The roles played by Aspergillus nidulans apoptosis-inducing factor (AIF)-like mitochondrial oxidoreductase (AifA) and NADH-ubiquinone oxidoreductases (NdeA-B and NdiA) in farnesol resistance

Fungal Genetics and Biology

Volumn 47, Issue 12, 2010, Pages 1055-1069

  Dinamarco, Taísa Magnani ^a   Figueiredo Pimentel, Bárbara de Castro ^a   Savoldi, Marcela ^a   Malavazi, Iran ^b   Soriani, Frederico Marianetti ^a   Uyemura, Sérgio Akira ^a   Ludovico, Paula ^c   Goldman, Maria Helena S ^a   Goldman, Gustavo Henrique ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO CARLOS   (Brazil)

^c UNIVERSITY OF MINHO   (Portugal)

Author keywords

Apopotosis inducing factor; Aspergillus nidulans; Farnesol; NADH ubiquinone oxidoreductases

Indexed keywords

APOPTOSIS INDUCING FACTOR; FARNESOL; NDEA PROTEIN; NDIA PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; ASPERGILLUS NIDULANS; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; FUNGAL STRAIN; GENE OVEREXPRESSION; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL;

APOPTOSIS INDUCING FACTOR; ASPERGILLUS NIDULANS; ELECTRON TRANSPORT COMPLEX I; FARNESOL; FUNGAL PROTEINS; MITOCHONDRIA; REACTIVE OXYGEN SPECIES;

EMERICELLA NIDULANS;

EID: 78449236025     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2010.07.006     Document Type: Article

References (77)

