1887

Abstract

Primary isolates of human and simian immunodeficiency viruses (HIV and SIV) use the chemokine receptor CCR5, in association with CD4, as coreceptor. During AIDS progression, HIV-1 and HIV-2 often adapt to use additional cofactors, particularly CXCR4. In contrast, SIV isolates do not use CXCR4, but other coreceptors such as BOB/GPR15 and Bonzo/STRL33. Only limited information is currently available on usage of BOB/GPR15 and Bonzo/STRL33 by HIV-1. Therefore, we investigated a panel of gp160 clones from 15 primary isolates, representing 5 different subtypes, for utilization of these cofactors. The majority of HIV-1 envelopes mediated entry into BOB/GPR15-expressing cells, albeit often with low efficiency. Usage of Bonzo/STRL33 was less common and usually inefficient. To investigate if HIV-1 entry via these orphan receptors is sufficient to allow virus replication, 15 uncloned primary HIV-1 isolates and 7 molecular clones were used to infect target cells expressing CD4 and Bonzo/STRL33 or BOB/GPR15. Three primary isolates and two molecular clones replicated efficiently in cells expressing BOB/GPR15. Two of these isolates were X4-tropic, two were R5X4-tropic and one was R5-tropic. In contrast, none of the HIV-1 variants showed significant levels of replication in Bonzo/STRL33-expressing cells. Our data show that some HIV-1 isolates of different genetic subtype and of different biological phenotype use BOB/GPR15 for productive infection and suggest that this cofactor may play a role in HIV-1 pathogenesis and transmission.

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1999-05-01
2024-04-24
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References

  1. Alkhatib G., Combadiere C., Broder C. C., Feng Y., Kennedy P. E., Murphy P. M., Berger E. A. 1996; CC-CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272:1955–1958
    [Google Scholar]
  2. Alkhatib G., Liao F., Berger E. A., Farber J. M., Peden K. W. 1997; A new SIV co-receptor, STRL33 [letter]. Nature 388:238
    [Google Scholar]
  3. Ashorn P. A., Berger E. A., Moss B. 1990; Human immunodeficiency virus envelope glycoprotein/CD4-mediated fusion of non-primate cells with human cells. Journal of Virology 64:2149–2156
    [Google Scholar]
  4. Berger E. A. 1997; HIV entry and tropism: the chemokine receptor connection. AIDS 11:3–16
    [Google Scholar]
  5. Bieniasz P. D., Cullen B. R. 1998; Chemokine receptors and human immunodeficiency virus infection. Frontiers in Bioscience 3:44–58
    [Google Scholar]
  6. Bjorndal A., Deng H., Jansson M., Fiore J. R., Colognesi C., Karlsson A., Albert J., Scarlatti G., Littman D. R., Fenyo E. M. 1997; Coreceptor usage of primary human immunodeficiency virus type 1 isolates varies according to biological phenotype. Journal of Virology 71:7478–7487
    [Google Scholar]
  7. Chen Z., Zhou P., Ho D. D., Landau N. R., Marx P. A. 1997; Genetically divergent strains of simian immunodeficiency virus use CCR5 as a coreceptor for entry. Journal of Virology 71:2705–2714
    [Google Scholar]
  8. Choe H., Farzan M., Sun Y., Sullivan N., Rollins B., Ponath P. D., Wu L., Mackay C. R., LaRosa G., Newman W., Gerard N., Gerard C., Sodroski J. 1996; The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85:1135–1148
    [Google Scholar]
  9. Choe H., Farzan M., Konkel M., Martin K., Sun Y., Marcon L., Cayabyab M., Berman M., Dorf M. E., Gerard N., Gerard C., Sodroski J. 1998; The orphan seven-transmembrane receptor apj supports the entry of primary T-cell-line-tropic and dualtropic human immunodeficiency virus type 1. Journal of Virology 72:6113–6118
    [Google Scholar]
  10. Connor R. I., Chen B. K., Choe S., Landau N. R. 1995; Vpr is required for efficient replication of HIV-1 in mononuclear phagocytes. Virology 206:935–944
    [Google Scholar]
  11. Dalgleish A. G., Beverley P. C. L., Clapham P. R., Crawford D. H., Greaves M. F., Weiss R. A. 1984; The CD4 (T4) antigen is an essential component of the receptor for the AIDS virus. Nature 312:763–767
    [Google Scholar]
  12. Deng H., Liu R., Ellmeier W., Choe S., Unutmaz D., Burkhart M., Di Marzio P., Marmon S., Sutton R. E., Hill C. M., Davis C. B., Peiper S. C., Schall T. J., Littman D. R., Landau N. R. 1996; Identification of a major co-receptor for primary isolates of HIV-1. Nature 381:661–666
