Differences in mitochondrial NADH dehydrogenase activities in trypanosomatids

. 2021 Sep ; 148 (10) : 1161-1170. [epub] 20210107

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33407966

Complex I (NADH dehydrogenase) is the first enzyme in the respiratory chain. It catalyses the electron transfer from NADH to ubiquinone that is associated with proton pumping out of the matrix. In this study, we characterized NADH dehydrogenase activity in seven monoxenous trypanosomatid species: Blechomonas ayalai, Herpetomonas tarakana, Kentomonas sorsogonicus, Leptomonas seymouri, Novymonas esmeraldas, Sergeia podlipaevi and Wallacemonas raviniae. We also investigated the subunit composition of the complex I in dixenous Phytomonas serpens, in which its presence and activity have been previously documented. In addition to P. serpens, the complex I is functionally active in N. esmeraldas and S. podlipaevi. We also identified 24-32 subunits of the complex I in individual species by using mass spectrometry. Among them, for the first time, we recognized several proteins of the mitochondrial DNA origin.

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Abdrakhmanova A, Zickermann V, Bostina M, Radermacher M, Schagger H, Kerscher S and Brandt U (2004) Subunit composition of mitochondrial complex I from the yeast Yarrowia lipolytica. Biochimica et Biophysica Acta 1658, 148–156. PubMed

Acestor N, Zíková A, Dalley RA, Anupama A, Panigrahi AK and Stuart KD (2011) Trypanosoma brucei mitochondrial respiratome: composition and organization in procyclic form. Molecular and Cellular Proteomics 10, M110006908. PubMed PMC

Angerer H, Nasiri HR, Niedergesass V, Kerscher S, Schwalbe H and Brandt U (2012) Tracing the tail of ubiquinone in mitochondrial complex I. Biochimica et Biophysica Acta 1817, 1776–1784. PubMed

Aslett M, Aurrecoechea C, Berriman M, Brestelli J, Brunk BP, Carrington M, Depledge DP, Fischer S, Gajria B, Gao X, Gardner MJ, Gingle A, Grant G, Harb OS, Heiges M, Hertz-Fowler C, Houston R, Innamorato F, Iodice J, Kissinger JC, Kraemer E, Li W, Logan FJ, Miller JA, Mitra S, Myler PJ, Nayak V, Pennington C, Phan I, Pinney DF, Ramasamy G, Rogers MB, Roos DS, Ross C, Sivam D, Smith DF, Srinivasamoorthy G, Stoeckert CJ Jr, Subramanian S, Thibodeau R, Tivey A, Treatman C, Velarde G and Wang H (2010) TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Research 38, D457–D462. PubMed PMC

Beattie DS and Howton MM (1996) The presence of rotenone-sensitive NADH dehydrogenase in the long slender bloodstream and the procyclic forms of Trypanosoma brucei brucei. European Journal of Biochemistry 241, 888–894. PubMed

Berrisford JM and Sazanov LA (2009) Structural basis for the mechanism of respiratory complex I. Journal of Biological Chemistry 284, 29773–29783. PubMed PMC

Blum B and Simpson L (1990) Guide RNAs in kinetoplastid mitochondria have a nonencoded 3' oligo(U) tail involved in recognition of the preedited region. Cell 62, 391–397. PubMed

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254. PubMed

Brandt U (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annual Review of Biochemistry 75, 69–92. PubMed

Brandt U (2013) Inside view of a giant proton pump. Angewandte Chemie 52, 7358–7360. PubMed

Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K and Madden TL (2009) BLAST+: architecture and applications. BMC Bioinformatics 10, 421. PubMed PMC

Carranza JC, Kowaltowski AJ, Mendonca MA, de Oliveira TC, Gadelha FR and Zingales B (2009) Mitochondrial bioenergetics and redox state are unaltered in Trypanosoma cruzi isolates with compromised mitochondrial complex I subunit genes. Journal of Bioenergetics and Biomembranes 41, 299–308. PubMed

Carroll J, Fearnley IM, Skehel JM, Shannon RJ, Hirst J and Walker JE (2006) Bovine complex I is a complex of 45 different subunits. Journal of Biological Chemistry 281, 32724–32727. PubMed

Čermáková P, Verner Z, Man P, Lukeš J and Horváth A (2007) Characterization of the NADH:ubiquinone oxidoreductase (complex I) in the trypanosomatid Phytomonas serpens (Kinetoplastida). FEBS Journal 274, 3150–3158. PubMed