1. Adam-Vizi V., Chinopoulos C. Bioenergetics and the formation of mitochondrial reactive oxygen species. Trends Pharmacol. Sci. 2006, 27:639-645.
2. Adany I., Yazlovitskaya E.M., Haug J.S., Voziyan P.A., Melnykovych G. Differences in sensitivity to farnesol toxicity between neoplastically- and non-neoplastically-derived cells in culture. Cancer Lett. 1994, 79:175-179.
3. Apostolova N., Cervera A.M., Victor V.M., Cadenas S., Sanjuan-Pla A., Alvarez-Barrientos A., Esplugues J.V., McCreath K.J. Loss of apoptosis-inducing factor leads to an increase in reactive oxygen species, and an impairment of respiration that can be reversed by antioxidants. Cell Death Differ. 2006, 13:354-357.
4. Bifulco M. Role of the isoprenoid pathway in ras transforming activity, cytoskeleton organization, cell proliferation and apoptosis. Life Sci. 2005, 77:1740-1749.
5. Boujrad H., Gubkina O., Robert N., Slavica K., Susin S.A. AIF-mediated programmed necrosis. Cell Cycle 2007, 6:2612-2619.
6. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
7. Burke Y.D., Ayoubi A.S., Werner S.R., McFarland B.C., Heilman D.K., Ruggeri B.A., Crowell P.L. Effects of the isoprenoids perillyl alcohol and farnesol on apoptosis biomarkers in pancreatic cancer chemoprevention. Anticancer Res. 2002, 22:3127-3134.
8. Burke Y.D., Stark M.J., Roach S.L., Sen S.E., Crowell P.L. Inhibition of pancreatic cancer growth by the dietary isoprenoids farnesol and geraniol. Lipids 1997, 32:151-156.
9. Carneiro P., Duarte M., Videira A. The external alternative NAD(P)H dehydrogeanse NDE3 is localized both in the mitochondria and in the cytoplasm of Neurospora crassa. J. Mol. Evol. 2007, 38:1114-1121.
10. Carneiro P., Duarte M., Videira A. The main external alternative NAD(P)H dehydrogenase of Neurospora crassa. Biochim. Biophys. Acta 2004, 1608:45-52.
11. Castro A., Lemos C., Falcão A., Glass N.L., Videira A. Increased resistance of complex I mutants to phytosphingosine-induced programmed cell death. J. Biol. Chem. 2008, 283:19314-19321.
12. Chaveroche M.K., Ghigo J.M., d'Enfert C. A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res. 2000, 28:E97-E104.
13. Cheung E.C., Joza N., Steenaart N.A., McClellan K.A., Neuspiel M., McNamara S., McNamara S., MacLaurin J.G., Rippstein P., Park D.S., Shore G.C., McBride H.M., Penninger J.M., Slack R.S. Dissociating the dual roles of apoptosis-inducing factor in maintaining mitochondrial structure and apoptosis. EMBO J. 2006, 25:4061-4073.
14. Chinta S.J., Rane A., Yadava N., Andersen J.K., Nicholls D.G., Polster B.M. Reactive oxygen species regulation by AIF- and complex I-depleted brain mitochondria. Free Rad. Biol. Med. 2009, 46:939-947.
15. Circu M.L., Aw T.Y. Reactive oxygen species, cellular redox systems, and apoptosis. Free Rad. Biol. Med. 2010, 48:749-762.
16. Colot H.V., Park G., Turner G.E., Ringelberg C., Crew C.M., Litvinkova L., Weiss R.L., Borkovich K.A., Dunlap J.C. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. USA 2006, 103:10352-10357.
17. Crowell P.L. Prevention and therapy of cancer by dietary monoterpenes. J. Nutr. 1999, 129:775-778.
18. Duarte M., Peters M., Schulte U., Videira A. The internal alternative NADH dehydrogenase of Neurospora crassa mitochondria. Biochem. J. 2003, 371:1005-1011.
19. Edwards P.A., Ericsson J. Sterols and isoprenoids. Signalling molecules derived from the cholesterol biosynthetic pathway. Annu. Rev. Biochem. 1999, 68:157-185.
20. Fairn G.D., MacDonald K., McMaster C.R. A chemogenomic screen in Saccharomyces cerevisiae uncovers a primary role for the mitochondria in farnesol toxicity and its regulation by the Pkc1 pathway. J. Biol. Chem. 2007, 282:4868-4874.
