Virus cell-to-cell transmission

Journal of Virology

Volumn 84, Issue 17, 2010, Pages 8360-8368

  Mothes, Walther ^a   Sherer, Nathan M ^b   Jin, Jing ^a   Zhong, Peng ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; CLAUDIN 1; INTERCELLULAR ADHESION MOLECULE 1; OCCLUDIN; UVOMORULIN;

ANTIGEN PRESENTING CELL; CELL ADHESION; CELL CONTACT; HEPATITIS C VIRUS; HERPES VIRUS; HUMAN IMMUNODEFICIENCY VIRUS; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PRIORITY JOURNAL; RETROVIRUS; REVIEW; T LYMPHOCYTE; TIGHT JUNCTION; VIRION; VIRUS ENTRY; VIRUS INFECTION; VIRUS TRANSMISSION; ANIMAL; DISEASE TRANSMISSION; VIRAL PHENOMENA AND FUNCTIONS; VIROLOGY; VIRUS RELEASE;

ANIMALS; VIRUS DISEASES; VIRUS INTERNALIZATION; VIRUS PHYSIOLOGICAL PHENOMENA; VIRUS RELEASE;

EID: 77956643036     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00443-10     Document Type: Review

References (138)

1. Abe, K., O. Chisaka, F. Van Roy, and M. Takeichi. 2004. Stability of dendritic spines and synaptic contacts is controlled by alpha N-catenin. Nat. Neurosci. 7:357-363.
2. Agosto, L. M., J. J. Yu, M. K. Liszewski, C. Baytop, N. Korokhov, L. M. Humeau, and U. O'Doherty. 2009. The CXCR4-tropic human immunode- ficiency virus envelope promotes more-efficient gene delivery to resting CD4+ T cells than the vesicular stomatitis virus glycoprotein G envelope. J. Virol. 83:8153-8162.
3. Akins, M. R., and T. Biederer. 2006. Cell-cell interactions in synaptogenesis. Curr. Opin. Neurobiol. 16:83-89.
4. Alfsen, A., H. Yu, A. Magerus-Chatinet, A. Schmitt, and M. Bomsel. 2005. HIV-1-infected blood mononuclear cells form an integrin- and agrin-dependent viral synapse to induce efficient HIV-1 transcytosis across epithelial cell monolayer. Mol. Biol. Cell 16:4267-4279.
5. Arhel, N., M. Lehmann, K. Clauss, G. U. Nienhaus, V. Piguet, and F. Kirchhoff. 2009. The inability to disrupt the immunological synapse between infected human T cells and APCs distinguishes HIV-1 from most other primate lentiviruses. J. Clin. Invest. 119:2965-2975.
6. Azar, G. A., F. Lemaitre, E. A. Robey, and P. Bousso. 2010. Subcellular dynamics of T cell immunological synapses and kinapses in lymph nodes. Proc. Natl. Acad. Sci. U. S. A. 107:3675-3680.
7. Balabanian, K., J. Harriague, C. Decrion, B. Lagane, S. Shorte, F. Baleux, J. L. Virelizier, F. Arenzana-Seisdedos, and L. A. Chakrabarti. 2004. CXCR4-tropic HIV-1 envelope glycoprotein functions as a viral chemokine in unstimulated primary CD4+ T lymphocytes. J. Immunol. 173:7150-7160.
8. Balfe, P., and J. A. McKeating. 2009. The complexities of hepatitis C virus entry. J. Hepatol. 51:609-611.
9. Bangham, C. R. 2003. The immune control and cell-to-cell spread of human T-lymphotropic virus type 1. J. Gen. Virol. 84:3177-3189.
10. Barcia, C., N. S. Sanderson, R. J. Barrett, K. Wawrowsky, K. M. Kroeger, M. Puntel, C. Liu, M. G. Castro, and P. R. Lowenstein. 2008. T cells' immunological synapses induce polarization of brain astrocytes in vivo and in vitro: a novel astrocyte response mechanism to cellular injury. PLoS One 3:e2977.
11. Barton, E. S., J. C. Forrest, J. L. Connolly, J. D. Chappell, Y. Liu, F. J. Schnell, A. Nusrat, C. A. Parkos, and T. S. Dermody. 2001. Junction adhesion molecule is a receptor for reovirus. Cell 104:441-451.
