Altered Activity, Social Behavior, and Spatial Memory in Mice Lacking the NTAN1p Amidase and the Asparagine Branch of the N-End Rule Pathway

REFERENCES

• Alagramam, K., Naider, F., and Becker, J. M.. 1995. A recognition component of the ubiquitin system is required for peptide transport in Saccharomyces cerevisiae. Mol. Microbiol. 15:225–234
   PubMedGoogle Scholar
• Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Smith, J. A., Seidman, J. G., and Struhl, K.. 1998. Current protocols in molecular biology. Wiley-Interscience, New York, N.Y
   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. Science 234:179–186
   PubMed Web of Science ®Google Scholar
• Bachmair, A., and Varshavsky, A.. 1989. The degradation signal in a short-lived protein. Cell 56:1019–1032
   PubMed Web of Science ®Google Scholar
• Baker, R. T., and Varshavsky, A.. 1991. Inhibition of the N-end rule pathway in living cells. Proc. Natl. Acad. Sci. USA 87:2374–2378
   Google Scholar
• Baker, R. T., and Varshavsky, A.. 1995. Yeast N-terminal amidase. A new enzyme and component of the N-end rule pathway. J. Biol. Chem. 270:12065–12074
   PubMedGoogle Scholar
• Balogh, S. A., McDowell, C. S., Stavnezer, A., and Denenberg, V. H.. 1999. A behavioral and neuroanatomical assessment of an inbred substrain of 129 mice, with behavioral comparisons to C57BL/6J mice. Brain Res. 836:38–48
   PubMed Web of Science ®Google Scholar
• Balzi, E., Choder, M., Chen, W., Varshavsky, A., and Goffeau, A.. 1990. Cloning and functional analysis of the arginyl-tRNA-protein transferase gene ATE1 of Saccharomyces cerevisiae. J. Biol. Chem. 265:7464–7471
   PubMed Web of Science ®Google Scholar
• Baron, U., Schnappinger, D., Helbl, V., Gossen, M., Hillen, W., and Bujard, H.. 1999. Generation of conditional mutants in higher eukaryotes by switching between the expression of two genes. Proc. Natl. Acad. Sci. USA 96:1013–1018
   PubMedGoogle Scholar
• Baumeister, W., Walz, J., Zühl, F., and Seemüller, E.. 1998. The proteasome: paradigm of a self-compartmentalizing protease. Cell 92:367–380
   PubMed Web of Science ®Google Scholar
• Beaudin, S., and Lalonde, R.. 1997. The effects of pentobarbital on spatial learning, motor coordination, and exploration. Pharmacol. Biochem. Behav. 57:111–114
   PubMedGoogle Scholar
• Byrd, C., Turner, G. C., and Varshavsky, A.. 1998. The N-end rule pathway controls the import of peptides through degradation of a transcriptional repressor. EMBO J. 17:269–277
   PubMed Web of Science ®Google Scholar
• Capecchi, M. R.. 1989. Altering the genome by homologous recombination. Science 244:1288–1292
   PubMed Web of Science ®Google Scholar
• Chang, S. E., Keen, J., Lane, E. B., and Taylor-Papadimitriou, J.. 1982. Establishment and characterization of SV40-transformed human breast epithelial cell lines. Cancer Res. 42:2040–2053
   PubMedGoogle Scholar
• Chau, V., Tobias, J. W., Bachmair, A., Marriott, D., Ecker, D. J., Gonda, D. K., and Varshavsky, A.. 1989. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243:1576–1583
   PubMed Web of Science ®Google Scholar
• Conlon, R. A., and Rossant, J.. 1992. Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development 116:357–368
   PubMedGoogle Scholar
• Coux, O., Tanaka, K., and Goldberg, A. L.. 1996. Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 65:801–817
