Impact of the N-terminal amino acid on targeted protein degradation
-
, and
Abstract
The N-terminus of any protein may be used as a destabilization signal for targeted protein degradation. In the eukaryotic cytosol, the signal – the so-called N-degron – is recognized for degradation by (i) the N-end rule, a well-described degradation process involving ɛ-ubiquitination; or (ii) N-terminal ubiquitination, a more recently described pathway. Dedicated E3 ubiquitin ligases known as N-recognins then act on the protein. The proteolytic pathways involve ATP-dependent chambered proteases, such as the 26S proteasome in the cytosol, which generate short oligopeptides. The N-terminus of the polypeptide chain is also important for post-proteasome degradation by specific aminopeptidases, which complete peptide cleavage to generate free amino acids. Finally, in each compartment of the eukaryotic cell, N-terminal methionine excision creates a variety of N-termini for mature proteins. It has recently been shown that the N-terminal methionine excision pathway has a major impact early in targeted protein degradation.
References
Adam, Z., Adamska, I., Nakabayashi, K., Ostersetzer, O., Haussuhl, K., Manuell, A., Zheng, B., Vallon, O., Rodermel, S.R., Shinozaki, K., and Clarke, A.K. (2001). Chloroplast and mitochondrial proteases in Arabidopsis.A proposed nomenclature. Plant Physiol.125, 1912–1918.Search in Google Scholar
Adam, Z. and Clarke, A.K. (2002). Cutting edge of chloroplast proteolysis. Trends Plant Sci.7, 451–456.10.1016/S1360-1385(02)02326-9Search in Google Scholar
Adams, J.M. (1968). On the release of the formyl group from nascent protein. J. Mol. Biol.33, 571–589.10.1016/0022-2836(68)90307-0Search in Google Scholar
Ades, S.E. (2004). Proteolysis: Adaptor, adaptor, catch me a catch. Curr. Biol.14, R924–926.10.1016/j.cub.2004.10.015Search in Google Scholar
Arfin, S.M., Kendall, R.L., Hall, L., Weaver, L.H., Stewart, A.E., Matthews, B.W., and Bradshaw, R.A. (1995). Eukaryotic methionyl aminopeptidases: two classes of cobalt-dependent enzymes. Proc. Natl. Acad. Sci. USA92, 7714–7718.10.1073/pnas.92.17.7714Search in Google Scholar
Bachmair, A. and Varshavsky, A. (1989). The degradation signal in a short-lived protein. Cell56, 1019–1032.10.1016/0092-8674(89)90635-1Search in Google Scholar
Bachmair, A., Finley, D., and Varshavsky, A. (1986). In vivo half-life of a protein is a function of its amino-terminal residue. Science234, 179–186.10.1126/science.3018930Search in Google Scholar PubMed
Baldwin, E.T., Harris, M.S., Yem, A.W., Wolfe, C.L., Vosters, A.F., Curry, K.A., Murray, R.W., Bock, J.H., Marshall, V.P., Cialdella, J.I., et al. (2002). Crystal structure of type II peptide deformylase from Staphylococcus aureus. J. Biol. Chem.277, 31163–31171.10.1074/jbc.M202750200Search in Google Scholar PubMed
Bartling, D. and Weiler, E.W. (1992). Leucine aminopeptidase from Arabidopsis thaliana. Molecular evidence for a phylogenetically conserved enzyme of protein turnover in higher plants. Eur. J. Biochem.205, 425–431.Search in Google Scholar
Bazan, J.F., Weaver, L.H., Roderick, S.L., Huber, R., and Matthews, B.W. (1994). Sequence and structure comparison suggest that methionine aminopeptidase, prolidase, aminopeptidase P, and creatinase share a common fold. Proc. Natl. Acad. Sci. USA91, 2473–2477.10.1073/pnas.91.7.2473Search in Google Scholar PubMed PubMed Central
Ben-Bassat, A., Bauer, K., Chang, S.Y., Myambo, K., Boosman, A., and Chang, S. (1987). Processing of the initiation methionine from proteins: properties of the Escherichia coli methionine aminopeptidase and its gene structure. J. Bacteriol.169, 751–757.10.1128/jb.169.2.751-757.1987Search in Google Scholar PubMed PubMed Central
Beninga, J., Rock, K.L., and Goldberg, A.L. (1998). Interferon-gamma can stimulate post-proteasomal trimming of the N terminus of an antigenic peptide by inducing leucine aminopeptidase. J. Biol. Chem.273, 18734–18742.10.1074/jbc.273.30.18734Search in Google Scholar PubMed
Ben-Saadon, R., Fajerman, I., Ziv, T., Hellman, U., Schwartz, A.L., and Ciechanover, A. (2004). The tumor suppressor protein p16(INK4a) and the human papillomavirus oncoprotein-58 E7 are naturally occurring lysine-less proteins that are degraded by the ubiquitin system. Direct evidence for ubiquitination at the N-terminal residue. J. Biol. Chem.279, 41414–41421.Search in Google Scholar
Boisson, B. and Meinnel, T. (2003). A continuous assay of myristoyl-CoA:protein N-myristoyltransferase for proteomic analysis. Anal. Biochem.322, 116–123.10.1016/j.ab.2003.07.007Search in Google Scholar
