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Cited by 17HIV Research and TreatmentHIV/AIDS Research and InterventionsImmunotherapy and Immune Responses

HIV-Captured DCs Regulate T Cell Migration and Cell-Cell Contact Dynamics to Enhance Viral Spread

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Koh, Wan Hon, Lopez, Paul, Ajibola, Oluwaseun, Parvarchian, Roshan, Mohammad, Umar, Hnatiuk, Ryan, Kindrachuk, Jason, Murooka, Thomas T.·2020·iScience
DOI 10.1016/j.isci.2020.101427PMC PMC7452485
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Abstract

Trafficking of cell-associated HIV-1 from the genital mucosa to lymphoid organs represents a critical first step toward systemic infection. Mature DCs capture and transmit HIV-1 to T cells, but insights into DC-to-T cell viral spread dynamics within a 3-dimensional environment is lacking. Using live-cell imaging, we show that mature DCs rapidly compartmentalize HIV-1 within surface-accessible invaginations near the uropod. HIV-1 capture did not interfere with DC migration toward lymph node homing chemo-attractants and their ability to enter lymphatic vessels. However, HIV-captured DCs engaged in prolonged contacts with autologous CD4+ T cells, which led to high T cell infection. Interestingly, we show that surface bound, virion-associated Env induced signal transduction in motile T cells that facilitated prolonged DC:T cell interactions, partially through high-affinity LFA-1 expression. Together, we describe a mechanism by which surface bound HIV-1 particles function as signaling receptors that regulate T cell motility, cell-cell contact dynamics, and productive infection.

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  • DCs that captured HIV migrate in 3D collagen towards lymph-node-homing chemoattractants and establish infectious synapse with CD4+ lymphocytes, implicating DC-mediated dissemination upon sexual transmission.

    “DCs that have captured HIV can migrate in 3D collagen towards lymph-node-homing chemo-attractant gradients, and establish infectious synapse with CD4+ lymphocytes [133], implicating the role of DC-mediated dissemination of HIV upon sexual transmission.”

    From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [133]

    The Results section on lymph-node-homing chemokines reports that HIV-captured DCs respond to CCL19/21 and S1P gradients, while the Results section on DC–T-cell engagement reports prolonged contacts and increased CD4+ T-cell infection in 3D collagen. But chemotaxis was tested in a transwell assay and an ex vivo skin model, not in 3D collagen; the paper discusses a potential role in dissemination after sexual transmission rather than demonstrating that process directly. Page numbers are unavailable in our copy. (LLM, conf=0.88)

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  1. Akiyama H. Ramirez N.G.P. Gudheti M.V. Gummuluru S. CD169-mediated trafficking of HIV to plasma membrane invaginations in dendritic cells attenuates efficacy of anti-gp120 broadly neutralizing antibodies. PLOS Pathogens 11 2015 e1004751 25760631 PMC4356592
  2. Andreotti A.H. Schwartzberg P.L. Joseph R.E. Berg L.J. T-cell signaling regulated by the tec family kinase, Itk Csh Perspect. Biol. 2 2010 a002287 PMC2890196 20519342
  3. Asano K. Nabeyama A. Miyake Y. Qiu C.-H. Kurita A. Tomura M. Kanagawa O. Fujii S.-i. Tanaka M. CD169-Positive macrophages dominate antitumor immunity by crosspresenting dead cell-associated antigens Immunity 34 2011 85 95 21194983