12. Bennett, A. E., K. Narayan, D. Shi, L. M. Hartnell, K. Gousset, H. He, B. C. Lowekamp, T. S. Yoo, D. Bliss, E. O. Freed, and S. Subramaniam. 2009. Ion-abrasion scanning electron microscopy reveals surface-connected tubular conduits in HIV-infected macrophages. PLoS Pathog. 5:e1000591.
13. Biederer, T., Y. Sara, M. Mozhayeva, D. Atasoy, X. Liu, E. T. Kavalali, and T. C. Sudhof. 2002. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297:1525-1531.
14. Black, F. L., and J. L. Melnick. 1955. Microepidemiology of poliomyelitis and herpes-B infections: spread of the viruses within tissue cultures. J. Immunol. 74:236-242.
15. Boes, M., J. Cerny, R. Massol, M. Op den Brouw, T. Kirchhausen, J. Chen, and H. L. Ploegh. 2002. T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature 418:983-988.
16. Bromley, S. K., D. A. Peterson, M. D. Gunn, and M. L. Dustin. 2000. Cutting edge: hierarchy of chemokine receptor and TCR signals regulating T cell migration and proliferation. J. Immunol. 165:15-19.
17. Burckhardt, C. J., and U. F. Greber. 2009. Virus movements on the plasma membrane support infection and transmission between cells. PLoS Pathog. 5:e1000621.
18. Cameron, P. U., P. S. Freudenthal, J. M. Barker, S. Gezelter, K. Inaba, and R. M. Steinman. 1992. Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells. Science 257:383-387.
19. Chen, P., W. Hubner, M. A. Spinelli, and B. K. Chen. 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.
20. Ch'ng, T. H., and L. W. Enquist. 2005. Neuron-to-cell spread of pseudorabies virus in a compartmented neuronal culture system. J. Virol. 79:10875-10889.
21. Contento, R. L., B. Molon, C. Boularan, T. Pozzan, S. Manes, S. Marullo, and A. Viola. 2008. CXCR4-CCR5: a couple modulating T cell functions. Proc. Natl. Acad. Sci. U. S. A. 105:10101-10106.
22. Crawford, S., and S. P. Goff. 1985. A deletion mutation in the 5′ part of the pol gene of Moloney murine leukemia virus blocks proteolytic processing of the gag and pol polyproteins. J. Virol. 53:899-907.
23. Cudmore, S., P. Cossart, G. Griffiths, and M. Way. 1995. Actin-based motility of vaccinia virus. Nature 378:636-638.
24. Curanovic, D., and L. Enquist. 2009. Directional transneuronal spread of alpha-herpesvirus infection. Future Virol. 4:591.
25. Das, V., B. Nal, A. Dujeancourt, M. I. Thoulouze, T. Galli, P. Roux, A. Dautry-Varsat, and A. Alcover. 2004. Activation-induced polarized recycling targets T cell antigen receptors to the immunological synapse; involvement of SNARE complexes. Immunity 20:577-588.
26. Davis, D. M. 2009. Mechanisms and functions for the duration of intercellular contacts made by lymphocytes. Nat. Rev. Immunol. 9:543-555.
27. DeFalco, J., M. Tomishima, H. Liu, C. Zhao, X. Cai, J. D. Marth, L. Enquist, and J. M. Friedman. 2001. Virus-assisted mapping of neural inputs to a feeding center in the hypothalamus. Science 291:2608-2613.
28. De Regge, N., H. J. Nauwynck, K. Geenen, C. Krummenacher, G. H. Cohen, R. J. Eisenberg, T. C. Mettenleiter, and H. W. Favoreel. 2006. Alphaherpesvirus glycoprotein D interaction with sensory neurons triggers formation of varicosities that serve as virus exit sites. J. Cell Biol. 174:267-275.
29. Dimitrov, D. S., R. L. Willey, H. Sato, L. J. Chang, R. Blumenthal, and M. A. Martin. 1993. Quantitation of human immunodeficiency virus type 1 infection kinetics. J. Virol. 67:2182-2190.
30. Doceul, V., M. Hollinshead, L. van der Linden, and G. L. Smith. 2010. Repulsion of superinfecting virions: a mechanism for rapid virus spread. Science 327:873-876.
31. Dupin, I., E. Camand, and S. Etienne-Manneville. 2009. Classical cadherins control nucleus and centrosome position and cell polarity. J. Cell Biol. 185:779-786.
