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. 1993 Nov;2(11):1901–1917. doi: 10.1002/pro.5560021112

Import of cytochrome b2 to the mitochondrial intermembrane space: the tightly folded heme-binding domain makes import dependent upon matrix ATP.

B S Glick 1, C Wachter 1, G A Reid 1, G Schatz 1
PMCID: PMC2142280  PMID: 8268801

Abstract

Cytochrome b2 is synthesized as a precursor in the cytoplasm and imported to the intermembrane space of yeast mitochondria. We show here that the precursor contains a tightly folded heme-binding domain and that translocation of this domain across the outer membrane requires ATP. Surprisingly, it is ATP in the mitochondrial matrix rather than external ATP that drives import of the heme-binding domain. When the folded structure of the heme-binding domain is disrupted by mutation or by urea denaturation, import and correct processing take place in ATP-depleted mitochondria. These results indicate that (1) cytochrome b2 reaches the intermembrane space without completely crossing the inner membrane, and (2) some precursors fold outside the mitochondria but remain translocation-competent, and import of these precursors in vitro does not require ATP-dependent cytosolic chaperone proteins.

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Selected References

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  1. Arkowitz R. A., Joly J. C., Wickner W. Translocation can drive the unfolding of a preprotein domain. EMBO J. 1993 Jan;12(1):243–253. doi: 10.1002/j.1460-2075.1993.tb05650.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beasley E. M., Müller S., Schatz G. The signal that sorts yeast cytochrome b2 to the mitochondrial intermembrane space contains three distinct functional regions. EMBO J. 1993 Jun;12(6):2303–2311. doi: 10.1002/j.1460-2075.1993.tb05884.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beasley E. M., Wachter C., Schatz G. Putting energy into mitochondrial protein import. Curr Opin Cell Biol. 1992 Aug;4(4):646–651. doi: 10.1016/0955-0674(92)90084-p. [DOI] [PubMed] [Google Scholar]
  4. Beckmann R. P., Mizzen L. E., Welch W. J. Interaction of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly. Science. 1990 May 18;248(4957):850–854. doi: 10.1126/science.2188360. [DOI] [PubMed] [Google Scholar]
  5. Brunt C. E., Cox M. C., Thurgood A. G., Moore G. R., Reid G. A., Chapman S. K. Isolation and characterization of the cytochrome domain of flavocytochrome b2 expressed independently in Escherichia coli. Biochem J. 1992 Apr 1;283(Pt 1):87–90. doi: 10.1042/bj2830087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Caplan A. J., Cyr D. M., Douglas M. G. YDJ1p facilitates polypeptide translocation across different intracellular membranes by a conserved mechanism. Cell. 1992 Dec 24;71(7):1143–1155. doi: 10.1016/s0092-8674(05)80063-7. [DOI] [PubMed] [Google Scholar]
  7. Chen W. J., Douglas M. G. The role of protein structure in the mitochondrial import pathway. Unfolding of mitochondrially bound precursors is required for membrane translocation. J Biol Chem. 1987 Nov 15;262(32):15605–15609. [PubMed] [Google Scholar]
  8. Chirico W. J., Waters M. G., Blobel G. 70K heat shock related proteins stimulate protein translocation into microsomes. Nature. 1988 Apr 28;332(6167):805–810. doi: 10.1038/332805a0. [DOI] [PubMed] [Google Scholar]
  9. Deshaies R. J., Koch B. D., Schekman R. The role of stress proteins in membrane biogenesis. Trends Biochem Sci. 1988 Oct;13(10):384–388. doi: 10.1016/0968-0004(88)90180-6. [DOI] [PubMed] [Google Scholar]
  10. Deshaies R. J., Koch B. D., Werner-Washburne M., Craig E. A., Schekman R. A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature. 1988 Apr 28;332(6167):800–805. doi: 10.1038/332800a0. [DOI] [PubMed] [Google Scholar]
  11. Driessen A. J. Bacterial protein translocation: kinetic and thermodynamic role of ATP and the protonmotive force. Trends Biochem Sci. 1992 Jun;17(6):219–223. doi: 10.1016/0968-0004(92)90381-i. [DOI] [PubMed] [Google Scholar]
