Divergence of Erv1-associated mitochondrial import and export pathways in trypanosomes and anaerobic protists

Eukaryotic Cell

Volumn 12, Issue 2, 2013, Pages 343-355

  Basu, Somsuvro ^a   Leonard, Joanne C ^b   Desai, Nishal ^b   Mavridou, Despoina A I ^b   Tang, Kong Ho ^b   Goddard, Alan D ^b,d   Ginger, Michael L ^c   Lukeš, Julius ^a   Allen, James W A ^b  

^a UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c LANCASTER UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF LINCOLN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; MITOCHONDRIAL PROTEIN; OXIDIZING AGENT; OXIDOREDUCTASE; OXYGEN; PROTOZOAL PROTEIN; THIOL OXIDASE;

AMINO ACID SUBSTITUTION; ARTICLE; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; GENE SILENCING; GENETICS; KINETICS; MITOCHONDRION; MITOCHONDRION SWELLING; MOLECULAR EVOLUTION; OXIDATION REDUCTION REACTION; PHYLOGENY; PROTEIN FOLDING; PROTEIN TRANSPORT; RNA INTERFERENCE; SITE DIRECTED MUTAGENESIS; TRYPANOSOMA BRUCEI; ULTRASTRUCTURE;

AMINO ACID SUBSTITUTION; CYTOCHROMES C; EVOLUTION, MOLECULAR; GENE KNOCKDOWN TECHNIQUES; KINETICS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL SWELLING; MUTAGENESIS, SITE-DIRECTED; OXIDANTS; OXIDATION-REDUCTION; OXIDOREDUCTASES; OXYGEN; PHYLOGENY; PROTEIN FOLDING; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RNA INTERFERENCE; TRYPANOSOMA BRUCEI BRUCEI;

EID: 84873116001     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00304-12     Document Type: Article

References (73)

