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Alternative oxidase inhibitors as antiparasitic agents against scuticociliatosis

Published online by Cambridge University Press:  14 May 2014

NATALIA MALLO ,
JESÚS LAMAS  and
JOSÉ M. LEIRO
NATALIA MALLO
Affiliation:
Department of Microbiology and Parasitology, Laboratory of Parasitology, Institute of Research and Food Analysis, University of Santiago de Compostela, Spain
JESÚS LAMAS
Affiliation:
Department of Cell Biology and Ecology, Faculty of Biology, University of Santiago de Compostela, Spain
JOSÉ M. LEIRO*
Affiliation:
Department of Microbiology and Parasitology, Laboratory of Parasitology, Institute of Research and Food Analysis, University of Santiago de Compostela, Spain
*
* Corresponding author: Laboratorio de Parasitología, Instituto de Investigación y Análisis Alimentarios, c/ Constantino Candeira s/n, 15782, Santiago de Compostela (La Coruña), Spain. E-mail: [email protected]
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Summary

Philasterides dicentrarchi causes a severe disease in turbot, and at present there are no drugs available to treat infected fish. We have previously demonstrated that, in addition to the classical respiratory pathway, P. dicentrarchi possesses an alternative mitochondrial respiratory pathway that is cyanide-insensitive and salicylhydroxamic acid (SHAM)-sensitive. In this study, we found that during the initial phase of growth in normoxia, ciliate respiration is sensitive to the natural polyphenol resveratrol (RESV) and to Antimycin A (AMA). However, under hypoxic conditions, the parasite utilizes AMA-insensitive respiration, which is completely inhibited by RESV and by the antioxidant propyl gallate (PG), an alternative oxidase (AOX) inhibitor. PG caused significantly dose-dependent inhibition of the in vitro growth of the parasite under normoxia and hypoxia and an over-expression of heat shock proteins of the Hsp70 subfamily. RESV and PG may affect the protective role of the AOX against mitochondrial oxidative stress, leading to an impaired mitochondrial membrane potential and mitochondrial dysfunction, which the parasite attempts to neutralize by increasing the expression of Hsp70. In view of the antiparasitic effects induced by AOX inhibitors and the absence of AOX in their host, this enzyme constitutes a potential target for the development of new drugs against scuticociliatosis.

Keywords

Philasterides dicentarchiscuticociliatosisalternative oxidasepropyl gallateresveratrolmitochondriaHsp70
Type
Research Article
Information
Parasitology , Volume 141 , Issue 10 , September 2014 , pp. 1311 - 1321
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Atta, H. M. and Ahmad, M. S. (2009). Antimycin-A antibiotic biosynthesis produced by Streptomyces Sp. AZ-AR-262: taxonomy, fermentation, purification and biological activities. Australian Journal of Basic and Applied Sciences 3, 125–135.Google Scholar
Barrow, C. J., Oleynek, J. J., Marinelli, V., Sun, H. H., Kaplita, P., Kim, H., Esser, L., Hossain, M. B., Xia, D., Yu, C. A., Rizo, J., Helm, D. and Deisenhofer, J. (1999). Structure of antimycin A1, a specific electron transfer inhibitor of ubiquinol-cytochrome c oxidoreductase. Journal of the American Chemical Society 121, 4902–4903.Google Scholar
Budiño, B., Lamas, J., Pata, M. P., Arranz, J. A., Sanmartín, M. L. and Leiro, J. (2011). Intraspecific variability in several isolates of Philasterides dicentrarchi (syn. Miamiensis avidus), a scuticociliate parasite of farmed turbot. Veterinary Parasitology 175, 260–272.Google Scholar
