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

Volumn 2, Issue 9, 2007, Pages

  Salemi, Marco ^a   Burkhardt, Brant R ^a,d   Gray, Rebecca R ^a,b   Ghaffari, Guity ^a   Sleasman, John W ^c   Goodenow, Maureen M ^a  

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

^b University of South Florida and All Children's Hospital ^*  (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; RNA DIRECTED DNA POLYMERASE INHIBITOR; GLYCOPROTEIN GP 120; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ARTICLE; CASE REPORT; CHILD; CONTROLLED STUDY; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC SELECTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN TISSUE; INFECTION CONTROL; LYMPH NODE; LYMPHOID TISSUE; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHYLODYNAMIC ANALYSIS; SEQUENCE ANALYSIS; SPLEEN; STRAIN DIFFERENCE; THYMUS; VIRAL GENETICS; VIRUS ENVELOPE; VIRUS IDENTIFICATION; VIRUS MUTATION; VIRUS STRAIN; CLASSIFICATION; CYTOLOGY; GENETIC RECOMBINATION; GENETICS; GENOTYPE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFANT; METABOLISM; MONONUCLEAR CELL; PHYLOGENY; PRESCHOOL CHILD; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CHILD; CHILD, PRESCHOOL; GENE PRODUCTS, ENV; GENOTYPE; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; INFANT; LEUKOCYTES, MONONUCLEAR; LYMPHOID TISSUE; PHYLOGENY; RECEPTORS, CXCR4; RECOMBINATION, GENETIC; THYMUS GLAND;

EID: 41649086532     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0000950     Document Type: Article

References (79)

