medigraphic.com
ISSN 2395-8723 (Electronic)
ISSN 1405-888X (Print)
TIP Revista Especializada en Ciencias Químico-Biológicas

2022, Number 1

<< Back Next >>

TIP Rev Esp Cienc Quim Biol 2022; 25 (1)

The alternative oxidase, a metalloprotein conserved in fungi

Romero-Aguilar L, Luqueño-Bocardo OI, Guerra-Sánchez G, Matus-Ortega G, Pardo JP

Language: Spanish
References: 48
Page: 1-11
PDF size: 805.71 Kb.


ABSTRACT

The alternative oxidase (AOX) is a monotopic metalloprotein attached to the inner surface of the inner mitochondrial membrane. This enzyme catalyzes the transfer of electrons from ubiquinol to oxygen, with the production of water. When the cytochrome pathway is inhibited by cyanide or other xenobiotic molecules, the AOX allows the flux of electrons from NADH to oxygen and thus, the catabolic and anabolic activity of the Krebs cycle. The AOX is found in plants, fungi, some protists and a few primitive metazoans. It has been proposed that this enzyme has important roles in the response against osmotic and oxidative stresses. In this review, we analyze the structure of the enzyme, address its participation in the responses of fungi to osmotic stress and analyze the influence of AOX on ATP synthesis.


REFERENCES

  1. Albury, M. S., Elliott, C. & Moore, A. L. (2009). Towards astructural elucidation of the alternative oxidase in plants.Physiologia Plantarum, 137(4), 316–327. https://doi.org/10.1111/j.1399-3054.2009.01270.x

  2. Albury, M. S., Elliott, C. & Moore, A. L. (2010). Ubiquinolbindingsite in the alternative oxidase: Mutagenesis revealsfeatures important for substrate binding and inhibition.Biochimica. Biophysica Acta, 1797(12), 1933–1939. https://doi.org/10.1016/j.bbabio..2010.01.013

  3. Atteia, A., van Lis, R., van Hellemond, J. J., Tielens, A. G.M., Martin, W. & Henze, K. (2004). Identification ofprokaryotic homologues indicates an endosymbiotic originfor the alternative oxidases of mitochondria (AOX) andchloroplasts (PTOX). Gene, 330, 143–148. https://doi.org/10.1016/j.gene.2004.01.015

  4. Avila-Adame, C. & Köller, W. (2002). Disruption of thealternative oxidase gene in Magnaporthe grisea andits impact on host infection. Molecular Plant-MicrobeInteractions: MPMI, 15(5), 493–500. https://doi.org/10.1094/MPMI.2002.15.5.493

  5. Berthold, D. A., Andersson, M. E. & Nordlund, P. (2000). Newinsight into the structure and function of the alternativeoxidase. Biochimica. Biophysica Acta, 1460(2–3), 241–254.https://doi.org/10.1016/s0005-2728(00)00149-3

  6. Bosnjak, N., Smith, K. M., Asaria, I., Lahola-Chomiak, A.,Kishore, N., Todd, A. T., Freitag, M. & Nargang, F. E.(2019). Involvement of a G Protein Regulatory Circuit inAlternative Oxidase Production in Neurospora crassa. G3(Bethesda, Md.), 9(10), 3453–3465. https://doi.org/10.1534/g3.119.400522

  7. Cárdenas-Monroy, C. A., Pohlmann, T., Piñón-Zárate, G.,Matus-Ortega, G., Guerra, G., Feldbrügge, M. & Pardo,J. P. (2017). The mitochondrial alternative oxidase Aox1is needed to cope with respiratory stress but dispensablefor pathogenic development in Ustilago maydis. PLOSONE, 12(3), e0173389. https://doi.org/10.1371/journal.pone.0173389

  8. Chae, M. S., Lin, C. C., Kessler, K. E., Nargang, C. E., Tanton,L. L., Hahn, L. B. & Nargang, F. E. (2007). Identification ofan alternative oxidase induction motif in the promoter regionof the aod-1 gene in Neurospora crassa. Genetics, 175(4),1597–1606. https://doi.org/10.1534/genetics.106.068635

  9. Chaudhuri, M., Ott, R. D. & Hill, G. C. (2006). Trypanosomealternative oxidase: From molecule to function. Trends inparasitology, 22(10), 484–491. https://doi.org/10.1016/j.pt.2006.08.007