Budiño, B., Pata, M. P., Leiro, J. and Lamas, J. (2012). Differences in the in vitro susceptibility to resveratrol and other chemical compounds among several Philasterides dicentrarchi isolates from turbot. Parasitology Research 110, 1573–1578.Google Scholar
Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., Vandesompele, J. and Wittwer, C. T. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55, 611–622.CrossRefGoogle ScholarPubMed
Caruso, F., Mendoza, L., Castro, P., Cotoras, M., Aguirre, M., Matsurhiro, B., Isaacs, M., Rossi, M., Viglianti, A. and Antonioletti, R. (2011). Antifungal activity of resveratrol against Botrytis cinerea is improved using 2-furyl derivatives. PLoS ONE 6, e25421.CrossRefGoogle ScholarPubMed
Chaudhuri, M., Ott, R. D. and Hill, G. C. (2006). Trypanosome alternative oxidase: from molecule to function. Trends in Parasitology 22, 484–491.CrossRefGoogle ScholarPubMed
Chung, K.-T., Stevens, S. E., Lin, W.-F. and Wei, C. I. (1993). Growth inhibition of related food-borne bacteria by tannic acid, propyl gallate and related compounds. Letters in Applied Microbiology 17, 29–32.Google Scholar
Chung, K.-T., Lu, Z. and Chou, M. W. (1998). Mechanisms of inhibition of tannic acid and related compounds on the growth of intestinal bacteria. Food and Chemical Toxicology 36, 1053–1060.Google Scholar
Clarkson, A. B., Bienen, E. J., Pollakis, G. and Grady, R. J. (1989). Respiration of blood-stream forms of the parasite Trypanosoma brucei brucei is dependent on a plant-like alternative oxidase. Journal of Biological Chemistry 264, 17770–17776.Google Scholar
Costa, J. H., Mota, E. F., Cambursano, M. V., Lauxman, M. A., Nogueira de Oliveira, L. M., Silva Lima, M. G., Orellano, E. G. and Fernandes de Melo, D. (2010). Stress-induced co-expression of two alternative oxidase (VuAox1 and 2b) genes in Vigna unguiculata . Journal of Plant Physiology 167, 561–570.CrossRefGoogle ScholarPubMed
Czarna, M. and Jarmuszkiewicz, W. (2005). Activation of alternative oxidase and uncoupling protein lowers hydrogen peroxide formation in amoeba Acanthamoeba castellanii mitochondria. FEBS Letters 579, 3136–3140.Google Scholar
Czarna, M., Sluse, F. E. and Jarmuszkiewicz, W. (2007). Mitochondrial function plasticity in Acanthamoeba castellanii during growth in batch culture. Journal of Bioenergetics and Biomembranes 39, 149–157.CrossRefGoogle ScholarPubMed
Czarna, M., Mathy, G., MacCord, A., Dobson, R., Jarmuszkiewicz, W., Sluse-Goffart, C. M., Leprince, P., De Pauw, E. and Sluse, F. E. (2010). Dynamics of the Dictyostelium discoideum mitochondrial proteome during vegetative growth starvation and early stages of development. Proteomics 10, 6–22.Google Scholar
Dyková, I. and Figueras, A. (1994). Histopathological changes in turbot Scophthalmus maximus due to a histiophagous ciliate. Diseases of Aquatic Organisms 18, 5–9.CrossRefGoogle Scholar
Eisen, J. A., Coyne, R. S., Wu, M., Wu, D., Thiagarajan, M., Wortman, J. R., Badger, J. H., Ren, Q., Amedeo, P., Jones, K. M., Tallon, L. J., Delcher, A. L., Salzberg, S. L., Silva, J. C., Haas, B. J., Majoros, W. H., Farzad, M., Carlton, J. M., Smith, R. K. Jr, Garg, J., Pearlman, R. E., Karrer, K. M., Sun, L., Manning, G., Elde, N. C., Turkewitz, A. P., Asai, D. J., Wilkes, D. E., Wang, Y., Cai, H., Collins, K., Stewart, B. A., Lee, S. R., Wilamowska, K., Weinberg, Z., Ruzzo, W. L., Wloga, D., Gaertig, J., Frankel, J., Tsao, C. C., Gorovsky, M. A., Keeling, P. J., Waller, R. F., Patron, N. J., Cherry, J. M., Stover, N. A., Krieger, C. J., del Toro, C., Ryder, H. F., Williamson, S. C., Barbeau, R. A., Hamilton, E. P. and Orias, E. (2006). Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biology 4, e286.CrossRefGoogle ScholarPubMed
