High intrapatient HIV-1 evolutionary rate is associated with CCR5-to-CXCR4 coreceptor switch

Infection, Genetics and Evolution

Volumn 19, Issue , 2013, Pages 369-377

  Mild, Mattias ^a,b   Gray, Rebecca R ^c   Kvist, Anders ^d   Lemey, Philippe ^e   Goodenow, Maureen M ^f   Fenyö, Eva Maria ^d   Albert, Jan ^a   Salemi, Marco ^f   Esbjörnsson, Joakim ^a,e,g   Medstrand, Patrik ^d,g  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d LUND UNIVERSITY   (Sweden)

^e REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^f UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^g LUND UNIVERSITY   (Sweden)

Author keywords

CCR5 and CXCR4 use; Coreceptor switch; Hierarchical phylogenetic model; Intrapatient HIV 1 evolutionary rate; R5 and X4 virus populations; Synonymous and non synonymous substitutions

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; GLYCOPROTEIN GP 120;

AMINO ACID SUBSTITUTION; ARTICLE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; DISEASE COURSE; ENVELOPE GENE; EVOLUTIONARY RATE; GENETIC SELECTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; SELECTION PRESSURE; UNINDEXED SEQUENCE; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CCR5 AND CXCR4 USE; CORECEPTOR SWITCH; HIERARCHICAL PHYLOGENETIC MODEL; INTRAPATIENT HIV-1 EVOLUTIONARY RATE; R5 AND X4 VIRUS POPULATIONS; SYNONYMOUS AND NON-SYNONYMOUS SUBSTITUTIONS;

BAYES THEOREM; EVOLUTION, MOLECULAR; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; PHYLOGENY; RECEPTORS, CCR5; RECEPTORS, CXCR4; VIRAL TROPISM;

EID: 84885174441     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2013.05.004     Document Type: Article

References (70)

