The human mitochondrial import receptor, hTom20p, prevents a cryptic matrix targeting sequence from gaining access to the protein translocation machinery

Journal of Cell Biology

Volumn 134, Issue 2, 1996, Pages 307-313

  McBride, Heidi M ^a   Goping, Ing Swie ^a   Shore, Gordon C ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MATRIX PROTEIN; RECEPTOR; SIGNAL PEPTIDE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HEART MITOCHONDRION; HUMAN; HUMAN TISSUE; LIPID BILAYER; LIVER MITOCHONDRION; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TARGETING; PROTEIN TRANSPORT; RAT; SIGNAL TRANSDUCTION; YEAST;

ANIMALS; BASE SEQUENCE; BIOLOGICAL TRANSPORT; CYTOCHROME REDUCTASES; DNA, FUNGAL; FUNGAL PROTEINS; HUMANS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIA; MITOCHONDRIA, HEART; MITOCHONDRIA, LIVER; MOLECULAR SEQUENCE DATA; PROTEIN SORTING SIGNALS; RATS; RECEPTORS, CELL SURFACE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPECIES SPECIFICITY; TETRAHYDROFOLATE DEHYDROGENASE;

EID: 8944248278     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.134.2.307     Document Type: Article

References (59)

1. Allison, D.S., and G. Schatz. 1986. Artificial mitochondrial presequences. Proc. Natl. Acad. Sci. USA. 83:9011-9015.
2. Attardi, G., and G. Schatz. 1988. The biogenesis of mitochondria. Annu. Rev. Cell Biol. 4:289-333.
3. Baker, A., and G. Schatz. 1987. Sequences from a prokaryotic genome or the mouse dihydrofolate reductase gene can restore the import of a truncated precursor protein into yeast. Proc. Natl. Acad. Sci. USA. 84:3117-3121.
4. Baker, K.P., A. Schaniel, D. Vestweber, and G. Schatz. 1990. A yeast mitochondrial outer membrane protein essential for protein import and cell viability. Nature (Lond.). 348:605-609.
5. Bolliger, L., T. Junne, G. Schatz, and T Lithgow. 1995. Acidic receptor domains on both sides of the outer membrane mediate translocation of precursor proteins into yeast mitochondria. EMBO (Eur. Mol. Biol. Organ.) J. 14:6318-6326.
6. Gasser, S.M., and G. Schatz. 1983. Import of proteins into mitochondria. In vitro studies on the biogenesis of the outer membrane. J. Biol. Chem. 258: 3427-3430.
7. Gavel, Y., and G. von Heijne. 1992. The distribution of charged amino acids in mitochondrial inner membrane proteins suggests different modes of membrane integration for nuclearly and mitochondrially encoded proteins. Eur. J. Biochem. 205:1207-1215.
8. Gillespie, L.L., C. Argan, A.T. Taneja, R.S. Hodges, K.B. Freeman, and G.C. Shore. 1985. A synthetic signal peptide blocks import of precursor proteins destined for the mitochondrial inner membrane or matrix. J. Biol. Chem. 260:16045-16048.
9. Glick, B.S., A. Brandt, K. Cunningham, S. Muller, R.L. Hallberg, and G. Schatz. 1992. Cytochromes c1 and b2 are sorted to the intermembrane space of yeast mitochondria by a stop-transfer mechanism. Cell. 69:809-822.
10. Goping, I.S., D.G. Millar, and G.C. Shore. 1995. Identification of the human mitochondrial protein import receptor, huMas20p. Complementation of Δmas20 in yeast. FEBS (Fed. Eur. Biochem. Soc.) Lett. 373:45-50.
11. Gratzer, S., T. Lithgow, R.E. Bauer, E. Lamping, F. Paltauf, S.D. Kohlwein, V. Haucke, T. Junne, G. Schatz, and M. Horst. 1995. Mas37p, a novel receptor subunit for protein import into mitochondria. J. Cell Biol. 129:25-34.
