Early emergence and selection of a SIV-LTR C/EBP site variant in SIV-Infected macaques that increases virus infectivity

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Ravimohan, Shruthi ^a   Gama, Lucio ^b   Engle, Elizabeth L ^b   Zink, M Christine ^b   Clements, Janice E ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; BETA INTERFERON; CCAAT ENHANCER BINDING PROTEIN BETA; CYTOSINE; GUANINE; INTERLEUKIN 6; MESSENGER RNA;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BRAIN; C EBP BINDING SITE; CONTROLLED STUDY; DISEASE COURSE; DNA SEQUENCE; GENE EXPRESSION; GENOTYPE; IN VIVO STUDY; LONG TERMINAL REPEAT; MACACA NEMESTRINA; MACROPHAGE; NONHUMAN; SEQUENCE ANALYSIS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; SPLEEN; T LYMPHOCYTE; VIRUS INFECTIVITY; VIRUS LOAD; VIRUS REPLICATION;

ANIMALS; BRAIN; CCAAT-ENHANCER-BINDING PROTEINS; DISEASE PROGRESSION; GENETIC VARIATION; GENOTYPE; HEK293 CELLS; HUMANS; IN SITU HYBRIDIZATION; INTERFERON-BETA; INTERLEUKIN-6; MACACA; MACROPHAGES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; SPLEEN; TERMINAL REPEAT SEQUENCES; TIME FACTORS; VIRUS REPLICATION;

EID: 84865426301     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042801     Document Type: Article

References (73)

1. Witwer KW, Gama L, Li M, Bartizal CM, Queen SE, et al. (2009) Coordinated regulation of SIV replication and immune responses in the CNS. PLoS One 4: e8129.
2. An SF, Groves M, Gray F, Scaravilli F, (1999) Early entry and widespread cellular involvement of HIV-1 DNA in brains of HIV-1 positive asymptomatic individuals. J Neuropathol Exp Neurol 58: 1156-1162.
3. Davis LE, Hjelle BL, Miller VE, Palmer DL, Llewellyn AL, et al. (1992) Early viral brain invasion in iatrogenic human immunodeficiency virus infection. Neurology 42: 1736-1739.
4. Price RW, Brew B, Sidtis J, Rosenblum M, Scheck AC, et al. (1988) The brain in AIDS: central nervous system HIV-1 infection and AIDS dementia complex. Science 239: 586-592.
5. Price RW, Brew B, (1988) Infection of the central nervous system by human immunodeficiency virus. Role of the immune system in pathogenesis. Ann N Y Acad Sci 540: 162-175.
6. Cysique LA, Brew BJ, (2009) Neuropsychological functioning and antiretroviral treatment in HIV/AIDS: a review. Neuropsychol Rev 19: 169-185.
7. McArthur JC, (2004) HIV dementia: an evolving disease. J Neuroimmunol 157: 3-10.
8. Ellis RJ, (2007) Evidence-based treatment for HIV-associated dementia and cognitive impairment: why so little? PLoS Clin Trials 2: e15.
9. Sacktor N, McDermott MP, Marder K, Schifitto G, Selnes OA, et al. (2002) HIV-associated cognitive impairment before and after the advent of combination therapy. J Neurovirol 8: 136-142.
10. Boutwell CL, Rolland MM, Herbeck JT, Mullins JI, Allen TM, (2010) Viral evolution and escape during acute HIV-1 infection. J Infect Dis 202Suppl 2: S309-314.
11. McMichael AJ, Phillips RE, (1997) Escape of human immunodeficiency virus from immune control. Annu Rev Immunol 15: 271-296.
12. Griffin DE, (2003) Immune responses to RNA-virus infections of the CNS. Nat Rev Immunol 3: 493-502.
13. Barber SA, Gama L, Dudaronek JM, Voelker T, Tarwater PM, et al. (2006) Mechanism for the establishment of transcriptional HIV latency in the brain in a simian immunodeficiency virus-macaque model. J Infect Dis 193: 963-970.
14. Dudaronek JM, Barber SA, Clements JE, (2007) CUGBP1 is required for IFNbeta-mediated induction of dominant-negative CEBPbeta and suppression of SIV replication in macrophages. J Immunol 179: 7262-7269.
15. Honda Y, Rogers L, Nakata K, Zhao BY, Pine R, et al. (1998) Type I interferon induces inhibitory 16-kD CCAAT/enhancer binding protein (C/EBP)beta, repressing the HIV-1 long terminal repeat in macrophages: pulmonary tuberculosis alters C/EBP expression, enhancing HIV-1 replication. J Exp Med 188: 1255-1265.