1. Berger EA, Murphy PM, Farber JM (1999) Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Ann Rev Immunol 17: 675-7007
2. van'T Wout AB, Koonstra NA, Mulder-Kampinga CA, Albrecht-van Lent N, Scherpbier HJ, et al. (1994) Macrophage-tropic variants initiate human immunodeficiency virus type 1 infection after sexual, parenteral, and vertical transmission. J Clin Invest 94: 2060-2067.
3. Shankarappa R, Margolick JB, Gange SJ, Rodrigo AG, Upchurch D, et al. (1999) Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J Virus 73: 10489-10502.
4. + cell depletion and progression to AIDS. Ann Intern Med 118: 681-688.
5. Connor RI, Sheridan KE, Ceradini D, Choe S, Landau NR (1997) Change in coreceptor use correlates with disease progression in HIV-1-infected individuals. J Exp Med 185: 621-628.
6. Regoes RR, Bonhoeffer S (2005) The HIV coreceptor switch: a population dynamical perspective. Trends Microbiol 6: 269-277.
7. Westby M, Lewis M, Whitcomb J, Youle M, Pozniak AL, et al. (2006) Emergence of CXCR4-using human immunodeficiency virus type 1 (HIV-1) variants in a minority of HIV-1-infected patients following treatment with CCR5 antagonist Macaviroc is from a pretreatment CXCR4-using virus reservoirs. J Virol 80: 4909-4920.
8. Clevestig P, Maljkovic I, Casper G, Carlenor E, Lindgen S, et al. (2005) The X4 phenotype of HIV-1 evolves from R5 in two children of mothers, carrying X4, and is not linked to transmission. AIDS Res Hum Retrovir 5: 371-378.
9. Ghaffari G, Tuttle DL, Briggs D, Burkhardt BR, Bhatt D, et al. (2005) Complex determinants in human immunodeficiency virus type 1 envelope gp120 mediate CXCR4-dependent infection in macrophages. J Virol 79: 13250-13261.
10. Margolis L, Shattock R (2006) Selective transmission of CCR5-utilizing HIV-1: the 'gatekeeper' problem resolved? Nat Rev Microbiol 4: 312-317.
11. Cann AJ, Curcher MJ, Boyd M, O'Brien W, Zhao JQ. et al. (1992) The region of the envelope gene of human immunodeficiency virus type 1 responsible for determination of cell tropism. J Virol 66: 305-309.
12. Stamatos L, Cheng-Mayer G (1993) Evidence that the structural conformation of envelope gp 120 affects human immunodeficiency virus type 1 infectivity, host range, and syncytium-forming ability. J Virol 67: 5635-5639.
13. Milich LB, Margolin B, Swanstrom R (1997) Patterns of amino acid variability in NSI-like and SI-like V3 sequences and a linked change in the CD4-binding domain of the HIV-1 Env protein. Virology 239: 108-118.
14. Pastore C, Nedellec R, Ramos A, Pontow S, Ratner L, et al. (2006) Human immunodeficiency virus type 1 coreceptor switching. V1/V2 gain-of-fitness mutations compensate for V3 loss-of-fitness mutations. J Virol 80: 750-758.
15. Cho MW, Lee MK, Carney MG, Berson JF, Doms RW, Martin MA (1998) Identification of determinants on a dualtropic human immunodeficiency virus type 1 envelope glycoprotein that confer usage of CXCR4. J Virol. 72: 2509-2515.
16. Pontow S;, Ratner L (2001) Evidence for common structural determinants of human immunodefiency virus type 1 coreceptor activity provided through functional analysis of CCR5/CXCR4 chimeric coreceptors. J Virol. 75: 11503-11514.
17. Blankson JN, Persaud D, Siliciano RF (2002) The challenge of viral reservoirs in HIV-1 infection. Annual Reviews in Medicine 53: 557-593.
18. Chun TW, Nickle DG, Justement JS, Large D, Semerjian A, et al. (2005) HIV-infected individuals receiving effective antiviral therapy for extended periods of time continually replenish their viral reservoir. J Clin Invest 115: 3250-3255.
19. Poss M, Rodrigo AG, Gosink JJ, Learn GH, de Vange Panteleeff D, et al. (1998) Evolution of envelope sequences from the genital tract and peripheral blood of women infected with clade A human immunodeficiency virus type 1. J Virol 72: 8240-51.
20. Craigo JK, Patterson BK, Paranjpe S, Kulka K, Ding M, et al. (2004) Persistent HIV type 1 infection in semen and blood compartments in patients after long-term potent antiretroviral therapy. AIDS Res Hum Retrovir 20: 1196-11209.
21. Korber BT, Kunstman KJ, Patterson BK, Furtado M, McEvilly MM, et al. (1994) Genetic differences between blood-and brain-derived viral sequences from human immunodeficiency virus type 1-infected patients: Evidence of conserved elements in the V3 region of the envelope protein of brain-derived sequences. J Virol. 68: 7467-7481.
22. Chang J, Jozwtak R, Wang B, Ng T, Ge YC, et al. (1998) Unique HIV type 1 V3 region sequences derived from six different regions of brain: region-specific evolution within host-determined quasispecies. AIDS Res Hum Retrovir 14: 25-30.
23. Shapshak P, Segal DM, Crandall K.A, Fujimura RK, Zhang BT, et al. (1999) Independent evolution of HIV type 1 in different brain regions. AIDS Res Hum Retrovir 15: 811-820.
24. Nickle DC, Jensen MA, Shriner D, Brodie SJ, Frenkel LM, et al. (2003) Evolutionary Indicators of human immunodeficiency virus type 1 reservoirs and compartments. J Virol 77: 5540-5546.