  4. Baggaley R.F. White R.G. Boily M.-C. HIV transmission risk through anal intercourse: systematic review, meta-analysis and implications for HIV prevention Int. J. Epidemiol. 39 2010 1048 1063 20406794 PMC2929353
  5. Barreiro O. Zamai M. Yanez-Mo M. Tejera E. Lopez-Romero P. Monk P.N. Gratton E. Caiolfa V.R. Sanchez-Madrid F. Endothelial adhesion receptors are recruited to adherent leukocytes by inclusion in preformed tetraspanin nanoplatforms J. Cell Biol. 183 2008 527 542 18955551 PMC2575792
  6. Bertram K.M. Botting R.A. Baharlou H. Rhodes J.W. Rana H. Graham J.D. Patrick E. Fletcher J. Plasto T.M. Truong N.R. Identification of HIV transmitting CD11c(+) human epidermal dendritic cells Nat. Commun. 10 2019 2759 31227717 PMC6588576
  7. Bousso P. Robey E. Dynamics of CD8(+) T cell priming by dendritic cells in intact lymph nodes Nat. Immunol. 4 2003 579 585 12730692
  8. Bromley S.K. Burack W.R. Johnson K.G. Somersalo K. Sims T.N. Sumen C. Davis M.M. Shaw A.S. Allen P.M. Dustin M.L. The immunological synapse Annu. Rev. Immunol. 19 2001 375 396 11244041
  9. Bromley S.K. Peterson D.A. Gunn M.D. Dustin M.L. Cutting edge: hierarchy of chemokine receptor and TCR signals regulating T cell migration and proliferation J. Immunol. 165 2000 15 19 10861029
  10. Bromley S.K. Thomas S.Y. Luster A.D. Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics Nat. Immunol. 6 2005 895 901 16116469
  11. Brown M.N. Fintushel S.R. Lee M.H. Jennrich S. Geherin S.A. Hay J.B. Butcher E.C. Debes G.F. Chemoattractant receptors and lymphocyte egress from extralymphoid tissue: changing requirements during the course of inflammation J. Immunol. 185 2010 4873 4882 20833836 PMC3327166
  12. Cameron P.U. Freudenthal P.S. Barker J.M. Gezelter S. Inaba K. Steinman R.M. Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells Science 257 1992 383 387 1352913
  13. Cavrois M. Neidleman J. Kreisberg J.F. Greene W.C. In vitro derived dendritic cells trans-infect CD4 T cells primarily with surface-bound HIV-1 virions PLoS Pathog. 3 2007 e4 17238285 PMC1779297
  14. Cicala C. Arthos J. Censoplano N. Cruz C. Chung E. Martinelli E. Lempicki R.A. Natarajan V. VanRyk D. Daucher M. HIV-1 gp120 induces NFAT nuclear translocation in resting CD4+ T-cells Virology 345 2006 105 114 16260021
  15. Crocker P.R. Paulson J.C. Varki A. Siglecs and their roles in the immune system Nat. Rev. Immunol. 2007 255 266 17380156
  16. Cuevas B.D. Abell A.N. Johnson G.L. Role of mitogen-activated protein kinase kinase kinases in signal integration Oncogene 26 2007 3159 3171 17496913
  17. Cunningham A.L. Donaghy H. Harman A.N. Kim M. Turville S.G. Manipulation of dendritic cell function by viruses Curr. Opin. Microbiol. 13 2010 524 529 20598938
  18. Czeloth N. Bernhardt G. Hofmann F. Genth H. Forster R. Sphingosine-1-Phosphate mediates migration of mature dendritic cells J. Immunol. 175 2005 2960 2967 16116182
  19. Debes G.F. Arnold C.N. Young A.J. Krautwald S. Lipp M. Hay J.B. Butcher E.C. Chemokine receptor CCR7 required for T lymphocyte exit from peripheral tissues Nat. Immunol. 6 2005 889 894 16116468 PMC2144916
  20. Deruaz M. Murooka T.T. Ji S. Gavin M.A. Vrbanac V.D. Lieberman J. Tager A.M. Mempel T.R. Luster A.D. Chemoattractant-mediated leukocyte trafficking enables HIV dissemination from the genital mucosa JCI insight 2 2017 e88533 28405607 PMC5374062
  21. Douek D.C. Brenchley J.M. Betts M.R. Ambrozak D.R. Hill B.J. Okamoto Y. Casazza J.P. Kuruppu J. Kunstman K. Wolinsky S. HIV preferentially infects HIV-specific CD4+ T cells Nature 417 2002 95 98 11986671