Čermáková P, Kovalinka T, Ferenczyová K and Horváth A (2019) Coenzyme Q2 is a universal substrate for the measurement of respiratory chain enzyme activities in trypanosomatids. Parasite 26, 17. PubMed PMC

Chomyn A, Mariottini P, Cleeter MW, Ragan CI, Matsuno-Yagi A, Hatefi Y, Doolittle RF and Attardi G (1985) Six unidentified reading frames of human mitochondrial DNA encode components of the respiratory-chain NADH dehydrogenase. Nature 314, 592–597. PubMed

Coustou V, Besteiro S, Rivière L, Biran M, Biteau N, Franconi JM, Boshart M, Baltz T and Bringaud F (2005) A mitochondrial NADH-dependent fumarate reductase involved in the production of succinate excreted by procyclic Trypanosoma brucei. Journal of Biological Chemistry 280, 16559–16570. PubMed

Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV and Mann M (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. Journal of Proteome Research 10, 1794–1805. PubMed

Degli Esposti M (1998) Inhibitors of NADH-ubiquinone reductase: an overview. Biochimica et Biophysica Acta 1364, 222–235. PubMed

Denicola-Seoane A, Rubbo H, Prodanov E and Turrens JF (1992) Succinate-dependent metabolism in Trypanosoma cruzi epimastigotes. Molecular and Biochemical Parasitology 54, 43–50. PubMed

Duarte M and Tomás AM (2014) The mitochondrial complex I of trypanosomatids – an overview of current knowledge. Journal of Bioenergetics and Biomembranes 46, 299–311. PubMed

Fang J and Beattie DS (2002) Novel FMN-containing rotenone-insensitive NADH dehydrogenase from Trypanosoma brucei mitochondria: isolation and characterization. Biochemistry 41, 3065–3072. PubMed

Fang J, Wang Y and Beattie DS (2001) Isolation and characterization of complex I, rotenone-sensitive NADH: ubiquinone oxidoreductase, from the procyclic forms of Trypanosoma brucei. European Journal of Biochemistry 268, 3075–3082. PubMed

Gabaldón T, Rainey D and Huynen MA (2005) Tracing the evolution of a large protein complex in the eukaryotes, NADH:ubiquinone oxidoreductase (complex I). Journal of Molecular Biology 348, 857–870. PubMed

Gonzalez-Halphen D and Maslov DA (2004) NADH-ubiquinone oxidoreductase activity in the kinetoplasts of the plant trypanosomatid Phytomonas serpens. Parasitology Research 92, 341–346. PubMed

Grba DN and Hirst J (2020) Mitochondrial complex I structure reveals ordered water molecules for catalysis and proton translocation. Nature Structural & Molecular Biology 27, 892–900. PubMed PMC

Grybchuk D, Akopyants NS, Kostygov AY, Konovalovas A, Lye LF, Dobson DE, Zangger H, Fasel N, Butenko A, Frolov AO, Votýpka J, d'Avila-Levy CM, Kulich P, Moravcová J, Plevka P, Rogozin IB, Serva S, Lukeš J, Beverley SM and Yurchenko V (2018a) Viral discovery and diversity in trypanosomatid protozoa with a focus on relatives of the human parasite Leishmania. Proceedings of the National Academy of Sciences of the United States of America 115, E506–E515. PubMed PMC

Grybchuk D, Kostygov AY, Macedo DH, Votypka J, Lukes J and Yurchenko V (2018b) RNA viruses in Blechomonas (Trypanosomatidae) and evolution of Leishmaniavirus. MBio 9, e01932–e01918. PubMed PMC

Hernandez FR and Turrens JF (1998) Rotenone at high concentrations inhibits NADH-fumarate reductase and the mitochondrial respiratory chain of Trypanosoma brucei and T. cruzi. Molecular and Biochemical Parasitology 93, 135–137. PubMed

Horváth A, Berry EA and Maslov DA (2000a) Translation of the edited mRNA for cytochrome b in trypanosome mitochondria. Science (New York, N.Y.) 287, 1639–1640. PubMed

Horváth A, Kingan TG and Maslov DA (2000b) Detection of the mitochondrially encoded cytochrome c oxidase subunit I in the trypanosomatid protozoan Leishmania tarentolae. Evidence for translation of unedited mRNA in the kinetoplast. Journal of Biological Chemistry 275, 17160–17165. PubMed

Horváth A, Nebohacova M, Lukeš J and Maslov DA (2002) Unusual polypeptide synthesis in the kinetoplast-mitochondria from Leishmania tarentolae. Identification of individual de novo translation products. Journal of Biological Chemistry 277, 7222–7230. PubMed

