Structural properties of substrate proteins determine their proteolysis by the mitochondrial AAA+ protease Pim1

References

Bateman, J.M., Iacovino, M., Perlman, P.S., and Butow, R.A. (2002). Mitochondrial DNA instability mutants of the bifunctional protein Ilv5p have altered organization in mitochondria and are targeted for degradation by Hsp78 and the Pim1p protease. J. Biol. Chem.277, 47946–47953.10.1074/jbc.M209071200Suche in Google Scholar

Beasley, E.M., Müller, S., and Schatz, G. (1993). The signal that sorts yeast cytochrome b₂ to the mitochondrial intermembrane space contains three distinct functional regions. EMBO J.12, 2303–2311.10.1002/j.1460-2075.1993.tb05884.xSuche in Google Scholar

Bota, D.A. and Davies, K.J. (2002). Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat. Cell Biol.4, 674–680.10.1038/ncb836Suche in Google Scholar

Elsasser, S. and Finley, D. (2005). Delivery of ubiquitinated substrates to protein-unfolding machines. Nat. Cell Biol.7, 742–749.10.1038/ncb0805-742Suche in Google Scholar

Esaki, M., Kanamori, T., Nishikawa, S., and Endo, T. (1999). Two distinct mechanisms drive protein translocation across the mitochondrial outer membrane in the late step of the cytochrome b₂ import pathway. Proc. Natl. Acad. Sci. USA96, 11770–11775.10.1073/pnas.96.21.11770Suche in Google Scholar

Flynn, J.M., Neher, S.B., Kim, Y.I., Sauer, R.T., and Baker, T.A. (2003). Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol. Cell11, 671–683.10.1016/S1097-2765(03)00060-1Suche in Google Scholar

Gaume, B., Klaus, C., Ungermann, C., Guiard, B., Neupert, W., and Brunner, M. (1998). Unfolding of preproteins upon import into mitochondria. EMBO J.17, 6497–6507.10.1093/emboj/17.22.6497Suche in Google Scholar

Herman, C., Prakash, S., Lu, C.Z., Matouschek, A., and Gross, C.A. (2003). Lack of a robust unfoldase activity confers a unique level of substrate specificity to the universal AAA protease FtsH. Mol. Cell11, 659–669.10.1016/S1097-2765(03)00068-6Suche in Google Scholar

Hilt, W. and Wolf, D.H. (1996). Proteasomes: destruction as a programme. Trends Biochem. Sci.21, 96–102.10.1016/S0968-0004(96)10012-8Suche in Google Scholar

Hori, O., Ichinoda, F., Tamatani, T., Yamaguchi, A., Sato, N., Ozawa, K., Kitao, Y., Miyazaki, M., Harding, H.P., Ron, D., et al. (2002). Transmission of cell stress from endoplasmic reticulum to mitochondria: enhanced expression of Lon protease. J. Cell Biol.157, 1151–1160.10.1083/jcb.200108103Suche in Google Scholar PubMed PubMed Central

Horwich, A.L., Weber-Ban, E.U., and Finley, D. (1999). Chaperone rings in protein folding and degradation. Proc. Natl. Acad. Sci. USA96, 11033–11040.10.1073/pnas.96.20.11033Suche in Google Scholar

Hoskins, J.R., Pak, M., Maurizi, M.R., and Wickner, S. (1998). The role of the ClpA chaperone in proteolysis by ClpAP. Proc. Natl. Acad. Sci. USA95, 12135–12140.10.1073/pnas.95.21.12135Suche in Google Scholar

Hoskins, J.R., Singh, S.K., Maurizi, M.R., and Wickner, S. (2000). Protein binding and unfolding by the chaperone ClpA and degradation by the protease ClpAP. Proc. Natl. Acad. Sci. USA97, 8892–8897.10.1073/pnas.97.16.8892Suche in Google Scholar

Huang, S., Ratliff, K.S., Schwartz, M.P., Spenner, J.M., and Matouschek, A. (1999). Mitochondria unfold precursor proteins by unraveling them from their N-termini. Nat. Struct. Biol.6, 1132–1138.Suche in Google Scholar

Karzai, A.W., Roche, E.D., and Sauer, R.T. (2000). The SsrA-SmpB system for protein tagging, directed degradation and ribosome rescue. Nat. Struct. Biol.7, 449–455.10.1038/75843Suche in Google Scholar

Langer, T. and Neupert, W. (1996). Regulated protein degradation in mitochondria. Experientia52, 1069–1076.10.1007/BF01952104Suche in Google Scholar

Lee, C., Schwartz, M.P., Prakash, S., Iwakura, M., and Matouschek, A. (2001). ATP-dependent proteases degrade their substrates by processively unraveling them from the degradation signal. Mol. Cell7, 627–637.10.1016/S1097-2765(01)00209-XSuche in Google Scholar

