The HIV-1 Vpu protein induces apoptosis in drosophila via activation of JNK signaling

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Marchal, Christelle ^a,d   Vinatier, Gérald ^a   Sanial, Matthieu ^b   Plessis, Anne ^b   Pret, Anne Marie ^a,c   Limbourg Bouchon, Bernadette ^a   Théodore, Laurent ^a,d   Netter, Sophie ^a,c  

^a LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

^b INSTITUT JACQUES MONOD   (France)

^c CNRS   (France)

^d UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TRANSDUCINE REPEAT CONTAINING PROTEIN; CASPASE; DRONC CASPASE; F BOX PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN 1; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; VPU PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; VIRUS PROTEIN; VPU PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; EXPERIMENTAL MODEL; EYE DEVELOPMENT; FORELIMB; GENE; GENETIC SCREENING; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VIVO STUDY; INTRACELLULAR SIGNALING; LIMB DEVELOPMENT; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REAPER GENE; UPREGULATION; VIRUS CELL INTERACTION; WING DEVELOPMENT; ANIMAL; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; METABOLISM; PHENOTYPE; SIGNAL TRANSDUCTION; TRANSGENE; TRANSGENIC ANIMAL;

HUMAN IMMUNODEFICIENCY VIRUS 1; INTRACISTERNAL A-PARTICLES; MAMMALIA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; CASPASES; DROSOPHILA MELANOGASTER; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, VIRAL; HIV-1; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; MAP KINASE KINASE 4; PHENOTYPE; SIGNAL TRANSDUCTION; TRANSGENES; VIRAL REGULATORY AND ACCESSORY PROTEINS; WING;

EID: 84859031319     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034310     Document Type: Article

References (92)