21. Fang J., Beattie D.S. External alternative NADH dehydrogenase of Saccharomyces cerevisiae: a potential source of superoxide. Free Rad. Biol. Med. 2003, 34:478-488.
22. Fernie A.R., Carrari F., Sweetlove L.J. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr. Opin. Plant Biol. 2004, 7:254-261.
23. Flipphi M., Kocialkowska J., Felenbok B. Characteristics of physiological inducers of the ethanol utilization (alc) pathway in Aspergillus nidulans. Biochem. J. 2002, 15:25-31.
24. Glass N.L., Dementhon K. Non-self recognition and programmed cell death in filamentous fungi. Curr. Opin. Microbiol. 2006, 9:553-558.
25. Goldman G.H., dos Reis Marques E., Duarte Ribeiro D.C., de Souza Bernardes L.A., Quiapin A.C., Vitorelli P.M., Savoldi M., Semighini C.P., de Oliveira R.C., Nunes L.R., Travassos L.R., Puccia R., Batista W.L., Ferreira L.E., Moreira J.C., Bogossian A.P., Tekaia F., Nobrega M.P., Nobrega F.G., Goldman M.H. Expressed sequence tag analysis of the human pathogen Paracoccidioides brasiliensis yeast phase: identification of putative homologues of Candida albicans virulence and pathogenicity genes. Eukaryot. Cell 2003, 2:34-48.
26. Goldstein J.L., Brown M.S. Regulation of the mevalonate pathway. Nature 1990, 343:425-430.
27. Guerrero-Castillo S., Vázquez-Acevedo M., González-Halphen D., Uribe-Carvajal S. In Yarrowia lipolytica mitochondria, the alternative NADH dehydrogenase interacts specifically with the cytochrome complexes of the classic respiratory pathway. Biochim. Biophys. Acta 2009, 1787:75-85.
28. Hangen E., Blomgren K., Bénit P., Kroemer G., Modjtahedi N. Life with or without AIF. Trends Biochem. Sci. 2010, 35:278-287.
29. He L., Mo H., Hadisusilo S., Oureshi A.A., Elson C.E. Isoprenoids suppress the growth of murine B16 melanomas in vitro and in vivo. J. Nutr. 1997, 127:668-674.
30. Helmerhorst E.J., Murphy M.P., Troxler R.F., Oppenheim F.G. Characterization of the mitochondrial respiratory pathways in Candida albicans. Biochim. Biophys. Acta 2002, 1556:73-80.
31. Hornby J.M., Jensen E.C., Lisec A.D., Tasto J.J., Jahnke B., Shoemaker R., et al. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl. Environ. Microbiol. 2001, 67:2982-2992.
32. Hudes G.R., Szarka C.E., Adams A., Ranganathan S., McCauley R.A., Weiner L.M., Langer C.J., Litwin S., Yeslow G., Halberr T., Qian M., Gallo J.M. Phase I pharmacokinetic trial of perillyl alcohol (NSC 641066) in patients with refractory solid malignancies. Clin. Cancer Res. 2000, 6:3071-3080.
33. Hutchinson E., Brown S., Tian C., Glass N.L. Transcriptional profiling and functional analysis of heterokaryon incompatibility in Neurospora crassa reveals that reactive oxygen species, but not metacaspases, are associated with programmed cell death. Microbiology 2009, 155:3957-3970.
34. Joo J.H., Jetten A.M. Molecular mechanisms involved in farnesol-induced apoptosis. Cancer Lett. 2010, 287:123-135.
35. Joseph-Horne T., Hollomon D.W., Wood P.M. Fungal respiration: a fusion of standard and alternative components. Biochim. Biophys. Acta 2001, 1504:179-195.
36. Joza N., Oudit G.Y., Brown D., Bénit P., Kassiri Z., Vahsen N., Benoit L., Patel M.M., Nowikovsky K., Vassault A., Backx P.H., Wada T., Kroemer G., Rustin P., Penninger J.M. Muscle-specific loss of apoptosis-inducing factor leads to mitochondrial dysfunction, skeletal muscle atrophy, and dilated cardiomyopathy. Mol. Cell. Biol. 2005, 25:10261-10272.
37. Joza N., Galindo K., Pospisilik J.A., Benit P., Rangachari M., Kanitz E.E., Nakashima Y., Neely G.G., Rustin P., Abrams J.M., Kroemer G., Penninger J.M. The molecular archaeology of a mitochondrial death effector: AIF in Drosophila. Cell Death Differ. 2008, 15:1009-1018.
38. Kafer E. Meiotic and mitotic recombination in Aspergillus and its chromosomal aberrations. Adv. Genet. 1977, 19:33-131.