1. Berger E.A. HIV entry and tropism: the chemokine receptor connection. AIDS 1997, 11(Suppl. A):S3-S16.
2. Brieu N., Portales P., Carles M.J., Corbeau P. Interleukin-7 induces HIV type 1 R5-to-X4 switch. Blood 2011, 117:2073-2074.
3. Briggs D.R., Tuttle D.L., Sleasman J.W., Goodenow M.M. Envelope V3 amino acid sequence predicts HIV-1 phenotype (co-receptor usage and tropism for macrophages). AIDS 2000, 14:2937-2939.
4. Bruen T.C., Philippe H., Bryant D. A simple and robust statistical test for detecting the presence of recombination. Genetics 2006, 172:2665-2681.
5. Bunnik E.M., Quakkelaar E.D., van Nuenen A.C., Boeser-Nunnink B., Schuitemaker H. Increased neutralization sensitivity of recently emerged CXCR4-using human immunodeficiency virus type 1 strains compared to coexisting CCR5-using variants from the same patient. J. Virol. 2007, 81:525-531.
6. Burcham J., Marmor M., Dubin N., Tindall B., Cooper D.A., Berry G., Penny R. CD4% is the best predictor of development of AIDS in a cohort of HIV-infected homosexual men. AIDS 1991, 5:365-372.
7. Carrillo A., Ratner L. Cooperative effects of the human immunodeficiency virus type 1 envelope variable loops V1 and V3 in mediating infectivity for T cells. J. Virol. 1996, 70:1310-1316.
8. Carrillo A., Ratner L. Human immunodeficiency virus type 1 tropism for T-lymphoid cell lines: role of the V3 loop and C4 envelope determinants. J. Virol. 1996, 70:1301-1309.
9. Coetzer M., Nedellec R., Salkowitz J., McLaughlin S., Liu Y., Heath L., Mullins J.I., Mosier D.E. Evolution of CCR5 use before and during coreceptor switching. J. Virol. 2008, 82:11758-11766.
10. Connor R.I., Sheridan K.E., Ceradini D., Choe S., Landau N.R. Change in coreceptor use correlates with disease progression in HIV-1 - infected individuals. J. Exp. Med. 1997, 185:621-628.
11. De Jong J.J., De Ronde A., Keulen W., Tersmette M., Goudsmit J. Minimal requirements for the human immunodeficiency virus type 1 V3 domain to support the syncytium-inducing phenotype: analysis by single amino acid substitution. J. Virol. 1992, 66:6777-6780.
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. Identification of a major co-receptor for primary isolates of HIV-1. Nature 1996, 381:661-666.
13. Drummond A.J., Ho S.Y., Phillips M.J., Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 2006, 4:e88.
14. Drummond A.J., Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007, 7:214.
15. Drummond A.J., Rambaut A., Shapiro B., Pybus O.G. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 2005, 22:1185-1192.
16. Edo-Matas D., Lemey P., Tom J.A., Serna-Bolea C., Van Den Blink A.E., Van Wout A.B., Schuitemaker H., Suchard M.A. Impact of CCR5delta32 host genetic background and disease progression on HIV-1 intrahost evolutionary processes: efficient hypothesis testing through hierarchical phylogenetic models. Mol. Biol. Evol. 2011, 28:1605-1616.
17. Edo-Matas D., Rachinger A., Setiawan L.C., Boeser-Nunnink B.D., Van Wout A.B., Lemey P., Schuitemaker H. The evolution of human immunodeficiency virus type-1 (HIV-1) envelope molecular properties and coreceptor use at all stages of infection in an HIV-1 donor-recipient pair. Virology 2012, 422:70-80.
18. Esbjornsson J., Mansson F., Martinez-Arias W., Vincic E., Biague A.J., da Silva Z.J., Fenyo E.M., Norrgren H., Medstrand P. Frequent CXCR4 tropism of HIV-1 subtype A and CRF02_AG during late-stage disease - indication of an evolving epidemic in West Africa. Retrovirology 2010, 7:23.
19. Fatkenheuer G., Nelson M., Lazzarin A., Konourina I., Hoepelman A.I., Lampiris H., Hirschel B., Tebas P., Raffi F., Trottier B., Bellos N., Saag M., Cooper D.A., Westby M., Tawadrous M., Sullivan J.F., Ridgway C., Dunne M.W., Felstead S., Mayer H., van der Ryst E. Subgroup analyses of maraviroc in previously treated R5 HIV-1 infection. N. Engl. J. Med. 2008, 359:1442-1455.