  22. Duncan C.J.A. Williams J.P. Schiffner T. Gartner K. Ochsenbauer C. Kappes J. Russell R.A. Frater J. Sattentau Q.J. High-multiplicity HIV-1 infection and neutralizing antibody evasion mediated by the macrophage-T cell virological synapse J. Virol. 88 2014 2025 2034 24307588 PMC3911534
  23. Edgar L.J. Kawasaki N. Nycholat C.M. Paulson J.C. Targeted delivery of antigen to activated CD169+ macrophages induces bias for expansion of CD8+ T cells Cell Chem. Biol. 26 2019 131 136.e4 30393066 PMC6338492
  24. Fackler O.T. Murooka T.T. Imle A. Mempel T.R. Adding new dimensions: towards an integrative understanding of HIV-1 spread Nat. Rev. Microbiol. 12 2014 563 574 25029025 PMC5687059
  25. Felts R.L. Narayan K. Estes J.D. Shi D. Trubey C.M. Fu J. Hartnell L.M. Ruthel G.T. Schneider D.K. Nagashima K. 3D visualization of HIV transfer at the virological synapse between dendritic cells and T cells Proc. Natl. Acad. Sci. U S A 107 2010 13336 13341 20624966 PMC2922156
  26. Forster R. Schubel A. Breitfeld D. Kremmer E. Renner-Muller I. Wolf E. Lipp M. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs Cell 99 1999 23 33 10520991
  27. Francois F. Klotman M.E. Phosphatidylinositol 3-kinase regulates human immunodeficiency virus type 1 replication following viral entry in primary CD4+ T lymphocytes and macrophages J. Virol. 77 2003 2539 2549 12551992 PMC141101
  28. Geijtenbeek T.B. Kwon D.S. Torensma R. van Vliet S.J. van Duijnhoven G.C. Middel J. Cornelissen I.L. Nottet H.S. KewalRamani V.N. Littman D.R. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells Cell 100 2000 587 597 10721995
  29. Girard J.-P. Springer T.A. High endothelial venules (HEVs): specialized endothelium for lymphocyte migration Immunol. Today 16 1995 449 457 7546210
  30. Goldman F. Jensen W.A. Johnson G.L. Heasley L. Cambier J.C. gp120 ligation of CD4 induces p56lck activation and TCR desensitization independent of TCR tyrosine phosphorylation J. Immunol. 153 1994 2905 2917 7522245
  31. Gollmann G. Neuwirt H. Tripp C.H. Mueller H. Konwalinka G. Heufler C. Romani N. Tiefenthaler M. Sphingosine-1-phosphate receptor type-1 agonism impairs blood dendritic cell chemotaxis and skin dendritic cell migration to lymph nodes under inflammatory conditions Int. Immunol. 20 2008 911 923 18495625
  32. Gousset K. Ablan S.D. Coren L.V. Ono A. Soheilian F. Nagashima K. Ott D.E. Freed E.O. Real-time visualization of HIV-1 GAG trafficking in infected macrophages PLoS Pathog. 4 2008 e1000015 18369466 PMC2267008
  33. Grabowska J. Lopez-Venegas M.A. Affandi A.J. Den Haan J.M.M. CD169+ macrophages capture and dendritic cells instruct: the interplay of the gatekeeper and the general of the immune system Front. Immunol. 9 2018 1 14 30416504 PMC6212557
  34. Gummuluru S. Pina Ramirez N.G. Akiyama H. CD169-dependent cell-associated HIV-1 transmission: a driver of virus dissemination J. Infect. Dis. 210 Suppl 3 2014 S641 S647 25414418 PMC4303078
  35. Haase A.T. Targeting early infection to prevent HIV-1 mucosal transmission Nature 464 2010 217 223 20220840
  36. Haase A.T. Early events in sexual transmission of HIV and SIV and opportunities for interventions Annu. Rev. Med. 62 2011 127 139 21054171
  37. Hammonds J.E. Beeman N. Ding L. Takushi S. Francis A.C. Wang J.J. Melikyan G.B. Spearman P. Siglec-1 initiates formation of the virus-containing compartment and enhances macrophage-to-T cell transmission of HIV-1 PLoS Pathog. 13 2017 1 28 PMC5298340 28129379
  38. Hatch S.C. Sardo L. Chen J. Burdick R. Gorelick R. Fivash M.J. Pathak V.K. Hu W.-S. Gag-dependent enrichment of HIV-1 RNA near the uropod membrane of polarized T cells J. Virol. 87 2013 11912 11915 23966405 PMC3807364
