HIV-1 Nef induces proinflammatory state in macrophages through its acidic cluster domain: Involvement of TNF alpha receptor associated factor 2

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Mangino, Giorgio ^a,b   Percario, Zulema A ^a   Fiorucci, Gianna ^c   Vaccari, Gabriele ^d   Acconcia, Filippo ^a   Chiarabelli, Cristiano ^a   Leone, Stefano ^a   Noto, Alessia ^a   Horenkamp, Florian A ^e   Manrique, Santiago ^e   Romeo, Giovanna ^b   Polticelli, Fabio ^a   Geyer, Matthias ^e   Affabris, Elisabetta ^a  

^a ROMA TRE UNIVERSITY   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c CNR   (Italy)

^d ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^e Abteilung Physikalische Biochemie   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; MITOGEN ACTIVATED PROTEIN KINASE; NEF PROTEIN; STAT1 PROTEIN; STAT2 PROTEIN; STAT3 PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; VIRUS PROTEIN; AUTACOID; CHEMOKINE; INTERLEUKIN 6; IRF3 PROTEIN, HUMAN; MYRISTIC ACID; PHOSPHOTYROSINE; STAT PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; MACROPHAGE; MONOCYTE; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; BINDING SITE; BIOSYNTHESIS; CHEMISTRY; CONSENSUS SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; INFLAMMATION; METABOLISM; MOLECULAR GENETICS; MUTATION; PATHOLOGY; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

AMINO ACID SEQUENCE; BINDING SITES; CHEMOKINES; CONSENSUS SEQUENCE; GENE EXPRESSION REGULATION; HIV-1; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; INTERLEUKIN-6; MACROPHAGES; MOLECULAR SEQUENCE DATA; MUTATION; MYRISTIC ACID; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; NF-KAPPA B; PHOSPHOTYROSINE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; STAT TRANSCRIPTION FACTORS; STRUCTURE-ACTIVITY RELATIONSHIP; TNF RECEPTOR-ASSOCIATED FACTOR 2; TNF RECEPTOR-ASSOCIATED FACTOR 6; TUMOR NECROSIS FACTOR-ALPHA;

EID: 80051998389     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022982     Document Type: Article

References (64)

