Replicative fitness of CCR5-using and CXCR4-using human immunodeficiency virus type 1 biological clones

Virology

Volumn 347, Issue 1, 2006, Pages 65-74

  Ariën, Kevin K ^a   Gali, Youssef ^a   El Abdellati, Abdelkarim ^a   Heyndrickx, Leo ^a   Janssens, Wouter ^a   Vanham, Guido ^a,b  

^a INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

AIDS; CCR5; CD4 + T cell; CXCR4; Dendritic cell; fitness; HIV 1; Replication capacity; Transmission

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ARTICLE; CD4+ T LYMPHOCYTE; COCULTURE; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LYMPHOCYTE CULTURE; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; T LYMPHOCYTE; VIROGENESIS; VIRUS CELL INTERACTION; VIRUS ISOLATION; VIRUS REPLICATION; VIRUS TRANSMISSION;

ACQUIRED IMMUNODEFICIENCY SYNDROME; AMINO ACID SEQUENCE; BASE SEQUENCE; CLONING, MOLECULAR; DNA, VIRAL; GENES, ENV; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; LEUKOCYTES, MONONUCLEAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PHENOTYPE; PHYLOGENY; RECEPTORS, CCR5; RECEPTORS, CXCR4; SEQUENCE HOMOLOGY, AMINO ACID; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 33645028309     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2005.11.045     Document Type: Article

References (59)