  39. Henrickson S.E. Mempel T.R. Mazo I.B. Liu B. Artyomov M.N. Zheng H. Peixoto A. Flynn M.P. Senman B. Junt T. T cell sensing of antigen dose governs interactive behavior with dendritic cells and sets a threshold for T cell activation Nat. Immunol. 9 2008 282 291 18204450 PMC2698867
  40. Hioe C.E. Tuen M. Vasiliver-Shamis G. Alvarez Y. Prins K.C. Banerjee S. Nádas A. Cho M.W. Dustin M.L. Kachlany S.C. HIV envelope gp120 activates LFA-1 on CD4 T-lymphocytes and increases cell susceptibility to LFA-1-targeting leukotoxin (LtxA) PLoS One 6 2011 1 11 PMC3151267 21850260
  41. Hladik F. Sakchalathorn P. Ballweber L. Lentz G. Fialkow M. Eschenbach D. McElrath M.J. Initial events in establishing vaginal entry and infection by human immunodeficiency virus type-1 Immunity 26 2007 257 270 17306567 PMC1885958
  42. Hu J. Gardner M.B. Miller C.J. Simian immunodeficiency virus rapidly penetrates the cervicovaginal mucosa after intravaginal inoculation and infects intraepithelial dendritic cells J. Virol. 74 2000 6087 6095 10846092 PMC112107
  43. Hu Q. Frank I. Williams V. Santos J.J. Watts P. Griffin G.E. Moore J.P. Pope M. Shattock R.J. Blockade of attachment and fusion receptors inhibits HIV-1 infection of human cervical tissue J. Exp. Med. 199 2004 1065 1075 15078900 PMC2211899
  44. Idzko M. Panther E. Corinti S. Morelli A. Ferrari D. Herouy Y. Dichmann S. Mockenhaupt M. Gebicke-Haerter P. Di Virgilio F. Sphingosine 1-phosphate induces chemotaxis of immature and modulates cytokine-release in mature human dendritic cells for emergence of Th2 immune responses FASEB J. 16 2002 625 627 11919175
  45. Izquierdo-Useros N. Blanco J. Erkizia I. Fernandez-Figueras M.T. Borras F.E. Naranjo-Gomez M. Bofill M. Ruiz L. Clotet B. Martinez-Picado J. Maturation of blood-derived dendritic cells enhances human immunodeficiency virus type 1 capture and transmission J. Virol. 81 2007 7559 7570 17475656 PMC1933337
  46. Izquierdo-Useros N. Lorizate M. Contreras F.X. Rodriguez-Plata M.T. Glass B. Erkizia I. Prado J.G. Casas J. Fabriàs G. Kräusslich H.G. Sialyllactose in viral membrane gangliosides is a novel molecular recognition pattern for mature dendritic cell capture of HIV-1 PLoS Biol. 10 2012 e1001315 22545022 PMC3335875
  47. Izquierdo-Useros N. Lorizate M. McLaren P.J. Telenti A. Krausslich H.G. Martinez-Picado J. HIV-1 capture and transmission by dendritic cells: the role of viral glycolipids and the cellular receptor Siglec-1 PLoS Pathog. 10 2014 e1004146 25033082 PMC4102576
  48. Jacque J.M. Mann A. Enslen H. Sharova N. Brichacek B. Davis R.J. Stevenson M. Modulation of HIV-1 infectivity by MAPK, a virion-associated kinase EMBO J. 17 1998 2607 2618 9564043 PMC1170602
  49. Jolly C. Kashefi K. Hollinshead M. Sattentau Q.J. HIV-1 cell to cell transfer across an env-induced, actin-dependent synapse J. Exp. Med. 199 2004 283 293 14734528 PMC2211771
  50. Jolly C. Mitar I. Sattentau Q.J. Adhesion molecule interactions facilitate human immunodeficiency virus type 1-induced virological synapse formation between T cells J. Virol. 2007 13916 13921 17913807 PMC2168851
  51. Jolly C. Sattentau Q.J. Retroviral spread by induction of virological synapses Traffic 5 2004 643 650 15296489
  52. Jolly C. Sattentau Q.J. Human immunodeficiency virus type 1 virological synapse formation in T cells requires lipid raft integrity J. Virol. 79 2005 12088 12094 16140785 PMC1212596
  53. Juszczak R.J. Turchin H. Truneh A. Culp J. Kassis S. Effect of human immunodeficiency virus gp120 glycoprotein on the association of the protein tyrosine kinase p56lck with CD4 in human T lymphocytes J. Biol. Chem. 266 1991 11176 11183 2040625