   PubMed Web of Science ®Google Scholar
• Davydov, I. V., Patra, D., and Varshavsky, A.. 1998. The N-end rule pathway in Xenopus egg extracts. Arch. Biochem. Biophys. 357:317–325
   PubMedGoogle Scholar
• deGroot, R. J., Rümenapf, T., Kuhn, R. J., and Strauss, J. H.. 1991. Sindbis virus RNA polymerase is degraded by the N-end rule pathway. Proc. Natl. Acad. Sci. USA 88:8967–8971
   PubMedGoogle Scholar
• DeMartino, G. N., and Slaughter, C. A.. 1999. The proteasome, a novel protease regulated by multiple mechanisms. J. Biol. Chem. 274:22123–22126
   PubMed Web of Science ®Google Scholar
• Denenberg, V. H., Talgo, N., Carroll, D. A., Freter, S., and Deni, R.. 1991. A computer-aided procedure for measuring Lashley III maze performance. Physiol. Behav. 50:857–861
   PubMedGoogle Scholar
• Denenberg, V. H., Talgo, N. W., Waters, N. S., and Kenner, G. H.. 1990. A computer-aided procedure for measuring swim rotation. Physiol. Behav. 47:1023–1025
   PubMedGoogle Scholar
• Gonda, D. K., Bachmair, A., Wünning, 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
   PubMed Web of Science ®Google Scholar
• Grigoryev, S., Stewart, A. E., Kwon, Y. T., Arfin, S. M., Bradshaw, R. A., Jenkins, N. A., Copeland, N. G., and Varshavsky, A.. 1996. A mouse amidase specific for N-terminal asparagine. The gene, the enzyme, and their function in the N-end rule pathway. J. Biol. Chem. 271:28521–28532
   PubMedGoogle Scholar
• Haas, A. J., and Siepman, T. J.. 1997. Pathways of ubiquitin conjugation. FASEB J. 11:1257–1268
   PubMed Web of Science ®Google Scholar
• Hershko, A., and Ciechanover, A.. 1998. The ubiquitin system. Annu. Rev. Biochem. 76:425–479
   Google Scholar
• Hochstrasser, M.. 1996. Ubiquitin-dependent protein degradation. Annu. Rev. Genet. 30:405–439
   PubMed Web of Science ®Google Scholar
• Hondermarck, H., Sy, J., Bradshaw, R. A., and Arfin, S. M.. 1992. Dipeptide inhibitors of ubiquitin-mediated protein turnover prevent growth factor-induced neurite outgrowth in rat pheochromocytoma PC12 cells. Biochem. Biophys. Res. Commun. 30:280–288
   Google Scholar
• Hyde, L. A., and Denenberg, V. H.. 1999. BXSB mice can learn complex pattern discrimination. Physiol. Behav. 66:437–439
   PubMedGoogle Scholar
• Hyde, L. A., Hoplight, B. J., and Denenberg, V. H.. 1998. Water version of the radial-arm maze: learning in three inbred strains of mice. Brain Res. 785:236–244
   PubMedGoogle Scholar
• Jiang, Y. H., Armstrong, D., Albrecht, U., Atkins, C. M., Noebels, J. L., Eichele, G., Sweatt, J. D., and Beaudet, A. L.. 1998. Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron 21:799–811
   PubMed Web of Science ®Google Scholar
• Johnson, E. S., Gonda, D. K., and Varshavsky, A.. 1990. Cis-trans recognition and subunit-specific degradation of short-lived proteins. Nature 346:287–291
   PubMed Web of Science ®Google Scholar
• Kishino, T., Lalande, M., and Wagstaff, J.. 1997. UBE3A/E6-AP mutations cause Angelman syndrome. Nat. Genet. 15:70–73
   PubMed Web of Science ®Google Scholar
• Kwon, Y. T., Kashina, A. S., and Varshavsky, A.. 1999. Alternative splicing results in differential expression, activity, and localization of the two forms of arginyl-tRNA-protein transferase, a component of the N-end rule pathway. Mol. Cell. Biol. 19:182–193
