSIS; FROG VIRUS 3; GOLGI COMPLEX; IRIDOVIRUS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TIGER FROG VIRUS; VIRION; VIRUS ENTRY; ANIMAL; CYTOLOGY; HUMAN; LIVER; METABOLISM; PATHOGENICITY; PHYSIOLOGY; VIROLOGY;

FROG VIRUS 3; HOPLOBATRACHUS TIGERINUS; IRIDOVIRIDAE; IRIDOVIRUS; RANAVIRUS; TIGER FROG VIRUS; VERTEBRATA;

ACTINS; ANIMALS; CAVEOLAE; CHOLESTEROL; DYNAMINS; ENDOCYTOSIS; HEP G2 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; LIVER; RANAVIRUS; VIRUS INTERNALIZATION;

EID: 80052064799     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01500-10     Document Type: Article

References (68)

1. Abazeed, M. E., J. M. Blanchette, and R. S. Fuller. 2005. Cell-free transport from the trans-golgi network to late endosome requires factors involved in formation and consumption of clathrin-coated vesicles. J. Biol. Chem. 280: 4442-4450.
2. Beer, C., D. S. Andersen, A. Rojek, and L. Pedersen. 2005. Caveola-dependent endocytic entry of amphotropic murine leukemia virus. J. Virol. 79: 10776-10787.
3. Benmerah, A., M. Bayrou, N. Cerf-Bensussan, and A. Dautry-Varsat. 1999. Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J. Cell Sci. 112:1303-1311.
4. Bernatchez, P. N., et al. 2005. Dissecting the molecular control of endothelial NO synthase by caveolin-1 using cell-permeable peptides. Proc. Natl. Acad. Sci. U. S. A. 102:761-766.
5. Bishop, N. E. 1997. An update on non-clathrin-coated endocytosis. Rev. Med. Virol. 7:199-209.
6. Braunwald, J., H. Nonnenmacher, and F. Tripier-Darcy. 1985. Ultrastructural and biochemical study of frog virus 3 uptake by BHK-21 cells. J. Gen. Virol. 66:283-293.
7. Chinchar, V. G., et al. 2005. Family Iridoviridae virus, p. 145-162. In C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger, and L. A. Ball (ed.), Taxonomy of virus. Elsevier/Academic Press, San Diego, CA.
8. Chinchar, V. G., A. Hyatt, T. Miyazaki, and T. Williams. 2009. Family Iridoviridae: poor viral relations no longer. Curr. Top. Microbiol. Immunol. 328:123-170.
9. Chu, J. J., and M. L. Ng. 2004. Infectious entry of West Nile virus occurs through a clathrin-mediated endocytic pathway. J. Virol. 78:10543-10555.
10. Delius, H., G. Darai, and R. M. Flügel. 1984. DNA analysis of insect iridescent virus 6: evidence for circular permutation and terminal redundancy. J. Virol. 49:609-614.
11. Dimitrov, D. S. 2004. Virus entry: molecular mechanisms and biomedical applications. Nat. Rev. Microbiol. 2:109-122.
12. Eash, S., W. Querbes, and W. J. Atwood. 2004. Infection of vero cells by BK virus is dependent on caveolae. J. Virol. 78:11583-11590.
13. Gilbert, J. M., and T. L. Benjamin. 2000. Early steps of polyomavirus entry into cells. J. Virol. 74:8582-8588.
14. Goorha, R. 1982. Frog virus 3 DNA replication occurs in two stages. J. Virol. 43:519-528.
15. Goorha, R., and A. Granoff. 1979. Icosahedral cytoplasmic deoxyriboviruses, p. 347-399. In H. Fraenkel-Conrat and R. R. Wagner (ed.), Comprehensive virology. Plenum, New York, NY.
16. Goorha, R., and K. G. Murti. 1982. The genome of frog virus 3, an animal DNA virus, is circularly permuted and terminally redundant. Proc. Natl. Acad. Sci. U. S. A. 79:248-252.
17. Guo, C. J., et al. 2009. The Jak and Stat family members of the mandarin fish Siniperca chuatsi: molecular cloning, tissues distribution and immunobiological activity. Fish Shellfish Immunol. 27:349-359.
18. Hasebe, R., et al. 2009. Infectious entry of equine herpesvirus-1 into host cells through different endocytic pathways. Virology 393:198-209.
19. He, J. G., et al. 2002. Sequence analysis of the complete genome of an iridovirus isolated from the tiger frog. Virology 292:185-197.
20. Henley, J. R., E. W. Krueger, B. J. Oswald, and M. A. McNiven. 1998. Dynamin-mediated internalization of caveolae. J. Cell Biol. 141:85-99.
