[en] Subunit II of cytochrome c oxidase (Cox2) is usually encoded in the mitochondrial genome, synthesized in the organelle, inserted co-translationally into the inner mitochondrial membrane, and assembled into the respiratory complex. In chlorophycean algae however, the cox2 gene was split into the cox2a and cox2b genes, and in some algal species like Chlamydomonas reinhardtii and Polytomella sp. both fragmented genes migrated to the nucleus. The corresponding Cox2A and Cox2B subunits are imported into mitochondria forming a heterodimeric Cox2 subunit. When comparing the sequences of chlorophycean Cox2Aand Cox2B proteins with orthodox Cox2 subunits, a C-terminal extension in Cox2A and an N-terminal extension in Cox2B were identified. It was proposed that these extensions favor the Cox2A/Cox2B interaction. In vitro studies carried out in this work suggest that the removal of the Cox2B extension only partially affects binding of Cox2B to Cox2A.We conclude that this extension is dispensable, but when present it weakly reinforces the Cox2A/Cox2B interaction.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Jiménez-Suárez, Alejandra; Universidad Nacional Autónoma de México > Instituto de Fisiología Celular > Departamento de GenéticaMolecular
Vázquez-Acevedo, Miriam; Universidad Nacional Autónoma de México > Instituto de Fisiología Celular > Departamento de GenéticaMolecular
Miranda Astudillo, Héctor Vicente ; Universidad Nacional Autónoma de México > Instituto de Fisiología Celular > Departamento de GenéticaMolecular
González-Halphen, Diego; Universidad Nacional Autónoma de México > Instituto de Fisiología Celular > Departamento de GenéticaMolecular
Language :
English
Title :
Cox2A/Cox2B subunit interaction in Polytomella sp. cytochrome c oxidase: role of the Cox2B subunit extension
Publication date :
22 September 2017
Journal title :
Journal of Bioenergetics and Biomembranes
ISSN :
0145-479X
eISSN :
1573-6881
Publisher :
Kluwer Academic/Plenum Publishers, New York, United States - New York
Adams KL, Palmer JD (2003) Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogenet Evol 29:380–395. https://doi.org/10.1016/S1055-7903(03)00194-5
Adams KL, Song K, Roessler PG, Nugent JM, Doyle JL, Doyle JJ, Palmer JD (1999) Intracellular gene transfer in action: dual transcription and multiple silencings of nuclear and mitochondrial cox2 genes in legumes. Proc Natl Acad Sci U S A 96:13863–13868. https://doi.org/10.1073/pnas.96.24.13863
Adams KL, Ong HC, Palmer JD (2001) Mitochondrial Gene Transfer in Pieces: Fission of the Ribosomal Protein Gene rpl2 and Partial or Complete Gene Transfer to the Nucleus. Mol Biol Evol 18:2289–2297. https://doi.org/10.1093/oxfordjournals.molbev.a003775
Biasini M, Bienert S, Waterhouse A (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42:W252–W258. https://doi.org/10.1093/nar/gku340
Burgess RR (2009) Refolding solubilized inclusion body proteins. In: Burgess RR, Deutscher MP (eds) Methods in enzymology: Guide to protein purification, 2nd edn. Elsevier, New York, pp 259–282
Clarkson GH, Poyton RO (1989) A role for membrane potential in the biogenesis of cytochrome c oxidase subunit II, a mitochondrial gene product. J Biol Chem 264:10114–10118
Daley DO, Clifton R, Whelan J (2002) Intracellular gene transfer: reduced hydrophobicity facilitates gene transfer for subunit 2 of cytochrome c oxidase. Proc Natl Acad Sci U S A 99:10510–10515. https://doi.org/10.1073/pnas.122354399
Denovan-Wright EM, Nedelcu AM, Lee RW (1998) Complete sequence of the mitochondrial DNA of Chlamydomonas eugametos. Plant Mol Biol 36:285–295. https://doi.org/10.1023/A:1005995718091
Fan J, Lee RW (2002) Mitochondrial genome of the colorless green alga Polytomella parva: two linear DNA molecules with homologous inverted repeat termini. Mol Biol Evol 19:999–1007. https://doi.org/10.1093/oxfordjournals.molbev.a004180
Ferguson-Miller S, Hiser C, Liu J (2012) Gating and regulation of the cytochrome c oxidase proton pump. Biochim Biophys Acta 1817:489–494. https://doi.org/10.1016/j.bbabio.2011.11.018
Funes S, Davidson E, Claros MG, van Lis R, Pérez-Martinez X, Vázquez-Acevedo M, King MP, González-Halphen D (2002a) The typically mitochondrial DNA-encoded ATP6 subunit of the F1F0-ATPase is encoded by a nuclear gene in Chlamydomonas reinhardtii. J Biol Chem 277:6051–6058. https://doi.org/10.1074/jbc.M109993200
Funes S, Davidson E, Reyes-Prieto A, Magallón S, Herion P, King MP, González-Halphen D (2002b) A green algal apicoplast ancestor. Science 298:2155. https://doi.org/10.1126/science.1076003
González-Halphen D, Lindorfer MA, Capaldi RA (1988) Subunit arrangement in beef heart complex III. Biochemistry 27:7021–7031. https://doi.org/10.1021/bi00418a053
Hall RA (2004) Studying protein-protein interactions via blot overlay or Far Western blot. In: Fu H (ed) Protein-Protein Interaction: Methods and Applications. Humana Press, New Jersey, pp 167–174