39. Kawasaki L., Aguirre J. Multiple catalase genes are differentially regulated in Aspergillus nidulans. J. Bacteriol. 2001, 183:1434-1440.
40. Klein J.A., Longo-Guess C.M., Rossmann M.P., Seburn K.L., Hurd R.E., Frankel W.N., Bronson R.T., Ackerman S.L. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 2002, 419:367-374.
41. Krantic S., Mechawar N., Reix S., Quirio R. Apoptosis-inducing factor: a matter of neuron life and death. Progr. Neurobiol. 2007, 81:179-196.
42. Langford M.L., Atkin A.L., Nickerson K.W. Cellular interactions of farnesol, a quorum-sensing molecule produced by Candida albicans. Future Microbiol. 2009, 4:1353-1362.
43. Li W., Sun L., Liang Q., Wang J., Mo W., Zhou B. Yeast AMID homologue Ndi1p displays respiration-restricted apoptotic activity and is involved in chronological aging. Mol. Biol. Cell 2006, 17:1802-1811.
44. Liu S.S. Generating, partitioning, targeting and functioning of superoxide in mitochondria. Biosci. Rep. 1997, 17:259-272.
45. Luttik M.A.H., Overkamp K.M., Kötter P., de Vries S., van Dijken J.P., Pronk J.T. The Saccharomyces cerevisiae NDE1 and NDE2 genes encode separate mitochondrial NADH dehydrogenases catalyzing the oxidation of cytosolic NADH. J. Biol. Chem. 1998, 273:24529-24534.
46. Machida K., Tanaka T. Farnesol-induced generation of reactive oxygen species dependent on mitochondrial transmembrane potential hyperpolarization mediated by F(0)F(1)-ATPase in yeast. FEBS Lett. 1999, 462:108-112.
47. Machida K., Tanaka T., Fujita K., Taniguchi M. Farnesol-induced generation of reactive oxygen species via indirect inhibition of the mitochondrial electron transport chain in the yeast Saccharomyces cerevisiae. J. Bacteriol. 1998, 180:4460-4465.
48. Machida K., Tanaka T., Yano Y., Otani S., Taniguchi M. Farnesol-induced growth inhibition in Saccharomyces cerevisiae by a cell cycle mechanism. Microbiology 1999, 145:293-299.
49. McTaggart S.J. Isoprenylated proteins. Cell Mol. Life Sci. 2006, 63:255-267.
50. Melo A.M.P., Duarte M., Moller I.M., Prokisch H., Dolan P.L., Pinto L., Nelson M.A., Videira A. The external calcium-dependent NADPH dehydrogenase from Neurospora crassa mitochondria. J. Biol. Chem. 2001, 276:3947-3951.
51. Miquel K., Pradines A., Favre G. Farnesol and geranylgeraniol induce actin cytoskeleton disorganization and apoptosis in A549 lung adenocarcinoma cells. Biochem. Biophys. Res. Commun. 1996, 225:869-876.
52. Modjtahedi N., Giordanetto F., Madeo F., Kroemer G. Apoptosis-inducing factor: vital and lethal. Trends Cell Biol. 2006, 16:264-272.
53. Moller I.M. Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001, 52:561-591.
54. Nickerson K.W., Atkin A.L., Hornby J.M. Quorum sensing in dimorphic fungi: farnesol and beyond. Appl. Environ. Microbiol. 2006, 72:3805-3813.
55. Ohizumi H., Masuda Y., Nakajo S., Sakai I., Ohsawa S., Nakaya K. Geranylgeraniol is a potent inducer of apoptosis in tumor cells. J. Biochem. 1995, 117:11-13.
56. Osmani S.A., May G.S., Morris N.R. Regulation of the mRNA levels of nimA, a gene required for the G2-M transition in Aspergillus nidulans. J. Cell Biol. 1987, 104:1495-1504.
57. Otera H., Ohsakaya S., Nagaura Z., Ishihara N., Mihara K. Export of mitochondrial AIF in response proapoptotic stimuli depends on processing at the intermembrane space. EMBO J. 2005, 24:1375-1386.
58. Noventa-Jordão M.A., do Nascimento A.M., Goldman M.H., Terenzi H.F., Goldman G.H. Molecular characterization of ubiquitin genes from Aspergillus nidulans: mRNA expression on different stress and growth conditions. Biochim. Biophys. Acta 1999, 1490:237-244.
59. Porter A.G., Urbano A.G.L. Does apoptosis-inducing factor (AIF) have both life and death functions in cells?. BioEssays 2006, 28:834-843.
