Three Distinct Isoforms of ATP Synthase Subunit c Are Expressed in T. brucei and Assembled into the Mitochondrial ATP Synthase Complex

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Gulde, Paul E ^a   Christen, Linda ^a   Brown, Silvia V ^a   Williams, Noreen ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISOENZYME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE C; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; ATPC 1 GENE; ATPC 2 GENE; ATPC 3 GENE; ENZYME ACTIVITY; GENE; GENETIC TRANSCRIPTION; GENOME ANALYSIS; LIFE CYCLE; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RNA PROCESSING; TRYPANOSOMA BRUCEI;

ADENOSINE TRIPHOSPHATE; GENE EXPRESSION; MITOCHONDRIA; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; PROTEIN ISOFORMS; TRYPANOSOMA BRUCEI BRUCEI;

TRYPANOSOMA BRUCEI;

EID: 84872225470     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054039     Document Type: Article

References (44)

1. Bringaud F, Riviere L, Coustou V, (2006) Energy metabolism of trypanosomatids: adaptation to available carbon sources. Mol Biochem Parasitol 149: 1-9.
2. Hellemond JV, Opperdoes F, Tielens A, (2005) The extraordinary mitochondrion and unusual citric acid cycle in Trypanosoma brucei. Biochem Soc Trans 33: 967-971.
3. Brown BS, Chi TB, Williams N, (2001) The Trypanosoma brucei mitochondrial ATP synthase is developmentally regulated at the level of transcript stability. Mol Biochem Parasitol 2001: 177-187.
4. Williams N, (1994) The mitochondrial ATP synthase of Trypanosoma brucei: structure and regulation. J Bioenerg Biomembr 26: 173-178.
5. Nolan DP, Voorheis HP, (1992) The mitochondrion in bloodstream forms of Trypanosoma brucei is energized by the electrogenic pumping of protons catalysed by the F1F0-ATPase. Eur J Biochem 209: 207-216.
6. Suzuki T, Murakami T, Iino R, Suzuki J, Ono S, et al. (2003) F0F1-ATPase/synthase is geared to the synthesis mode by conformational rearrangement of epsilon subunit in response to proton motive force and ADP/ATP balance. J Biol Chem 278: 46840-46846.
7. Nolan DP, Voorheis HP, (1991) Bioenergetic studies of bloodstream forms of Trypanosoma brucei electrical H+ gradients. Soc Trans 18: 735-739.
8. Vercesi AE, Docampo R, Moreno SN, (1992) Energization-dependent Ca2+ accumulation in Trypanosoma brucei bloodstream and procyclic trypomastigotes mitochondria. Mol Biochem Parasitol 56: 251-257.
9. Brown S, Hosking P, Li J, Williams N, (2006) ATP synthase is responsible for maintaining mitochondrial membrane potential in bloodstream form Trypanosoma brucei. Eukaryot Cell 5: 45-53.
10. Schnaufer A, Clark-Walker G, Steinberg A, Stuart K, (2005) The F1-ATP synthase complex in bloodstream stage trypanosomes has an unusual and essential function. EMBO J 24: 4029-4040.
11. Devenish R, Prescott M, Rodgers A, (2008) The structure and function of mitochondrial F1F0-ATP synthases. Int Rev Cell Mol Biol 267: 1-58.
12. Baker L, Watt I, Runswick M, Walker J, Rubinstein J, (2012) Arrangement of subunits in intact mammalian mitochondrial ATP synthase determined by cryo-EM. Proc Natl Acad Sci U S A 109: 11675-11680.
13. Collinson IR, Runswick MJ, Buchanan SK, Fearnley IM, Skehel JM, et al. (1994) F0 membrane domain of ATP synthase from bovine heart mitochondria: purification, subunit composition, and reconstitution with F1-ATPase. Biochem 33: 7971-7978.
14. Zikova A, Schnaufer A, Dailey R, Panigrahi A, Stuart K, (2009) The F0F1-ATP synthase complex contains novel subunits and is essential for procyclic Trypanosoma brucei. PLOS Pathogens 5: e1000436.
15. Williams N, Frank PH, (1990) The mitochondrial ATP synthase of Trypanosoma brucei: Isolation and characterization of an intact F1 moiety. Mol Biochem Parasitol 43: 125-132.
16. Boyer PD, (1997) The ATP synthase-a splendid molecular machine. Annual Review of Biochemistry 66: 717-749.
17. Girvin ME, Fillingame RH, (1993) Helical structure and folding of subunit c of F1F0 ATP synthase: 1H NMR resonance assignments and NOE analysis. Biochem 32: 12167-12177.
18. Symersky J, Pagadala V, Osowski D, Krah A, Meier T, et al. (2012) Structure of the c(10) ring of the yeast mitochondrial ATP synthase in the open conformation. Nat Struct Mol Biol 19: 485-491.
19. Rak M, Zeng X, Briere J-J, Tzagoloff A, (2009) Assembly of F0 in Saccharomyces cerevisiae. Biochim Biophys Acta 1793: 108-116.
