The HIV-1 Viral Protein R Induces Apoptosis via a Direct Effect on the Mitochondrial Permeability Transition Pore

doi:10.1084/jem.191.1.33

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© The Rockefeller University Press, 0022-1007/2000/1/33/ $5.00
The Journal of Experimental Medicine, Volume 191, Number 1, January 3, 2000 33-46

Original Article

The HIV-1 Viral Protein R Induces Apoptosis via a Direct Effect on the Mitochondrial Permeability Transition Pore

Etienne Jacotot^a, Luigi Ravagnan^a, Markus Loeffler^a, Karine F. Ferri^a, Helena L.A. Vieira^a, Naoufal Zamzami^a, Paola Costantini^a, Sabine Druillennec^b, Johan Hoebeke^c, Jean Paul Briand^c, Theano Irinopoulou^d, Eric Daugas^a, Santos A. Susin^a, Denis Cointe^e, Zhi Hua Xie^f, John C. Reed^f, Bernard P. Roques^b, and Guido Kroemer^a
^a Centre National de la Recherche Scientifique, F-94801 Villejuif, France
^b Unité de Pharmacochimie Moléculaire et Structurale, Institut National de la Santé et de Recherche Médicale (INSERM) U266, CNRS UMR 860, Université René Descartes (Paris V), 75006 Paris, France
^c Institut de Biologie Moléculaire et Cellulaire, Centre National de la Recherche Scientifique, 67084 Strasbourg, France
^d INSERM U430, Broussais Hospital, 75014 Paris, France
^e Laboratoire de Virologie et Immunologie, Hopital Antoine Beclère, 92141 Clamart, France
^f The Burnham Institute, La Jolla, California 92037

Correspondence to: Guido Kroemer, 19 rue Guy Môquet, B.P. 8, F-94801 Villejuif, France. Tel:33-1-49-58-35-13 Fax:33-1-49-58-35-09 E-mail:kroemer{at}infobiogen.fr.

Viral protein R (Vpr) encoded by HIV-1 is a facultative inducerof apoptosis. When added to intact cells or purified mitochondria,micromolar and submicromolar doses of synthetic Vpr cause arapid dissipation of the mitochondrial transmembrane potential( ${Delta}$ ${Psi}$ _m), as well as the mitochondrial release of apoptogenic proteinssuch as cytochrome c or apoptosis inducing factor. The samestructural motifs relevant for cell killing are responsiblefor the mitochondriotoxic effects of Vpr. Both mitochondrialand cytotoxic Vpr effects are prevented by Bcl-2, an inhibitorof the permeability transition pore complex (PTPC). Coincubationof purified organelles revealed that nuclear apoptosis is onlyinduced by Vpr when mitochondria are present yet can be abolishedby PTPC inhibitors. Vpr favors the permeabilization of artificialmembranes containing the purified PTPC or defined PTPC componentssuch as the adenine nucleotide translocator (ANT) combined withBax. Again, this effect is prevented by addition of recombinantBcl-2. The Vpr COOH terminus binds purified ANT, as well asa molecular complex containing ANT and the voltage-dependentanion channel (VDAC), another PTPC component. Yeast strainslacking ANT or VDAC are less susceptible to Vpr-induced killingthan control cells yet recover Vpr sensitivity when retransfectedwith yeast ANT or human VDAC. Hence, Vpr induces apoptosis viaa direct effect on the mitochondrial PTPC.

Key Words: apoptosis, Bcl-2, cell death, mitochondria, Vpr

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