The interferon-induced antiviral protein PML (TRIM19) promotes the restriction and transcriptional silencing of lentiviruses in a context-specific, isoform-specific fashion

Retrovirology

Volumn 13, Issue 1, 2016, Pages

  Masroori, Nasser ^a   Merindol, Natacha ^a   Berthoux, Lionel ^a  

^a UNIVERSITÉ DU QUÉBEC À TROIS RIVIÈRES   (Canada)

Author keywords

HIV 1; Innate immunity; Interferon; Latency; Lentivirus; PML; Restriction factor

Indexed keywords

ALPHA INTERFERON; ANTIVIRUS AGENT; APOLIPOPROTEIN B; BETA INTERFERON; DISULFIRAM; HISTONE DEACETYLASE INHIBITOR; INTERFERON; ISOPROTEIN; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEIN KINASE C INHIBITOR; VORINOSTAT; NUCLEAR PROTEIN; PML PROTEIN, HUMAN; PML PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INNATE IMMUNITY; LENTIVIRINAE; LENTIVIRUS INFECTION; MOUSE; NONHUMAN; PROTEIN MOTIF; REVERSE TRANSCRIPTION; T LYMPHOCYTE; VIRUS INHIBITION; VIRUS LOAD; VIRUS REPLICATION; VIRUS TRANSCRIPTION; ANIMAL; CELL LINE; DNA SEQUENCE; GENETIC TRANSCRIPTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; SIMIAN IMMUNODEFICIENCY VIRUS;

ANIMALS; CELL LINE; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON TYPE I; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROMYELOCYTIC LEUKEMIA PROTEIN; REVERSE TRANSCRIPTION; SEQUENCE ANALYSIS, DNA; SIMIAN IMMUNODEFICIENCY VIRUS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS; VIRUS REPLICATION;

EID: 84962449725     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-016-0253-1     Document Type: Article

References (77)

