Nna1-like proteins are active metallocarboxypeptidases of a new and diverse M14 subfamily

FASEB Journal

Volumn 21, Issue 3, 2007, Pages 851-865

  Rodriguez De La Vega, Monica ^a   Sevilla, Rafael G ^b   Hermoso, Antoni ^a   Lorenzo, Julia ^a   Tanco, Sebastian ^a   Diez, Amalia ^b   Fricker, Lloyd D ^c   Bautista, José M ^b   Avilés, Francesc X ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

CCP; Degradome; Peptidase classification; Tubulin processing; Tubulinyl Tyr carboxypeptidase

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BENZYLCARBONYLGLUTAMYLTYROSINE; CARBOXYPEPTIDASE; DIPEPTIDE; ENZYME VARIANT; METALLOCARBOXYPEPTIDASE M14A; METALLOCARBOXYPEPTIDASE M14B; METALLOCARBOXYPEPTIDASE M14C; PROTEIN NNA1; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME SPECIFICITY; GENOME ANALYSIS; MOLECULAR CLONING; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN VARIANT; SEQUENCE ANALYSIS;

ANIMALS; BACTERIA; BASE SEQUENCE; BINDING SITES; CARBOXYPEPTIDASES; GTP-BINDING PROTEINS; MICE; MOLECULAR SEQUENCE DATA; PEPTIDE HYDROLASES; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SERINE-TYPE D-ALA-D-ALA CARBOXYPEPTIDASE;

ANIMALIA; CAENORHABDITIS ELEGANS; EUKARYOTA; PROTISTA;

EID: 33847393315     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-7330com     Document Type: Article

References (74)