El-Khoury, R., Dufour, E., Rak, M., Ramanantsoa, N., Grandchamp, N., Csaba, Z., Duvillié, B., Bénit, P., Gallego, J., Gressens, P., Sarkis, C., Jacobs, H. T. and Rustin, P. (2013). Alternative oxidase expression in the mouse enables bypassing cytochrome c oxidase blockade and limits mitochondrial ROS overproduction. PloS Genetics 9, e1003182.CrossRefGoogle ScholarPubMed
Fujita, K.-I. and Kubo, I. (2002). Antifungal activity of octyl gallate. International Journal of Food Microbiology 79, 193–201.CrossRefGoogle ScholarPubMed
Garrido, J., Garrido, E. M. and Borges, F. (2012). Studies on the food additive propyl gallate: synthesis, structural characterization, and evaluation of the antioxidant activity. Journal of Chemical Education 89, 130–133.Google Scholar
Genevois, M. L. (1929). Sur la fermentation et sur la respiration chez les végétaux chlorophylliens. Revue Génétique Botanique 41, 252–271.Google Scholar
Gupta, K. J., Zalbalza, A. and Van Dongen, J. T. (2009). Regulation of respiration when the oxygen availability changes. Physiologia Plantarum 137, 383–391.Google Scholar
Harikrishnan, R., Balasundaram, C. and Heo, M. S. (2010). Scuticociliatosis and its recent prophylactic measures in aquaculture with special reference to South Korea taxonomy, diversity and diagnosis of scuticociliatosis. Part I. Control strategies of scuticociliatosis: part II. Fish and Shellfish Immunology 29, 15–31.CrossRefGoogle ScholarPubMed
Hart, J. H. (1981). Role of phytostilbenes in decay and disease resistant. Annual Review of Phytopathology 19, 437–458.Google Scholar
Haynes, C. M. and Ron, D. (2010). The mitochondrial UPR protecting organelle protein homeostasis. Journal of Cell Science 123, 3849–3855.Google Scholar
Hedley, C. and Huntington, T. (2009). Restricciones legales y reglamentarias de la acuicultura europea. Dirección General de Políticas internas de la Unión. Departamento temático B: Políticas estatales y de cohesión. Pesca. Parlamento Europeo. B-1047, Bruselas.Google Scholar
Henry, M.-F. and Nyns, E.-J. (1975). Cyanide-insensitive respiration. An alternative mitochondrial pathway. Sub-Cellular Biochemistry 4, 1–65.Google Scholar
Hsu, F. L., Chen, P.-S., Chang, H.-T. and Chang, S.-T. (2009). Effects of alkyl chain length of gallates on their antifungal property and potency as a environmentally benign preservative against wood-decay fungi. International Biodeterioration and Biodegradation 63, 543–547.Google Scholar
Iglesias, R., Paramá, A., Álvarez, M. F., Leiro, J., Fernández, J. and Sanmartín, M. L. (2001). Philasterides dicentrarchi (Ciliophora, Scuticocilatida) as the causative agent of scuticociliatosis in farmed turbot Scophthalmus maximus in Galicia (NW Spain). Diseases of Aquatic Organisms 46, 47–55.Google Scholar
Iglesias, R., Paramá, A., Álvarez, M. F., Leiro, J. and Sanmartín, M. L. (2002). Antiprotozoals effective in vitro against the scuticociliate fish pathogen Philasterides dicentrarchi . Diseases of Aquatic Organisms 49, 191–197.CrossRefGoogle ScholarPubMed
Iglesias, R., Paramá, A., Álvarez, M. F., Leiro, J., Ubeira, F. M. and Sanmartín, M. L. (2003). Philasterides dicentrarchi (Ciliophora: Scuticociliatida) expresses surface immobilization antigens that probably induce protective immune responses in turbot. Parasitology 126, 125–134.CrossRefGoogle ScholarPubMed
Inoue, K., Tsurumi, T., Ishii, H., Park, P. and Ikeda, K. (2012). Cytological evaluation of the effect of azoxystrobin and alternative oxidase inhibitors in Botrytis cinerea . FEMS Microbiology Letters 326, 83–90.Google Scholar
