Directionality of polypeptide transfer in the mitochondrial pathway of chaperone-mediated protein folding

Biological Chemistry

Volumn 379, Issue 3, 1998, Pages 301-309

  Heyrovská, Neela ^a,e   Frydman, Judith ^b   Höhfeld, Jörg ^c   Hartl, F Ulrich ^d  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^e Weill Cornell Medical Center   (United States)

Author keywords

Chaperonin; GroEl; Hsp60; Hsp70; Mitochondrial protein import; Protein folding in vivo

Indexed keywords

CHAPERONE; CHAPERONIN; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; LUCIFERASE; POLYPEPTIDE; PROTEIN; SIGNAL PEPTIDE;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

EID: 0031896846     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: 10.1515/bchm.1998.379.3.301     Document Type: Article

References (53)

1. Anfinsen, C.B. (1973). Principles that govern the folding of protein chains. Science 181, 223-230.
2. Buchberger, A., Schröder, H., Hesterkamp, T., Schönfeld, H.-J., and Bukau, B. (1996). Substrate shuttling between the DnaK and GroEL systems indicates a chaperone network promoting protein folding. J. Mol. Biol. 261, 328-333.
3. Cheng, M.Y., Hartl, F.U., Martin, J., Pollock, R.A., Kalousek, F., Neupert, W., Hallberg, E.M., Hallberg, R.L., and Horwich, A.L. (1989). Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337, 620-625.
4. Ellis, J. (1987). Proteins as molecular chaperones. Nature 328, 378-379.
5. Ellis, R.J. (1993). The general concept of molecular chaperones. Philos. Trans. R. Soc. Lond. Biol. 339, 257-261.
6. Ellis, R.J., and Hartl, F.U. (1996). Protein folding in the cell: Competing models of chaperonin function. FASEB J. 10, 20-26.
7. Ewalt, K.L., Hendrick, J.P., Houry, W.A., and Hartl, F.U. (1997). In vivo observation of polypeptide flux through the bacterial chaperonin system. Cell 90, 491-500.
8. Frydman, J., and Hartl, F.U. (1996). Principles of chaperone-assisted protein folding: Differences between in vitro and in vivo mechanisms. Science 272, 1497-1502.
9. Frydman, J., Nimmesgern, E., Erdjument-Bromage, H., Wall, J.S., Tempst, P., and Hartl, F.U. (1992). Function in protein folding of TRiC, a cytosolic ring complex containing TCP-1 and structurally related subunits. EMBO J. 11, 4767-4778.
10. Frydman, J., Nimmesgern, E., Ohtsuka, K., and Hartl, F.U. (1994). Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature 370, 111-117.
11. Gaitanaris, G.A., Vysokanov, A., Hung, S.-Z., Gottesman, M., and Gragerov, A. (1994). Successive action of E. coli chaperones in vivo. Mol. Microbiol. 14, 861-869.
12. Georgopoulos, C., and Welch, W.J. (1993). Role of the major heat shock proteins as molecular chaperones. Annu. Rev. Cell Biol. 9, 601-634.
13. Gragerov, A., Nudler, E., Komissarova, N., Gaitanaris, G.A., Gottesman, M.E., and Nikiforov, V. (1992). Cooperation of GroEL/GroES and DnaK/DnaJ heat shock proteins in preventing protein misfolding in Escherichia coli. Proc. Natl. Acad. Sci. USA 89, 10341-10344.
14. Hartl, F.U. (1996). Molecular chaperones in cellular protein folding. Nature 381, 571-580.
15. Hartl, F.U., Ostermann, J., Guiard, B., and Neupert, W. (1987). Successive translocation into and out of the mitochondrial matrix: Targeting of proteins to the intermembrane space by a bipartite signal peptide. Cell 51, 1027-1037.
16. Hayer-Hartl, M.K., Weber, F., and Hartl, F.U. (1996). Mechanism of chaperonin action: GroES binding and release can drive GroEL-mediated protein folding in the absence of ATP hydrolysis. EMBO J. 15, 6111-6121.