25. Smit TK, Brew BJ, Tourtelotte W, Morgello S, Gelman BB, et al. (2004) Independent evolution of human immunodeficiency virus (HIV) drug resistance mutations in diverse areas of the brain in HIV-infected patients, with and without dementia, on antiretroviral treatment.
26. Salemi M, Lamers SL, Yu S, de Oliveira T, Fitch WM, et al. (2005) HIV-1 phylodynamic analysis in distinct brain compartments provides a model for the neuropathogenesis of AIDS. J Virol 79: 11343-11352.
27. Bleul CC, Wu L, Hoxie JA, Springer TA, Mackay CR (1997) The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc Natl Acad Sci USA 94: 1925-1930.
28. Zhang L, He T, Talal A, Wang G, Frankel SH, et al. (1998) In vivo distribution of the human immunodeficiency virus/simian immunodeficiency virus coreceptors: CXCR4, CCR3, CCR5. J Virol 72: 5035-5045.
29. Rosenzweig M, Clark DP, Gaulton GN (1993) Selective thymocyte depletion in neonatal HIV-1 thymic infection. AIDS 7: 1601-1605.
30. Kitchen SG, Zack JA (1997) CXCR4 expression during lymphopoiesis: implications for human immunodeficiency virus type 1 infection of the thymus. J Virol. 171: 6928-6934.
31. Zaitseva MB, Lee S, Rabin RL, Tiffany HL, Farber JM, et al. (1998) CXCR4 and CCR5 on human thymocytes: biological function and role in HIV-1 infection. J Immunol 161: 3103-13.
32. Uittenbogaart CH, Boscardin WJ, Anisman-Posner DJ, Koka PS, Bristol G, et al. (2000) Effect of cytokines on HIV-induced deplection of thymocytes in vivo. AIDS 14: 1317-1325.
33. Brooks DG, Kitchen SG, Kitchen CM, Scripture-Adams DD, Zack JA (2001) Generation of HIV latency during thymopoiesis. Nat Med 7: 459-464.
34. Douek DC, Betts MR, Hill BJ, Little SJ, Lempicki R, et al. (2001) Evidence for increase T-cell turnover and decreased thymic output in HIV infection. J Immunol 167: 6663-6668.
35. Dion ML, Poulin JF, Bordi R, Sylvestre M, Corsini R,. et al. (2004) HIV infection rapidly induces and maintains a substantial suppression of thymocytes proliferation. Immunity 21: 757-768.
36. Kourtis AP, Ibeghu G, Nahmias AJ, Lee FK, Clark WS, et al. (1997) Early progression of disease in HIV-infected infants with thymus dysfunction. N Engl J Med 335: 1431-1436, Erratum in: New Engl J Med 336: 595.
37. Alves K, Canzian M, Delwart EL (2002) HIV type 1 envelope quasispecies in the thymus and lymph nodes of AIDS patients. AIDS Res Hum Retrovir 2:. 161-165.
38. Grenfell BT, Pybus OG, Gog JR, Wood JL, Daly JM, et al. (2004) Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303: 327-332.
39. Briggs DR, Tuttle DL, Sleasman JW, Goodenow MM (2000) Envelope V3 amino acid sequence predicts HIV-1 phenotype (coreceptor usage and tropism for macrophages). AIDS 14: 2937-2939.
40. Jensen MA, Li FS, van't Wout AB, Nickle DC, Shriner D, et al. (2003) Improved coreceptor usage prediction and genotypic monitoring of R5-to-X4 transition by motif analysis of human immunodeficiency virus type 1 Env V3 loop sequences. J. Virol. 77: 13376-13388.
41. Jensen MA, Coetzer M, van't Wout AB, Morris L, JI (2006) A Reliable Phenotype Predictor for Human Immunodeficiency Virus Type 1 Subtype C Based on Envelope V3 Sequences. J. Virol. 80: 4698-4704.
42. Morris A, Marsden M, Halcrow K, Hughes ES, Brettle RP, et al. (1999) Mosaic structure of the human immunodeficiency virus type 1 genome infecting lymphoid cells and the brain: evidence for frequent in vivo recombination events in the evolution of regional populations. J. Virol. 73: 8720-8731.
43. Shriner D, Rodrigo AG, Nickle DC, Mullins JI (2004) Pervasive genomic recombination of HIV-1 in vivo. Genetics 167: 1573-1583.
44. Mild M, Esbjornnson J, Fenyo EM, Medstrand P (2007) Frequent intrapatient recombination between human immunodeficiency virus type 1 R5 and X4 envelopes: implications for coreceptor switch. J. Virol. 81: 3369-3376.
45. Meyerhans A, Vartanian JP, Wain-Hobson S (1990) Recombination during PCR. Nucleic Acids Res. 18: 1687-1691.
46. Howell RM, Fitzgibbon JE, Noe M, Ren ZJ, Gocke DJ, et al. (1991) In vivo sequence of HIV-1 enve gene: evidence for recombination among variants found in a single individual AIDS Res. Hum. Retroviruses 7: 869-876.
47. Fouchier RAM, Brouwer M, Broersen SM, Schuitemaker H (1995) Simple determination of human immunodeficiency virus type 1 syncytium-inducing V3 genotype by PCR. J Clin Microbiol 33: 906-911.
48. Messier W, Stewart CB (1997) Episodic adaptive evolution of primate lysozymes. Nature 385: 151-154.
49. Shriner D, Shankarappa R, Jensen MA, Nickle DC, Mittler JE, et al. (2004b) Influence of random genetic drift on human immunodeficiency virus type 1 env evolution during chronic infection. Genetics 166: 1155-1164.
50. Edwards CT, Holmes EC, Pybus OG, Wilson DJ, Viscidi RP, et al. (2006) Evolution of the human immunodeficiency virus envelope gene is dominated by purifying selection. Genetics. 174: 1441-1453.
51. Kiselyeva Y, Nedellec R, Ramos A, Pastore C, Margolis LB, et al. (2007) Evolution of CXCR4-using HIV-1 SF162 is associated with two unique envelope mutations. J Virol 0: JVI.02310-06v1.
