Naturally occurring carboxypeptidase A6 mutations: Effect on enzyme function and association with epilepsy

Journal of Biological Chemistry

Volumn 287, Issue 51, 2012, Pages 42900-42909

  Sapio, Matthew R ^a   Salzmann, Annick ^b   Vessaz, Monique ^c   Crespel, Arielle ^d   Lyons, Peter J ^e   Malafosse, Alain ^b,c   Fricker, Lloyd D ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^d MONTPELLIER UNIVERSITY HOSPITAL   (France)

^e ANDREWS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYPEPTIDASE; ENZYME FUNCTIONS; EXTRACELLULAR; EXTRACELLULAR MATRICES; FOCAL EPILEPSY; HEK293 CELLS; NATURALLY OCCURRING; POINT MUTATIONS; PROTEIN LEVEL; PROTEIN STRUCTURES; SINGLE NUCLEOTIDE POLYMORPHISMS; TEMPORAL LOBE EPILEPSY;

AMINO ACIDS; ENZYME ACTIVITY; PROTEIN FOLDING; PROTEINS; TISSUE;

NEUROLOGY;

CARBOXYPEPTIDASE A; CARBOXYPEPTIDASE A6; HYDROGEN PEROXIDE; UNCLASSIFIED DRUG;

ADULT; AMINO ACID SUBSTITUTION; ARTICLE; CARBOXYPEPTIDASE A6 GENE; CELL STRAIN HEK293; CHILD; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; EXON; EXTRACELLULAR MATRIX; FEBRILE CONVULSION; FEMALE; FOCAL EPILEPSY; GENE EXPRESSION; GENE FREQUENCY; GENE MUTATION; GENETIC ASSOCIATION; GENETIC LINKAGE; GENETIC SCREENING; GENETIC VARIABILITY; HETEROZYGOSITY; HUMAN; LOSS OF FUNCTION MUTATION; MAJOR CLINICAL STUDY; MALE; MISSENSE MUTATION; MUTATIONAL ANALYSIS; NEUROPROTECTION; NONSENSE MUTATION; POINT MUTATION; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN UNFOLDING; SCHOOL CHILD; SINGLE NUCLEOTIDE POLYMORPHISM;

ADOLESCENT; ADULT; ALLELES; CARBOXYPEPTIDASES A; CASE-CONTROL STUDIES; CHILD; DEMOGRAPHY; ENZYME PRECURSORS; ENZYME STABILITY; EPILEPSY; FAMILY; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENETIC TESTING; HEK293 CELLS; HOT TEMPERATURE; HUMANS; HYDROGEN PEROXIDE; MALE; MODELS, MOLECULAR; MUTANT PROTEINS; MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; TRYPSIN;

EID: 84871139031     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.414094     Document Type: Article

References (45)