  10. Costa-de-Oliveira, S., Sampaio-Marques, B., Barbosa, M.,Ricardo, E., Pina-Vaz, C., Ludovico, P. & Rodrigues, A.G. (2012). An alternative respiratory pathway on Candidakrusei: Implications on susceptibility profile and oxidativestress. FEMS Yeast Research, 12(4), 423–429. https://doi.org/10.1111/j.1567-1364.2012.00789.x

  11. Delano, W. (2004). Use of PyMOL as a communications toolfor molecular science. Abstracts of Papers of the AmericanChemical Society, Amer. Chemical Soc., 16th St, NWWashington, DC, Volume 228, p. U228–U230.

  12. Descheneau, A. T., Cleary, I. A. & Nargang, F. E. (2005). GeneticEvidence for a Regulatory Pathway Controlling AlternativeOxidase Production in Neurosporacrassa. Genetics, 169(1),123–135. https://doi.org/10.1534/genetics.104.034017

  13. Dunn, A. K. (2018). Alternative Oxidase Activity ReducesStress in Vibrio fischeri Cells Exposed to Nitric Oxide.Journal of Bacteriologists, 200(15), e00797-17. https://doi.org/10.1128/JB.00797-17

  14. Ebiloma, G. U., Balogun, E. O., Cueto-Díaz, E. J., de Koning, H.P. & Dardonville, C. (2019). Alternative oxidase inhibitors:Mitochondrion-targeting as a strategy for new drugsagainst pathogenic parasites and fungi. Medicinal ResearchReviews, 39(5), 1553–1602. DOI:10.1002/med.21560.

  15. García, J. J., Morales-Ríos, E., Cortés-Hernandez, P. &Rodríguez-Zavala, J. S. (2006). The inhibitor protein (IF1)promotes dimerization of the mitochondrial F1F0-ATPsynthase. Biochemistry, 45(42), 12695–12703. https://doi.org/10.1021/bi060339j

  16. Garcia-Neto, W., Cabrera-Orefice, A., Uribe-Carvajal, S.,Kowaltowski, A. J. & Alberto Luévano-Martínez, L. (2017).High Osmolarity Environments Activate the MitochondrialAlternative Oxidase in Debaryomyces hansenii. PLOSOne, 12(1), e0169621. https://doi.org/10.1371/journal.pone.0169621

  17. Grahl, N., Dinamarco, T. M., Willger, S. D., Goldman, G. H. &Cramer, R. A. (2012). Aspergillus fumigatus mitochondrialelectron transport chain mediates oxidative stresshomeostasis, hypoxia responses and fungal pathogenesis.Molecular Microbiology, 84(2), 383–399. https://doi.org/10.1111/j.1365-2958.2012.08034.x

  18. Kaye, Y., Huang, W., Clowez, S., Saroussi, S., Idoine, A., Sanz-Luque, E. & Grossman, A.R. (2019). The mitochondrialalternative oxidase from Chlamydomonas reinhardtiienables survival in high light. The Journal of BiologicalChemistry, 294(4), 1380–1395. https://doi.org/10.1074/jbc.RA118.004667.

  19. Grover, S. D. & Laties, G. G. (1981). Disulfiram inhibition ofthe alternative respiratory pathway in plant mitochondria.Plant Physiology, 68(2), 393–400. https://doi.org/10.1104/pp.68.2.393

  20. Johnson, K. L. (2019). Turning Up the Heat: The AlternativeOxidase Pathway Drives Thermogenesis in Cycad Cones.Plant Physiology, 180(2), 689–690. DOI:10.1104/pp.19.00443

  21. Juárez, O., Guerra, G., Martínez, F. & Pardo, J. P. (2004).The mitochondrial respiratory chain of Ustilago maydis.Biochimica Et Biophysica Acta, 1658(3), 244–251. https://doi.org/10.1016/j.bbabio.2004.06.005.

  22. Laskowski, R. A. & Swindells, M. B. (2011, October 5).LigPlot+: Multiple Ligand–Protein Interaction Diagramsfor Drug Discovery (world) [Product-review]. ACSPublications; American Chemical Society. https://doi.org/10.1021/ci200227u

  23. Li, Q., Ritzel, R. G., McLean, L. L., McIntosh, L., Ko, T.,Bertrand, H. & Nargang, F. E. (1996). Cloning and analysisof the alternative oxidase gene of Neurospora crassa.Genetics, 142(1), 129–140.