60. Pospisilik J.A., Knauf C., Joza N., Benit P., Orthofer M., Cani P.D., Ebersberger I., Nakashima T., Sarao R., Neely G., Esterbauer H., Kozlov A., Kahn C.R., Kroemer G., Rustin P., Burcelin R., Penninger J.M. Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 2007, 131:476-491.
61. Pradelli L.A., Bénéteau M., Ricci J.E. Mitochondrial control of caspase-dependent and -independent cell death. Cell Mol. Life Sci. 2010, 67:1589-1597.
62. Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. third ed.
63. Savoldi M., Malavazi I., Soriani F.M., Capellaro J.L., Goldman M.H.S., da Silva Ferreira M.E., Goldman G.H. Farnesol induces the transcriptional accumulation of the Aspergillus nidulans apoptosis inducing factor (AIF)-like mitochondrial oxidoreductase. Mol. Microbiol. 2008, 70:44-59.
64. Schiestl R.H., Gietz R.D. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet. 1989, 16:339-346.
65. Semighini C.P., Marins M., Goldman M.H.S., Goldman G.H. Quantitative analysis of the relative transcript levels of ABC transporter Atr genes in Aspergillus nidulans by real-time reverse transcription-PCR assay. Appl. Environ. Microbiol. 2002, 68:1351-1357.
66. Semighini C.P., Savoldi M., Goldman G.H., Harris S.D. Functional characterization of the putative Aspergillus nidulans poly(ADP-Ribose) polymerase homolog PrpA. Genetics 2006, 173:87-98.
67. Shirtliff M.E., Krom B.P., Meijering R.A.M., Peters B.M., Zhu J., Scheper M.A., Harris M.L., Jabra-Rizk M.A. Farnesol-induced apoptosis in Candida albicans. Antimicrob. Agents Chemother. 2009, 53:2392-2401.
68. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., Mangion J., Jacotot E., Costantini P., Loeffler M., Larochette N., Goodlett D.R., Aebersold R., Siderovski D.P., Penninger J.M., Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999, 397:441-446.
69. Tarrío N., Cérdan M.E., Siso M.I.G. Characterization of the second external alternative dehydrogenase from mitochondria of the respiratory yeast Kluyveromyces lactis. Biochim. Biophys. Acta 2006, 1757:1476-1484.
70. Tudella V.G., Curti C., Soriani F.M., Santos A.C., Uyemura S.A. In situ evidence of an alternative oxidase and an uncoupling protein in the respiratory chain of Aspergillus fumigatus. Int. J. Biochem. Cell Biol. 2004, 36:162-172.
71. Van Aken O., Giraud E., Clifton R., Whelan J. Alternative oxidase: a target and regulator of stress responses. Physiol. Plantarum 2009, 137:354-361.
72. Vahsen N., Candé C., Brière J.J., Bénit P., Joza N., Larochette N., Mastroberardino P.G., Pequignot M.O., Casares N., Lazar V., Feraud O., Debili N., Wissing S., Engelhardt S., Madeo F., Piacentini M., Penninger J.M., Schägger H., Rustin P., Kroemer G. AIF deficiency compromises oxidative phosphorylation. EMBO J. 2004, 23:4679-4689.
73. Videira A., Duarte M. On complex I and other NADH:ubiquinone reductases of Neurospora crassa. J. Bioenerg. Biomembr. 2001, 33:197-203.
74. Videira A., Duarte M. From NADH to ubiquinone in Neurospora mitochondria. Biochim. Biophys. Acta 2002, 10:187-191.
75. Videira A., Kasuga T., Tian C., Lemos C., Castro A., Glass N.L. Transcriptional analysis of the response of Neurospora crassa to phytosphingosine reveals links to mitochondrial function. Microbiology 2009, 155:3134-3141.
76. Wiseman D.A., Werner S.R., Crowell P.L. Cell cycle arrest by the isoprenoids perillyl alcohol, geraniol, and farnesol is mediated by p21(Cip1) and p27 (Kip1) adenocarcinoma cells. J. Pharmacol. Exp. Ther. 2007, 320:1163-1170.
77. Wissing S., Ludovico P., Herker E., Buttner S., Engelhardt S.M., Decker T., Link A., Proksch A., Rodrigues F., Corte-Real M., Fröhlich K.U., Manns J., Candé C., Sigrist S.J., Kroemer G., Madeo F. An AIF orthologue regulates apoptosis in yeast. J. Cell Biol. 2004, 166:969-974.