16. Weiden M, Tanaka N, Qiao Y, Zhao BY, Honda Y, et al. (2000) Differentiation of monocytes to macrophages switches the Mycobacterium tuberculosis effect on HIV-1 replication from stimulation to inhibition: modulation of interferon response and CCAAT/enhancer binding protein beta expression. J Immunol 165: 2028-2039.
17. Barber SA, Herbst DS, Bullock BT, Gama L, Clements JE, (2004) Innate immune responses and control of acute simian immunodeficiency virus replication in the central nervous system. J Neurovirol 10Suppl 1: 15-20.
18. Ravimohan S, Gama L, Barber SA, Clements JE, (2010) Regulation of SIV mac 239 basal long terminal repeat activity and viral replication in macrophages: functional roles of two CCAAT/enhancer-binding protein beta sites in activation and interferon beta-mediated suppression. J Biol Chem 285: 2258-2273.
19. Henderson AJ, Calame KL, (1997) CCAAT/enhancer binding protein (C/EBP) sites are required for HIV-1 replication in primary macrophages but not CD4(+) T cells. Proc Natl Acad Sci U S A 94: 8714-8719.
20. Henderson AJ, Connor RI, Calame KL, (1996) C/EBP activators are required for HIV-1 replication and proviral induction in monocytic cell lines. Immunity 5: 91-101.
21. Henderson AJ, Zou X, Calame KL, (1995) C/EBP proteins activate transcription from the human immunodeficiency virus type 1 long terminal repeat in macrophages/monocytes. J Virol 69: 5337-5344.
22. Dumais N, Bounou S, Olivier M, Tremblay MJ, (2002) Prostaglandin E(2)-mediated activation of HIV-1 long terminal repeat transcription in human T cells necessitates CCAAT/enhancer binding protein (C/EBP) binding sites in addition to cooperative interactions between C/EBPbeta and cyclic adenosine 5′-monophosphate response element binding protein. J Immunol 168: 274-282.
23. Ross HL, Gartner S, McArthur JC, Corboy JR, McAllister JJ, et al. (2001) HIV-1 LTR C/EBP binding site sequence configurations preferentially encountered in brain lead to enhanced C/EBP factor binding and increased LTR-specific activity. J Neurovirol 7: 235-249.
24. Hogan TH, Stauff DL, Krebs FC, Gartner S, Quiterio SJ, et al. (2003) Structural and functional evolution of human immunodeficiency virus type 1 long terminal repeat CCAAT/enhancer binding protein sites and their use as molecular markers for central nervous system disease progression. J Neurovirol 9: 55-68.
25. Burdo TH, Nonnemacher M, Irish BP, Choi CH, Krebs FC, et al. (2004) High-affinity interaction between HIV-1 Vpr and specific sequences that span the C/EBP and adjacent NF-kappaB sites within the HIV-1 LTR correlate with HIV-1-associated dementia. DNA Cell Biol 23: 261-269.
26. Anderson MG, Clements JE, (1991) Comparison of the transcriptional activity of the long terminal repeats of simian immunodeficiency viruses SIVmac251 and SIVmac239 in T-cell lines and macrophage cell lines. J Virol 65: 51-60.
27. Anderson MG, Clements JE, (1992) Two strains of SIVmac show differential transactivation mediated by sequences in the promoter. Virology 191: 559-568.
28. Babas T, Vieler E, Hauer DA, Adams RJ, Tarwater PM, et al. (2001) Pathogenesis of SIV pneumonia: selective replication of viral genotypes in the lung. Virology 287: 371-381.
29. Flaherty MT, Hauer DA, Mankowski JL, Zink MC, Clements JE, (1997) Molecular and biological characterization of a neurovirulent molecular clone of simian immunodeficiency virus. J Virol 71: 5790-5798.
30. Clements JE, Babas T, Mankowski JL, Suryanarayana K, Piatak M Jr, et al. (2002) The central nervous system as a reservoir for simian immunodeficiency virus (SIV): steady-state levels of SIV DNA in brain from acute through asymptomatic infection. J Infect Dis 186: 905-913.
31. Zink MC, Amedee AM, Mankowski JL, Craig L, Didier P, et al. (1997) Pathogenesis of SIV encephalitis. Selection and replication of neurovirulent SIV. Am J Pathol 151: 793-803.
32. Zink MC, Spelman JP, Robinson RB, Clements JE, (1998) SIV infection of macaques-modeling the progression to AIDS dementia. J Neurovirol 4: 249-259.
33. Falk S, Stutte HJ, (1990) The spleen in HIV infection-morphological evidence of HIV-associated macrophage dysfunction. Res Virol 141: 161-169.