17. Hendrick, J.P., Langer, T., Davis, T.A., Hartl, F.U., and Wiedmann, M. (1993). Control of folding and membrane translocation by binding of the chaperone DnaJ to nascent polypeptides. Proc. Natl. Acad. Sci. USA 90, 10216-10220.
18. Höhfeld, J., and Hartl, F.U. (1994a). Post-translational protein import and folding. Current Op. Cell Biol. 6, 499-509.
19. Höhfeld, J., and Hartl, F.U. (1994b). Role of the chaperonin cofactor HsplO in protein folding and sorting in yeast mitochondria. J. Cell Biol. 126, 305-315.
20. Kandror, O., Busconi, L., Sherman, M., and Goldberg, A.L. (1994). Rapid degradation of an abnormal protein in Escherichia coli involves the chaperones GroEL and GroES. J. Biol. Chem. 269, 23575-23582.
21. Kang, P.J., Ostermann, J., Shilling, J., Neupert, W., Craig, E.A., and Pfanner, N. (1990). Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature 348, 137-143.
22. Kudlicki, W., Odom, O.W., Kramer, G., and Hardesty, B. (1994). Chaperone-dependent folding and activation of ribosome-bound nascent rhodanese. Analysis by fluorescence. J. Mol. Biol. 244, 319-331.
23. Langer, T., and Neupert, W. (1996). In: Chaperonins, R.J. Ellis, ed., (San Diego, USA: Academic Press Inc.), pp. 91-106.
24. Langer, T., Lu, C., Echols, H., Flanagan, J., Hayer, M.K., and Hartl, F.U. (1992). Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding. Nature 356, 683-689.
25. Liberek, K., Marszalek, J., Ang, D., Georgopoulos, C., and Zylicz, M. (1991). Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc. Natl. Acad. Sci. USA 88, 2874-2878.
26. Manning-Krieg, U.C., Scherer, P.E., and Schatz, G. (1991). Sequential action of mitochondrial chaperones in protein import into the matrix. EMBO J. 10, 3273-3280.
27. Martin, J. and Hartl, F.U. (1997). The effect of macromolecular crowding on chaperonin-mediated protein folding. Proc. Natl. Acad. Sci. USA 94, 1107-1112.
28. Martin, J., Langer, T., Boteva, R., Schramel, A., Horwich, A.L., and Hartl, F.U. (1991) Chaperonin-mediated protein folding at the surface of groEL through a 'molten globule'-like intermediate. Nature 352, 36-42.
29. Martin, J., Horwich, A.L., and Hartl, F.U. (1992). Prevention of protein denaturation under heat stress by the chaperonin Hsp60. Science 258, 995-998.
30. Martin, J., Mayhew, M., Langer, T., and Hartl, F.U. (1993). The reaction cycle of GroEL and GroES in chaperonin-assisted protein folding. Nature 366, 228-233.
31. Mayhew, M., Da Silva, A.C.R., Martin, J., Erdjument-Bromage, H., Tempst, P. and Hartl, F.U. (1996). Protein folding in the central cavity of the GroEL-GroES chaperonin complex. Nature 379, 420-426.
32. Neupert, W. (1997). Protein import into mitochondria. A. Rev. Biochemistry 66, 863-917.
33. Nimmesgern, E., and Hartl, F.U. (1993). ATP-dependent protein refolding activity in reticulocyte lysate. Evidence for the participation of different chaperone components. FEBS Lett. 331, 25-30.
34. Ostermann, J., Horwich, A.L., Neupert, W., and Hartl, F.-U. (1989). Protein folding in mitochondria requires complex formation with hsp60 and ATP hydrolysis. Nature 341, 125-130.
35. Petit, M.A., Bedale, W., Osipiuk, J., Lu, C., Rajagopalan, M., Mclnerney, P., Goodman, M.F., and Echols, H. (1994). Sequential folding of UmuC by the Hsp70 and Hsp60 chaperone complexes of Escherichia coli. J. Biol. Chem. 269, 23824-23829.