12. Hachiya, N., T. Alam, Y. Sakasegawa, M. Sakaguchi, K. Mihara, and T. Omura. 1993. A mitochondrial import factor purified from rat liver cytosol is an ATP-dependent conformational modulator for precursor proteins. EMBO (Eur. Mol. Biol. Organ.) J. 12:1579-1586.
13. Hachiya, N., K. Mihara, K. Suda, M. Horst, G. Schatz, and T. Lithgow. 1995. Reconstitution of the initial steps of mitochondrial protein import. Nature (Lond.). 376:705-709.
14. Hahne, K., R. Haucke, L. Ramage, and G. Schatz. 1994. Incomplete arrest in the outer membrane sorts NADH-Cytochrome b5 reductase to two different submitochondrial compartments. Cell. 79:829-839.
15. Hanson, B., S. Nuttal, and N. Hoogenraad. 1996. A receptor for the import of proteins into human mitochondria. Eur. J. Biochem. 235:750-753.
16. Hartl, F.-U., and W. Neupert. 1990. Protein sorting to mitochondria. Evolutionary conservation of folding and assembly. Science (Wash. DC). 247:930-938.
17. Hase, T., U. Muller, H. Reizman, and G. Schatz. 1984. A 70 kDa protein of the mitochondrial outer membrane is targeted and anchored via its extreme amino terminus. EMBO (Eur. Mol. Biol. Organ.) J. 3:3157-3164.
18. Hauke, V., M. Horst, G. Schatz, and T. Lithgow. 1996. The Mas20p and Mas70p subunits of the protein import receptor of yeast mitochondria interact via the tetratricopeptide repeat motif in Mas20p: evidence for a single heterooligomeric receptor. EMBO (Eur. Mol. Biol. Organ.) J. 15:1231-1237.
19. Hines, V., A. Brandt, G. Griffits, H. Horstmann, H. Brütsch, and G. Schutz. 1990. Protein import into yeast mitochondria is accelerated by the outer membrane protein MAS70. EMBO (Eur. Mol. Biol. Organ.) J. 9:3191-3200.
20. Hurt, E.C., and G. Schatz. 1987. A cytosolic protein contains a cryptic mitochondrial targeting signal. Nature (Lond.). 325:499-503.
21. Hurt, E.C., U. Muller, and G. Schatz. 1985. The first twelve amino acids of a yeast outer mitochondrial membrane protein can direct a nuclear-encoded cytochrome oxidase subunit to the mitochondrial inner membrane. EMBO (Eur. Mol. Biol. Organ.) J. 4:3509-3518.
22. Kassenbrock, C.K., W. Cao, and M.G. Douglas. 1993. Genetic and biochemical characterization of ISP6, a small mitochondrial outer membrane protein associated with the protein translocation complex. EMBO (Eur. Mol. Biol. Organ.) J. 12:3023-3034.
23. Kiebler, M., R. Pfaller, T. Sollner, G. Griffiths, H. Horstmann, N. Pfanner, and W. Neupert. 1990. Identification of a mitochondrial receptor complex required for recognition and membrane insertion of precusor proteins. Nature (Lond.). 348:610-616.
24. Kiebler, M., K. Becker, N. Pfanner, and W. Neupert. 1993. Mitochondrial protein import: specific recognition and membrane translocation of preproteins. J. Membr. Biol. 135:191-207.
25. Komiya, T., M. Sakaguchi, and K. Mihara. 1996. Cytoplasmic chaperones determine the targeting pathway of precursor proteins to mitochondria. EMBO (Eur. Mol. Biol. Organ.) J. 407:399-407.
26. Kubrich, M., K. Dietmeier, and N. Pfanner. 1995. Genetic and biochemical dissection of the mitochondrial protein-import machinery. Curr. Genet. 27: 393-403.
27. Li, J.-M., and G.C. Shore. 1992a. Reversal of the orientation of an integral protein of the mitochondrial outer membrane. Science (Wash. DC). 256:1815-1817.