1. Kalinina, E., Biswas, R., Berezniuk, I., Hermoso, A., Aviles, F. X., and Fricker, L. D. (2007) A novel subfamily of mouse cytosolic carboxypeptidases. FASEB J. 20, In press
2. Rawlings, N. D., Morton, F. R., and Barrett, A. J. (2006) MEROPS: the peptidase database. Nucleic Acids Res. 34, D270-272
3. Vendrell, J., Aviles, F. X., and Fricker, L. D. (2004) Metallocarboxypeptidases. In Handbook of Metallopeptidases (Messerschmidt, A., Bode, W., and Cygler, M., eds) pp. 167-192, John Wiley & Sons, Chichester, UK
4. Barrett, A. J., Rawlings, N. D., and Woessner, J. F. (1999) Introduction: clan MC containing metallocarboxypeptidases. In Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) CDROM, chapter 450, Academic, San Diego, CA
5. Hourdou, M. L., Guinand, M., Vacheron, M. J., Michel, G., Denoroy, L., Duez, C., Englebert, S., Joris, B., Weber, G., and Ghuysen, J. M. (1993) Characterization of the sporulation-related gamma-D-glutamyl-( L)meso-diaminopimelic-acid-hydrolysing peptidase I of Bacillus sphaericus NCTC 9602 as a member of the metallo(zinc) carboxypeptidase A family. Modular design of the protein. Biochem. J. 292, 563-570
6. Webster, D. R. (2004) Tubulinyl-Tyr carboxypeptidase. In Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., eds) pp. 2111-2113, Elsevier, London. UK
7. He, G. P., Muise, A., Li, A. W., and Ro, H. S. (1995) A eukaryotic transcriptional repressor with carboxypeptidase activity. Nature 378, 92-96
8. Too, C. K., Vickaryous, N., Boudreau, R. T., and Sangster, S. M. (2001) Identification and nuclear localization of a novel prolactin and cytokine-responsive carboxypeptidase D. Endocrinology 142, 1357-1367
9. Harris, A., Morgan, J. I., Pecot, M., Soumare, A., Osborne, A., and Soares, H. D. (2000) Regenerating motor neurons express Nna1, a novel ATP/GTP-binding protein related to zinc carboxypeptidases. Mol. Cell. Neurosci. 16, 578-596
10. Fernandez-Gonzalez, A., La Spada, A. R., Treadaway, J., Higdon, J. C., Harris, B. S., Sidman, R. L., Morgan, J. I., and Zuo, J. (2002) Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene, Nna1. Science 295, 1904-1906
11. Wang, T., Parris, J., Li, L., and Morgan, J. I. (2006) The carboxypeptidase-like substrate-binding site in Nna1 is essential for the rescue of the Purkinje cell degeneration (pcd) phenotype. Mol. Cell. Neurosci. 33, 200-213
12. Wu, C. H., Yeh, L. S., Huang, H., Arminski, L., Castro-Alvear, J., Chen, Y., Hu, Z., Kourtesis, P., Ledley, R. S., Suzek, B. E., et al. (2003) The Protein Information Resource. Nucleic Acids Res. 31, 345-347
13. Durbin, R., Eddy, S., Krogh, A., and Mitchison, G. (1998) Hidden Markov models. In Biological Sequence Analysis: Probabilistic Models of Proteins and Nucleic Acids (Durbin, R., Eddy, S., and Krogh, A., eds) Cambridge University Press, Cambridge, UK
14. Bateman, A., Coin, L., Durbin, R., Finn, R. D., Hollich, V., Griffiths-Jones, S., Khanna, A., Marshall, M., Moxon, S., Sonnhammer, E. L., et al. (2004) The Pfam protein families database. Nucleic Acids Res. 32, D138-D141
15. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410
16. Felsenstein, J. (2005) PHYLIP (Phylogeny Inference Package) Free package from the University of Washington, Department of Genome Sciences, Seattle, WA
17. Mizuguchi, K., Deane, C. M., Blundell, T. L., Johnson, M. S., and Overington, J. P. (1998) JOY: protein sequence-structure representation and analysis. Bioinformatics 14, 617-623
18. Ning, Z., Cox, A. J., and Mullikin, J. C. (2001) SSAHA: a fast search method for large DNA databases. Genome Res. 11, 1725-1729
19. Birney, E., Andrews, D., Caccamo, M., Chen, Y., Clarke, L., Coates, G., Cox, T., Cunningham, F., Curwen, V., Cutts, T., et al. (2006) Ensembl 2006. Nucleic Acids Res. 34, D556-D561
20. McGuffin, L. J., Bryson, K., and Jones, D. T. (2000) The PSIPRED protein structure prediction server. Bioinformatics 16, 404-405
21. Shi, J., Blundell, T. L., and Mizuguchi, K. (2001) FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J. Mol. Biol. 310, 243-257
22. Sali, A., and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815
23. Fiser, A., and Sali, A. (2003) Modeller: generation and refinement of homology-based protein structure models. Methods Enzymol. 374, 461-491
24. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486
25. Eisenberg, D., Luthy, R., and Bowie, J. U. (1997) VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol. 277, 396-404