21. Hernaez, B., and C. Alonso. 2010. Dynamin- and clathrin-dependent endocytosis in African swine fever virus entry. J. Virol. 84:2100-2109.
22. Huang, H., et al. 2006. Human herpesvirus 6 envelope cholesterol is required for virus entry. J. Gen. Virol. 87:277-285.
23. Inoue, Y., et al. 2007. Clathrin-dependent entry of severe acute respiratory syndrome coronavirus into target cells expressing ACE2 with the cytoplasmic tail deleted. J. Virol. 81:8722-8729.
24. Jeonga, J. B., et al. 2006. Molecular comparison of iridoviruses isolated from marine fish cultured in Korea and imported from China. Aquaculture 255: 105-116.
25. Jin, M., et al. 2002. Hantaan virus enters cells by clathrin-dependent receptor-mediated endocytosis. Virology 294:60-69.
26. Kee, S. H., et al. 2004. Effects of endocytosis inhibitory drugs on rubella virus entry into VeroE6 cells. Microbiol. Immunol. 48:823-829.
27. Kizhatil, K., and L. M. Albritton. 1997. Requirements for different components of the host cell cytoskeleton distinguish ecotropic murine leukemia virus entry via endocytosis from entry via surface fusion. J. Virol. 71:7145- 7156.
28. Klasse, P. J., R. Bron, and M. Marsh. 1998. Mechanisms of enveloped virus entry into animal cells. Adv. Drug Deliv. Rev. 34:65-91.
29. Lamaze, C., et al. 2001. Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol. Cell 7:661-671.
30. Le, P. U., and I. R. Nabi. 2003. Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum. J. Cell Sci. 116:1059-1071.
31. Luo, Y., et al. 2009. Tiger frog virus can infect zebrafish cells for studying upor down-regulated genes by proteomics approach. Virus Res. 171-179.
32. Marsh, M., and A. Helenius. 2006. Virus entry: open sesame. Cell 124:729- 740.
33. Martinez, M. G., S. M. Cordo, and N. A. Candurra. 2007. Characterization of Junin arenavirus cell entry. J. Gen. Virol. 88:1776-1784.
34. McAuslana1, B. R., and W. R. Smith. 1968. Deoxyribonucleic acid synthesis in FV-3-infected mammalian cells. J. Virol. 2:1006-1015.
35. Minshall, R. D., et al. 2000. Endothelial cell-surface gp60 activates vesicle formation and trafficking via G(i)-coupled Src kinase signaling pathway. J. Cell Biol. 150:1057-1070.
36. Morikawa, R. K., et al. 2009. Intracellular phospholipase A1gamma (iPLA1gamma) is a novel factor involved in coat protein complex I- and Rab6-independent retrograde transport between the endoplasmic reticulum and the Golgi complex. J. Biol. Chem. 284:26620-26630.
37. Nabi, I. R., and P. U. Le. 2003. Caveolae/raft-dependent endocytosis. J. Cell Biol. 161:673-677.
38. Newton, A. J., T. Kirchhausen, and V. N. Murthy. 2006. Inhibition of dynamin completely blocks compensatory synaptic vesicle endocytosis. Proc. Natl. Acad. Sci. U. S. A. 103:17955-17960.
39. Nichols, B. 2003. Caveosomes and endocytosis of lipid rafts. J. Cell Sci. 116:4707-4714.
40. Nichols, B. J. 2002. A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nat. Cell Biol. 4:374-378.
41. Nomura, R., et al. 2004. Human coronavirus 229E binds to CD13 in rafts and enters the cell through caveolae. J. Virol. 78:8701-8718.
42. O'Donnell, V., M. Larocco, and B. Baxt. 2008. Heparan sulfate-binding foot-and-mouth disease virus enters cells via caveola-mediated endocytosis. J. Virol. 82:9075-9085.
43. Orlandi, P. A., and P. H. Fishman. 1998. Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J. Cell Biol. 141:905-915.
44. Pelkmans, L., and A. Helenius. 2003. Insider information: what viruses tell us about endocytosis. Curr. Opin. Cell Biol. 15:414-422.
45. Pelkmans, L., J. Kartenbeck, and A. Helenius. 2001. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3:473-483.
