A HIV-1 Tat mutant protein disrupts HIV-1 Rev function by targeting the DEAD-box RNA helicase DDX1

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  Lin, Min Hsuan ^a   Sivakumaran, Haran ^a   Jones, Alun ^b   Li, Dongsheng ^a   Harper, Callista ^b   Wei, Ting ^a   Jin, Hongping ^a   Rustanti, Lina ^a   Meunier, Frederic A ^b   Spann, Kirsten ^b   Harrich, David ^a,b  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

DDX1; Helicase; HIV 1; Nullbasic; Rev; RNA export; Tat

Indexed keywords

DEAD BOX PROTEIN; MUTANT PROTEIN; PROTEIN DDX1; PROTEIN DDX17; PROTEIN DDX3; PROTEIN NULLBASIC; REV PROTEIN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; VIRUS MESSENGER RNA; VIRUS RNA; DDX1 PROTEIN, HUMAN;

ARTICLE; BIO LAYER INTERFEROMETRY ASSAY; CELL LYSATE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOPRECIPITATION; INHIBITION KINETICS; MASS SPECTROMETRY; NONHUMAN; NUCLEOLUS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN OVEREXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN REPORTER ASSAY; PROTEOMICS; RNA SPLICING; VIRUS CAPSID; VIRUS CELL INTERACTION; WILD TYPE; ANTAGONISTS AND INHIBITORS; CELL LINE; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN ANALYSIS; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CELL LINE; DEAD-BOX RNA HELICASES; HIV-1; HUMANS; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MUTANT PROTEINS; PROTEIN INTERACTION MAPPING; PROTEOMICS; REV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; VIRUS REPLICATION;

EID: 84924190525     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-014-0121-9     Document Type: Article

References (61)

