Cellular entry via an actin and clathrin-dependent route is required for Lv2 restriction of HIV-2

Virology

Volumn 415, Issue 1, 2011, Pages 47-55

  Harrison, I P ^a,b   Mcknight, A ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Cell entry; Endocytosis; HIV 2; Lv2

Indexed keywords

ACTIN; CLATHRIN; GENE PRODUCT; RESTRICTION FACTOR LV2; TRANSCRIPTION FACTOR AP 2; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; HELA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 2; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS GENE; VIRUS VIRULENCE;

ACTINS; ADAPTOR PROTEIN COMPLEX 2; BLOTTING, WESTERN; CELL LINE, TUMOR; CLATHRIN; ENDOCYTOSIS; GENE PRODUCTS, ENV; HELA CELLS; HIV-2; HUMANS; MEMBRANE LIPIDS; MUTATION; RNA, SMALL INTERFERING; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

HUMAN IMMUNODEFICIENCY VIRUS 2; MIRIDAE;

EID: 79956201246     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.04.001     Document Type: Article

References (52)

1. Boucrot E., Saffarian S., Massol R., Kirchhausen T., Ehrlich M. Role of lipids and actin in the formation of clathrin-coated pits. Exp. Cell Res. 2006, 312(20):4036-4048.
2. Bukrinskaya A., Brichacek B., Mann A., Stevenson M. Establishment of a functional human immunodeficiency virus type 1 (HIV-1) reverse transcription complex involves the cytoskeleton. J. Exp. Med. 1998, 188(11):2113-2125.
3. Campbell E.M., Nunez R., Hope T.J. Disruption of the actin cytoskeleton can complement the ability of Nef to enhance human immunodeficiency virus type 1 infectivity. J. Virol. 2004, 78(11):5745-5755.
4. Cannon P.M., Kim N., Kingsman S.M., Kingsman A.J. Murine leukemia virus-based Tat-inducible long terminal repeat replacement vectors: a new system for anti-human immunodeficiency virus gene therapy. J. Virol. 1996, 70(11):8234-8240.
5. Chackerian B., Long E.M., Luciw P.A., Overbaugh J. Human immunodeficiency virus type 1 coreceptors participate in postentry stages in the virus replication cycle and function in simian immunodeficiency virus infection. J. Virol. 1997, 71(5):3932-3939.
6. Chazal N., Singer G., Aiken C., Hammarskjold M.L., Rekosh D. Human immunodeficiency virus type 1 particles pseudotyped with envelope proteins that fuse at low pH no longer require Nef for optimal infectivity. J. Virol. 2001, 75(8):4014-4018.
7. Cureton D.K., Massol R.H., Saffarian S., Kirchhausen T.L., Whelan S.P. Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog. 2009, 5(4):e1000394.
8. Daecke J., Fackler O.T., Dittmar M.T., Krausslich H.G. Involvement of clathrin-mediated endocytosis in human immunodeficiency virus type 1 entry. J. Virol. 2005, 79(3):1581-1594.
9. Del Real G., Jimenez-Baranda S., Lacalle R.A., Mira E., Lucas P., Gomez-Mouton C., Carrera A.C., Martinez A.C., Manes S. Blocking of HIV-1 infection by targeting CD4 to nonraft membrane domains. J. Exp. Med. 2002, 196(3):293-301.
10. Dwivedi Y., Pandey G.N. Effects of treatment with haloperidol, chlorpromazine, and clozapine on protein kinase C (PKC) and phosphoinositide-specific phospholipase C (PI-PLC) activity and on mRNA and protein expression of PKC and PLC isozymes in rat brain. J. Pharmacol. Exp. Ther. 1999, 291(2):688-704.
11. Goff S.P. Retrovirus restriction factors. Mol. Cell 2004, 16(6):849-859.
12. Han Y., Wang X., Dang Y., Zheng Y.H. Demonstration of a novel HIV-1 restriction phenotype from a human T cell line. PLoS One 2008, 3(7):e2796.
13. Holmes R.K., Malim M.H., Bishop K.N. APOBEC-mediated viral restriction: not simply editing?. Trends Biochem. Sci. 2007, 32(3):118-128.