International Journal of Toxicology (2007). Final report on the amended safety assessment of propyl gallate. International Journal of Toxicology 26 (Suppl. 3), 89–118.Google Scholar
Jarmuszkiewicz, W. (2001). Uncoupling proteins in mitochondria of plants and some microorganisms. Acta Biochimica Polonica 48, 145–155.Google Scholar
Jarmuszkiewicz, W., Wagner, A. M., Wagner, M. J. and Hryniewiecka, L. (1997). Immunological identification of the alternative oxidase of Acanthamoeba castellanii mitochondria. FEBS Letters 411, 110–114.Google Scholar
Jarmuszkiewicz, W., Sluse-Goffart, C. M., Hryniewiecka, I., Michejda, J. and Sluse, F. E. (1998). Electron partitioning between the two branching quinol-oxidizing pathways in Acanthamoeba castellani mitochondria during steady-state state 3 respiration. Journal of Biological Chemistry 273, 10174–10180.Google Scholar
Jarmuszkiewicz, W., Sluse-Goffart, C. M., Hryniewiecka, L. and Sluse, F. E. (1999). Identification and characterization of a protozoan uncoupling protein in Acanthamoeba castellanii . Journal of Biological Chemistry 274, 23198–23202.Google Scholar
Jarmuszkiewicz, W., Behrendt, M., Navet, R. and Sluse, F. E. (2002). Uncoupling protein and alternative oxidase of Dictyostelium discoideum: ocurrence, properties and protein expression during vegetative life and starvation-induced early development. FEBS Letters 532, 459–464.Google Scholar
Jin, C. N., Harikrishnan, R., Moon, Y. C., Kim, M. C., Kim, J. S., Balasundaram, C. and Heo, M. S. (2010). Effectiveness of chemotherapeutants against scuticociliate Philasterides dicentrarchi, a parasite of olive flounder. Veterinary Parasitology 168, 19–24.Google Scholar
Jordan, H. V., Bowler, A. E. and Berger, N. D. (1961). Testing of antioxidants against experimental caries in rats. Journal of Dental Research 40, 878–883.Google Scholar
Joshi, D. C. and Bakowska, J. C. (2011). Determination of mitochondrial membrane potential and reactive oxygen species in live rat cortical neurons. Journal of Visualized Experiments 23, 2704.Google Scholar
Kadenbach, B., Ramzan, R. and Vogt, S. (2013). High efficiency versus maximal performance – the cause of oxidative stress in eukaryotes: a hypothesis. Mitochondrion 13, 1–6.Google Scholar
Karpova, O. V., Kuzmin, E. V., Elthon, T. E. and Newton, K. J. (2002). Differential expression of alternative oxidase genes in maize mitochondrial mutants. Plant Cell 14, 3271–3284.Google Scholar
Kim, S. M., Cho, J. B., Kim, S. K., Nam, Y. K. and Kim, K. H. (2004). Occurrence of scuticociliatosis in olive flounder Paralichthys olivaceus by Philasterides dicentrarchi (Ciliophora: Scuticociliatida). Diseases of Aquatic Organisms 62, 233–238.CrossRefGoogle ScholarPubMed
Kubo, I., Xiao, P. and Fujita, K.-I. (2001). Antifungal activity of octyl gallate: structural criteria and mode of action. Bioinorganic and Medical Chemistry Letters 11, 347–350.CrossRefGoogle ScholarPubMed
Kubo, I., Fujita, K. and Nihei, K. (2002). Anti-Salmonella activity of alkyl gallates. Journal of Agricultural and Food Chemistry 50, 6692–6696.Google Scholar
Kushnareva, Y. E. and Sokolove, P. M. (2000). Prooxidants open both the mitochondrial permeability transition pore and a low-conductance channel in the inner mitochondrial membrane. Archives of Biochemistry and Biophysics 376, 377–388.Google Scholar
Kutik, S., Guiard, B., Meyer, H. E., Wiedemann, N. and Pfanner, N. (2007). Cooperation of translocase complexes in mitochondrial protein import. Journal of Cell Biology 179, 585–591.Google Scholar
