The presence of HIV-1 Tat protein second exon delays Fas protein-mediated apoptosis in CD4+ T lymphocytes: A potential mechanism for persistent viral production

Journal of Biological Chemistry

Volumn 288, Issue 11, 2013, Pages 7626-7644

  López Huertas, María Rosa ^a   Mateos, Elena ^a   Del Cojo, María Sánchez ^a   Gómez Esquer, Francisco ^b   Díaz Gil, Gema ^b   Rodríguez Mora, Sara ^a   López, Juan Antonio ^c   Calvo, Enrique ^c   López Campos, Guillermo ^d   Alcamí, José ^a   Coiras, Mayte ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b UNIVERSIDAD REY JUAN CARLOS   (Spain)

^c CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-APOPTOTIC PROTEIN; EXTRACELLULAR MEDIUM; MITOCHONDRIAL CYTOCHROME C; MITOCHONDRIAL MEMBRANES; PERIPHERAL BLOOD LYMPHOCYTES; POTENTIAL MECHANISM; PRO-APOPTOTIC FACTORS; VIRAL TRANSCRIPTION;

AMINO ACIDS; CELL MEMBRANES; ENZYME ACTIVITY; MITOCHONDRIA; PROTEINS; T-CELLS;

CELL DEATH;

CASPASE; CASPASE 8; CASPASE 9; CYTOCHROME C; FAS ANTIGEN; FAS LIGAND; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN TAT101; PROTEIN TAT72; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; ENZYME ACTIVATION; EXON; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOREACTIVITY; INTRACELLULAR SIGNALING; LEUKEMIA CELL LINE; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; TRANSCRIPTION ELONGATION; VIRUS GENOME; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ANTIGENS, CD95; APOPTOSIS; CASPASE 3; CASPASE 8; CASPASE 9; CD4-POSITIVE T-LYMPHOCYTES; CYTOCHROMES C; EXONS; GENE EXPRESSION REGULATION; HIV-1; HUMANS; JURKAT CELLS; MITOCHONDRIA; MUTAGENESIS, SITE-DIRECTED; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEOME; PROTEOMICS; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TRANSFECTION;

EID: 84875123749     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.408294     Document Type: Article

References (113)

1. Piatak, M., Jr., Saag, M. S., Yang, L. C., Clark, S. J., Kappes, J. C., Luk, K. C., Hahn, B. H., Shaw, G. M., and Lifson, J. D. (1993) High levels of HIV-1 in plasma during all stages of infection determined by competitive PCR. Science 259, 1749-1754
2. Lelièvre, J. D., Mammano, F., Arnoult, D., Petit, F., Grodet, A., Estaquier, J., and Ameisen, J. C. (2004) A novel mechanism for HIV1-mediated bystander CD4+ T-cell death: neighboring dying cells drive the capacity of HIV1 to kill noncycling primary CD4+ T cells. Cell Death Differ. 11, 1017-1027
3. Gougeon, M. L. (2005) To kill or be killed: how HIV exhausts the immune system. Cell Death Differ. 12, 845-854
4. Varbanov, M., Espert, L., and Biard-Piechaczyk, M. (2006) Mechanisms of CD4 T-cell depletion triggered by HIV-1 viral proteins. AIDS Rev. 8, 221-236
5. Lum, J. J., Cohen, O. J., Nie, Z., Weaver, J. G., Gomez, T. S., Yao, X. J., Lynch, D., Pilon, A. A., Hawley, N., Kim, J. E., Chen, Z., Montpetit, M., Sanchez-Dardon, J., Cohen, E. A., and Badley, A. D. (2003) Vpr R77Q is associated with long-term nonprogressive HIV infection and impaired induction of apoptosis. J. Clin. Invest. 111, 1547-1554