  54. Klemke R.L. Cai S. Giannini A.L. Gallagher P.J. de Lanerolle P. Cheresh D.A. Regulation of cell motility by mitogen-activated protein kinase J. Cell Biol. 137 1997 481 492 9128257 PMC2139771
  55. Krueger J.S. Keshamouni V.G. Atanaskova N. Reddy K.B. Temporal and quantitative regulation of mitogen-activated protein kinase (MAPK) modulates cell motility and invasion Oncogene 20 2001 4209 4218 11464287
  56. Laguette N. Sobhian B. Casartelli N. Ringeard M. Chable-Bessia C. Segeral E. Yatim A. Emiliani S. Schwartz O. Benkirane M. SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx Nature 474 2011 654 657 21613998 PMC3595993
  57. Lan Y.Y. De Creus A. Colvin B.L. Abe M. Brinkmann V. Coates P.T.H. Thomson A.W. The sphingosine-1-phosphate receptor agonist FTY720 modulates dendritic cell trafficking in vivo Am. J. Transpl. 5 2005 2649 2659 16212624
  58. Lan Y.Y. Tokita D. Wang Z. Wang H.C. Zhan J. Brinkmann V. Thomson A.W. Sphingosine 1-phosphate receptor agonism impairs skin dendritic cell migration and homing to secondary lymphoid tissue: association with prolonged allograft survival Transpl. Immunol. 20 2008 88 94 18694829
  59. Laufer J.M. Kindinger I. Artinger M. Pauli A. Legler D.F. CCR7 is recruited to the immunological synapse, acts as Co-stimulatory molecule and drives LFA-1 clustering for efficient T cell adhesion through ZAP70 Front. Immunol. 9 2018 3115 30692994 PMC6339918
  60. Len A.C.L. Starling S. Shivkumar M. Jolly C. HIV-1 activates T cell signaling independently of antigen to drive viral spread Cell Rep. 2017 1062 1074 28122231 PMC5289937
  61. Lindquist R.L. Shakhar G. Dudziak D. Wardemann H. Eisenreich T. Dustin M.L. Nussenzweig M.C. Visualizing dendritic cell networks in vivo Nat. Immunol. 18 2004 1243 1250 15543150
  62. Lopez P. Koh W.H. Hnatiuk R. Murooka T.T. HIV infection stabilizes macrophage:T cell interactions to promote cell-cell HIV spread J. Virol. 93 2019 e00805–19 PMC6714792 31270227
  63. Lore K. Smed-Sorensen A. Vasudevan J. Mascola J.R. Koup R.A. Myeloid and plasmacytoid dendritic cells transfer HIV-1 preferentially to antigen-specific CD4+ T cells J. Exp. Med. 201 2005 2023 2033 15967828 PMC2212038
  64. Martín-Fontecha A. Lanzavecchia A. Sallusto F. Dendritic cell migration to peripheral lymph nodes Handb. Exp. Pharmacol. 188 2009 31 50 19031020
  65. Masurier C. Salomon B. Guettari N. Pioche C. Lachapelle F. Guigon M. Klatzmann D. Dendritic cells route human immunodeficiency virus to lymph nodes after vaginal or intravenous administration to mice J. Virol. 72 1998 7822 7829 9733818 PMC110098
  66. McDonald D. Wu L. Bohks S.M. KewalRamani V.N. Unutmaz D. Hope T.J. Recruitment of HIV and its receptors to dendritic cell-T cell junctions Science 300 2003 1295 1297 12730499
  67. Melar M. Ott D.E. Hope T.J. Physiological levels of virion-associated human immunodeficiency virus type 1 envelope induce coreceptor-dependent calcium flux J. Virol. 81 2007 1773 1785 17121788 PMC1797554
  68. Mempel T.R. Henrickson S.E. von Andrian U.H. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases Nature 427 2004 154 159 14712275
  69. Menager M.M. Littman D.R. Actin dynamics regulates dendritic cell-mediated transfer of HIV-1 to T cells Cell 2016 695 709 PMC4752894 26830877
  70. Miller C.J. Li Q. Abel K. Kim E.Y. Ma Z.M. Wietgrefe S. La Franco-Scheuch L. Compton L. Duan L. Shore M.D. Propagation and dissemination of infection after vaginal transmission of simian immunodeficiency virus J. Virol. 79 2005 9217 9227 15994816 PMC1168785
