Farnesol induces the transcriptional accumulation of the Aspergillus nidulans Apoptosis-Inducing Factor (AIF)-like mitochondrial oxidoreductase

Molecular Microbiology

Volumn 70, Issue 1, 2008, Pages 44-59

  Savoldi, Marcela ^a   Malavazi, Iran ^a   Soriani, Frederico Marianetti ^a   Capellaro, José Luiz ^a   Kitamoto, Katsuhiko ^b   Da Silva Ferreira, Márcia Eliana ^a   Goldman, Maria Helena S ^a   Goldman, Gustavo Henrique ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS INDUCING FACTOR; FARNESOL; MESSENGER RNA; MITOCHONDRIAL PROTEIN; OXIDOREDUCTASE; PROTEIN KINASE C;

AMINO ACID TRANSPORT; ARTICLE; ASPERGILLUS NIDULANS; AUTOPHAGY; BACTERIAL STRAIN; BIOGENESIS; CONTROLLED STUDY; GENE EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA PROCESSING; RNA TRANSCRIPTION; RNA TRANSLATION;

APOPTOSIS; APOPTOSIS INDUCING FACTOR; ASPERGILLUS NIDULANS; AUTOPHAGY; FARNESOL; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; OXIDOREDUCTASES; PROTEIN KINASE C; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, FUNGAL; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EMERICELLA NIDULANS; FUNGI;

EID: 51649108152     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06385.x     Document Type: Article

References (66)

