Productive entry of HIV-1 during cell-to-cell transmission via dynamin-dependent endocytosis

Journal of Virology

Volumn 87, Issue 14, 2013, Pages 8110-8123

  Sloan, Richard D ^a,d   Kuhl, Björn D ^a,b   Mesplède, Thibault ^a   Münch, Jan ^c   Donahue, Daniel A ^a,b   Wainberga, Mark A ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF ULM   (Germany)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; CLATHRIN; DYNAMIN II; PROTEIN AP180; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RECEPTOR;

ANTIGEN BINDING; ARTICLE; CD4+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MEMBRANE BINDING; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; SENSITIVITY ANALYSIS; VIRUS ENTRY; VIRUS TRANSMISSION;

CD4-POSITIVE T-LYMPHOCYTES; DYNAMINS; ENDOCYTOSIS; HEK293 CELLS; HIV INFECTIONS; HIV-1; HUMANS; JURKAT CELLS; LEUKOCYTES, MONONUCLEAR; MODELS, BIOLOGICAL; MONOMERIC CLATHRIN ASSEMBLY PROTEINS; RNA INTERFERENCE; VIRUS INTERNALIZATION;

EID: 84880276534     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00815-13     Document Type: Article

References (72)

1. Chen P, Hübner W, Spinelli MA, Chen BK. 2007. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J. Virol. 81:12582-12595.
2. Murooka TT, Deruaz M, Marangoni F, Vrbanac VD, Seung E, von Andrian UH, Tager AM, Luster AD, Mempel TR. 2012. HIV-infected T cells are migratory vehicles for viral dissemination. Nature 490:283-287.
3. Grakoui A, Bromley SK, Sumen C, Davis MM, Shaw AS, Allen PM, Dustin ML. 1999. The immunological synapse: a molecular machine controlling T cell activation. Science 285:221-227.
4. Igakura T, Stinchcombe JC, Goon PK, Taylor GP, Weber JN, Griffiths GM, Tanaka Y, Osame M, Bangham CR. 2003. Spread of HTLV-I between lymphocytes by virus-induced polarization of the cytoskeleton. Science 299:1713-1716.
5. Jolly C, Kashefi K, Hollinshead M, Sattentau QJ. 2004. HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J. Exp. Med. 199:283-293.
6. Rudnicka D, Feldmann J, Porrot F, Wietgrefe S, Guadagnini S, Prévost MC, Estaquier J, Haase AT, Sol-Foulon N, Schwartz O. 2009. Simultaneous cell-to-cell transmission of human immunodeficiency virus to multiple targets through polysynapses. J. Virol. 83:6234-6246.
7. Groot F, Welsch S, Sattentau QJ. 2008. Efficient HIV-1 transmission from macrophages to T cells across transient virological synapses. Blood 111:4660-4663.
8. Sowinski S, Jolly C, Berninghausen O, Purbhoo MA, Chauveau A, Köhler K, Oddos S, Eissmann P, Brodsky FM, Hopkins C, Onfelt B, Sattentau Q, Davis DM. 2008. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat. Cell Biol. 10:211-219.
9. Lehmann MJ, Sherer NM, Marks CB, Pypaert M, Mothes W. 2005. Actin-and myosin-driven movement of viruses along filopodia precedes their entry into cells. J. Cell Biol. 170:317-325.
10. Sherer NM, Lehmann MJ, Jimenez-Soto LF, Horensavitz C, Pypaert M, Mothes W. 2007. Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat. Cell Biol. 9:310-315.
11. Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littman DR, Figdor CG, van Kooyk Y. 2000. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100: 587-597.
12. Dale BM, Alvarez RA, Chen BK. 2013. Mechanisms of enhanced HIV spread through T-cell virological synapses. Immunol. Rev. 251:113-124.
13. Sattentau QJ. 2010. Cell-to-cell spread of retroviruses. Viruses 2:1306-1321.
14. Jolly C, Mitar I, Sattentau QJ. 2007. Requirement for an intact T-cell actin and tubulin cytoskeleton for efficient assembly and spread of human immunodeficiency virus type 1. J. Virol. 81:5547-5560.
15. Jolly C, Sattentau QJ. 2005. Human immunodeficiency virus type 1 virological synapse formation in T cells requires lipid raft integrity. J. Virol. 79:12088-12094.