  12. Eilers M., Schatz G. Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature. 1986 Jul 17;322(6076):228–232. doi: 10.1038/322228a0. [DOI] [PubMed] [Google Scholar]
  13. Ellis R. J., van der Vies S. M. Molecular chaperones. Annu Rev Biochem. 1991;60:321–347. doi: 10.1146/annurev.bi.60.070191.001541. [DOI] [PubMed] [Google Scholar]
  14. Endo T., Eilers M., Schatz G. Binding of a tightly folded artificial mitochondrial precursor protein to the mitochondrial outer membrane involves a lipid-mediated conformational change. J Biol Chem. 1989 Feb 15;264(5):2951–2956. [PubMed] [Google Scholar]
  15. Gasser S. M., Ohashi A., Daum G., Böhni P. C., Gibson J., Reid G. A., Yonetani T., Schatz G. Imported mitochondrial proteins cytochrome b2 and cytochrome c1 are processed in two steps. Proc Natl Acad Sci U S A. 1982 Jan;79(2):267–271. doi: 10.1073/pnas.79.2.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gervais M., Tegoni M. Spontaneous dissociation of a cytochrome core and a biglobular flavoprotein after mild trypsinolysis of the bifunctional Saccharomyces cerevisiae flavocytochrome b2. Eur J Biochem. 1980 Oct;111(2):357–367. doi: 10.1111/j.1432-1033.1980.tb04949.x. [DOI] [PubMed] [Google Scholar]
  17. Ghrir R., Lederer F. Study of a zone highly sensitive to proteases in flavocytochrome b2 from Saccharomyces cerevisiae. Eur J Biochem. 1981 Nov;120(2):279–287. doi: 10.1111/j.1432-1033.1981.tb05701.x. [DOI] [PubMed] [Google Scholar]
  18. Glick B. S., Beasley E. M., Schatz G. Protein sorting in mitochondria. Trends Biochem Sci. 1992 Nov;17(11):453–459. doi: 10.1016/0968-0004(92)90487-t. [DOI] [PubMed] [Google Scholar]
  19. Glick B. S., Brandt A., Cunningham K., Müller S., Hallberg R. L., Schatz G. Cytochromes c1 and b2 are sorted to the intermembrane space of yeast mitochondria by a stop-transfer mechanism. Cell. 1992 May 29;69(5):809–822. doi: 10.1016/0092-8674(92)90292-k. [DOI] [PubMed] [Google Scholar]
  20. Glick B. S. Protein import into isolated yeast mitochondria. Methods Cell Biol. 1991;34:389–399. doi: 10.1016/s0091-679x(08)61693-3. [DOI] [PubMed] [Google Scholar]
  21. Glick B., Schatz G. Import of proteins into mitochondria. Annu Rev Genet. 1991;25:21–44. doi: 10.1146/annurev.ge.25.120191.000321. [DOI] [PubMed] [Google Scholar]
  22. Glover L. A., Lindsay J. G. Targeting proteins to mitochondria: a current overview. Biochem J. 1992 Jun 15;284(Pt 3):609–620. doi: 10.1042/bj2840609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Guiard B., Lederer F. Complete amino acid sequence of the heme-binding core in bakers' yeast cytochrome b2 (L-(+)-lactate dehydrogenase). Biochimie. 1976;58(3):305–316. doi: 10.1016/s0300-9084(76)80437-3. [DOI] [PubMed] [Google Scholar]
  24. Guiard B., Lederer F., Jacq C. More similarity between bakers'yeast L-(+)-lactate dehydrogenase and liver microsomal cytochrome b5. Nature. 1975 May 29;255(5507):422–423. doi: 10.1038/255422a0. [DOI] [PubMed] [Google Scholar]
  25. Guiard B. Structure, expression and regulation of a nuclear gene encoding a mitochondrial protein: the yeast L(+)-lactate cytochrome c oxidoreductase (cytochrome b2). EMBO J. 1985 Dec 1;4(12):3265–3272. doi: 10.1002/j.1460-2075.1985.tb04076.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hachiya N., Alam R., Sakasegawa Y., Sakaguchi M., Mihara K., Omura T. A mitochondrial import factor purified from rat liver cytosol is an ATP-dependent conformational modulator for precursor proteins. EMBO J. 1993 Apr;12(4):1579–1586. doi: 10.1002/j.1460-2075.1993.tb05802.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hallberg E. M., Shu Y., Hallberg R. L. Loss of mitochondrial hsp60 function: nonequivalent effects on matrix-targeted and intermembrane-targeted proteins. Mol Cell Biol. 1993 May;13(5):3050–3057. doi: 10.1128/mcb.13.5.3050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hannavy K., Rospert S., Schatz G. Protein import into mitochondria: a paradigm for the translocation of polypeptides across membranes. Curr Opin Cell Biol. 1993 Aug;5(4):694–700. doi: 10.1016/0955-0674(93)90142-d. [DOI] [PubMed] [Google Scholar]