   PubMed Web of Science ®Google Scholar
• Kwon, Y. T., Lévy, F., and Varshavsky, A.. 1999. Bivalent inhibitor of the N-end rule pathway. J. Biol. Chem. 274:18135–18139
   PubMedGoogle Scholar
• Kwon, Y. T., Reiss, Y., Fried, V. A., Hershko, A., Yoon, J. K., Gonda, D. K., Sangan, P., Copeland, N. G., Jenkins, N. A., and Varshavsky, A.. 1998. The mouse and human genes encoding the recognition component of the N-end rule pathway. Proc. Natl. Acad. Sci. USA 95:7898–7903
   PubMed Web of Science ®Google Scholar
• Laney, J. D., and Hochstrasser, M.. 1999. Substrate targeting in the ubiquitin system. Cell 97:427–430
   PubMed Web of Science ®Google Scholar
• Lawson, T. G., Gronros, D. L., Evans, P. E., Bastien, M. C., Michalewich, K. M., Clark, J. K., Edmonds, J. H., Graber, K. H., Werner, J. A., Lurvey, B. A., and Cate, J. M.. 1999. Identification and characterization of a protein destruction signal in the encephalomyocarditis virus 3C protease. J. Biol. Chem. 274:9871–9880
   PubMedGoogle Scholar
• Lecker, S. H., Solomon, V., Price, S. R., Kwon, Y. T., Mitch, W. E., and Goldberg, A. L.. 1999. Ubiquitin conjugation by the N-end rule pathway and mRNAs for its components increase in muscles of diabetic rats. J. Clin. Investig. 104:1411–1420
   PubMed Web of Science ®Google Scholar
• Lévy, F., Johnsson, N., Rumenapf, T., and Varshavsky, A.. 1996. Using ubiquitin to follow the metabolic fate of a protein. Proc. Natl. Acad. Sci. USA 93:4907–4912
   PubMedGoogle Scholar
• Li, J., and Pickart, C.. 1995. Inactivation of arginyl-tRNA protein transferase by a bifunctional arsenoxide: identification of residues proximal to arsenoxide site. Biochemistry 34:139–147
   PubMedGoogle Scholar
• Lister, R. G.. 1987. The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology 92:180–185
   PubMed Web of Science ®Google Scholar
• Madura, K., and Varshavsky, A.. 1994. Degradation of Gα by the N-end rule pathway. Science 265:1454–1458
   PubMed Web of Science ®Google Scholar
• Maniatis, T.. 1999. A ubiquitin ligase complex essential for the NF-κB, Wnt/Wingless, and Hedgehog signaling pathways. Genes Dev. 13:505–510
   PubMedGoogle Scholar
• Matsuura, T., Sutcliffe, J. S., Fang, P., Galjaard, R. J., Jiang, Y. H., Benton, C. S., Rommens, J. M., and Beaudet, A. L.. 1997. De novo truncating mutations in E6-AP ubiquitin-protein ligase gene (UBE3A) in Angelman syndrome. Nat. Genet. 15:74–77
   PubMed Web of Science ®Google Scholar
• Morris, R.. 1984. Development of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11:47–60
   PubMed Web of Science ®Google Scholar
• Ota, I. M., and Varshavsky, A.. 1993. A yeast protein similar to bacterial two-component regulators. Science 262:566–569
   PubMed Web of Science ®Google Scholar
• Peters, J.-M., King, R. W., and Deshaies, R. J.. 1998. Cell cycle control by ubiquitin-dependent proteolysis Ubiquitin and the biology of the cell. Peters, J. M., Harris, J. R., and Finley, D. 345–387 Plenum Press, New York, N.Y
   Google Scholar
• Pickart, C. M.. 1997. Targeting of substrates to the 26S proteasome. FASEB J. 11:1055–1066
   PubMed Web of Science ®Google Scholar