32. Eugenin, E. A., P. J. Gaskill, and J. W. Berman. 2009. Tunneling nanotubes (TNT) are induced by HIV-infection of macrophages: a potential mechanism for intercellular HIV trafficking. Cell Immunol. 254:142-148.
33. Evans, M. J., T. von Hahn, D. M. Tscherne, A. J. Syder, M. Panis, B. Wolk, T. Hatziioannou, J. A. McKeating, P. D. Bieniasz, and C. M. Rice. 2007. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446:801-805.
34. Fackler, O. T., A. Alcover, and O. Schwartz. 2007. Modulation of the immunological synapse: a key to HIV-1 pathogenesis? Nat. Rev. Immunol. 7:310-317.
35. Fiala, J. C., M. Feinberg, V. Popov, and K. M. Harris. 1998. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J. Neurosci. 18:8900-8911.
36. Finlay, B. B., and P. Cossart. 1997. Exploitation of mammalian host cell functions by bacterial pathogens. Science 276:718-725.
37. Frischknecht, F., V. Moreau, S. Rottger, S. Gonfloni, I. Reckmann, G. Superti-Furga, and M. Way. 1999. Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401:926-929.
38. Fukudome, K., M. Furuse, N. Fukuhara, S. Orita, T. Imai, S. Takagi, M. Nagira, Y. Hinuma, and O. Yoshie. 1992. Strong induction of ICAM-1 in human T cells transformed by human T-cell-leukemia virus type 1 and depression of ICAM-1 or LFA-1 in adult T-cell-leukemia-derived cell lines. Int. J. Cancer. 52:418-427.
39. Ganesh, L., K. Leung, K. Lore, R. Levin, A. Panet, O. Schwartz, R. A. Koup, and G. J. Nabel. 2004. Infection of specific dendritic cells by CCR5-tropic human immunodeficiency virus type 1 promotes cell-mediated transmission of virus resistant to broadly neutralizing antibodies. J. Virol. 78:11980-11987.
40. Geijtenbeek, T. B., D. S. Kwon, R. Torensma, S. J. van Vliet, G. C. van Duijnhoven, J. Middel, I. L. Cornelissen, H. S. Nottet, V. N. KewalRamani, D. R. Littman, C. G. Figdor, and Y. van Kooyk. 2000. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100:587-597.
41. Gerdes, H. H., and R. N. Carvalho. 2008. Intercellular transfer mediated by tunneling nanotubes. Curr. Opin. Cell Biol. 20:470-475.
42. Golovkina, T. V., A. Chervonsky, J. P. Dudley, and S. R. Ross. 1992. Transgenic mouse mammary tumor virus superantigen expression prevents viral infection. Cell 69:637-645.
43. Gousset, K., S. D. Ablan, L. V. Coren, A. Ono, F. Soheilian, K. Nagashima, D. E. Ott, and E. O. Freed. 2008. Real-time visualization of HIV-1 GAG trafficking in infected macrophages. PLoS Pathog. 4:e1000015.
44. Grakoui, A., S. K. Bromley, C. Sumen, M. M. Davis, A. S. Shaw, P. M. Allen, and M. L. Dustin. 1999. The immunological synapse: a molecular machine controlling T cell activation. Science 285:221-227. (Pubitemid 29329988)
45. Green, N., T. M. Shinnick, O. Witte, A. Ponticelli, J. G. Sutcliffe, and R. A. Lerner. 1981. Sequence-specific antibodies show that maturation of Moloney leukemia virus envelope polyprotein involves removal of a COOHterminal peptide. Proc. Natl. Acad. Sci. U. S. A. 78:6023-6027.
46. Gummuluru, S., C. M. Kinsey, and M. Emerman. 2000. An in vitro rapidturnover assay for human immunodeficiency virus type 1 replication selects for cell-to-cell spread of virus. J. Virol. 74:10882-10891.
47. Gupta, P., R. Balachandran, M. Ho, A. Enrico, and C. Rinaldo. 1989. Cell-to-cell transmission of human immunodeficiency virus type 1 in the presence of azidothymidine and neutralizing antibody. J. Virol. 63:2361-2365.
48. Held, W., G. A. Waanders, A. N. Shakhov, L. Scarpellino, H. Acha-Orbea, and H. R. MacDonald. 1993. Superantigen-induced immune stimulation amplifies mouse mammary tumor virus infection and allows virus transmission. Cell 74:529-540.