34. McIlroy D, Autran B, Cheynier R, Clauvel JP, Oksenhendler E, et al. (1996) Low infection frequency of macrophages in the spleens of HIV+ patients. Res Virol 147: 115-121.
35. Igarashi T, Brown CR, Endo Y, Buckler-White A, Plishka R, et al. (2001) Macrophage are the principal reservoir and sustain high virus loads in rhesus macaques after the depletion of CD4+ T cells by a highly pathogenic simian immunodeficiency virus/HIV type 1 chimera (SHIV): Implications for HIV-1 infections of humans. Proc Natl Acad Sci U S A 98: 658-663.
36. Steiniger B (2005) Spleen. Encyclopedia of Life Sciences.
37. Zink MC, Suryanarayana K, Mankowski JL, Shen A, Piatak M Jr, et al. (1999) High viral load in the cerebrospinal fluid and brain correlates with severity of simian immunodeficiency virus encephalitis. J Virol 73: 10480-10488.
38. Babas T, Dewitt JB, Mankowski JL, Tarwater PM, Clements JE, et al. (2006) Progressive selection for neurovirulent genotypes in the brain of SIV-infected macaques. Aids 20: 197-205.
39. Babas T, Munoz D, Mankowski JL, Tarwater PM, Clements JE, et al. (2003) Role of microglial cells in selective replication of simian immunodeficiency virus genotypes in the brain. J Virol 77: 208-216.
40. Smith DB, McAllister J, Casino C, Simmonds P, (1997) Virus 'quasispecies': making a mountain out of a molehill? J Gen Virol 78 (Pt 7): 1511-1519.
41. Lundberg KS, Shoemaker DD, Adams MW, Short JM, Sorge JA, et al. (1991) High-fidelity amplification using a thermostable DNA polymerase isolated from Pyrococcus furiosus. Gene 108: 1-6.
42. Koop BF, Rowan L, Chen WQ, Deshpande P, Lee H, et al. (1993) Sequence length and error analysis of Sequenase and automated Taq cycle sequencing methods. Biotechniques 14: 442-447.
43. Preston BD, Poiesz BJ, Loeb LA, (1988) Fidelity of HIV-1 reverse transcriptase. Science 242: 1168-1171.
44. Roos JW, Maughan MF, Liao Z, Hildreth JE, Clements JE, (2000) LuSIV cells: a reporter cell line for the detection and quantitation of a single cycle of HIV and SIV replication. Virology 273: 307-315.
45. Kornbluth RS, Matsuzaki H, Meylan PR, Richman DD (1994) Interferon interactions with HIV1 in macrophages. Res Immunol 145: 664-666; discussion 666-668.
46. Nonnemacher MR, Hogan TH, Quiterio S, Wigdahl B, Henderson A, et al. (2003) Identification of binding sites for members of the CCAAT/enhancer binding protein transcription factor family in the simian immunodeficiency virus long terminal repeat. Biomed Pharmacother 57: 34-40.
47. Akira S, Isshiki H, Sugita T, Tanabe O, Kinoshita S, et al. (1990) A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. Embo J 9: 1897-1906.
48. Hungness ES, Luo GJ, Pritts TA, Sun X, Robb BW, et al. (2002) Transcription factors C/EBP-beta and-delta regulate IL-6 production in IL-1beta-stimulated human enterocytes. J Cell Physiol 192: 64-70.
49. Poli V, Mancini FP, Cortese R, (1990) IL-6DBP, a nuclear protein involved in interleukin-6 signal transduction, defines a new family of leucine zipper proteins related to C/EBP. Cell 63: 643-653.
50. Spooner CJ, Guo X, Johnson PF, Schwartz RC, (2007) Differential roles of C/EBP beta regulatory domains in specifying MCP-1 and IL-6 transcription. Mol Immunol 44: 1384-1392.
51. Niehof M, Streetz K, Rakemann T, Bischoff SC, Manns MP, et al. (2001) Interleukin-6-induced tethering of STAT3 to the LAP/C/EBPbeta promoter suggests a new mechanism of transcriptional regulation by STAT3. J Biol Chem 276: 9016-9027.
52. Gartner S, (2000) HIV infection and dementia. Science 287: 602-604.
53. Gartner S, Markovits P, Markovitz DM, Betts RF, Popovic M, (1986) Virus isolation from and identification of HTLV-III/LAV-producing cells in brain tissue from a patient with AIDS. Jama 256: 2365-2371.