Lamas, J., Morais, P., Arranz, J. A., Sanmartín, M. L., Orallo, F. and Leiro, J. (2009). Resveratrol promotes an inhibitory effect on the turbot scuticociliate parasite Philasterides dicentrarchi by mechanisms related to cellular detoxification. Veterinary Parasitology 161, 307–315.Google Scholar
Lambowitz, A. M., Sabourin, J. R., Bertrand, H., Nickels, R. and McIntosh, L. (1989). Immunological identification of the alternative oxidase of Neurospora crassa mitochondria. Molecular and Cellular Biology 9, 1362–1364.Google Scholar
Leiro, J., Arranz, J. A., Paramá, A., Álvarez, M. F. and Sanmartín, M. L. (2004). In vitro effects of the polyphenols resveratrol, mangiferin and (-)-epigallocatechin-3-gallate on the scuticociliate fish pathogen Philasterides dicentrarchi . Diseases of Aquatic Organisms 59, 171–174.Google Scholar
Lenaz, G. (2012). Mitochondria and reactive oxygen species. Which role in physiology and pathology? Advances in Experimental Medicine and Biology 942, 93–136.CrossRefGoogle ScholarPubMed
Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25, 402–408.CrossRefGoogle Scholar
Mallo, N., Lamas, J. and Leiro, J. (2013 a). Evidence of an alternative oxidase pathway for mitochondrial respiration in the scuticociliate Philasterides dicentrarchi . Protist 164, 824–836.Google Scholar
Mallo, N., Lamas, J. and Leiro, J. (2013 b). Hydrogenosome metabolism is the key target for antiparasitic activity of resveratrol against Trichomonas vaginalis . Antimicrobial Agents and Chemotherapy 57, 2476–2484.CrossRefGoogle ScholarPubMed
Martindale, J. L. and Holbrook, N. J. (2002). Cellular response to oxidative stress: signaling for suicide and survival. Journal of Cellular Physiology 192, 1–15.Google Scholar
Maxwell, D. P., Wang, Y. and McIntosh, L. (1999). The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proceedings of the National Academy of Sciences USA 96, 8271–8276.CrossRefGoogle ScholarPubMed
McDonald, A., Vanlerberghe, G. C. and Staples, J. F. (2009). Alternative oxidase in animals: unique characteristics and taxonomic distribution. Journal of Experimental Biology 212, 2627–2634.Google Scholar
Mlejnek, P. (2013). Cytokinin-induced cell death is associated with elevated expression of alternative oxidase in tobacco BY-2 cells. Protoplasma 250, 1195–1202.Google Scholar
Moore, A. L. and Albury, M. S. (2008). Further insights into the structure of the alternative oxidase: from plants to parasites. Biochemical Society Transactions 36, 1022–1026.Google Scholar
Moore, A. L., Shiba, T., Young, L., Harada, S., Kita, K. and Ito, K. (2013). Unraveling the heater: new insights into the structure of the alternative oxidase. Annual Review of Plant Biology 64, 637–663.CrossRefGoogle ScholarPubMed
Morais, P., Lamas, J., Sanmartín, M. L., Orallo, F. and Leiro, J. (2009). Resveratrol induces mitochondrial alterations, autophagy and a cryptobiosis-like state in scuticociliates. Protist 160, 552–564.Google Scholar
Morais, P., Piazzon, C., Lamas, J., Mallo, N. and Leiro, J. M. (2013). Effect of resveratrol on oxygen consumption by Philasterides dicentrarchi, a scuticociliate parasite of turbot. Protist 164, 206–217.Google Scholar
Mosser, D. D., Caron, A. W., Bourget, L., Meriin, A. B., Sherman, M. Y., Morimoto, R. I. and Massie, B. (2000). The chaperone function of Hsp70 is required for protection against stress-induced apoptosis. Molecular and Cellular Biology 20, 7146–7159.Google Scholar
Murphy, A. D., Doeller, J., Hearn, B. and Lang-Unnasch, N. (1997). Plasmodium falciparum: cyanide resistant oxygen consumption. Experimental Parasitology 87, 112–120.CrossRefGoogle ScholarPubMed