14. Hubner W., McNerney G.P., Chen P., Dale B.M., Gordon R.E., Chuang F.Y., Li X.D., Asmuth D.M., Huser T., Chen B.K. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 2009, 323(5922):1743-1747.
15. Ivanov, A. I. (2008). Exocytosis and endocytosis. Methods Mol Biol 440, v-vi.
16. Jeetendra E., Robison C.S., Albritton L.M., Whitt M.A. The membrane-proximal domain of vesicular stomatitis virus G protein functions as a membrane fusion potentiator and can induce hemifusion. J. Virol. 2002, 76(23):12300-12311.
17. Johannsdottir H.K., Mancini R., Kartenbeck J., Amato L., Helenius A. Host cell factors and functions involved in vesicular stomatitis virus entry. J. Virol. 2009, 83(1):440-453.
18. Kizhatil K., Albritton L.M. Requirements for different components of the host cell cytoskeleton distinguish ecotropic murine leukemia virus entry via endocytosis from entry via surface fusion. J. Virol. 1997, 71(10):7145-7156.
19. Komano J., Miyauchi K., Matsuda Z., Yamamoto N. Inhibiting the Arp2/3 complex limits infection of both intracellular mature vaccinia virus and primate lentiviruses. Mol. Biol. Cell 2004, 15(12):5197-5207.
20. Larsson C. Protein kinase C and the regulation of the actin cytoskeleton. Cell. Signal. 2006, 18(3):276-284.
21. Marchant D., Neil S.J., Aubin K., Schmitz C., McKnight A. An envelope-determined, pH-independent endocytic route of viral entry determines the susceptibility of human immunodeficiency virus type 1 (HIV-1) and HIV-2 to Lv2 restriction. J. Virol. 2005, 79(15):9410-9418.
22. Marechal V., Prevost M.C., Petit C., Perret E., Heard J.M., Schwartz O. Human immunodeficiency virus type 1 entry into macrophages mediated by macropinocytosis. J. Virol. 2001, 75(22):11166-11177.
23. Marsh M., Bron R. SFV infection in CHO cells: cell-type specific restrictions to productive virus entry at the cell surface. J. Cell Sci. 1997, 110(Pt 1):95-103.
24. Marsh M., Helenius A. Virus entry: open sesame. Cell 2006, 124(4):729-740.
25. McDonald D., Vodicka M.A., Lucero G., Svitkina T.M., Borisy G.G., Emerman M., Hope T.J. Visualization of the intracellular behavior of HIV in living cells. J. Cell Biol. 2002, 159(3):441-452.
26. McKnight A., Griffiths D.J., Dittmar M., Clapham P., Thomas E. Characterization of a late entry event in the replication cycle of human immunodeficiency virus type 2. J. Virol. 2001, 75(15):6914-6922.
27. Milzani A., DalleDonne I. Effects of chlorpromazine on actin polymerization: slackening of filament elongation and filament annealing. Arch. Biochem. Biophys. 1999, 369(1):59-67.
28. Miyauchi K., Kim Y., Latinovic O., Morozov V., Melikyan G.B. HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 2009, 137(3):433-444.
29. Motley A., Bright N.A., Seaman M.N., Robinson M.S. Clathrin-mediated endocytosis in AP-2-depleted cells. J. Cell Biol. 2003, 162(5):909-918.
30. Nisole S., Stoye J.P., Saib A. TRIM family proteins: retroviral restriction and antiviral defence. Nat. Rev. Microbiol. 2005, 3(10):799-808.
31. Pelkmans L., Fava E., Grabner H., Hannus M., Habermann B., Krausz E., Zerial M. Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 2005, 436(7047):78-86.
32. Permanyer M., Ballana E., Este J.A. Endocytosis of HIV: anything goes. Trends Microbiol. 2010, 18(12):543-551.
33. Pineda M.J., Orton B.R., Overbaugh J. A TRIM5alpha-independent post-entry restriction to HIV-1 infection of macaque cells that is dependent on the path of entry. Virology 2007, 363(2):310-318.