1. Grossman Z, Meier-Schellersheim M, Paul WE, Picker LJ, (2006) Pathogenesis of HIV infection: what the virus spares is as important as what it destroys. Nature medicine 12: 289-295.
2. Bour S, Strebel K, (2003) The HIV-1 Vpu protein: a multifunctional enhancer of viral particle release. Microbes and infection/Institut Pasteur 5: 1029-1039.
3. Willey RL, Maldarelli F, Martin MA, Strebel K, (1992) Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4. Journal of virology 66: 7193-7200.
4. Schubert U, Anton LC, Bacik I, Cox JH, Bour S, et al. (1998) CD4 glycoprotein degradation induced by human immunodeficiency virus type 1 Vpu protein requires the function of proteasomes and the ubiquitin-conjugating pathway. Journal of virology 72: 2280-2288.
5. Nomaguchi M, Fujita M, Adachi A, (2008) Role of HIV-1 Vpu protein for virus spread and pathogenesis. Microbes and infection/Institut Pasteur 10: 960-967.
6. Magadan JG, Bonifacino JS, (2012) Transmembrane Domain Determinants of CD4 Downregulation by HIV-1 Vpu. Journal of virology 86: 757-772.
7. Meusser B, Sommer T, (2004) Vpu-mediated degradation of CD4 reconstituted in yeast reveals mechanistic differences to cellular ER-associated protein degradation. Molecular cell 14: 247-258.
8. Binette J, Dube M, Mercier J, Halawani D, Latterich M, et al. (2007) Requirements for the selective degradation of CD4 receptor molecules by the human immunodeficiency virus type 1 Vpu protein in the endoplasmic reticulum. Retrovirology 4: 75.
9. Magadan JG, Perez-Victoria FJ, Sougrat R, Ye Y, Strebel K, et al. (2010) Multilayered mechanism of CD4 downregulation by HIV-1 Vpu involving distinct ER retention and ERAD targeting steps. PLoS pathogens 6: e1000869.
10. Margottin F, Bour SP, Durand H, Selig L, Benichou S, et al. (1998) A novel human WD protein, h-beta TrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Molecular cell 1: 565-574.
11. Estrabaud E, Le Rouzic E, Lopez-Verges S, Morel M, Belaidouni N, et al. (2007) Regulated degradation of the HIV-1 Vpu protein through a betaTrCP-independent pathway limits the release of viral particles. PLoS pathogens 3: e104.
12. Douglas JL, Viswanathan K, McCarroll MN, Gustin JK, Fruh K, et al. (2009) Vpu directs the degradation of the human immunodeficiency virus restriction factor BST-2/Tetherin via a beta-TrCP-dependent mechanism. Journal of virology 83: 7931-7947.
13. Mitchell RS, Katsura C, Skasko MA, Fitzpatrick K, Lau D, et al. (2009) Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking. PLoS pathogens 5: e1000450.
14. Dube M, Roy BB, Guiot-Guillain P, Binette J, Mercier J, et al. (2010) Antagonism of tetherin restriction of HIV-1 release by Vpu involves binding and sequestration of the restriction factor in a perinuclear compartment. PLoS pathogens 6: e1000856.
15. Neil SJ, Zang T, Bieniasz PD, (2008) Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451: 425-430.
16. Van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R, et al. (2008) The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell host & microbe 3: 245-252.
17. Dube M, Bego MG, Paquay C, Cohen EA, (2010) Modulation of HIV-1-host interaction: role of the Vpu accessory protein. Retrovirology 7: 114.
18. Tervo HM, Homann S, Ambiel I, Fritz JV, Fackler OT, et al. (2011) beta-TrCP is dispensable for Vpu's ability to overcome the CD317/Tetherin-imposed restriction to HIV-1 release. Retrovirology 8: 9.
19. Hsu K, Seharaseyon J, Dong P, Bour S, Marban E, (2004) Mutual functional destruction of HIV-1 Vpu and host TASK-1 channel. Molecular cell 14: 259-267.
20. Akari H, Bour S, Kao S, Adachi A, Strebel K, (2001) The human immunodeficiency virus type 1 accessory protein Vpu induces apoptosis by suppressing the nuclear factor kappaB-dependent expression of antiapoptotic factors. The Journal of experimental medicine 194: 1299-1311.
21. Bour S, Perrin C, Akari H, Strebel K, (2001) The human immunodeficiency virus type 1 Vpu protein inhibits NF-kappa B activation by interfering with beta TrCP-mediated degradation of Ikappa B. The Journal of biological chemistry 276: 15920-15928.
22. Besnard-Guerin C, Belaidouni N, Lassot I, Segeral E, Jobart A, et al. (2004) HIV-1 Vpu sequesters beta-transducin repeat-containing protein (betaTrCP) in the cytoplasm and provokes the accumulation of beta-catenin and other SCFbetaTrCP substrates. The Journal of biological chemistry 279: 788-795.