28. Li, J.-M., and G.C. Shore. 1992b. Protein sorting between mitochondrial outer and inner membranes. Insertion of an outer membrane protein into the inner membrane. Biochim. Biophys. Acta. 1106:233-241.
29. Lill, R., and W. Neupert. 1996. Mechanisms of protein import across the mitochondrial outer membrane. Trends Cell Biol. 6:56-61.
30. Lithgow, T., T. Junne, K. Suda, S. Gratzer, and G. Schatz. 1994. The mitochondrial outer membrane protein Mas22p is essential for protein import and viability of yeast. Proc. Natl. Acad. Sci. USA. 91:11973-11977.
31. Lithgow, T., B.S. Glick, and G. Schatz. 1995. The protein import receptor of mitochondria. Trends Biochem. Sci. 20:98-101.
32. Liu, X., A.W. Bell, K.B. Freeman, and G.C. Shore. 1988. Topogenesis of mitochondrial inner membrane uncoupling protein. Re-routing transmembrane segments to the soluble matrix compartment. J. Cell Biol. 107:503-509.
33. Martin, J., K. Mahlke, and N. Pfanner. 1991. Role of an energized inner membrane potential in mitochondrial protein import. Δψ drives the movement of presequences. J. Biol. Chem. 266:18051-18057.
34. Mayer, A., W. Neupert, and R. Lill. 1995. Mitochondrial protein import: reversible binding of the presequence at the trans side of the outer membrane drives partial translocation and unfolding. Cell. 80:127-137.
35. McBride, H.M., D.G. Millar, J.-M. Li, and G.C. Shore. 1992. A signal-anchor sequence selective for the mitochondrial outer membrane. J. Cell Biol. 119: 1451-1457.
36. McBride, H.M., J.R. Silvius, and G.C. Shore. 1995. Insertion of an uncharged polypeptide into the mitochodrial inner membrane does not require a transbilayer electrochemical potential: effects of positive charges. Biochim. Biophys. Acta. 1237:162-168.
37. Mihara, K., and T. Omura. 1996. Cytoplasmic chaperones in precursor targeting to mitochondria: the role of MSF and hsp70. Trends Cell Biol. 6:104-108.
38. Mihara, K., G. Blobel, and R. Sato. 1982. In vitro synthesis and integration into mitochondria of porin, a major protein of the outer mitochondrial membrane of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 79:7102-7106.
39. Miller, J.D., and P. Walter. 1993. A GTPase cycle in initiation of protein translocation across the endoplasmic reticulum membrane. Ciba Found. Symp. 176:147-159.
40. Moczko, M., B. Ehmann, F. Gartner, A. Honlinger, E. Schafer, and N. Pfanner. 1994. Deletion of the receptor MOM19 strongly impairs import of cleavable preproteins into Saccharomyces cerevisiae mitochondria. J. Biol. Chem. 269: 9045-9051.
41. Nakai, M., and T. Endo. 1995. Identification of yeast MAS17 encoding the functional counterpart of the mitochondrial receptor complex protein MOM22 of Neurospora crassa. FEBS (Fed. Eur. Biochem. Soc.) Lett. 357:202-206.
42. Nguyen, M., and G.C. Shore. 1987. Import of hybrid vesicular stomatitis G protein to the mitochondrial inner membrane. J. Biol. Chem. 262:3929-3931.
43. Nguyen, M., C. Argan, C.J. Lusty, and G.C. Shore. 1986. Import and processing of hybrid proteins by mammalian mitochondria in vitro. J. Biol. Chem. 261: 800-805.
44. Nguyen, M., D.G. Millar, V.W. Yong, S.J. Korsmeyer, and G.C. Shore. 1993. Targeting of Bcl-2 to the mitochodrial outer membrane by a COOH-terminal signal-anchor sequence. J. Biol. Chem. 268:25265-25268.