52. Sha M, Smit TK, Morgello S, Tourtelotte W, Gelman B, et al. (2006) Env gp 120 sequence analysis of HIV type 1 strains from diverse areas of the brain shows preponderance of CCR5 usage. AIDS Res Hum Retrovir 22: 177-181.
53. Cocchi F, DeVico AL, Garzino-Demo A, Ayra SK, Gallo RC, et al. (1985) The V3 domain of the HIV-1 gp12O envelope glycoprotein is critical for chemokine-mediated blockade of infection. Science 270: 1811-1815.
54. Ho SH, Tasca S, Shek L, Li A, Gettie A, et al. (2007) Coreceptor switch in R5-tropic simian/human immunodeficiency virus-infected macaques. J Virol 81: 8621-8633.
55. Chene L, Nugeyre MT, Guillemard E, Moulian N, Barre-Sinoussi F, et al. (1999) Thymocyte-thymic epithelial cell interaction leads to high-level replication of human immunodeficiency virus exclusively in mature CD4(+) CD8(-) CD3(+) thymocytes: a critical role for tumor necrosis factor and interleukin-7. J Virol 73: 7533-7542.
56. Picker LJ, Butcher EC (1992) Physiological and molecular mechanisms of lymphocyte homing. Annu Rev Immunol 10: 561-591.
57. Ribeiro RM, Hazenberg MD, Perelson AS, Davenport MP (2006) Naïve and memory cell turnover as drivers of CCR5-to-CXCR4 tropism switch in human immunodeficiency virus type 1: implications for therapy. J Virol 80: 802-809.
58. Simpson JG, Gray ES, Beck JS (1975) Age involution in the normal human adult thymus. Clin Exp Immunol 19: 261-265.
59. Leino L, Lilius E-M, Nikoskelainen J, Pelliniemi T-T, Rajamaki A (1991) The reappearance of 10 differentiation antigens on peripheral blood lymphocytes after allogenic bone marrow transplantation. Bone Mar Transpl 8: 339-344.
60. Mackall C, Fleisher T, Brown M, Andrich M, Chen C, et al. (1995) Age, thymopoiesis, and CD4+ T-lymphocyte regeneration afdter intensive chemotherapy, N Engl J Med 332: 143-149.
61. Douek DG, Koup RA (2000) Evidence for thymic function in the elderly. Vaccine 18: 1638-1641.
62. Douek DG, McFarland RD, Keiser PH, Gage EA, Massey JM, et al. (1998) Changes in thymic function with age and during the treatment of HIV infection. Nature 396: 690-695.
63. Lamers SL,. Sleasman JW, She JX, Barrie KA, Pomeroy SM, et al. (1993) Independent variation and positive selection in env V1 and V2 domains within maternal-infant strains of human immunodeficiency virus type 1 in vivo. J Virol 67: 3951-3960.
64. Tuttle DL, Harrison JK, Anders C, Sleasman JW, Goodenow MM (1998). Expression of CCR5 increases during monocyte differentiation and directly mediates macrophage susceptibility to infection by human immunodeficiency virus type 1. J Virol 72: 4962-4969.
65. Burkhardt B, Kephart D, Coberley C, Sleasman J, Goodenow M (1999) Postmortem isolation and analysis of human genomic DNA and HIV-infected tissues: a molecular diagnostics application. Promega Notes 71: 30-31.
66. Tuttle DL, Anders CB, Aquino-DeJesus MJ, Poole PP, Lamers SL, et al. (2002) Increased replication of non-syncytium-inducing HIV type 1 isolates in monocyte-derived macrophages is linked to advanced disease in infected children. AIDS Res Hum Retroviruses 20: 353-362.
67. Lamers S, Beason S, Dunlap L, Compton R, Salemi M (2003) HIVbase: a PC/ Windows-based software offering storage and querying power for locally held HIV-1 genetic, experimental and clinical data. Bioinformatics 20: 436-438.
68. Lamers SL, Sleasman JW, Goodenow MM (1996) A model for alignment of env V1 and V2 hypervariable domains from human and simian immunodeficiency viruses. AIDS Res Hum Retrovir 12: 1169-1178.
69. Goodenow MM, Gollman RG (2006) HIV-1 coreceptor preference is distinct from target cell tropism: related but independent viral phenotypes. J Leuc Biol 80: 965-972.
70. Bruen TC, Herve P, Bryant D (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics 172: 2665-2681.
71. Huson DH, Bryant D (2005) Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23: 254-267.
72. Lole KS, Bollinger PC, Paranjape RS, Gadkari D,,Kulkarni SS, et al. (1999) Full-length human immunodeficiency virus type 1, genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol. 73: 152-160.
73. Salminen M (2003) Detecting recombination in viral sequences. In: Salemi M, Vandamme AM, eds. The Phylogenetic Handbook-a practical approach to DNA and protein phylogeny. New York: Cambridge University Press. pp 348-377.
74. Swofford D, Sullivan J (2003) Phylogeny Inference based on parsimony and other methods with PAUP*. In: Salemi M, Vandamine AM, eds. The Phylogenetic Handbook-a practical approach to DNA and protein phylogeny. New York: Cambridge University Press. pp 160-206.
75. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) -Relaxed Phylogenetics and Dating with Confidence. PLoS Biol 4. 1-12.
76. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Cabios 13: 555-556.
77. Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155: 431-449.
78. Slatikin M, Maddison WP (1989) A cladistic measure of gene flow inferred from the phylogenies alleles. Genetics 123: 401-416.
79. Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20: 401-416.