The Saccharomyces Cerevisiae ATP22 Gene Codes for the Mitochondrial ATPase Subunit 6-specific Translation Factor

Overview

Journal Genetics

Publisher Oxford University Press

Specialty Genetics

Date 2006 Nov 18

PMID 17110482

Citations 19

Authors

Xiaomei Zeng

Audrey Hourset

Alexander Tzagoloff

Affiliations

Soon will be listed here.

Abstract

Mutations in the Saccharomyces cerevisiae ATP22 gene were previously shown to block assembly of the F0 component of the mitochondrial proton-translocating ATPase. Further inquiries into the function of Atp22p have revealed that it is essential for translation of subunit 6 of the mitochondrial ATPase. The mutant phenotype can be partially rescued by the presence in the same cell of wild-type mitochondrial DNA and a rho- deletion genome in which the 5'-UTR, first exon, and first intron of COX1 are fused to the fourth codon of ATP6. The COX1/ATP6 gene is transcribed and processed to the mature mRNA by splicing of the COX1 intron from the precursor. The hybrid protein translated from the novel mRNA is proteolytically cleaved at the normal site between residues 10 and 11 of the subunit 6 precursor, causing the release of the polypeptide encoded by the COX1 exon. The ability of the rho- suppressor genome to express subunit 6 in an atp22 null mutant constitutes strong evidence that translation of subunit 6 depends on the interaction of Atp22p with the 5'-UTR of the ATP6 mRNA.

Citing Articles

Molecular basis of diseases induced by the mitochondrial DNA mutation m.9032T>C.

Baranowska E, Niedzwiecka K, Panja C, Charles C, Dautant A, di Rago J Hum Mol Genet. 2022; 32(8):1313-1323.

PMID: 36434790 PMC: 10077503. DOI: 10.1093/hmg/ddac292.

Genetic Complementation of ATP Synthase Deficiency Due to Dysfunction of TMEM70 Assembly Factor in Rat.

Markovic A, Tauchmannova K, Simakova M, Mlejnek P, Kaplanova V, Pecina P Biomedicines. 2022; 10(2).

PMID: 35203486 PMC: 8869460. DOI: 10.3390/biomedicines10020276.

Assembly-dependent translation of subunits 6 (Atp6) and 9 (Atp9) of ATP synthase in yeast mitochondria.

Kabala A, Binko K, Godard F, Charles C, Dautant A, Baranowska E Genetics. 2022; 220(3).

PMID: 35100419 PMC: 8893259. DOI: 10.1093/genetics/iyac007.

Molluscan mitochondrial genomes break the rules.

Ghiselli F, Gomes-Dos-Santos A, Adema C, Lopes-Lima M, Sharbrough J, Boore J Philos Trans R Soc Lond B Biol Sci. 2021; 376(1825):20200159.

PMID: 33813887 PMC: 8059616. DOI: 10.1098/rstb.2020.0159.

Mammalian RNA switches: Molecular rheostats in gene regulation, disease, and medicine.

Subbaiah K, Hedaya O, Wu J, Jiang F, Yao P Comput Struct Biotechnol J. 2019; 17:1326-1338.

PMID: 31741723 PMC: 6849081. DOI: 10.1016/j.csbj.2019.10.001.

References

Pelissier P, Camougrand N, Manon S, Velours G, Guerin M . Regulation by nuclear genes of the mitochondrial synthesis of subunits 6 and 8 of the ATP synthase of Saccharomyces cerevisiae. J Biol Chem. 1992; 267(4):2467-73. View

Dieckmann C, Koerner T, Tzagoloff A . Assembly of the mitochondrial membrane system. CBP1, a yeast nuclear gene involved in 5' end processing of cytochrome b pre-mRNA. J Biol Chem. 1984; 259(8):4722-31. View

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

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

Vaillier J, Benabdelhak H, Velours J, SLONIMSKI P, di Rago J . Identification of a nuclear gene (FMC1) required for the assembly/stability of yeast mitochondrial F(1)-ATPase in heat stress conditions. J Biol Chem. 2000; 276(9):6789-96. DOI: 10.1074/jbc.M009557200. View