1. Pollard VW, Malim MH: The HIV-1 Rev protein. Annu Rev Microbiol 1998, 52:491-532.
2. Venkatesh LK, Mohammed S, Chinnadurai G: Functional domains of the HIV-1 rev gene required for trans-regulation and subcellular localization. Virology 1990, 176(1):39-47.
3. Henderson BR, Percipalle P: Interactions between HIV Rev and nuclear import and export factors: the Rev nuclear localisation signal mediates specific binding to human importin-beta. J Mol Biol 1997, 274(5):693-707.
4. Szebeni A, Mehrotra B, Baumann A, Adam SA, Wingfield PT, Olson MO: Nucleolar protein B23 stimulates nuclear import of the HIV-1 Rev protein and NLS-conjugated albumin. Biochemistry (Mosc) 1997, 36(13):3941-3949.
5. Truant R, Cullen BR: The arginine-rich domains present in human immunodeficiency virus type 1 Tat and Rev function as direct importin beta-dependent nuclear localization signals. Mol Cell Biol 1999, 19(2):1210-1217.
6. Malim MH, Hauber J, Le SY, Maizel JV, Cullen BR: The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature 1989, 338(6212):254-257.
7. Cochrane AW, Chen CH, Rosen CA: Specific interaction of the human immunodeficiency virus Rev protein with a structured region in the env mRNA. Proc Natl Acad Sci U S A 1990, 87(3):1198-1202.
8. Fischer U, Huber J, Boelens WC, Mattaj IW, Luhrmann R: The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell 1995, 82(3):475-483.
9. Szilvay AM, Brokstad KA, Kopperud R, Haukenes G, Kalland KH: Nuclear export of the human immunodeficiency virus type 1 nucleocytoplasmic shuttle protein Rev is mediated by its activation domain and is blocked by transdominant negative mutants. J Virol 1995, 69(6):3315-3323.
10. Neville M, Stutz F, Lee L, Davis LI, Rosbash M: The importin-beta family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr Biol 1997, 7(10):767-775.
11. Askjaer P, Jensen TH, Nilsson J, Englmeier L, Kjems J: The specificity of the CRM1-Rev nuclear export signal interaction is mediated by RanGTP. J Biol Chem 1998, 273(50):33414-33422.
12. Malim MH, Cullen BR: HIV-1 structural gene expression requires the binding of multiple Rev monomers to the viral RRE: implications for HIV-1 latency. Cell 1991, 65(2):241-248.
13. Thomas SL, Oft M, Jaksche H, Casari G, Heger P, Dobrovnik M, Bevec D, Hauber J: Functional analysis of the human immunodeficiency virus type 1 Rev protein oligomerization interface. J Virol 1998, 72(4):2935-2944.
14. Hoffmann D, Schwarck D, Banning C, Brenner M, Mariyanna L, Krepstakies M, Schindler M, Millar DP, Hauber J: Formation of trans-activation competent HIV-1 Rev:RRE complexes requires the recruitment of multiple protein activation domains. PLoS One 2012, 7(6):e38305.
15. Fornerod M, Ohno M, Yoshida M, Mattaj IW: CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 1997, 90(6):1051-1060.
16. Fukuda M, Asano S, Nakamura T, Adachi M, Yoshida M, Yanagida M, Nishida E: CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature 1997, 390(6657):308-311.
17. Arnold M, Nath A, Hauber J, Kehlenbach RH: Multiple importins function as nuclear transport receptors for the Rev protein of human immunodeficiency virus type 1. J Biol Chem 2006, 281(30):20883-20890.
18. Groom HC, Anderson EC, Lever AM: Rev: beyond nuclear export. J Gen Virol 2009, 90(Pt 6):1303-1318.
19. Grewe B, Uberla K: The human immunodeficiency virus type 1 Rev protein: menage a trois during the early phase of the lentiviral replication cycle. J Gen Virol 2010, 91(Pt 8):1893-1897.
20. Yedavalli VS, Jeang KT: Trimethylguanosine capping selectively promotes expression of Rev-dependent HIV-1 RNAs. Proc Natl Acad Sci U S A 2010, 107(33):14787-14792.
21. Linder P, Jankowsky E: From unwinding to clamping - the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 2011, 12(8):505-516.
22. Linder P, Fuller-Pace FV: Looking back on the birth of DEAD-box RNA helicases. Biochim Biophys Acta 2013, 1829(8):750-755.
23. Putnam AA, Jankowsky E: DEAD-box helicases as integrators of RNA, nucleotide and protein binding. Biochim Biophys Acta 2013, 1829(8):884-893.
24. Lorgeoux RP, Guo F, Liang C: From promoting to inhibiting: diverse roles of helicases in HIV-1 replication. Retrovirology 2012, 9(1):79.
25. Robertson-Anderson RM, Wang J, Edgcomb SP, Carmel AB, Williamson JR, Millar DP: Single-molecule studies reveal that DEAD box protein DDX1 promotes oligomerization of HIV-1 Rev on the Rev response element. J Mol Biol 2011, 410(5):959-971.
26. Fang J, Kubota S, Yang B, Zhou N, Zhang H, Godbout R, Pomerantz RJ: A DEAD box protein facilitates HIV-1 replication as a cellular co-factor of Rev. Virology 2004, 330(2):471-480.
27. Edgcomb SP, Carmel AB, Naji S, Ambrus-Aikelin G, Reyes JR, Saphire AC, Gerace L, Williamson JR: DDX1 is an RNA-dependent ATPase involved in HIV-1 Rev function and virus replication. J Mol Biol 2012, 415(1):61-74.
28. Fang J, Acheampong E, Dave R, Wang F, Mukhtar M, Pomerantz RJ: The RNA helicase DDX1 is involved in restricted HIV-1 Rev function in human astrocytes. Virology 2005, 336(2):299-307.
29. Yedavalli VS, Neuveut C, Chi YH, Kleiman L, Jeang KT: Requirement of DDX3 DEAD box RNA helicase for HIV-1 Rev-RRE export function. Cell 2004, 119(3):381-392.
30. Ishaq M, Hu J, Wu X, Fu Q, Yang Y, Liu Q, Guo D: Knockdown of cellular RNA helicase DDX3 by short hairpin RNAs suppresses HIV-1 viral replication without inducing apoptosis. Mol Biotechnol 2008, 39(3):231-238.
