Analysis of multiply spliced transcripts in lymphoid tissue reservoirs of rhesus macaques infected with RT-SHIV during HAART

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Deere, Jesse D ^a   Kauffman, Robert C ^a   Cannavo, Elda ^a   Higgins, Joanne ^a   Villalobos, Andradi ^a   Adamson, Lourdes ^a   Schinazi, Raymond F ^b   Luciw, Paul A ^a   North, Thomas W ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; GAG PROTEIN; VIRUS RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DRUG EFFICACY; EXON; GAPDH GENE; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENETIC TRANSCRIPTION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; LYMPHOID TISSUE; MALE; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; RHESUS MONKEY; RNA SEQUENCE; RNA SPLICING; RT SHIV INFECTION; SEQUENCE ANALYSIS; STRUCTURAL GENE; TISSUE LEVEL; VIRUS GENE; VIRUS INFECTION; VIRUS LATENCY; VIRUS LOAD;

ANIMALS; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; CD4-POSITIVE T-LYMPHOCYTES; HIV INFECTIONS; HIV-1; HUMANS; MACACA MULATTA; MALE; RNA, MESSENGER; RNA, VIRAL; VIRAL LOAD; VIRUS REPLICATION;

EID: 84895555704     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087914     Document Type: Article

References (67)

1. Poles MA, Boscardin WJ, Elliott J, Taing P, Fuerst MM, et al. (2006) Lack of decay of HIV-1 in gut-associated lymphoid tissue reservoirs in maximally suppressed individuals. J Acquir Immune Defic Syndr 43: 65-68. (Pubitemid 44306490)
2. Deeks SG, Wrin T, Liegler T, Hoh R, Hayden M, et al. (2001) Virologic and immunologic consequences of discontinuing combination antiretroviral-drug therapy in HIV-infected patients with detectable viremia. N Engl J Med 344: 472-480. (Pubitemid 32164898)
3. Harrigan PR, Whaley M, Montaner JS (1999) Rate of HIV-1 RNA rebound upon stopping antiretroviral therapy. AIDS 13: F59-62. (Pubitemid 29240180)
4. Havlir DV, Bassett R, Levitan D, Gilbert P, Tebas P, et al. (2001) Prevalence and predictive value of intermittent viremia with combination hiv therapy. JAMA 286: 171-179. (Pubitemid 32640848)
5. Gunthard HF, Frost SD, Leigh-Brown AJ, Ignacio CC, Kee K, et al. (1999) Evolution of envelope sequences of human immunodeficiency virus type 1 in cellular reservoirs in the setting of potent antiviral therapy. J Virol 73: 9404-9412. (Pubitemid 29487096)
6. Ramratnam B, Mittler JE, Zhang L, Boden D, Hurley A, et al. (2000) The decay of the latent reservoir of replication-competent HIV-1 is inversely correlated with the extent of residual viral replication during prolonged anti-retroviral therapy. Nat Med 6: 82-85. (Pubitemid 30048531)
7. Havlir DV, Strain MC, Clerici M, Ignacio C, Trabattoni D, et al. (2003) Productive infection maintains a dynamic steady state of residual viremia in human immunodeficiency virus type 1-infected persons treated with suppressive antiretroviral therapy for five years. J Virol 77: 11212-11219. (Pubitemid 37204311)
8. Maldarelli F, Palmer S, King MS, Wiegand A, Polis MA, et al. (2007) ART suppresses plasma HIV-1 RNA to a stable set point predicted by pretherapy viremia. PLoS Pathog 3: e46.
9. Palmer S, Maldarelli F, Wiegand A, Bernstein B, Hanna GJ, et al. (2008) Low-level viremia persists for at least 7 years in patients on suppressive antiretroviral therapy. Proc Natl Acad Sci U S A 105: 3879-3884. (Pubitemid 351723493)
10. Palmer S, Wiegand AP, Maldarelli F, Bazmi H, Mican JM, et al. (2003) New real-time reverse transcriptase-initiated PCR assay with single-copy sensitivity for human immunodeficiency virus type 1 RNA in plasma. J Clin Microbiol 41: 4531-4536. (Pubitemid 37259753)
11. Chun TW, Nickle DC, 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. (Pubitemid 41567589)
12. Tobin NH, Learn GH, Holte SE, Wang Y, Melvin AJ, et al. (2005) Evidence that low-level viremias during effective highly active antiretroviral therapy result from two processes: expression of archival virus and replication of virus. J Virol 79: 9625-9634. (Pubitemid 41022306)
13. Gavegnano C, Schinazi RF (2009) Antiretroviral therapy in macrophages: implication for HIV eradication. Antivir Chem Chemother 20: 63-78.