49. Hioe, C. E., P. C. Chien, Jr., C. Lu, T. A. Springer, X. H. Wang, J. Bandres, and M. Tuen. 2001. LFA-1 expression on target cells promotes human immunodeficiency virus type 1 infection and transmission. J. Virol. 75: 1077-1082.
50. Huang, B., S. A. Jones, B. Brandenburg, and X. Zhuang. 2008. Whole-cell 3D STORM reveals interactions between cellular structures with nanometer- scale resolution. Nat. Methods 5:1047-1052.
51. Hubner, W., G. P. McNerney, P. Chen, B. M. Dale, R. E. Gordon, F. Y. Chuang, X. D. Li, D. M. Asmuth, T. Huser, and B. K. Chen. 2009. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323:1743-1747.
52. Huppa, J. B., and M. M. Davis. 2003. T-cell-antigen recognition and the immunological synapse. Nat. Rev. Immunol. 3:973-983.
53. Igakura, T., J. C. Stinchcombe, P. K. Goon, G. P. Taylor, J. N. Weber, G. M. Griffiths, Y. Tanaka, M. Osame, and C. R. Bangham. 2003. Spread of HTLV-I between lymphocytes by virus-induced polarization of the cytoskeleton. Science 299:1713-1716.
54. Iwasaki, Y., and H. F. Clark. 1975. Cell to cell transmission of virus in the central nervous system. II. Experimental rabies in mouse. Lab. Invest. 33:391-399.
55. Jin, J., N. Sherer, and W. Mothes. 2010. Surface transmission or polarized egress? Lessons learned from HTLV cell-to-cell transmission. Viruses 2:601-605.
56. Jin, J., N. M. Sherer, G. Heidecker, D. Derse, and W. Mothes. 2009. Assembly of the murine leukemia virus is directed towards sites of cell-cell contact. PLoS Biol. 7:e1000163.
57. Johnson, D. C., and M. T. Huber. 2002. Directed egress of animal viruses promotes cell-to-cell spread. J. Virol. 76:1-8.
58. Jolly, C., K. Kashefi, M. Hollinshead, and Q. J. Sattentau. 2004. HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J. Exp. Med. 199:283-293.
59. Jolly, C., I. Mitar, and Q. J. Sattentau. 2007. Adhesion molecule interactions facilitate human immunodeficiency virus type 1-induced virological synapse formation between T cells. J. Virol. 81:13916-13921.
60. Jolly, C., and Q. J. Sattentau. 2004. Retroviral spread by induction of virological synapses. Traffic 5:643-650.
61. Jones, C. T., M. T. Catanese, L. M. Law, S. R. Khetani, A. J. Syder, A. Ploss, T. S. Oh, J. W. Schoggins, M. R. Macdonald, S. N. Bhatia, and C. M. Rice. 2010. Real-time imaging of hepatitis C virus infection using a fluorescent cell-based reporter system. Nat. Biotechnol. 28:167-171.
62. Jouvenet, N., M. Windsor, J. Rietdorf, P. Hawes, P. Monaghan, M. Way, and T. Wileman. 2006. African swine fever virus induces filopodia-like projections at the plasma membrane. Cell Microbiol. 8:1803-1811.
63. Kaizuka, Y., A. D. Douglass, R. Varma, M. L. Dustin, and R. D. Vale. 2007. Mechanisms for segregating T cell receptor and adhesion molecules during immunological synapse formation in Jurkat T cells. Proc. Natl. Acad. Sci. U. S. A. 104:20296-20301.
64. Knott, G. W., A. Holtmaat, L. Wilbrecht, E. Welker, and K. Svoboda. 2006. Spine growth precedes synapse formation in the adult neocortex in vivo. Nat. Neurosci. 9:1117-1124.
65. Kuhn, J. R., and M. Poenie. 2002. Dynamic polarization of the microtubule cytoskeleton during CTL-mediated killing. Immunity 16:111-121.
66. Kupfer, A., G. Dennert, and S. J. Singer. 1983. Polarization of the Golgi apparatus and the microtubule-organizing center within cloned natural killer cells bound to their targets. Proc. Natl. Acad. Sci. U. S. A. 80:7224-7228.
