Thioredoxin-dependent regulation of AIF-mediated DNA damage

Free Radical Biology and Medicine

Volumn 87, Issue , 2015, Pages 125-136

  Shelar, Sandeep B ^a,e   Kaminska, Kamila K ^a   Reddy, Shridhivya A ^a   Kumar, Dilip ^b   Tan, Chong Teik ^a   Yu, Victor C ^a   Lu, Jun ^c   Holmgren, Arne ^c   Hagen, Thilo ^d   Chew, Eng Hui ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b AGENCY FOR SCIENCE   (Singapore)

^c KAROLINSKA INSTITUTE   (Sweden)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e University of Alabama at Birmingham   (United States)

Author keywords

Apoptosis inducing factor; Oxidative stress; Protein protein interaction; Thioredoxin

Indexed keywords

APOPTOSIS INDUCING FACTOR; CYSTEINE; DNA; THIOREDOXIN 1; AIFM1 PROTEIN, HUMAN; THIOREDOXIN; TXN PROTEIN, HUMAN;

ARTICLE; CELL DEATH; CELL NUCLEUS; CYTOSOL; DNA DAMAGE; HUMAN; HUMAN CELL; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; ANIMAL; GENETICS; HEK293 CELL LINE; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; PROTEIN PROTEIN INTERACTION;

MAMMALIA;

ANIMALS; APOPTOSIS INDUCING FACTOR; DNA DAMAGE; HEK293 CELLS; HUMANS; MITOCHONDRIA; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN INTERACTION MAPS; THIOREDOXINS;

EID: 84940031408     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.06.029     Document Type: Article

References (62)