1. Herrmann JM, Riemer J. 2012. Mitochondrial disulfide relay: redoxregulated protein import into the intermembrane space. J. Biol. Chem. 287:4426-4433.
2. Lange H, Lisowsky T, Gerber J, Muhlenhoff U, Kispal G, Lill R. 2001. An essential function of the mitochondrial sulfhydryl oxidase Erv1p/ALR in the maturation of cytosolic Fe/S proteins. EMBO Rep. 2:715-720.
3. Lill R. 2009. Function and biogenesis of iron-sulphur proteins. Nature 460:831-838.
4. Netz DJ, Stumpfig M, Dore C, Muhlenhoff U, Pierik AJ, Lill R. 2010. Tah18 transfers electrons to Dre2 in cytosolic iron-sulfur protein biogenesis. Nat. Chem. Biol. 6:758-765.
5. Stehling O, Vashisht AA, Mascarenhas J, Jonsson ZO, Sharma T, Netz DJ, Pierik AJ, Wohlschlegel JA, Lill R. 2012. MMS19 assembles ironsulfur proteins required for DNA metabolism and genomic integrity. Science 337:195-199.
6. Allen JW, Ferguson SJ, Ginger ML. 2008. Distinctive biochemistry in the trypanosome mitochondrial intermembrane space suggests a model for stepwise evolution of the MIA pathway for import of cysteine-rich proteins. FEBS Lett. 582:2817-2825.
7. Carrie C, Murcha MW, Whelan J. 2010. An in silico analysis of the mitochondrial protein import apparatus of plants. BMC Plant Biol. 10:249. doi:10.1186/1471-2229-10-249.
8. Eckers E, Cyrklaff M, Simpson L, Deponte M. 2012. Mitochondrial protein import pathways are functionally conserved among eukaryotes despite compositional diversity of the import machineries. Biol. Chem. 393:513-524.
9. Harsman A, Niemann M, Pusnik M, Schmidt O, Burmann BM, Hiller S, Meisinger C, Schneider A, Wagner R. 2012. Bacterial origin of a mitochondrial outer membrane protein translocase: new perspectives from comparative single channel electrophysiology. J. Biol. Chem. 287: 31437-31445.
10. Pusnik M, Schmidt O, Perry AJ, Oeljeklaus S, Niemann M, Warscheid B, Lithgow T, Meisinger C, Schneider A. 2011. Mitochondrial preprotein translocase of trypanosomatids has a bacterial origin. Curr. Biol. 21:1738-1743.
11. Embley TM, Martin W. 2006. Eukaryotic evolution, changes and challenges. Nature 440:623-630.
12. Katz LA. 2012. Origin and diversification of eukaryotes. Annu. Rev. Microbiol. 66:411-427.
13. Hampl V, Hug L, Leigh JW, Dacks JB, Lang BF, Simpson AG, Roger AJ. 2009. Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic "supergroups. " Proc. Natl. Acad. Sci. U. S. A. 106:3859-3864.
14. Cavalier-Smith T. 2010. Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biol. Lett. 6:342-345.
15. Miroux B, Walker JE. 1996. Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels, J. Mol. Biol. 260:289-298.
16. Fulop V, Sam KA, Ferguson SJ, Ginger ML, Allen JW. 2009. Structure of a trypanosomatid mitochondrial cytochrome c with heme attached via only one thioether bond and implications for the substrate recognition requirements of heme lyase. FEBS J. 276:2822-2832.
17. Faeder EJ, Siegel LM. 1973. A rapid micromethod for determination of FMN and FAD in mixtures. Anal. Biochem. 53:332-336.
18. Wirtz E, Leal S, Ochatt C, Cross GA. 1999. A tightly regulated inducible expression system for conditional gene knock-outs and dominantnegative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99:89-101.
19. Brun R, Schonenberger M. 1979. Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Acta Trop. 36:289-292.
20. Hirumi H, Hirumi K. 1989. Continuous cultivation of Trypanosoma brucei blood stream forms in a medium containing a low concentration of serum protein without feeder cell layers. J. Parasitol. 75:985-989.
21. Wickstead B, Ersfeld K, Gull K. 2002. Targeting of a tetracyclineinducible expression system to the transcriptionally silent minichromosomes of Trypanosoma brucei. Mol. Biochem. Parasitol. 125:211-216.
22. Vondrušková E, van den Burg J, Zíková A, Ernst NL, Stuart K, Benne R, Lukeš J. 2005. RNA interference analyses suggest a transcript-specific regulatory role for mitochondrial RNA-binding proteins MRP1 and MRP2 in RNA editing and other RNA processing in Trypanosoma brucei. J. Biol. Chem. 280:2429-2438.
23. Burkard G, Fragoso CM, Roditi I. 2007. Highly efficient stable transformation of bloodstream forms of Trypanosoma brucei. Mol. Biochem. Parasitol. 153:220-223.
24. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
25. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
26. Letunic I, Doerks T, Bork P. 2012. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 40:D302-D305.
27. Bihlmaier K, Mesecke N, Terziyska N, Bien M, Hell K, Herrmann JM. 2007. The disulfide relay system of mitochondria is connected to the respiratory chain. J. Cell Biol. 179:389-395.