14. Finzi D, Hermankova M, Pierson T, Carruth LM, Buck C, et al. (1997) Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 278: 1295-1300. (Pubitemid 27495742)
15. Finzi D, Blankson J, Siliciano JD, Margolick JB, Chadwick K, et al. (1999) Latent infection of CD4+ T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy. Nat Med 5: 512-517. (Pubitemid 29220209)
16. Chun TW, Engel D, Berrey MM, Shea T, Corey L, et al. (1998) Early establishment of a pool of latently infected, resting CD4(+) T cells during primary HIV-1 infection. Proc Natl Acad Sci U S A 95: 8869-8873. (Pubitemid 28350581)
17. Lassen K, Han Y, Zhou Y, Siliciano J, Siliciano RF (2004) The multifactorial nature of HIV-1 latency. Trends Mol Med 10: 525-531. (Pubitemid 39433821)
18. Chun TW, Carruth L, Finzi D, Shen X, DiGiuseppe JA, et al. (1997) Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 387: 183-188. (Pubitemid 27209433)
19. Mok HP, Lever AM (2007) Chromatin, gene silencing and HIV latency. Genome Biol 8: 228.
20. Jordan A, Defechereux P, Verdin E (2001) The site of HIV-1 integration in the human genome determines basal transcriptional activity and response to Tat transactivation. Embo J 20: 1726-1738. (Pubitemid 32299409)
21. Jordan A, Bisgrove D, Verdin E (2003) HIV reproducibly establishes a latent infection after acute infection of T cells in vitro. Embo J 22: 1868-1877. (Pubitemid 36460143)
22. Bednarik DP, Mosca JD, Raj NB (1987) Methylation as a modulator of expression of human immunodeficiency virus. J Virol 61: 1253-1257. (Pubitemid 17044042)
23. Brady T, Agosto LM, Malani N, Berry CC, O'Doherty U, et al. (2009) HIV integration site distributions in resting and activated CD4+ T cells infected in culture. AIDS 23: 1461-1471.
24. Schulze-Forster K, Gotz F, Wagner H, Kroger H, Simon D (1990) Transcription of HIV1 is inhibited by DNA methylation. Biochem Biophys Res Commun 168: 141-147. (Pubitemid 20142596)
25. Lin X, Irwin D, Kanazawa S, Huang L, Romeo J, et al. (2003) Transcriptional profiles of latent human immunodeficiency virus in infected individuals: effects of Tat on the host and reservoir. J Virol 77: 8227-8236. (Pubitemid 36871450)
26. Adams M, Sharmeen L, Kimpton J, Romeo JM, Garcia JV, et al. (1994) Cellular latency in human immunodeficiency virus-infected individuals with high CD4 levels can be detected by the presence of promoter-proximal transcripts. Proc Natl Acad Sci U S A 91: 3862-3866. (Pubitemid 24139532)
27. Dayton AI, Sodroski JG, Rosen CA, Goh WC, Haseltine WA (1986) The transactivator gene of the human T cell lymphotropic virus type III is required for replication. Cell 44: 941-947. (Pubitemid 16045340)
28. Fisher AG, Feinberg MB, Josephs SF, Harper ME, Marselle LM, et al. (1986) The trans-activator gene of HTLV-III is essential for virus replication. Nature 320: 367-371. (Pubitemid 16077280)
29. Kao SY, Calman AF, Luciw PA, Peterlin BM (1987) Anti-termination of transcription within the long terminal repeat of HIV-1 by tat gene product. Nature 330: 489-493. (Pubitemid 18006431)
30. Peterlin BM, Luciw PA, Barr PJ, Walker MD (1986) Elevated levels of mRNA can account for the trans-activation of human immunodeficiency virus. Proc Natl Acad Sci U S A 83: 9734-9738. (Pubitemid 17223431)
31. Sodroski J, Goh WC, Rosen C, Dayton A, Terwilliger E, et al. (1986) A second post-transcriptional trans-activator gene required for HTLV-III replication. Nature 321: 412-417. (Pubitemid 16055491)
32. Feinberg MB, Jarrett RF, Aldovini A, Gallo RC, Wong-Staal F (1986) HTLV-III expression and production involve complex regulation at the levels of splicing and translation of viral RNA. Cell 46: 807-817. (Pubitemid 16027929)
33. Malim MH, Hauber J, Le SY, Maizel JV, Cullen BR (1989) The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 338: 254-257. (Pubitemid 19086926)
34. Felber BK, Hadzopoulou-Cladaras M, Cladaras C, Copeland T, Pavlakis GN (1989) rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA. Proc Natl Acad Sci U S A 86: 1495-1499. (Pubitemid 19078934)
35. Lassen KG, Ramyar KX, Bailey JR, Zhou Y, Siliciano RF (2006) Nuclear retention of multiply spliced HIV-1 RNA in resting CD4+ T cells. PLoS Pathog 2: e68.