Boisson, B., Giglione, C., and Meinnel, T. (2003). Unexpected protein families including cell defense components feature in the N-myristoylome of a higher eukaryote. J. Biol. Chem.278, 43418–43429.10.1074/jbc.M307321200Search in Google Scholar
Book, A.J., Yang, P., Scalf, M., Smith, L.M., and Vierstra, R.D. (2005). Tripeptidyl peptidase II. An oligomeric protease complex from Arabidopsis. Plant Physiol.138, 1046–1057.10.1104/pp.104.057406Search in Google Scholar
Botbol, V., and Scornik, O.A. (1983). Peptide intermediates in the degradation of cellular proteins. Bestatin permits their accumulation in mouse liver in vivo. J. Biol. Chem.258, 1942–1949.Search in Google Scholar
Boxem, M., Tsai, C.W., Zhang, Y., Saito, R.M., and Liu, J.O. (2004). The C. elegans methionine aminopeptidase 2 analog map-2 is required for germ cell proliferation. FEBS Lett.576, 245–250.Search in Google Scholar
Bradshaw, R.A., Brickey, W.W., and Walker, K.W. (1998). N-terminal processing: the methionine aminopeptidase and N α-acetyl transferase families. Trends Biochem. Sci.23, 263–267.10.1016/S0968-0004(98)01227-4Search in Google Scholar
Brannigan, J.A., Dodson, G., Duggleby, H.J., Moody, P.C., Smith, J.L., Tomchick, D.R., and Murzin, A.G. (1995). A protein catalytic framework with an N-terminal nucleophile is capable of self-activation. Nature378, 416–419.10.1038/378416a0Search in Google Scholar PubMed
Chang, S.Y., McGary, E.C., and Chang, S. (1989). Methionine aminopeptidase gene of Escherichia coli is essential for cell growth. J. Bacteriol.171, 4071–4072.10.1128/jb.171.7.4071-4072.1989Search in Google Scholar PubMed PubMed Central
Chao, W.S., Gu, Y.Q., Pautot, V.V., Bray, E.A., and Walling, L.L. (1999). Leucine aminopeptidase RNAs, proteins, and activities increase in response to water deficit, salinity, and the wound signals systemin, methyl jasmonate, and abscisic acid. Plant Physiol.120, 979–992.10.1104/pp.120.4.979Search in Google Scholar PubMed PubMed Central
Chen, D.Z., Patel, D.V., Hackbarth, C.J., Wang, W., Dreyer, G., Young, D.C., Margolis, P.S., Wu, C., Ni, Z.J., Trias, J., et al. (2000). Actinonin, a naturally occurring antibacterial agent, is a potent deformylase inhibitor. Biochemistry39, 1256–12562.10.1021/bi992245ySearch in Google Scholar PubMed
Chen, S., Vetro, J.A., and Chang, Y.H. (2002). The specificity in vivo of two distinct methionine aminopeptidases in Saccharomyces cerevisiae. Arch. Biochem. Biophys.398, 87–93.10.1006/abbi.2001.2675Search in Google Scholar PubMed
Choi, K.H. and Licht, S. (2005). Control of peptide product sizes by the energy-dependent protease ClpAP. Biochemistry44, 13921–13931.10.1021/bi0505060Search in Google Scholar PubMed
Ciechanover, A. (1998). The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J.17, 7151–7160.10.1093/emboj/17.24.7151Search in Google Scholar
Ciechanover, A. (2005). Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat. Rev. Mol. Cell Biol.6, 79–87.10.1038/nrm1552Search in Google Scholar
Ciechanover, A. and Ben-Saadon, R. (2004). N-terminal ubiquitination: more protein substrates join in. Trends Cell Biol.14, 103–106.10.1016/j.tcb.2004.01.004Search in Google Scholar
Colombo, S., Longhi, R., Alcaro, S., Ortuso, F., Sprocati, T., Flora, A., and Borgese, N. (2005). N-myristoylation determines dual targeting of mammalian NADH-cytochrome b5 reductase to ER and mitochondrial outer membranes by a mechanism of kinetic partitioning. J. Cell Biol.168, 735–745.10.1083/jcb.200407082Search in Google Scholar
Dardel, F., Ragusa, S., Lazennec, C., Blanquet, S., and Meinnel, T. (1998). Solution structure of nickel-peptide deformylase. J. Mol. Biol.280, 501–513.10.1006/jmbi.1998.1882Search in Google Scholar
Datta, B. (2000). MAPs and POEP of the roads from prokaryotic to eukaryotic kingdoms. Biochimie82, 95–107.10.1016/S0300-9084(00)00383-7Search in Google Scholar
Datta, R., Choudhury, P., Ghosh, A., and Datta, B. (2003). A glycosylation site, 60SGTS63, of p67 is required for its ability to regulate the phosphorylation and activity of eukaryotic initiation factor 2a. Biochemistry42, 5453–5460.10.1021/bi020699gSearch in Google Scholar
Dougan, D.A., Mogk, A., Zeth, K., Turgay, K., and Bukau, B. (2002). AAA+ proteins and substrate recognition, it all depends on their partner in crime. FEBS Lett.529, 6–10.10.1016/S0014-5793(02)03179-4Search in Google Scholar
Ducker, C.E., Upson, J.J., French, K.J., and Smith, C.D. (2005). Two N-myristoyltransferase isozymes play unique roles in protein myristoylation, proliferation, and apoptosis. Mol. Cancer Res.3, 463–476.10.1158/1541-7786.MCR-05-0037Search in Google Scholar PubMed PubMed Central
