Characterization of Gtf1p, the Connector Subunit of Yeast Mitochondrial TRNA-dependent Amidotransferase

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2011 Jul 30

PMID 21799017

Citations 6

Authors

Mario H Barros

Malgorzata Rak

Janaina A Paulela

Alexander Tzagoloff

Affiliations

Soon will be listed here.

Abstract

The bacterial GatCAB operon for tRNA-dependent amidotransferase (AdT) catalyzes the transamidation of mischarged glutamyl-tRNA(Gln) to glutaminyl-tRNA(Gln). Here we describe the phenotype of temperature-sensitive (ts) mutants of GTF1, a gene proposed to code for subunit F of mitochondrial AdT in Saccharomyces cerevisiae. The ts gtf1 mutants accumulate an electrophoretic variant of the mitochondrially encoded Cox2p subunit of cytochrome oxidase and an unstable form of the Atp8p subunit of the F(1)-F(0) ATP synthase that is degraded, thereby preventing assembly of the F(0) sector. Allotopic expression of recoded ATP8 and COX2 did not significantly improve growth of gtf1 mutants on respiratory substrates. However, ts gft1 mutants are partially rescued by overexpression of PET112 and HER2 that code for the yeast homologues of the catalytic subunits of bacterial AdT. Additionally, B66, a her2 point mutant has a phenotype similar to that of gtf1 mutants. These results provide genetic support for the essentiality, in vivo, of the GatF subunit of the heterotrimeric AdT that catalyzes formation of glutaminyl-tRNA(Gln) (Frechin, M., Senger, B., Brayé, M., Kern, D., Martin, R. P., and Becker, H. D. (2009) Genes Dev. 23, 1119-1130).

Citing Articles

Mitochondrial ribosome bL34 mutants present diminished translation of cytochrome c oxidase subunits.

Guedes-Monteiro R, Ribamar Ferreira-Junior J, Bleicher L, Nobrega F, Barrientos A, Barros M Cell Biol Int. 2017; 42(6):630-642.

PMID: 29160602 PMC: 5962420. DOI: 10.1002/cbin.10913.

Aep3p-dependent translation of yeast mitochondrial .

Barros M, Tzagoloff A Mol Biol Cell. 2017; 28(11):1426-1434.

PMID: 28404747 PMC: 5449143. DOI: 10.1091/mbc.E16-11-0775.

Partial suppression of the respiratory defect of qrs1/her2 glutamyl-tRNA amidotransferase mutants by overexpression of the mitochondrial pentatricopeptide Msc6p.

Moda B, Ribamar Ferreira-Junior J, Barros M Curr Genet. 2016; 62(3):607-17.

PMID: 26780366 DOI: 10.1007/s00294-016-0566-6.

Crystal structure of Saccharomyces cerevisiae mitochondrial GatFAB reveals a novel subunit assembly in tRNA-dependent amidotransferases.

Araiso Y, Huot J, Sekiguchi T, Frechin M, Fischer F, Enkler L Nucleic Acids Res. 2014; 42(9):6052-63.

PMID: 24692665 PMC: 4027206. DOI: 10.1093/nar/gku234.

The putative GTPase encoded by MTG3 functions in a novel pathway for regulating assembly of the small subunit of yeast mitochondrial ribosomes.

Paul M, Alushin G, Barros M, Rak M, Tzagoloff A J Biol Chem. 2012; 287(29):24346-55.

PMID: 22621929 PMC: 3397861. DOI: 10.1074/jbc.M112.363309.

References

Curnow A, Hong K, Yuan R, Kim S, Martins O, Winkler W . Glu-tRNAGln amidotransferase: a novel heterotrimeric enzyme required for correct decoding of glutamine codons during translation. Proc Natl Acad Sci U S A. 1997; 94(22):11819-26. PMC: 23611. DOI: 10.1073/pnas.94.22.11819. View

Tzagoloff A . Assembly of the mitochondrial membrane system. I. Characterization of some enzymes of the inner membrane of yeast mitochondria. J Biol Chem. 1969; 244(18):5020-6. View

Jan P, Esser K, Pratje E, Michaelis G . Som1, a third component of the yeast mitochondrial inner membrane peptidase complex that contains Imp1 and Imp2. Mol Gen Genet. 2000; 263(3):483-91. DOI: 10.1007/s004380051192. View

Steele D, Butler C, Fox T . Expression of a recoded nuclear gene inserted into yeast mitochondrial DNA is limited by mRNA-specific translational activation. Proc Natl Acad Sci U S A. 1996; 93(11):5253-7. PMC: 39231. DOI: 10.1073/pnas.93.11.5253. View