1. Narayan O, Clements JE, Strandberg JD, Cork LC, Griffin DE, (1980) Biological characterization of the virus causing leukoencephalitis and arthritis in goats. J Gen Virol 50: 69-79.
2. Anderson LW, Klevjer-Anderson P, Liggitt HD, (1983) Susceptibility of blood-derived monocytes and macrophages to caprine arthritis-encephalitis virus. Infect Immun 41: 837-840.
3. Gendelman HE, Narayan O, Kennedy-Stoskopf S, Kennedy PG, Ghotbi Z, et al. (1986) Tropism of sheep lentiviruses for monocytes: susceptibility to infection and virus gene expression increase during maturation of monocytes to macrophages. J Virol 58: 67-74.
4. Gartner S, Markovits P, Markovitz DM, Kaplan MH, Gallo RC, et al. (1986) The role of mononuclear phagocytes in HTLV-III/LAV infection. Science 233: 215-219.
5. Koenig S, Gendelman HE, Orenstein JM, Dal Canto MC, Pezeshkpour GH, et al. (1986) Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science 233: 1089-1093.
6. Desrosiers RC, (1990) The simian immunodeficiency viruses. Annu Rev Immunol 8: 557-578.
7. Dow SW, Mathiason CK, Hoover EA, (1999) In vivo monocyte tropism of pathogenic feline immunodeficiency viruses. J Virol 73: 6852-6861.
8. Wolfs TF, Zwart G, Bakker M, Goudsmit J, (1992) HIV-1 genomic RNA diversification following sexual and parenteral virus transmission. Virology 189: 103-110.
9. Zhu T, Mo H, Wang N, Nam DS, Cao Y, et al. (1993) Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science 261: 1179-1181.
10. Aquaro S, Calio R, Balzarini J, Bellocchi MC, Garaci E, et al. (2002) Macrophages and HIV infection: therapeutical approaches toward this strategic virus reservoir. Antiviral Res 55: 209-225.
11. Swingler S, Mann A, Jacque J, Brichacek B, Sasseville VG, et al. (1999) HIV-1 Nef mediates lymphocyte chemotaxis and activation by infected macrophages. Nat Med 5: 997-1003.
12. Swingler S, Brichacek B, Jacque JM, Ulich C, Zhou J, et al. (2003) HIV-1 Nef intersects the macrophage CD40L signalling pathway to promote resting-cell infection. Nature 424: 213-219.
13. Mangino G, Percario Z, Fiorucci G, Vaccari G, Manrique S, et al. (2007) In vitro treatment of human monocytes/macrophages with myristoylated recombinant Nef of human immunodeficiency virus type 1 leads to the activation of mitogen-activated protein kinases, IkappaB kinases, and interferon regulatory factor 3 and to the release of beta interferon. J Virol 81: 2777-2791.
14. Olivetta E, Percario Z, Fiorucci G, Mattia G, Schiavoni I, et al. (2003) HIV-1 Nef induces the release of inflammatory factors from human monocyte/macrophages: involvement of Nef endocytotic signals and NF-kappaB activation. J Immunol 170: 1716-1727.
15. Geyer M, Fackler OT, Peterlin BM, (2001) Structure-function relationships in HIV-1 Nef. EMBO Rep 2: 580-585.
16. 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.
17. Daniel MD, Kirchhoff F, Czajak SC, Sehgal PK, Desrosiers RC, (1992) Protective effects of a live attenuated SIV vaccine with a deletion in the nef gene. Science 258: 1938-1941.
18. Deacon NJ, Tsykin A, Solomon A, Smith K, Ludford-Menting M, et al. (1995) Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 270: 988-991.
19. Kirchhoff F, Greenough TC, Brettler DB, Sullivan JL, Desrosiers RC, (1995) Brief report: absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. N Engl J Med 332: 228-232.
20. Gulizia RJ, Collman RG, Levy JA, Trono D, Mosier DE, (1997) Deletion of nef slows but does not prevent CD4-positive T-cell depletion in human immunodeficiency virus type 1-infected human-PBL-SCID mice. J Virol 71: 4161-4164.
21. Hanna Z, Kay DG, Rebai N, Guimond A, Jothy S, et al. (1998) Nef harbors a major determinant of pathogenicity for an AIDS-like disease induced by HIV-1 in transgenic mice. Cell 95: 163-175.
22. Ye H, Park YC, Kreishman M, Kieff E, Wu H, (1999) The structural basis for the recognition of diverse receptor sequences by TRAF2. Mol Cell 4: 321-330.
23. Ye H, Arron JR, Lamothe B, Cirilli M, Kobayashi T, et al. (2002) Distinct molecular mechanism for initiating TRAF6 signalling. Nature 418: 443-447.