Dummitt, B., Micka, W.S., and Chang, Y.H. (2005). Yeast glutamine-fructose-6-phosphate aminotransferase (Gfa1) requires methionine aminopeptidase activity for proper function. J. Biol. Chem.280, 14356–14360.10.1074/jbc.M501059200Search in Google Scholar PubMed
Duronio, R.J., Towler, D.A., Heuckeroth, R.O., and Gordon, J.I. (1989). Disruption of the yeast N-myristoyl transferase gene causes recessive lethality. Science243, 796–800.10.1126/science.2644694Search in Google Scholar
Fieulaine, S., Juillan-Binard, C., Serero, A., Dardel, F., Giglione, C., Meinnel, T., and Ferrer, J.L. (2005). The crystal structure of mitochondrial (type 1A) peptide deformylase provides clear guidelines for the design of inhibitors specific for the bacterial forms. J. Biol. Chem.280, 42315–42324.10.1074/jbc.M507155200Search in Google Scholar
Flinta, C., Persson, B., Jornvall, H., and von Heijne, G. (1986). Sequence determinants of cytosolic N-terminal protein processing. Eur. J. Biochem.154, 193–196.10.1111/j.1432-1033.1986.tb09378.xSearch 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)00060-1Search in Google Scholar
Frick, L. and Wolfenden, R. (1985). Mechanistic implications of the inhibition of peptidases by amino aldehydes and bestatin. Biochim. Biophys. Acta829, 311–318.10.1016/0167-4838(85)90238-9Search in Google Scholar
Fry, K.T. and Lamborg, M.R. (1967). Amidohydrolase activity of Escherichia coli extracts with formylated amino acids and dipeptides as substrates. J. Mol. Biol.28, 423–433.10.1016/S0022-2836(67)80091-3Search in Google Scholar
Giglione, C. and Meinnel, T. (2001). Organellar peptide deformylases: universality of the N-terminal methionine cleavage mechanism. Trends Plant Sci.6, 566–572.10.1016/S1360-1385(01)02151-3Search in Google Scholar
Giglione, C., Serero, A., Pierre, M., Boisson, B., and Meinnel, T. (2000). Identification of eukaryotic peptide deformylases reveals universality of N-terminal protein processing mechanisms. EMBO J.19, 5916–5929.10.1093/emboj/19.21.5916Search in Google Scholar PubMed PubMed Central
Giglione, C., Vallon, O., and Meinnel, T. (2003). Control of protein life-span by N-terminal methionine excision. EMBO J.22, 13–23.10.1093/emboj/cdg007Search in Google Scholar PubMed PubMed Central
Giglione, C., Boularot, A., and Meinnel, T. (2004). Protein N-terminal methionine excision. Cell Mol. Life Sci.61, 1455–1474.10.1007/s00018-004-3466-8Search in Google Scholar PubMed
Glotzer, M., Murray, A.W., and Kirschner, M.W. (1991). Cyclin is degraded by the ubiquitin pathway. Nature349, 132–138.10.1038/349132a0Search in Google Scholar
Gonda, D.K., Bachmair, A., Wunning, I., Tobias, J.W., Lane, W.S., and Varshavsky, A. (1989). Universality and structure of the N-end rule. J. Biol. Chem.264, 16700–16712.10.1016/S0021-9258(19)84762-2Search in Google Scholar
Gribun, A., Kimber, M.S., Ching, R., Sprangers, R., Fiebig, K.M., and Houry, W.A. (2005). The ClpP double ring tetradecameric protease exhibits plastic ring-ring interactions, and the N-termini of its subunits form flexible loops that are essential for ClpXP and ClpAP complex formation. J. Biol. Chem.280, 16185–16196.10.1074/jbc.M414124200Search in Google Scholar
Gu, Y.Q., Chao, W.S., and Walling, L.L. (1996). Localization and post-translational processing of the wound-induced leucine aminopeptidase proteins of tomato. J. Biol. Chem.271, 25880–25887.10.1074/jbc.271.42.25880Search in Google Scholar
Gu, Y.Q., Holzer, F.M., and Walling, L.L. (1999). Overexpression, purification and biochemical characterization of the wound-induced leucine aminopeptidase of tomato. Eur. J. Biochem.263, 726–735.10.1046/j.1432-1327.1999.00548.xSearch in Google Scholar
Guilloteau, J.P., Mathieu, M., Giglione, C., Blanc, V., Dupuy, A., Chevrier, M., Gil, P., Famechon, A., Meinnel, T., and Mikol, V. (2002). The crystal structures of four peptide deformylases bound to the antibiotic actinonin reveal two distinct types: a platform for the structure-based design of antibacterial agents. J. Mol. Biol.320, 951–962.10.1016/S0022-2836(02)00549-1Search in Google Scholar
Halperin, T., Zheng, B., Itzhaki, H., Clarke, A.K., and Adam, Z. (2001). Plant mitochondria contain proteolytic and regulatory subunits of the ATP-dependent Clp protease. Plant Mol. Biol.45, 461–468.10.1023/A:1010677220323Search in Google Scholar
Hara-Nishimura, I., Hatsugai, N., Nakaune, S., Kuroyanagi, M., and Nishimura, M. (2005). Vacuolar processing enzyme: an executor of plant cell death. Curr. Opin. Plant Biol.8, 404–408.10.1016/j.pbi.2005.05.016Search in Google Scholar PubMed