31. Lai MC, Wang SW, Cheng L, Tarn WY, Tsai SJ, Sun HS: Human DDX3 interacts with the HIV-1 Tat protein to facilitate viral mRNA translation. PLoS One 2013, 8(7):e68665.
32. Yasuda-Inoue M, Kuroki M, Ariumi Y: DDX3 RNA helicase is required for HIV-1 Tat function. Biochem Biophys Res Commun 2013, 441(3):607-611.
33. Yasuda-Inoue M, Kuroki M, Ariumi Y: Distinct DDX DEAD-box RNA helicases cooperate to modulate the HIV-1 Rev function. Biochem Biophys Res Commun 2013, 434(4):803-808.
34. Naji S, Ambrus G, Cimermancic P, Reyes JR, Johnson JR, Filbrandt R, Huber MD, Vesely P, Krogan NJ, Yates JR 3rd, Saphire AC, Gerace L: Host cell interactome of HIV-1 Rev includes RNA helicases involved in multiple facets of virus production. Mol Cell Proteomics 2012, 11(4):M111 015313.
35. Meredith LW, Sivakumaran H, Major L, Suhrbier A, Harrich D: Potent inhibition of HIV-1 replication by a Tat mutant. PLoS One 2009, 4(11):e7769.
36. Apolloni A, Sivakumaran H, Lin MH, Li D, Kershaw MH, Harrich D: A mutant Tat protein provides strong protection from HIV-1 infection in human CD4+ T cells. Hum Gene Ther 2013, 24:270-282.
37. Lin MH, Sivakumaran H, Apolloni A, Wei T, Jans DA, Harrich D: Nullbasic, a Potent Anti-HIV Tat Mutant, Induces CRM1-Dependent Disruption of HIV Rev Trafficking. PLoS One 2012, 7(12):e51466.
38. Wodrich H, Schambach A, Krausslich HG: Multiple copies of the Mason-Pfizer monkey virus constitutive RNA transport element lead to enhanced HIV-1 Gag expression in a context-dependent manner. Nucleic Acids Res 2000, 28(4):901-910.
39. Lorgeoux RP, Pan Q, Le Duff Y, Liang C: DDX17 promotes the production of infectious HIV-1 particles through modulating viral RNA packaging and translation frameshift. Virology 2013, 443(2):384-392.
40. Concepcion J, Witte K, Wartchow C, Choo S, Yao D, Persson H, Wei J, Li P, Heidecker B, Ma W, Varma R, Zhao LS, Perillat D, Carricato G, Recknor M, Du K, Ho H, Ellis T, Gamez J, Howes M, Phi-Wilson J, Lockard S, Zuk R, Tan H: Label-free detection of biomolecular interactions using BioLayer interferometry for kinetic characterization. Comb Chem High Throughput Screen 2009, 12(8):791-800.
41. Wallner J, Lhota G, Jeschek D, Mader A, Vorauer-Uhl K: Application of Bio-Layer Interferometry for the analysis of protein/liposome interactions. J Pharm Biomed Anal 2013, 72:150-154.
42. Suhasini M, Reddy TR: Cellular proteins and HIV-1 Rev function. Curr HIV Res 2009, 7(1):91-100.
43. Yedavalli VS, Jeang KT: Rev-ing up post-transcriptional HIV-1 RNA expression. RNA Biol 2011, 8(2):195-199.
44. Jeang KT: Multi-Faceted Post-Transcriptional Functions of HIV-1 Rev. Biology (Basel) 2012, 1(2):165-174.
45. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, Lockett S: Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 2004, 86(6):3993-4003.
46. Daelemans D, Costes SV, Cho EH, Erwin-Cohen RA, Lockett S, Pavlakis GN: In vivo HIV-1 Rev multimerization in the nucleolus and cytoplasm identified by fluorescence resonance energy transfer. J Biol Chem 2004, 279(48):50167-50175.
47. Daelemans D, Costes SV, Lockett S, Pavlakis GN: Kinetic and molecular analysis of nuclear export factor CRM1 association with its cargo in vivo. Mol Cell Biol 2005, 25(2):728-739.
48. Li J, Tang H, Mullen TM, Westberg C, Reddy TR, Rose DW, Wong-Staal F: A role for RNA helicase A in post-transcriptional regulation of HIV type 1. Proc Natl Acad Sci U S A 1999, 96(2):709-714.
49. Dayton AI: Matrin 3 and HIV Rev regulation of mRNA. Retrovirology 2011, 8:62.
50. Kula A, Guerra J, Knezevich A, Kleva D, Myers MP, Marcello A: Characterization of the HIV-1 RNA associated proteome identifies Matrin 3 as a nuclear cofactor of Rev function. Retrovirology 2011, 8:60.
51. Yedavalli VS, Jeang KT: Matrin 3 is a co-factor for HIV-1 Rev in regulating post-transcriptional viral gene expression. Retrovirology 2011, 8:61.
52. Kula A, Gharu L, Marcello A: HIV-1 pre-mRNA commitment to Rev mediated export through PSF and Matrin 3. Virology 2013, 435(2):329-340.
53. Zuo P, Manley JL: Functional domains of the human splicing factor ASF/SF2. EMBO J 1993, 12(12):4727-4737.
54. Powell DM, Amaral MC, Wu JY, Maniatis T, Greene WC: HIV Rev-dependent binding of SF2/ASF to the Rev response element: possible role in Rev-mediated inhibition of HIV RNA splicing. Proc Natl Acad Sci U S A 1997, 94(3):973-978.
55. Pongoski J, Asai K, Cochrane A: Positive and negative modulation of human immunodeficiency virus type 1 Rev function by cis and trans regulators of viral RNA splicing. J Virol 2002, 76(10):5108-5120.
56. Gautier VW, Gu L, O'Donoghue N, Pennington S, Sheehy N, Hall WW: In vitro nuclear interactome of the HIV-1 Tat protein. Retrovirology 2009, 6:47.
57. Jarboui MA, Bidoia C, Woods E, Roe B, Wynne K, Elia G, Hall WW, Gautier VW: Nucleolar protein trafficking in response to HIV-1 Tat: rewiring the nucleolus. PLoS One 2012, 7(11):e48702.
58. Arrigo SJ, Weitsman S, Zack JA, Chen IS: Characterization and expression of novel singly spliced RNA species of human immunodeficiency virus type 1. J Virol 1990, 64(9):4585-4588.
59. Dignam JD, Lebovitz RM, Roeder RG: Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 1983, 11(5):1475-1489.
60. Abmayr SM, Yao T, Parmely T, Workman JL: Preparation of nuclear and cytoplasmic extracts from mammalian cells. Curr Protoc Mol Biol 2006, 75:12.1:12.1.1-12.1.10.
61. Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.