Hamaji T, Smith DR, Noguchi H, Toyoda A, Suzuki M, Kawai-Toyooka H, Fujiyama A, Nishii I, Marriage T, Olson BJ, Nozaki H (2013) Mitochondrial and plastid genomes of the colonial green alga Gonium pectorale give insights into the origins of organelle DNA architecture within the volvocales. PLoS One 8:e57177. https://doi.org/10.1371/journal.pone.0057177
Jiménez-Suárez A, Vázquez-Acevedo M, Rojas-Hernández A, Funes S, Uribe-Carvajal S, González-Halphen D (2012) In Polytomella sp. mitochondria, biogenesis of the heterodimeric COX2 subunit of cytochrome c oxidase requires two different import pathways. Biochim Biophys Acta 1817:819–827. https://doi.org/10.1016/j.bbabio.2012.02.038
Markwell MAK, Hass SM, Bieber LL, Tolbert NE (1978) A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87:206–210. https://doi.org/10.1016/0003-2697(78)90586-9
Merchant SS, Prochnik SE, Vallon O et al (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–250. https://doi.org/10.1126/science.1143609
Miranda-Astudillo H, Cano-Estrada A, Vázquez-Acevedo M, Colina-Tenorio L, Downie-Velasco A, Cardol P, Remacle C, Domínguez-Ramírez L, González-Halphen D (2014) Interactions of subunits Asa2, Asa4 and Asa7 in the peripheral stalk of the mitochondrial ATP synthase of the chlorophycean alga Polytomella sp. Biochim Biophys Acta 1837:1–13. https://doi.org/10.1016/j.bbabio.2013.08.001
Pérez-Martínez X, Vázquez-Acevedo M, Tolkunova E, Funes S, Claros MG, Davidson E, King MP, González-Halphen D (2000) Unusual location of a mitochondrial gene. Subunit III of cytochrome c oxidase is encoded in the nucleus of Chlamydomonad algae. J Biol Chem 275:30144–30152. https://doi.org/10.1074/jbc.M003940200
Pérez-Martínez X, Antaramian A, Vázquez-Acevedo M, Funes S, Tolkunova E, d'Alayer J, Claros MG, Davidson E, King MP, González-Halphen D (2001) Subunit II of cytochrome c oxidase in Chlamydomonad algae is a heterodimer encoded by two independent nuclear genes. J Biol Chem 276:11302–11309. https://doi.org/10.1074/jbc.M010244200
Pérez-Martínez X, Funes S, Tolkunova E, Davidson E, King MP, González-Halphen D (2002) Structure of nuclear-localized cox3 genes in Chlamydomonas reinhardtii and in its colorless close relative Polytomella sp. Curr Genet 40:399–404. https://doi.org/10.1007/s00294-002-0270-6
Prochnik SE, Umen J, Nedelcu AM et al (2010) Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329:223–226. https://doi.org/10.1126/science.1188800
Rodríguez-Salinas E, Riveros-Rosas H, Li Z, Fucíková K, Brand JJ, Lewis LA, González-Halphen D (2012) Lineage-specific fragmentation and nuclear relocation of the mitochondrial cox2 gene in chlorophycean green algae (Chlorophyta). Mol Phylogenet Evol 64:166–176. https://doi.org/10.1016/j.ympev.2012.03.014
Schägger H (1994) Denaturing Electrophoretic Techniques. In: von Jagow G, Schägger H (eds) A Practical Guide to Membrane Protein Purification. Academic Press, San Diego, pp 59–79
Smith DR, Lee LW (2009) The mitochondrial and plastid genomes of Volvox carteri: bloated molecules rich in repetitive DNA. BMC Genomics 10:132. https://doi.org/10.1186/1471-2164-10-132
Smith DR, Lee RW, Cushman JC, Magnuson JK, Tran D, Polle JE (2010) The Dunaliella salina organelle genomes: large sequences, inflated with intronic and intergenic DNA. BMC Plant Biol 10:83. https://doi.org/10.1186/1471-2229-10-83
Soto IC, Fontanesi F, Liu J, Barrientos A (2012) Biogenesis and assembly of eukaryotic cytochrome c oxidase catalytic core. Biochim Biophys Acta 1817:883–897. https://doi.org/10.1016/j.bbabio.2011.09.005
Szafranski P (2017) Evolutionary recent, insertional fission of mitochondrial cox2 into complementary genes in bilaterian Metazoa. BMC Genomics 18:269. https://doi.org/10.1186/s12864-017-3626-5
Tovchigrechko A, Vakser IA (2006) GRAMM-X public web server for protein–protein docking. Nucleic Acids Res 34:W310–W314. https://doi.org/10.1093/nar/gkl206
Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76:4350–4354
Vahrenholz C, Riemen G, Pratje E, Dujon B, Michaelis G (1993) Mitochondrial DNA of Chlamydomonas reinhardtii: the structure of the ends of the linear 15.8-kb genome suggests mechanisms for DNA replication. Curr Genet 24:241–247. https://doi.org/10.1007/BF00351798
Wallace AC, Laskowski RA, Thornton JM (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8:127–134. https://doi.org/10.1093/protein/8.2.127
Watanabe KI, Ohama T (2001) Regular spliceosomal introns are invasive in Chlamydomonas reinhardtii: 15 introns in the recently relocated mitochondrial cox2 and cox3 genes. J Mol Evol 53:333–339. https://doi.org/10.1007/s002390010223
Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y (2015) The I-TASSER Suite: Protein structure and function prediction. Nat Methods 12:7–8. https://doi.org/10.1038/nmeth.3213
Yoshikawa S, Shinzawa-Itoh K, Nakashima R et al (1998) Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280:1723–1729. https://doi.org/10.1126/science.280.5370.1723
Yoshikawa S, Muramoto K, Shinzawa-Itoh K, Mochizuki M (2012) Structural studies on bovine heart cytochrome c oxidase. Biochim Biophys Acta 1817:579–589. https://doi.org/10.1016/j.bbabio.2011.12.012