Hattori, A. and Tsujimoto, M. (2004). Processing of antigenic peptides by aminopeptidases. Biol. Pharm. Bull.27, 777–780.10.1248/bpb.27.777Search in Google Scholar PubMed
Hershko, A. and Ciechanover, A. (1998). The ubiquitin system. Annu. Rev. Biochem.67, 425–479.10.1146/annurev.biochem.67.1.425Search in Google Scholar PubMed
Hipp, M.S., Kalveram, B., Raasi, S., Groettrup, M., and Schmidtke, G. (2005). FAT10, a ubiquitin-independent signal for proteasomal degradation. Mol. Cell Biol.25, 3483–3491.10.1128/MCB.25.9.3483-3491.2005Search in Google Scholar PubMed PubMed Central
Hirel, P.H., Schmitter, M.J., Dessen, P., Fayat, G., and Blanquet, S. (1989). Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the side-chain length of the penultimate amino acid. Proc. Natl. Acad. Sci. USA86, 8247–8251.10.1073/pnas.86.21.8247Search in Google Scholar PubMed PubMed Central
Hu, R.G., Sheng, J., Qi, X., Xu, Z., Takahashi, T.T., and Varshavsky, A. (2005). The N-end rule pathway as a nitric oxide sensor controlling the levels of multiple regulators. Nature437, 981–986.10.1038/nature04027Search in Google Scholar PubMed
Johnson, E.S., Ma, P.C., Ota, I.M., and Varshavsky, A. (1995). A proteolytic pathway that recognizes ubiquitin as a degradation signal. J. Biol. Chem.270, 17442–17456.10.1074/jbc.270.29.17442Search in Google Scholar PubMed
Kang, S.G., Dimitrova, M.N., Ortega, J., Ginsburg, A., and Maurizi, M.R. (2005). Human mitochondrial ClpP is a stable heptamer that assembles into a tetradecamer in the presence of ClpX. J. Biol. Chem.280, 35424–35432.10.1074/jbc.M507240200Search in Google Scholar PubMed
Keller, J.N., Dimayuga, E., Chen, Q., Thorpe, J., Gee, J., and Ding, Q. (2004). Autophagy, proteasomes, lipofuscin, and oxidative stress in the aging brain. Int. J. Biochem. Cell Biol.36, 2376–2391.10.1016/j.biocel.2004.05.003Search in Google Scholar PubMed
Kisselev, A.F., Akopian, T.N., Woo, K.M., and Goldberg, A.L. (1999). The sizes of peptides generated from protein by mammalian 26 and 20 S proteasomes. Implications for understanding the degradative mechanism and antigen presentation. J. Biol. Chem.274, 3363–3371.10.1074/jbc.274.6.3363Search in Google Scholar PubMed
Kozak, M. (1983). Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles. Microbiol. Rev.47, 1–45.10.1128/mr.47.1.1-45.1983Search in Google Scholar PubMed PubMed Central
Kuo, M.L., den Besten, W., Bertwistle, D., Roussel, M.F., and Sherr, C.J. (2004). N-Terminal polyubiquitination and degradation of the Arf tumor suppressor. Genes Dev.18, 1862–1874.10.1101/gad.1213904Search in Google Scholar PubMed PubMed Central
Kwon, Y.T., Balogh, S.A., Davydov, I.V., Kashina, A.S., Yoon, J.K., Xie, Y., Gaur, A., Hyde, L., Denenberg, V.H., and Varshavsky, A. (2000). Altered activity, social behavior, and spatial memory in mice lacking the NTAN1p amidase and the asparagine branch of the N-end rule pathway. Mol. Cell. Biol.20, 4135–4148.10.1128/MCB.20.11.4135-4148.2000Search in Google Scholar PubMed PubMed Central
Kwon, Y.T., Kashina, A.S., Davydov, I.V., Hu, R.G., An, J.Y., Seo, J.W., Du, F., and Varshavsky, A. (2002). An essential role of N-terminal arginylation in cardiovascular development. Science297, 96–99.10.1126/science.1069531Search in Google Scholar
Kwon, Y.T., Xia, Z., An, J.Y., Tasaki, T., Davydov, I.V., Seo, J.W., Sheng, J., Xie, Y., and Varshavsky, A. (2003). Female lethality and apoptosis of spermatocytes in mice lacking the UBR2 ubiquitin ligase of the N-end rule pathway. Mol. Cell. Biol.23, 8255–8271.10.1128/MCB.23.22.8255-8271.2003Search in Google Scholar
Lee, M.J., Tasaki, T., Moroi, K., An, J.Y., Kimura, S., Davydov, I.V., and Kwon, Y.T. (2005). RGS4 and RGS5 are in vivo substrates of the N-end rule pathway. Proc. Natl. Acad. Sci. USA102, 15030–15035.10.1073/pnas.0507533102Search in Google Scholar
Levy, F., Johnsson, N., Rumenapf, T., and Varshavsky, A. (1996). Using ubiquitin to follow the metabolic fate of a protein. Proc. Natl. Acad. Sci. USA93, 4907–4912.10.1073/pnas.93.10.4907Search in Google Scholar
Li, X., and Chang, Y.H. (1995). Amino-terminal protein processing in Saccharomyces cerevisiae is an essential function that requires two distinct methionine aminopeptidases. Proc. Natl. Acad. Sci. USA92, 12357–12361.10.1073/pnas.92.26.12357Search in Google Scholar
Liu, S., Widom, J., Kemp, C.W., Crews, C.M., and Clardy, J. (1998). Structure of human methionine aminopeptidase-2 complexed with fumagillin. Science282, 1324–1327.10.1126/science.282.5392.1324Search in Google Scholar
