The HIV-1 Nef Protein Binds Argonaute-2 and Functions as a Viral Suppressor of RNA Interference

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Aqil, Madeeha ^a   Naqvi, Afsar Raza ^a,b   Bano, Aalia Shahr ^a   Jameel, Shahid ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 2 PROTEIN; GLYCINE; NEF PROTEIN; RNA INDUCED SILENCING COMPLEX; TRYPTOPHAN; ARGONAUTE PROTEIN; AUTOANTIGEN; AUTOANTIGEN GW182, HUMAN; EIF2C2 PROTEIN, HUMAN; MICRORNA; NEF PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; PROTEIN BINDING; RNA BINDING PROTEIN;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MUTATION; NONHUMAN; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; VIRAL PHENOMENA AND FUNCTIONS; VIRUS INFECTIVITY; VIRUS INHIBITION; VIRUS YIELD; AMINO ACID SEQUENCE; CELL LINE; CHEMISTRY; EXOSOME; GENETICS; METABOLISM; MOLECULAR GENETICS; MULTIVESICULAR BODY; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN TRANSPORT; RNA SPLICING;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ARGONAUTE PROTEINS; AUTOANTIGENS; CELL LINE; CONSERVED SEQUENCE; EXOSOMES; HIV-1; HUMANS; MICRORNAS; MOLECULAR SEQUENCE DATA; MULTIVESICULAR BODIES; MUTATION; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; PROTEIN BINDING; PROTEIN TRANSPORT; RNA INTERFERENCE; RNA SPLICING; RNA-BINDING PROTEINS;

EID: 84883414693     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074472     Document Type: Article

References (46)