6. Jacotot, E., Ravagnan, L., Loeffler, M., Ferri, K. F., Vieira, H. L., Zamzami, N., Costantini, P., Druillennec, S., Hoebeke, J., Briand, J. P., Irinopoulou, T., Daugas, E., Susin, S. A., Cointe, D., Xie, Z. H., Reed, J. C., Roques, B. P., and Kroemer, G. (2000) The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore. J. Exp. Med. 191, 33-46
7. Brenner, C., and Kroemer, G. (2003) The mitochondriotoxic domain of Vpr determines HIV-1 virulence. J. Clin. Invest. 111, 1455-1457
8. Deniaud, A., Brenner, C., and Kroemer, G. (2004) Mitochondrial membrane permeabilization by HIV-1 Vpr. Mitochondrion 4, 223-233
9. Conti, L., Rainaldi, G., Matarrese, P., Varano, B., Rivabene, R., Columba, S., Sato, A., Belardelli, F., Malorni, W., and Gessani, S. (1998) The HIV-1 Vpr protein acts as a negative regulator of apoptosis in a human lymphoblastoid T cell line: possible implications for the pathogenesis of AIDS. J. Exp. Med. 187, 403-413
10. Moon, H. S., and Yang, J. S. (2006) Role of HIV Vpr as a regulator of apoptosis and an effector on bystander cells. Mol. Cells 21, 7-20
11. Finkel, T. H., Tudor-Williams, G., Banda, N. K., Cotton, M. F., Curiel, T., Monks, C., Baba, T. W., Ruprecht, R. M., and Kupfer, A. (1995) Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat. Med. 1, 129-134
12. Nardelli, B., Gonzalez, C. J., Schechter, M., and Valentine, F. T. (1995) CD4+ blood lymphocytes are rapidly killed in vitro by contact with autologous human immunodeficiency virus-infected cells. Proc. Natl. Acad. Sci. U.S.A. 92, 7312-7316
13. Aillet, F., Masutani, H., Elbim, C., Raoul, H., Chêne, L., Nugeyre, M. T., Paya, C., Barré-Sinoussi, F., Gougerot-Pocidalo, M. A., and Israël, N. (1998) Human immunodeficiency virus induces a dual regulation of Bcl-2, resulting in persistent infection of CD4+ T- or monocytic cell lines. J. Virol. 72, 9698-9705
14. Zhang, M., Li, X., Pang, X., Ding, L., Wood, O., Clouse, K., Hewlett, I., and Dayton, A. I. (2001) Identification of a potential HIV-induced source of bystander-mediated apoptosis in T cells: up-regulation of trail in primary human macrophages by HIV-1 tat. J. Biomed. Sci. 8, 290-296
15. McCloskey, T. W., Ott, M., Tribble, E., Khan, S. A., Teichberg, S., Paul, M. O., Pahwa, S., Verdin, E., and Chirmule, N. (1997) Dual role of HIV Tat in regulation of apoptosis in T cells. J. Immunol. 158, 1014-1019
16. Bannwarth, S., and Gatignol, A. (2005) HIV-1 TAR RNA: the target of molecular interactions between the virus and its host. Curr. HIV Res. 3, 61-71
17. Berkhout, B., and Jeang, K. T. (1989) Trans activation of human immunodeficiency virus type 1 is sequence-specific for both the singlestranded bulge and loop of the trans-acting-responsive hairpin: a quantitative analysis. J. Virol. 63, 5501-5504
18. Gatignol, A., and Jeang, K. T. (2000) Tat as a transcriptional activator and a potential therapeutic target for HIV-1. Adv. Pharmacol. 48, 209-227
19. Pugliese, A., Vidotto, V., Beltramo, T., Petrini, S., and Torre, D. (2005) A review of HIV-1 Tat protein biological effects. Cell Biochem. Funct. 23, 223-227
20. Carroll, R., Martarano, L., and Derse, D. (1991) Identification of lentivirus tat functional domains through generation of equine infectious anemia virus/human immunodeficiency virus type 1 tat gene chimeras. J. Virol. 65, 3460-3467