Maurer-Stroh, S., Eisenhaber, B., and Eisenhaber, F. (2002). N-Terminal N-myristoylation of proteins: prediction of substrate proteins from amino acid sequence. J. Mol. Biol.317, 541–557.10.1006/jmbi.2002.5426Search in Google Scholar
Meinnel, T. (2000). Peptide deformylase of eukaryotic protists: a target for new antiparasitic agents? Parasitol. Today16, 165–168.10.1016/S0169-4758(99)01627-0Search in Google Scholar
Meinnel, T. and Blanquet, S. (1994). Characterization of the Thermus thermophilus locus encoding peptide deformylase and methionyl-tRNA(fMet) formyltransferase. J. Bacteriol.176, 7387–7390.10.1128/jb.176.23.7387-7390.1994Search in Google Scholar
Meinnel, T., Mechulam, Y., and Blanquet, S. (1993). Methionine as translation start signal: a review of the enzymes of the pathway in Escherichia coli. Biochimie75, 1061–1075.10.1016/0300-9084(93)90005-DSearch in Google Scholar
Meinnel, T., Blanquet, S., and Dardel, F. (1996). A new subclass of the zinc metalloproteases superfamily revealed by the solution structure of peptide deformylase. J. Mol. Biol.262, 375–386.10.1006/jmbi.1996.0521Search in Google Scholar PubMed
Meinnel, T., Peynot, P., and Giglione, C. (2005). Processed N-termini of mature proteins in higher eukaryotes and their major contribution to dynamic proteomics. Biochimie87, 701–712.10.1016/j.biochi.2005.03.011Search in Google Scholar PubMed
Mitsiades, C.S., Mitsiades, N., Hideshima, T., Richardson, P.G., and Anderson, K.C. (2005). Proteasome inhibitors as therapeutics. Essays Biochem.41, 205–218.10.1042/bse0410205Search in Google Scholar
Nishizawa, M., Okazaki, K., Furuno, N., Watanabe, N., and Sagata, N. (1992). The ‘second-codon rule’ and autophosphorylation govern the stability and activity of Mos during the meiotic cell cycle in Xenopus oocytes. EMBO J.11, 2433–2446.10.1002/j.1460-2075.1992.tb05308.xSearch in Google Scholar PubMed PubMed Central
Nishizawa, M., Furuno, N., Okazaki, K., Tanaka, H., Ogawa, Y., and Sagata, N. (1993). Degradation of Mos by the N-terminal proline (Pro2)-dependent ubiquitin pathway on fertilization of Xenopus eggs: possible significance of natural selection for Pro2 in Mos. EMBO J.12, 4021–4027.10.1002/j.1460-2075.1993.tb06080.xSearch in Google Scholar PubMed PubMed Central
Ntwasa, M., Aapies, S., Schiffmann, D.A., and Gay, N.J. (2001). Drosophila embryos lacking N-myristoyltransferase have multiple developmental defects. Exp. Cell Res.262, 134–144.10.1006/excr.2000.5086Search in Google Scholar PubMed
Peltier, J.B., Ytterberg, J., Liberles, D.A., Roepstorff, P., and van Wijk, K.J. (2001). Identification of a 350-kDa ClpP protease complex with 10 different Clp isoforms in chloroplasts of Arabidopsis thaliana. J. Biol. Chem.276, 16318–16327.10.1074/jbc.M010503200Search in Google Scholar PubMed
Perrier, J., Durand, A., Giardina, T., and Puigserver, A. (2005). Catabolism of intracellular N-terminal acetylated proteins: involvement of acylpeptide hydrolase and acylase. Biochimie87, 673–685.10.1016/j.biochi.2005.04.002Search in Google Scholar PubMed
Pesaresi, P., Gardner, N.A., Masiero, S., Dietzmann, A., Eichacker, L., Wickner, R., Salamini, F., and Leister, D. (2003). Cytoplasmic N-terminal protein acetylation is required for efficient photosynthesis in Arabidopsis. Plant Cell15, 1817–1832.10.1105/tpc.012377Search in Google Scholar PubMed PubMed Central
Pfleger, C.M. and Kirschner, M.W. (2000). The KEN box: an APC recognition signal distinct from the D box targeted by Cdh1. Genes Dev.14, 655–665.10.1101/gad.14.6.655Search in Google Scholar
Pine, M.J. (1969). Kinetics of maturation of the amino termini of the cell proteins of Escherichia coli. Biochim. Biophys. Acta174, 359–372.10.1016/0005-2787(69)90261-5Search in Google Scholar
Polevoda, B. and Sherman, F. (2000). N a-terminal acetylation of eukaryotic proteins. J. Biol. Chem.275, 36479–36482.10.1074/jbc.R000023200Search in Google Scholar
Polevoda, B. and Sherman, F. (2003). N-terminal acetyltransferases and sequence requirements for N-terminal acetylation of eukaryotic proteins. J. Mol. Biol.325, 595–622.10.1016/S0022-2836(02)01269-XSearch in Google Scholar
Polevoda, B., Norbeck, J., Takakura, H., Blomberg, A., and Sherman, F. (1999). Identification and specificities of N-terminal acetyltransferases from Saccharomyces cerevisiae. EMBO J.18, 6155–6168.10.1093/emboj/18.21.6155Search in Google Scholar
Ray, M.K., Datta, B., Chakraborty, A., Chattopadhyay, A., Meza-Keuthen, S., and Gupta, N.K. (1992). The eukaryotic initiation factor 2-associated 67-kDa polypeptide (p67) plays a critical role in regulation of protein synthesis initiation in animal cells. Proc. Natl. Acad. Sci. USA89, 539–543.10.1073/pnas.89.2.539Search in Google Scholar