67. Lawrence, D. M., C. E. Patterson, T. L. Gales, J. L. D'Orazio, M. M. Vaughn, and G. F. Rall. 2000. Measles virus spread between neurons requires cell contact but not CD46 expression, syncytium formation, or extracellular virus production. J. Virol. 74:1908-1918.
68. Lehmann, M. J., N. M. Sherer, C. B. Marks, M. Pypaert, and W. Mothes. 2005. Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J. Cell Biol. 170:317-325.
69. Lidke, D. S., K. A. Lidke, B. Rieger, T. M. Jovin, and D. J. Arndt-Jovin. 2005. Reaching out for signals: filopodia sense EGF and respond by directed retrograde transport of activated receptors. J. Cell Biol. 170:619-626.
70. Lidke, D. S., P. Nagy, R. Heintzmann, D. J. Arndt-Jovin, J. N. Post, H. E. Grecco, E. A. Jares-Erijman, and T. M. Jovin. 2004. Quantum dot ligands provide new insights into erbB/HER receptor-mediated signal transduction. Nat. Biotechnol. 22:198-203.
71. Loewy, A. D. 1998. Viruses as transneuronal tracers for defining neural circuits. Neurosci. Biobehav Rev. 22:679-684.
72. Ludford-Menting, M. J., J. Oliaro, F. Sacirbegovic, E. T. Cheah, N. Pedersen, S. J. Thomas, A. Pasam, R. Iazzolino, L. E. Dow, N. J. Waterhouse, A. Murphy, S. Ellis, M. J. Smyth, M. H. Kershaw, P. K. Darcy, P. O. Humbert, and S. M. Russell. 2005. A network of PDZ-containing proteins regulates T cell polarity and morphology during migration and immunological synapse formation. Immunity 22:737-748.
73. Majorovits, E., M. Nejmeddine, Y. Tanaka, G. P. Taylor, S. D. Fuller, and C. R. Bangham. 2008. Human T-lymphotropic virus-1 visualized at the virological synapse by electron tomography. PLoS One 3:e2251.
74. Martin, N., S. Welsch, C. Jolly, J. A. Briggs, D. Vaux, and Q. J. Sattentau. 2010. Virological synapse-mediated spread of human immunodeficiency virus type 1 between T cells is sensitive to entry inhibition. J. Virol. 84: 3516-3527.
75. Martin-Cofreces, N. B., J. Robles-Valero, J. R. Cabrero, M. Mittelbrunn, M. Gordon-Alonso, C. H. Sung, B. Alarcon, J. Vazquez, and F. Sanchez-Madrid. 2008. MTOC translocation modulates IS formation and controls sustained T cell signaling. J. Cell Biol. 182:951-962.
76. Masurier, C., B. Salomon, N. Guettari, C. Pioche, F. Lachapelle, M. Guigon, and D. Klatzmann. 1998. Dendritic cells route human immunodeficiency virus to lymph nodes after vaginal or intravenous administration to mice. J. Virol. 72:7822-7829.
77. Mazurov, D., A. Ilinskaya, G. Heidecker, P. A. Lloyed, and D. Derse. 2010. Quantitative comparison of HTLV-1 and HIV-1cell-to-cell infection with new replication dependent vectors. PLoS Pathog. 6:e1000788.
78. McCarthy, K. M., D. W. Tank, and L. W. Enquist. 2009. Pseudorabies virus infection alters neuronal activity and connectivity in vitro. PLoS Pathog. 5:e1000640.
79. McDonald, D., L. Wu, S. M. Bohks, V. N. KewalRamani, D. Unutmaz, and T. J. Hope. 2003. Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science 300:1295-1297.
80. Medeiros, N. A., D. T. Burnette, and P. Forscher. 2006. Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat. Cell Biol. 8:215-226.
81. Mercer, J., and A. Helenius. 2008. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320:531-535.
82. Merz, D. C., A. Scheid, and P. W. Choppin. 1980. Importance of antibodies to the fusion glycoprotein of paramyxoviruses in the prevention of spread of infection. J. Exp. Med. 151:275-288.
83. Molon, B., G. Gri, M. Bettella, C. Gomez-Mouton, A. Lanzavecchia, A. C. Martinez, S. Manes, and A. Viola. 2005. T cell costimulation by chemokine receptors. Nat. Immunol. 6:465-471.
84. Monks, C. R., B. A. Freiberg, H. Kupfer, N. Sciaky, and A. Kupfer. 1998. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395:82-86.