20. Feng Y., Broder C.C., Kennedy P.E., Berger E.A. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 1996, 272:872-877.
21. Fiser A.L., Vincent T., Brieu N., Lin Y.L., Portales P., Mettling C., Reynes J., Corbeau P. High CD4(+) T-cell surface CXCR4 density as a risk factor for R5 to X4 switch in the course of HIV-1 infection. J. Acquir. Immune Defic. Syndr. 2010, 55:529-535.
22. Fouchier R.A., Brouwer M., Broersen S.M., Schuitemaker H. Simple determination of human immunodeficiency virus type 1 syncytium-inducing V3 genotype by PCR. J. Clin. Microbiol. 1995, 33:906-911.
23. Fouchier R.A., Groenink M., Kootstra N.A., Tersmette M., Huisman H.G., Miedema F., Schuitemaker H. Phenotype-associated sequence variation in the third variable domain of the human immunodeficiency virus type 1 gp120 molecule. J. Virol. 1992, 66:3183-3187.
24. Giorgi J.V., Hultin L.E., McKeating J.A., Johnson T.D., Owens B., Jacobson L.P., Shih R., Lewis J., Wiley D.J., Phair J.P., Wolinsky S.M., Detels R. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J. Infect. Dis. 1999, 179:859-870.
25. Goldman N., Yang Z. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol. Biol. Evol. 1994, 11:725-736.
26. Guindon S., Delsuc F., Dufayard J.F., Gascuel O. Estimating maximum likelihood phylogenies with PhyML. Methods Mol. Biol. 2009, 537:113-137.
27. Hartley O., Klasse P.J., Sattentau Q.J., Moore J.P. V3: HIV's switch-hitter. AIDS Res. Hum. Retroviruses 2005, 21:171-189.
28. Heger E., Thielen A., Gilles R., Obermeier M., Lengauer T., Kaiser R., Trapp S. APOBEC3G/F as one possible driving force for co-receptor switch of the human immunodeficiency virus-1. Med. Microbiol. Immunol. 2012, 201:7-16.
29. Ho S.H., Tasca S., Shek L., Li A., Gettie A., Blanchard J., Boden D., Cheng-Mayer C. Coreceptor switch in R5-tropic simian/human immunodeficiency virus-infected macaques. J. Virol. 2007, 81:8621-8633.
30. Huang W., Toma J., Fransen S., Stawiski E., Reeves J.D., Whitcomb J.M., Parkin N., Petropoulos C.J. Coreceptor tropism can be influenced by amino acid substitutions in the gp41 transmembrane subunit of human immunodeficiency virus type 1 envelope protein. J. Virol. 2008, 82:5584-5593.
31. Hudson R.R., Boos D.D., Kaplan N.L. A statistical test for detecting geographic subdivision. Mol. Biol. Evol. 1992, 9:138-151.
32. Huson D.H., Bryant D. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 2006, 23:254-267.
33. Jansson M., Backstrom E., Bjorndal A., Holmberg V., Rossi P., Fenyo E.M., Popovic M., Albert J., Wigzell H. Coreceptor usage and RANTES sensitivity of non-syncytium-inducing HIV-1 isolates obtained from patients with AIDS. J. Hum. Virol. 1999, 2:325-338.
34. Jansson M., Backstrom E., Scarlatti G., Bjorndal A., Matsuda S., Rossi P., Albert J., Wigzell H. Length variation of glycoprotein 120 V2 region in relation to biological phenotypes and coreceptor usage of primary HIV type 1 isolates. AIDS Res. Hum. Retroviruses 2001, 17:1405-1414.
35. Karlsson A., Parsmyr K., Sandstrom E., Fenyo E.M., Albert J. MT-2 cell tropism as prognostic marker for disease progression in human immunodeficiency virus type 1 infection. J. Clin. Microbiol. 1994, 32:364-370.
36. Kass R.E., Raftery A.E. Bayes factors. J. Am. Statist. Assoc. 1995, 90:773-795.
37. Keele B.F., Giorgi E.E., Salazar-Gonzalez J.F., Decker J.M., Pham K.T., Salazar M.G., Sun C., Grayson T., Wang S., Li H., Wei X., Jiang C., Kirchherr J.L., Gao F., Anderson J.A., Ping L.H., Swanstrom R., Tomaras G.D., Blattner W.A., Goepfert P.A., Kilby J.M., Saag M.S., Delwart E.L., Busch M.P., Cohen M.S., Montefiori D.C., Haynes B.F., Gaschen B., Athreya G.S., Lee H.Y., Wood N., Seoighe C., Perelson A.S., Bhattacharya T., Korber B.T., Hahn B.H., Shaw G.M. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. USA 2008, 105:7552-7557.