20. von Ballmoos C, Cook G, Dimroth P, (2008) Unique rotary ATP synthase and its biological diversity. Annu Rev Biophys 37: 43-64.
21. Schemidt R, Qu J, Williams J, Brusilow W, (1998) Effects of carbon source on expression of F0 genes and on the stoiciometry of the c subunit in the F1F0 ATPase of Escherichia coli. J Bact 180: 3205-3208.
22. Andersson U, Houstek J, Cannon B, (1997) ATP synthase subunit c expression: physiological regulation of the P1 and P2 genes. Biochem J 323: 379-385.
23. De Grassi A, Lanave C, Saccone C, (2006) Evolution of ATP synthase subunit c and cytochrome c gene families in selected Metazoan classes. Gene 371: 224-233.
24. Dyer MR, Walker JE, (1993) Sequences of members of the human gene family for the c subunit of mitochondrial ATP synthase. Biochem J 293: 51-64.
25. Hirumi H, Hirumi K, (1989) Continuous cultivation of Trypanosoma brucei bloodstream forms in a medium containing a low concentration of serum protein without feeder cell layers. J Parasitol 75: 985-989.
26. Cunningham I, (1977) New culture medium for maintenance of tsetse tissues and growth of trypanosomatids. J Protozool 24: 325-329.
27. Fisk J, Ammerman M, Presnyak V, Read L, (2008) TbRGG2, an essential RNA editing accessory factor in two Trypanosoma brucei life cycle stages. J Biol Chem 283: 23016-23025.
28. Williams N, Choi SY, Ruyechan WT, Frank PH, (1991) The mitochondrial ATP synthase of Trypanosoma brucei: developmental regulation through the life cycle. Arch Biochem Biophys 288: 509-515.
29. Chi TB, Brown SV, Williams N, (1998) Subunit 9 of the mitochondrial ATP synthase of Trypanosoma brucei is nuclearly encoded and developmentally regulated. Mol Biochem Parasitol 92: 29-38.
30. Brenndörfer M, Boshart M, (2010) Selection of reference genes for mRNA quantification in Trypanosoma brucei. Mol Biochem Parasitol 172: 52-55.
31. Livak K, Schmittgen T, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-delta delta C(T) method. Methods 25: 402-408.
32. Wittig I, Carrozzo R, Santorelli F, Schägger H, (2007) Functional assays in high-resolution clear native gels to quantify mitochondrial complexes in human biopsies and cell lines. Electrophoresis 28: 3811-3820.
33. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, et al. (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309: 416-422.
34. Hausler T, Stierhof YD, Blattner J, Clayton C, (1997) Conservation of mitochondrial targeting sequence function in mitochondrial and hydrogenosomal proteins from the early-branching eukaryotes Crithidia, Trypanosoma and Trichomonas. Eur J Cell Biol 73: 240-251.
35. Priest JW, Hajduk SL, (1995) The trypanosomatid Rieske iron-sulfur proteins have a cleaved presequence that may direct mitochondrial import. Biochim Biophys Acta 1269: 201-204.
36. Clayton C, Hausler T, Blattner J, (1995) Protein trafficking in Kinetoplastid protozoa. Microbiol Rev 59: 325-344.
37. Matthews KR, (1999) Developments in the differentiation of Trypanosoma brucei. Parasitol Today 15: 76-80.
38. Hensgens L, Grivell L, Borst P, Bos JL, (1979) Nucleotide sequence of the mitochondrial structural gene for subunit 9 of yeast ATPase complex. Proc Natl Acad Sci USA 76: 1663-1667.
39. Pogoryelov D, Klyszejko A, Krasnoselska GO, Heller E-M, Leone V, et al. (2012) Engineering rotor ring stoichiometries in the ATP synthase. Proc Natl Acad Sci U S A 109: E1599-1608.
40. Vives-Bauza C, Magrané J, Andreu A, Manfredi G, (2010) Novel role of ATPase subunit c targeting peptides beyond mitochondrial protein import. Mol Cell Biol 21: 131-139.
41. Gay NJ, Walker JE, (1985) Two genes encoding the bovine mitochondrial ATP synthase proteolipid specify precursors with different import sequences and are expressed in a tissue-specific manner. EMBO J 4: 3519-3524.
42. Meier T, Morgner N, Matthies D, Pogoryelov D, Keis S, et al. (2007) A tridecameric c ring of the adenosine triphosphate (ATP) synthase from the thermoalkaliphilic Bascillus so. strain TA2.A1 facilitates ATP synthesis at low electrochemical proton potential. Mol Micro 65: 1181-1192.
43. Alsford S, Turner D, Obado S, Sanchez-Flores A, Glover L, et al. (2011) High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res 21: 915-924.
44. Symersky J, Osowski D, Walters D, Mueller D, (2012) Oligomycin frames a common drug-binding site in the ATP synthase. Proc Natl Acad Sci U S A 109: 13961-13965.