1. W.C. Burhans, and N.H. Heintz. The cell cycle is a redox cycle: linking phase-specific targets to cell fate Free Radic. Biol. Med. 47 2009 1282 1293
2. M. Schieber, and N.S. Chandel ROS function in redox signaling and oxidative stress Curr. Biol. 24 2014 R453 R462
3. C. Ufer, C.C. Wang, A. Borchert, D. Heydeck, and H. Kuhn Redox control in mammalian embryo development Antioxid. Redox Signal. 13 2010 833 875
4. M.A. Lovell, and W.R. Markesbery Amyloid beta peptide, 4-hydroxynonenal and apoptosis Curr. Alzheimer Res. 3 2006 359 364
5. G.S. Gaki, and A.G. Papavassiliou Oxidative stress-induced signaling pathways implicated in the pathogenesis of Parkinson's disease Neuromolecular Med. 16 2014 217 230
6. R. Anuradha, M. Saraswati, K.G. Kumar, and S.H. Rani Apoptosis of beta cells in diabetes mellitus DNA Cell. Biol. 33 2014 743 748
7. L. Rochette, M. Zeller, Y. Cottin, and C. Vergely Diabetes, oxidative stress and therapeutic strategies Biochim. Biophys. Acta 2709-2729 1840 2014
8. G.I. Giles The redox regulation of thiol dependent signaling pathways in cancer Curr. Pharm. Des 12 2006 4427 4443
9. M. Valko, C.J. Rhodes, J. Moncol, M. Izakovic, and M. Mazur Free radicals, metals and antioxidants in oxidative stress-induced cancer Chem. Biol. Interact. 160 2006 1 40
10. C.H. Lillig, and A. Holmgren Thioredoxin and related molecules - from biology to health and disease Antioxid. Redox Signal. 9 2007 25 47
11. R. Sengupta, and A. Holmgren The role of thioredoxin in the regulation of cellular processes by S-nitrosylation Biochim. Biophys. Acta 689-700 2012 1820
12. J. Lu, and A. Holmgren Thioredoxin system in cell death progression Antioxid. Redox Signal. 17 2012 1738 1747
13. S.A. Susin, H.K. Lorenzo, N. Zamzami, I. Marzo, B.E. Snow, G.M. Brothers, J. Mangion, E. Jacotot, P. Costantini, M. Loeffler, N. Larochette, D.R. Goodlett, R. Aebersold, D.P. Siderovski, J.M. Penninger, and G. Kroemer Molecular characterization of mitochondrial apoptosis-inducing factor Nature 397 1999 441 446
14. S.A. Susin, N. Zamzami, M. Castedo, T. Hirsch, P. Marchetti, A. Macho, E. Daugas, M. Geuskens, and G. Kroemer Bcl-2 inhibits the mitochondrial release of an apoptogenic protease J. Exp. Med. 184 1996 1331 1341
15. D. Arnoult, P. Parone, J.C. Martinou, B. Antonsson, J. Estaquier, and J.C. Ameisen Mitochondrial release of apoptosis-inducing factor occurs downstream of cytochrome c release in response to several proapoptotic stimuli J. Cell. Biol. 159 2002 923 929
16. G.P. Colo, M.F. Rubio, I.M. Nojek, S.E. Werbajh, P.C. Echeverría, C.V. Alvarado, V.E. Nahmod, M.D. Galigniana, and M.A. Costas The p160 nuclear receptor co-activator RAC3 exerts an anti-apoptotic role through a cytoplasmatic action Oncogene 27 2008 2430 2444
17. Y.O. Son, Y.S. Jang, J.S. Heo, W.T. Chung, K.C. Choi, and J.C. Lee Apoptosis-inducing factor plays a critical role in caspase-independent, pyknotic cell death in hydrogen peroxide-exposed cells Apoptosis 14 2009 796 808
18. N. Doti, C. Reuther, P.L. Scognamiglio, A.M. Dolga, N. Plesnila, M. Ruvo, and C. Culmsee Inhibition of the AIF/CypA complex protects against intrinsic death pathways induced by oxidative stress Cell Death Dis 5 2014 e993
19. H.K. Lorenzo, S.A. Susin, and G. Kroemer Cytofluorometric quantitation of nuclear apoptosis induced in a cell-free system Methods Enzymol 322 2000 198 201
20. S.A. Susin, N. Zamzami, M. Castedo, E. Daugas, H.G. Wang, S. Geley, F. Fassy, J.C. Reed, and G. Kroemer The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Fas/APO-1/CD95- and ceramide-induced apoptosis J Exp Med 186 1997 25 37
21. C.C. Deocaris, S.C. Kaul, and R. Wadhwa On the brotherhood of the mitochondrial chaperones mortalin and heat shock protein 60 Cell Stress Chaperones 11 2006 116 128
22. M. Loeffler, E. Daugas, S.A. Susin, N. Zamzami, D. Metivier, A.L. Nieminen, G. Brothers, J.M. Penninger, and G. Kroemer Dominant cell death induction by extramitochondrially targeted apoptosis-inducing factor FASEB J 15 2001 758 767
23. M. Wu, L.G. Xu, X. Li, Z. Zhai, and H.B. Shu AMID, an apoptosis-inducing factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis J. Biol. Chem. 277 2002 25617 25623
24. C. Candé, N. Vahsen, I. Kouranti, E. Schmitt, E. Daugas, C. Spahr, J. Luban, R.T. Kroemer, F. Giordanetto, C. Garrido, J.M. Penninger, and G. Kroemer AIF and cyclophilin A cooperate in apoptosis-associated chromatinolysis Oncogene 23 2004 1514 1521