34. Pitcher C., Honing S., Fingerhut A., Bowers K., Marsh M. Cluster of differentiation antigen 4 (CD4) endocytosis and adaptor complex binding require activation of the CD4 endocytosis signal by serine phosphorylation. Mol. Biol. Cell 1999, 10(3):677-691.
35. Poupon V., Girard M., Legendre-Guillemin V., Thomas S., Bourbonniere L., Philie J., Bright N.A., McPherson P.S. Clathrin light chains function in mannose phosphate receptor trafficking via regulation of actin assembly. Proc. Natl Acad. Sci. U S A 2008, 105(1):168-173.
36. Quirin K., Eschli B., Scheu I., Poort L., Kartenbeck J., Helenius A. Lymphocytic choriomeningitis virus uses a novel endocytic pathway for infectious entry via late endosomes. Virology 2008, 378(1):21-33.
37. Reuter S., Kaumanns P., Buschhorn S.B., Dittmar M.T. Role of HIV-2 envelope in Lv2-mediated restriction. Virology 2005, 332(1):347-358.
38. Robertson A.S., Smythe E., Ayscough K.R. Functions of actin in endocytosis. Cell. Mol. Life Sci. 2009, 66(13):2049-2065.
39. Saffarian S., Cocucci E., Kirchhausen T. Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol. 2009, 7(9):e1000191.
40. Schmitz C., Marchant D., Neil S.J., Aubin K., Reuter S., Dittmar M.T., McKnight A. Lv2, a novel postentry restriction, is mediated by both capsid and envelope. J. Virol. 2004, 78(4):2006-2016.
41. Schwartz O., Marechal V., Friguet B., Arenzana-Seisdedos F., Heard J.M. Antiviral activity of the proteasome on incoming human immunodeficiency virus type 1. J. Virol. 1998, 72(5):3845-3850.
42. Smythe E., Ayscough K.R. Actin regulation in endocytosis. J. Cell Sci. 2006, 119(Pt 22):4589-4598.
43. Soneoka Y., Cannon P.M., Ramsdale E.E., Griffiths J.C., Romano G., Kingsman S.M., Kingsman A.J. A transient three-plasmid expression system for the production of high titer retroviral vectors. Nucleic Acids Res. 1995, 23(4):628-633.
44. Sun X., Yau V.K., Briggs B.J., Whittaker G.R. Role of clathrin-mediated endocytosis during vesicular stomatitis virus entry into host cells. Virology 2005, 338(1):53-60.
45. Taunton J. Actin filament nucleation by endosomes, lysosomes and secretory vesicles. Curr. Opin. Cell Biol. 2001, 13(1):85-91.
46. Thomas E.R., Shotton C., Weiss R.A., Clapham P.R., McKnight A. CD4-dependent and CD4-independent HIV-2: consequences for neutralization. AIDS 2003, 17(3):291-300.
47. Uratsuji Y., Nakanishi H., Takeyama Y., Kishimoto A., Nishizuka Y. Activation of cellular protein kinase C and mode of inhibitory action of phospholipid-interacting compounds. Biochem. Biophys. Res. Commun. 1985, 130(2):654-661.
48. Wei B.L., Denton P.W., O'Neill E., Luo T., Foster J.L., Garcia J.V. Inhibition of lysosome and proteasome function enhances human immunodeficiency virus type 1 infection. J. Virol. 2005, 79(9):5705-5712.
49. Wrenn R.W., Katoh N., Schatzman R.C., Kuo J.F. Inhibition by phenothiazine antipsychotic drugs of calcium-dependent phosphorylation of cerebral cortex proteins regulated by phospholipid or calmodulin. Life Sci. 1981, 29(7):725-733.
50. Yan Y., Kozak C.A. Novel postentry resistance to AKV ecotropic mouse gammaretroviruses in the African pygmy mouse, Mus minutoides. J. Virol. 2008, 82(13):6120-6129.
51. Yoder A., Yu D., Dong L., Iyer S.R., Xu X., Kelly J., Liu J., Wang W., Vorster P.J., Agulto L., Stephany D.A., Cooper J.N., Marsh J.W., Wu Y. HIV envelope-CXCR4 signaling activates cofilin to overcome cortical actin restriction in resting CD4 T cells. Cell 2008, 134(5):782-792.
52. Zhou T., Han Y., Dang Y., Wang X., Zheng Y.H. A novel HIV-1 restriction factor that is biologically distinct from APOBEC3 cytidine deaminases in a human T cell line CEM.NKR. Retrovirology 2009, 6(1):31.