1. A. Abebe, D. Demissie, J. Goudsmit, M. Brouwer, C.L. Kuiken, G. Pollakis, H. Schuitemaker, A.L. Fontanet, and T.F. Rinke de Wit HIV-1 subtype C syncytium- and non-syncytium-inducing phenotypes and coreceptor usage among Ethiopian patients with AIDS AIDS 13 11 1999 1305 1311
2. W.W. Agace, A. Amara, A.I. Roberts, J.L. Pablos, S. Thelen, M. Uguccioni, X.Y. Li, J. Marsal, F. Arenzana-Seisdedos, T. Delaunay, E.C. Ebert, B. Moser, and C.M. Parker Constitutive expression of stromal derived factor-1 by mucosal epithelia and its role in HIV transmission and propagation Curr. Biol. 10 6 2000 325 328
3. K.K. Ariën, R.M. Troyer, Y. Gali, R.L. Colebunders, E.J. Arts, and G. Vanham Replicative fitness of historical and recent HIV-1 isolates suggests HIV-1 attenuation over time AIDS 19 15 2005 1555 1564
4. K.K. Ariën, A. Abraha, M.E. Quinones-Mateu, L. Kestens, G. Vanham, and E.J. Arts The replicative fitness of primary human immunodeficiency virus type 1 (HIV-1) group M, group O and HIV-2 isolates J. Virol. 79 14 2005 8979 8990
5. B. Asjo, L. Morfeldt-Manson, J. Albert, G. Biberfeld, A. Karlsson, K. Lidman, and E.M. Fenyo Replicative capacity of human immunodeficiency virus from patients with varying severity of HIV infection Lancet 2 8508 1986 660 662
6. S.C. Ball, A. Abraha, K.R. Collins, A.J. Marozsan, H. Baird, M.E. Quinones-Mateu, A. Penn-Nicholson, M. Murray, N. Richard, M. Lobritz, P.A. Zimmerman, T. Kawamura, A. Blauvelt, and E.J. Arts Comparing the ex vivo fitness of CCR5-tropic human immunodeficiency virus type 1 isolates of subtypes B and C J. Virol. 77 2 2003 1021 1038
7. E. Beirnaert, B. Willems, M. Peeters, A. Bouckaert, L. Heyndrickx, P. Zhong, K. Vereecken, S. Coppens, D. Davis, P. Ndumbe, W. Janssens, and G. van der Groen Design and evaluation of an in-house HIV-1 (group M and O), SIVmnd and SIVcpz antigen capture assay J. Virol. Methods 73 1 1998 65 70
8. E.A. Berger, P.M. Murphy, and J.M. Farber Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease Ann. Rev. Immunol. 17 1999 657 700
9. H. Blaak, M. Brouwer, L.J. Ran, F. de Wolf, and H. Schuitemaker In vitro replication kinetics of human immunodeficiency virus type 1 (HIV-1) variants in relation to virus load in long-term survivors of HIV-1 infection J. Infect. Dis. 177 3 1998 600 610
10. A. Blauvelt, H. Asada, M.W. Saville, V. Klaus-Kovtun, D.J. Altman, R. Yarchoan, and S.I. Katz Productive infection of dendritic cells by HIV-1 and their ability to capture virus are mediated through separate pathways J. Clin. Invest. 100 8 1997 2043 2053
11. M. Cornelissen, G. Mulder-Kampinga, J. Veenstra, F. Zorgdrager, C. Kuiken, S. Hartman, J. Dekker, L. van der Hoek, C. Sol, R. Coutinho, and J. Goudsmit Syncytium-inducing (SI) phenotype suppression at seroconversion after intramuscular inoculation of a non-syncytium-inducing/SI phenotypically mixed human immunodeficiency virus population J. Virol. 69 3 1995 1810 1888
12. T.B. Geijtenbeek, D.S. Kwon, R. Torensma, S.J. van Vliet, G.C. van Duijnhoven, J. Middel, I.L. Cornelissen, H.S. Nottet, V.N. KewalRamani, D.R. Littman, C.G. Figdor, and Y. van Kooyk DC-SIGN, a dendritic cell-specific HIV-1 binding protein that enhances trans-infection of T-cells Cell 100 5 2000 587 597
13. H.E. Gendelman, J.M. Orenstein, M.A. Martin, C. Ferrua, R. Mitra, T. Phipps, L.A. Wahl, H.C. Lane, A.S. Fauci, D.S. Burke, D. Skillman, and M.S. Meltzer Efficient isolation and propagation of human immunodeficiency virus on recombinant colony-stimulating factor 1-treated monocytes J. Exp. Med. 167 4 1988 1428 1441
14. J.-C. Grivel, and L.B. Margolis CCR5- and CXCR4-tropic HIV-1 are equally cytopathic for their T-cell targets in human lymphoid tissue Nat. Med. 5 3 1999 344 346
15. P. Gupta, K.B. Collins, D. Ratner, S. Watkins, G.J. Naus, D.V. Landers, and B.K. Patterson Memory CD4(+) T cells are the earliest detectable human immunodeficiency virus type 1 (HIV-1)-infected cells in the female genital mucosal tissue during HIV-1 transmission in an organ culture system J. Virol. 76 19 2002 9868 9876
16. J.M. Harouse, A. Gettie, R.C. Tan, J. Blanchard, and C. Cheng-Mayer Distinct pathogenic sequela in rhesus macaques infected with CCR5 or CXCR4 utilizing SHIVs Science 284 5415 1999 816 819
17. P.R. Harrigan, S. Bloor, and B.A. Larder Relative replicative fitness of zidovudine-resistant human immunodeficiency virus type 1 isolates in vitro J. Virol. 72 5 1998 3773 3778
18. F. Hlakdik, G. Lentz, R.E. Akridge, G. Peterson, H. Kelley, A. McElroy, and M.J. McElrath Dendritic cell-T-cell interactions support coreceptor-independent human immunodeficiency virus type 1 transmission in the human genital tract J. Virol. 73 7 1999 5833 5842
