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PMID: 2820723 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Deficiency in mRNA splicing in a cytochrome c mutant of neurospora crassa: importance of carboxy terminus for import of apocytochrome c into mitochondria.

The EMBO journal ·Vol. 6 ·No. 7 ·1987-07-00 ·Pages 2131-7

Stuart RA, Neupert W, Tropschug M

Abstract

Molecular cloning and characterization of cytochrome c cDNA clones of Neurospora crassa wild-type (74A) and a cytochrome c-deficient mutant (cyc1-1) are described. Southern blot analysis of genomic DNA indicates that only one cytochrome c gene exists in the N. crassa genome. The cDNA sequence of the wild-type cytochrome c confirmed the previously determined protein sequence. Sequence analysis of the cyc1-1 cDNA for cytochrome c revealed the presence of a larger open reading frame, owing to the presence of an unspliced intron in the 3' end of the coding region. Splicing of this intron is obviously prevented due to the presence of two base exchanges in the highly conserved intron consensus sequences. Consequently, cyc1-1 synthesizes apocytochrome c with an altered carboxy terminus, 19 amino acids longer than the wild-type cytochrome c, with the final 27 amino acids being of an unrelated sequence. This alteration in the carboxy terminus renders the apocytochrome c incompetent for binding to mitochondria and, consequently, import into mitochondria. Thus, unlike other mitochondrial precursor proteins, where it has been demonstrated that the amino terminus alone is sufficient to target the protein to the mitochondria, an intact carboxy terminus is required for efficient import of apocytochrome c into mitochondria. This is independent confirmation for the view that the import pathway of cytochrome c is unique with respect to all other mitochondrial proteins studied to date.