Lim, J.H., Martin, F., Guiard, B., Pfanner, N., and Voos, W. (2001). The mitochondrial Hsp70-dependent import system actively unfolds preproteins and shortens the lag phase of translocation. EMBO J.20, 941–950.10.1093/emboj/20.5.941Suche in Google Scholar

Lupas, A.N. and Martin, J. (2002). AAA proteins. Curr. Opin. Struct. Biol.12, 746–753.10.1016/S0959-440X(02)00388-3Suche in Google Scholar

Neuwald, A.F., Aravind, L., Spouge, J.L., and Koonin, E.V. (1999). AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res.9, 27–43.10.1101/gr.9.1.27Suche in Google Scholar

Ondrovicova, G., Liu, T., Singh, K., Tian, B., Li, H., Gakh, O., Perecko, D., Janata, J., Granot, Z., Orly, J., Kutejova, E., and Suzuki, C.K. (2005). Cleavage site selection within a folded substrate by the ATP-dependent lon protease. J. Biol. Chem.280, 25103–25110.10.1074/jbc.M502796200Suche in Google Scholar PubMed

Pickart, C.M. and Cohen, R.E. (2004). Proteasomes and their kin: proteases in the machine age. Nat. Rev. Mol. Cell Biol.5, 177–187.10.1038/nrm1336Suche in Google Scholar PubMed

Prakash, S., Tian, L., Ratliff, K.S., Lehotzky, R.E., and Matouschek, A. (2004). An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat. Struct. Mol. Biol.11, 830–837.10.1038/nsmb814Suche in Google Scholar PubMed

Rep, M. and Grivell, L.A. (1996). The role of protein degradation in mitochondrial function and biogenesis. Curr. Genet.30, 367–380.10.1007/s002940050145Suche in Google Scholar PubMed

Rep, M., van Dijl, J.M., Suda, K., Schatz, G., Grivell, L.A., and Suzuki, C.K. (1996). Promotion of mitochondrial membrane complex assembly by a proteolytically inactive yeast Lon. Science274, 103–106.10.1126/science.274.5284.103Suche in Google Scholar PubMed

Röttgers, K., Zufall, N., Guiard, B., and Voos, W. (2002). The ClpB homolog Hsp78 is required for the efficient degradation of proteins in the mitochondrial matrix. J. Biol. Chem.277, 45829–45837.10.1074/jbc.M207152200Suche in Google Scholar PubMed

Rousseau, E., Dehay, B., Ben-Haiem, L., Trottier, Y., Morange, M., and Bertolotti, A. (2004). Targeting expression of expanded polyglutamine proteins to the endoplasmic reticulum or mitochondria prevents their aggregation. Proc. Natl. Acad. Sci. USA101, 9648–9653.10.1073/pnas.0403015101Suche in Google Scholar PubMed PubMed Central

Savel'ev, A.S., Novikova, L.A., Kovaleva, I.E., Luzikov, V.N., Neupert, W., and Langer, T. (1998). ATP-dependent proteolysis in mitochondria. m-AAA protease and PIM1 protease exert overlapping substrate specificities and cooperate with the mtHsp70 system. J. Biol. Chem.273, 20596–20602.10.1074/jbc.273.32.20596Suche in Google Scholar PubMed

Schmidt, S., Strub, A., Röttgers, K., Zufall, N., and Voos, W. (2001). The two mitochondrial heat shock proteins 70, Ssc1 and Ssq1, compete for the cochaperone Mge1. J. Mol. Biol.313, 13–26.10.1006/jmbi.2001.5013Suche in Google Scholar PubMed

Smith, C.K., Baker, T.A., and Sauer, R.T. (1999). Lon and Clp family proteases and chaperones share homologous substrate-recognition domains. Proc. Natl. Acad. Sci. USA96, 6678–6682.10.1073/pnas.96.12.6678Suche in Google Scholar PubMed PubMed Central

Stahlberg, H., Kutejova, E., Suda, K., Wolpensinger, B., Lustig, A., Schatz, G., Engel, A., and Suzuki, C.K. (1999). Mitochondrial Lon of Saccharomyces cerevisiae is a ring-shaped protease with seven flexible subunits. Proc. Natl. Acad. Sci. USA96, 6787–6790.10.1073/pnas.96.12.6787Suche in Google Scholar PubMed PubMed Central

Suzuki, C.K., Suda, K., Wang, N., and Schatz, G. (1994). Requirement for the yeast gene LON in intramitochondrial proteolysis and maintenance of respiration. Science264, 273–276.10.1126/science.8146662Suche in Google Scholar