  24. Lin, Z., Wu, J., Jamieson, P. A. & Zhang, C. (2019).Alternative Oxidase Is Involved in the Pathogenicity,Development, and Oxygen Stress Response of Botrytiscinerea. Phytopathology, 109(10), 1679–1688. https://doi.org/10.1094/PHYTO-01-19-0012-R

  25. Martins, V. P., Dinamarco, T. M., Soriani, F. M., Tudella, V.G., Oliveira, S. C., Goldman, G. H., Curti, C. & Uyemura,S. A. (2011). Involvement of an alternative oxidase inoxidative stress and mycelium-to-yeast differentiationin Paracoccidioides brasiliensis. Eukaryot Cell, 10(2),237–248. https://doi.org/10.1128/EC.00194-10

  26. McDonald, A. E., Vanlerberghe, G. C. & Staples, J. F. (2009).Alternative oxidase in animals: Unique characteristicsand taxonomic distribution. J. Exp. Biol., 212(Pt 16),2627–2634. https://doi.org/10.1242/jeb.032151

  27. Medentsev, A. G. & Akimenko, V. K. (1999). Developmentand activation of cyanide-resistant respiration in the yeastYarrowia lipolytica. Biochemistry Biokhimiia, 64(8),945–951.

  28. Menzies, S.K., Tulloch, L.B., Florence, G. J. & Smith, T. K.(2018). The trypanosome alternative oxidase: a potentialdrug target? Parasitology, 145(2), 175-183. DOI: 10.1017/S0031182016002109.

  29. Moore, A. L., Shiba, T., Young, L., Harada, S., Kita, K. & Ito,K. (2013). Unraveling the heater: New insights into thestructure of the alternative oxidase. Annual Review of PlantBiology, 64, 637–663. https://doi.org/10.1146/annurevarplant-042811-105432

  30. Nargang, F. E., Adames, K., Rüb, C., Cheung, S., Easton, N.,Nargang, C. E. & Chae, M. S. (2012). Identification ofgenes required for alternative oxidase production in theNeurospora crassa gene knockout library. G3 (Bethesda,Md.), 2(11), 1345–1356. https://doi.org/10.1534/g3.112.004218

  31. Neimanis, K., Staples, J. F., Huner, N. P. & McDonald, A.E. (2013). Identification, expression, and taxonomicdistribution of alternative oxidases in non-angiospermplants. Gene, 526(2), 275–286. https://doi.org/10.1016/j.gene.2013.04.072

  32. Ordog, S. H., Higgins, V. J. & Vanlerberghe, G. C. (2002).Mitochondrial Alternative Oxidase Is Not a CriticalComponent of Plant Viral Resistance But May Play a Rolein the Hypersensitive Response. Plant Physiology, 129(4),1858–1865. https://doi.org/10.1104/pp.003855

  33. Petrovic, U. (2006). Role of oxidative stress in the extremelysalt-tolerant yeast Hortaea werneckii. FEMS YeastResearch, 6(5), 816–822. https://doi.org/10.1111/j.1567-1364.2006.00063.x

  34. PyMOL | pymol.org. (n.d.). Retrieved March 14, 2022, fromhttps://pymol.org/2/

  35. Qi, Z., Smith, K. M., Bredeweg, E. L., Bosnjak, N., Freitag, M.& Nargang, F. E. (2016). Alternative Oxidase TranscriptionFactors AOD2 and AOD5 of Neurospora crassa Control theExpression of Genes Involved in Energy Production andMetabolism. G3: Genes|Genomes|Genetics, 7(2), 449–466.https://doi.org/10.1534/g3.116.035402

  36. Romero-Aguilar, L., Cárdenas-Monroy, C., Garrido-Bazán, V.,Aguirre, J., Guerra-Sánchez, G. & Pardo, J. P. (2020). Onthe use of n-octyl gallate and salicylhydroxamic acid tostudy the alternative oxidase role. Archives of Biochemistryand Biophysics, 694, 108603. https://doi.org/10.1016/j.abb.2020.108603

  37. Saha, B., Borovskii, G. & Panda, S. K. (2016). Alternativeoxidase and plant stress tolerance. Plant Signaling &Behavior, 11(12), e1256530. https://doi.org/10.1080/15592324.2016.1256530

  38. Saisho, D., Nambara, E., Naito, S., Tsutsumi, N., Hirai, A.& Nakazono, M. (1997). Characterization of the genefamily for alternative oxidase from Arabidopsis thaliana.Plant Molecular Biology, 35(5), 585–596. https://doi.org/10.1023/A:1005818507743.