  29. Hartl F. U., Neupert W. Protein sorting to mitochondria: evolutionary conservations of folding and assembly. Science. 1990 Feb 23;247(4945):930–938. doi: 10.1126/science.2406905. [DOI] [PubMed] [Google Scholar]
  30. Hartl F. U., Ostermann J., Guiard B., Neupert W. Successive translocation into and out of the mitochondrial matrix: targeting of proteins to the intermembrane space by a bipartite signal peptide. Cell. 1987 Dec 24;51(6):1027–1037. doi: 10.1016/0092-8674(87)90589-7. [DOI] [PubMed] [Google Scholar]
  31. Hurt E. C., Pesold-Hurt B., Schatz G. 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):3149–3156. doi: 10.1002/j.1460-2075.1984.tb02272.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hurt E. C., Pesold-Hurt B., Schatz G. The cleavable prepiece of an imported mitochondrial protein is sufficient to direct cytosolic dihydrofolate reductase into the mitochondrial matrix. FEBS Lett. 1984 Dec 10;178(2):306–310. doi: 10.1016/0014-5793(84)80622-5. [DOI] [PubMed] [Google Scholar]
  33. Hwang S. T., Wachter C., Schatz G. Protein import into the yeast mitochondrial matrix. A new translocation intermediate between the two mitochondrial membranes. J Biol Chem. 1991 Nov 5;266(31):21083–21089. [PubMed] [Google Scholar]
  34. Jensen R. E., Schmidt S., Mark R. J. Mutations in a 19-amino-acid hydrophobic region of the yeast cytochrome c1 presequence prevent sorting to the mitochondrial intermembrane space. Mol Cell Biol. 1992 Oct;12(10):4677–4686. doi: 10.1128/mcb.12.10.4677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Johnson C. M., Cooper A., Stockley P. G. Differential scanning calorimetry of thermal unfolding of the methionine repressor protein (MetJ) from Escherichia coli. Biochemistry. 1992 Oct 13;31(40):9717–9724. doi: 10.1021/bi00155a027. [DOI] [PubMed] [Google Scholar]
  36. Kang P. J., Ostermann J., Shilling J., Neupert W., Craig E. A., Pfanner N. Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature. 1990 Nov 8;348(6297):137–143. doi: 10.1038/348137a0. [DOI] [PubMed] [Google Scholar]
  37. Koll H., Guiard B., Rassow J., Ostermann J., Horwich A. L., Neupert W., Hartl F. U. Antifolding activity of hsp60 couples protein import into the mitochondrial matrix with export to the intermembrane space. Cell. 1992 Mar 20;68(6):1163–1175. doi: 10.1016/0092-8674(92)90086-r. [DOI] [PubMed] [Google Scholar]
  38. Leach F. R., Webster J. J. Commercially available firefly luciferase reagents. Methods Enzymol. 1986;133:51–70. doi: 10.1016/0076-6879(86)33055-6. [DOI] [PubMed] [Google Scholar]
  39. Lill R., Stuart R. A., Drygas M. E., Nargang F. E., Neupert W. Import of cytochrome c heme lyase into mitochondria: a novel pathway into the intermembrane space. EMBO J. 1992 Feb;11(2):449–456. doi: 10.1002/j.1460-2075.1992.tb05074.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Manning-Krieg U. C., Scherer P. E., Schatz G. Sequential action of mitochondrial chaperones in protein import into the matrix. EMBO J. 1991 Nov;10(11):3273–3280. doi: 10.1002/j.1460-2075.1991.tb04891.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Mattingly J. R., Jr, Youssef J., Iriarte A., Martinez-Carrion M. Protein folding in a cell-free translation system. The fate of the precursor to mitochondrial aspartate aminotransferase. J Biol Chem. 1993 Feb 25;268(6):3925–3937. [PubMed] [Google Scholar]
  42. Murakami H., Pain D., Blobel G. 70-kD heat shock-related protein is one of at least two distinct cytosolic factors stimulating protein import into mitochondria. J Cell Biol. 1988 Dec;107(6 Pt 1):2051–2057. doi: 10.1083/jcb.107.6.2051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Murakami K., Tanase S., Morino Y., Mori M. Presequence binding factor-dependent and -independent import of proteins into mitochondria. J Biol Chem. 1992 Jul 5;267(19):13119–13122. [PubMed] [Google Scholar]
  44. Nelson R. J., Ziegelhoffer T., Nicolet C., Werner-Washburne M., Craig E. A. The translation machinery and 70 kd heat shock protein cooperate in protein synthesis. Cell. 1992 Oct 2;71(1):97–105. doi: 10.1016/0092-8674(92)90269-i. [DOI] [PubMed] [Google Scholar]