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

SLONIMSKI P, Tzagoloff A . Localization in yeast mitochondrial DNA of mutations expressed in a deficiency of cytochrome oxidase and/or coenzyme QH2-cytochrome c reductase. Eur J Biochem. 1976; 61(1):27-41. DOI: 10.1111/j.1432-1033.1976.tb09994.x. View

Muller P, Reif M, Zonghou S, Sengstag C, Mason T, Fox T . A nuclear mutation that post-transcriptionally blocks accumulation of a yeast mitochondrial gene product can be suppressed by a mitochondrial gene rearrangement. J Mol Biol. 1984; 175(4):431-52. DOI: 10.1016/0022-2836(84)90178-5. View

Helfenbein K, Ellis T, Dieckmann C, Tzagoloff A . ATP22, a nuclear gene required for expression of the F0 sector of mitochondrial ATPase in Saccharomyces cerevisiae. J Biol Chem. 2003; 278(22):19751-6. DOI: 10.1074/jbc.M301679200. View

10.

King E . The colorimetric determination of phosphorus. Biochem J. 1932; 26(2):292-7. PMC: 1260904. DOI: 10.1042/bj0260292. View

11.

Pelissier P, Camougrand N, Velours G, Guerin M . NCA3, a nuclear gene involved in the mitochondrial expression of subunits 6 and 8 of the Fo-F1 ATP synthase of S. cerevisiae. Curr Genet. 1995; 27(5):409-16. DOI: 10.1007/BF00311209. View

12.

Tzagoloff A, Dieckmann C . PET genes of Saccharomyces cerevisiae. Microbiol Rev. 1990; 54(3):211-25. PMC: 372773. DOI: 10.1128/mr.54.3.211-225.1990. View

13.

Ackerman S, Tzagoloff A . Identification of two nuclear genes (ATP11, ATP12) required for assembly of the yeast F1-ATPase. Proc Natl Acad Sci U S A. 1990; 87(13):4986-90. PMC: 54246. DOI: 10.1073/pnas.87.13.4986. View

14.

Costanzo M, Fox T . Control of mitochondrial gene expression in Saccharomyces cerevisiae. Annu Rev Genet. 1990; 24:91-113. DOI: 10.1146/annurev.ge.24.120190.000515. View

15.

Feinberg A, Vogelstein B . A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983; 132(1):6-13. DOI: 10.1016/0003-2697(83)90418-9. View

16.

Manthey G, McEwen J . The product of the nuclear gene PET309 is required for translation of mature mRNA and stability or production of intron-containing RNAs derived from the mitochondrial COX1 locus of Saccharomyces cerevisiae. EMBO J. 1995; 14(16):4031-43. PMC: 394481. DOI: 10.1002/j.1460-2075.1995.tb00074.x. View

17.

Camougrand N, Pelissier P, Velours G, Guerin M . NCA2, a second nuclear gene required for the control of mitochondrial synthesis of subunits 6 and 8 of ATP synthase in Saccharomyces cerevisiae. J Mol Biol. 1995; 247(4):588-96. DOI: 10.1006/jmbi.1995.0165. View

18.

PAUL M, Velours J, Arselin de Chateaubodeau G, Aigle M, Guerin B . The role of subunit 4, a nuclear-encoded protein of the F0 sector of yeast mitochondrial ATP synthase, in the assembly of the whole complex. Eur J Biochem. 1989; 185(1):163-71. DOI: 10.1111/j.1432-1033.1989.tb15098.x. View

19.

Arselin G, Vaillier J, Graves P, Velours J . ATP synthase of yeast mitochondria. Isolation of the subunit h and disruption of the ATP14 gene. J Biol Chem. 1996; 271(34):20284-90. DOI: 10.1074/jbc.271.34.20284. View

20.

Costanzo M, Fox T . Specific translational activation by nuclear gene products occurs in the 5' untranslated leader of a yeast mitochondrial mRNA. Proc Natl Acad Sci U S A. 1988; 85(8):2677-81. PMC: 280061. DOI: 10.1073/pnas.85.8.2677. View