Rotenone enhances the antifungal properties of staurosporine

Eukaryotic Cell

Volumn 9, Issue 6, 2010, Pages 906-914

  Castro, Ana ^a,b   Lemos, Catarina ^a,b   Falcão, Artur ^a   Fernandes, Andreia S ^a   Louise Glass, N ^c   Videira, Arnaldo ^a,d  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSIDADE FERNANDO PESSOA   (Portugal)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFUNGAL AGENT; ROTENONE; STAUROSPORINE;

ARTICLE; CELL DEATH; DRUG EFFECT; METABOLISM; NEUROSPORA CRASSA; SACCHAROMYCES CEREVISIAE; DRUG EFFECTS;

ANTIFUNGAL AGENTS; CELL DEATH; NEUROSPORA CRASSA; ROTENONE; SACCHAROMYCES CEREVISIAE; STAUROSPORINE;

ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; FUNGI; NEUROSPORA CRASSA; SACCHAROMYCES CEREVISIAE;

EID: 77953792885     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00003-10     Document Type: Article

References (63)

1. Akerboom, T. P., and H. Sies. 1981. Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Methods Enzymol. 77:373-382.
2. Aldieri, E., C. Riganti, M. Polimeni, E. Gazzano, C. Lussiana, I. Campia, and D. Ghigo. 2008. Classical inhibitors of NOX NAD(P)H oxidases are not specific. Curr. Drug Metab. 9:686-696.
3. Almeida, B., A. Silva, A. Mesquita, B. Sampaio-Marques, F. Rodrigues, and P. Ludovico. 2008. Drug-induced apoptosis in yeast. Biochim. Biophys. Acta 1783:1436-1448.
4. Armstrong, J. S. 2006. Mitochondria: a target for cancer therapy. Br. J. Pharmacol. 147:239-248.
5. Belmokhtar, C. A., J. Hillion, and E. Ségal-Bendirdjian. 2001. Staurosporine induces apoptosis through both caspase-dependent and caspase-independent mechanisms. Oncogene 20:3354-3362.
6. Cannon, R. D., E. Lamping, A. R. Holmes, K. Niimi, P. V. Baret, M. V. Keniya, K. Tanabe, M. Niimi, A. Goffeau, and B. C. Monk. 2009. Efflux-mediated antifungal drug resistance. Clin. Microbiol. Rev. 22:291-321.
7. Carneiro, P., M. Duarte, and A. Videira. 2007. The external alternative NAD(P)H dehydrogenase NDE3 is localized both in the mitochondria and in the cytoplasm of Neurospora crassa. J. Mol. Biol. 368:1114-1121.
8. Castro, A., C. Lemos, A. Falcão, N. L. Glass, and A. Videira. 2008. Increased resistance of complex I mutants to phytosphingosine-induced programmed cell death. J. Biol. Chem. 283:19314-19321.
9. Cheng, J., T.-S. Park, L.-C. Chio, A. S. Fischl, and X. S. Ye. 2003. Induction of apoptosis by sphingoid long-chain bases in Aspergillus nidulans. Mol. Cell. Biol. 23:163-177.
10. Cheng, W. C., K. M. Leach, and J. M. Hardwick. 2008. Mitochondrial death pathways in yeast and mammalian cells. Biochim. Biophys. Acta 1783:1272-1279.
11. Choi, W. S., S. E. Kruse, R. D. Palmiter, and Z. Xia. 2008. Mitochondrial complex I inhibition is not required for dopaminergic neuron death induced by rotenone, MPP, or paraquat. Proc. Natl. Acad. Sci. U. S. A. 39:15136-15141.
12. Circu, M. L., S. Stringer, C. A. Rhoads, M. P. Moyer, and T. Y. Aw. 2009. The role of GSH efflux in staurosporine-induced apoptosis in colonic epithelial cells. Biochem. Pharmacol. 77:76-85.
13. Davis, R. H., and F. J. de Serres. 1970. Genetic and microbiological research techniques for Neurospora crassa. Methods Enzymol. 17A:79-143.
14. Davis, R. H., and D. D. Perkins. 2002. Timeline: Neurospora: a model of model microbes. Nat. Rev. Genet. 3:397-403.
15. Deshmukh, M., and E. M. Johnson Jr. 2000. Staurosporine-induced neuronal death: multiple mechanisms and methodological implications. Cell Death Differ. 7:250-261.