Simon M, Faye G . Organization and processing of the mitochondrial oxi3/oli2 multigenic transcript in yeast. Mol Gen Genet. 1984; 196(2):266-74. DOI: 10.1007/BF00328059. View

Nagao A, Suzuki T, Suzuki T . Aminoacyl-tRNA surveillance by EF-Tu in mammalian mitochondria. Nucleic Acids Symp Ser (Oxf). 2007; (51):41-2. DOI: 10.1093/nass/nrm021. View

Frechin M, Senger B, Braye M, Kern D, Martin R, Becker H . Yeast mitochondrial Gln-tRNA(Gln) is generated by a GatFAB-mediated transamidation pathway involving Arc1p-controlled subcellular sorting of cytosolic GluRS. Genes Dev. 2009; 23(9):1119-30. PMC: 2682957. DOI: 10.1101/gad.518109. View

Faye G, Kujawa C, Fukuhara H . Physical and genetic organization of petite and grande yeast mitochondrial DNA. IV. In vivo transcription products of mitochondrial DNA and localization of 23 S ribosomal RNA in petite mutants of saccharomyces cerevisiae. J Mol Biol. 1974; 88(1):185-203. DOI: 10.1016/0022-2836(74)90304-0. View

Claros M, Vincens P . Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem. 1996; 241(3):779-86. DOI: 10.1111/j.1432-1033.1996.00779.x. View

10.

Poutre C, Fox T . PET111, a Saccharomyces cerevisiae nuclear gene required for translation of the mitochondrial mRNA encoding cytochrome c oxidase subunit II. Genetics. 1987; 115(4):637-47. PMC: 1203096. DOI: 10.1093/genetics/115.4.637. View

11.

Wilcox M . Gamma-glutamyl phosphate attached to glutamine-specific tRNA. A precursor of glutaminyl-tRNA in Bacillus subtilis. Eur J Biochem. 1969; 11(3):405-12. DOI: 10.1111/j.1432-1033.1969.tb00788.x. View

12.

Roy H, Becker H, Mazauric M, Kern D . Structural elements defining elongation factor Tu mediated suppression of codon ambiguity. Nucleic Acids Res. 2007; 35(10):3420-30. PMC: 1904265. DOI: 10.1093/nar/gkm211. View

13.

Rak M, Tetaud E, Godard F, Sagot I, Salin B, Duvezin-Caubet S . Yeast cells lacking the mitochondrial gene encoding the ATP synthase subunit 6 exhibit a selective loss of complex IV and unusual mitochondrial morphology. J Biol Chem. 2007; 282(15):10853-64. DOI: 10.1074/jbc.M608692200. View

14.

Rinehart J, Krett B, Rubio M, Alfonzo J, Soll D . Saccharomyces cerevisiae imports the cytosolic pathway for Gln-tRNA synthesis into the mitochondrion. Genes Dev. 2005; 19(5):583-92. PMC: 551578. DOI: 10.1101/gad.1269305. View

15.

Nakagawa K, Morishima N, Shibata T . A maturase-like subunit of the sequence-specific endonuclease endo.SceI from yeast mitochondria. J Biol Chem. 1991; 266(3):1977-84. View

16.

Supekova L, Supek F, Greer J, Schultz P . A single mutation in the first transmembrane domain of yeast COX2 enables its allotopic expression. Proc Natl Acad Sci U S A. 2010; 107(11):5047-52. PMC: 2841951. DOI: 10.1073/pnas.1000735107. View

17.

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

18.

Kim S, Stange-Thomann N, Martins O, Hong K, Soll D, Fox T . A nuclear genetic lesion affecting Saccharomyces cerevisiae mitochondrial translation is complemented by a homologous Bacillus gene. J Bacteriol. 1997; 179(17):5625-7. PMC: 179443. DOI: 10.1128/jb.179.17.5625-5627.1997. View

19.

Broach J, Strathern J, Hicks J . Transformation in yeast: development of a hybrid cloning vector and isolation of the CAN1 gene. Gene. 1979; 8(1):121-33. DOI: 10.1016/0378-1119(79)90012-x. View

20.

Hell K, Herrmann J, Pratje E, Neupert W, Stuart R . Oxa1p mediates the export of the N- and C-termini of pCoxII from the mitochondrial matrix to the intermembrane space. FEBS Lett. 1998; 418(3):367-70. DOI: 10.1016/s0014-5793(97)01412-9. View