Transport of Proteins to the Mitochondrial Intermembrane Space: the 'matrix-targeting' and the 'sorting' Domains in the Cytochrome C1 Presequence

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1987 Aug 1

PMID 2822392

Citations 27

Authors

A P van Loon

A W Brandli

D Blank

G Schatz

Affiliations

Soon will be listed here.

Abstract

We reported earlier that the yeast cytochrome c1 presequence (length: 61 amino acids) directs attached proteins to the mitochondrial intermembrane space and that it appears to contain two functional domains: a 'matrix-targeting' domain, and a 'sorting' domain. We have now used gene manipulation together with two different in vivo import assays to map these two domains within the cytochrome c1 presequence. The 'matrix-targeting' domain is contained within the N-terminal 16 residues (or less); by itself, it directs attached proteins to the matrix. The 'sorting' domain extends into the C-terminal 13 residues of the presequence; while it does not mediate intracellular protein transport by itself, it acts together with the preceding 'matrix-targeting' sequence in sorting attached proteins into the intermembrane space. On replacing the authentic 'matrix-targeting' sequence with artificial sequences of different lengths we found that sorting of proteins between the outer membrane and the intermembrane space is not exclusively determined by the length of the N-terminal 'matrix-targeting' sequence.

Citing Articles

Interplay between Mitochondrial Protein Import and Respiratory Complexes Assembly in Neuronal Health and Degeneration.

Needs H, Protasoni M, Henley J, Prudent J, Collinson I, Pereira G Life (Basel). 2021; 11(5).

PMID: 34064758 PMC: 8151517. DOI: 10.3390/life11050432.

Genome-wide CRISPRi screening identifies OCIAD1 as a prohibitin client and regulatory determinant of mitochondrial Complex III assembly in human cells.

Le Vasseur M, Friedman J, Jost M, Xu J, Yamada J, Kampmann M Elife. 2021; 10.

PMID: 34034859 PMC: 8154037. DOI: 10.7554/eLife.67624.

Complexome profile of Toxoplasma gondii mitochondria identifies divergent subunits of respiratory chain complexes including new subunits of cytochrome bc1 complex.

Maclean A, Bridges H, Silva M, Ding S, Ovciarikova J, Hirst J PLoS Pathog. 2021; 17(3):e1009301.

PMID: 33651838 PMC: 7987180. DOI: 10.1371/journal.ppat.1009301.

Mitochondrial Structure and Bioenergetics in Normal and Disease Conditions.

Protasoni M, Zeviani M Int J Mol Sci. 2021; 22(2).

PMID: 33435522 PMC: 7827222. DOI: 10.3390/ijms22020586.

Mitochondrial Dynamics and Heart Failure.

Knowlton A, Liu T Compr Physiol. 2016; 6(1):507-26.

PMID: 26756641 PMC: 5695672. DOI: 10.1002/cphy.c150022.

References

Allison D, Schatz G . Artificial mitochondrial presequences. Proc Natl Acad Sci U S A. 1986; 83(23):9011-5. PMC: 387064. DOI: 10.1073/pnas.83.23.9011. View

Hartl F, Schmidt B, Wachter E, Weiss H, Neupert W . Transport into mitochondria and intramitochondrial sorting of the Fe/S protein of ubiquinol-cytochrome c reductase. Cell. 1986; 47(6):939-51. DOI: 10.1016/0092-8674(86)90809-3. View

Boyer H . A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol. 1969; 41(3):459-72. DOI: 10.1016/0022-2836(69)90288-5. View

Bolivar F, Backman K . Plasmids of Escherichia coli as cloning vectors. Methods Enzymol. 1979; 68:245-67. DOI: 10.1016/0076-6879(79)68018-7. View

Li Y, Leonard K, Weiss H . Membrane-bound and water-soluble cytochrome c1 from Neurospora mitochondria. Eur J Biochem. 1981; 116(1):199-205. DOI: 10.1111/j.1432-1033.1981.tb05319.x. View

