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Journal of Virology, February 2000, p. 1948-1960, Vol. 74, No. 4
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Selective Interactions of Polyanions with Basic Surfaces on Human Immunodeficiency Virus Type 1 gp120

Maxime Moulard,1,dagger Hugues Lortat-Jacob,2 Isabelle Mondor,1 Guillaume Roca,1 Richard Wyatt,3 Joseph Sodroski,3 Lu Zhao,4 William Olson,4 Peter D. Kwong,5 and Quentin J. Sattentau1,*

Centre d'Immunologie de Marseille-Luminy, 13288 Marseille Cedex 9,1 and Institut de Biologie Structurale, 38027 Grenoble Cedex 01,2 France; Department of Cancer Immunology and AIDS, Dana-Farber Cancer Institute, Harvard Medical School, Boston, Massachusetts 021153; Progenics Pharmaceuticals Inc., Tarrytown, New York 105914; and Department of Biochemistry and Molecular Biophysics, College of Physicians and Surgeons, Columbia University, New York, New York 100325

Received 25 June 1999/Accepted 17 November 1999

It is well established that the gp120 V3 loop of T-cell-line-adapted human immunodeficiency virus type 1 (HIV-1) binds both cell-associated and soluble polyanions. Virus infectivity is increased by interactions between HIV-1 and heparan sulfate proteoglycans on some cell types, and soluble polyanions such as heparin and dextran sulfate neutralize HIV-1 in vitro. However, the analysis of gp120-polyanion interactions has been limited to T-cell-line-adapted, CXCR4-using virus and virus-derived gp120, and the polyanion binding ability of gp120 regions other than the V3 loop has not been addressed. Here we demonstrate by monoclonal-antibody inhibition, labeled heparin binding, and surface plasmon resonance studies that a second site, most probably corresponding to the newly defined, highly conserved coreceptor binding region on gp120, forms part of the polyanion binding surface. Consistent with the binding of polyanions to the coreceptor binding surface, dextran sulfate interfered with the gp120-CXCR4 association while having no detectable effect on the gp120-CD4 interaction. The interaction between polyanions and X4 or R5X4 gp120 was readily detectable, whereas weak or undetectable binding was observed with R5 gp120. Analysis of mutated forms of X4 gp120 demonstrated that the V3 loop is the major determinant for polyanion binding whereas other regions, including the V1/V2 loop structure and the NH2 and COOH termini, exert a more subtle influence. A molecular model of the electrostatic potential of the conserved coreceptor binding region confirmed that it is basic but that the overall charge on this surface is dominated by the V3 loop. These results demonstrate a selective interaction of gp120 with polyanions and suggest that the conserved coreceptor binding surface may present a novel and conserved target for therapeutic intervention.

* Corresponding author. Present address: Imperial College of Science, Technology and Medicine, Jefferiss Research Trust Laboratories, Norfolk Pl., London W2 1PG, England. Phone: 44-171 886 1539. Fax: 44-171 886 6645. E-mail: quentin.sattentau{at}pathology.oxford.ac.uk.

dagger Present address: Department of Immunology, The Scripps Research Institute, La Jolla, CA 92037.

Journal of Virology, February 2000, p. 1948-1960, Vol. 74, No. 4
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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