1. Ozato K, Shin DM, Chang TH, Morse HC 3rd. TRIM family proteins and their emerging roles in innate immunity. Nat Rev Immunol. 2008;8:849-60.
2. de The H, Lavau C, Marchio A, Chomienne C, Degos L, Dejean A. The PML-RAR alpha fusion mRNA generated by the t(15;17) translocation in acute promyelocytic leukemia encodes a functionally altered RAR. Cell. 1991;66:675-84.
3. Goddard AD, Borrow J, Freemont PS, Solomon E. Characterization of a zinc finger gene disrupted by the t(15;17) in acute promyelocytic leukemia. Science. 1991;254:1371-4.
4. Pandolfi PP, Grignani F, Alcalay M, Mencarelli A, Biondi A, LoCoco F, Grignani F, Pelicci PG. Structure and origin of the acute promyelocytic leukemia myl/RAR alpha cDNA and characterization of its retinoid-binding and transactivation properties. Oncogene. 1991;6:1285-92.
5. Stadler M, Chelbi-Alix MK, Koken MH, Venturini L, Lee C, Saib A, Quignon F, Pelicano L, Guillemin MC, Schindler C, et al. Transcriptional induction of the PML growth suppressor gene by interferons is mediated through an ISRE and a GAS element. Oncogene. 1995;11:2565-73.
6. Borden KL. Pondering the promyelocytic leukemia protein (PML) puzzle: possible functions for PML nuclear bodies. Mol Cell Biol. 2002;22:5259-69.
7. Lallemand-Breitenbach V, de Thé H. PML nuclear bodies. Cold Spring Harb Perspect Biol. 2010;2:a000661.
8. Salomoni P, Pandolfi PP. The role of PML in tumor suppression. Cell. 2002;108:165-70.
9. Chelbi-Alix MK, Pelicano L, Quignon F, Koken MH, Venturini L, Stadler M, Pavlovic J, Degos L, de The H. Induction of the PML protein by interferons in normal and APL cells. Leukemia. 1995;9:2027-33.
10. Guldner HH, Szostecki C, Grotzinger T, Will H. IFN enhance expression of Sp100, an autoantigen in primary biliary cirrhosis. J Immunol. 1992;149:4067-73.
11. Everett RD. Interactions between DNA viruses, ND10 and the DNA damage response. Cell Microbiol. 2006;8:365-74.
12. Maul GG, Guldner HH, Spivack JG. Modification of discrete nuclear domains induced by herpes simplex virus type 1 immediate early gene 1 product (ICP0). J Gen Virol. 1993;74(Pt 12):2679-90.
13. Maul GG, Everett RD. The nuclear location of PML, a cellular member of the C3HC4 zinc-binding domain protein family, is rearranged during herpes simplex virus infection by the C3HC4 viral protein ICP0. J Gen Virol. 1994;75(Pt 6):1223-33.
14. Saffert RT, Kalejta RF. Inactivating a cellular intrinsic immune defense mediated by Daxx is the mechanism through which the human cytomegalovirus pp71 protein stimulates viral immediate-early gene expression. J Virol. 2006;80:3863-71.
15. Woodhall DL, Groves IJ, Reeves MB, Wilkinson G, Sinclair JH. Human Daxx-mediated repression of human cytomegalovirus gene expression correlates with a repressive chromatin structure around the major immediate early promoter. J Biol Chem. 2006;281:37652-60.
16. Chelbi-Alix MK, Quignon F, Pelicano L, Koken MH, de The H. Resistance to virus infection conferred by the interferon-induced promyelocytic leukemia protein. J Virol. 1998;72:1043-51.
17. Regad T, Saib A, Lallemand-Breitenbach V, Pandolfi PP, de The H, Chelbi-Alix MK. PML mediates the interferon-induced antiviral state against a complex retrovirus via its association with the viral transactivator. EMBO J. 2001;20:3495-505.
18. Kuroki M, Ariumi Y, Hijikata M, Ikeda M, Dansako H, Wakita T, Shimotohno K, Kato N. PML tumor suppressor protein is required for HCV production. Biochem Biophys Res Commun. 2013;430:592-7.
19. Day PM, Baker CC, Lowy DR, Schiller JT. Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression. Proc Natl Acad Sci USA. 2004;101:14252-7.