24. Horenkamp FA, Breuer S, Schulte A, Lülf S, Weyand M, et al. (2011) Conformation of the dileucine-based sorting motif in HIV-1 Nef revealed by intermolecular domain assembly. Traffic doi:10.1111/j.1600-0854.2011.01205.x.
25. Widmer U, Manogue KR, Cerami A, Sherry B, (1993) Genomic cloning and promoter analysis of macrophage inflammatory protein (MIP)-2, MIP-1 alpha, and MIP-1 beta, members of the chemokine superfamily of proinflammatory cytokines. J Immunol 150: 4996-5012.
26. Cogswell JP, Godlevski MM, Wisely GB, Clay WC, Leesnitzer LM, et al. (1994) NF-kappa B regulates IL-1 beta transcription through a consensus NF-kappa B binding site and a nonconsensus CRE-like site. J Immunol 153: 712-723.
27. Kuprash DV, Udalova IA, Turetskaya RL, Rice NR, Nedospasov SA, (1995) Conserved kappa B element located downstream of the tumor necrosis factor alpha gene: distinct NF-kappa B binding pattern and enhancer activity in LPS activated murine macrophages. Oncogene 6: 97-106.
28. Vanden Berghe W, De Bosscher K, Boone E, Plaisance S, Haegeman G, (1999) The nuclear factor-kappaB engages CBP/p300 and histone acetyltransferase activity for transcriptional activation of the interleukin-6 gene promoter. J Biol Chem 274: 32091-32098.
29. Burke JR, Pattoli MA, Gregor KR, Brassil PJ, MacMaster JF, et al. (2003) BMS-345541 is a highly selective inhibitor of I kappa B kinase that binds at an allosteric site of the enzyme and blocks NF-kappa B-dependent transcription in mice. J Biol Chem 278: 1450-1456.
30. Kawai T, Takeuchi O, Fujita T, Inoue J, Muhlradt PF, et al. (2001) Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J Immunol 167: 5887-5894.
31. Kawai T, Akira S, (2005) Pathogen recognition with Toll-like receptors. Curr Opin Immunol 17: 338-344.
32. Matsukura S, Kokubu F, Kurokawa M, Kawaguchi M, Ieki K, et al. (2006) Synthetic double-stranded RNA induces multiple genes related to inflammation through Toll-like receptor 3 depending on NF-kappaB and/or IRF-3 in airway epithelial cells. Clin Exp Allergy 36: 1049-1062.
33. Federico M, Percario Z, Olivetta E, Fiorucci G, Muratori C, et al. (2001) HIV-1 Nef activates STAT1 in human monocytes/macrophages through the release of soluble factors. Blood 98: 2752-2761.
34. Percario Z, Olivetta E, Fiorucci G, Mangino G, Peretti S, et al. (2003) Human immunodeficiency virus type 1 (HIV-1) Nef activates STAT3 in primary human monocyte/macrophages through the release of soluble factors: involvement of Nef domains interacting with the cell endocytotic machinery. J Leukoc Biol 74: 821-832.
35. Quaranta MG, Mattioli B, Spadaro F, Straface E, Giordani L, et al. (2003) HIV-1 Nef triggers Vav-mediated signaling pathway leading to functional and morphological differentiation of dendritic cells. FASEB J 17: 2025-2036.
36. 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.
37. Xu W, Santini PA, Sullivan JS, He B, Shan M, et al. (2009) HIV-1 evades virus-specific IgG2 and IgA responses by targeting systemic and intestinal B cells via long-range intercellular conduits. Nat Immunol 10: 1008-1017.
38. Fujii Y, Otake K, Tashiro M, Adachi A, (1996) Soluble Nef antigen of HIV-1 is cytotoxic for human CD4+ T cells. FEBS Lett 393: 93-96.
39. Pantaleo G, Graziosi C, Butini L, Pizzo PA, Schnittman SM, et al. (1991) Lymphoid organs function as major reservoirs for human immunodeficiency virus. Proc Natl Acad Sci USA 88: 9838-9842.
40. Blagoveshchenskaya AD, Thomas L, Feliciangeli SF, Hung CH, Thomas G, (2002) HIV-1 Nef downregulates MHC-I by a PACS-1- and PI3K-regulated ARF6 endocytic pathway. Cell 111: 853-866.
41. Shugars DC, Smith MS, Glueck DH, Nantermet PV, Seillier-Moiseiwitsch F, et al. (1993) Analysis of human immunodeficiency virus type 1 nef gene sequences present in vivo. J Virol 67: 4639-4650.
42. Kirchhoff F, Easterbrook PJ, Douglas N, Troop M, Greenough TC, et al. (1999) Sequence variations in human immunodeficiency virus type 1 Nef are associated with different stages of disease. J Virol 73: 5497-5508.
43. Baugh LL, Garcia JV, Foster JL, (2008) Functional characterization of the human immunodeficiency virus type 1 Nef acidic domain. J Virol 82: 9657-9667.