19. P. Jayakumar, I. Berger, F. Autschbach, M. Weinstein, B. Funke, E. Verdin, M.A. Goldsmith, and O.T. Keppler Tissue-resident macrophages are productively infected ex vivo by primary X4 isolates of human immunodeficiency virus type 1 J. Virol. 79 8 2005 5220 5226
20. F.A. Koning, R.P. van Rij, and H. Schuitemaker Biological and molecular aspects of HIV-1 coreceptor usage C.L. Kuiken B. Foley E. Freed B. Hahn B. Korber P.A. Marx F. McCutchan J.W. Mellors S. Wolinsky HIV Sequence Compendium 2002 2002 Theoretical Biology and Biophysics Group, Los Alamos National Laboratory Los Alamos, NM (LA-UR 03-3564)
21. + cell depletion and progression to AIDS Ann. Intern. Med. 118 9 1993 681 688
22. J.F. Kreisberg, D. Kwa, B. Schramm, V. Trautner, R. Connor, H. Schuitemaker, J.I. Mullins, A.B. van 't Wout, and M.A. Goldsmith Cytopathicity of human immunodeficiency virus type 1 primary isolates depends on coreceptor usage and not patient disease status J. Virol. 75 18 2001 8842 8847
23. + T cells Nature 343 7037 2005 1148 1152
24. A.J. Marozsan, D.M. Moore, M.A. Lobritz, E. Fraundorf, A. Abraha, J.D. Reeves, and E.J. Arts Differences in the fitness of two diverse wild-type human immunodeficiency virus type 1 isolates are related to the efficiency of cell binding and entry J. Virol. 79 11 2005 7121 7134
25. J. Martinez-Picado, A.V. Savara, L. Sutton, and R.T. D'Aquila Replicative fitness of protease inhibitor-resistant mutants of human immunodeficiency virus type 1 J. Virol. 73 5 1999 3744 3752
26. + T cells in multiple tissues during acute SIV infection Nature 434 7037 2005 1093 1097
27. J.P. Moore, S.G. Kitchen, P. Pugach, and J.A. Zack The CCR5 and CXCR4 coreceptors-central to understanding the transmission and pathogenesis of human immunodeficiency virus type 1 infection AIDS Res. Hum. Retroviruses 20 1 2004 111 126
28. M. Nijhuis, R. Schuurman, D. de Jong, J. Erickson, E. Gustchina, J. Albert, P. Schipper, S. Gulnik, and C.A. Boucher Increased fitness of drug resistant HIV-1 protease as a result of acquisition of compensatory mutations during suboptimal therapy AIDS 13 17 1999 2349 2359
29. C. Nobile, C. Petit, A. Moris, K. Skrabal, J.-P. Abastado, F. Mammano, and O. Schwartz Covert human immunodeficiency virus replication in dendritic cells and in DC-SIGN-expressing cells promotes long-term transmission to lymphocytes J. Virol. 79 9 2005 5386 5399
30. J.M. Orenstein, C. Fox, and S.M. Wahl Macrophages as a source of HIV during opportunistic infections Science 276 5320 1997 1857 1861
31. M. Peeters, R. Vincent, J.L. Perret, M. Lasky, D. Patrel, F. Liegeois, V. Courgnaud, R. Seng, T. Matton, S. Molinier, and E. Delaporte Evidence for differences in MT2 cell tropism according to genetic subtypes of HIV-1: syncytium-inducing variants seem rare among subtype C HIV-1 viruses J. Acquired Immune Defic. Syndr. Hum. Retrovirol. 20 2 1999 115 121
32. S.M. Philpott HIV-1 coreceptor usage, transmission, and disease progression Curr. HIV Res. 1 2 2003 217 227
33. M.A. Poles, J. Elliot, P. Taing, P.A. Anton, and I.S. Chen A preponderance of CCR5(+) CXCR4(+) mononuclear cells enhances gastrointestinal mucosal susceptibility to human immunodeficiency virus type 1 infection J. Virol. 75 18 2001 8390 8399
34. M. Prakash, M.S. Kapembwa, F. Gotch, and S. Patterson Chemokine receptor expression on mucosal dendritic cells from the endocervix of healthy women J. Infect. Dis. 190 2 2004 246 250
35. M.E. Quinones-Mateu, and E.J. Arts HIV-1 fitness: implications for drug resistance, disease progression, and global epidemic evolution C.L. Kuiken B. Foley B. Hahn B. Korber P.A. Marx F. McCutchan J.W. Mellors S. Wolinsky HIV Sequence Compendium 2001 2001 Theoretical Biology and Biophysics Group, Los Alamos National Laboratory Los Alamos, NM (LA-UR 02-2877)
36. M.E. Quinones-Mateu, S.C. Ball, A.J. Marozsan, V.S. Torre, J.L. Albright, G. Vanham, G. van der Groen, R.L. Colebunders, and E.J. Arts A dual infection/competition assay shows a correlation between ex vivo human immunodeficiency virus type 1 fitness and disease progression J. Virol. 74 19 2000 9222 9233
37. H.R. Rangel, J. Weber, B. Chakraborty, A. Gutierrez, M.L. Marotta, M. Mirza, P. Kiser, M.A. Martinez, J.A. Este, and M.E. Quinones-Mateu Role of the human immunodeficiency virus type 1 envelope gene in viral fitness J. Virol. 77 16 2003 9069 9073
38. L.J. Reed, and H. Muench A simple method of estimating fifty percent endpoints Am. J. Hyg. 27 1938 493 497
39. H. Schmidtmayerova, M. Alfano, G. Nuovo, and M. Bukrinsky Human immunodeficiency virus type 1 T-lymphotropic strains enter macrophages via a CD4- and CXCR4-mediated pathway: replication is restricted at a postentry level J. Virol. 72 6 1998 4633 4642