20. Berthoux L, Towers GJ, Gurer C, Salomoni P, Pandolfi PP, Luban J. As(2)O(3) enhances retroviral reverse transcription and counteracts Ref1 antiviral activity. J Virol. 2003;77:3167-80.
21. Turelli P, Doucas V, Craig E, Mangeat B, Klages N, Evans R, Kalpana G, Trono D. Cytoplasmic recruitment of INI1 and PML on incoming HIV preintegration complexes: interference with early steps of viral replication. Mol Cell. 2001;7:1245-54.
22. Kahle T, Volkmann B, Eissmann K, Herrmann A, Schmitt S, Wittmann S, Merkel L, Reuter N, Stamminger T, Gramberg T. TRIM19/PML restricts HIV infection in a cell type-dependent manner. Viruses. 2015. doi: 10.3390/v8010002.
23. Dutrieux J, Maarifi G, Portilho DM, Arhel NJ, Chelbi-Alix MK, Nisole S. PML/TRIM19-dependent inhibition of retroviral reverse-transcription by Daxx. PLoS Pathog. 2015;11:e1005280.
24. Holkmann Olsen C, Mocroft A, Kirk O, Vella S, Blaxhult A, Clumeck N, Fisher M, Katlama C, Phillips AN, Lundgren JD, Euro SSG. Interruption of combination antiretroviral therapy and risk of clinical disease progression to AIDS or death. HIV Med. 2007;8:96-104.
25. Chomont N, El-Far M, Ancuta P, Trautmann L, Procopio FA, Yassine-Diab B, Boucher G, Boulassel MR, Ghattas G, Brenchley JM, et al. HIV reservoir size and persistence are driven by T cell survival and homeostatic proliferation. Nat Med. 2009;15:893-900.
26. Soriano-Sarabia N, Bateson RE, Dahl NP, Crooks AM, Kuruc JD, Margolis DM, Archin NM. Quantitation of replication-competent HIV-1 in populations of resting CD4+ T cells. J Virol. 2014;88:14070-7.
27. Han Y, Lassen K, Monie D, Sedaghat AR, Shimoji S, Liu X, Pierson TC, Margolick JB, Siliciano RF, Siliciano JD. Resting CD4+ T cells from human immunodeficiency virus type 1 (HIV-1)-infected individuals carry integrated HIV-1 genomes within actively transcribed host genes. J Virol. 2004;78:6122-33.
28. Ruelas Debbie S, Greene Warner C. An integrated overview of HIV-1 latency. Cell. 2013;155:519-29.
29. Archin NM, Espeseth A, Parker D, Cheema M, Hazuda D, Margolis DM. Expression of latent HIV induced by the potent HDAC inhibitor suberoylanilide hydroxamic acid. AIDS Res Hum Retrovir. 2009;25:207-12.
30. Xing S, Bullen CK, Shroff NS, Shan L, Yang HC, Manucci JL, Bhat S, Zhang H, Margolick JB, Quinn TC, et al. Disulfiram reactivates latent HIV-1 in a Bcl-2-transduced primary CD4+ T cell model without inducing global T cell activation. J Virol. 2011;85:6060-4.
31. Laird GM, Bullen CK, Rosenbloom DI, Martin AR, Hill AL, Durand CM, Siliciano JD, Siliciano RF. Ex vivo analysis identifies effective HIV-1 latency-reversing drug combinations. J Clin Invest. 2015;125:1901-12.
32. Lusic M, Marini B, Ali H, Lucic B, Luzzati R, Giacca M. Proximity to PML nuclear bodies regulates HIV-1 latency in CD4+ T cells. Cell Host Microbe. 2013;13:665-77.
33. He J, Chen Y, Farzan M, Choe H, Ohagen A, Gartner S, Busciglio J, Yang X, Hofmann W, Newman W, et al. CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature. 1997;385:645-9.
34. Cowan S, Hatziioannou T, Cunningham T, Muesing MA, Gottlinger HG, Bieniasz PD. Cellular inhibitors with Fv1-like activity restrict human and simian immunodeficiency virus tropism. Proc Natl Acad Sci USA. 2002;99:11914-9.
35. Soboleski MR, Oaks J, Halford WP. Green fluorescent protein is a quantitative reporter of gene expression in individual eukaryotic cells. FASEB J. 2005;19:440-2.
36. Liao H-K, Gu Y, Diaz A, Marlett J, Takahashi Y, Li M, Suzuki K, Xu R, Hishida T, Chang C-J, et al. Use of the CRISPR/Cas9 system as an intracellular defense against HIV-1 infection in human cells. Nat Commun 2015;6.
37. Stremlau M, Perron M, Welikala S, Sodroski J. Species-specific variation in the B30.2 (SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction. J Virol. 2005;79:3139-45.