23. Verma S, Ali A, Arora S, Banerjea AC, (2011) Inhibition of beta-TrcP-dependent ubiquitination of p53 by HIV-1 Vpu promotes p53-mediated apoptosis in human T cells. Blood 117: 6600-6607.
24. Casella CR, Rapaport EL, Finkel TH, (1999) Vpu increases susceptibility of human immunodeficiency virus type 1-infected cells to fas killing. Journal of virology 73: 92-100.
25. Adamson AL, Wright N, LaJeunesse DR, (2005) Modeling early Epstein-Barr virus infection in Drosophila melanogaster: the BZLF1 protein. Genetics 171: 1125-1135.
26. Steinberg R, Shemer-Avni Y, Adler N, Neuman-Silberberg S, (2008) Human cytomegalovirus immediate-early-gene expression disrupts embryogenesis in transgenic Drosophila. Transgenic research 17: 105-119.
27. Kotadia S, Kao LR, Comerford SA, Jones RT, Hammer RE, et al. (2008) PP2A-dependent disruption of centrosome replication and cytoskeleton organization in Drosophila by SV40 small tumor antigen. Oncogene 27: 6334-6346.
28. Battaglia PA, Zito S, Macchini A, Gigliani F, (2001) A Drosophila model of HIV-Tat-related pathogenicity. Journal of cell science 114: 2787-2794.
29. Ponti D, Troiano M, Bellenchi GC, Battaglia PA, Gigliani F, (2008) The HIV Tat protein affects processing of ribosomal RNA precursor. BMC cell biology 9: 32.
30. Lee SB, Park J, Jung JU, Chung J, (2005) Nef induces apoptosis by activating JNK signaling pathway and inhibits NF-kappaB-dependent immune responses in Drosophila. Journal of cell science 118: 1851-1859.
31. Leulier F, Marchal C, Miletich I, Limbourg-Bouchon B, Benarous R, et al. (2003) Directed expression of the HIV-1 accessory protein Vpu in Drosophila fat-body cells inhibits Toll-dependent immune responses. EMBO reports 4: 976-981.
32. Brand AH, Perrimon N, (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
33. Miletich I, Limbourg-Bouchon B, (2000) Drosophila null slimb clones transiently deregulate Hedgehog-independent transcription of wingless in all limb discs, and induce decapentaplegic transcription linked to imaginal disc regeneration. Mechanisms of development 93: 15-26.
34. Jiang J, Struhl G, (1998) Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature 391: 493-496.
35. Theodosiou NA, Zhang S, Wang WY, Xu T, (1998) slimb coordinates wg and dpp expression in the dorsal-ventral and anterior-posterior axes during limb development. Development 125: 3411-3416.
36. Rorth P, (1996) A modular misexpression screen in Drosophila detecting tissue-specific phenotypes. Proceedings of the National Academy of Sciences of the United States of America 93: 12418-12422.
37. Schubert U, Bour S, Ferrer-Montiel AV, Montal M, Maldarell F, et al. (1996) The two biological activities of human immunodeficiency virus type 1 Vpu protein involve two separable structural domains. Journal of virology 70: 809-819.
38. Holley CL, Olson MR, Colon-Ramos DA, Kornbluth S, (2002) Reaper eliminates IAP proteins through stimulated IAP degradation and generalized translational inhibition. Nature cell biology 4: 439-444.
39. Ryoo HD, Bergmann A, Gonen H, Ciechanover A, Steller H, (2002) Regulation of Drosophila IAP1 degradation and apoptosis by reaper and ubcD1. Nature cell biology 4: 432-438.
40. Yoo SJ, Huh JR, Muro I, Yu H, Wang L, et al. (2002) Hid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms. Nature cell biology 4: 416-424.
41. Goyal L, McCall K, Agapite J, Hartwieg E, Steller H, (2000) Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. The EMBO journal 19: 589-597.
42. Yan N, Wu JW, Chai J, Li W, Shi Y, (2004) Molecular mechanisms of DrICE inhibition by DIAP1 and removal of inhibition by Reaper, Hid and Grim. Nature structural & molecular biology 11: 420-428.
43. Xu D, Woodfield SE, Lee TV, Fan Y, Antonio C, et al. (2009) Genetic control of programmed cell death (apoptosis) in Drosophila. Fly 3: 78-90.
44. Martin FA, Perez-Garijo A, Morata G, (2009) Apoptosis in Drosophila: compensatory proliferation and undead cells. The International journal of developmental biology 53: 1341-1347.
45. Huh JR, Guo M, Hay BA, (2004) Compensatory proliferation induced by cell death in the Drosophila wing disc requires activity of the apical cell death caspase Dronc in a nonapoptotic role. Current biology: CB 14: 1262-1266.
46. Perez-Garijo A, Martin FA, Morata G, (2004) Caspase inhibition during apoptosis causes abnormal signalling and developmental aberrations in Drosophila. Development 131: 5591-5598.