16. Duarte, M., and A. Videira. 2007. Mitochondrial NAD(P)H dehydrogenases in filamentous fungi, p. 55-68. In M. I. Gonsález Siso (ed.), Complex I and alternative dehydrogenases. Transworld Research Network, Trivandrum, Kerala, India.
17. Dunlap, J. C., K. A. Borkovich, M. R. Henn, G. E. Turner, M. S. Sachs, N. L. Glass, K. McCluskey, M. Plamann, J. E. Galagan, B. W. Birren, R. L. Weiss, J. P. Townsend, J. J. Loros, M. A. Nelson, R. Lambreghts, H. V. Colot, G. Park, P. Collopy, C. Ringelberg, C. Crew, L. Litvinkova, D. DeCaprio, H. M. Hood, S. Curilla, M. Shi, M. Crawford, M. Koerhsen, P. Montgomery, L. Larson, M. Pearson, T. Kasuga, C. Tian, M. Basturkmen, L. Altamirano, and J. Xu. 2007. Enabling a community to dissect an organism: overview of the Neurospora Functional Genomics Project. Adv. Genet. 57:49-96.
18. Eisenberg, T., S. Büttner, G. Kroemer, and F. Madeo. 2007. The mitochondrial pathway in yeast apoptosis. Apoptosis 12:1011-1023.
19. Fecke, W., V. D. Sled, T. Ohnishi, and H. Weiss. 1994. Disruption of the gene encoding the NADH-binding subunit of NADH: ubiquinone oxidoreductase in Neurospora crassa. Formation of a partially assembled enzyme without FMN and the iron-sulphur cluster N-3. Eur. J. Biochem. 220:551-558.
20. Fendel, U., M. A. Tocilescu, S. Kerscher, and U. Brandt. 2008. Exploring the inhibitor binding pocket of respiratory complex I. Biochim. Biophys. Acta 1777:660-665.
21. Franco, R., and J. A. Cidlowski. 2009. Apoptosis and glutathione: beyond an antioxidant. Cell Death Differ. 16:1303-1314.
22. Franco, R., M. I. Panayiotidis, and J. A. Cidlowski. 2007. Glutathione depletion is necessary for apoptosis in lymphoid cells independent of reactive oxygen species formation. J. Biol. Chem. 282:30452-30465.
23. Galagan, J. E., S. E. Calvo, K. A. Borkovich, E. U. Selker, N. D. Read, D. Jaffe, W. FitzHugh, L.-J. Ma, S. Smirnov, S. Purcell, B. Rehman, T. Elkins, R. Engels, S. Wang, C. B. Nielsen, J. Butler, M. Endrizzi, D. Qui, P. Ianakiev, D. Bell-Pedersen, M. A. Nelson, M. Werner-Washburne, C. P. Selitrennikoff, J. A. Kinsey, E. L. Braun, A. Zelter, U. Schulte, G. O. Kothe, G. Jedd, W. Mewes, C. Staben, E. Marcotte, D. Greenberg, A. Roy, K. Foley, J. Naylor, N. Stange-Thomann, R. Barrett, S. Gnerre, M. Kamal, M. Kamvysselis, E. Mauceli, C. Bielke, S. Rudd, D. Frishman, S. Krystofova, C. Rasmussen, R. L. Metzenberg, D. D. Perkins, S. Kroken, C. Cogoni, G. Macino, D. Catcheside, W. Li, R. J. Pratt, S. A. Osmani, C. P. C. DeSouza, L. Glass, M. J. Orbach, J. A. Berglund, R. Voelker, O. Yarden, M. Plamann, S. Seiler, J. Dunlap, A. Radford, R. Aramayo, D. O. Natvig, L. A. Alex, G. Mannhaupt, D. J. Ebbole, M. Freitag, I. Paulsen, M. S. Sachs, E. S. Lander, C. Nusbaum, and B. Birren. 2003. The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859-868.
24. Gil, J., S. Almeida, C. R. Oliveira, and A. C. Rego. 2003. Cytosolic and mitochondrial ROS in staurosporine-induced retinal cell apoptosis. Free Radic. Biol. Med. 35:1500-1514.
25. Green, D. R., and G. Kroemer. 2004. The pathophysiology of mitochondrial cell death. Science 305:626-629.
26. Grivennikova, V. G., and A. D. Vinogradov. 2006. Generation of superoxide by the mitochondrial complex I. Biochim. Biophys. Acta 1757:553-561.
27. Hamann, A., D. Brust, and H. D. Osiewacz. 2008. Apoptosis pathways in fungal growth, development and ageing. Trends Microbiol. 16:276-283.
28. Hammond, C. L., R. Marchan, S. M. Krance, and N. Ballatori. 2007. Glutathione export during apoptosis requires functional multidrug resistance-associated proteins. J. Biol. Chem. 282:14337-14347.