26. Nicholas, K. B., Nicholas H.B. Jr., and Deerfield, D. W. (1997) GeneDoc: analysis and visualization of genetic variation. EMBNEW 4, 14
27. Sali, A., and Blundell, T. L. (1990) Definition of general topological equivalence in protein structures. A procedure involving comparison of properties and relationships through simulated annealing and dynamic programming. J. Mol. Biol. 212, 403-428
28. DeLano, W. L. (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA (http://www.pymol.org)
29. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882
30. Kumar, S., Tamura, K., and Nei, M. (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5, 150-163
31. Saitou, N., and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425
32. Jones, D. T., Taylor, W. R., and Thornton, J. M. (1992) The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8, 275-282
33. Abascal, F., Zardoya, R., and Posada, D. (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105
34. Felsenstein, J. (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783-791
35. Walhout, A. J., Temple, G. F., Brasch, M. A., Hartley, J. L., Lorson, M. A., van den Heuvel, S., and Vidal, M. (2000) GATEWAY recombinational cloning: application to the cloning of large numbers of open reading frames or ORFeomes. Methods Enzymol. 328, 575-592
36. Aslanidis, C., and de Jong, P. J. (1990) Ligation-independent cloning of PCR products (LIC-PCR). Nucleic Acids Res. 18, 6069-6074
37. Peterson, L. M., Holmquist, B., and Bethune, J. L. (1982) A unique activity assay for carboxypeptidase A in human serum. Anal. Biochem. 125, 420-426
38. Mock, W. L., Liu, Y., and Stanford, D. J. (1996) Arazoformyl peptide surrogates as spectrophotometric kinetic assay substrates for carboxypeptidase A. Anal. Biochem. 239, 218-222
39. Plummer, T. H., Jr., and Kimmel, M. T. (1980) An improved spectrophotometric assay for human plasma carboxypeptidase N1. Anal. Biochem. 108, 348-353
40. Mock, W. L., and Stanford, D. J. (2002) Anisylazoformylarginine: a superior assay substrate for carboxypeptidase B type enzymes. Bioorg. Med. Chem. Lett. 12, 1193-1194
41. Aravind, L., Iyer, L. M., Wellems, T. E., and Miller, L. H. (2003) Plasmodium biology: genomic gleanings. Cell 115, 771-785
42. Ventura, S., Villegas, V., Sterner, J., Larson, J., Vendrell, J., Hershberger, C. L., and Aviles, F. X. (1999) Mapping the pro-region of carboxypeptidase B by protein engineering. Cloning, overexpression, and mutagenesis of the porcine proenzyme. J. Biol. Chem. 274, 19925-19933
43. Jones, D. T. (1999) GenTHREADER: an efficient and reliable protein fold recognition method for genomic sequences. J. Mol. Biol. 287, 797-815
44. McGuffin, L. J., and Jones, D. T. (2003) Improvement of the GenTHREADER method for genomic fold recognition. Bioinformatics 19, 874-881
45. Altschul, S. F., and Koonin, E. V. (1998) Iterated profile searches with PSI-BLAST-a tool for discovery in protein databases. Trends. Biochem. Sci. 23, 444-447
46. Bateman, A., and Bycroft, M. (2000) The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J. Mol. Biol. 299, 1113-1119
47. Bayes, A., Comellas-Bigler, M., Rodriguez de la Vega, M., Maskos, K., Bode, W., Aviles, F. X., Jongsma, M. A., Beekwilder, J., and Vendrell, J. (2005) Structural basis of the resistance of an insect carboxypeptidase to plant protease inhibitors. Proc. Natl. Acad. Sci. U.S.A. 102, 16602-16607
48. Kim, H., and Lipscomb, W. N. (1990) Crystal structure of the complex of carboxypeptidase A with a strongly bound phosphonate in a new crystalline form: comparison with structures of other complexes. Biochemistry 29, 5546-5555
49. Rees, D. C., and Lipscomb, W. N. (1981) Binding of ligands to the active site of carboxypeptidase A. Proc. Natl. Acad. Sci. U.S.A. 78, 5455-5459
50. Christianson, D. W., and Lipscomb, W. N. (1986) X-ray crystallographic investigation of substrate binding to carboxypeptidase A at subzero temperature. Proc. Natl. Acad. Sci. U.S.A. 83, 7568-7572
51. Gardell, S. J., Craik, C. S., Hilvert, D., Urdea, M. S., and Rutter, W. J. (1985) Site-directed mutagenesis shows that tyrosine 248 of carboxypeptidase A does not play a crucial role in catalysis. Nature 317, 551-555
52. Cho, J. H., Kim, D. H., Lee, K. J., Kim, D. H., and Choi, K. Y. (2001) The role of Tyr248 probed by mutant bovine carboxypeptidase A: insight into the catalytic mechanism of carboxypeptidase A. Biochemistry 40, 10197-10203