54. Gartner S, Popovic M, (1990) Macrophage tropism of HIV-1. AIDS Res Hum Retroviruses 6: 1017-1021.
55. Williams KC, Corey S, Westmoreland SV, Pauley D, Knight H, et al. (2001) Perivascular macrophages are the primary cell type productively infected by simian immunodeficiency virus in the brains of macaques: implications for the neuropathogenesis of AIDS. J Exp Med 193: 905-915.
56. Clements JE, Mankowski JL, Gama L, Zink MC, (2008) The accelerated simian immunodeficiency virus macaque model of human immunodeficiency virus-associated neurological disease: from mechanism to treatment. J Neurovirol 14: 309-317.
57. Zink MC, Clements JE, (2002) A novel simian immunodeficiency virus model that provides insight into mechanisms of human immunodeficiency virus central nervous system disease. J Neurovirol 8Suppl 2: 42-48.
58. Descombes P, Schibler U, (1991) A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 67: 569-579.
59. Poli G, Bressler P, Kinter A, Duh E, Timmer WC, et al. (1990) Interleukin 6 induces human immunodeficiency virus expression in infected monocytic cells alone and in synergy with tumor necrosis factor alpha by transcriptional and post-transcriptional mechanisms. J Exp Med 172: 151-158.
60. Muesing MA, Smith DH, Capon DJ, (1987) Regulation of mRNA accumulation by a human immunodeficiency virus trans-activator protein. Cell 48: 691-701.
61. Wei P, Garber ME, Fang SM, Fischer WH, Jones KA, (1998) A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 92: 451-462.
62. Mancebo HS, Lee G, Flygare J, Tomassini J, Luu P, et al. (1997) P-TEFb kinase is required for HIV Tat transcriptional activation in vivo and in vitro. Genes Dev 11: 2633-2644.
63. Mameli G, Deshmane SL, Ghafouri M, Cui J, Simbiri K, et al. (2007) C/EBPbeta regulates human immunodeficiency virus 1 gene expression through its association with cdk9. J Gen Virol 88: 631-640.
64. Ambrosino C, Ruocco MR, Chen X, Mallardo M, Baudi F, et al. (1997) HIV-1 Tat induces the expression of the interleukin-6 (IL6) gene by binding to the IL6 leader RNA and by interacting with CAAT enhancer-binding protein beta (NF-IL6) transcription factors. J Biol Chem 272: 14883-14892.
65. Abraham S, Sweet T, Sawaya BE, Rappaport J, Khalili K, et al. (2005) Cooperative interaction of C/EBP beta and Tat modulates MCP-1 gene transcription in astrocytes. J Neuroimmunol 160: 219-227.
66. Li Y, Bevilacqua E, Chiribau CB, Majumder M, Wang C, et al. (2008) Differential control of the CCAAT/enhancer-binding protein beta (C/EBPbeta) products liver-enriched transcriptional activating protein (LAP) and liver-enriched transcriptional inhibitory protein (LIP) and the regulation of gene expression during the response to endoplasmic reticulum stress. J Biol Chem 283: 22443-22456.
67. Zink MC, Uhrlaub J, DeWitt J, Voelker T, Bullock B, et al. (2005) Neuroprotective and anti-human immunodeficiency virus activity of minocycline. Jama 293: 2003-2011.
68. Szeto GL BA, Yang HC, Barber SA, Siliciano RF, Clements JE (2009) Minocycline Attenuates HIV Infection and Reactivation by Suppressing Cellular Activation in Human CD4(+) T Cells. J Infect Dis.
69. Amedee AM, Lacour N, Gierman JL, Martin LN, Clements JE, et al. (1995) Genotypic selection of simian immunodeficiency virus in macaque infants infected transplacentally. J Virol 69: 7982-7990.
70. Murphey-Corb M, Montelaro RC, Miller MA, West M, Martin LN, et al. (1991) Efficacy of SIV/deltaB670 glycoprotein-enriched and glycoprotein-depleted subunit vaccines in protecting against infection and disease in rhesus monkeys. Aids 5: 655-662.
71. Spouge JL, (1992) Statistical analysis of sparse infection data and its implications for retroviral treatment trials in primates. Proc Natl Acad Sci U S A 89: 7581-7585.
72. Zhang JY, Martin LN, Watson EA, Montelaro RC, West M, et al. (1988) Simian immunodeficiency virus/delta-induced immunodeficiency disease in rhesus monkeys: relation of antibody response and antigenemia. J Infect Dis 158: 1277-1286.
73. Wright EK Jr, Page SH, Barber SA, Clements JE, (2008) Prep1/Pbx2 complexes regulate CCL2 expression through the-2578 guanine polymorphism. Genes Immun 9: 419-430.