1. Hauser, W. A., Annegers, J. F., and Rocca, W. A. (1996) Descriptive epidemiology of epilepsy. Contributions of population-based studies from Rochester, Minnesota. Mayo. Clin. Proc. 71, 576-586
2. Sander, J. W., Hart, Y. M., Johnson, A. L., and Shorvon, S. D. (1990) National General Practice Study of Epilepsy. Newly diagnosed epileptic seizures in a general population. Lancet 336, 1267-1271 (Pubitemid 20382979)
3. Commission on Classification and Terminology of the International League Against Epilepsy. (1989) Proposal for revised classification of epilepsies and epileptic syndromes. Epilepsia 30, 389-399
4. Falconer, M. A., Serafetinides, E. A., and Corsellis, J. A. (1964) Etiology and Pathogenesis of Temporal Lobe Epilepsy. Arch Neurol. 10, 233-248
5. Baulac, S., Gourfinkel-An, I., Nabbout, R., Huberfeld, G., Serratosa, J., Leguern, E., and Baulac, M. (2004) Fever, genes, and epilepsy. Lancet Neurol. 3, 421-430 (Pubitemid 38796480)
6. Hauser, W. A. (1994) The prevalence and incidence of convulsive disorders in children. Epilepsia 35, S1-S6
7. Rich, S. S., Annegers, J. F., Hauser, W. A., and Anderson, V. E. (1987) Complex segregation analysis of febrile convulsions. Am. J. Hum. Genet. 41, 249-257 (Pubitemid 17145621)
8. Ottman, R. (1989) Genetics of the partial epilepsies. A review. Epilepsia 30, 107-111
9. Nakayama, J. (2009) Progress in searching for the febrile seizure susceptibility genes. Brain Dev. 31, 359-365
10. Salzmann, A., Malafosse, A. (2012) Genetics of temporal lobe epilepsy. A review. Epilepsy Res. Treat. 863702
11. Salzmann, A., Guipponi, M., Lyons, P. J., Fricker, L. D., Sapio, M., Lambercy, C., Buresi, C., Ouled Amar Bencheikh, B., Lahjouji, F., Ouazzani, R., Crespel, A., Chaigne, D., and Malafosse, A. (2012) Carboxypeptidase A6 gene (CPA6) mutations in a recessive familial form of febrile seizures and temporal lobe epilepsy and in sporadic temporal lobe epilepsy. Hum. Mutat. 33, 124-135
12. 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 (Pubitemid 34952570)
13. Lyons, P. J., Callaway, M. B., and Fricker, L. D. (2008) Characterization of carboxypeptidase A6, an extracellular matrix peptidase. J. Biol. Chem. 283, 7054-7063
14. Vendrell, J., Querol, E., and Avilés, F. X. (2000) Metallocarboxypeptidases and their protein inhibitors. Structure, function, and biomedical properties. Biochim. Biophys. Acta 1477, 284-298 (Pubitemid 30119907)
15. Phillips, M. A., and Rutter, W. J. (1996) Role of the prodomain in folding and secretion of rat pancreatic carboxypeptidase A1. Biochemistry 35, 6771-6776 (Pubitemid 26172436)
16. Gomis-Rüth, F. X. (2008) Structure and mechanism of metallocarboxypeptidases. Crit. Rev. Biochem. Mol. Biol. 43, 319-345
17. Lyons, P. J., and Fricker, L. D. (2010) Substrate specificity of human carboxypeptidase A6. J. Biol. Chem. 285, 38234-38242
18. Fontenele-Neto, J. D., Kalinina, E., Feng, Y., and Fricker, L. D. (2005) Identification and distribution of mouse carboxypeptidase A-6. Brain Res. Mol. Brain Res. 137, 132-142 (Pubitemid 40798896)
19. Consensus statement. (1980) Febrile seizures. Long-term management of children with fever-associated seizures. Pediatrics 66, 1009-1012
20. Montgomery, J., Wittwer, C. T., Palais, R., and Zhou, L. (2007) Simultaneous mutation scanning and genotyping by high resolution DNA melting analysis. Nat. Protoc. 2, 59-66 (Pubitemid 47040069)
21. Taylor, C. F. (2009) Mutation scanning using high resolution melting. Biochem. Soc. Trans. 37, 433-437
22. Wojdacz, T. K., Dobrovic, A., and Hansen, L. L. (2008) Methylation-sensitive high resolution melting. Nat. Protoc. 3, 1903-1908
23. Dudbridge, F., and Koeleman, B. P. (2003) Rank truncated product of P-values, with application to genomewide association scans. Genet. Epidemiol. 25, 360-366 (Pubitemid 37486884)
24. Wallace, H., Shorvon, S., and Tallis, R. (1998) Age-specific incidence and prevalence rates of treated epilepsy in an unselected population of 2,052,922 and age-specific fertility rates of women with epilepsy. Lancet 352, 1970-1973 (Pubitemid 29000863)
25. Kim, Y. H., Berry, A. H., Spencer, D. S., and Stites, W. E. (2001) Comparing the effect on protein stability of methionine oxidation versus mutagenesis. Steps toward engineering oxidative resistance in proteins. Protein Eng. 14, 343-347 (Pubitemid 32655950)
26. Stern, C. (1943) The Hardy-Weinberg Law. Science 97, 137-138