Neupert, W. and Herrmann, J. M. (2007). Translocation of proteins into mitochondria. Annual Review of Biochemistry 76, 723–749.CrossRefGoogle ScholarPubMed
Nihei, C., Fukai, Y. and Kita, K. (2002). Trypanosome alternative oxidase as a target of chemotherapy. Biochimica et Biophysica Acta 1587, 234–239.Google Scholar
Paramá, P., Iglesias, R., Álvarez, M. F., Leiro, J., Aja, C. and Sanmartín, M. L. (2003). Philasterides dicentrarchi (Ciliophora, Scuticociliatida): experimental infection and possible routes of entry in farmed turbot (Scophthalmus maximus). Aquaculture 217, 73–80.CrossRefGoogle Scholar
Parrish, D. J. and Leopold, A. C. (1978). Confounding of alternative respiration by lipoxygenase activity. Plant Physiology 62, 470–472.Google Scholar
Peterman, T. K. and Siedow, J. N. (1983). Structural features required for inhibition of soybean lipoxygenase-2 by propyl gallate. Plant Physiology 71, 55–58.Google Scholar
Purvis, A. C. and Shewfelt, R. L. (1993). Does the alternative pathway ameliorate chilling injury in sensitive plant tissues? Physiologia Plantarum 88, 712–718.Google Scholar
Qi, Y., Wang, H., Zou, Y., Liu, C., Liu, Y., Wang, Y. and Zhang, W. (2011). Over-expression of mitochondrial heat shock protein 70 suppresses programmed cell death in rice. FEBS Letters 585, 231–239.Google Scholar
Rathore, G. S., Suthar, M., Pareek, A. and Gupta, R. N. (2011). Nutritional antioxidants: a battle for better health. Journal of Natural Pharmaceuticals 2, 2–14.Google Scholar
Roberts, C. W., Roberts, F., Henriquez, F. L., Akiyoshi, D., Samuel, B. U., Richards, T. A., Milhous, W., Kyle, D., McIntosh, L., Hill, G. C., Chaudhuri, M., Tzipori, S. and McLeod, R. (2004). Evidence for mitochondrial derived alternative oxidase in the apicomplexan parasite Cryptosporidium parvum: a potential anti-microbial agent target. International Journal for Parasitology 34, 297–308.CrossRefGoogle ScholarPubMed
Sakajo, S., Minagawa, N., Komiyama, T. and Yoshimoto, A. (1991). Molecular cloning of cDNA for antimycin A-inducible mRNA and its role in cyanide-resistant respiration in Hansenula anómala . Biochimica et Biophysica Acta 1090, 102–108.Google Scholar
Sakajo, S., Minagawa, N. and Yoshimoto, A. (1997). Effect of nucleotides on cyanide-resistant respiratory activity in mitochondria isolated from antimycin A-treated yeast Hansenula anómala . Bioscience Biotechnology and Biochemistry 61, 396–399.CrossRefGoogle ScholarPubMed
Sbaghi, M., Jeandet, P., Bessis, R. and Leroux, P. (1996). Degradation of stilbene-type phytoalexins in relation to the pathogenicity of Botrytis cinerea to grapevines. Plant Pathology 45, 139–144.CrossRefGoogle Scholar
Seeber, F., Limenitakis, J. and Soldati-Favre, D. (2008). Apicomplexan mitochondrial metabolism: a story of gains, losses and retentions. Trends in Parasitology 24, 468–478.Google Scholar
Shiomi, K., Hatae, K., Hatano, H., Matsumoto, A., Takahashi, Y., Jiang, C. L., Tomoda, H., Kobayashi, S., Tanaka, H. and Omura, S. (2005). A new antibiotic, antimycin Ag, produced by Streptomyces sp. K01–0031. Journal of Antibiotics (Tokyo) 58, 74–78.Google Scholar
Siedow, J. N. and Girvin, M. E. (1980). Alternative respiratory pathway. Its role in seed respiration and its inhibition by propyl gallate. Plant Physiology 65, 669–674.Google Scholar
Sierra-Campos, E., Valdez-Solana, M. A., Matuz-Mares, D., Velázquez, I. and Pardo, J. P. (2009). Induction of morphological changes in Ustilago maydis cells by octyl gallate. Microbiology 155, 604–611.Google Scholar