38. Koot M., Keet I.P., Vos A.H., de Goede R.E., Roos M.T., Coutinho R.A., Miedema F., Schellekens P.T., Tersmette M. Prognostic value of HIV-1 syncytium-inducing phenotype for rate of CD4+ cell depletion and progression to AIDS. Ann. Intern. Med. 1993, 118:681-688.
39. Koot M., van Leeuwen R., de Goede R.E., Keet I.P., Danner S., Eeftinck Schattenkerk J.K., Reiss P., Tersmette M., Lange J.M., Schuitemaker H. Conversion rate towards a syncytium-inducing (SI) phenotype during different stages of human immunodeficiency virus type 1 infection and prognostic value of SI phenotype for survival after AIDS diagnosis. J. Infect. Dis. 1999, 179:254-258.
40. Labrosse B., Treboute C., Brelot A., Alizon M. Cooperation of the V1/V2 and V3 domains of human immunodeficiency virus type 1 gp120 for interaction with the CXCR4 receptor. J. Virol. 2001, 75:5457-5464.
41. Lee H.Y., Perelson A.S., Park S.C., Leitner T. Dynamic correlation between intrahost HIV-1 quasispecies evolution and disease progression. PLoS Comput. Biol. 2008, 4:e1000240.
42. Lemey P., Kosakovsky Pond S.L., Drummond A.J., Pybus O.G., Shapiro B., Barroso H., Taveira N., Rambaut A. Synonymous substitution rates predict HIV disease progression as a result of underlying replication dynamics. PLoS Comput. Biol. 2007, 3(e29).
43. Markham R.B., Wang W.C., Weisstein A.E., Wang Z., Munoz A., Templeton A., Margolick J., Vlahov D., Quinn T., Farzadegan H., Yu X.F. Patterns of HIV-1 evolution in individuals with differing rates of CD4 T cell decline. Proc. Natl. Acad. Sci. USA 1998, 95:12568-12573.
44. Mikhail M., Wang B., Lemey P., Beckthold B., Vandamme A.M., Gill M.J., Saksena N.K. Role of viral evolutionary rate in HIV-1 disease progression in a linked cohort. Retrovirology 2005, 2:41.
45. Mild M., Esbjornsson J., Fenyo E.M., Medstrand P. Frequent intrapatient recombination between human immunodeficiency virus type 1 R5 and X4 envelopes: implications for coreceptor switch. J. Virol. 2007, 81:3369-3376.
46. Mild M., Kvist A., Esbjornsson J., Karlsson I., Fenyo E.M., Medstrand P. Differences in molecular evolution between switch (R5 to R5X4/X4-tropic) and non-switch (R5-tropic only) HIV-1 populations during infection. Infect. Genet. Evol. 2010, 10:356-364.
47. Nabatov A.A., Pollakis G., Linnemann T., Kliphius A., Chalaby M.I., Paxton W.A. Intrapatient alterations in the human immunodeficiency virus type 1 gp120 V1V2 and V3 regions differentially modulate coreceptor usage, virus inhibition by CC/CXC chemokines, soluble CD4, and the b12 and 2G12 monoclonal antibodies. J. Virol. 2004, 78:524-530.
48. Ogert R.A., Lee M.K., Ross W., Buckler-White A., Martin M.A., Cho M.W. N-linked glycosylation sites adjacent to and within the V1/V2 and the V3 loops of dualtropic human immunodeficiency virus type 1 isolate DH12 gp120 affect coreceptor usage and cellular tropism. J. Virol. 2001, 75:5998-6006.
49. Pollakis G., Kang S., Kliphuis A., Chalaby M.I., Goudsmit J., Paxton W.A. N-linked glycosylation of the HIV type-1 gp120 envelope glycoprotein as a major determinant of CCR5 and CXCR4 coreceptor utilization. J. Biol. Chem. 2001, 276:13433-13441.
50. Polzer S., Dittmar M.T., Schmitz H., Meyer B., Muller H., Krausslich H.G., Schreiber M. Loss of N-linked glycans in the V3-loop region of gp120 is correlated to an enhanced infectivity of HIV-1. Glycobiology 2001, 11:11-19.
51. Regoes R.R., Bonhoeffer S. The HIV coreceptor switch: a population dynamical perspective. Trends Microbiol. 2005, 13:269-277.
52. Repits J., Oberg M., Esbjornsson J., Medstrand P., Karlsson A., Albert J., Fenyo E.M., Jansson M. Selection of human immunodeficiency virus type 1 R5 variants with augmented replicative capacity and reduced sensitivity to entry inhibitors during severe immunodeficiency. J. Gen. Virol. 2005, 86:2859-2869.
53. Salemi M., Burkhardt B.R., Gray R.R., Ghaffari G., Sleasman J.W., Goodenow M.M. Phylodynamics of HIV-1 in lymphoid and non-lymphoid tissues reveals a central role for the thymus in emergence of CXCR4-using quasispecies. PLoS ONE 2007, 2:e950.