85. Munch, J., E. Rucker, L. Standker, K. Adermann, C. Goffinet, M. Schindler, S. Wildum, R. Chinnadurai, D. Rajan, A. Specht, G. Gimenez-Gallego, P. C. Sanchez, D. M. Fowler, A. Koulov, J. W. Kelly, W. Mothes, J. C. Grivel, L. Margolis, O. T. Keppler, W. G. Forssmann, and F. Kirchhoff. 2007. Semen-derived amyloid fibrils drastically enhance HIV infection. Cell 131:1059-1071.
86. Neil, S. J., S. W. Eastman, N. Jouvenet, and P. D. Bieniasz. 2006. HIV-1 Vpu promotes release and prevents endocytosis of nascent retrovirus particles from the plasma membrane. PLoS Pathog. 2:e39.
87. Neil, S. J., T. Zang, and P. D. Bieniasz. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425-430.
88. Newsome, T. P., I. Weisswange, F. Frischknecht, and M. Way. 2006. Abl collaborates with Src family kinases to stimulate actin-based motility of vaccinia virus. Cell Microbiol. 8:233-241.
89. Niell, C. M., M. P. Meyer, and S. J. Smith. 2004. In vivo imaging of synapse formation on a growing dendritic arbor. Nat. Neurosci. 7:254-260.
90. Oddos, S., C. Dunsby, M. A. Purbhoo, A. Chauveau, D. M. Owen, M. A. Neil, D. M. Davis, and P. M. French. 2008. High-speed high-resolution imaging of intercellular immune synapses using optical tweezers. Biophys. J. 95:L66-L68.
91. O'Doherty, U., W. J. Swiggard, and M. H. Malim. 2000. Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J. Virol. 74:10074-10080.
92. Pais-Correia, A. M., M. Sachse, S. Guadagnini, V. Robbiati, R. Lasserre, A. Gessain, O. Gout, A. Alcover, and M. I. Thoulouze. 2010. Biofilm-like extracellular viral assemblies mediate HTLV-1 cell-to-cell transmission at virological synapses. Nat. Med. 16:83-89.
93. Pan, Y. W., J. M. Scarlett, T. T. Luoh, and P. Kurre. 2007. Prolonged adherence of human immunodeficiency virus-derived vector particles to hematopoietic target cells leads to secondary transduction in vitro and in vivo. J. Virol. 81:639-649.
94. Perez-Caballero, D., T. Zang, A. Ebrahimi, M. W. McNatt, D. A. Gregory, M. C. Johnson, and P. D. Bieniasz. 2009. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 139:499-511.
95. Phillips, D. M. 1994. The role of cell-to-cell transmission in HIV infection. AIDS 8:719-731.
96. Piguet, V., and R. M. Steinman. 2007. The interaction of HIV with dendritic cells: outcomes and pathways. Trends Immunol. 28:503-510.
97. Platt, E. J., S. L. Kozak, J. P. Durnin, T. J. Hope, and D. Kabat. 2010. Rapid dissociation of HIV-1 from cultured cells severely limits infectivity assays, causes the inactivation ascribed to entry inhibitors, and masks the inherently high level of infectivity of virions. J. Virol. 84:3106-3110.
98. Ploss, A., M. J. Evans, V. A. Gaysinskaya, M. Panis, H. You, Y. P. de Jong, and C. M. Rice. 2009. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457:882-886.
99. Poo, W. J., L. Conrad, and C. A. Janeway, Jr. 1988. Receptor-directed focusing of lymphokine release by helper T cells. Nature 332:378-380.
100. Reeves, P. M., B. Bommarius, S. Lebeis, S. McNulty, J. Christensen, A. Swimm, A. Chahroudi, R. Chavan, M. B. Feinberg, D. Veach, W. Bornmann, M. Sherman, and D. Kalman. 2005. Disabling poxvirus pathogenesis by inhibition of Abl-family tyrosine kinases. Nat. Med. 11:731-739.
101. Rein, A., J. Mirro, J. G. Haynes, S. M. Ernst, and K. Nagashima. 1994. Function of the cytoplasmic domain of a retroviral transmembrane protein: p15E-p2E cleavage activates the membrane fusion capability of the murine leukemia virus Env protein. J. Virol. 68:1773-1781.