21. Westendorp, M. O., Shatrov, V. A., Schulze-Osthoff, K., Frank, R., Kraft, M., Los, M., Krammer, P. H., Dröge, W., and Lehmann, V. (1995) HIV-1 Tat potentiates TNF-induced NF-κB activation and cytotoxicity by altering the cellular redox state. EMBO J. 14, 546-554
22. Xiao, H., Neuveut, C., Benkirane, M., and Jeang, K. T. (1998) Interaction of the second coding exon of Tat with human EF-1δ delineates a mechanism for HIV-1-mediated shut-off of host mRNA translation. Biochem. Biophys. Res. Commun. 244, 384-389
23. Lopez-Huertas, M. R., Callejas, S., Abia, D., Mateos, E., Dopazo, A., Alcami, J., and Coiras, M. (2010) Modifications in host cell cytoskeleton structure and function mediated by intracellular HIV-1 Tat protein are greatly dependent on the second coding exon. Nucleic Acids Res. 38, 3287-3307
24. Yedavalli, V. S., Benkirane, M., and Jeang, K. T. (2003) Tat and transactivation-responsive (TAR) RNA-independent induction of HIV-1 long terminal repeat by human and murine cyclin T1 requires Sp1. J. Biol. Chem. 278, 6404-6410
25. Dandekar, D. H., Ganesh, K. N., and Mitra, D. (2004) HIV-1 Tat directly binds to NFκB enhancer sequence: role in viral and cellular gene expression. Nucleic Acids Res. 32, 1270-1278
26. Yang, L., Morris, G. F., Lockyer, J. M., Lu, M., Wang, Z., and Morris, C. B. (1997) Distinct transcriptional pathways of TAR-dependent and TARindependent human immunodeficiency virus type-1 transactivation by Tat. Virology 235, 48-64
27. Ott, M., Emiliani, S., Van Lint, C., Herbein, G., Lovett, J., Chirmule, N., McCloskey, T., Pahwa, S., and Verdin, E. (1997) Immune hyperactivation of HIV-1-infected T cells mediated by Tat and the CD28 pathway. Science 275, 1481-1485
28. Coiras, M., Camafeita, E., Ureña, T., López, J. A., Caballero, F., Fernández, B., López-Huertas, M. R., Pérez-Olmeda, M., and Alcamí, J. (2006) Modifications in the human T cell proteome induced by intracellular HIV-1 Tat protein expression. Proteomics 6, S63-S73
29. Pincus, S. H., Messer, K. G., Nara, P. L., Blattner, W. A., Colclough, G., and Reitz, M. (1994) Temporal analysis of the antibody response to HIV envelope protein in HIV-infected laboratory workers. J. Clin. Invest. 93, 2505-2513
30. Smith, S. M., Pentlicky, S., Klase, Z., Singh, M., Neuveut, C., Lu, C. Y., Reitz, M. S., Jr., Yarchoan, R., Marx, P. A., and Jeang, K. T. (2003) An in vivo replication-important function in the second coding exon of Tat is constrained against mutation despite cytotoxic T lymphocyte selection. J. Biol. Chem. 278, 44816-44825
31. Borgatti, P., Zauli, G., Colamussi, M. L., Gibellini, D., Previati, M., Cantley, L. L., and Capitani, S. (1997) Extracellular HIV-1 Tat protein activates phosphatidylinositol 3- and Akt/PKB kinases in CD4+ T lymphoblastoid Jurkat cells. Eur. J. Immunol. 27, 2805-2811
32. Jones, M., Olafson, K., Del Bigio, M. R., Peeling, J., and Nath, A. (1998) Intraventricular injection of human immunodeficiency virus type 1 (HIV-1) Tat protein causes inflammation, gliosis, apoptosis, and ventricular enlargement. J. Neuropathol. Exp. Neurol. 57, 563-570
33. Gibellini, D., Re, M. C., Ponti, C., Vitone, F., Bon, I., Fabbri, G., Grazia Di Iasio, M., and Zauli, G. (2005) HIV-1 Tat protein concomitantly downregulates apical caspase-10 and up-regulates c-FLIP in lymphoid T cells: a potential molecular mechanism to escape TRAIL cytotoxicity. J. Cell Physiol. 203, 547-556