25. C. Artus, H. Boujrad, A. Bouharrour, M.N. Brunelle, S. Hoos, V.J. Yuste, P. Lenormand, J.C. Rousselle, A. Namane, P. England, H.K. Lorenzo, and S.A. Susin AIF promotes chromatinolysis and caspase-independent programmed necrosis by interacting with histone H2AX EMBO J 29 2010 1585 1599
26. K. Tobiume, M. Saitoh, and H. Ichijo Activation of apoptosis signal-regulating kinase 1 by the stress-induced activating phosphorylation of pre-formed oligomer J. Cell. Physiol. 191 2002 95 104
27. P.J. Nadeau, S.J. Charette, M.B. Toledano, and J. Landry Disulfide Bond-mediated multimerization of Ask1 and its reduction by thioredoxin-1 regulate H(2)O(2)-induced c-Jun NH(2)-terminal kinase activation and apoptosis Mol. Biol. Cell 18 2007 3903 3913
28. D.R. Green, L. Galluzzi, and G. Kroemer Cell biology. Metabolic control of cell death Science 345 2014 1250256
29. M.L. Circu, and T.Y. Aw Reactive oxygen species, cellular redox systems, and apoptosis Free Radic. Biol. Med. 48 2010 749 762
30. S. Ueda, H. Masutani, H. Nakamura, T. Tanaka, M. Ueno, and J. Yodoi Redox control of cell death Antioxid. Redox Signal. 4 2002 405 414
31. M. Saitoh, H. Nishitoh, M. Fujii, K. Takeda, K. Tobiume, Y. Sawada, M. Kawabata, K. Miyazono, and H. Ichijo Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1 EMBO J 17 1998 2596 2606
32. Y. Liu, and W. Min Thioredoxin promotes ASK1 ubiquitination and degradation to inhibit ASK1-mediated apoptosis in a redox activity-independent manner Circ. Res. 90 2002 1259 1266
33. R. Zhang, R. Al-Lamki, L. Bai, J.W. Streb, J.M. Miano, J. Bradley, and W. Min Thioredoxin-2 inhibits mitochondria-located ASK1-mediated apoptosis in a JNK-independent manner Circ. Res. 94 2004 1483 1491
34. A. Nishiyama, M. Matsui, S. Iwata, K. Hirota, H. Masutani, H. Nakamura, Y. Takagi, H. Sono, Y. Gon, and J. Yodoi Identification of thioredoxin-binding protein-2/vitamin D(3) up-regulated protein 1 as a negative regulator of thioredoxin function and expression J. Biol. Chem. 274 1999 21645 21650
35. P. Patwari, L.J. Higgins, W.A. Chutkow, J. Yoshioka, and R.T. Lee The interaction of thioredoxin with Txnip. Evidence for formation of a mixed disulfide by disulfide exchange J. Biol. Chem. 281 2006 21884 21891
36. N. Joza, K. Galindo, J.A. Pospisilik, P. Benit, M. Rangachari, E.E. Kanitz, Y. Nakashima, G.G. Neely, P. Rustin, J.M. Abrams, G. Kroemer, and J.M. Penninger The molecular archaeology of a mitochondrial death effector: AIF in Drosophila Cell Death Differ. 15 2008 1009 1018
37. H. Bauer, S.M. Kanzok, and R.H. Schirmer Thioredoxin-2 but not thioredoxin-1 is a substrate of thioredoxin peroxidase-1 from Drosophila melanogaster: isolation and characterization of a second thioredoxin in D. Melanogaster and evidence for distinct biological functions of Trx-1 and Trx-2 J. Biol. Chem. 277 2002 17457 17463
38. L.S. Nakao, R.A. Everley, S.M. Marino, S.M. Lo, L.E. de Souza, S.P. Gygi, and V.N. Gladyshev Mechanism-based proteomic screening identifies targets of thioredoxin-like proteins J. Biol. Chem. 290 2015 5685 5695
39. E. Daugas, D. Nochy, L. Ravagnan, M. Loeffler, S.A. Susin, N. Zamzami, and G. Kroemer Apoptosis-inducing factor (AIF): a ubiquitous mitochondrial oxidoreductase involved in apoptosis FEBS Lett. 476 2000 118 123
40. H. Ye, C. Cande, N.C. Stephanou, S. Jiang, S. Gurbuxani, N. Larochette, E. Daugas, C. Garrido, G. Kroemer, and H. Wu DNA binding is required for the apoptogenic action of apoptosis inducing factor Nat. Struct. Biol 9 2002 680 684
41. I.F. Sevrioukova Apoptosis-inducing factor: structure, function, and redox regulation Antioxid. Redox Signal. 14 2011 2545 2579
42. H. Otera, S. Ohsakaya, Z. Nagaura, N. Ishihara, and K. Mihara Export of mitochondrial AIF in response to proapoptotic stimuli depends on processing at the intermembrane space EMBO J 24 2005 1375 1386
43. M.J. Maté, M. Ortiz-Lombardía, B. Boitel, A. Haouz, D. Tello, S.A. Susin, J. Penninger, G. Kroemer, and P.M. Alzari The crystal structure of the mouse apoptosis-inducing factor AIF Nat. Struct. Biol 9 2002 442 446
44. T. Senda, T. Yamada, N. Sakurai, M. Kubota, T. Nishizaki, E. Masai, M. Fukuda, and Y. Mitsuidagger Crystal structure of NADH-dependent ferredoxin reductase component in biphenyl dioxygenase J. Mol. Biol. 304 2000 397 410