38. Browne EP, Littman DR. Species-specific restriction of apobec3-mediated hypermutation. J Virol. 2008;82:1305-13.
39. Jia B, Serra-Moreno R, Neidermyer W Jr, Rahmberg A, Mackey J, Fofana IB, Johnson WE, Westmoreland S, Evans DT. Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog. 2009;5:e1000429.
40. Wang ZG, Delva L, Gaboli M, Rivi R, Giorgio M, Cordon-Cardo C, Grosveld F, Pandolfi PP. Role of PML in cell growth and the retinoic acid pathway. Science. 1998;279:1547-51.
41. Hatziioannou T, Cowan S, Goff SP, Bieniasz PD, Towers GJ. Restriction of multiple divergent retroviruses by Lv1 and Ref1. EMBO J. 2003;22:385-94.
42. Butler SL, Hansen MS, Bushman FD. A quantitative assay for HIV DNA integration in vivo. Nat Med. 2001;7:631-4.
43. Berthoux L, Sebastian S, Sokolskaja E, Luban J. Cyclophilin A is required for TRIM5{alpha}-mediated resistance to HIV-1 in Old World monkey cells. Proc Natl Acad Sci USA. 2005;102:14849-53.
44. Besnier C, Ylinen L, Strange B, Lister A, Takeuchi Y, Goff SP, Towers GJ. Characterization of murine leukemia virus restriction in mammals. J Virol. 2003;77:13403-6.
45. He G, Margolis DM. Counterregulation of chromatin deacetylation and histone deacetylase occupancy at the integrated promoter of human immunodeficiency virus type 1 (HIV-1) by the HIV-1 repressor YY1 and HIV-1 activator Tat. Mol Cell Biol. 2002;22:2965-73.
46. Archin NM, Liberty AL, Kashuba AD, Choudhary SK, Kuruc JD, Crooks AM, Parker DC, Anderson EM, Kearney MF, Strain MC, et al. Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy. Nature. 2012;487:482-5.
47. Salsman J, Zimmerman N, Chen T, Domagala M, Frappier L. Genome-wide screen of three herpesviruses for protein subcellular localization and alteration of PML nuclear bodies. PLoS Pathog. 2008;4:e1000100.
48. Lavau C, Marchio A, Fagioli M, Jansen J, Falini B, Lebon P, Grosveld F, Pandolfi PP, Pelicci PG, Dejean A. The acute promyelocytic leukaemia-associated PML gene is induced by interferon. Oncogene. 1995;11:871-6.
49. Mogensen KE, Lewerenz M, Reboul J, Lutfalla G, Uze G. The type I interferon receptor: structure, function, and evolution of a family business. J Interferon Cytokine Res. 1999;19:1069-98.
50. Cuchet D, Sykes A, Nicolas A, Orr A, Murray J, Sirma H, Heeren J, Bartelt A, Everett RD. PML isoforms I and II participate in PML-dependent restriction of HSV-1 replication. J Cell Sci. 2011;124:280-91.
51. Hofmann W, Schubert D, LaBonte J, Munson L, Gibson S, Scammell J, Ferrigno P, Sodroski J. Species-specific, postentry barriers to primate immunodeficiency virus infection. J Virol. 1999;73:10020-8.
52. Bieniasz PD, Cullen BR. Multiple blocks to human immunodeficiency virus type 1 replication in rodent cells. J Virol. 2000;74:9868-77.
53. Baumann JG, Unutmaz D, Miller MD, Breun SK, Grill SM, Mirro J, Littman DR, Rein A, KewalRamani VN. Murine T cells potently restrict human immunodeficiency virus infection. J Virol. 2004;78:12537-47.
54. Tsurutani N, Yasuda J, Yamamoto N, Choi BI, Kadoki M, Iwakura Y. Nuclear import of the preintegration complex is blocked upon infection by human immunodeficiency virus type 1 in mouse cells. J Virol. 2007;81:677-88.
55. Noser JA, Towers GJ, Sakuma R, Dumont JM, Collins MK, Ikeda Y. Cyclosporine increases human immunodeficiency virus type 1 vector transduction of primary mouse cells. J Virol. 2006;80:7769-74.
56. Kim YE, Ahn JH. Positive role of promyelocytic leukemia protein in type I interferon response and its regulation by human cytomegalovirus. PLoS Pathog. 2015;11:e1004785.
57. Zhang J-X, Diehl GE, Littman DR. Relief of preintegration inhibition and characterization of additional blocks for HIV replication in primary mouse T cells. PLoS One. 2008;3:e2035.