  45. Neupert W., Hartl F. U., Craig E. A., Pfanner N. How do polypeptides cross the mitochondrial membranes? Cell. 1990 Nov 2;63(3):447–450. doi: 10.1016/0092-8674(90)90437-j. [DOI] [PubMed] [Google Scholar]
  46. Nunnari J., Walter P. Protein targeting to and translocation across the membrane of the endoplasmic reticulum. Curr Opin Cell Biol. 1992 Aug;4(4):573–580. doi: 10.1016/0955-0674(92)90074-m. [DOI] [PubMed] [Google Scholar]
  47. Ono H., Tuboi S. Purification and identification of a cytosolic factor required for import of precursors of mitochondrial proteins into mitochondria. Arch Biochem Biophys. 1990 Aug 1;280(2):299–304. doi: 10.1016/0003-9861(90)90333-t. [DOI] [PubMed] [Google Scholar]
  48. Pfanner N., Hartl F. U., Guiard B., Neupert W. Mitochondrial precursor proteins are imported through a hydrophilic membrane environment. Eur J Biochem. 1987 Dec 1;169(2):289–293. doi: 10.1111/j.1432-1033.1987.tb13610.x. [DOI] [PubMed] [Google Scholar]
  49. Pfanner N., Rassow J., Guiard B., Söllner T., Hartl F. U., Neupert W. Energy requirements for unfolding and membrane translocation of precursor proteins during import into mitochondria. J Biol Chem. 1990 Sep 25;265(27):16324–16329. [PubMed] [Google Scholar]
  50. Pfanner N., Tropschug M., Neupert W. Mitochondrial protein import: nucleoside triphosphates are involved in conferring import-competence to precursors. Cell. 1987 Jun 19;49(6):815–823. doi: 10.1016/0092-8674(87)90619-2. [DOI] [PubMed] [Google Scholar]
  51. Pilon M., Rietveld A. G., Weisbeek P. J., de Kruijff B. Secondary structure and folding of a functional chloroplast precursor protein. J Biol Chem. 1992 Oct 5;267(28):19907–19913. [PubMed] [Google Scholar]
  52. Rassow J., Guiard B., Wienhues U., Herzog V., Hartl F. U., Neupert W. Translocation arrest by reversible folding of a precursor protein imported into mitochondria. A means to quantitate translocation contact sites. J Cell Biol. 1989 Oct;109(4 Pt 1):1421–1428. doi: 10.1083/jcb.109.4.1421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Rassow J., Hartl F. U., Guiard B., Pfanner N., Neupert W. Polypeptides traverse the mitochondrial envelope in an extended state. FEBS Lett. 1990 Nov 26;275(1-2):190–194. doi: 10.1016/0014-5793(90)81469-5. [DOI] [PubMed] [Google Scholar]
  54. Rassow J., Pfanner N. Mitochondrial preproteins en route from the outer membrane to the inner membrane are exposed to the intermembrane space. FEBS Lett. 1991 Nov 18;293(1-2):85–88. doi: 10.1016/0014-5793(91)81157-4. [DOI] [PubMed] [Google Scholar]
  55. Reid G. A., Yonetani T., Schatz G. Import of proteins into mitochondria. Import and maturation of the mitochondrial intermembrane space enzymes cytochrome b2 and cytochrome c peroxidase in intact yeast cells. J Biol Chem. 1982 Nov 10;257(21):13068–13074. [PubMed] [Google Scholar]
  56. Rothman J. E. Polypeptide chain binding proteins: catalysts of protein folding and related processes in cells. Cell. 1989 Nov 17;59(4):591–601. doi: 10.1016/0092-8674(89)90005-6. [DOI] [PubMed] [Google Scholar]
  57. 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 Sep;3(9):2137–2143. doi: 10.1002/j.1460-2075.1984.tb02103.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Schatz G. 17th Sir Hans Krebs lecture. Signals guiding proteins to their correct locations in mitochondria. Eur J Biochem. 1987 May 15;165(1):1–6. doi: 10.1111/j.1432-1033.1987.tb11186.x. [DOI] [PubMed] [Google Scholar]
  59. Scherer P. E., Krieg U. C., Hwang S. T., Vestweber D., Schatz G. A precursor protein partly translocated into yeast mitochondria is bound to a 70 kd mitochondrial stress protein. EMBO J. 1990 Dec;9(13):4315–4322. doi: 10.1002/j.1460-2075.1990.tb07880.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Schleyer M., Neupert W. Transport of proteins into mitochondria: translocational intermediates spanning contact sites between outer and inner membranes. Cell. 1985 Nov;43(1):339–350. doi: 10.1016/0092-8674(85)90039-x. [DOI] [PubMed] [Google Scholar]