• Ramboz, S., Oosting, R., Amara, D. A., Kung, H. F., Blier, P., Mendelsohn, M., Mann, J. J., Brunner, D., and Hen, R.. 1998. Serotonin receptor 1A knockout: an animal model of anxiety-related disorder. Proc. Natl. Acad. Sci. USA 95:14476–14481
   PubMed Web of Science ®Google Scholar
• Rechsteiner, M.. 1998. The 26S proteasome Ubiquitin and the biology of the cell. Peters, J. M., Harris, J. R., and Finley, D. 147–189 Plenum Press, New York, N.Y
   Google Scholar
• Robertson, E. J.. 1987. Embryo-derived stem cell lines Teratocarcinomas and embryonic stem cells: a practical approach. Robertson, E. J. 71–112 IRL Press, Oxford, United Kingdom
   Google Scholar
• Royce, J. R.. 1972. Avoidance conditioning in nine strains of inbred mice using optimal stimulus parameters. Behav. Genet. 2:107–110
   PubMedGoogle Scholar
• Schauber, C., Chen, L., Tongaonkar, P., Vega, I., and Madura, K.. 1998. Sequence elements that contribute to the degradation of yeast G-alpha. Genes Cells 3:307–319
   PubMedGoogle Scholar
• Schwenk, F., Kuhn, R., Angrand, P. O., Rajewsky, K., and Stewart, A. F.. 1998. Temporally and spatially regulated somatic mutagenesis in mice. Nucleic Acids Res. 26:1427–1432
   PubMed Web of Science ®Google Scholar
• Sijts, A. J., Pilip, I., and Pamer, E. G.. 1997. The Listeria monocytogenes-secreted p60 protein is an N-end rule substrate in the cytosol of infected cells. Implications for major histocompatibility complex class I antigen processing of bacterial proteins. J. Biol. Chem. 272:19261–19268
   PubMedGoogle Scholar
• Solomon, V., Baracos, V., Sarraf, P., and Goldberg, A.. 1998. Rates of ubiquitin conjugation increase when muscles atrophy, largely through activation of the N-end rule pathway. Proc. Natl. Acad. Sci. USA 95:12602–12607
   PubMedGoogle Scholar
• Stewart, A.. 1995. Trends in genetics nomenclature guide. Elsevier Science, Ltd., Cambridge, United Kingdom
   Google Scholar
• Stewart, A. E., Arfin, S. M., and Bradshaw, R. A.. 1995. The sequence of porcine protein NH2-terminal asparagine amidohydrolase. A new component of the N-end rule pathway. J. Biol. Chem. 270:25–28
   PubMedGoogle Scholar
• Suzuki, T., and Varshavsky, A.. 1999. Degradation signals in the lysine-asparagine sequence space. EMBO J. 18:6017–6026
   PubMedGoogle Scholar
• Taban, C. H., Hondermarck, H., Bradshaw, R. A., and Boilly, B.. 1996. Effect of a dipeptide inhibiting ubiquitin-mediated protein degradation on nerve-dependent limb regeneration in the newt. Experientia 52:865–870
   PubMedGoogle Scholar
• Tobias, J. W., and Varshavsky, A.. 1991. Cloning and functional analysis of the ubiquitin-specific protease gene UBP1 of Saccharomyces cerevisiae. J. Biol. Chem. 266:12021–12028
   PubMed Web of Science ®Google Scholar
• Varshavsky, A.. 1996. The N-end rule: functions, mysteries, uses. Proc. Natl. Acad. Sci. USA 93:12142–12149
   PubMed Web of Science ®Google Scholar
• Varshavsky, A.. 1997. The ubiquitin system. Trends Biochem. Sci. 22:383–387
   PubMed Web of Science ®Google Scholar
• Wang, Y. M., and Ingoglia, N. A.. 1997. N-terminal arginylation of sciatic nerve and brain proteins following injury. Neurochem. Res. 22:1453–1459
   PubMedGoogle Scholar
• Wilkinson, K., and Hochstrasser, M.. 1998. The deubiquitinating enzymes Ubiquitin and the biology of the cell. Peters, J.-M., Harris, J. R., and Finley, D. 99–126 Plenum Press, New York, N.Y
   Google Scholar