44. Kashiwada M, Shirakata Y, Inoue JI, Nakano H, Okazaki K, et al. (1998) Tumor necrosis factor receptor-associated factor 6 (TRAF6) stimulates extracellular signal-regulated kinase (ERK) activity in CD40 signaling along a ras-independent pathway. J Exp Med 187: 237-244.
45. Lee HH, Dempsey PW, Parks TP, Zhu X, Baltimore D, et al. (1999) Specificities of CD40 signaling: involvement of TRAF2 in CD40-induced NF-kappaB activation and intercellular adhesion molecule-1 up-regulation. Proc Natl Acad Sci USA 96: 1421-1426.
46. Lomaga MA, Yeh WC, Sarosi I, Duncan GS, Furlonger C, et al. (1999) TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev 13: 1015-1024.
47. Li H, Nord EP, (2002) CD40 ligation stimulates MCP-1 and IL-8 production, TRAF6 recruitment, and MAPK activation in proximal tubule cells. Am J Physiol Renal Physiol 282: F1020-1033.
48. Nguyen LT, Duncan GS, Mirtsos C, Ng M, Speiser DE, et al. (1999) TRAF2 deficiency results in hyperactivity of certain TNFR1 signals and impairment of CD40-mediated responses. Immunity 11: 379-389.
49. Devin A, Lin Y, Yamaoka S, Li Z, Karin M, et al. (2001) The alpha and beta subunits of IkappaB kinase (IKK) mediate TRAF2-dependent IKK recruitment to tumor necrosis factor (TNF) receptor 1 in response to TNF. Mol Cell Biol 21: 3986-3994.
50. Arold S, Hoh F, Domergue S, Birck C, Delsuc MA, et al. (2000) Characterization and molecular basis of the oligomeric structure of HIV-1 nef protein. Protein Sci 9: 1137-1148.
51. Ishida T, Mizushima S, Azuma S, Kobayashi N, Tojo T, et al. (1996) Identification of TRAF6, a novel tumor necrosis factor receptor-associated factor protein that mediates signaling from an amino-terminal domain of the CD40 cytoplasmic region. J Biol Chem 271: 28745-28748.
52. Muroi M, Tanamoto K, (2008) TRAF6 distinctively mediates MyD88- and IRAK-1-induced activation of NF-kappaB. J Leukoc Biol 83: 702-707.
53. Dong W, Liu Y, Peng J, Chen L, Zou T, et al. (2006) The IRAK-1-BCL10-MALT1-TRAF6-TAK1 cascade mediates signaling to NF-kappaB from Toll-like receptor 4. J Biol Chem 281: 26029-26040.
54. Sandberg M, Hammerschmidt W, Sugden B, (1997) Characterization of LMP-1's association with TRAF1, TRAF2, and TRAF3. J Virol 71: 4649-4656.
55. Brinkmann M, Glenn M, Rainbow L, Kieser A, Henke-Gendo C, et al. (2003) Activation of mitogen-activated protein kinase and NF-kappaB pathways by a Kaposi's sarcoma-associated herpesvirus K15 membrane protein. J Virol 77: 9346-9358.
56. Garcia M, Kaserman J, Chung Y, Jung J, Lee S, (2007) Herpesvirus saimiri STP-A oncoprotein utilizes Src family protein tyrosine kinase and tumor necrosis factor receptor-associated factors to elicit cellular signal transduction. J Virol 81: 2663-2674.
57. Park K, Choi S, Choi D, Park J, Yie S, et al. (2003) Hepatitis C virus NS5A protein modulates c-Jun N-terminal kinase through interaction with tumor necrosis factor receptor-associated factor 2. J Biol Chem 278: 30711-30718.
58. Tsuchiya S, Yamabe M, Yamaguchi Y, Kobayashi Y, Konno T, et al. (1980) Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int J Cancer 26: 171-176.
59. Giard DJ, Aaronson SA, Todaro GJ, Arnstein P, Kersey JH, et al. (1973) In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J Natl Cancer Inst 51: 1417-1423.
60. Breuer S, Gerlach H, Kolaric B, Urbanke C, Opitz N, et al. (2006) Biochemical Indication for Myristoylation-Dependent Conformational Changes in HIV-1 Nef. Biochemistry 45: 2339-2349.
61. Sessa F, Mapelli M, Ciferri C, Tarricone C, Areces L, et al. (2005) Mechanism of Aurora B activation by INCENP and inhibition by hesperadin. Mol Cell 18: 379-391.
62. Oudijk E, Nijhuis E, Zwank M, van de Graaf E, Mager H, et al. (2005) Systemic inflammation in COPD visualised by gene profiling in peripheral blood neutrophils. Thorax 60: 538-544.
63. Keller C, Keller P, Marshal S, Pedersen B, (2003) IL-6 gene expression in human adipose tissue in response to exercise-effect of carbohydrate ingestion. J Physiol 550: 927-931.
64. Brink N, Szamel M, Young A, Wittern K, Bergemann J, (2000) Comparative quantification of IL-1beta, IL-10, IL-10r, TNFalpha and IL-7 mRNA levels in UV-irradiated human skin in vivo. Inflamm Res 49: 290-296.