45. M.D. Miramar, P. Costantini, L. Ravagnan, L.M. Saraiva, D. Haouzi, G. Brothers, J.M. Penninger, M.L. Peleato, G. Kroemer, and S.A. Susin NADH oxidase activity of mitochondrial apoptosis-inducing factor J. Biol. Chem. 276 2001 16391 16398
46. J.A. Klein, C.M. Longo-Guess, M.P. Rossmann, K.L. Seburn, R.E. Hurd, W.N. Frankel, R.T. Bronson, and S.L. Ackerman The harlequin mouse mutation downregulates apoptosis-inducing factor Nature 419 2002 367 374
47. N. Vahsen, C. Candé, J.J. Brière, P. Bénit, N. Joza, N. Larochette, P.G. Mastroberardino, M.O. Pequignot, N. Casares, V. Lazar, O. Feraud, N. Debili, S. Wissing, S. Engelhardt, F. Madeo, M. Piacentini, J.M. Penninger, H. Schägger, P. Rustin, and G. Kroemer AIF deficiency compromises oxidative phosphorylation EMBO J 23 2004 4679 4689
48. B.M. Polster, G. Basañez, A. Etxebarria, J.M. Hardwick, and D.G. Nicholls Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria J. Biol. Chem. 280 2005 6447 6454
49. L. Ravagnan, S. Gurbuxani, S.A. Susin, C. Maisse, E. Daugas, N. Zamzami, T. Mak, M. Jäättelä, J.M. Penninger, C. Garrido, and G. Kroemer Heat-shock protein 70 antagonizes apoptosis-inducing factor Nat. Cell Biol. 3 2001 839 843
50. S. Gurbuxani, E. Schmitt, C. Cande, A. Parcellier, A. Hammann, E. Daugas, I. Kouranti, C. Spahr, A. Pance, G. Kroemer, and C. Garrido Heat shock protein 70 binding inhibits the nuclear import of apoptosis-inducing factor Oncogene 22 2003 6669 6678
51. Y. Matsumori, S.M. Hong, K. Aoyama, Y. Fan, T. Kayama, R.A. Sheldon, Z.S. Vexler, D.M. Ferriero, P.R. Weinstein, and J. Liu Hsp70 overexpression sequesters AIF and reduces neonatal hypoxic/ischemic brain injury J. Cereb. Blood Flow Metab. 25 2005 899 910
52. J.C. Lui, and S.K. Kong Heat shock protein 70 inhibits the nuclear import of apoptosis-inducing factor to avoid DNA fragmentation in TF-1 cells during erythropoiesis FEBS Lett. 581 2007 109 117
53. C. Zhu, X. Wang, J. Deinum, Z. Huang, J. Gao, N. Modjtahedi, M.R. Neagu, M. Nilsson, P.S. Eriksson, H. Hagberg, J. Luban, G. Kroemer, and K. Blomgren Cyclophilin A participates in the nuclear translocation of apoptosis-inducing factor in neurons after cerebral hypoxia-ischemia J Exp Med 204 2007 1741 1748
54. M. Baritaud, H. Boujrad, H.K. Lorenzo, S. Krantic, and S.A. Susin Histone H2AX: The missing link in AIF-mediated caspase-independent programmed necrosis Cell Cycle 9 2010 3166 3173
55. K. Hirota, M. Matsui, S. Iwata, A. Nishiyama, K. Mori, and J. Yodoi AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1 Proc. Natl. Acad. Sci. USA 94 1997 3633 3638
56. K. Hirota, M. Murata, Y. Sachi, H. Nakamura, J. Takeuchi, K. Mori, and J. Yodoi Distinct roles of thioredoxin in the cytoplasm and in the nucleus. A two-step mechanism of redox regulation of transcription factor NF-kappaB J. Biol. Chem. 274 1999 27891 27897
57. R.L. Poerschke, and P.J. Moos Thioredoxin reductase 1 knockdown enhances selenazolidine cytotoxicity in human lung cancer cells via mitochondrial dysfunction Biochem. Pharmacol. 81 2011 211 221
58. M. Berggren, A. Gallegos, J.R. Gasdaska, P.Y. Gasdaska, J. Warneke, and G. Powis Thioredoxin and thioredoxin reductase gene expression in human tumors and cell lines, and the effects of serum stimulation and hypoxia Anticancer Res. 16 1996 3459 3466
59. K. Kahlos, Y. Soini, M. Saily, P. Koistinen, S. Kakko, P. Paakko, A. Holmgren, and V.L. Kinnula Up-regulation of thioredoxin and thioredoxin reductase in human malignant pleural mesothelioma Int. J. Cancer 95 2001 198 204
60. Y. Soini, K. Kahlos, U. Napankangas, R. Kaarteenaho-Wiik, M. Saily, P. Koistinen, P. Paaakko, A. Holmgren, and V.L. Kinnula Widespread expression of thioredoxin and thioredoxin reductase in non-small cell lung carcinoma Clin. Cancer Res. 7 2001 1750 1757
61. J. Raffel, A.K. Bhattacharyya, A. Gallegos, H. Cui, J.G. Einspahr, D.S. Alberts, and G. Powis Increased expression of thioredoxin-1 in human colorectal cancer is associated with decreased patient survival J. Lab. Clin. Med. 142 2003 46 51
62. S.J. Kim, Y. Miyoshi, T. Taguchi, Y. Tamaki, H. Nakamura, J. Yodoi, K. Kato, and S. Noguchi High thioredoxin expression is associated with resistance to docetaxel in primary breast cancer Clin. Cancer Res. 11 2005 8425 8430