45. Ono, H., and A. Ito. 1984. Transport of the precursor for sulfite oxidase into intermembrane space of liver mitochondria: characterization of import and processing activities. J. Biochem. 95:345-352.
46. Pfaller, R., H.F. Steger, J. Rassow, N. Pfanner, and W. Neupert. 1988. Import pathways of precursor proteins into mitochondria: multiple receptor sites are followed by a common membrane insertion site. J. Cell Biol. 107:2483-2490.
47. Pfanner, N., R. Pfaller, and W. Neupert. 1988. How finicky is mitochondrial protein import? Trends Biochem. Sci. 13:165-167.
48. Pfanner, N., M.G. Douglas, T. Endo, N.J. Hoogenraad, R.E. Jensen, M. Meijer, W. Neupert, G. Schatz, U.K. Schmitz, and G.C. Shore. 1996. Uniform nomenclature for the protein tranport machinery of the mitochondrial membranes. Trends Biochem. Sci. 21:51-52.
49. Ramage, L., T. Junne, K. Hahne, T. Lithgow, and G. Schatz. 1993. Functional cooperation of mitochondrial protein import receptors in yeast. EMBO (Eur. Mol. Biol. Organ.) J. 12:4115-4123.
50. Roise, D., S.J. Horvath, J.M. Tomich, J.H. Richards, and G. Schatz. 1986. A chemically synthesized pre-sequence of an imported mitochondrial protein can form an amphiphilic helix and perturb natural and artificial phospholipid bilayers. EMBO (Eur. Mol. Biol. Organ.) J. 5:1327-1334.
51. Ryan, K.R., and R.E. Jensen. 1995. Protein translocation across mitochondrial membranes: What a long, strange trip it is. Cell. 83:517-519.
52. Schlossmann, J., and W. Neupert. 1995. Assembly of the preprotein receptor MOM72/MAS70 into the protein import complex of the outer membrane of mitochondria. J. Biol. Chem. 270:27116-27121.
53. Seki, N., M. Moczko, T. Nagase, N. Zufall, B. Ehmann, K. Dietmeier, E. Schafer, N. Nomura, and N. Pfanner. 1995. A human homolog of the mitochondrial protein import receptor MOM19 can assemble with the yeast mitochondrial receptor complex. FEBS (Fed. Eur. Biochem. Soc.) Lett. 375: 307-310.
54. Sheffield, W.P., G.C. Shore, and S.K. Randall. 1990. Mitochondrial precursor protein. Effects of 70-kilodalton heat shock protein on polypeptide folding, aggregation, and import competence. J. Biol. Chem. 265:11069-11076.
55. Shore, G.C., H.M. McBride, D.G. Millar, N.A.E. Steenaart, and M. Nguyen. 1995. Import and insertion of proteins into the mitochondrial outer membrane. Eur. J. Biochem. 227:9-18.
56. Smith, M.D., M. Petrak, P.D. Boucher, K.N. Barton, L. Carter, G. Reddy, E. Blachly-Dyson, M. Forte, J. Price, K. Verner, and R.B. McCauley. 1995. Lysine residues at positions 234 and 236 in yeast porin are involved in its assembly into the mitochondrial outer membrane. J. Biol. Chem. 270:28331-28336.
57. Söllner, T., R. Pfaller, G. Griffiths, N. Pfanner, and W. Neupert. 1990. A mitochondrial import receptor for the ADP/ATP carrier. Cell. 62:107-115.
58. Söllner, T., J. Rassow, M. Wiedmann, J. Schlossmann, P. Keil, W. Neupert, and N. Pfanner. 1992. Mapping of the protein import machinery in the mitochondrial outer membrane by crosslinking of translocation intermediates. Nature (Lond.). 355:84-87.
59. Vestweber, D., J. Brunner, A. Baker, and G. Schatz. 1989. A 42K outer-membrane protein is a component of the yeast mitochondrial protein import site. Nature (Lond.). 341:205-209.