1. Adany, I., Yazlovitskaya, E.M., Haug, J.S., Voziyan, P.A. Melnykovych, G. (1994) Differences in sensitivity to farnesol toxicity between neoplastically- and non-neoplastically-derived cells in culture. Cancer Lett 79 : 175 179.
2. Apostolova, N., Cervera, A.M., Victor, V.M., Cadenas, S., Sanjuan-Pla, A., Alvarez-Barrientos, A., et al. (2006) 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 13 : 354 357.
3. Bifulco, M. (2005) Role of the isoprenoid pathway in ras transforming activity, cytoskeleton organization, cell proliferation and apoptosis. Life Sci 77 : 1740 1749.
4. Burke, Y.D., Stark, M.J., Roach, S.L., Sen, S.E. Crowell, P.L. (1997) Inhibition of pancreatic cancer growth by the dietary isoprenoids farnesol and geraniol. Lipids 32 : 151 156.
5. Burke, Y.D., Ayoubi, A.S., Werner, S.R., McFarland, B.C., Heilman, D.K., Ruggeri, B.A. Crowell, P.L. (2002) Effects of the isoprenoids perillyl alcohol and farnesol on apoptosis biomarkers in pancreatic cancer chemoprevention. Anticancer Res 22 : 3127 3134.
6. Candé, C., Vahsen, N., Métivier, D., Tourrière, H., Chebli, K., Garrido, C., et al. (2004) Regulation of cytoplasmic stress granules by apoptosis-inducing factor. J Cell Sci 117 : 4461 4468.
7. Cao, Y.-Y., Cao, Y.-B., Xu, Z., Ying, K., Li, Y., Xie, Y., et al. (2005) cDNA microarray analysis of differential gene expression in Candida albicans biofilm exposed to farnesol. Antimicrob Agents Chemother 49 : 584 589.
8. Chaveroche, M.K., Ghigo, J.M., and d'Enfert, C. (2000) A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res 28 : E97 E104.
9. Colot, H.V., Park, G., Turner, G.E., Ringelberg, C., Crew, C.M., Litvinkova, L., et al. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci USA 103 : 10352 10357.
10. Crowell, P.L. (1999) Prevention and therapy of cancer by dietary monoterpenes. J Nutr 129 : 775 778.
11. Edwards, P.A. Ericsson, J. (1999) Sterols and isoprenoids. Signalling molecules derived from the cholesterol biosynthetic pathway. Ann Rev Biochem 68 : 157 185.
12. Enjalbert, B. Whiteway, M. (2005) Release from quorum-sensing molecules triggers hyphal formation during Candida albicans resumption of growth. Eukaryot Cell 4 : 1203 1210.
13. NBS1 genes show genetic interactions during recovery from replication stress and DNA damage. Eukaryot Cell 4 : 1239 1252.
14. Fairn, G.D., MacDonald, K. McMaster, C.R. (2007) 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 282 : 4868 4874.
15. Fass, E., Shvets, E., Degani, I., Hirschberg, K. Elazar, Z. (2006) Microtubules support production of starvation-induced autophagosomes but not their targeting and fusion with lysosomes. J Biol Chem 281 : 36303 36316.
16. Flipphi, M., Kocialkowska, J. Felenbok, B. (2002) Characteristics of physiological inducers of the ethanol utilization (alc) pathway in Aspergillus nidulans. Biochem J 15 : 25 31.
17. Futerman, A.H. Riezman, H. (2005) The ins and outs of sphingolipid synthesis. Trends Cell Biol 15 : 312 318.
18. Ghannoum, M.A. Rice, L.B. (1999) Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin Microbiol Rev 12 : 501 517.
19. Glass, N.L. Dementhon, K. (2006) Non-self recognition and programmed cell death in filamentous fungi. Curr Opin Microbiol 9 : 553 558.
20. Goldman, G.H., dos Reis Marques, E., Duarte Ribeiro, D.C., de Souza Bernardes, L.A., Quiapin, A.C., Vitorelli, P.M., et al. (2003) 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 2 : 34 48.
21. Goldstein, J.L. Brown, M.S. (1990) Regulation of the mevalonate pathway. Nature 343 : 425 430.
22. He, L., Mo, H., Hadisusilo, S., Oureshi, A.A. Elson, C.E. (1997) Isoprenoids suppress the growth of murine B16 melanomas in vitro and in vivo. J Nutr 127 : 668 674.
23. Hermann, M., Spröte, P. Brakhage, A.A. (2006) Protein kinase C (PkcA) of Aspergillus nidulans is involved in penicillin production. Appl Environ Microbiol 72 : 2957 2970.
24. Hornby, J.M. Nickerson, K.W. (2004) Enhanced production of farnesol by Candida albicans treated with four azoles. Antimicrob Agents Chemother 48 : 2305 2307.
25. Hornby, J.M., Jensen, E.C., Lisec, A.D., Tasto, J.J., Jahnke, B., Shoemaker, R., et al. (2001) Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol 67 : 2982 2992.
26. Hornby, J.M., Kebaara, B.W. Nickerson, K.W. (2003) Farnesol biosynthesis in Candida albicans: cellular response to sterol inhibition by zaragozic acid B. Antimicrob Agents Chemother 47 : 2366 2369.
27. Hudes, G.R., Szarka, C.E., Adams, A., Ranganathan, S., McCauley, R.A., Weiner, L.M., et al. (2000) Phase I pharmacokinetic trial of perillyl alcohol (NSC 641066) in patients with refractory solid malignancies. Clin Cancer Res 6 : 3071 3080.
28. Joo, J.H., Liao, G., Collins, J.B., Grissom, S.F. Jetten, A.M. (2007) Farnesol-induced apoptosis in human lung carcinoma cells is coupled to the endoplasmic reticulum stress response. Cancer Res 67 : 7929 7936.
29. Kafer, E. (1977) Meiotic and mitotic recombination in Aspergillus and its chromosomal aberrations. Adv Genet 19 : 33 131.
30. Kikuma, T., Ohneda, M., Arioka, M. Kitamoto, K. (2006) Functional analysis of the ATG8 homologue Aoatg8 and role of autophagy in differentiation and germination in Aspergillus oryzae. Eukaryotic Cell 5 : 1328 1336.
31. Klein, J.A., Longo-Guess, C.M., Rossmann, M.P., Seburn, K.L., Hurd, R.E., Frnakel, W.N., et al. (2002) The harlequin mouse mutation down-regulates apoptosis-inducing factor. Nature 419 : 367 374.
32. Krantic, S., Mechawar, N., Reix, S. Quirio, R. (2007) Apoptosis-inducing factor: a matter of neuron life and death. Progr Neurobiol 81 : 179 196.