Horváth A, Horáková E, Dunajčíková P, Verner Z, Pravdová E, Šlapetová I, Cuninková L and Lukeš J (2005) Downregulation of the nuclear-encoded subunits of the complexes III and IV disrupts their respective complexes but not complex I in procyclic Trypanosoma brucei. Molecular Microbiology 58, 116–130. PubMed

Janssen RJ, Nijtmans LG, van den Heuvel LP and Smeitink JA (2006) Mitochondrial complex I: structure, function and pathology. Journal of Inherited Metabolic Disease 29, 499–515. PubMed

Kampjut D and Sazanov LA (2020) The coupling mechanism of mammalian respiratory complex I. Science (New York, N.Y.) 370, eabc4209. PubMed

Kmita K and Zickermann V (2013) Accessory subunits of mitochondrial complex I. Biochemical Society Transactions 41, 1272–1279. PubMed

Kostygov AY and Yurchenko V (2017) Revised classification of the subfamily Leishmaniinae (Trypanosomatidae). Folia Parasitologica 64, 020. PubMed

Kostygov AY, Grybchuk-Ieremenko A, Malysheva MN, Frolov AO and Yurchenko V (2014) Molecular revision of the genus Wallaceina. Protist 165, 594–604. PubMed

Kostygov A, Dobáková E, Grybchuk-Ieremenko A, Váhala D, Maslov DA, Votýpka J, Lukeš J and Yurchenko V (2016) Novel trypanosomatid – bacterium association: evolution of endosymbiosis in action. MBio 7, e01985–e01915. PubMed PMC

Kostygov AY, Butenko A, Nenarokova A, Tashyreva D, Flegontov P, Lukeš J and Yurchenko V (2017) Genome of Ca. Pandoraea novymonadis, an endosymbiotic bacterium of the trypanosomatid Novymonas esmeraldas. Frontiers in Microbiology 8, 1940. PubMed PMC

Kraeva N, Butenko A, Hlaváčová J, Kostygov A, Myškova J, Grybchuk D, Leštinová T, Votýpka J, Volf P, Opperdoes F, Flegontov P, Lukeš J and Yurchenko V (2015) Leptomonas seymouri: adaptations to the dixenous life cycle analyzed by genome sequencing, transcriptome profiling and co-infection with Leishmania donovani. PLoS Pathogens 11, e1005127. PubMed PMC

Lukeš J, Paris Z, Regmi S, Breitling R, Mureev S, Kushnir S, Pyatkov K, Jirků M and Alexandrov K (2006) Translational initiation in Leishmania tarentolae and Phytomonas serpens (Kinetoplastida) is strongly influenced by pre-ATG triplet and its 5' sequence context. Molecular and Biochemical Parasitology 148, 125–132. PubMed

Lukeš J, Butenko A, Hashimi H, Maslov DA, Votýpka J and Yurchenko V (2018) Trypanosomatids are much more than just trypanosomes: clues from the expanded family tree. Trends in Parasitology 34, 466–480. PubMed

Maslov DA, Zíková A, Kyselová I and Lukeš J (2002) A putative novel nuclear-encoded subunit of the cytochrome c Oxidase complex in trypanosomatids. Molecular and Biochemical Parasitology 125, 113–125. PubMed

Maslov DA, Opperdoes FR, Kostygov AY, Hashimi H, Lukeš J and Yurchenko V (2019) Recent advances in trypanosomatid research: genome organization, expression, metabolism, taxonomy and evolution. Parasitology 146, 1–27. PubMed

Matus-Ortega MG, Salmeron-Santiago KG, Flores-Herrera O, Guerra-Sanchez G, Martinez F, Rendon JL and Pardo JP (2011) The alternative NADH dehydrogenase is present in mitochondria of some animal taxa. Comparative Biochemistry and Physiology. Part D, Genomics & Proteomics 6, 256–263. PubMed

Michalski A, Damoc E, Lange O, Denisov E, Nolting D, Muller M, Viner R, Schwartz J, Remes P, Belford M, Dunyach JJ, Cox J, Horning S, Mann M and Makarov A (2012) Ultra high resolution linear ion trap Orbitrap mass spectrometer (Orbitrap Elite) facilitates top down LC MS/MS and versatile peptide fragmentation modes. Molecular and Cellular Proteomics 11, O111 013698. PubMed PMC

Moyses DN and Barrabin H (2004) Rotenone-sensitive mitochondrial potential in Phytomonas serpens: electrophoretic Ca2+ accumulation. Biochimica et Biophysica Acta 1656, 96–103. PubMed