Rechsteiner, M. and Rogers, S.W. (1996). PEST sequences and regulation by proteolysis. Trends Biochem. Sci.21, 267–271.10.1016/S0968-0004(96)10031-1Search in Google Scholar
Roderick, S.L. and Matthews, B.W. (1993). Structure of the cobalt-dependent methionine aminopeptidase from Escherichia coli: a new type of proteolytic enzyme. Biochemistry32, 3907–3912.10.1021/bi00066a009Search in Google Scholar PubMed
Romisch, K. (2005). Endoplasmic reticulum-associated degradation. Annu. Rev. Cell Dev. Biol.21, 435–456.10.1146/annurev.cellbio.21.012704.133250Search in Google Scholar PubMed
Ross, S., Giglione, C., Pierre, M., Espagne, C., and Meinnel, T. (2005). Functional and developmental impact of cytosolic protein N-terminal methionine excision in Arabidopsis. Plant Physiol.137, 623–637.10.1104/pp.104.056861Search in Google Scholar PubMed PubMed Central
Sadis, S., Atienza, C. Jr., and Finley, D. (1995). Synthetic signals for ubiquitin-dependent proteolysis. Mol. Cell. Biol.15, 4086–4094.10.1128/MCB.15.8.4086Search in Google Scholar PubMed PubMed Central
Sanchez-Moran, E., Jones, G.H., Franklin, F.C., and Santos, J.L. (2004). A puromycin-sensitive aminopeptidase is essential for meiosis in Arabidopsis thaliana. Plant Cell16, 2895–2909.10.1105/tpc.104.024992Search in Google Scholar PubMed PubMed Central
Sanmartin, M., Jaroszewski, L., Raikhel, N.V., and Rojo, E. (2005). Caspases. Regulating death since the origin of life. Plant Physiol.137, 841–847.Search in Google Scholar
Saric, T., Graef, C.I., and Goldberg, A.L. (2004). Pathway for degradation of peptides generated by proteasomes: a key role for thimet oligopeptidase and other metallopeptidases. J. Biol. Chem.279, 46723–46732.10.1074/jbc.M406537200Search in Google Scholar PubMed
Sauer, R.T., Bolon, D.N., Burton, B.M., Burton, R.E., Flynn, J.M., Grant, R.A., Hersch, G.L., Joshi, S.A., Kenniston, J.A., Levchenko, I., et al. (2004). Sculpting the proteome with AAA+ proteases and disassembly machines. Cell119, 9–18.10.1016/j.cell.2004.09.020Search in Google Scholar PubMed PubMed Central
Sawant, S.V., Kiran, K., Singh, P.K., and Tuli, R. (2001). Sequence architecture downstream of the initiator codon enhances gene expression and protein stability in plants. Plant Physiol.126, 1630–1636.10.1104/pp.126.4.1630Search in Google Scholar PubMed PubMed Central
Seemuller, E., Lupas, A., and Baumeister, W. (1996). Autocatalytic processing of the 20S proteasome. Nature382, 468–471.10.1038/382468a0Search in Google Scholar PubMed
Serero, A., Giglione, C., and Meinnel, T. (2001). Distinctive features of the two classes of eukaryotic peptide deformylases. J. Mol. Biol.314, 695–708.10.1006/jmbi.2001.5175Search in Google Scholar PubMed
Serero, A., Giglione, C., Sardini, A., Martinez-Sanz, J., and Meinnel, T. (2003). An unusual peptide deformylase features in the human mitochondrial N-terminal methionine excision pathway. J. Biol. Chem.278, 52953–52963.10.1074/jbc.M309770200Search in Google Scholar PubMed
Serwold, T., Gonzalez, F., Kim, J., Jacob, R., and Shastri, N. (2002). ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature419, 480–483.10.1038/nature01074Search in Google Scholar PubMed
Shanklin, J., DeWitt, N.D., and Flanagan, J.M. (1995). The stroma of higher plant plastids contain ClpP and ClpC, functional homologs of Escherichia coli ClpP and ClpA: an archetypal two-component ATP-dependent protease. Plant Cell7, 1713–1722.10.1105/tpc.7.10.1713Search in Google Scholar PubMed PubMed Central
Sheng, J., Kumagai, A., Dunphy, W.G., and Varshavsky, A. (2002). Dissection of c-MOS degron. EMBO J.21, 6061–6071.10.1093/emboj/cdf626Search in Google Scholar PubMed PubMed Central
Sherman, F., Stewart, J.W., and Tsunasawa, S. (1985). Methionine or not methionine at the beginning of a protein. BioEssays3, 27–31.10.1002/bies.950030108Search in Google Scholar
Shrader, T.E., Tobias, J.W., and Varshavsky, A. (1993). The N-end rule in Escherichia coli: cloning and analysis of the leucyl, phenylalanyl-tRNA-protein transferase gene aat. J. Bacteriol.175, 4364–4374.10.1128/jb.175.14.4364-4374.1993Search in Google Scholar
Smith, K.J., Petit, C.M., Aubart, K., Smyth, M., McManus, E., Jones, J., Fosberry, A., Lewis, C., Lonetto, M., and Christensen, S.B. (2003). Structural variation and inhibitor binding in polypeptide deformylase from four different bacterial species. Protein Sci.12, 349–360.10.1110/ps.0229303Search in Google Scholar
Solbiati, J., Chapman-Smith, A., Miller, J.L., Miller, C.G., and Cronan, J.E. Jr. (1999). Processing of the N termini of nascent polypeptide chains requires deformylation prior to methionine removal. J. Mol. Biol.290, 607–614.10.1006/jmbi.1999.2913Search in Google Scholar