34. Golstein, P. (1998) Cell death in us and others. Science 281, 1283
35. Takahashi, T., Tanaka, M., Brannan, C. I., Jenkins, N. A., Copeland, N. G., Suda, T., and Nagata, S. (1994) Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 76, 969-976
36. Alimonti, J. B., Ball, T. B., and Fowke, K. R. (2003) Mechanisms of CD4+ T lymphocyte cell death in human immunodeficiency virus infection and AIDS. J. Gen. Virol. 84, 1649-1661
37. Barnhart, B. C., Alappat, E. C., and Peter, M. E. (2003) The CD95 type I/type II model. Semin. Immunol. 15, 185-193
38. Donepudi, M., Mac Sweeney, A., Briand, C., and Grütter, M. G. (2003) Insights into the regulatory mechanism for caspase-8 activation. Mol. Cell 11, 543-549
39. Yu, J. W., and Shi, Y. (2008) FLIP and the death effector domain family. Oncogene 27, 6216-6227
40. Adams, J. M. (2003) Ways of dying: multiple pathways to apoptosis. Genes Dev. 17, 2481-2495
41. Uren, R. T., Dewson, G., Bonzon, C., Lithgow, T., Newmeyer, D. D., and Kluck, R. M. (2005) Mitochondrial release of pro-apoptotic proteins: electrostatic interactions can hold cytochrome c but not Smac/DIABLO to mitochondrial membranes. J. Biol. Chem. 280, 2266-2274
42. Ola, M. S., Nawaz, M., and Ahsan, H. (2011) Role of Bcl-2 family proteins and caspases in the regulation of apoptosis. Mol. Cell. Biochem. 351, 41-58
43. Li, H., Zhu, H., Xu, C. J., and Yuan, J. (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501
44. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., and Wang, X. (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94, 481-490
45. Scaffidi, C., Fulda, S., Srinivasan, A., Friesen, C., Li, F., Tomaselli, K. J., Debatin, K. M., Krammer, P. H., and Peter, M. E. (1998) Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17, 1675-1687
46. Kim, H. E., Du, F., Fang, M., and Wang, X. (2005) Formation of apoptosome is initiated by cytochrome c-induced dATP hydrolysis and subsequent nucleotide exchange on Apaf-1. Proc. Natl. Acad. Sci. U.S.A. 102, 17545-17550
47. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S., and Wang, X. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479-489
48. Riedl, S. J., and Salvesen, G. S. (2007) The apoptosome: signaling platform of cell death. Nat. Rev. Mol. Cell Biol. 8, 405-413
49. Karin, M., and Lin, A. (2002) NF-κB at the crossroads of life and death. Nat. Immunol. 3, 221-227
50. Safa, A. R., Day, T. W., and Wu, C. H. (2008) Cellular FLICE-like inhibitory protein (C-FLIP): a novel target for cancer therapy. Curr. Cancer Drug Targets 8, 37-46
51. Krueger, A., Schmitz, I., Baumann, S., Krammer, P. H., and Kirchhoff, S. (2001) Cellular FLICE-inhibitory protein splice variants inhibit different steps of caspase-8 activation at the CD95 death-inducing signaling complex. J. Biol. Chem. 276, 20633-20640
52. Golks, A., Brenner, D., Fritsch, C., Krammer, P. H., and Lavrik, I. N. (2005) c-FLIPR, a new regulator of death receptor-induced apoptosis. J. Biol. Chem. 280, 14507-14513