102. Rudnicka, D., J. Feldman, F. Porrot, S. Wietgrefe, S. Guadagnini, M. C. Prevost, J. Estaquier, A. T. Haase, N. Sol-Foulon, and O. Schwartz. 2009. Simultaneous cell-to-cell transmission of human immunodeficiency virus to multiple targets through polysynapses. J. Virol. 83:6234-6246.
103. Rudolph, J. M., N. Eickel, C. Haller, M. Schindler, and O. T. Fackler. 2009. Inhibition of T-cell receptor-induced actin remodeling and relocalization of Lck are evolutionarily conserved activities of lentiviral Nef proteins. J. Virol. 83:11528-11539.
104. Sabin, A. B. 1938. Progression of different nasally instilled viruses along different nervous pathways in the same host. Proc. Soc. Exp. Biol. Med. 38:270-275.
105. Sabin, A. B., and P. K. Olitsky. 1938. Influence of host factors on neuroinvasiveness of vesicular stomatitis virus. IV. Variations in neuroinvasiveness in different species. J. Exp. Med. 67:229-249.
106. Sainz, B., Jr., V. TenCate, and S. L. Uprichard. 2009. Three-dimensional Huh7 cell culture system for the study of Hepatitis C virus infection. Virol. J. 6:103.
107. Sanchez-Madrid, F., and J. M. Serrador. 2009. Bringing up the rear: defining the roles of the uropod. Nat. Rev. Mol. Cell Biol. 10:353-359.
108. Sattentau, Q. 2008. Avoiding the void: cell-to-cell spread of human viruses. Nat. Rev. Microbiol. 6:815-826.
109. Scheiffele, P., J. Fan, J. Choih, R. Fetter, and T. Serafini. 2000. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101:657-669.
110. Schelhaas, M., H. Ewers, M. L. Rajamaki, P. M. Day, J. T. Schiller, and A. Helenius. 2008. Human papillomavirus type 16 entry: retrograde cell surface transport along actin-rich protrusions. PLoS Pathog. 4:e1000148.
111. Sherer, N. M., J. Jin, and W. Mothes. 2010. Directional spread of surface associated retroviruses regulated by differential virus-cell interactions. J. Virol. 84:3248-3258.
112. Sherer, N. M., M. J. Lehmann, L. F. Jimenez-Soto, C. Horensavitz, M. Pypaert, and W. Mothes. 2007. Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat. Cell Biol. 9:310-315.
113. Sherer, N. M., and W. Mothes. 2008. Cytonemes and tunneling nanotubules in cell-cell communication and viral pathogenesis. Trends Cell Biol. 18:414-420.
114. Smith, G. A., S. P. Gross, and L. W. Enquist. 2001. Herpesviruses use bidirectional fast-axonal transport to spread in sensory neurons. Proc. Natl. Acad. Sci. U. S. A. 98:3466-3470.
115. Smith, J. L., D. S. Lidke, and M. A. Ozbun. 2008. Virus activated filopodia promote human papillomavirus type 31 uptake from the extracellular matrix. Virology 381:16-21.
116. Sol-Foulon, N., M. Sourisseau, F. Porrot, M. I. Thoulouze, C. Trouillet, C. Nobile, F. Blanchet, V. di Bartolo, N. Noraz, N. Taylor, A. Alcover, C. Hivroz, and O. Schwartz. 2007. ZAP-70 kinase regulates HIV cell-to-cell spread and virological synapse formation. EMBO J. 26:516-526.
117. Sourisseau, M., N. Sol-Foulon, F. Porrot, F. Blanchet, and O. Schwartz. 2007. Inefficient human immunodeficiency virus replication in mobile lymphocytes. J. Virol. 81:1000-1012.
118. Sowinski, S., C. Jolly, O. Berninghausen, M. A. Purbhoo, A. Chauveau, K. Kohler, S. Oddos, P. Eissmann, F. M. Brodsky, C. Hopkins, B. Onfelt, Q. Sattentau, and D. M. Davis. 2008. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat. Cell Biol. 10:211-219.
119. Stagi, M., A. I. Fogel, and T. Biederer. 2010. SynCAM 1 participates in axo-dendritic contact assembly and shapes neuronal growth concs. Proc. Natl. Acad. Sci. U. S. A. 107:7568-7573.
120. Stinchcombe, J. C., G. Bossi, S. Booth, and G. M. Griffiths. 2001. The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 15:751-761.