Gasser S, Daum G, Schatz G . Import of proteins into mitochondria. Energy-dependent uptake of precursors by isolated mitochondria. J Biol Chem. 1982; 257(21):13034-41. View

Ito H, Fukuda Y, Murata K, Kimura A . Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983; 153(1):163-8. PMC: 217353. DOI: 10.1128/jb.153.1.163-168.1983. View

Kaput J, Goltz S, Blobel G . Nucleotide sequence of the yeast nuclear gene for cytochrome c peroxidase precursor. Functional implications of the pre sequence for protein transport into mitochondria. J Biol Chem. 1982; 257(24):15054-8. View

Vieira J, Messing J . The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982; 19(3):259-68. DOI: 10.1016/0378-1119(82)90015-4. View

10.

Haid A, Suissa M . Immunochemical identification of membrane proteins after sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Methods Enzymol. 1983; 96:192-205. DOI: 10.1016/s0076-6879(83)96017-2. View

11.

Hay R, Bohni P, Gasser S . How mitochondria import proteins. Biochim Biophys Acta. 1984; 779(1):65-87. DOI: 10.1016/0304-4157(84)90004-2. View

12.

Hase T, Riezman H, Suda K, Schatz G . Import of proteins into mitochondria: nucleotide sequence of the gene for a 70-kd protein of the yeast mitochondrial outer membrane. EMBO J. 1983; 2(12):2169-72. PMC: 555429. DOI: 10.1002/j.1460-2075.1983.tb01718.x. View

13.

Suissa M, Suda K, Schatz G . Isolation of the nuclear yeast genes for citrate synthase and fifteen other mitochondrial proteins by a new screening method. EMBO J. 1984; 3(8):1773-81. PMC: 557595. DOI: 10.1002/j.1460-2075.1984.tb02045.x. View

14.

Sadler I, Suda K, Schatz G, Kaudewitz F, Haid A . Sequencing of the nuclear gene for the yeast cytochrome c1 precursor reveals an unusually complex amino-terminal presequence. EMBO J. 1984; 3(9):2137-43. PMC: 557655. DOI: 10.1002/j.1460-2075.1984.tb02103.x. View

15.

Johnston M, Davis R . Sequences that regulate the divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae. Mol Cell Biol. 1984; 4(8):1440-8. PMC: 368932. DOI: 10.1128/mcb.4.8.1440-1448.1984. View

16.

Maarse A, van Loon A, Riezman H, Gregor I, Schatz G, Grivell L . Subunit IV of yeast cytochrome c oxidase: cloning and nucleotide sequencing of the gene and partial amino acid sequencing of the mature protein. EMBO J. 1984; 3(12):2831-7. PMC: 557773. DOI: 10.1002/j.1460-2075.1984.tb02216.x. View

17.

Stueber D, Ibrahimi I, Cutler D, Dobberstein B, Bujard H . A novel in vitro transcription-translation system: accurate and efficient synthesis of single proteins from cloned DNA sequences. EMBO J. 1984; 3(13):3143-8. PMC: 557830. DOI: 10.1002/j.1460-2075.1984.tb02271.x. View

18.

Hase T, Muller U, Riezman H, Schatz G . A 70-kd protein of the yeast mitochondrial outer membrane is targeted and anchored via its extreme amino terminus. EMBO J. 1984; 3(13):3157-64. PMC: 557833. DOI: 10.1002/j.1460-2075.1984.tb02274.x. View

19.

Dowhan W, Bibus C, Schatz G . The cytoplasmically-made subunit IV is necessary for assembly of cytochrome c oxidase in yeast. EMBO J. 1985; 4(1):179-84. PMC: 554168. DOI: 10.1002/j.1460-2075.1985.tb02334.x. View

20.

Hurt E, Suda K, Oppliger W, Schatz G . The first twelve amino acids (less than half of the pre-sequence) of an imported mitochondrial protein can direct mouse cytosolic dihydrofolate reductase into the yeast mitochondrial matrix. EMBO J. 1985; 4(8):2061-8. PMC: 554462. DOI: 10.1002/j.1460-2075.1985.tb03892.x. View