53. Irmler, M., Thome, M., Hahne, M., Schneider, P., Hofmann, K., Steiner, V., Bodmer, J. L., Schröter, M., Burns, K., Mattmann, C., Rimoldi, D., French, L. E., and Tschopp, J. (1997) Inhibition of death receptor signals by cellular FLIP. Nature 388, 190-195
54. Hyer, M. L., Samuel, T., and Reed, J. C. (2006) The FLIP-side of Fas signaling. Clin. Cancer Res. 12, 5929-5931
55. Zauli, G., Gibellini, D., Caputo, A., Bassini, A., Negrini, M., Monne, M., Mazzoni, M., and Capitani, S. (1995) The human immunodeficiency virus type-1 Tat protein up-regulates Bcl-2 gene expression in Jurkat T-cell lines and primary peripheral blood mononuclear cells. Blood 86, 3823-3834
56. Corallini, A., Sampaolesi, R., Possati, L., Merlin, M., Bagnarelli, P., Piola, C., Fabris, M., Menegatti, M. A., Talevi, S., Gibellini, D., Rocchetti, R., Caputo, A., and Barbanti-Brodano, G. (2002) Inhibition of HIV-1 Tat activity correlates with down-regulation of bcl-2 and results in reduction of angiogenesis and oncogenicity. Virology 299, 1-7
57. Weiss, A., Wiskocil, R. L., and Stobo, J. D. (1984) The role of T3 surface molecules in the activation of humanTcells: a two-stimulus requirement for IL 2 production reflects events occurring at a pre-translational level. J. Immunol. 133, 123-128
58. Arenzana-Seisdedos, F., Fernandez, B., Dominguez, I., Jacqué, J. M., Thomas, D., Diaz-Meco, M. T., Moscat, J., and Virelizier, J. L. (1993) Phosphatidylcholine hydrolysis activates NF-κB and increases human immunodeficiency virus replication in human monocytes andTlymphocytes. J. Virol. 67, 6596-6604
59. Adachi, A., Gendelman, H. E., Koenig, S., Folks, T., Willey, R., Rabson, A., and Martin, M. A. (1986) Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59, 284-291
60. Jablonski, J. A., and Caputi, M. (2009) Role of cellular RNA processing factors in human immunodeficiency virus type 1 mRNA metabolism, replication, and infectivity. J. Virol. 83, 981-992
61. Laín de Lera, T., Folgueira, L., Martín, A. G., Dargemont, C., Pedraza, M. A., Bermejo, M., Bonay, P., Fresno, M., and Alcami, J. (1999) Expression of IκBα in the nucleus of human peripheral blood T lymphocytes. Oncogene 18, 1581-1588
62. Liu, Y., Graham, C., Li, A., Fisher, R. J., and Shaw, S. (2002) Phosphorylation of the protein kinase C-θ activation loop and hydrophobic motif regulates its kinase activity, but only activation loop phosphorylation is critical to in vivo nuclear factor-κB induction. Biochem. J. 361, 255-265
63. Paulo, J. A., Kadiyala, V., Banks, P. A., Steen, H., and Conwell, D. L. (2012) Mass spectrometry-based proteomics for translational research: a technical overview. Yale J. Biol. Med. 85, 59-73
64. Yates, J. R., 3rd, Eng, J. K., McCormack, A. L., and Schieltz, D. (1995) Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal. Chem. 67, 1426-1436
65. Just, M. A., Carpenter, P. A., Keller, T. A., Emery, L., Zajac, H., and Thulborn, K. R. (2001) Interdependence of nonoverlapping cortical systems in dual cognitive tasks. Neuroimage 14, 417-426
66. Szklarczyk, D., Franceschini, A., Kuhn, M., Simonovic, M., Roth, A., Minguez, P., Doerks, T., Stark, M., Muller, J., Bork, P., Jensen, L. J., and von Mering, C. (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 39, D561-D568
67. Levy, J. A. (1993) Pathogenesis of human immunodeficiency virus infection. Microbiol. Rev. 57, 183-289