36. Lassen KG, Bailey JR, Siliciano RF (2004) Analysis of human immunodeficiency virus type 1 transcriptional elongation in resting CD4+ T cells in vivo. J Virol 78: 9105-9114. (Pubitemid 39096521)
37. North TW, Higgins J, Deere JD, Hayes TL, Villalobos A, et al. (2010) Viral sanctuaries during highly active antiretroviral therapy in a nonhuman primate model for AIDS. J Virol 84: 2913-2922.
38. North TW, Van Rompay KK, Higgins J, Matthews TB, Wadford DA, et al. (2005) Suppression of virus load by highly active antiretroviral therapy in rhesus macaques infected with a recombinant simian immunodeficiency virus containing reverse transcriptase from human immunodeficiency virus type 1. J Virol 79: 7349-7354. (Pubitemid 40756770)
39. Ambrose Z, Palmer S, Boltz VF, Kearney M, Larsen K, et al. (2007) Suppression of viremia and evolution of human immunodeficiency virus type 1 drug resistance in a macaque model for antiretroviral therapy. J Virol 81: 12145-12155. (Pubitemid 350085830)
40. Hatziioannou T, Ambrose Z, Chung NP, Piatak M, Jr., Yuan F, et al. (2009) A macaque model of HIV-1 infection. Proc Natl Acad Sci U S A 106: 4425-4429.
41. Dinoso JB, Rabi SA, Blankson JN, Gama L, Mankowski JL, et al. (2009) A simian immunodeficiency virus-infected macaque model to study viral reservoirs that persist during highly active antiretroviral therapy. J Virol 83: 9247-9257.
42. Uberla K, Stahl-Hennig C, Bottiger D, Matz-Rensing K, Kaup FJ, et al. (1995) Animal model for the therapy of acquired immunodeficiency syndrome with reverse transcriptase inhibitors. Proc Natl Acad Sci U S A 92: 8210-8214.
43. Ambrose Z, Boltz V, Palmer S, Coffin JM, Hughes SH, et al. (2004) In vitro characterization of a simian immunodeficiency virus-human immunodeficiency virus (HIV) chimera expressing HIV type 1 reverse transcriptase to study antiviral resistance in pigtail macaques. J Virol 78: 13553-13561. (Pubitemid 39612755)
44. Reinhart TA, Rogan MJ, Viglianti GA, Rausch DM, Eiden LE, et al. (1997) A new approach to investigating the relationship between productive infection and cytopathicity in vivo. Nat Med 3: 218-221. (Pubitemid 27064708)
45. Leutenegger CM, Higgins J, Matthews TB, Tarantal AF, Luciw PA, et al. (2001) Real-time TaqMan PCR as a specific and more sensitive alternative to the branched-chain DNA assay for quantitation of simian immunodeficiency virus RNA. AIDS Res Hum Retroviruses 17: 243-251. (Pubitemid 32113572)
46. Deere JD, Higgins J, Cannavo E, Villalobos A, Adamson L, et al. (2010) Viral decay kinetics in the highly active antiretroviral therapy-treated rhesus macaque model of AIDS. PLoS One 5: e11640.
47. Zhang L, Chung C, Hu BS, He T, Guo Y, et al. (2000) Genetic characterization of rebounding HIV-1 after cessation of highly active antiretroviral therapy. J Clin Invest 106: 839-845.
48. Chun TW, Davey RT, Jr., Ostrowski M, Shawn Justement J, Engel D, et al. (2000) Relationship between pre-existing viral reservoirs and the re-emergence of plasma viremia after discontinuation of highly active anti-retroviral therapy. Nat Med 6: 757-761. (Pubitemid 30469423)
49. Lewin SR, Vesanen M, Kostrikis L, Hurley A, Duran M, et al. (1999) Use of real-time PCR and molecular beacons to detect virus replication in human immunodeficiency virus type 1-infected individuals on prolonged effective antiretroviral therapy. J Virol 73: 6099-6103. (Pubitemid 29274900)
50. Unger RE, Stout MW, Luciw PA (1991) Simian immunodeficiency virus (SIVmac) exhibits complex splicing for tat, rev, and env mRNA. Virology 182: 177-185.