47. Ryoo HD, Gorenc T, Steller H, (2004) Apoptotic cells can induce compensatory cell proliferation through the JNK and the Wingless signaling pathways. Developmental cell 7: 491-501.
48. Perez-Garijo A, Shlevkov E, Morata G, (2009) The role of Dpp and Wg in compensatory proliferation and in the formation of hyperplastic overgrowths caused by apoptotic cells in the Drosophila wing disc. Development 136: 1169-1177.
49. Adachi-Yamada T, Fujimura-Kamada K, Nishida Y, Matsumoto K, (1999) Distortion of proximodistal information causes JNK-dependent apoptosis in Drosophila wing. Nature 400: 166-169.
50. Moreno E, Basler K, Morata G, (2002) Cells compete for decapentaplegic survival factor to prevent apoptosis in Drosophila wing development. Nature 416: 755-759.
51. Lee JH, Koh H, Kim M, Park J, Lee SY, et al. (2006) JNK pathway mediates apoptotic cell death induced by tumor suppressor LKB1 in Drosophila. Cell death and differentiation 13: 1110-1122.
52. Neisch AL, Speck O, Stronach B, Fehon RG, (2010) Rho1 regulates apoptosis via activation of the JNK signaling pathway at the plasma membrane. The Journal of cell biology 189: 311-323.
53. McEwen DG, Peifer M, (2005) Puckered, a Drosophila MAPK phosphatase, ensures cell viability by antagonizing JNK-induced apoptosis. Development 132: 3935-3946.
54. Kuranaga E, Kanuka H, Igaki T, Sawamoto K, Ichijo H, et al. (2002) Reaper-mediated inhibition of DIAP1-induced DTRAF1 degradation results in activation of JNK in Drosophila. Nature cell biology 4: 705-710.
55. Martin-Blanco E, Gampel A, Ring J, Virdee K, Kirov N, et al. (1998) puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes & development 12: 557-570.
56. Sluss HK, Han Z, Barrett T, Goberdhan DC, Wilson C, et al. (1996) A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes & development 10: 2745-2758.
57. Takatsu Y, Nakamura M, Stapleton M, Danos MC, Matsumoto K, et al. (2000) TAK1 participates in c-Jun N-terminal kinase signaling during Drosophila development. Molecular and cellular biology 20: 3015-3026.
58. Stronach B, Perrimon N, (2002) Activation of the JNK pathway during dorsal closure in Drosophila requires the mixed lineage kinase, slipper. Genes & development 16: 377-387.
59. Sathyanarayana P, Barthwal MK, Lane ME, Acevedo SF, Skoulakis EM, et al. (2003) Drosophila mixed lineage kinase/slipper, a missing biochemical link in Drosophila JNK signaling. Biochimica et biophysica acta 1640: 77-84.
60. Igaki T, (2009) Correcting developmental errors by apoptosis: lessons from Drosophila JNK signaling. Apoptosis: an international journal on programmed cell death 14: 1021-1028.
61. Su YC, Treisman JE, Skolnik EY, (1998) The Drosophila Ste20-related kinase misshapen is required for embryonic dorsal closure and acts through a JNK MAPK module on an evolutionarily conserved signaling pathway. Genes & development 12: 2371-2380.
62. Cha GH, Cho KS, Lee JH, Kim M, Kim E, et al. (2003) Discrete functions of TRAF1 and TRAF2 in Drosophila melanogaster mediated by c-Jun N-terminal kinase and NF-kappaB-dependent signaling pathways. Molecular and cellular biology 23: 7982-7991.
63. Agnes F, Suzanne M, Noselli S, (1999) The Drosophila JNK pathway controls the morphogenesis of imaginal discs during metamorphosis. Development 126: 5453-5462.
64. Igaki T, Kanda H, Yamamoto-Goto Y, Kanuka H, Kuranaga E, et al. (2002) Eiger, a TNF superfamily ligand that triggers the Drosophila JNK pathway. The EMBO journal 21: 3009-3018.
65. Moreno E, Yan M, Basler K, (2002) Evolution of TNF signaling mechanisms: JNK-dependent apoptosis triggered by Eiger, the Drosophila homolog of the TNF superfamily. Current biology: CB 12: 1263-1268.
66. Kanda H, Igaki T, Kanuka H, Yagi T, Miura M, (2002) Wengen, a member of the Drosophila tumor necrosis factor receptor superfamily, is required for Eiger signaling. The Journal of biological chemistry 277: 28372-28375.
67. Kauppila S, Maaty WS, Chen P, Tomar RS, Eby MT, et al. (2003) Eiger and its receptor, Wengen, comprise a TNF-like system in Drosophila. Oncogene 22: 4860-4867.
68. Spiegelman VS, Stavropoulos P, Latres E, Pagano M, Ronai Z, et al. (2001) Induction of beta-transducin repeat-containing protein by JNK signaling and its role in the activation of NF-kappaB. The Journal of biological chemistry 276: 27152-27158.
69. Murphy TD, (2003) Drosophila skpA, a component of SCF ubiquitin ligases, regulates centrosome duplication independently of cyclin E accumulation. Journal of cell science 116: 2321-2332.