    [Google Scholar]
  13. Deng H. K., Unutmaz D., KewalRamani V. N., Littman D. R. 1997; Expression cloning of new receptors used by simian and human immunodeficiency viruses. Nature 388:296–300
    [Google Scholar]
  14. Doranz B. J., Rucker J., Yi Y., Smyth R. J., Samson M., Peiper S. C., Parmentier M., Collman R. G., Doms R. W. 1996; A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell 85:1149–1158
    [Google Scholar]
  15. Dragic T., Litwin V., Allaway G. P., Martin S. R., Huang Y., Nagashima K. A., Cayanan C., Maddon P. J., Koup R. A., Moore J. P., Paxton W. A. 1996; HIV-1 entry into CD4 + cells is mediated by the chemokine receptor CC-CKR-5. Nature 381:667–673
    [Google Scholar]
  16. Edinger A. L., Amedee A., Miller K., Doranz B. J., Endres M., Sharron M., Samson M., Lu Z. H., Clements J. E., Murphey-Corb M., Peiper S. C., Parmentier M., Broder C. C., Doms R. W. 1997; Differential utilization of CCR5 by macrophage and T cell tropic simian immunodeficiency virus strains. Proceedings of the National Academy of Sciences, USA 94:4005–4010
    [Google Scholar]
  17. Edinger A. L., Hoffman T. L., Sharron M., Lee B., O’Dowd B., Doms R. W. 1998; Use of GPR1, GPR15, and STRL33 as coreceptors by diverse human immunodeficiency virus type 1 and simian immunodeficiency virus envelope proteins. Virology 249:367–378
    [Google Scholar]
  18. Farzan M., Choe H., Martin K., Maroon L., Hofmann W., Karlsson G., Sun Y., Barrett P., Marchand N., Sullivan N., Gerard N., Gerard C., Sodroski J. 1997; Two orphan seven-transmembrane segment receptors which are expressed in CD4-positive cells support simian immunodeficiency virus infection. Journal of Experimental Medicine 186:405–411
    [Google Scholar]
  19. Feng Y., Broder C. C., Kennedy P. E., Berger E. A. 1996; HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272:872–877
    [Google Scholar]
  20. Gao F., Yue L., White A. T., Pappas P. G., Barchue J., Hanson A. P., Greene B. M., Sharp P. M., Shaw G. M., Hahn B. H. 1992; Human infection by genetically diverse SIVSM-related HIV-2 in west Africa. Nature 358:495–499
    [Google Scholar]
  21. Gao F., Yue L., Craig S., Thornton C. L., Robertson D. L., McCutchan F. E., Bradac J. A., Sharp P. M., Hahn B. H. 1994; Genetic variation of HIV type 1 in four World Health Organization-sponsored vaccine evaluation sites: generation of functional envelope (glycoprotein 160) clones representative of sequence subtypes A, B, C, and E. WHO Network for HIV Isolation and Characterization. AIDS Research and Human Retroviruses 10:1359–1368
    [Google Scholar]
  22. Gao F., Morrison S. G., Robertson D. L., Thornton C. L., Craig S., Karlsson G., Sodroski J., Morgado M., Galvao-Castro B., von Briesen H., Hahn B. H. 1996; Molecular cloning and analysis of functional envelope genes from human immunodeficiency virus type 1 sequence subtypes A through G. The WHO and NIAID Networks for HIV Isolation and Characterization. Journal of Virology 70:1651–1667
    [Google Scholar]
  23. James W., Weiss R. A., Simon J. H. 1996; The receptor for HIV: dissection of CD4 and studies on putative accessory factors. Current Topics in Microbiology and Immunology 205:137–158
    [Google Scholar]
  24. Kirchhoff F., Pӧhlmann S., Hamacher M., Means R. E., Kraus T., Überla K., Di Marzio P. 1997; SIVmac variants with differential T-cell and macrophage tropism use CCR5, and an unidentified cofactor expressed in CEM x 174 cells for efficient entry. Journal of Virology 71:6509–6516
    [Google Scholar]
  25. Kozak S. L., Platt E. J., Madani N., Ferro F. E., Peden K., Kabat D. 1997; CD4, CXCR-4, and CCR5 dependencies for infections by primary patient and laboratory-adapted isolates of human immunodeficiency virus type 1. Journal of Virology 71:873–882
    [Google Scholar]
  26. Li Y., Hui H., Burgess C. J., Price R. W., Sharp P. M., Hahn B. H., Shaw G. M. 1992; Complete nucleotide sequence, genome organization, and biological properties of human immunodeficiency virus type 1 in vivo: evidence for limited defectivness and complementation. Journal of Virology 66:6587–6600
    [Google Scholar]