29. Harkness, T. A., R. A. Rothery, J. H. Weiner, S. Werner, J. E. Azevedo, A. Videira, and F. E. Nargang. 1995. Disruption of the gene encoding the 78-kilodalton subunit of the peripheral arm of complex I in Neurospora crassa by repeat induced point mutation (RIP). Curr. Genet. 27:339-350.
30. Hatefi, Y. 1985. The mitochondrial electron transport and oxidative phosphorylation system. Annu. Rev. Biochem. 54:1015-1069.
31. Huang, G., Y. Chen, H. Lu, and X. Cao. 2007. Coupling mitochondrial respiratory chain to cell death: an essential role of mitochondrial complex I in the interferon-beta and retinoic acid-induced cancer cell death. Cell Death Differ. 14:327-337.
32. Kimchi, A. 2007. Programmed cell death: from novel gene discovery to studies on network connectivity and emerging biomedical implications. Cytokine Growth Factor Rev. 18:435-440.
33. Ladha, J. S., M. K. Tripathy, and D. Mitra. 2005. Mitochondrial complex I activity is impaired during HIV-1-induced T-cell apoptosis. Cell Death Differ. 12:1417-1428.
34. Li, N., K. Ragheb, G. Lawler, J. Sturgis, B. Rajwa, J. A. Melendez, and J. P. Robinson. 2003. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 278:8516-8525.
35. Li, Q., E. F. Sato, X. Zhu, and M. Inoue. 2009. A simultaneous release of SOD1 with cytochrome c regulates mitochondria-dependent apoptosis. Mol. Cell. Biochem. 322:151-159.
36. Li, W., L. Sun, Q. Liang, J. Wang, W. Mo, and B. Zhou. 2006. Yeast AMID homologue Ndi1p displays respiration-restricted apoptotic activity and is involved in chronological aging. Mol. Biol. Cell 17:1802-1811.
37. Majander, A., M. Finel, and M. Wikstrom. 1994. Diphenyleneiodonium inhibits reduction of iron-sulfur clusters in the mitochondrial NADH-ubiquinone oxidoreductase (complex I). J. Biol. Chem. 269:21037-21042.
38. Majors, B. S., M. J. Betenbaugh, and G. G. Chiang. 2007. Links between metabolism and apoptosis in mammalian cells: applications for anti-apoptosis engineering. Metab. Eng. 9:317-326.
39. Marella, M., B. B. Seo, A. Matsuno-Yagi, and T. Yagi. 2007. Mechanism of cell death caused by complex I defects in a rat dopaminergic cell line. J. Biol. Chem. 282:24146-24156.
40. Marella, M., B. B. Seo, E. Nakamaru-Ogiso, J. T. Greenamyre, A. Matsuno-Yagi, and T. Yagi. 2008. Protection by the NDI1 gene against neurodegeneration in a rotenone rat model of Parkinson's disease. PLoS One 3:e1433.
41. Marques, I., M. Duarte, J. Assunção, A. V. Ushakova, and A. Videira. 2005. Composition of complex I from Neurospora crassa and disruption of two "accessory" subunits. Biochim. Biophys. Acta 1707:211-220.
42. Martinvalet, D., D. M. Dykxhoorn, R. Ferrini, and J. Lieberman. 2008. Granzyme A cleaves a mitochondrial complex I protein to initiate caspase-independent cell death. Cell 133:681-692.
43. McCluskey, K. 2003. The Fungal Genetics Stock Center: from molds to molecules. Adv. Appl. Microbiol. 52:245-262.
44. Miyoshi, N., H. Oubrahim, P. B. Chock, and E. R. Stadtman. 2006. Age-dependent cell death and the role of ATP in hydrogen peroxide-induced apoptosis and necrosis. Proc. Natl. Acad. Sci. U. S. A. 103:1727-1731.
45. Muyderman, H., A. L. Wadey, M. Nilsson, and N. R. Sims. 2007. Mitochon-drial glutathione protects against cell death induced by oxidative and nitrative stress in astrocytes. J. Neurochem. 102:1369-1382.
46. Nedelcu, A. M. 2009. Comparative genomics of phylogenetically diverse unicellular eukaryotes provide new insights into the genetic basis for the evolution of the programmed cell death machinery. J. Mol. Evol. 68:256-268.