  71. Miller M.J. Hejazi A.S. Wei S.H. Cahalan M.D. Parker I. T cell repertoire scanning is promoted by dynamic dendritic cell behavior and random T cell motility in the lymph node Proc. Natl. Acad. Sci. U S A 101 2004 998 1003 14722354 PMC327133
  72. Miller M.J. Wei S.H. Cahalan M.D. Parker I. Autonomous T cell trafficking examined in vivo with intravital two-photon microscopy Proc. Natl. Acad. Sci. U S A 100 2003 2604 2609 12601158 PMC151387
  73. Murooka T.T. Deruaz M. Marangoni F. Vrbanac V.D. Seung E. von Andrian U.H. Tager A.M. Luster A.D. Mempel T.R. HIV-infected T cells are migratory vehicles for viral dissemination Nature 2012 283 287 PMC3470742 22854780
  74. Murooka T.T. Mempel T.R. Multiphoton intravital microscopy to study lymphocyte motility in lymph nodes Methods Mol. Biol. 2012 247 257 21909917
  75. Murooka T.T. Mempel T.R. Intravital microscopy in BLT-humanized mice to study cellular dynamics in HIV infection J. Infect. Dis. 208 2013 S137 S144 24151320 PMC3807971
  76. Nabel G. Baltimore D. An inducible transcription factor activates expression of human immunodeficiency virus in T cells Nature 326 1987 711 713 3031512
  77. Nasr N. Lai J. Botting R.A. Mercier S.K. Harman A.N. Kim M. Turville S. Center R.J. Domagala T. Gorry P.R. Inhibition of two temporal phases of HIV-1 transfer from primary Langerhans cells to T cells: the role of langerin J. Immunol. 193 2014 2554 2564 25070850
  78. Nickol M.E. Ciric J. Falcinelli S.D. Chertow D.S. Kindrachuk J. Characterization of host and bacterial contributions to lung barrier dysfunction following Co-infection with 2009 pandemic influenza and methicillin resistant Staphylococcus aureus Viruses 11 2019 116 PMC6409999 30699912
  79. Pena-Cruz V. Agosto L.M. Akiyama H. Olson A. Moreau Y. Larrieux J.R. Henderson A. Gummuluru S. Sagar M. HIV-1 replicates and persists in vaginal epithelial dendritic cells J. Clin. Invest. 128 2018 3439 3444 29723162 PMC6063466
  80. Perez-Zsolt D. Cantero-Pérez J. Erkizia I. Benet S. Pino M. Serra-Peinado C. Hernández-Gallego A. Castellví J. Tapia G. Arnau-Saz V. Dendritic cells from the cervical mucosa capture and transfer HIV-1 via Siglec-1 Front. Immunol. 10 2019 1 14 31114569 PMC6503733
  81. Permanyer M. Bošnjak B. Förster R. Dendritic cells, T cells and lymphatics: dialogues in migration and beyond Curr. Opin. Immunol. 53 2018 173 179 29857205
  82. Phan T. Green J. Gray E. Xu Y. Cyster J. Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation Nat. Immunol. 10 2009 786 793 19503106 PMC2776777
  83. Planas D. Zhang Y. Monteiro P. Goulet J.P. Gosselin A. Grandvaux N. Hope T.J. Fassati A. Routy J.P. Ancuta P. HIV-1 selectively targets gut-homing CCR6+CD4+ T cells via mTOR-dependent mechanisms JCI Insight 2 2017 e93230 PMC5543920 28768913
  84. Platt A.M. Randolph G.J. Dendritic cell migration through the lymphatic vasculature to lymph nodes Adv. Immunol. 120 2013 51 68 24070380
  85. Popik W. Hesselgesser J.E. Pitha P.M. Binding of human immunodeficiency virus type 1 to CD4 and CXCR4 receptors differentially regulates expression of inflammatory genes and activates the MEK/ERK signaling pathway J. Virol. 72 1998 6406 6413 9658081 PMC109793
  86. Randolph G.J. Angeli V. Swartz M.A. Dendritic-cell trafficking to lymph nodes through lymphatic vessels Nat. Rev. Immunol. 2005 617 628 16056255
  87. Rodriguez-Garcia M. Shen Z. Barr F.D. Boesch A.W. Ackerman M.E. Kappes J.C. Ochsenbauer C. Wira C.R. Dendritic cells from the human female reproductive tract rapidly capture and respond to HIV Mucosal Immunol. 10 2017 531 544 27579858 PMC5332537
  88. Rudnicka D. Schwartz O. Intrusive HIV-1-infected cells Nat. Immunol. 10 2009 933 934 19692990