  39. Shiba, T., Kido, Y., Sakamoto, K., Inaoka, D. K., Tsuge, C.,Tatsumi, R., Takahashi, G., Balogun, E. O., Nara, T., Aoki,T., Honma, T., Tanaka, A., Inoue, M., Matsuoka, S., Saimoto,H., Moore, A. L., Harada, S. & Kita, K. (2013). Structureof the trypanosome cyanide-insensitive alternative oxidase.Proceedings of the National Academy of Sciences of theUnited States of America, 110(12), 4580–4585. https://doi.org/10.1073/pnas.1218386110

  40. Siedow, J. N. (2013). ATP Synthesis: Mitochondrial Cyanide-Resistant Terminal Oxidases. In W. J. Lennarz & M.D. Lane (Eds.), Encyclopedia of Biological Chemistry(Second Edition) (pp. 145–148). Academic Press. https://doi.org/10.1016/B978-0-12-378630-2.00285-1

  41. Tian, F., Lee, S. Y., Woo, S. Y. & Chun, H. S. (2020).Alternative Oxidase: A Potential Target for ControllingAflatoxin Contamination and Propagation of Aspergillusflavus. Frontiers in Microbiology, 11, 419. DOI:10.3389/fmicb.2020.00419

  42. Veiga, A., Arrabaca, J. D. & Loureiro-Dias, M. C. (2000).Cyanide-resistant respiration is frequent, but confinedto yeasts incapable of aerobic fermentation. FEMSMicrobiology Letters, 190(1), 93–97. https://doi.org/10.1111/j.1574-6968.2000.tb09268.x

  43. Veiga, A., Arrabaca, J. D. & Loureiro-Dias, M. C. (2003a). Stresssituations induce cyanide-resistant respiration in spoilageyeasts. Journal of Applied Microbiology, 95(2), 364–371.https://doi.org/10.1046/j.1365-2672.2003.01992.x

  44. Veiga, A., Arrabaca, J. D., Sansonetty, F., Ludovico, P., Corte-Real, M. & Loureiro-Dias, M. C. (2003). Energy conversioncoupled to cyanide-resistant respiration in the yeasts Pichiamembranifaciens and Debaryomyces hansenii. FEMS YeastResearch, 3(2), 141–148. https://doi.org/10.1016/S1567-1356(02)00189-7

  45. West, R. A., Cunningham, T., Pennicott, L. E., Rao, S. P. S. &Ward, S. E. (2018). Toward More Drug Like Inhibitors ofTrypanosome Alternative Oxidase. ACS Infectious Diseases,4(4), 592–604. https://doi.org/10.1021/acsinfecdis.7b00218

  46. Xu, T., Wang, Y.-T., Liang, W.-S., Yao, F., Li, Y.-H., Li,D.-R., Wang, H. & Wang, Z.-Y. (2013). Involvementof alternative oxidase in the regulation of sensitivity ofSclerotinia sclerotiorum to the fungicides azoxystrobin andprocymidone. Journal of Microbiology, 51(3), 352–358.https://doi.org/10.1007/s12275-013-2534-x

  47. Yan, L., Li, M., Cao, Y., Gao, P., Cao, Y., Wang, Y. & Jiang,Y. (2009). The alternative oxidase of Candida albicanscauses reduced fluconazole susceptibility. The Journal ofAntimicrobial Chemotherapy, 64(4), 764–773. https://doi.org/10.1093/jac/dkp273

  48. Zhu, Y., Lu, J., Wang, J., Chen, F., Leng, F. & Li, H. (2011).Regulation of thermogenesis in plants: The interaction ofalternative oxidase and plant uncoupling mitochondrialprotein. Journal of Integrative Plant Biology, 53(1), 7–13.




2020     |     www.medigraphic.com