33. Machida, K. Tanaka, T. (1999) Farnesol-induced generation of reactive oxygen species dependent on mitochondrial transmembrane potential hyperpolarization mediated by F(0)F(1)-ATPase in yeast. FEBS Lett 462 : 108 112.
34. Machida, K., Tanaka, T., Fujita, K. Taniguchi, M. (1998) Farnesol-induced generation of reactive oxygen species via indirect inhibition of the mitochondrial electron transport chain in the yeast Saccharomyces cerevisiae. J Bacteriol 180 : 4460 4465.
35. Machida, K., Tanaka, T., Yano, Y., Otani, S. Taniguchi, M. (1999) Farnesol-induced growth inhibition in Saccharomyces cerevisiae by a cell cycle mechanism. Microbiology 145 : 293 299.
36. Martin, S.W. Konopka, J.B. (2004) Lipid raft polarization contributes to hyphal growth in Candida albicans. Eukaryot Cell 3 : 675 684.
37. Maxfield, F.R. Menon, A.K. (2006) Intracellular sterol transport and distribution. Curr Opin Cell Biol 18 : 379 385.
38. Miquel, K., Pradines, A. Favre, G. (1996) Farnesol and geranylgeraniol induce actin cytoskeleton disorganization and apoptosis in A549 lung adenocarcinoma cells. Biochem Biophys Res Commun 225 : 869 876.
39. Modjtahedi, N., Giordanetto, F., Madeo, F. Kroemer, G. (2006) Apoptosis-inducing factor: vital and lethal. Trends Cell Biol 16 : 264 272.
40. Nickerson, K.W., Atkin, A.L. Hornby, J.M. (2006) Quorum sensing in dimorphic fungi: farnesol and beyond. Appl Environ Microbiol 72 : 3805 3813.
41. Noventa-Jordão, M.A., do Nascimento, A.M., Goldman, M.H., Terenzi, H.F. Goldman, G.H. (1999) Molecular characterization of ubiquitin genes from Aspergillus nidulans: mRNA expression on different stress and growth conditions. Biochim Biophys Acta 1490 : 237 244.
42. Oakley, B.R. Osmani, S.A. (1993) Cell cycle analysis using the filamentous fungus Aspergillus nidulans. In The Cell Cycle: A Practical Approach. Fantes, P. Brooks, R. (eds). Oxford : Oxford University Press, pp. 127 142.
43. Ohizumi, H., Masuda, Y., Nakajo, S., Sakai, I., Ohsawa, S. Nakaya, K. (1995) Geranylgeraniol is a potent inducer of apoptosis in tumor cells. J Biochem 117 : 11 13.
44. Osmani, S.A., May, G.S. Morris, N.R. (1987) Regulation of the mRNA levels of nimA, a gene required for the G2-M transition in Aspergillus nidulans. J Cell Biol 104 : 1495 1504.
45. Otera, H., Ohsakaya, S., Nagaura, Z., Ishihara, N. Mihara, K. (2005) Export of mitochondrial AIF in response proapoptotic stimuli depends on processing at the intermembrane space. EMBO J 24 : 1375 1386.
46. Ozpolat, B., Akar, U., Mehta, K. Lopez-Berentein, G. (2007) PKC delta and tissue transglutaminase are novel inhibitors of autophagy in pancreatic cancer cells. Autophagy 3 : 480 483.
47. Pearson, C.L., Xu, X., Sharpless, K.E. Harris, S.D. (2004) MesA, a novel fungal protein required for the stabilization of polarity axes in Aspergillus nidulans. Mol Biol Cell 15 : 3658 3672.
48. Pichler, H. Riezman, H. (2004) Where sterols are required for endocytosis. Biochim Biophys Acta 3 : 51 61.
49. Pinan-Lucarré, B., Balguerie, A. Clavé, A. (2005) Accelerated cell death in Podospora autophagy mutants. Eukaryot Cell 4 : 1765 1774.
50. Pinan-Lucarré, B., Paoletti, M. Clavé, C. (2007) Cell death by incompatibility in the fungus Podospora. Sem Cancer Biol 17 : 101 111.
51. Reggiori, F., Monastyrska, I., Shintani, T. Klionsky, D.J. (2005) The actin cytoskeleton is required for selective types of autophagy, but not nonspecific autophagy, in the yeast Saccharomyces cerevisiae. Mol Biol Cell 16 : 5843 5856.
52. Reyland, M.E. (2007) Protein kinase C delta and apoptosis. Biochem Soc Trans 35 : 1001 1004.
53. Reynolds, E.S. (1963) The use of the lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17 : 208 212.
54. Rossignol, T., Logue, M.E., Reynolds, K., Grenon, M., Lowndes, N.F. Butler, G. (2007) Transcriptional response of Candida parapsilosis following exposure to farnesol. Antimicrob Agents Chemother 51 : 2304 2312.
55. Sambrook, J. Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press.
56. Schiestl, R.H. Gietz, R.D. (1989) High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet 16 : 339 346.
57. Semighini, C.P., Marins, M., Goldman, M.H.S. Goldman, G.H. (2002) 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 68 : 1351 1357.
58. Semighini, C.P., Hornby, J.M., Dumitru, R., Nickerson, K.W. Harris, S.D. (2006) Farnesol-induced apoptosis in Aspergillus nidulans reveals a possible mechanism for antagonistic interactions between fungi. Mol Microbiol 59 : 753 764.
59. Susin, S.A., Lorenzo, H.K., Zamzami, N., Marzo, I., Snow, B.E., Brothers, G.M., et al. (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397 : 441 446.
60. Teepe, A.G., Loprete, D.M., He, Z., Hoggard, T.A. Hill, T.W. (2007) The protein kinase C orthologue PkcA plays a role in cell wall integrity and polarized growth in Aspergillus nidulans. Fungal Genet Biol 44 : 554 562.
61. Urbano, A., Lakshmanan, U., Choo, P.H., Kwan, J.C., Ng, P.Y., Guo, K., et al. (2005) AIF suppresses chemical stress-induced apoptosis and maintains the transformed state of tumor cells. EMBO J 24 : 2815 2826.
62. Vahsen, N., Candé, C., Brière, J.J., Bénit, P., Joza, N., Larochette, N., et al. (2004) AIF deficiency compromises oxidative phosphorylation. EMBO J 23 : 4679 4689.
63. Wiseman, D.A., Werner, S.R. Crowell, P.L. (2007) 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 320 : 1163 1170.
64. Wissing, S., Ludovico, P., Herker, E., Buttner, S., Engelhardt, S.M., Decker, T., et al. (2004) An AIF orthologue regulates apoptosis in yeast. J Cell Biol 166 : 969 974.
65. Yoshida, K. (2007) PKCδ signaling: mechanisms of DNA damage response and apoptosis. Cell Signal 19 : 892 901.
66. Youle, R.J. Karbowski, M. (2005) Mitochondrial fission in apoptosis. Nature Rev Mol Cell Biol 6 : 657 663.