MeSH Terms
Amino Acid Sequence Base Sequence Biological Transport Cloning, Molecular Cytochrome c Group/genetics DNA/metabolism DNA, Fungal/genetics Genes Genes, Fungal Mitochondria/metabolism Molecular Sequence Data Mutation Neurospora/genetics Neurospora crassa/genetics,metabolism RNA Splicing RNA, Messenger/genetics
Chemicals
Cytochrome c Group DNA, Fungal RNA, Messenger DNA
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Stuart R A
Institut für Physiologische Chemie, Physikalische Biochemie und Zellbiologie der Universität München, FRG.
Neupert W
Tropschug M
References (48)
48 references, click to expand
  1. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  2. Complementation analysis of temperature-sensitive host specificity mutations in Escherichia coli.
    J Mol Biol. 1970 May 28;50(1):111-27 PMID: 4916553
  3. Detection of polyadenylic acid sequences in viral and eukaryotic RNA(polu(U)-cellulose columns-poly(U) filters-fiberglass-HeLa cells-bacteriophage T4).
    Proc Natl Acad Sci U S A. 1972 Feb;69(2):417-21 PMID: 4501121
  4. Neurospora crassa and Humicola lanuginosa cytochromes c: more homology in the heme region.
    Biochem Biophys Res Commun. 1974 Jan 23;56(2):317-23 PMID: 4363050
  5. Detection of specific sequences among DNA fragments separated by gel electrophoresis.
    J Mol Biol. 1975 Nov 5;98(3):503-17 PMID: 1195397
  6. Colony hybridization: a method for the isolation of cloned DNAs that contain a specific gene.
    Proc Natl Acad Sci U S A. 1975 Oct;72(10):3961-5 PMID: 1105573
  7. 3' non-coding region sequences in eukaryotic messenger RNA.
    Nature. 1976 Sep 16;263(5574):211-4 PMID: 822353
  8. An efficient mRNA-dependent translation system from reticulocyte lysates.
    Eur J Biochem. 1976 AUG 1;67(1):247-56 PMID: 823012
  9. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I.
    J Mol Biol. 1977 Jun 15;113(1):237-51 PMID: 881736
  10. Transport of cytoplasmically synthesized proteins into the mitochondria in a cell free system from Neurospora crassa.
    Eur J Biochem. 1977 Dec;81(3):533-44 PMID: 145943
  11. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  12. A bacterial clone synthesizing proinsulin.
    Proc Natl Acad Sci U S A. 1978 Aug;75(8):3727-31 PMID: 358198
  13. Synthesis of a larger precursor for the proteolipid subunit of the mitochondrial ATPase complex of Neurospora crassa in a cell-free wheat germ system.
    FEBS Lett. 1979 May 15;101(2):373-6 PMID: 156127
  14. A rapid alkaline extraction procedure for screening recombinant plasmid DNA.
    Nucleic Acids Res. 1979 Nov 24;7(6):1513-23 PMID: 388356
  15. Cell-free synthesis of cytochrome c.
    FEBS Lett. 1979 Dec 1;108(1):141-6 PMID: 230077
  16. Isolation and sequence of the gene for iso-2-cytochrome c in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1980 Jan;77(1):541-5 PMID: 6244566
  17. Isolation and structure of a rat cytochrome c gene.
    J Biol Chem. 1981 Jun 25;256(12):6480-6 PMID: 6263917
  18. Mouse beta 2-microglobulin cDNA clones: a screening procedure for cDNA clones corresponding to rare mRNAs.
    Proc Natl Acad Sci U S A. 1981 Apr;78(4):2253-7 PMID: 6166005
  19. Different transport pathways of individual precursor proteins in mitochondria.
    Eur J Biochem. 1981 Jun 1;116(3):455-60 PMID: 6167439
  20. In vitro synthesis and posttranslational uptake of cytochrome c into isolated mitochondria: role of a specific addressing signal in the apocytochrome.
    Proc Natl Acad Sci U S A. 1981 Jul;78(7):4368-72 PMID: 6270674
  21. Sequence of the yeast iso-1-cytochrome c mRNA.
    J Biol Chem. 1981 Dec 25;256(24):12958-61 PMID: 6273415
  22. Cytochrome c gene-related sequences in mammalian genomes.
    Proc Natl Acad Sci U S A. 1982 Feb;79(3):739-43 PMID: 6278493
  23. Structure of the Schizosaccharomyces pombe cytochrome c gene.
    Mol Cell Biol. 1982 Feb;2(2):106-16 PMID: 6287225
  24. Nonallelic members of the cytochrome c multigene family of the rat may arise through different messenger RNAs.
    Cell. 1983 Feb;32(2):473-82 PMID: 6130852
  25. Studies on transformation of Escherichia coli with plasmids.
    J Mol Biol. 1983 Jun 5;166(4):557-80 PMID: 6345791
  26. Buffer gradient gels and 35S label as an aid to rapid DNA sequence determination.
    Proc Natl Acad Sci U S A. 1983 Jul;80(13):3963-5 PMID: 6575390
  27. Receptor sites involved in posttranslational transport of apocytochrome c into mitochondria: specificity, affinity, and number of sites.
    Proc Natl Acad Sci U S A. 1983 Aug;80(16):4963-7 PMID: 6308663
  28. Evidence for formation of two thioether bonds to link heme to apocytochrome c by partially purified cytochrome c synthetase.
    J Biol Chem. 1983 Sep 25;258(18):10963-6 PMID: 6309825
  29. A simple and very efficient method for generating cDNA libraries.
    Gene. 1983 Nov;25(2-3):263-9 PMID: 6198242
  30. Import of proteins into mitochondria: a 70 kilodalton outer membrane protein with a large carboxy-terminal deletion is still transported to the outer membrane.
    EMBO J. 1983;2(12):2161-8 PMID: 6321150
  31. The complete nucleotide sequence of the Neurospora crassa am (NADP-specific glutamate dehydrogenase) gene.
    Gene. 1983 Dec;26(2-3):253-60 PMID: 6231215
  32. Isolation and characterization of two alleles of the chicken cytochrome c gene.
    Nucleic Acids Res. 1983 Dec 20;11(24):8931-50 PMID: 6324108
  33. Nucleotide sequence of the cloned mRNA and gene of the ADP/ATP carrier from Neurospora crassa.
    EMBO J. 1984 Feb;3(2):377-82 PMID: 6325169
  34. The imported preprotein of the proteolipid subunit of the mitochondrial ATP synthase from Neurospora crassa. Molecular cloning and sequencing of the mRNA.
    EMBO J. 1982;1(5):565-71 PMID: 6329691
  35. Intracellular targeting and import of an F1-ATPase beta-subunit-beta-galactosidase hybrid protein into yeast mitochondria.
    Proc Natl Acad Sci U S A. 1984 Jul;81(13):3983-7 PMID: 6330727
  36. A novel in vitro transcription-translation system: accurate and efficient synthesis of single proteins from cloned DNA sequences.
    EMBO J. 1984 Dec 20;3(13):3143-8 PMID: 6526014
  37. The amino-terminal region of an imported mitochondrial precursor polypeptide can direct cytoplasmic dihydrofolate reductase into the mitochondrial matrix.
    EMBO J. 1984 Dec 20;3(13):3149-56 PMID: 6098467
  38. A 70-kd protein of the yeast mitochondrial outer membrane is targeted and anchored via its extreme amino terminus.
    EMBO J. 1984 Dec 20;3(13):3157-64 PMID: 6396085
  39. Supercoil sequencing: a fast and simple method for sequencing plasmid DNA.
    DNA. 1985 Apr;4(2):165-70 PMID: 3996185
  40. Characterization of a mouse somatic cytochrome c gene and three cytochrome c pseudogenes.
    Nucleic Acids Res. 1985 Jan 25;13(2):617-30 PMID: 2987801
  41. Neurospora crassa cytochrome c. II. Chymotryptic peptides, tryptic peptides, cyanogen bromide peptides, and the complete amino acid sequence.
    J Biol Chem. 1966 Jul 10;241(13):3165-80 PMID: 5950080
  42. A membrane-filter technique for the detection of complementary DNA.
    Biochem Biophys Res Commun. 1966 Jun 13;23(5):641-6 PMID: 5963888
  43. Characterization of two Drosophila melanogaster cytochrome c genes and their transcripts.
    Nucleic Acids Res. 1985 Jan 25;13(2):631-44 PMID: 2987802
  44. Molecular cloning and sequencing of cDNA for yeast porin, an outer mitochondrial membrane protein: a search for targeting signal in the primary structure.
    EMBO J. 1985 Mar;4(3):769-74 PMID: 2408884
  45. Investigations on the insertion of the mitochondrial precursor protein apocytochrome c into model membranes.
    Biochim Biophys Acta. 1985 Sep 10;818(3):398-409 PMID: 2994729
  46. Transport of proteins into mitochondria: a potassium diffusion potential is able to drive the import of ADP/ATP carrier.
    EMBO J. 1985 Nov;4(11):2819-25 PMID: 2998756
  47. 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 Aug;4(8):2061-8 PMID: 2998781
  48. Import of cytochrome c into mitochondria. Cytochrome c heme lyase.
    Eur J Biochem. 1987 Apr 1;164(1):147-57 PMID: 3030750
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1987-07-00
Pages
2131-7
Language
English
Region
England
NLM ID
8208664
PMCID
PMC553605
Subset
IM
Databases
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