1. Freed EO, Martin MA (2007) in Field's Virology, eds Knipe DM, Howley PM (Wolters Kluwer Lippincott, Williams & Wilkins, Philadelphia), 2107-2185.
2. Kestler HW 3rd, Ringler DJ, Mori K, Panicali DL, Sehgal PK, et al. (1991) Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 65: 651-662.
3. Leonard JA, Filzen T, Carter CC, Schaefer M, Collins KL, (2011) HIV-1 Nef disrupts intracellular trafficking of major histocompatibility complex class I, CD4, CD8, and CD28 by distinct pathways that share common elements. J Virol 85: 6867-6881.
4. Kirchhoff F, Schindler M, Specht A, Arhel N, Münch J, (2008) Role of Nef in primate lentiviral immunopathogenesis. Cell Mol Life Sci 65: 2621-2636.
5. Han YH, Luo YJ, Wu Q, Jovel J, Wang XH, et al. (2011) RNA-based immunity terminates viral infection in adult Drosophila in the absence of viral suppression of RNA interference: characterization of viral small interfering RNA populations in wild-type and mutant flies. J Virol 85: 13153-13163.
6. Haasnoot J, Berkhout B, (2011) RNAi and cellular miRNAs in infections by mammalian viruses. Methods Mol Biol 721: 23-41.
7. Voinnet O, Lederer C, Baulcombe DC, (2000) A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103: 157-167.
8. Jeang KT, (2012) RNAi in the regulation of mammalian viral infections. BMC Biology10: 58.
9. Matskevich AA, Moelling K, (2007) Dicer is involved in protection against influenza A virus infection. J Gen Virol 88: 2627-2635.
10. Otsuka M, Jing Q, Georgel P, New L, Chen J, et al. (2007) Hypersusceptibility to vesicular stomatitis virus infection in Dicer1-deficient mice is due to impaired miR24 and miR93 expression. Immunity 27: 123-134.
11. Huang J, Wang F, Argyris E, Chen K, Liang Z, et al. (2007) Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. Nat Med 13: 1241-1247.
12. Kumar A, Jeang KT, (2008) Insights into cellular microRNAs and human immunodeficiency virus type 1 (HIV-1). J Cell Physiol 216: 327-331.
13. Nathans R, Chu CY, Serquina AK, Lu CC, Cao H, et al. (2009) Cellular microRNA and P bodies modulate host-HIV-1 interactions. Mol Cell 34: 696-709.
14. Yeung ML, Bennasser Y, Watashi K, Le SY, Houzet L, et al. (2009) Pyrosequencing of small non-coding RNAs in HIV-1 infected cells: evidence for the processing of a viral-cellular double-stranded RNA hybrid. Nucleic Acids Res 37: 6575-6586.
15. Triboulet R, Mari B, Lin YL, Chable-Bessia C, Bennasser Y, et al. (2007) Suppression of microRNA-silencing pathway by HIV-1 during virus replication. Science 315: 1579-1582.
16. Houzet L, Jeang KT, (2011) MicroRNAs and human retroviruses. Biochim Biophys Acta 1809: 686-693.
17. Ouellet DL, Plante I, Barat C, Tremblay MJ, Provost P, (2009) Emergence of a complex relationship between HIV-1 and the microRNA pathway. Methods Mol Biol 487: 415-433.
18. Song L, Gao S, Jiang W, Chen S, Liu Y, et al. (2011) Silencing suppressors: viral weapons for countering host cell defenses. Protein Cell 2: 273-281.
19. Christensen HS, Daher A, Soye KJ, Frankel LB, Alexander MR, et al. (2007) Small interfering RNAs against the TAR RNA binding protein, TRBP, a Dicer cofactor, inhibit human immunodeficiency virus type 1 long terminal repeat expression and viral production. J Virol 81: 5121-5131.
20. Sanghvi VR, Steel LF, (2011) A re-examination of global suppression of RNA interference by HIV-1. PLoS One 6: e17246.
21. Cikaluk DE, Tahbaz N, Hendricks LC, DiMattia GE, Hansen D, et al. (1999) GERp95, a membrane-associated protein that belongs to a family of proteins involved in stem cell differentiation. Mol Biol Cell 10: 3357-3372.
22. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O, (2009) Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 11: 1143-1149.
23. Gibbings D, Voinnet O, (2010) Control of RNA silencing and localization by endolysosomes. Trends Cell Biol 20: 491-501.
24. Lee YS, Pressman S, Andress AP, Kim K, White JL, et al. (2009) Silencing by small RNAs is linked to endosomal trafficking. Nat Cell Biol 11: 1150-1156.
25. Lenassi M, Cagney G, Liao M, Vaupotic T, Bartholomeeusen K, et al. (2010) HIV Nef is secreted in exosomes and triggers apoptosis in bystander CD4+ T cells. Traffic 11: 110-122.
26. Simpson RJ, Lim JW, Moritz RL, Mathivanan S, (2009) Exosomes: proteomic insights and diagnostic potential. Expert Rev Proteomics 6: 267-283.
27. Stumptner-Cuvelette P, Jouve M, Helft J, Dugast M, Glouzman AS, et al. (2003) Human immunodeficiency virus-1 Nef expression induces intracellular accumulation of multivesicular bodies and major histocompatibility complex class II complexes: potential role of phosphatidylinositol 3-kinase. Mol Biol Cell 14: 4857-4870.
28. Benaroch P, Billard E, Gaudin R, Schindler M, Jouve M, (2010) HIV-1 assembly in macrophages. Retrovirology 7: 29.
29. Chaudhry A, Das SR, Hussain A, Mayor S, George A, et al. (2005) The Nef protein of HIV-1 induces loss of cell surface costimulatory molecules CD80 and CD86 in APCs. J Immunol 175: 4566-4574.
30. Sherer NM, Lehmann MJ, Jimenez-Soto LF, Ingmundson A, Horner SM, et al. (2003) Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic 4: 785-801.
31. Miyoshi K, Tsukumo H, Nagami T, Siomi H, Siomi MC, (2005) Slicer function of Drosophila Argonautes and its involvement in RISC formation. Genes Dev 19: 2837-2848.
32. Thery C, Amigorena S, Raposo G, Clayton A (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol Chapter 3, Unit 3.22.
33. Folks TM, Justement J, Kinter A, Dinarello CA, Fauci AS, (1987) Cytokine-induced expression of HIV-1 in a chronically infected promonocyte cell line. Science 238: 800-802.
34. Fabian MR, Sonenberg N, Filipowicz W, (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79: 351-379.
35. Takimoto K, Wakiyama M, Yokoyama S, (2009) Mammalian GW182 contains multiple Argonaute-binding sites and functions in microRNA-mediated translational repression. RNA 15: 1078-1089.
36. Azevedo J, Garcia D, Pontier D, Ohnesorge S, Yu A, et al. (2010) Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen-encoded GW repeat protein. Genes Dev 24: 904-915.
37. Giner A, Lakatos L, Garcia-Chapa M, Lopez-Moya JJ, Burgyan J, (2010) Viral protein inhibits RISC activity by argonaute binding through conserved WG/GW motifs. PLoS Pathog 6: e1000996.
38. Schirle NT, MacRae IJ, (2012) The crystal structure of human Argonaute2. Science 336: 1037-1040.
39. Costa LJ, Chen N, Lopes A, Aguiar RS, Tanuri A, et al. (2006) Interactions between Nef and AIP1 proliferate multivesicular bodies and facilitate egress of HIV-1. Retrovirology 3: 33.
40. Rawlings RA, Krishnan V, Walter NG, (2011) Viral RNAi suppressor reversibly binds siRNA to outcompete Dicer and RISC via multiple turnover. J Mol Biol 408: 262-276.
41. Muratori C, Cavallin LE, Krätzel K, Tinari A, De Milito A, et al. (2009) Massive secretion by T cells is caused by HIV Nef in infected cells and by Nef transfer to bystander cells. Cell Host Microbe 6: 218-230.
42. Ali SA, Huang MB, Campbell PE, Roth WW, Campbell T, et al. (2010) Genetic characterization of HIV type 1 Nef-induced vesicle secretion. AIDS Res Hum Retroviruses 26: 173-192.
43. Echarri A, Gonzalez ME, Carrasco L, (1997) The N-terminal Arg-rich region of human immunodeficiency virus types 1 and 2 and simian immunodeficiency virus Nef is involved in RNA binding. Eur J Biochem 246: 38-44.
44. Li WX, Li H, Lu R, Li F, Dus M, et al. (2004) Interferon antagonist proteins of imfluenza and vaccinica viruses are suppressors of RNA silencing. PNAS 101: 1350-1355.
45. Nayak A, Berry B, Tassetto M, Kunitomi M, Acevedo A, et al. (2010) Cricket paralysis virus antagonizes Argonaute 2 to modulate antiviral defense in Drosophila. Nat Struct Mol Biol 17: 547-554.
46. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, et al. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659.