68. Cossarizza, A., Baccarani-Contri, M., Kalashnikova, G., and Franceschi, C. (1993) A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5′,6,6′-tetrachloro-1,1′,3,3′- tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem. Biophys. Res. Commun. 197, 40-45
69. Schmitz, I., Weyd, H., Krueger, A., Baumann, S., Fas, S. C., Krammer, P. H., and Kirchhoff, S. (2004) Resistance of short term activated T cells to CD95-mediated apoptosis correlates with de novo protein synthesis of c-FLIPshort. J. Immunol. 172, 2194-2200
70. Mahlknecht, U., Dichamp, I., Varin, A., Van Lint, C., and Herbein, G. (2008) NF-κB-dependent control of HIV-1 transcription by the second coding exon of Tat in T cells. J. Leukocyte Biol. 83, 718-727
71. Mocarski, E. S., Upton, J. W., and Kaiser, W. J. (2012) Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways. Nat. Rev. Immunol. 12, 79-88
72. Richard, A., and Tulasne, D. (2012) Caspase cleavage of viral proteins, another way for viruses to make the best of apoptosis. Cell Death Dis. 3, e277
73. Cuconati, A., and White, E. (2002) Viral homologs of BCL-2: role of apoptosis in the regulation of virus infection. Genes Dev. 16, 2465-2478
74. Zachos, G., Koffa, M., Preston, C. M., Clements, J. B., and Conner, J. (2001) Herpes simplex virus type 1 blocks the apoptotic host cell defense mechanisms that target Bcl-2 and manipulates activation of p38 mitogen- activated protein kinase to improve viral replication. J. Virol. 75, 2710-2728
75. Stewart, S. A., Poon, B., Jowett, J. B., and Chen, I. S. (1997) Human immunodeficiency virus type 1 Vpr induces apoptosis following cell cycle arrest. J. Virol. 71, 5579-5592
76. Yao, X. J., Mouland, A. J., Subbramanian, R. A., Forget, J., Rougeau, N., Bergeron, D., and Cohen, E. A. (1998) Vpr stimulates viral expression and induces cell killing in human immunodeficiency virus type 1-infected dividing Jurkat T cells. J. Virol. 72, 4686-4693
77. Gibellini, D., Caputo, A., Celeghini, C., Bassini, A., La Placa, M., Capitani, S., and Zauli, G. (1995) Tat-expressing Jurkat cells show an increased resistance to different apoptotic stimuli, including acute human immunodeficiency virus-type 1 (HIV-1) infection. Br. J. Haematol. 89, 24-33
78. Fernández Larrosa, P. N., Croci, D. O., Riva, D. A., Bibini, M., Luzzi, R., Saracco, M., Mersich, S. E., Rabinovich, G. A., and Martínez Peralta, L. (2008) Apoptosis resistance in HIV-1 persistently infected cells is independent of active viral replication and involves modulation of the apoptotic mitochondrial pathway. Retrovirology 5, 19
79. Casula, M., Bosboom-Dobbelaer, I., Smolders, K., Otto, S., Bakker, M., de Baar, M. P., Reiss, P., and de Ronde, A. (2005) Infection with HIV-1 induces a decrease in mtDNA. J. Infect. Dis. 191, 1468-1471
80. Chipuk, J. E., and Green, D. R. (2008) How do BCL-2 proteins induce mitochondrial outer membrane permeabilization?. Trends Cell Biol. 18, 157-164
81. Kelly, G. L., and Strasser, A. (2011) The essential role of evasion from cell death in cancer. Adv. Cancer Res. 111, 39-96
82. Shawgo, M. E., Shelton, S. N., and Robertson, J. D. (2009) Caspase-9 activation by the apoptosome is not required for fas-mediated apoptosis in type II Jurkat cells. J. Biol. Chem. 284, 33447-33455