36. Pripbuus, C., Westermann, B., Schmitt, M., Langer, T., Neupert, W., and Schwarz, E. (1996). Role of the mitochondrial DnaJ homologue, Mdj1p, in the prevention of heat-induced protein aggregation. FEBS Lett. 380, 142-146.
37. Rassow, J., Mohrs, K., Koidl, S., Barthelmess, I.B., Pfanner, N., and Tropschug, M. (1995a). Cyclophilin 20 is involved in mitochondrial protein folding in cooperation with molecular chaperones Hsp70 and Hsp60. Mol. Cell. Biol. 15, 2654-2662.
38. Rassow, J., Voos, W., and Pfanner, N. (1995b). Partner proteins determine multiple functions of Hsp70. Trends Cell Biol. 5, 207-212.
39. Rospert, S., Muller, S., Schatz, G., and Glick, B.S. (1994). Fusion proteins containing the cytochrome b2 presequence are sorted to the mitochondrial intermembrane space independently of hsp60. J. Biol. Chem. 269, 17279-17288.
40. Rospert, S., Looser, R., Dubaquie, Y., Matouschek, A., Click, B.S., and Schatz, G. (1996). Hsp60-independent protein folding in the matrix of yeast mitochondria. EMBO J. 15, 764-774.
41. Rowley, N., Prip, B.C., Westermann, B., Brown, C., Schwarz, E., Barrell, B., and Neupert, W. (1994). Mdj1p, a novel chaperone of the DnaJ family, is involved in mitochondrial biogenesis and protein folding. Cell 77, 249-259.
42. Schröder, H., Langer, T., Hartl, F.U., and Bukau, B. (1993). DnaK, DnaJ and GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage. EMBO J. 12, 4137-4144.
43. Sikorski, R.S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
44. Stuart, R., Cyr, D.M., Craig, E.A., and Neupert, W. (1994). Mitochondrial molecular chaperones: their role in protein translocation. Trends in Biochem. Sci. 19, 87-92.
45. Szabo, A., Langer, T., Schroder, H., Flanagan, J., Bukau, B., and Hartl, F.U. (1994). The ATP hydrolysis-dependent reaction cycle of the Escherichia coli Hsp70 system DnaK, DnaJ, and GrpE. Proc. Natl. Acad. Sci. USA 91, 10345-10349.
46. Todd, M.J., Viitanen, P.V., and Lorimer, G.H. (1994). Dynamics of the chaperonin ATPase cycle: implications for facilitated protein folding. Science 265, 659-666.
47. Todd, M.J., Lorimer, G.H., and Thirumalai, D. (1996). Chaperonin-facilitated protein folding: Optimization of rate and yield by an iterative annealing mechanism. Proc. Natl. Acad. Sci. USA 93, 4030-4035.
48. Viebrock, A., Perz and Sebald, W. (1982). The imported preprotein of the proteolipid subunit of the mitochondrial ATP synthase from Neurospora crassa: Molecular cloning and sequencing of them RNA. EMBO J. 1, 565-571.
49. Wagner, I., Arit, H., van Dyck, L., Langer, T., and Neupert, W. (1994). Molecular chaperones cooperate with PIM1 protease in the degradation of misfolded proteins in mitochondria. EMBO J. 13, 5135-5145.
50. Weissman, J.S., Kashi, Y., Fenton, W.A., and Horwich, A.L. (1994). GroEL-mediated protein folding proceeds by multiple rounds of binding and release of nonnative forms. Cell 78, 693-702.
51. Weissman, J.S., Rye, H.S., Fenton, W.A., Beechem, J.M., and Horwich, A.L. (1996). Characterization of the active intermediate of a GroEL-GroES-mediated protein folding reaction. Cell 84, 481-490.
52. Westermann, B., Pripbuus, C., Neupert, W., and Schwarz, E. (1995) The role of the GrpE homologue, Mge1p, in mediating protein import and protein folding in mitochondria. EMBO J. 14, 3452-3460.
53. Zimmermann, S.B., and Minton, A.P. (1993). Macromolecular crowding: Biochemical, biophysical, and physiological consequences. A. Rev. Biophys. Biomol. Struct. 22, 27-65.