51. Viglianti GA, Sharma PL, Mullins JI (1990) Simian immunodeficiency virus displays complex patterns of RNA splicing. J Virol 64: 4207-4216. (Pubitemid 20279828)
52. Viglianti GA, Mullins JI (1988) Functional comparison of transactivation by simian immunodeficiency virus from rhesus macaques and human immunodeficiency virus type 1. J Virol 62: 4523-4532. (Pubitemid 19006113)
53. Regier DA, Desrosiers RC (1990) The complete nucleotide sequence of a pathogenic molecular clone of simian immunodeficiency virus. AIDS Res Hum Retroviruses 6: 1221-1231.
54. Park IW, Steen R, Li Y (1991) Characterization of multiple mRNA species of simian immunodeficiency virus from macaques in a CD4+ lymphoid cell line. J Virol 65: 2987-2992.
55. Reinhart TA, Rogan MJ, Haase AT (1996) RNA splice site utilization by simian immunodeficiency viruses derived from sooty mangabey monkeys. Virology 224: 338-344. (Pubitemid 26358133)
56. Schwartz S, Felber BK, Benko DM, Fenyo EM, Pavlakis GN (1990) Cloning and functional analysis of multiply spliced mRNA species of human immunodeficiency virus type 1. J Virol 64: 2519-2529. (Pubitemid 20171235)
57. Purcell DF, Martin MA (1993) Alternative splicing of human immunodeficiency virus type 1 mRNA modulates viral protein expression, replication, and infectivity. J Virol 67: 6365-6378. (Pubitemid 23309100)
58. Kodama T, Wooley DP, Naidu YM, Kestler HW 3rd, Daniel MD, et al. (1989) Significance of premature stop codons in env of simian immunodeficiency virus. J Virol 63: 4709-4714. (Pubitemid 19257848)
59. Shen A, Zink MC, Mankowski JL, Chadwick K, Margolick JB, et al. (2003) Resting CD4+ T lymphocytes but not thymocytes provide a latent viral reservoir in a simian immunodeficiency virus-Macaca nemestrina model of human immunodeficiency virus type 1-infected patients on highly active antiretroviral therapy. J Virol 77: 4938-4949. (Pubitemid 36402842)
60. Yukl SA, Gianella S, Sinclair E, Epling L, Li Q, et al. (2010) Differences in HIV burden and immune activation within the gut of HIV-positive patients receiving suppressive antiretroviral therapy. J Infect Dis 202: 1553-1561.
61. Yukl SA, Shergill AK, McQuaid K, Gianella S, Lampiris H, et al. (2010) Effect of raltegravir-containing intensification on HIV burden and T-cell activation in multiple gut sites of HIV-positive adults on suppressive antiretroviral therapy. AIDS 24: 2451-2460.
62. Hofman MJ, Higgins J, Matthews TB, Pedersen NC, Tan C, et al. (2004) Efavirenz therapy in rhesus macaques infected with a chimera of simian immunodeficiency virus containing reverse transcriptase from human immunodeficiency virus type 1. Antimicrob Agents Chemother 48: 3483-3490. (Pubitemid 39129349)
63. Soderberg K, Denekamp L, Nikiforow S, Sautter K, Desrosiers RC, et al. (2002) A nucleotide substitution in the tRNA(Lys) primer binding site dramatically increases replication of recombinant simian immunodeficiency virus containing a human immunodeficiency virus type 1 reverse transcriptase. J Virol 76: 5803-5806. (Pubitemid 34517931)
64. Van Rompay KK, Brignolo LL, Meyer DJ, Jerome C, Tarara R, et al. (2004) Biological effects of short-term or prolonged administration of 9-[2-(phosphonomethoxy) propyl]adenine (tenofovir) to newborn and infant rhesus macaques. Antimicrob Agents Chemother 48: 1469-1487. (Pubitemid 38544348)
65. Kestler H, Kodama T, Ringler D, Marthas M, Pedersen N, et al. (1990) Induction of AIDS in rhesus monkeys by molecularly cloned simian immunodeficiency virus. Science 248: 1109-1112.
66. Lee C, Kim J, Shin SG, Hwang S (2006) Absolute and relative QPCR quantification of plasmid copy number in Escherichia coli. J Biotechnol 123: 273-280. (Pubitemid 44294582)
67. Baumgarth N, Szubin R, Dolganov GM, Watnik MR, Greenspan D, et al. (2004) Highly tissue substructure-specific effects of human papilloma virus in mucosa of HIV-infected patients revealed by laser-dissection microscopy-assisted gene expression profiling. Am J Pathol 165: 707-718. (Pubitemid 39129279)