54. Salemi M., Gray R.R., Goodenow M.M. An exploratory algorithm to identify intra-host recombinant viral sequences. Mol. Phylogenet. Evol. 2008, 49:618-628.
55. Salemi M., Lamers S.L., Yu S., de Oliveira T., Fitch W.M., McGrath M.S. Phylodynamic analysis of human immunodeficiency virus type 1 in distinct brain compartments provides a model for the neuropathogenesis of AIDS. J. Virol. 2005, 79:11343-11352.
56. Salminen M.O., Carr J.K., Burke D.S., McCutchan F.E. Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res. Hum. Retroviruses 1995, 11:1423-1425.
57. Scarlatti G., Tresoldi E., Bjorndal A., Fredriksson R., Colognesi C., Deng H.K., Malnati M.S., Plebani A., Siccardi A.G., Littman D.R., Fenyo E.M., Lusso P. In vivo evolution of HIV-1 co-receptor usage and sensitivity to chemokine-mediated suppression. Nat. Med. 1997, 3:1259-1265.
58. Schierup M.H., Hein J. Consequences of recombination on traditional phylogenetic analysis. Genetics 2000, 156:879-891.
59. Schuitemaker H., Koot M., Kootstra N.A., Dercksen M.W., de Goede R.E., van Steenwijk R.P., Lange J.M., Schattenkerk J.K., Miedema F., Tersmette M. 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. 1992, 66:1354-1360.
60. Seo T.K., Kishino H., Thorne J.L. Estimating absolute rates of synonymous and nonsynonymous nucleotide substitution in order to characterize natural selection and date species divergences. Mol. Biol. Evol. 2004, 21:1201-1213.
61. Shankarappa R., Margolick J.B., Gange S.J., Rodrigo A.G., Upchurch D., Farzadegan H., Gupta P., Rinaldo C.R., Learn G.H., He X., Huang X.L., Mullins J.I. Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J. Virol. 1999, 73:10489-10502.
62. Shepherd J.C., Jacobson L.P., Qiao W., Jamieson B.D., Phair J.P., Piazza P., Quinn T.C., Margolick J.B. Emergence and persistence of CXCR4-tropic HIV-1 in a population of men from the multicenter AIDS cohort study. J. Infect. Dis. 2008, 198:1104-1112.
63. Shioda T., Levy J.A., Cheng-Mayer C. Small amino acid changes in the V3 hypervariable region of gp120 can affect the T-cell-line and macrophage tropism of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 1992, 89:9434-9438.
64. Shriner D., Shankarappa R., Jensen M.A., Nickle D.C., Mittler J.E., Margolick J.B., Mullins J.I. Influence of random genetic drift on human immunodeficiency virus type 1 env evolution during chronic infection. Genetics 2004, 166:1155-1164.
65. Skar H., Borrego P., Wallstrom T.C., Mild M., Marcelino J.M., Barroso H., Taveira N., Leitner T., Albert J. HIV-2 genetic evolution in patients with advanced disease is faster than that in matched HIV-1 patients. J. Virol. 2010, 84:7412-7415.
66. Trouplin V., Salvatori F., Cappello F., Obry V., Brelot A., Heveker N., Alizon M., Scarlatti G., Clavel F., Mammano F. Determination of coreceptor usage of human immunodeficiency virus type 1 from patient plasma samples by using a recombinant phenotypic assay. J. Virol. 2001, 75:251-259.
67. Troyer R.M., Collins K.R., Abraha A., Fraundorf E., Moore D.M., Krizan R.W., Toossi Z., Colebunders R.L., Jensen M.A., Mullins J.I., Vanham G., Arts E.J. Changes in human immunodeficiency virus type 1 fitness and genetic diversity during disease progression. J. Virol. 2005, 79:9006-9018.
68. Van Wout A.B., Blaak H., Ran L.J., Brouwer M., Kuiken C., Schuitemaker H. 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 infection. J. Virol. 1998, 72:5099-5107.
69. van Rij R.P., Hazenberg M.D., van Benthem B.H., Otto S.A., Prins M., Miedema F., Schuitemaker H. Early viral load and CD4+ T cell count, but not percentage of CCR5+ or CXCR4+ CD4+ T cells, are associated with R5-to-X4 HIV type 1 virus evolution. AIDS Res. Hum. Retroviruses 2003, 19:389-398.
70. Williamson S. Adaptation in the env gene of HIV-1 and evolutionary theories of disease progression. Mol. Biol. Evol. 2003, 20:1318-1325.