  61. Schneider A., Behrens M., Scherer P., Pratje E., Michaelis G., Schatz G. Inner membrane protease I, an enzyme mediating intramitochondrial protein sorting in yeast. EMBO J. 1991 Feb;10(2):247–254. doi: 10.1002/j.1460-2075.1991.tb07944.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Schwarz E., Seytter T., Guiard B., Neupert W. Targeting of cytochrome b2 into the mitochondrial intermembrane space: specific recognition of the sorting signal. EMBO J. 1993 Jun;12(6):2295–2302. doi: 10.1002/j.1460-2075.1993.tb05883.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Segui-Real B., Stuart R. A., Neupert W. Transport of proteins into the various subcompartments of mitochondria. FEBS Lett. 1992 Nov 16;313(1):2–7. doi: 10.1016/0014-5793(92)81171-h. [DOI] [PubMed] [Google Scholar]
  64. Simon S. M., Peskin C. S., Oster G. F. What drives the translocation of proteins? Proc Natl Acad Sci U S A. 1992 May 1;89(9):3770–3774. doi: 10.1073/pnas.89.9.3770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Skerjanc I. S., Sheffield W. P., Randall S. K., Silvius J. R., Shore G. C. Import of precursor proteins into mitochondria: site of polypeptide unfolding. J Biol Chem. 1990 Jun 5;265(16):9444–9451. [PubMed] [Google Scholar]
  66. 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 Dec 20;3(13):3143–3148. doi: 10.1002/j.1460-2075.1984.tb02271.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Teintze M., Slaughter M., Weiss H., Neupert W. Biogenesis of mitochondrial ubiquinol:cytochrome c reductase (cytochrome bc1 complex). Precursor proteins and their transfer into mitochondria. J Biol Chem. 1982 Sep 10;257(17):10364–10371. [PubMed] [Google Scholar]
  68. Wachter C., Schatz G., Glick B. S. Role of ATP in the intramitochondrial sorting of cytochrome c1 and the adenine nucleotide translocator. EMBO J. 1992 Dec;11(13):4787–4794. doi: 10.1002/j.1460-2075.1992.tb05584.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Wienhues U., Becker K., Schleyer M., Guiard B., Tropschug M., Horwich A. L., Pfanner N., Neupert W. Protein folding causes an arrest of preprotein translocation into mitochondria in vivo. J Cell Biol. 1991 Dec;115(6):1601–1609. doi: 10.1083/jcb.115.6.1601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Wienhues U., Neupert W. Protein translocation across mitochondrial membranes. Bioessays. 1992 Jan;14(1):17–23. doi: 10.1002/bies.950140105. [DOI] [PubMed] [Google Scholar]
  71. Xia Z. X., Mathews F. S. Molecular structure of flavocytochrome b2 at 2.4 A resolution. J Mol Biol. 1990 Apr 20;212(4):837–863. doi: 10.1016/0022-2836(90)90240-M. [DOI] [PubMed] [Google Scholar]
  72. Zimmermann R., Sagstetter M., Lewis M. J., Pelham H. R. Seventy-kilodalton heat shock proteins and an additional component from reticulocyte lysate stimulate import of M13 procoat protein into microsomes. EMBO J. 1988 Sep;7(9):2875–2880. doi: 10.1002/j.1460-2075.1988.tb03144.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. van Loon A. P., Brändli A. W., Pesold-Hurt B., Blank D., Schatz G. Transport of proteins to the mitochondrial intermembrane space: the 'matrix-targeting' and the 'sorting' domains in the cytochrome c1 presequence. EMBO J. 1987 Aug;6(8):2433–2439. doi: 10.1002/j.1460-2075.1987.tb02522.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. van Loon A. P., Brändli A. W., Schatz G. The presequences of two imported mitochondrial proteins contain information for intracellular and intramitochondrial sorting. Cell. 1986 Mar 14;44(5):801–812. doi: 10.1016/0092-8674(86)90846-9. [DOI] [PubMed] [Google Scholar]
  75. van Loon A. P., Schatz G. Transport of proteins to the mitochondrial intermembrane space: the 'sorting' domain of the cytochrome c1 presequence is a stop-transfer sequence specific for the mitochondrial inner membrane. EMBO J. 1987 Aug;6(8):2441–2448. doi: 10.1002/j.1460-2075.1987.tb02523.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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