Nawathean P and Maslov DA (2000) The absence of genes for cytochrome c oxidase and reductase subunits in maxicircle kinetoplast DNA of the respiration-deficient plant trypanosomatid Phytomonas serpens. Current Genetics 38, 95–103. PubMed

Okun JG, Lummen P and Brandt U (1999) Three classes of inhibitors share a common binding domain in mitochondrial complex I (NADH:ubiquinone oxidoreductase). Journal of Biological Chemistry 274, 2625–2630. PubMed

Opperdoes FR and Michels PA (2008) Complex I of Trypanosomatidae: does it exist? Trends in Parasitology 24, 310–317. PubMed

Opperdoes FR, Butenko A, Flegontov P, Yurchenko V and Lukeš J (2016) Comparative metabolism of free-living Bodo saltans and parasitic trypanosomatids. Journal of Eukaryotic Microbiology 63, 657–678. PubMed

Overkamp KM, Bakker BM, Kotter P, van Tuijl A, de Vries S, van Dijken JP and Pronk JT (2000) In vivo Analysis of the mechanisms for oxidation of cytosolic NADH by Saccharomyces cerevisiae mitochondria. Journal of Bacteriology 182, 2823–2830. PubMed PMC

Panigrahi AK, Ziková A, Dalley RA, Acestor N, Ogata Y, Anupama A, Myler PJ and Stuart KD (2008) Mitochondrial complexes in Trypanosoma brucei: a novel complex and a unique oxidoreductase complex. Molecular and Cellular Proteomics 7, 534–545. PubMed

Pereira B, Videira A and Duarte M (2013) Novel insights into the role of Neurospora crassa NDUFAF2, an evolutionarily conserved mitochondrial complex I assembly factor. Molecular and Cellular Biology 33, 2623–2634. PubMed PMC

Perez E, Lapaille M, Degand H, Cilibrasi L, Villavicencio-Queijeiro A, Morsomme P, Gonzalez-Halphen D, Field MC, Remacle C, Baurain D and Cardol P (2014) The mitochondrial respiratory chain of the secondary green alga Euglena gracilis shares many additional subunits with parasitic Trypanosomatidae. Mitochondrion 19, 338–349. PubMed

Schnaufer A, Domingo GJ and Stuart K (2002) Natural and induced dyskinetoplastic trypanosomatids: how to live without mitochondrial DNA. International Journal for Parasitology 32, 1071–1084. PubMed

Shevchenko A, Tomas H, Havlis J, Olsen JV and Mann M (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nature Protocols 1, 2856–2860. PubMed

Silva FM, Kostygov AY, Spodareva VV, Butenko A, Tossou R, Lukes J, Yurchenko V and Alves JMP (2018) The reduced genome of Candidatus Kinetoplastibacterium sorsogonicusi, the endosymbiont of Kentomonas sorsogonicus (Trypanosomatidae): loss of the haem-synthesis pathway. Parasitology 145, 1287–1293. doi: 10.1017/S003118201800046X. PubMed DOI

Simpson L, Wang SH, Thiemann OH, Alfonzo JD, Maslov DA and Avila HA (1998) U-insertion/deletion edited sequence database. Nucleic Acids Research 26, 170–176. PubMed PMC

Škodová-Sveráková I, Horváth A and Maslov DA (2015a) Identification of the mitochondrially encoded subunit 6 of F1FO ATPase in Trypanosoma brucei. Molecular and Biochemical Parasitology 201, 135–138. PubMed PMC

Škodová-Sveráková I, Verner Z, Skalický T, Votýpka J, Horváth A and Lukeš J (2015b) Lineage-specific activities of a multipotent mitochondrion of trypanosomatid flagellates. Molecular Microbiology 96, 55–67. PubMed

Sloof P, Arts GJ, van den Burg J, van der Spek H and Benne R (1994) RNA editing in mitochondria of cultured trypanosomatids: translatable mRNAs for NADH-dehydrogenase subunits are missing. Journal of Bioenergetics and Biomembranes 26, 193–203. PubMed

Stroud DA, Surgenor EE, Formosa LE, Reljic B, Frazier AE, Dibley MG, Osellame LD, Stait T, Beilharz TH, Thorburn DR, Salim A and Ryan MT (2016) Accessory subunits are integral for assembly and function of human mitochondrial complex I. Nature 538, 123–126. PubMed

Surve S, Heestand M, Panicucci B, Schnaufer A and Parsons M (2012) Enigmatic presence of mitochondrial complex I in Trypanosoma brucei bloodstream forms. Eukaryotic Cell 11, 183–193. PubMed PMC