  27. Liao F., Alkhatib G., Peden K. W., Sharma G., Berger E. A., Farber J. M. 1997; STRL33, a novel chemokine receptor-like protein, functions as a fusion cofactor for both macrophage-tropic and T cell line-tropic HIV-1. Journal of Experimental Medicine 185:2015–2023
    [Google Scholar]
  28. Liu R., Paxton W. A., Choe S., Ceradini D., Martin S. R., Horuk R., MacDonald M. E., Stuhlmann H., Koup R. A., Landau N. R. 1996; Homozygous defect in HIV-1 co-receptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86:367–377
    [Google Scholar]
  29. Maddon P. J., Dalgleish A. G., McDougal J. S., Clapham P. R., Weiss R. A., Axel R. 1986; The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell 47:333–348
    [Google Scholar]
  30. Marcon L., Choe H., Martin K. A., Farzan M., Ponath P. D., Wu L., Newman W., Gerard N., Gerard C., Sodroski J. 1997; Utilization of C-C chemokine receptor 5 by the envelope glycoproteins of a pathogenic simian immunodeficiency virus, SIVmac239. Journal of Virology 71:2522–2537
    [Google Scholar]
  31. Means R. E., Greenough T., Desrosiers R. C. 1997; Neutralization sensitivity of cell culture-passaged simian immunodeficiency virus. Journal of Virology 71:7895–7902
    [Google Scholar]
  32. Oberlin E., Amara A., Bachelerie F., Bessia C., Virelizier J. L., Arenzana-Seisdedos F., Schwartz O., Heard J. M., Clark-Lewis I., Legler D. F., Loetscher M., Baggiolini M., Moser B. 1996; The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 382:833–835
    [Google Scholar]
  33. Owen S. M., Ellenberger D., Rayfield M., Wiktor S., Michel P., Grieco M. H., Gao F., Hahn B. H., Lal R. B. 1998; Genetically divergent strains of human immunodeficiency virus type 2 use multiple coreceptors for viral entry. Journal of Virology 772:5425–5432
    [Google Scholar]
  34. Potts B. J. 1990 In Techniques in HIV Research pp 103–106 Edited by Aldovini A., Walker B. D. New York: Stockton;
    [Google Scholar]
  35. Rana S., Besson G., Cook D. G., Rucker J., Smyth R. J., Yi Y., Turner J., Guo H., Du J. -G., Peiper S. C., Lavi E., Samson M., Libert F., Liesnard C., Vassart G., Doms R. W., Parmentier M., Collman R. G. 1997; Role of CCR5 in infection of primary macrophages and lymphocytes by M-tropic strains of HIV: resistance to patient-derived and prototype isolates resulting from ccr5 mutation. Journal of Virology 71:3219–3227
    [Google Scholar]
  36. Rucker J., Edinger A. L., Sharron M., Samson M., Lee B., Berson J. F., Yi Y., Margulies B., Collman R. G., Doranz B. J., Parmentier M., Doms R. W. 1997; Utilization of chemokine receptors, orphan receptors, and herpesvirus-encoded receptors by diverse human and simian immunodeficiency viruses. Journal of Virology 71:8999–9007
    [Google Scholar]
  37. Samson M., Libert F., Doranz B. J., Rucker J., Liesnard C., Farber C. -M., Saragosti S., Lapoumeroulie C., Cogniaux J., Forceille C., Muyldermans G., Verhofsted C., Burtonboy G., Georges M., Imai T., Rana S., Yi Y., Smyth R. J., Collmam R. G., Doms R. W., Vassart G., Parmentier M. 1996; Resistance to HIV-1 infection of Caucasian individuals bearing mutant alleles of the CCR5 chemokine receptor gene. Nature 382:722–725
    [Google Scholar]
  38. Sharp P. M., Robertson D. L., Hahn B. H. 1995; Cross-species transmission and recombination of ′AIDS′ viruses. Philosophical Transactions of the Royal Society of London B Biological Sciences 349:41–47
    [Google Scholar]
  39. Zhang L., Huang Y., He T., Cao Y., Ho D. D. 1996; HIV-1 subtype and second-receptor use. Nature 383:768
    [Google Scholar]
  40. Zhang L., He T., Huang Y., Chen Z., Guo Y., Wu S., Kunstman K. J., Brown R. C., Phair J. P., Neuman A. U., Ho D. D., Wolinsky S. M. 1998a; Chemokine coreceptor usage by diverse primary isolates of human immunodeficiency virus type 1. Journal of Virology 72:9307–9312
    [Google Scholar]
  41. Zhang Y.-J., Dragic T., Cao Y., Kostrikis L., Kwon D. S., Littman D. R., Kewalramani V. N., Moore J. P. 1998b; Use of coreceptors other than CCR5 by non-syncytium-inducing adult and pediatric isolates of human immunodeficiency virus type 1 is rare in vitro. Journal of Virology 72:9337–9344
    [Google Scholar]
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