83. Li, C. Y., Lee, J. S., Ko, Y. G., Kim, J. I., and Seo, J. S. (2000) Heat shock protein 70 inhibits apoptosis downstream of cytochrome c release and upstream of caspase-3 activation. J. Biol. Chem. 275, 25665-25671
84. Itoh, H., Komatsuda, A., Ohtani, H., Wakui, H., Imai, H., Sawada, K., Otaka, M., Ogura, M., Suzuki, A., and Hamada, F. (2002) Mammalian HSP60 is quickly sorted into the mitochondria under conditions of dehydration. Eur. J. Biochem. 269, 5931-5938
85. Shan, Y. X., Liu, T. J., Su, H. F., Samsamshariat, A., Mestril, R., and Wang, P. H. (2003) Hsp10 and Hsp60 modulate Bcl-2 family and mitochondria apoptosis signaling induced by doxorubicin in cardiac muscle cells. J. Mol. Cell. Cardiol. 35, 1135-1143
86. Choudhary, C., Kumar, C., Gnad, F., Nielsen, M. L., Rehman, M., Walther, T. C., Olsen, J. V., and Mann, M. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834-840
87. Sarras, H., Alizadeh Azami, S., and McPherson, J. P. (2010) In search of a function for BCLAF1. Scientific World Journal 10, 1450-1461
88. Kong, S., Kim, S. J., Sandal, B., Lee, S. M., Gao, B., Zhang, D. D., and Fang, D. (2011) The type III histone deacetylase Sirt1 protein suppresses p300-mediated histone H3 lysine 56 acetylation at Bclaf1 promoter to inhibit T cell activation. J. Biol. Chem. 286, 16967-16975
89. Lindström, M. S. (2011) NPM1/B23: A multifunctional chaperone in ribosome biogenesis and chromatin remodeling. Biochem. Res. Int. 2011, 195209
90. Dhar, S. K., and St Clair, D. K. (2009) Nucleophosmin blocks mitochondrial localization of p53 and apoptosis. J. Biol. Chem. 284, 16409-16418
91. Szebeni, A., and Olson, M. O. (1999) Nucleolar protein B23 has molecular chaperone activities. Protein Sci. 8, 905-912
92. Gadad, S. S., Rajan, R. E., Senapati, P., Chatterjee, S., Shandilya, J., Dash, P. K., Ranga, U., and Kundu, T. K. (2011) HIV-1 infection induces acetylation of NPM1 that facilitates Tat localization and enhances viral transactivation. J. Mol. Biol. 410, 997-1007
93. Kerr, L. E., Birse-Archbold, J. L., Short, D. M., McGregor, A. L., Heron, I., Macdonald, D. C., Thompson, J., Carlson, G. J., Kelly, J. S., McCulloch, J., and Sharkey, J. (2007) Nucleophosmin is a novel Bax chaperone that regulates apoptotic cell death. Oncogene. 26, 2554-2562
94. Desagher, S., Osen-Sand, A., Nichols, A., Eskes, R., Montessuit, S., Lauper, S., Maundrell, K., Antonsson, B., and Martinou, J. C. (1999) Bidinduced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol. 144, 891-901
95. Marani, M., Tenev, T., Hancock, D., Downward, J., and Lemoine, N. R. (2002) Identification of novel isoforms of the BH3 domain protein Bim, which directly activate Bax to trigger apoptosis. Mol. Cell. Biol. 22, 3577-3589
96. Chiang, C. W., Yan, L., and Yang, E. (2008) Phosphatases and regulation of cell death. Methods Enzymol. 446, 237-257
97. Li, Z., Zhao, J., Du, Y., Park, H. R., Sun, S. Y., Bernal-Mizrachi, L., Aitken, A., Khuri, F. R., and Fu, H. (2008) Down-regulation of 14-3-3ζ suppresses anchorage-independent growth of lung cancer cells through anoikis activation. Proc. Natl. Acad. Sci. U.S.A. 105, 162-167