  89. Russo E. Teijeira A. Vaahtomeri K. Willrodt A.H. Bloch J.S. Nitschke M. Santambrogio L. Kerjaschki D. Sixt M. Halin C. Intralymphatic CCL21 promotes tissue egress of dendritic cells through afferent lymphatic vessels Cell Rep. 14 2016 1723 1734 26876174
  90. Satpathy A.T. Wu X. Albring J.C. Murphy K.M. Re(de)fining the dendritic cell lineage Nat. Immunol. 13 2012 1145 1154 23160217 PMC3644874
  91. Saunderson S.C. Dunn A.C. Crocker P.R. McLellan A.D. CD169 mediates the capture of exosomes in spleen and lymph node Blood 2014 208 216 24255917 PMC3888287
  92. Schwartzberg P.L. Finkelstein L.D. Readinger J.A. TEC-family kinases: regulators of T-helper-cell differentiation Nat. Rev. Immunol. 5 2005 284 295 15803148
  93. Sewald X. Ladinsky M.S. Uchil P.D. Beloor J. Pi R. Herrmann C. Motamedi N. Murooka T.T. Brehm M.A. Greiner D.L. Retroviruses use CD169-mediated trans-infection of permissive lymphocytes to establish infection Science 350 2015 563 567 26429886 PMC4651917
  94. Sigal A. Kim J.T. Balazs A.B. Dekel E. Mayo A. Milo R. Baltimore D. Cell-to-cell spread of HIV permits ongoing replication despite antiretroviral therapy Nature 477 2011 95 98 21849975
  95. Starling S. Jolly C. LFA-1 engagement triggers T cell polarization at the HIV-1 virological synapse J. Virol. 90 2016 9841 9854 27558417 PMC5068534
  96. Stieh D.J. Matias E. Xu H. Fought A.J. Blanchard J.L. Marx P.A. Veazey R.S. Hope T.J. Th17 cells are preferentially infected very early after vaginal transmission of SIV in macaques Cell Host Microbe 19 2016 529 540 27078070 PMC4841252
  97. Suárez H. Rocha-Perugini V. Álvarez S.S. Yáñez-Mó M. Tetraspanins, another piece in the HIV-1 replication puzzle Front. Immunol. 9 2018 1 9 30127789 PMC6088189
  98. Symeonides M. Murooka T.T. Bellfy L.N. Roy N.H. Mempel T.R. Thali M. HIV-1-induced small T cell syncytia can transfer virus particles to target cells through transient contacts Viruses 7 2015 6590 6603 26703714 PMC4690882
  99. Tal O. Lim H.Y. Gurevich I. Milo I. Shipony Z. Ng L.G. Angeli V. Shakhar G. DC mobilization from the skin requires docking to immobilized CCL21 on lymphatic endothelium and intralymphatic crawling J. Exp. Med. 208 2011 2141 2153 21930767 PMC3182054
  100. Tebit D.M. Ndembi N. Weinberg A. Quiñones-Mateu M.E. Mucosal transmission of human immunodeficiency virus Current HIV research 10 2012 3 8 22264040 PMC3744389
  101. Trifonova R.T. Bollman B. Barteneva N.S. Lieberman J. Myeloid cells in intact human cervical explants capture HIV and can transmit it to CD4 T cells Front. Immunol. 9 2018 2719 30532754 PMC6265349
  102. Turville S.G. Santos J.J. Frank I. Cameron P.U. Wilkinson J. Miranda-Saksena M. Dable J. Stossel H. Romani N. Piatak M. Jr. Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells Blood 103 2004 2170 2179 14630806
  103. Uchil P.D. Pi R. Haugh K.A. Ladinsky M.S. Ventura J.D. Barrett B.S. Santiago M.L. Bjorkman P.J. Kassiotis G. Sewald X. A protective role for the lectin CD169/siglec-1 against a pathogenic murine retrovirus Cell Host Microbe 25 2018 87 100.e10 30595553 PMC6331384
  104. Usmani S.M. Murooka T.T. Deruaz M. Koh W.H. Sharaf R.R. Di Pilato M. Power K.A. Lopez P. Hnatiuk R. Vrbanac V.D. HIV-1 balances the fitness costs and benefits of disrupting the host cell actin cytoskeleton early after mucosal transmission Cell Host Microbe 25 2019 73 86.e75 30629922 PMC6456338
  105. Vasiliver-Shamis G. Cho M.W. Hioe C.E. Dustin M.L. Human immunodeficiency virus type 1 envelope gp120-induced partial T-cell receptor signaling creates an F-actin-depleted zone in the virological synapse J. Virol. 83 2009 11341 11355 19710135 PMC2772796