40. H. Schuitemaker, N.A. Kootstra, R.E. de Goede, F. de Wolf, F. Miedema, and M. Tersmette Monocytotropic human immunodeficiency virus type 1 (HIV-1) variants detectable in all stages of HIV-1 infection lack T-cell line tropism and syncytium-inducing ability in primary T-cell culture J. Virol. 65 1 1991 356 363
41. H. Schuitemaker, M. Koot, N.A. Kootstra, M.W. Dercksen, R.E. de Goede, R.P. van Steenwijk, J.M. Lange, J.K. Schattenkerk, F. Miedema, and M. Tersmette Biological phenotype of human immunodeficiency virus type 1 clones at different stages of infection: progression of disease is associated with a shift from monocytotropic to T-cell-tropic virus population J. Virol. 66 3 1992 1354 1360
42. N. Shimizu, Y. Haraguchi, Y. Takeuchi, Y. Soda, K. Kanbe, and H. Hoshino Changes and discrepancies between cell tropisms and coreceptor uses of human immunodeficiency virus type 1 induced by single point mutations ate the V3 tip of the env protein Virology 259 1999 324 333
43. P. Sivard, W. Berlier, B. Picard, O. Sabido, C. Genin, and L. Misery HIV-1 infection of Langerhans cells in a reconstructed vaginal mucosa J. Infect. Dis. 190 2 2004 227 235
44. M. Tersmette, R.A. Gruters, F. de Wolf, R.E. de Goede, J.M. Lange, P.T. Schellekens, J. Goudsmit, H.G. Huisman, and F. Miedema Evidence for a role of virulent human immunodeficiency virus (HIV) variants in the pathogenesis of acquired immunodeficiency syndrome: studies on sequential HIV isolates J. Virol. 63 5 1989 2118 2125
45. R.M. Troyer, K.R. Collins, A. Abraha, E. Fraundorf, D.M. Moore, R.W. Krizan, Z. Toosi, R.L. Colebunders, M.A. Jensen, J.I. Mullins, G. Vanham, and E.J. Arts Changes in human immunodeficiency virus Type 1 fitness and genetic diversity during disease progression J. Virol. 79 14 2005 9006 9018
46. Y. Van de Peer, and R. De Wachter TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment Comput. Appl. Biosci. 10 1994 570 596
47. G. Vanham, L. Penne, H. Allemeersch, L. Kestens, B. Willems, G. van der Groen, K.T. Jeang, Z. Toossi, and E. Rich Modeling HIV transfer between dendritic cells and T cells: importance of HIV phenotype, dendritic cell-T cell contact and T-cell activation AIDS 14 15 2000 2299 2311
48. G. Vanham, D. Davis, B. Willems, L. Penne, L. Kestens, W. Janssens, and G. van der Groen Dendritic cells, exposed to primary, mixed phenotype HIV-1 isolates preferentially, but not exclusively, replicate CCR5-using clones AIDS 14 12 2000 1874 1876
49. R.P. van Rij, H. Blaak, J.A. Visser, M. Brouwer, R. Rientsma, S. Broersen, A.-M. de Roda Husman, and H. Schuitemaker Differential coreceptor expression allows for independent evolution of non-syncytium-inducing and syncytium-inducing HIV-1 J. Clin. Invest. 106 8 2000 1039 1052
50. A.B. van 't Wout, N.A. Kootstra, G.A. Mulder-Kampinga, N. Albrecht-van Lent, H.J. Scherpbier, J. Veenstra, K. Boer, R.A. Coutinho, F. Miedema, and H. Schuitemaker Macrophage-tropic variants initiate human immunodeficiency virus type 1 infection after sexual, parenteral, and vertical transmission J. Clin. Invest. 94 5 1994 2060 2067
51. A.B. van 't Wout, H. Blaak, L.J. Ran, M. Brouwer, C. Kuiken, and H. Schuitemaker Evolution of syncytium-inducing and non-syncytium-inducing biological virus clones in relation to replication kinetics during the course of human immunodeficiency virus type 1 J. Virol. 72 6 1998 5099 5107
52. R.S. Veazey, K.G. Mansfield, I.C. Tham, A.C. Carville, D.E. Shvetz, A.E. Forand, and A.A. Lackner Dynamics of CCR5 expression by CD4(+) T cells in lymphoid tissues during simian immunodeficiency virus infection J. Virol. 74 2000 11001 11007
53. R.S. Veazey, P.A. Marx, and A.A. Lackner The mucosal immune system: primary target for HIV infection and AIDS Trends Immunol. 22 11 2001 626 633
54. F. Verrier, A.M. Borman, D. Brand, and M. Girard Role of the HIV type 1 glycoprotein 120 V3 loop in determining coreceptor usage AIDS Res. Hum. Retroviruses 15 1999 731 743
55. R. Zamarchi, P. Allavena, A. Borsetti, L. Stievano, V. Tosello, N. Marcato, G. Esposito, V. Roni, C. Paganin, G. Bianchi, F. Titti, P. Verani, G. Gerosa, and A. Amadori Expression and functional activity of CXCR-4 and CCR-5 chemokine receptors in human thymocytes Clin. Exp. Immunol. 127 2 2002 321 330
56. L. Zhang, Y. Huang, T. He, Y. Cao, and D.D. Ho HIV-1 subtype and second-receptor use Nature 383 6603 1996 768
57. + T cells Science 286 5443 1999 1353 1357
58. P. Zhong, M. Peeters, W. Janssens, K. Fransen, L. Heyndrickx, G. Vanham, B. Willems, P. Piot, and G. van der Groen Correlation between genetic and biological properties of biologically cloned HIV type 1 viruses representing subtypes A, B, and D AIDS Res. Hum. Retroviruses 11 2 1995 239 248
59. T. Zhu, H. Mo, N. Wang, D.S. Nam, Y. Cao, R.A. Koup, and D.D. Ho Genotypic and phenotypic characterization of HIV-1 patients with primary infection Science 261 5125 1993 1179 1181