16. Jolly C, Mitar I, Sattentau QJ. 2007. Adhesion molecule interactions facilitate human immunodeficiency virus type 1-induced virological synapse formation between T cells. J. Virol. 81:13916-13921.
17. Jolly C, Sattentau QJ. 2007. Human immunodeficiency virus type 1 assembly, budding, and cell-cell spread in T cells take place in tetraspaninenriched plasma membrane domains. J. Virol. 81:7873-7884.
18. Sol-Foulon N, Sourisseau M, Porrot F, Thoulouze MI, Trouillet C, Nobile C, Blanchet F, di Bartolo V, Noraz N, Taylor N, Alcover A, Hivroz C, Schwartz O. 2007. ZAP-70 kinase regulates HIV cell-to-cell spread and virological synapse formation. EMBO J. 26:516-526.
19. + T cells contributes to human immunodeficiency virus type-1 cell-to-cell spread at the virological synapse. PLoS Pathog. 7:e1002226. doi:10.1371/journal.ppat.1002226.
20. Martin N, Welsch S, Jolly C, Briggs J, Vaux D, Sattentau Q. 2010. Virological synapse-mediated spread of human immunodeficiency virus type 1 between T cells is sensitive to entry inhibition. J. Virol. 84:3516-3527.
21. Hübner W, McNerney GP, Chen P, Dale BM, Gordon RE, Chuang FY, Li XD, Asmuth DM, Huser T, Chen BK. 2009. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323:1743-1747.
22. Bosch B, Grigorov B, Senserrich J, Clotet B, Darlix JL, Muriaux D, Este JA. 2008. A clathrin-dynamin-dependent endocytic pathway for the uptake of HIV-1 by direct T cell-T cell transmission. Antiviral Res. 80:185-193.
23. Schaeffer E, Soros VB, Greene WC. 2004. Compensatory link between fusion and endocytosis of human immunodeficiency virus type 1 in human CD4 T lymphocytes. J. Virol. 78:1375-1383.
24. Dale BM, McNerney GP, Thompson DL, Hubner W, de Los Reyes K, Chuang FY, Huser T, Chen BK. 2011. Cell-to-cell transfer of HIV-1 via virological synapses leads to endosomal virion maturation that activates viral membrane fusion. Cell Host Microbe 10:551-562.
25. Daecke J, Fackler OT, Dittmar MT, Kräusslich HG. 2005. Involvement of clathrin-mediated endocytosis in human immunodeficiency virus type 1 entry. J. Virol. 79:1581-1594.
26. de la Vega M, Marin M, Kondo N, Miyauchi K, Kim Y, Epand RF, Epand RM, Melikyan GB. 2011. Inhibition of HIV-1 endocytosis allows lipid mixing at the plasma membrane, but not complete fusion. Retrovirology 8:99. doi:10.1186/1742-4690-8-99.
27. Fackler OT, Peterlin BM. 2000. Endocytic entry of HIV-1. Curr. Biol. 10:1005-1008.
28. Miyauchi K, Kim Y, Latinovic O, Morozov V, Melikyan GB. 2009. HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 137:433-444.
29. von Kleist L, Stahlschmidt W, Bulut H, Gromova K, Puchkov D, Robertson MJ, Macgregor KA, Tomlin N, Pechstein A, Chau N, Chircop M, Sakoff J, von Kries JP, Saenger W, Kräusslich HG, Shupliakov O, Robinson PJ, McCluskey A, Haucke V. 2011. Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell 146:471-484.
30. Griffiths GM, Tsun A, Stinchcombe JC. 2010. The immunological synapse: a focal point for endocytosis and exocytosis. J. Cell Biol. 189:399-406.
31. Schindler M, Münch J, Kirchhoff F. 2005. Human immunodeficiency virus type 1 inhibits DNA damage-triggered apoptosis by a Nefindependent mechanism. J. Virol. 79:5489-5498.
32. Kuhl BD, Sloan RD, Donahue DA, Bar-Magen T, Liang C, Wainberg MA. 2010. Tetherin restricts direct cell-to-cell infection of HIV-1. Retrovirology 7:115. doi:10.1186/1742-4690-7-115.
33. Maréchal V, Clavel F, Heard JM, Schwartz O. 1998. Cytosolic Gag p24 as an index of productive entry of human immunodeficiency virus type 1. J. Virol. 72:2208-2212.