70. Morata G, Shlevkov E, Perez-Garijo A, (2011) Mitogenic signaling from apoptotic cells in Drosophila. Development, growth & differentiation 53: 168-176.
71. Xue L, Igaki T, Kuranaga E, Kanda H, Miura M, et al. (2007) Tumor suppressor CYLD regulates JNK-induced cell death in Drosophila. Developmental cell 13: 446-454.
72. Han ZS, Enslen H, Hu X, Meng X, Wu IH, et al. (1998) A conserved p38 mitogen-activated protein kinase pathway regulates Drosophila immunity gene expression. Molecular and cellular biology 18: 3527-3539.
73. Fleming Y, Armstrong CG, Morrice N, Paterson A, Goedert M, et al. (2000) Synergistic activation of stress-activated protein kinase 1/c-Jun N-terminal kinase (SAPK1/JNK) isoforms by mitogen-activated protein kinase kinase 4 (MKK4) and MKK7. The Biochemical journal 352 Pt 1: 145-154.
74. Geuking P, Narasimamurthy R, Lemaitre B, Basler K, Leulier F, (2009) A non-redundant role for Drosophila Mkk4 and hemipterous/Mkk7 in TAK1-mediated activation of JNK. PloS one 4: e7709.
75. Bergantinos C, Corominas M, Serras F, (2010) Cell death-induced regeneration in wing imaginal discs requires JNK signalling. Development 137: 1169-1179.
76. Singh J, Aaronson SA, Mlodzik M, (2010) Drosophila Abelson kinase mediates cell invasion and proliferation through two distinct MAPK pathways. Oncogene 29: 4033-4045.
77. Vidal M, Larson DE, Cagan RL, (2006) Csk-deficient boundary cells are eliminated from normal Drosophila epithelia by exclusion, migration, and apoptosis. Developmental cell 10: 33-44.
78. Wang X, Viswanath R, Zhao J, Tang S, Hewlett I, (2010) Changes in the level of apoptosis-related proteins in Jurkat cells infected with HIV-1 versus HIV-2. Molecular and cellular biochemistry 337: 175-183.
79. Blackman RK, Sanicola M, Raftery LA, Gillevet T, Gelbart WM, (1991) An extensive 3′ cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-beta family in Drosophila. Development 111: 657-666.
80. Staehling-Hampton K, Jackson PD, Clark MJ, Brand AH, Hoffmann FM, (1994) Specificity of bone morphogenetic protein-related factors: cell fate and gene expression changes in Drosophila embryos induced by decapentaplegic but not 60A. Cell growth & differentiation: the molecular biology journal of the American Association for Cancer Research 5: 585-593.
81. Nordstrom W, Chen P, Steller H, Abrams JM, (1996) Activation of the reaper gene during ectopic cell killing in Drosophila. Developmental biology 180: 213-226.
82. Netter S, Faucheux M, Theodore L, (2001) Developmental dynamics of a polyhomeotic-EGFP fusion in vivo. DNA and cell biology 20: 483-492.
83. Leulier F, Ribeiro PS, Palmer E, Tenev T, Takahashi K, et al. (2006) Systematic in vivo RNAi analysis of putative components of the Drosophila cell death machinery. Cell death and differentiation 13: 1663-1674.
84. Xu D, Wang Y, Willecke R, Chen Z, Ding T, et al. (2006) The effector caspases drICE and dcp-1 have partially overlapping functions in the apoptotic pathway in Drosophila. Cell death and differentiation 13: 1697-1706.
85. Xu D, Li Y, Arcaro M, Lackey M, Bergmann A, (2005) The CARD-carrying caspase Dronc is essential for most, but not all, developmental cell death in Drosophila. Development 132: 2125-2134.
86. Ishimaru S, Ueda R, Hinohara Y, Ohtani M, Hanafusa H, (2004) PVR plays a critical role via JNK activation in thorax closure during Drosophila metamorphosis. The EMBO journal 23: 3984-3994.
87. Buchon N, Broderick NA, Chakrabarti S, Lemaitre B, (2009) Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes & development 23: 2333-2344.
88. Rallis A, Moore C, Ng J, (2010) Signal strength and signal duration define two distinct aspects of JNK-regulated axon stability. Developmental biology 339: 65-77.
89. Grima B, Lamouroux A, Chelot E, Papin C, Limbourg-Bouchon B, et al. (2002) The F-box protein slimb controls the levels of clock proteins period and timeless. Nature 420: 178-182.
90. Monnier V, Dussillol F, Alves G, Lamour-Isnard C, Plessis A, (1998) Suppressor of fused links fused and Cubitus interruptus on the hedgehog signalling pathway. Current biology: CB 8: 583-586.
91. Monnier V, Girardot F, Cheret C, Andres O, Tricoire H, (2002) Modulation of oxidative stress resistance in Drosophila melanogaster by gene overexpression. Genesis 34: 76-79.
92. Yang QH, Du C, (2004) Smac/DIABLO selectively reduces the levels of c-IAP1 and c-IAP2 but not that of XIAP and livin in HeLa cells. The Journal of biological chemistry 279: 16963-16970.