Suzuki, C.K., Rep, M., Maarten van Dijl, J., Suda, K., Grivell, L.A., and Schatz, G. (1997). ATP-dependent proteases that also chaperone protein biogenesis. Trends Biochem. Sci.22, 118–123.10.1016/S0968-0004(97)01020-7Suche in Google Scholar

Teichmann, U., van Dyck, L., Guiard, B., Fischer, H., Glockshuber, R., Neupert, W., and Langer, T. (1996). Substitution of PIM1 protease in mitochondria by Escherichia coli Lon protease. J. Biol. Chem.271, 10137–10142.10.1074/jbc.271.17.10137Suche in Google Scholar

Truscott, K.N., Voos, W., Frazier, A.E., Lind, M., Li, Y., Geissler, A., Dudek, J., Müller, H., Sickmann, A., Meyer, H.E., et al. (2003). A J-protein is an essential subunit of the presequence translocase associated protein import motor of mitochondria. J. Cell Biol.163, 707–713.10.1083/jcb.200308004Suche in Google Scholar

Tsien, R.Y. (1998). The green fluorescent protein. Annu. Rev. Biochem.67, 509–544.10.1146/annurev.biochem.67.1.509Suche in Google Scholar

van Dijl, J.M., Kutejova, E., Suda, K., Perecko, D., Schatz, G., and Suzuki, C.K. (1998). The ATPase and protease domains of yeast mitochondrial Lon: roles in proteolysis and respiration-dependent growth. Proc. Natl. Acad. Sci. USA95, 10584–10589.10.1073/pnas.95.18.10584Suche in Google Scholar

Van Dyck, L., Pearce, D.A., and Sherman, F. (1994). PIM1 encodes a mitochondrial ATP-dependent protease that is required for mitochondrial function in the yeast Saccharomyces cerevisiae. J. Biol. Chem.269, 238–242.10.1016/S0021-9258(17)42340-4Suche in Google Scholar

Vestweber, D. and Schatz, G. (1988). Point mutations destabilizing a precursor protein enhance its post-translational import into mitochondria. EMBO J.7, 1147–1151.10.1002/j.1460-2075.1988.tb02924.xSuche in Google Scholar PubMed PubMed Central

von Ahsen, O., Lim, J.H., Caspers, P., Martin, F., Schönfeld, H.J., Rassow, J., and Pfanner, N. (2000). Cyclophilin-promoted folding of mouse dihydrofolate reductase does not include the slow conversion of the late-folding intermediate to the active enzyme. J. Mol. Biol.297, 809–818.10.1006/jmbi.2000.3574Suche in Google Scholar PubMed

Wagner, I., Arlt, 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, 5135–5145.10.1002/j.1460-2075.1994.tb06843.xSuche in Google Scholar PubMed PubMed Central

Wagner, I., van Dyck, L., Savel'ev, A.S., Neupert, W., and Langer, T. (1997). Autocatalytic processing of the ATP-dependent PIM1 protease: crucial function of a pro-region for sorting to mitochondria. EMBO J.16, 7317–7325.10.1093/emboj/16.24.7317Suche in Google Scholar PubMed PubMed Central

Weber-Ban, E.U., Reid, B.G., Miranker, A.D., and Horwich, A.L. (1999). Global unfolding of a substrate protein by the Hsp100 chaperone ClpA. Nature401, 90–93.10.1038/43481Suche in Google Scholar PubMed

Weissman, A.M. (2001). Themes and variations on ubiquitylation. Nat. Rev. Mol. Cell Biol.2, 169–178.10.1038/35056563Suche in Google Scholar PubMed

Wickner, S., Maurizi, M.R., and Gottesman, S. (1999). Posttranslational quality control: folding, refolding, and degrading proteins. Science286, 1888–1893.10.1126/science.286.5446.1888Suche in Google Scholar PubMed

Xia, Z.-X. and Mathews, F.S. (1990). Molecular structure of flavocytochrome b₂ at 2.4 Å resolution. J. Mol. Biol.212, 837–863.Suche in Google Scholar

Yang, T.T., Cheng, L., and Kain, S.R. (1996). Optimized codon usage and chromophore mutations provide enhanced sensitivity with the green fluorescent protein. Nucleic Acids Res.24, 4592–4593.10.1093/nar/24.22.4592Suche in Google Scholar PubMed PubMed Central

Zhang, M. and Coffino, P. (2004). Repeat sequence of Epstein-Barr virus-encoded nuclear antigen 1 protein interrupts proteasome substrate processing. J. Biol. Chem.279, 8635–8641.10.1074/jbc.M310449200Suche in Google Scholar PubMed

Zhang, M., MacDonald, A.I., Hoyt, M.A., and Coffino, P. (2004). Proteasomes begin ornithine decarboxylase digestion at the C terminus. J. Biol. Chem.279, 20959–20965.10.1074/jbc.M314043200Suche in Google Scholar PubMed