47. Okun, J. G., P. Lummen, and U. Brandt. 1999. Three classes of inhibitors share a common binding domain in mitochondrial complex I (NADH: ubiquinone oxidoreductase). J. Biol. Chem. 274:2625-2630.
48. Omura, S., Y. Iwai, A. Hirano, A. Nakagawa, J. Awaya, H. Tsuchya, Y. Takahashi, and R. Masuma. 1977. A new alkaloid AM-2282 of Streptomyces origin. Taxonomy, fermentation, isolation and preliminary characterization. J. Antibiot. (Tokyo) 30:275-282.
49. Overkamp, K. M., B. M. Bakker, P. Kotter, A. van Tuijl, S. de Vries, J. P. van Dijken, and J. T. Pronk. 2000. In vivo analysis of the mechanisms for oxidation of cytosolic NADH by Saccharomyces cerevisiae mitochondria. J. Bacteriol. 182:2823-2830.
50. Pereira, C., R. D. Silva, L. Saraiva, B. Johansson, M. J. Sousa, and M. Côrte-Real. 2008. Mitochondria-dependent apoptosis in yeast. Biochim. Bio-phys. Acta 1783:1286-1302.
51. Phillips, A. J., I. Sudbery, and M. Ramsdale. 2003. Apoptosis induced by environmental stresses and amphotericin B in Candida albicans. Proc. Natl. Acad. Sci. U. S. A. 100:14327-14332.
52. Ramsdale, M. 2008. Programmed cell death in pathogenic fungi. Biochim. Biophys. Acta 1783:1369-1380.
53. Reeves, M. B., A. A. Davies, B. P. McSharry, G. W. Wilkinson, and J. H. Sinclair. 2007. Complex I binding by a virally encoded RNA regulates mitochondria-induced cell death. Science 316:1345-1348.
54. Ricci, J.-E., C. Munoz-Pinedo, P. Fitzgerald, B. Bailly-Maitre, G. A. Perkins, N. Yadava, I. E. Scheffler, M. H. Ellisman, and D. R. Green. 2004. Disruption of mitochondrial function during apoptosis is mediated by caspase cleavage of the p75 subunit of complex I of the electron transport chain. Cell 117: 773-786.
55. Skulachev, V. 2006. Bioenergetic aspects of apoptosis, necrosis and mitoptosis. Apoptosis 11:473-485.
56. Tada-Oikawa, S., Y. Hiraku, M. Kawanishi, and S. Kawanishi. 2003. Mechanisms of generation of hydrogen peroxide and change of mitochondrial membrane potential during rotenone induced apoptosis. Life Sci. 73:3277-3288.
57. Tan, M. L., J. P. Ooi, N. Ismail, A. I. Moad, and T. S. Muhammad. 2009. Programmed cell death pathways and current antitumor targets. Pharm. Res. 26:1547-1560.
58. Videira, A. 1998. Complex I from the fungus Neurospora crassa. Biochim. Biophys. Acta 1364:89-100.
59. Videira, A., T. Kasuga, C. Tian, C. Lemos, A. Castro, and N. L. Glass. 2009. Transcriptional analysis of the response of Neurospora crassa to phytosphin-gosine reveals links to mitochondrial function. Microbiology 155:3134-3141.
60. Videira, A., M. Tropschug, and S. Werner. 1990. Primary structure and expression of a nuclear-coded subunit of complex I homologous to proteins specified by the chloroplast genome. Biochem. Biophys. Res. Commun. 171:1168-1174.
61. Watabe, M., and T. Nakaki. 2007. Mitochondrial complex I inhibitor rote-none-elicited dopamine redistribution from vesicles to cytosol in human dopaminergic SH-SY5Y cells. J. Pharmacol. Exp. Ther. 323:499-507.
62. Watabe, M., and T. Nakaki. 2008. Mitochondrial complex I inhibitor rote-none inhibits and redistributes vesicular monoamine transporter 2 via nitration in human dopaminergic SH-SY5Y cells. Mol. Pharmacol. 74:933-940.
63. Yeow, W. S., M. F. Ziauddin, J. B. Maxhimer, S. Shamimi-Noori, A. Baras, A. Chua, D. S. Schrump, and D. M. Nguyen. 2006. Potentiation of the anticancer effect of valproic acid, an antiepileptic agent with histone deacetylase inhibitory activity, by the kinase inhibitor staurosporine or its clinically relevant analogue UCN-01. Br. J. Cancer 94:1436-1445.