34. Münch J, Rücker E, Ständker L, Adermann K, Goffinet C, Schindler M, Wildum S, Chinnadurai R, Rajan D, Specht A, Giménez-Gallego G, Sànchez PC, Fowler DM, Koulov A, Kelly JW, Mothes W, Grivel JC, Margolis L, Keppler OT, Forssmann WG, Kirchhoff F. 2007. Semenderived amyloid fibrils drastically enhance HIV infection. Cell 131:1059-1071.
35. Schindler M, Münch J, Kutsch O, Li H, Santiago M, Bibollet-Ruche F, Müller-Trutwin M, Novembre F, Peeters M, Courgnaud V, Bailes E, Roques P, Sodora D, Silvestri G, Sharp P, Hahn B, Kirchhoff F. 2006. Nef-mediated suppression of T cell activation was lost in a lentiviral lineage that gave rise to HIV-1. Cell 125:1055-1067.
36. Blanco J, Bosch B, Fernàndez-Figueras MT, Barretina J, Clotet B, Esté JA. 2004. High level of coreceptor-independent HIV transfer induced by contacts between primary CD4 T cells. J. Biol. Chem. 279:51305-51314.
37. Schader SM, Colby-Germinario SP, Quashie PK, Oliveira M, Ibanescu RI, Moisi D, Mespléde T, Wainberg MA. 2012. HIV gp120 H375 is unique to HIV-1 subtype CRF01_AE and confers strong resistance to the entry inhibitor BMS-599793, a candidate microbicide drug. Antimicrob. Agents Chemother. 56:4257-4267.
38. Ferguson SM, De Camilli P. 2012. Dynamin, a membrane-remodelling GTPase. Nat. Rev. Mol. Cell Biol. 13:75-88.
39. Carter GC, Bernstone L, Baskaran D, James W. 2011. HIV-1 infects macrophages by exploiting an endocytic route dependent on dynamin, Rac1 and Pak1. Virology 409:234-250.
40. Pritschet K, Donhauser N, Schuster P, Ries M, Haupt S, Kittan NA, Korn K, Pöhlmann S, Holland G, Bannert N, Bogner E, Schmidt B. 2012. CD4-and dynamin-dependent endocytosis of HIV-1 into plasmacytoid dendritic cells. Virology 423:152-164.
41. Joshi S, Braithwaite AW, Robinson PJ, Chircop M. 2011. Dynamin inhibitors induce caspase-mediated apoptosis following cytokinesis fail-ure in human cancer cells and this is blocked by Bcl-2 overexpression. Mol. Cancer 10:78.
42. Quan A, McGeachie AB, Keating DJ, van Dam EM, Rusak J, Chau N, Malladi CS, Chen C, McCluskey A, Cousin MA, Robinson PJ. 2007. Myristyl trimethyl ammonium bromide and octadecyl trimethyl ammonium bromide are surface-active small molecule dynamin inhibitors that block endocytosis mediated by dynamin I or dynamin II. Mol. Pharmacol. 72:1425-1439.
43. Engel S, Heger T, Mancini R, Herzog F, Kartenbeck J, Hayer A, Helenius A. 2011. Role of endosomes in simian virus 40 entry and infection. J. Virol. 85:4198-4211.
44. Fra AM, Williamson E, Simons K, Parton RG. 1994. Detergentinsoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J. Biol. Chem. 269:30745-30748.
45. Harris J, Werling D, Hope JC, Taylor G, Howard CJ. 2002. Caveolae and caveolin in immune cells: distribution and functions. Trends Immunol. 23:158-164.
46. Hatanaka M, Maeda T, Ikemoto T, Mori H, Seya T, Shimizu A. 1998. Expression of caveolin-1 in human T cell leukemia cell lines. Biochem. Biophys. Res. Commun. 253:382-387.
47. Vallejo J, Hardin CD. 2005. Expression of caveolin-1 in lymphocytes induces caveolae formation and recruitment of phosphofructokinase to the plasma membrane. FASEB J. 19:586-587.
48. McMahon HT, Boucrot E. 2011. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12:517-533.
49. Ivanov AI. 2008. Pharmacological inhibition of endocytic pathways: is it specific enough to be useful? Methods Mol. Biol. 440:15-33.
50. Heuser JE, Anderson RG. 1989. Hypertonic media inhibit receptormediated endocytosis by blocking clathrin-coated pit formation. J. Cell Biol. 108:389-400.
51. von Kleist L, Haucke V. 2012. At the crossroads of chemistry and cell biology: inhibiting membrane traffic by small molecules. Traffic 13:495-504.
52. Fredericksen BL, Wei BL, Yao J, Luo T, Garcia JV. 2002. Inhibition of endosomal/lysosomal degradation increases the infectivity of human immunodeficiency virus. J. Virol. 76:11440-11446.