46. Pelkmans, L., D. Püntener, and A. Helenius. 2002. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296:535-539.
47. Peng, T., et al. 2009. Entry of dengue virus serotype 2 into ECV304 cells depends on clathrin-dependent endocytosis, but not on caveolae-dependent endocytosis. Can. J. Microbiol. 55:139-145.
48. Perret, E., A. Lakkaraju, S. Deborde, R. Schreiner, and E. Rodriguez-Boulan. 2005. Evolving endosomes: how many varieties and why? Curr. Opin. Cell Biol. 17:423-434.
49. Pho, M. T., A. Ashok, and W. J. Atwood. 2000. JC virus enters human glial cells by clathrin-dependent receptor-mediated endocytosis. J. Virol. 74: 2288-2292.
50. Pietiäinen, V. M., V. Marjomäki, J. Heino, and T. Hyypiä. 2005. Viral entry, lipid rafts and caveosomes. Ann. Med. 37:394-403.
51. Querbes, W., A. Benmerah, D. Tosoni, P. P. Di Fiore, and W. J. Atwood. 2004. A JC virus-induced signal is required for infection of glial cells by a clathrin- and eps15-dependent pathway. J. Virol. 78:250-256.
52. Sánchez-San Martín, C., T. López, C. F. Arias, and S. López. 2004. Characterization of rotavirus cell entry. J. Virol. 78:2310-2318.
53. Sieczkarski, S. B., and G. R. Whittaker. 2002. Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J. Virol. 76: 10455-10464.
54. Singh, R. D., et al. 2006. Caveolar endocytosis and microdomain association of a glycosphingolipid analog is dependent on its sphingosine stereochemistry. J. Biol. Chem. 281:30660-30668.
55. Snyers, L., H. Zwickl, and D. Blaas. 2003. Human rhinovirus type 2 is internalized by clathrin-mediated endocytosis. J. Virol. 77:5360-5369.
56. Stuart, A. D., and T. D. Brown. 2006. Entry of feline calicivirus is dependent on clathrin-mediated endocytosis and acidification in endosomes. J. Virol. 80:7500-7509.
57. Stuart, A. D., H. E. Eustace, T. A. McKee, and T. D. Brown. 2002. A novel cell entry pathway for a DAF-using human enterovirus is dependent on lipid rafts. J. Virol. 76:9307-9322.
58. Sun, X., V. K. Yau, B. J. Briggs, and G. R. Whittaker. 2005. Role of clathrin-mediated endocytosis during vesicular stomatitis virus entry into host cells. Virology 338:53-60.
59. Tan, W. G., T. J. Barkman, V. Gregory Chinchar, and K. Essani. 2004. Comparative genomic analyses of frog virus 3, type species of the genus Ranavirus (family Iridoviridae). Virology 323:70-84.
60. Tebar, F., T. Sorkina, A. Sorkin, M. Ericsson, and T. Kirchhausen. 1996. Eps15 is a component of clathrin-coated pits and vesicles and is located at the rim of coated pits. J. Biol. Chem. 271:28727-28730.
61. Thomas, C. M., and E. J. Smart. 2008. Caveolae structure and function. J. Cell. Mol. Med. 12:796-809.
62. Thomsen, P., K. Roepstorff, M. Stahlhut, and B. van Deurs. 2002. Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol. Biol. Cell 13:238-250.
63. Vidricaire, G., and M. J. Tremblay. 2007. A clathrin, caveolae, and dynaminindependent endocytic pathway requiring free membrane cholesterol drives HIV-1 internalization and infection in polarized trophoblastic cells. J. Mol. Biol. 368:1267-1283.
64. Wang, Q., et al. 2008. Identification of two novel membrane proteins from the Tiger frog virus (TFV). Virus Res. 136:35-42.
65. Weng, S. P., et al. 2002. Outbreaks of an iridovirus disease in cultured tiger frog, Rana tigrina rugulosa, in southern China. J. Fish Dis. 25:423-427.
66. White, J., K. Matlin, and A. Helenius. 1981. Cell fusion by Semliki Forest, influenza, and vesicular stomatitis viruses. J. Cell Biol. 89:674-679.
67. Whitley, D. S., et al. 2010. Frog virus 3 ORF 53R, a putative myristoylated membrane protein, is essential for virus replication in vitro. Virology 405: 448-456.
68. Williams, T., V. Barbosa-Solomieu, and V. G. Chinchar. 2005. A decade of advances in iridovirus research. Adv. Virus. Res. 65:173-248.