58. Wang P, Qu X, Wang X, Liu L, Zhu X, Zeng H, Zhu H. As2O3 synergistically reactivate latent HIV-1 by induction of NF-kappaB. Antivir Res. 2013;100:688-97.
59. Berthoux L, Sebastian S, Sokolskaja E, Luban J. Lv1 inhibition of human immunodeficiency virus type 1 is counteracted by factors that stimulate synthesis or nuclear translocation of viral cDNA. J Virol. 2004;78:11739-50.
60. Sebastian S, Sokolskaja E, Luban J. Arsenic counteracts human immunodeficiency virus type 1 restriction by various TRIM5 orthologues in a cell type-dependent manner. J Virol. 2006;80:2051-4.
61. Stalder R, Blanchet F, Mangeat B, Piguet V. Arsenic modulates APOBEC3G-mediated restriction to HIV-1 infection in myeloid dendritic cells. J Leukoc Biol. 2010;88:1251-8.
62. SM/HIV-2 lineage prior to integration. PLoS Pathog. 2015;11:e1005050.
63. Pion M, Stalder R, Correa R, Mangeat B, Towers GJ, Piguet V. Identification of an arsenic-sensitive block to primate lentiviral infection of human dendritic cells. J Virol. 2007;81:12086-90.
64. Zhang XW, Yan XJ, Zhou ZR, Yang FF, Wu ZY, Sun HB, Liang WX, Song AX, Lallemand-Breitenbach V, Jeanne M, et al. Arsenic trioxide controls the fate of the PML-RARalpha oncoprotein by directly binding PML. Science. 2010;328:240-3.
65. Jeanne M, Lallemand-Breitenbach V, Ferhi O, Koken M, Le Bras M, Duffort S, Peres L, Berthier C, Soilihi H, Raught B, de Thé H. PML/RARA oxidation and arsenic binding initiate the antileukemia response of As2O3. Cancer Cell. 2010;18:88-98.
66. Bieniasz PD, Cullen BR. Multiple blocks to human immunodeficiency virus type 1 replication in rodent cells. J Virol. 2000;74:9868-77.
67. Elinav H, Wu Y, Coskun A, Hryckiewicz K, Kemler I, Hu Y, Rogers H, Hao B, Ben Mamoun C, Poeschla E, Sutton R. Human CRM1 augments production of infectious human and feline immunodeficiency viruses from murine cells. J Virol. 2012;86:12053-68.
68. Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotech. 1997;15:871-5.
69. Naviaux RK, Costanzi E, Haas M, Verma IM. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J Virol. 1996;70:5701-5.
70. Bérubé J, Bouchard A, Berthoux L. Both TRIM5alpha and TRIMCyp have only weak antiviral activity in canine D17 cells. Retrovirology. 2007;4:68.
71. Berggren WL, Lutz M, Modesto V. General spinfection protocol. In: StemBook [Internet]. Salk Institute for Biological Studies, La Jolla; 2012.
72. Bock M, Bishop KN, Towers G, Stoye JP. Use of a transient assay for studying the genetic determinants of Fv1 restriction. J Virol. 2000;74:7422-30.
73. Neil S, Martin F, Ikeda Y, Collins M. Postentry restriction to human immunodeficiency virus-based vector transduction in human monocytes. J Virol. 2001;75:5448-56.
74. Mitrophanous K, Yoon S, Rohll J, Patil D, Wilkes F, Kim V, Kingsman S, Kingsman A, Mazarakis N. Stable gene transfer to the nervous system using a non-primate lentiviral vector. Gene Ther. 1999;6:1808-18.
75. Malbec M, Pham QT, Plourde MB, Létourneau-Hogan A, Nepveu-Traversy M-É, Berthoux L. Murine double minute 2 as a modulator of retroviral restrictions mediated by TRIM5α. Virology. 2010;405:414-23.
76. Pertel T, Hausmann S, Morger D, Züger S, Guerra J, Lascano J, Reinhard C, Santoni F, Uchil PD, Chatel L, et al. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature. 2011;472:361-5.
77. Veillette M, Bichel K, Pawlica P, Freund SM, Plourde MB, Pham QT, Reyes-Moreno C, James LC, Berthoux L. The V86M mutation in HIV-1 capsid confers resistance to TRIM5alpha by abrogation of cyclophilin A-dependent restriction and enhancement of viral nuclear import. Retrovirology. 2013;10:25.