98. Chowdhury, I., Xu, W., Stiles, J. K., Zeleznik, A., Yao, X., Matthews, R., Thomas, K., and Thompson, W. E. (2007) Apoptosis of rat granulosa cells after staurosporine and serum withdrawal is suppressed by adenovirusdirected overexpression of prohibitin. Endocrinology 148, 206-217
99. Chowdhury, I., Branch, A., Olatinwo, M., Thomas, K., Matthews, R., and Thompson, W. E. (2011) Prohibitin (PHB) acts as a potent survival factor against ceramide induced apoptosis in rat granulosa cells. Life Sci. 89, 295-303
100. Schories, B., Engel, K., Dörken, B., Gossen, M., and Bommert, K. (2004) Characterization of apoptosis-induced Mcm3 and Cdc6 cleavage reveals a proapoptotic effect for one Mcm3 fragment. Cell Death Differ. 11, 940-942
101. Schwab, B. L., Leist, M., Knippers, R., and Nicotera, P. (1998) Selective proteolysis of the nuclear replication factor MCM3 in apoptosis. Exp. Cell Res. 238, 415-421
102. Aumais, J. P., Williams, S. N., Luo, W., Nishino, M., Caldwell, K. A., Caldwell, G. A., Lin, S. H., and Yu-Lee, L. Y. (2003) Role for NudC, a dynein-associated nuclear movement protein, in mitosis and cytokinesis. J. Cell Sci. 116, 1991-2003
103. Finn, R. M., Browne, K., Hodgson, K. C., and Ausió, J. (2008) sNASP, a histone H1-specific eukaryotic chaperone dimer that facilitates chromatin assembly. Biophys. J. 95, 1314-1325
104. Osakabe, A., Tachiwana, H., Matsunaga, T., Shiga, T., Nozawa, R. S., Obuse, C., and Kurumizaka, H. (2010) Nucleosome formation activity of human somatic nuclear autoantigenic sperm protein (sNASP). J. Biol. Chem. 285, 11913-11921
105. Kurki, P., Lotz, M., Ogata, K., and Tan, E. M. (1987) Proliferating cell nuclear antigen (PCNA)/cyclin in activated human T lymphocytes. J. Immunol. 138, 4114-4120
106. Alekseev, O. M., Richardson, R. T., Alekseev, O., and O'Rand, M. G. (2009) Analysis of gene expression profiles in HeLa cells in response to overexpression or siRNA-mediated depletion of NASP. Reprod. Biol. Endocrinol. 7, 45
107. Shiozaki, E. N., Chai, J., Rigotti, D. J., Riedl, S. J., Li, P., Srinivasula, S. M., Alnemri, E. S., Fairman, R., and Shi, Y. (2003) Mechanism of XIAPmediated inhibition of caspase-9. Mol. Cell 11, 519-527
108. Deveraux, Q. L., Takahashi, R., Salvesen, G. S., and Reed, J. C. (1997) X-linked IAP is a direct inhibitor of cell-death proteases. Nature 388, 300-304
109. Stennicke, H. R., Ryan, C. A., and Salvesen, G. S. (2002) Reprieval from execution: the molecular basis of caspase inhibition. Trends Biochem. Sci. 27, 94-101
110. Bratton, S. B., Lewis, J., Butterworth, M., Duckett, C. S., and Cohen, G. M. (2002) XIAP inhibition of caspase-3 preserves its association with the Apaf-1 apoptosome and prevents CD95- and Bax-induced apoptosis. Cell Death Differ. 9, 881-892
111. Wang, C. Y., Mayo, M. W., Korneluk, R. G., Goeddel, D. V., and Baldwin, A. S., Jr. (1998) NF-κB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281, 1680-1683
112. Park, S. M., Yoon, J. B., and Lee, T. H. (2004) Receptor interacting protein is ubiquitinated by cellular inhibitor of apoptosis proteins (c-IAP1 and c-IAP2) in vitro. FEBS Lett. 566, 151-156
113. Wajant, H., and Scheurich, P. (2011) TNFR1-induced activation of the classical NF-κB pathway. FEBS J. 278, 862-876