Spector, S., Flynn, J.M., Tidor, B., Baker, T.A., and Sauer, R.T. (2003). Expression of N-formylated proteins in Escherichia coli. Protein Express. Purif.32, 317–322.10.1016/j.pep.2003.08.004Search in Google Scholar
Stary, S., Yin, X.J., Potuschak, T., Schlogelhofer, P., Nizhynska, V., and Bachmair, A. (2003). PRT1 of Arabidopsis is a ubiquitin protein ligase of the plant N-end rule pathway with specificity for aromatic amino-terminal residues. Plant Physiol.133, 1360–1366.10.1104/pp.103.029272Search in Google Scholar
Tahirov, T.H., Oki, H., Tsukihara, T., Ogasahara, K., Yutani, K., Ogata, K., Izu, Y., Tsunasawa, S., and Kato, I. (1998). Crystal structure of methionine aminopeptidase from hyperthermophile, Pyrococcus furiosus. J. Mol. Biol.284, 101–124.10.1006/jmbi.1998.2146Search in Google Scholar
Tasaki, T., Mulder, L.C., Iwamatsu, A., Lee, M.J., Davydov, I.V., Varshavsky, A., Muesing, M., and Kwon, Y.T. (2005). A family of mammalian E3 ubiquitin ligases that contain the UBR box motif and recognize N-degrons. Mol. Cell. Biol.25, 7120–7136.10.1128/MCB.25.16.7120-7136.2005Search in Google Scholar
Thompson, M.W., and Maurizi, M.R. (1994). Activity and specificity of Escherichia coli ClpAP protease in cleaving model peptide substrates. J. Biol. Chem.269, 18201–18208.10.1016/S0021-9258(17)32435-3Search in Google Scholar
Tobias, J.W., Shrader, T.E., Rocap, G., and Varshavsky, A. (1991). The N-end rule in bacteria. Science254, 1374–1377.10.1126/science.1962196Search in Google Scholar PubMed
Tomkinson, B. (1999). Tripeptidyl peptidases: enzymes that count. Trends Biochem. Sci.24, 355–359.10.1016/S0968-0004(99)01435-8Search in Google Scholar
Towne, C.F., York, I.A., Neijssen, J., Karow, M.L., Murphy, A.J., Valenzuela, D.M., Yancopoulos, G.D., Neefjes, J.J., and Rock, K.L. (2005). Leucine aminopeptidase is not essential for trimming peptides in the cytosol or generating epitopes for MHC class I antigen presentation. J. Immunol.175, 6605–6614.10.4049/jimmunol.175.10.6605Search in Google Scholar
Tso, J.Y., Hermodson, M.A., and Zalkin, H. (1982). Glutamine phosphoribosylpyrophosphate amidotransferase from cloned Escherichia coli purF. NH2-terminal amino acid sequence, identification of the glutamine site, and trace metal analysis. J. Biol. Chem.257, 3532–3536.Search in Google Scholar
Tsujimoto, M. and Hattori, A. (2005). The oxytocinase subfamily of M1 aminopeptidases. Biochim. Biophys. Acta1751, 9–18.10.1016/j.bbapap.2004.09.011Search in Google Scholar
Turk, V., Turk, B., and Turk, D. (2001). Lysosomal cysteine proteases: facts and opportunities. EMBO J.20, 4629–4633.10.1093/emboj/20.17.4629Search in Google Scholar
Varshavsky, A. (1992). The N-end rule. Cell69, 725–745.10.1016/0092-8674(92)90285-KSearch in Google Scholar
Varshavsky, A. (1996). The N-end rule: functions, mysteries, uses. Proc. Natl. Acad. Sci. USA93, 12142–12149.10.1073/pnas.93.22.12142Search in Google Scholar
Vetro, J.A. and Chang, Y.H. (2002). Yeast methionine aminopeptidase type 1 is ribosome-associated and requires its N-terminal zinc finger domain for normal function in vivo. J. Cell Biochem.85, 678–688.10.1002/jcb.10161Search in Google Scholar
Vierstra, R.D. (2003). The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci.8, 135–142.10.1016/S1360-1385(03)00014-1Search in Google Scholar
Voges, D., Zwickl, P., and Baumeister, W. (1999). The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu. Rev. Biochem.68, 1015–1068.10.1146/annurev.biochem.68.1.1015Search in Google Scholar PubMed
Wisniewski, K. and Zagdanska, B. (2001). Genotype-dependent proteolytic response of spring wheat to water deficiency. J. Exp. Bot.52, 1455–1463.10.1093/jexbot/52.360.1455Search in Google Scholar PubMed
Yang, G., Kirkpatrick, R.B., Ho, T., Zhang, G.F., Liang, P.H., Johanson, K.O., Casper, D.J., Doyle, M.L., Marino, J.P. Jr., Thompson, S.K., et al. (2001). Steady-state kinetic characterization of substrates and metal-ion specificities of the full-length and N-terminally truncated recombinant human methionine aminopeptidases (type 2). Biochemistry40, 10645–10654.10.1021/bi010806rSearch in Google Scholar PubMed
Yang, S.H., Shrivastav, A., Kosinski, C., Sharma, R.K., Chen, M.H., Berthiaume, L.G., Peters, L.L., Chuang, P.T., Young, S.G., and Bergo, M.O. (2005). N-Myristoyltransferase 1 is essential in early mouse development. J. Biol. Chem.280, 18990–18995.10.1074/jbc.M412917200Search in Google Scholar PubMed