53. Wei BL, Denton PW, O'Neill E, Luo T, Foster JL, Garcia JV. 2005. Inhibition of lysosome and proteasome function enhances human immunodeficiency virus type 1 infection. J. Virol. 79:5705-5712.
54. Bayer N, Schober D, Prchla E, Murphy RF, Blaas D, Fuchs R. 1998. Effect of bafilomycin A1 and nocodazole on endocytic transport in HeLa cells: implications for viral uncoating and infection. J. Virol. 72:9645-9655.
55. + T-cell clone (PM1): failure to downregulate CD4 and to interfere with cell-line-tropic HIV-1. J. Virol. 69:3712-3720.
56. Anantharam A, Bittner MA, Aikman RL, Stuenkel EL, Schmid SL, Axelrod D, Holz RW. 2011. A new role for the dynamin GTPase in the regulation of fusion pore expansion. Mol. Biol. Cell 22:1907-1918.
57. Sun Y, Tien P. 2013. From endocytosis to membrane fusion: emerging roles of dynamin in virus entry. Crit. Rev. Microbiol. 39:166-179.
58. Liu L, Oliveira NM, Cheney KM, Pade C, Dreja H, Bergin AM, Borgdorff V, Beach DH, Bishop CL, Dittmar MT, McKnight A. 2011. A whole genome screen for HIV restriction factors. Retrovirology 8:94. doi: 10.1186/1742-4690-8-94.
59. Harrison IP, McKnight A. 2011. Cellular entry via an actin and clathrindependent route is required for Lv2 restriction of HIV-2. Virology 415: 47-55.
60. Lu J, Pan Q, Rong L, He W, Liu SL, Liang C. 2011. The IFITM proteins inhibit HIV-1 infection. J. Virol. 85:2126-2137.
61. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM. 2011. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472:481-485.
62. Del Portillo A, Tripodi J, Najfeld V, Wodarz D, Levy DN, Chen BK. 2011. Multiploid inheritance of HIV-1 during cell-to-cell infection. J. Virol. 85:7169-7176.
63. Gobeil LA, Lodge R, Tremblay MJ. 2013. Macropinocytosis-like HIV-1 internalization in macrophages is CCR5-dependent and leads to efficient but delayed degradation in endosomal compartments. J. Virol. 87:735-745.
64. Permanyer M, Ballana E, Esté JA. 2010. Endocytosis of HIV: anything goes. Trends Microbiol. 18:543-551.
65. Zhong P, Agosto LM, Ilinskaya A, Dorjbal B, Truong R, Derse D, Uchil PD, Heidecker G, Mothes W. 2013. Cell-to-cell transmission can overcome multiple donor and target cell barriers imposed on cell-free HIV. PLoS One 8:e53138. doi:10.1371/journal.pone.0053138.
66. Maréchal V, Prevost MC, Petit C, Perret E, Heard JM, Schwartz O. 2001. Human immunodeficiency virus type 1 entry into macrophages mediated by macropinocytosis. J. Virol. 75:11166-11177.
67. Gobeil LA, Lodge R, Tremblay MJ. 2012. Differential HIV-1 endocytosis and susceptibility to virus infection in human macrophages correlate with the cell activation status. J. Virol. 86:10399-10407.
68. Vasiliver-Shamis G, Dustin ML, Hioe CE. 2010. HIV-1 virological synapse is not simply a copycat of the immunological synapse. Viruses 2:1239-1260.
69. Davis DM. 2007. Intercellular transfer of cell-surface proteins is common and can affect many stages of an immune response. Nat. Rev. Immunol. 7:238-243.
70. Abela IA, Berlinger L, Schanz M, Reynell L, Günthard HF, Rusert P, Trkola A. 2012. Cell-cell transmission enables HIV-1 to evade inhibition by potent CD4bs directed antibodies. PLoS Pathog. 8:e1002634. doi:10.1371/journal.ppat.1002634.
71. Durham ND, Yewdall AW, Chen P, Lee R, Zony C, Robinson JE, Chen BK. 2012. Neutralization resistance of virological synapse-mediated HIV-1 infection is regulated by the gp41 cytoplasmic tail. J. Virol. 86: 7484-7495.
72. Massanella M, Puigdomènech I, Cabrera C, Fernandez-Figueras MT, Aucher A, Gaibelet G, Hudrisier D, García E, Bofill M, Clotet B, Blanco J. 2009. Anti-gp41 antibodies fail to block early events of virological synapses but inhibit HIV spread between T cells. AIDS 23:183-188.