28. Dabir DV, Leverich EP, Kim SK, Tsai FD, Hirasawa M, Knaff DB, Koehler CM. 2007. A role for cytochrome c and cytochrome c peroxidase in electron shuttling from Erv1. EMBO J. 26:4801-4811.
29. Levitan A, Danon A, Lisowsky T. 2004. Unique features of plant mitochondrial sulfhydryl oxidase. J. Biol. Chem. 279:20002-20008.
30. Ang SK, Lu H. 2009. Deciphering structural and functional roles of individual disulfide bonds of the mitochondrial sulfhydryl oxidase Erv1p. J. Biol. Chem. 284:28754-28761.
31. Rodriguez-Roldan V, Garcia-Heredia JM, Navarro JA, Hervas M, De la Cerda B, Molina-Heredia FP, De la Rosa MA. 2006. A comparative kinetic analysis of the reactivity of plant, horse, and human respiratory cytochrome c towards cytochrome c oxidase. Biochem. Biophys. Res. Commun. 346:1108-1113.
32. Allen JW, Ginger ML, Ferguson SJ. 2004. Maturation of the unusual single-cysteine (XXXCH) mitochondrial c-type cytochromes found in trypanosomatids must occur through a novel biogenesis pathway. Biochem. J. 383:537-542.
33. Ginger ML, Sam KA, Allen JW. 2012. Probing why trypanosomes assemble atypical cytochrome c with an AxxCH haem-binding motif instead of CxxCH. Biochem. J. 448:253-260.
34. Fass D. 2008. The Erv family of sulfhydryl oxidases. Biochim. Biophys. Acta 1783:557-566.
35. Hofhaus G, Lee JE, Tews I, Rosenberg B, Lisowsky T. 2003. The N-terminal cysteine pair of yeast sulfhydryl oxidase Erv1p is essential for in vivo activity and interacts with the primary redox centre. Eur. J. Biochem. 270:1528-1535.
36. Wu CK, Dailey TA, Dailey HA, Wang BC, Rose JP. 2003. The crystal structure of augmenter of liver regeneration: a mammalian FADdependent sulfhydryl oxidase. Protein Sci. 12:1109-1118.
37. Vitu E, Bentzur M, Lisowsky T, Kaiser CA, Fass D. 2006. Gain of function in an ERV/ALR sulfhydryl oxidase by molecular engineering of the shuttle disulfide. J. Mol. Biol. 362:89-101.
38. Sevier CS, Kaiser CA. 2006. Disulfide transfer between two conserved cysteine pairs imparts selectivity to protein oxidation by Ero1. Mol. Biol. Cell 17:2256-2266.
39. Vala A, Sevier CS, Kaiser CA. 2005. Structural determinants of substrate access to the disulfide oxidase Erv2p. J. Mol. Biol. 354:952-966.
40. Banci L, Bertini I, Calderone V, Cefaro C, Ciofi-Baffoni S, Gallo A, Kallergi E, Lionaki E, Pozidis C, Tokatlidis K. 2011. Molecular recognition and substrate mimicry drive the electron-transfer process between MIA40 and ALR. Proc. Natl. Acad. Sci. U. S. A. 108:4811-4816.
41. Bien M, Longen S, Wagener N, Chwalla I, Herrmann JM, Riemer J. 2010. Mitochondrial disulfide bond formation is driven by intersubunit electron transfer in Erv1 and proofread by glutathione. Mol. Cell 37:516-528.
42. Becher D, Kricke J, Stein G, Lisowsky T. 1999. A mutant for the yeast scERV1 gene displays a new defect in mitochondrial morphology and distribution. Yeast 15:1171-1181.
43. Stojanovski D, Rissler M, Pfanner N, Meisinger C. 2006. Mitochondrial morphology and protein import-a tight connection? Biochim. Biophys. Acta 1763:414-421.
44. Long S, Jirku° M, Mach J, Ginger ML, Šuták R, Richardson D, Tachezy J, Lukeš J. 2008. Ancestral roles of eukaryotic frataxin: mitochondrial frataxin function and heterologous expression of hydrogenosomal Trichomonas homologues in trypanosomes. Mol. Microbiol. 69:94-109.
45. Long S, Changmai P, Tsaousis AD, Skalický T, Verner Z, Wen YZ, Roger AJ, Lukeš J. 2011. Stage-specific requirement for Isa1 and Isa2 proteins in the mitochondrion of Trypanosoma brucei and heterologous rescue by human and Blastocystis orthologues. Mol. Microbiol. 81:1403-1418.
46. Kispal G, Csere P, Prohl C, Lill R. 1999. The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J. 18:3981-3989.
47. Bruske EI, Sendfeld F, Schneider A. 2009. Thiolated tRNAs of Trypanosoma brucei are imported into mitochondria and dethiolated after import. J. Biol. Chem. 284:36491-36499.
48. Huynen MA, Snel B, Bork P, Gibson TJ. 2001. The phylogenetic distribution of frataxin indicates a role in iron-sulfur cluster protein assembly. Hum. Mol. Genet. 10:2463-2468.
49. Corradi N, Pombert JF, Farinelli L, Didier ES, Keeling PJ. 2010. The complete sequence of the smallest known nuclear genome from the microsporidian Encephalitozoon intestinalis. Nat. Commun. 1:77. doi:10.1038/ncomms1082.
50. Katinka MD, Duprat S, Cornillot E, Metenier G, Thomarat F, Prensier G, Barbe V, Peyretaillade E, Brottier P, Wincker P, Delbac F, El Alaoui H, Peyret P, Saurin W, Gouy M, Weissenbach J, Vivares CP. 2001. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414:450-453.
51. Soler N, Delagoutte E, Miron S, Facca C, Baille D, D'Autreaux B, Craescu G, Frapart YM, Mansuy D, Baldacci G, Huang ME, Vernis L. 2011. Interaction between the reductase Tah18 and highly conserved Fe-S containing Dre2 C-terminus is essential for yeast viability. Mol. Microbiol. 82:54-67.
