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 Blood, 19 March 2009, Vol. 113, No. 12, pp. 2732-2741.
Prepublished online as a Blood First Edition Paper on October 22, 2008; DOI 10.1182/blood-2008-05-158642.

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IMMUNOBIOLOGY

Capture and transfer of HIV-1 particles by mature dendritic cells converges with the exosome-dissemination pathway

Nuria Izquierdo-Useros1,*, Mar Naranjo-Gómez2,*, Jacob Archer3, Steven C. Hatch3, Itziar Erkizia1, Julià Blanco1, Francesc E. Borràs2, Maria Carmen Puertas1, John H. Connor3, Maria Teresa Fernández-Figueras4, Landon Moore5, Bonaventura Clotet1, Suryaram Gummuluru3,{dagger}, and Javier Martinez-Picado1,6,{dagger}

1 IrsiCaixa Foundation and 2 Laboratory of Immunobiology for Research and Application to Diagnosis (LIRAD), Blood and Tissue Bank, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol, Universitat Autònoma de Barcelona, Badalona, Spain; 3 Department of Microbiology, Boston University School of Medicine, MA; 4 Department of Pathology, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol, Universitat Autònoma de Barcelona, Badalona, Spain; 5 Department of Genetics and Genomics, Boston University School of Medicine, MA; and 6 Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain

Exosomes are secreted cellular vesicles that can be internalized by dendritic cells (DCs), contributing to antigen-specific naive CD4+ T-cell activation. Here, we demonstrate that human immunodeficiency virus type 1 (HIV-1) can exploit this exosome antigen-dissemination pathway intrinsic to mature DCs (mDCs) for mediating trans-infection of T lymphocytes. Capture of HIV-1, HIV-1 Gag-enhanced green fluorescent protein (eGFP) viral-like particles (VLPs), and exosomes by DCs was up-regulated upon maturation, resulting in localization within a CD81+ compartment. Uptake of VLPs or exosomes could be inhibited by a challenge with either particle, suggesting that the expression of common determinant(s) on VLP or exosome surface is necessary for internalization by mDCs. Capture by mDCs was insensitive to proteolysis but blocked when virus, VLPs, or exosomes were produced from cells treated with sphingolipid biosynthesis inhibitors that modulate the lipid composition of the budding particles. Finally, VLPs and exosomes captured by mDCs were transmitted to T lymphocytes in an envelope glycoprotein-independent manner, underscoring a new potential viral dissemination pathway.


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