27. Gomis-Rüth, F. X., Botelho, T. O., and Bode, W. (2012) A standard orientation for metallopeptidases. Biochim. Biophys. Acta 1824, 157-163
28. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0. Discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786
29. Desmet, F. O., Hamroun, D., Lalande, M., Collod-Béroud, G., Claustres, M., and Béroud, C. (2009) Human Splicing Finder. An online bioinformatics tool to predict splicing signals. Nucleic Acids Res. 37, e67
30. Chen, H., Jawahar, S., Qian, Y., Duong, Q., Chan, G., Parker, A., Meyer, J. M., Moore, K. J., Chayen, S., Gross, D. J., Glaser, B., Permutt, M. A., and Fricker, L. D. (2001) Missense polymorphism in the human carboxypeptidase E gene alters enzymatic activity. Hum. Mutat. 18, 120-131
31. Dibbens, L. M., Reid, C. A., Hodgson, B., Thomas, E. A., Phillips, A. M., Gazina, E., Cromer, B. A., Clarke, A. L., Baram, T. Z., Scheffer, I. E., Berkovic, S. F., and Petrou, S. (2010) Augmented currents of an HCN2 variant in patients with febrile seizure syndromes. Ann. Neurol. 67, 542-546
32. Volkers, L., Kahlig, K. M., Verbeek, N. E., Das, J. H., van Kempen, M. J., Stroink, H., Augustijn, P., van Nieuwenhuizen, O., Lindhout, D., George, A. L., Jr., Koeleman, B. P., and Rook, M. B. (2011) Nav 1.1 dysfunction in genetic epilepsy with febrile seizures-plus or Dravet syndrome. Eur. J. Neurosci. 34, 1268-1275
33. Escayg, A., and Goldin, A. L. (2010) Sodium channel SCN1A and epilepsy. Mutations and mechanisms. Epilepsia 51, 1650-1658
34. Kang, J. Q., Shen, W., and Macdonald, R. L. (2009) The GABRG2 mutation, Q351X, associated with generalized epilepsy with febrile seizures plus, has both loss of function and dominant-negative suppression. J. Neurosci. 29, 2845-2856
35. Liao, W. P., Shi, Y. W., Long, Y. S., Zeng, Y., Li, T., Yu, M. J., Su, T., Deng, P., Lei, Z. G., Xu, S. J., Deng, W. Y., Liu, X. R., Sun, W. W., Yi, Y. H., Xu, Z. C., and Duan, S. (2010) Partial epilepsy with antecedent febrile seizures and seizure aggravation by antiepileptic drugs. Associated with loss of function of Na(v) 1.1. Epilepsia 51, 1669-1678
36. Moulard, B., Picard, F., le Hellard, S., Agulhon, C., Weiland, S., Favre, I., Bertrand, S., Malafosse, A., and Bertrand, D. (2001) Ion channel variation causes epilepsies. Brain Res. Brain Res. Rev. 36, 275-284 (Pubitemid 33020758)
37. Mulley, J. C., Scheffer, I. E., Harkin, L. A., Berkovic, S. F., and Dibbens, L. M. (2005) Susceptibility genes for complex epilepsy. Hum. Mol. Genet. 14 Spec No. 2, R243-R249
38. Schlachter, K., Gruber-Sedlmayr, U., Stogmann, E., Lausecker, M., Hotzy, C., Balzar, J., Schuh, E., Baumgartner, C., Mueller, J. C., Illig, T., Wichmann, H. E., Lichtner, P., Meitinger, T., Strom, T. M., Zimprich, A., and Zimprich, F. (2009) A splice site variant in the sodium channel gene SCN1A confers risk of febrile seizures. Neurology 72, 974-978
39. Le Gal, F., Salzmann, A., Crespel, A., and Malafosse, A. (2011) Replication of association between a SCN1A splice variant and febrile seizures. Epilepsia 52, e135-138
40. Lossin, C. (2009) A catalog of SCN1A variants. Brain Dev. 31, 114-130
41. Winterthun, S., Ferrari, G., He, L., Taylor, R. W., Zeviani, M., Turnbull, D. M., Engelsen, B. A., Moen, G., and Bindoff, L. A. (2005) Autosomal recessive mitochondrial ataxic syndrome due to mitochondrial polymerase γ mutations. Neurology 64, 1204-1208
42. Tzoulis, C., Engelsen, B. A., Telstad, W., Aasly, J., Zeviani, M., Winterthun, S., Ferrari, G., Aarseth, J. H., and Bindoff, L. A. (2006) The spectrum of clinical disease caused by the A467T and W748S POLG mutations. A study of 26 cases. Brain 129, 1685-1692 (Pubitemid 43999403)
43. Roshal, D., Glosser, D., and Zangaladze, A. (2011) Parieto-occipital lobe epilepsy caused by a POLG1 compound heterozygous A467T/W748S genotype. Epilepsy Behav. 21, 206-210
44. Pizzuti, A., Calabrese, G., Bozzali, M., Telvi, L., Morizio, E., Guida, V., Gatta, V., Stuppia, L., Ion, A., Palka, G., and Dallapiccola, B. (2002) A peptidase gene in chromosome 8q is disrupted by a balanced translocation in a duane syndrome patient. Invest. Ophthalmol. Vis. Sci. 43, 3609-3612 (Pubitemid 35470593)
45. Lyons, P. J., Ma, L. H., Baker, R., and Fricker, L. D. (2010) Carboxypeptidase A6 in zebrafish development and implications for VIth cranial nerve pathfinding. PLoS One 5, e12967