121. Stinchcombe, J. C., E. Majorovits, G. Bossi, S. Fuller, and G. M. Griffiths. 2006. Centrosome polarization delivers secretory granules to the immunological synapse. Nature 443:462-465.
122. Stolp, B., M. Reichman-Fried, L. Abraham, X. Pan, S. I. Giese, S. Hannemann, P. Goulimari, E. Raz, R. Grosse, and O. T. Fackler. 2009. HIV-1 Nef interferes with host cell motility by deregulation of Cofilin. Cell Host Microbe 6:174-186.
123. Togashi, H., J. Miyoshi, T. Honda, T. Sakisaka, Y. Takai, and M. Takeichi. 2006. Interneurite affinity is regulated by heterophilic nectin interactions in concert with the cadherin machinery. J. Cell Biol. 174:141-151.
124. Valitutti, S., and L. Dupre. 2010. Plasticity of immunological synapses. Curr. Top. Microbiol. Immunol. 340:209-228.
125. van der Schaar, H. M., M. J. Rust, B. L. Waarts, H. van der Ende- Metselaar, R. J. Kuhn, J. Wilschut, X. Zhuang, and J. M. Smit. 2007. Characterization of the early events in dengue virus cell entry by biochemical assays and single-virus tracking. J. Virol. 81:12019-12028.
126. Vasiliver-Shamis, G., M. W. Cho, C. E. Hioe, and M. L. Dustin. 2009. Human immunodeficiency virus type 1 envelope gp120-induced partial Tcell receptor signaling creates an F-actin-depleted zone in the virological synapse. J. Virol. 83:11341-11355.
127. Vasiliver-Shamis, G., M. Tuen, T. W. Wu, T. Starr, T. O. Cameron, R. Thomson, G. Kaur, J. Liu, M. L. Visciano, H. Li, R. Kumar, R. Ansari, D. P. Han, M. W. Cho, M. L. Dustin, and C. E. Hioe. 2008. Human immunodeficiency virus type 1 envelope gp120 induces a stop signal and virological synapse formation in noninfected CD4+ T cells. J. Virol. 82:9445-9457.
128. Vasioukhin, V., C. Bauer, M. Yin, and E. Fuchs. 2000. Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100:209-219.
129. Vendrame, D., M. Sourisseau, V. Perrin, O. Schwartz, and F. Mammano. 2009. Partial inhibition of human immunodeficiency virus replication by type I interferons: impact of cell-to-cell viral transfer. J. Virol. 83:10527-10537.
130. Wang, J. H., C. Kwas, and L. Wu. 2009. Intercellular adhesion molecule 1 (ICAM-1), but not ICAM-2 and -3, is important for dendritic cell-mediated human immunodeficiency virus type 1 transmission. J. Virol. 83:4195-4204.
131. Wang, Y. L., F. Lanni, P. L. McNeil, B. R. Ware, and D. L. Taylor. 1982. Mobility of cytoplasmic and membrane-associated actin in living cells. Proc. Natl. Acad. Sci. U. S. A. 79:4660-4664.
132. Wulfing, C., and M. M. Davis. 1998. A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science 282:2266-2269.
133. Yamada, S., and W. J. Nelson. 2007. Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J. Cell Biol. 178:517-527.
134. Yamada, S., and W. J. Nelson. 2007. Synapses: sites of cell recognition, adhesion, and functional specification. Annu. Rev. Biochem. 76:267-294.
135. Yoder, A., D. Yu, L. Dong, S. R. Iyer, X. Xu, J. Kelly, J. Liu, W. Wang, P. J. Vorster, L. Agulto, D. A. Stephany, J. N. Cooper, J. W. Marsh, and Y. Wu. 2008. HIV envelope-CXCR4 signaling activates cofilin to overcome cortical actin restriction in resting CD4 T cells. Cell 134:782-792.
136. Yu, D., W. Wang, A. Yoder, M. Spear, and Y. Wu. 2009. The HIV envelope but not VSV glycoprotein is capable of mediating HIV latent infection of resting CD4 T cells. PLoS Pathog. 5:e1000633.
137. Yu, H. J., M. A. Reuter, and D. McDonald. 2008. HIV traffics through a specialized, surface-accessible intracellular compartment during trans-infection of T cells by mature dendritic cells. PLoS Pathog. 4:e1000134.
138. Ziv, N. E., and S. J. Smith. 1996. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17:91-102.