Zuo, S., Guo, Q., Ling, C., and Chang, Y.H. (1995). Evidence that two zinc fingers in the methionine aminopeptidase from Saccharomyces cerevisiae are important for normal growth. Mol. Gen. Genet.246, 247–253.10.1007/BF00294688Search in Google Scholar PubMed
©2006 by Walter de Gruyter Berlin New York
Articles in the same Issue
- 4th General Meeting of the International Proteolysis Society/International Conference on Protease Inhibitors
- Extracellular granzymes: current perspectives
- Impact of the N-terminal amino acid on targeted protein degradation
- Structural aspects of recently discovered viral deubiquitinating activities
- Cysteine cathepsins and caspases in silicosis
- The proprotein convertases and their implication in sterol and/or lipid metabolism
- PREPL: a putative novel oligopeptidase propelled into the limelight
- Human cathepsin L rescues the neurodegeneration and lethality in cathepsin B/L double-deficient mice
- Helicobacter pylori-induced downregulation of the secretory leukocyte protease inhibitor (SLPI) in gastric epithelial cell lines and its functional relevance for H. pylori-mediated diseases
- Increased local levels of granulocyte colony-stimulating factor are associated with the beneficial effect of pre-elafin (SKALP/trappin-2/WAP3) in experimental emphysema
- Interaction of a novel form of Pseudomonas aeruginosa alkaline protease (aeruginolysin) with interleukin-6 and interleukin-8
- Analysis of aldosterone-induced differential receptor-independent protein patterns using 2D-electrophoresis and mass spectrometry
- Modeling the 3D structure of wheat subtilisin/chymotrypsin inhibitor (WSCI). Probing the reactive site with two susceptible proteinases by time-course analysis and molecular dynamics simulations
- A stable analogue of glucose-dependent insulinotropic polypeptide, GIP(LysPAL16), enhances functional differentiation of mouse embryonic stem cells into cells expressing islet-specific genes and hormones
- Transcription factor FOXM1c is repressed by RB and activated by cyclin D1/Cdk4
- Despite its strong transactivation domain, transcription factor FOXM1c is kept almost inactive by two different inhibitory domains
- Inhibition of calcineurin by infusion of CsA causes hyperphosphorylation of tau and is accompanied by abnormal behavior in mice
- Isolation and properties of extracellular proteinases of Penicillium marneffei
- Isolation and comparative characterization of Ki-67 equivalent antibodies from the HuCAL® phage display library
Articles in the same Issue
- 4th General Meeting of the International Proteolysis Society/International Conference on Protease Inhibitors
- Extracellular granzymes: current perspectives
- Impact of the N-terminal amino acid on targeted protein degradation
- Structural aspects of recently discovered viral deubiquitinating activities
- Cysteine cathepsins and caspases in silicosis
- The proprotein convertases and their implication in sterol and/or lipid metabolism
- PREPL: a putative novel oligopeptidase propelled into the limelight
- Human cathepsin L rescues the neurodegeneration and lethality in cathepsin B/L double-deficient mice
- Helicobacter pylori-induced downregulation of the secretory leukocyte protease inhibitor (SLPI) in gastric epithelial cell lines and its functional relevance for H. pylori-mediated diseases
- Increased local levels of granulocyte colony-stimulating factor are associated with the beneficial effect of pre-elafin (SKALP/trappin-2/WAP3) in experimental emphysema
- Interaction of a novel form of Pseudomonas aeruginosa alkaline protease (aeruginolysin) with interleukin-6 and interleukin-8
- Analysis of aldosterone-induced differential receptor-independent protein patterns using 2D-electrophoresis and mass spectrometry
- Modeling the 3D structure of wheat subtilisin/chymotrypsin inhibitor (WSCI). Probing the reactive site with two susceptible proteinases by time-course analysis and molecular dynamics simulations
- A stable analogue of glucose-dependent insulinotropic polypeptide, GIP(LysPAL16), enhances functional differentiation of mouse embryonic stem cells into cells expressing islet-specific genes and hormones
- Transcription factor FOXM1c is repressed by RB and activated by cyclin D1/Cdk4
- Despite its strong transactivation domain, transcription factor FOXM1c is kept almost inactive by two different inhibitory domains
- Inhibition of calcineurin by infusion of CsA causes hyperphosphorylation of tau and is accompanied by abnormal behavior in mice
- Isolation and properties of extracellular proteinases of Penicillium marneffei
- Isolation and comparative characterization of Ki-67 equivalent antibodies from the HuCAL® phage display library