52. Carrie C, Giraud E, Duncan O, Xu L, Wang Y, Huang S, Clifton R, Murcha M, Filipovska A, Rackham O, Vrielink A, Whelan J. 2010. Conserved and novel functions for Arabidopsis thaliana MIA40 in assembly of proteins in mitochondria and peroxisomes. J. Biol. Chem. 285: 36138-36148.
53. Gentle IE, Perry AJ, Alcock FH, Likic VA, Dolezal P, Ng ET, Purcell AW, McConnville M, Naderer T, Chanez AL, Charriere F, Aschinger C, Schneider A, Tokatlidis K, Lithgow T. 2007. Conserved motifs reveal details of ancestry and structure in the small TIM chaperones of the mitochondrial intermembrane space. Mol. Biol. Evol. 24:1149-1160.
54. Yang ZR, Thomson R, McNeil P, Esnouf RM. 2005. RONN: the biobasis function neural network technique applied to the detection of natively disordered regions in proteins. Bioinformatics 21:3369-3376.
55. Farrell SR, Thorpe C. 2005. Augmenter of liver regeneration: a flavindependent sulfhydryl oxidase with cytochrome c reductase activity. Biochemistry 44:1532-1541.
56. Gnaiger E, Kuznetsov AV. 2002. Mitochondrial respiration at low levels of oxygen and cytochrome c. Biochem. Soc. Trans. 30:252-258.
57. 2 and ATP. Am. J. Physiol. 250:C663-C675.
58. Hellemond JJ, Bakker BM, Tielens AG. 2005. Energy metabolism and its compartmentation in Trypanosoma brucei. Adv. Microb. Physiol. 50:199-226.
59. Forman HJ, Azzi A. 1997. On the virtual existence of superoxide anions in mitochondria: thoughts regarding its role in pathophysiology. FASEB J. 11:374-375.
60. Oursler MJ, Bradley EW, Elfering SL, Giulivi C. 2005. Native, not nitrated, cytochrome c and mitochondria-derived hydrogen peroxide drive osteoclast apoptosis. Am. J. Physiol. Cell Physiol. 288:C156-C168.
61. Dean S, Marchetti R, Kirk K, Matthews KR. 2009. A surface transporter family conveys the trypanosome differentiation signal. Nature 459:213-217.
62. Spitznagel D, Ebikeme C, Biran M, Nic a' Bhaird N, Bringaud F, Henehan GT, Nolan DP. 2009. Alanine aminotransferase of Trypanosoma brucei-a key role in proline metabolism in procyclic life forms. FEBS J. 276:7187-7199.
63. Coustou V, Biran M, Besteiro S, Riviere L, Baltz T, Franconi JM, Bringaud F. 2006. Fumarate is an essential intermediary metabolite produced by the procyclic Trypanosoma brucei. J. Biol. Chem. 281:26832-26846.
64. Rada P, Doležal P, Jedelský PL, Bursac D, Perry AJ, Šedinová M, Smíšková K, Novotný M, Beltrán NC, Hrdý I, Lithgow T, Tachezy J. 2011. The core components of organelle biogenesis and membrane transport in the hydrogenosomes of Trichomonas vaginalis. PLoS One 6:e24428. doi:10.1371/journal.pone.0024428.
65. Muller M, Mentel M, van Hellemond JJ, Henze K, Woehle C, Gould SB, Yu RY, van der Giezen M, Tielens AG, Martin WF. 2012. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rev. 76:444-495.
66. Shiflett AM, Johnson PJ. 2010. Mitochondrion-related organelles in eukaryotic protists. Annu. Rev. Microbiol. 64:409-429.
67. Šuták R, Doležal P, Fiumera HL, Hrdý I, Dancis A, Delgadillo-Correa M, Johnson PJ, Muller M, Tachezy J. 2004. Mitochondrial-type assembly of FeS centers in the hydrogenosomes of the amitochondriate eukaryote Trichomonas vaginalis. Proc. Natl. Acad. Sci. U. S. A. 101:10368-10373.
68. Tovar J, Leon-Avila G, Sanchez LB, Šuták R, Tachezy J, van der Giezen M, Hernandez M, Muller M, Lucocq JM. 2003. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426:172-176.
69. Tsaousis AD, Ollagnier de Choudens S, Gentekaki E, Long S, Gaston D, Stechmann A, Vinella D, Py B, Fontecave M, Barras F, Lukeš J, Roger AJ. 2012. Evolution of Fe/S cluster biogenesis in the anaerobic parasite Blastocystis. Proc. Natl. Acad. Sci. U. S. A. 109:10426-10431.
70. Ali V, Shigeta Y, Tokumoto U, Takahashi Y, Nozaki T. 2004. An intestinal parasitic protist, Entamoeba histolytica, possesses a nonredundant nitrogen fixation-like system for iron-sulfur cluster assembly under anaerobic conditions. J. Biol. Chem. 279:16863-16874.
71. Maralikova B, Ali V, Nakada-Tsukui K, Nozaki T, van der Giezen M, Henze K, Tovar J. 2010. Bacterial-type oxygen detoxification and ironsulfur cluster assembly in amoebal relict mitochondria. Cell. Microbiol. 12:331-342.
72. van der Giezen M, Cox S, Tovar J. 2004. The iron-sulfur cluster assembly genes iscS and iscU of Entamoeba histolytica were acquired by horizontal gene transfer. BMC Evol. Biol. 4:7. doi:10.1186/1471-2148-4-7.
73. Daithankar VN, Schaefer SA, Dong M, Bahnson BJ, Thorpe C. 2010. Structure of the human sulfhydryl oxidase augmenter of liver regeneration and characterization of a human mutation causing an autosomal recessive myopathy. Biochemistry 49:6737-6745.