Surve SV, Jensen BC, Heestand M, Mazet M, Smith TK, Bringaud F, Parsons M and Schnaufer A (2017) NADH dehydrogenase of Trypanosoma brucei is important for efficient acetate production in bloodstream forms. Molecular and Biochemical Parasitology 211, 57–61. PubMed PMC

Svobodová M, Zídková L, Čepička I, Oborník M, Lukeš J and Votýpka J (2007) Sergeia podlipaevi gen. nov., sp. nov. (Trypanosomatidae, Kinetoplastida), a parasite of biting midges (Ceratopogonidae, Diptera). International Journal of Systematic and Evolutionary Microbiology 57, 423–432. PubMed

Thiemann OH, Maslov DA and Simpson L (1994) Disruption of RNA editing in Leishmania tarentolae by the loss of minicircle-encoded guide RNA genes. EMBO Journal 13, 5689–5700. PubMed PMC

Tocilescu MA, Fendel U, Zwicker K, Drose S, Kerscher S and Brandt U (2010) The role of a conserved tyrosine in the 49-kDa subunit of complex I for ubiquinone binding and reduction. Biochimica et Biophysica Acta 1797, 625–632. PubMed

Turrens JF (1989) The role of succinate in the respiratory chain of Trypanosoma brucei procyclic trypomastigotes. Biochemical Journal 259, 363–368. PubMed PMC

Verner Z, Čermáková P, Škodová I, Kriegová E, Horváth A and Lukeš J (2011) Complex I (NADH:ubiquinone oxidoreductase) is active in but non-essential for procyclic Trypanosoma brucei. Molecular and Biochemical Parasitology 175, 196–200. PubMed

Verner Z, Škodová I, Poláková S, Ďurišová-Benkovičová V, Horváth A and Lukeš J (2013) Alternative NADH dehydrogenase (NDH2): intermembrane-space-facing counterpart of mitochondrial complex I in the procyclic Trypanosoma brucei. Parasitology 140, 328–337. PubMed

Verner Z, Čermáková P, Škodová I, Kováčová B, Lukeš J and Horváth A (2014) Comparative analysis of respiratory chain and oxidative phosphorylation in Leishmania tarentolae, Crithidia fasciculata, Phytomonas serpens and procyclic stage of Trypanosoma brucei. Molecular and Biochemical Parasitology 193, 55–65. PubMed

Votýpka J, Suková E, Kraeva N, Ishemgulova A, Duží I, Lukeš J and Yurchenko V (2013) Diversity of trypanosomatids (Kinetoplastea: Trypanosomatidae) parasitizing fleas (Insecta: Siphonaptera) and description of a new genus Blechomonas Gen. n. Protist 164, 763–781. PubMed

Votýpka J, Kostygov AY, Kraeva N, Grybchuk-Ieremenko A, Tesařová M, Grybchuk D, Lukeš J and Yurchenko V (2014) Kentomonas Gen. n., a new genus of endosymbiont-containing trypanosomatids of Strigomonadinae subfam. n. Protist 165, 825–838. PubMed

Walker JE, Arizmendi JM, Dupuis A, Fearnley IM, Finel M, Medd SM, Pilkington SJ, Runswick MJ and Skehel JM (1992) Sequences of 20 subunits of NADH:ubiquinone oxidoreductase from bovine heart mitochondria. Application of a novel strategy for sequencing proteins using the polymerase chain reaction. Journal of Molecular Biology 226, 1051–1072. PubMed

Wallace FG (1977) Leptomonas seymouri sp. n. from the cotton stainer Dysdercus suturellus. The Journal of Protozoology 24, 483–484. PubMed

Wittig I, Karas M and Schagger H (2007) High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Molecular and Cellular Proteomics 6, 1215–1225. PubMed

Yagi T and Matsuno-Yagi A (2003) The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked. Biochemistry 42, 2266–2274. PubMed

Yurchenko V, Kostygov A, Havlová J, Grybchuk-Ieremenko A, Ševčíková T, Lukeš J, Ševčík J and Votýpka J (2016) Diversity of trypanosomatids in cockroaches and the description of Herpetomonas tarakana sp. n. Journal of Eukaryotic Microbiology 63, 198–209. PubMed

Zerbetto E, Vergani L and Dabbeni-Sala F (1997) Quantification of muscle mitochondrial oxidative phosphorylation enzymes via histochemical staining of blue native polyacrylamide gels. Electrophoresis 18, 2059–2064. PubMed

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