  106. Vasiliver-Shamis G. Dustin M.L. Hioe C.E. HIV-1 virological synapse is not simply a copycat of the immunological synapse Viruses 2 2010 1239 1260 20890395 PMC2947835
  107. Vasiliver-Shamis G. Tuen M. Wu T.W. Starr T. Cameron T.O. Thomson R. Kaur G. Liu J. Visciano M.L. Li H. Human immunodeficiency virus type 1 envelope gp120 induces a stop signal and virological synapse formation in noninfected CD4+ T cells J. Virol. 82 2008 9445 9457 18632854 PMC2546991
  108. Veninga H. Borg E.G. Vreeman K. Taylor P.R. Kalay H. van Kooyk Y. Kraal G. Martinez-Pomares L. den Haan J.M. Antigen targeting reveals splenic CD169+ macrophages as promoters of germinal center B-cell responses Eur. J. Immunol. 45 2015 747 757 25487358 PMC4843951
  109. Wang J.-H. Kwas C. Wu L. 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 2009 4195 4204 19211748 PMC2668448
  110. Weber M. Hauschild R. Schwarz J. Moussion C. de Vries I. Legler D.F. Luther S.A. Bollenbach T. Sixt M. Interstitial dendritic cell guidance by haptotactic chemokine gradients Science 339 2013 328 332 23329049
  111. Weissman D. Rabin R.L. Arthos J. Rubbert A. Dybul M. Swofford R. Venkatesan S. Farber J.M. Fauci A.S. Macrophage-tropic HIV and SIV envelope proteins induce a signal through the CCR5 chemokine receptor Nature 389 1997 981 985 9353123
  112. Whitney J.B. Hill A.L. Sanisetty S. Penaloza-MacMaster P. Liu J. Shetty M. Parenteau L. Cabral C. Shields J. Blackmore S. Rapid seeding of the viral reservoir prior to SIV viraemia in rhesus monkeys Nature 512 2014 74 77 25042999 PMC4126858
  113. Whitney J.B. Lim S.Y. Osuna C.E. Kublin J.L. Chen E. Yoon G. Liu P.T. Abbink P. Borducci E.N. Hill A. Prevention of SIVmac251 reservoir seeding in rhesus monkeys by early antiretroviral therapy Nat. Commun. 9 2018 5429 30575753 PMC6303321
  114. Wu L. KewalRamani V.N. Dendritic-cell interactions with HIV: infection and viral dissemination Nat. Rev. Immunol. 6 2006 859 868 17063186 PMC1796806
  115. Yang X. Gabuzda D. Regulation of human immunodeficiency virus type 1 infectivity by the ERK mitogen-activated protein kinase signaling pathway J. Virol. 73 1999 3460 3466 10074203 PMC104113
  116. Zhu P. Liu J. Bess J. Jr. Chertova E. Lifson J.D. Grise H. Ofek G.A. Taylor K.A. Roux K.H. Distribution and three-dimensional structure of AIDS virus envelope spikes Nature 441 2006 847 852 16728975

Cited by

Sorted by citations

Authors
Koh, W. H., Lopez, P., Ajibola, O., Parvarchian, R., Mohammad, U., Hnatiuk, R., Kindrachuk, J., & Murooka, T. T.
Affiliations
University of Manitoba (CA)
Corresponding author
Murooka, Thomas T.
ORCID
Venue
iScience
Publisher
Elsevier BV
Published
2020-08
Volume
23
Issue
8
Pages
101427
ISSN
2589-0042 (ISSN-L)
DOI
10.1016/j.isci.2020.101427
PMC
PMC7452485
OpenAlex
W3046650483
Cited by
17
References
5
Citations by year
2026: 2 · 2025: 2 · 2023: 4 · 2022: 8 · 2020: 1
FWCI
1.71
Type
journal article
Language
en
Open access
Licence
Locations
  • iScience (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Canadian Institutes of Health Research
  • Research Manitoba
Topics
  • Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
  • Health Sciences › Medicine › Infectious Diseases › HIV/AIDS Research and Interventions
  • Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Keywords
HIV-1, dendritic cells, viral spread, T cell migration, cell-cell contact, CD4+ T cells, LFA-1, uropod, lymph node homing, genital mucosa, viral capture, productive infection

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