53. Garcia-Saez, I., Reverter, D., Vendrell, J., Aviles, F. X., and Coll, M. (1997) The three-dimensional structure of human procarboxypeptidase A2. Deciphering the basis of the inhibition, activation and intrinsic activity of the zymogen. EMBO J. 16, 6906-6913
54. Wei, S., Segura, S., Vendrell, J., Aviles, F. X., Lanoue, E., Day, R., Feng, Y., and Fricker, L. D. (2002) Identification and characterization of three members of the human metallocarboxypeptidase gene family. J. Biol. Chem. 277, 14954-14964
55. Gomis-Ruth, F. X., Companys, V., Qian, Y., Fricker, L. D., Vendrell, J., Aviles, F. X., and Coll, M. (1999) Crystal structure of avian carboxypeptidase D domain II: a prototype for the regulatory metallocarboxypeptidase subfamily. EMBO J. 18, 5817-5826
56. Estebanez-Perpina, E., Bayes, A., Vendrell, J., Jongsma, M. A., Bown, D. P., Gatehouse, J. A., Huber, R., Bode, W., Aviles, F. X., and Reverter, D. (2001) Crystal structure of a novel mid-gut procarboxypeptidase from the cotton pest Helicoverpa armigera. J. Mol. Biol. 313, 629-638
57. Meyer, A., and Schartl, M. (1999) Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr. Opin. Cell Biol. 11, 699-704
58. McLysaght, A., Hokamp, K., and Wolfe, K. H. (2002) Extensive genomic duplication during early chordate evolution. Nat. Genet. 31, 200-204
59. Snell, E. A., Brooke, N. M., Taylor, W. R., Casane, D., Philippe, H., and Holland, P. W. (2006) An unusual choanoflagellate protein released by Hedgehog autocatalytic processing. Proc. Biol. Sci. 273, 401-407
60. Koonin, E. V., Makarova, K. S., and Aravind, L. (2001) Horizontal gene transfer in prokaryotes: quantification and classification. Annu. Rev. Microbiol. 55, 709-742
61. Ochman, H., Lawrence, J. G., and Groisman, E. A. (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299-304
62. Erck, C., Peris, L., Andrieux, A., Meissirel, C., Gruber, A. D., Vernet, M., Schweitzer, A., Saoudi, Y., Pointu, H., Bosc, C., et al. (2005) A vital role of tubulin-tyrosine-ligase for neuronal organization. Proc. Natl. Acad. Sci. U.S.A. 102, 7853-7858
63. Hallak, M. E., Rodriguez, J. A., Barra, H. S., and Caputto, R. (1977) Release of tyrosine from tyrosinated tubulin. Some common factors that affect this process and the assembly of tubulin. FEBS Lett. 73, 147-150
64. Argarana, C. E., Barra, H. S., and Caputto, R. (1978) Release of [14C]tyrosine from tubulinyl-[14C]tyrosine by brain extract. Separation of a carboxypeptidase from tubulin-tyrosine ligase. Mol. Cell. Biochem. 19, 17-21
65. Wehland, J., and Weber, K. (1987) Turnover of the carboxyterminal tyrosine of alpha-tubulin and means of reaching elevated levels of detyrosination in living cells. J. Cell Sci. 88, 185-203
66. Gundersen, G. G., Khawaja, S., and Bulinski, J. C. (1987) Postpolymerization detyrosination of alpha-tubulin: a mechanism for subcellular differentiation of microtubules. J. Cell Biol. 105, 251-264
67. Bosc, C., Cronk, J. D., Pirollet, F., Watterson, D. M., Haiech, J., Job, D., and Margolis, R. L. (1996) Cloning, expression, and properties of the microtubule-stabilizing protein STOP. Proc. Natl. Acad. Sci. U.S.A. 93, 2125-2130
68. Contin, M. A., and Arce, C. A. (2000) Tubulin carboxypeptidase/ microtubules association can be detected in the distal region of neural processes. Neurochem. Res. 25, 27-36
69. Han, P. J., Shukla, S., Subramanian, P. S., and Hoffman, P. N. (2004) Cyclic AMP elevates tubulin expression without increasing intrinsic axon growth capacity. Exp. Neurol. 189, 293-302
70. Webster, D. R., Modesti, N. M., and Bulinski, J. C. (1992) Regulation of cytoplasmic tubulin carboxypeptidase activity during neural and muscle differentiation: characterization using a microtubule-based assay. Biochemistry 31, 5849-5856
71. Mullins, F. H., Hargreaves, A. J., Li, J. Y., Dahlstrom, A., and McLean, W. G. (1994) Tyrosination state of alpha-tubulin in regenerating peripheral nerve. J. Neurochem. 62, 227-234
72. Alfa, C. E., and Hyams, J. S. (1991) Microtubules in the fission yeast Schizosaccharomyces pombe contain only the tyrosinated form of alpha-tubulin. Cell Motil. Cytoskeleton 18, 86-93
73. Bloom, K. (2004) Microtubule composition: cryptography of dynamic polymers. Proc. Natl. Acad. Sci. U.S.A. 101, 6839-6840
74. Badin-Larcon, A. C., Boscheron, C., Soleilhac, J. M., Piel, M., Mann, C., Denarier, E., Fourest-Lieuvin, A., Lafanechere, L., Bornens, M., and Job, D. (2004) Suppression of nuclear oscillations in Saccharomyces cerevisiae expressing Glu tubulin. Proc. Natl. Acad. Sci. U.S.A. 101, 5577-5582