Sircar, D., Cardoso, H. G., Mukherjee, C., Mitra, A. and Arnholdt-Schmitt, B. (2012). Alternative oxidase (AOX) and phenolic metabolism in methyl jasmonate-treated hairy root cultures of Daucus carota L. Journal of Plant Physiology 169, 657–663.Google Scholar
Skutnik, M. and Rychter, A. M. (2009). Differential response of antioxidant systems in leaves and roots of barley subjected to anoxia and post-anoxia. Journal of Plant Physiology 166, 926–937.Google Scholar
Sterud, E., Hansen, M. K. and Mo, T. A. (2000). Systemic infection with Uronema-like ciliates in farmed turbot, Scophthalmus maximus (L.). Journal of Fish Diseases 23, 33–37.Google Scholar
Suski, J. M., Lebiedzinska, M., Bonora, M., Pinton, P., Duszynski, J. and Wieckowski, M. R. (2012). Relation between mitochondrial membrane potential and ROS formation. Methods in Molecular Biology 810, 183–205.Google Scholar
Tamura, H., Mizutani, A., Yukioka, H., Miki, N., Ohba, H. and Masuko, M. (1999). Effect of the methoxyiminoacetamide fungicide, SSF129, on respiratory activity in Botrytis cinerea . Pesticide Science 55, 681–686.Google Scholar
Vanlerberghe, G. C. (2013). Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. International Journal of Molecular Science 14, 6805–6847.Google Scholar
Vanlerberghe, G. C. and McIntosh, L. (1994). Mitochondrial electron transport regulation of nuclear gene expression: studies with the alternative oxidase gene of tobacco. Plant Physiology 105, 867–874.Google Scholar
Vanlerberghe, G. C. and McIntosh, L. (1997). Alternative oxidase: from gene to function. Annual Review of Plant Physiology and Plant Molecular Biology 48, 703–734.CrossRefGoogle ScholarPubMed
Walker, R. Jr, Saha, L., Hill, G. C. and Chaudhuri, M. (2005). The effect of over-expression of the alternative oxidase in the procyclic forms of Typanosoma brucei . Molecular and Biochemical Parasitology 139, 153–162.Google Scholar
Williams, B. A. P., Elliot, C., Burri, L., Kido, Y., Kita, K., Moore, A. L. and Keeling, P. J. (2010). A broad distribution of the alternative oxidase in microsporidian parasites. PloS Pathogens 6, e1000761.Google Scholar
Williamson, C. L., Dabkowsk, E. R., Dillmann, W. H. and Hollander, J. M. (2008). Mitochondria protection from hypoxia/reoxygenation injury with mitochondria heat shock protein 70 over-expression. American Journal of Physiology and Heart Circulation 294, H249–H256.Google Scholar
Woyda-Ploszczyca, A., Sluse, F. E. and Jarmuskiewicz, W. (2009). Regulation of Acanthamoeba castellanii alternative oxidase activity by mutual exclusion of purine nucleotides; ATP's inhibitory effect. Biochimica et Biophysica Acta 1787, 264–271.CrossRefGoogle ScholarPubMed
Woyda-Ploszczyca, A., Koziel, A., Antos-Krzeminska, N. and Jarmuskiewicz, W. (2011). Impact of oxidative stress on Acanthamoeba castellanii mitochondrial bioenergetics depends on cell growth stage. Journal of Bioenergetics and Biomembranes 43, 217–225.Google Scholar
Yoshinaga, T. and Nakazoe, J. (1993). Isolation and in vitro cultivation of an unidentified ciliate causing scuticocilatosis in Japanese flounder (Paralichthys olivaceus). Gyobyo Kenkyu 28, 131–134.Google Scholar
Young, P. G. (1983). The SHAM-sensitive alternative oxidase in Tetrahymena pyriformis: activity as a function of growth state and chloramphenicol treatment. Journal of General Microbiology 129, 1357–1363.Google Scholar
Young, I. S. and Woodside, J. V. (2001). Antioxidants in health and disease. Journal of Clinical Pathology 54, 176–186.Google Scholar
Zini, R., Morin, C., Bertelli, A. A. and Tillement, J. P. (1999). Effects of resveratrol on the rat brain respiratory chain. Drugs under Experimental and Clinical Research 25, 87–97.Google Scholar