Novel carboxypeptidase A6 (CPA6) mutations identified in patients with juvenile myoclonic and generalized epilepsy

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Sapio, Matthew R ^a   Vessaz, Monique ^b   Thomas, Pierre ^c   Genton, Pierre ^d   Fricker, Lloyd D ^a   Salzmann, Annick ^e  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c UNIVERSITY HOSPITAL OF NICE   (France)

^d CENTRE SAINT PAUL   (France)

^e UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYPEPTIDASE A; CARBOXYPEPTIDASE A6; UNCLASSIFIED DRUG; ANTICONVULSIVE AGENT; CARBOXYPEPTIDASE A6, HUMAN;

ADULT; AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; CPA6 GENE; EMBRYO; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FEMALE; GENERALIZED EPILEPSY; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MALE; MISSENSE MUTATION; MUTATIONAL ANALYSIS; MYOCLONUS EPILEPSY; PROTEIN EXPRESSION; WILD TYPE; ADOLESCENT; ALLELE; AMINO ACID SEQUENCE; CASE CONTROL STUDY; CHEMISTRY; CHILD; CLINICAL TRIAL; DNA MUTATIONAL ANALYSIS; EPILEPSY, GENERALIZED; GENE EXPRESSION; GENETIC ASSOCIATION STUDY; GENETICS; MOLECULAR GENETICS; MOLECULAR MODEL; MULTICENTER STUDY; MUTATION; MYOCLONIC EPILEPSY, JUVENILE; PRESCHOOL CHILD; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SINGLE NUCLEOTIDE POLYMORPHISM; YOUNG ADULT;

ANIMALIA;

ADOLESCENT; ADULT; ALLELES; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTICONVULSANTS; CARBOXYPEPTIDASES A; CASE-CONTROL STUDIES; CHILD; CHILD, PRESCHOOL; DNA MUTATIONAL ANALYSIS; EPILEPSY, GENERALIZED; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; MYOCLONIC EPILEPSY, JUVENILE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; YOUNG ADULT;

EID: 84928923282     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0123180     Document Type: Article

References (57)

1. Berg AT, Berkovic SF, Brodie MJ, Buchhalter J, Cross JH, van Emde Boas W, et al. Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005-2009. Epilepsia. 2010; 51: 676-685. doi: 10.1111/j.1528-1167.2010. 02522.x PMID: 20196795
2. Jallon P, Latour P. Epidemiology of idiopathic generalized epilepsies. Epilepsia. 2005; 46 Suppl 9: 10-14. PMID: 16302871
3. Berg AT, Millichap JJ. The 2010 revised classification of seizures and epilepsy. Continuum. 2013; 19: 571-597. doi: 10.1212/01.CON.0000431377.44312.9e PMID: 23739099
4. Camfield CS, Striano P, Camfield PR. Epidemiology of juvenile myoclonic epilepsy. Epilepsy Behav. 2013; 28 Suppl 1: S15-17. doi: 10.1016/j.yebeh.2012.06.024 PMID: 23756473
5. Delgado-Escueta AV, Enrile-Bacsal F. Juvenile myoclonic epilepsy of Janz. Neurology. 1984; 34: 285-294. PMID: 6422321
6. Genton P, Thomas P, Kasteleijn-Nolst Trenite DG, Medina MT, Salas-Puig J. Clinical aspects of juvenile myoclonic epilepsy. Epilepsy Behav. 2013; 28 Suppl 1: S8-14. doi: 10.1016/j.yebeh.2012.10.034 PMID: 23756488
7. Kasteleijn-Nolst Trenite DG, Schmitz B, Janz D, Delgado-Escueta AV, Thomas P, Hirsch E, et al. Consensus on diagnosis and management of JME: From founder's observations to current trends. Epilepsy Behav. 2013; 28 Suppl 1: S87-90. doi: 10.1016/j.yebeh.2012.11.051 PMID: 23756490
8. Escayg A, De Waard M, Lee DD, Bichet D, Wolf P, Mayer T, et al. Coding and noncoding variation of the human calcium-channel beta4-subunit gene CACNB4 in patients with idiopathic generalized epilepsy and episodic ataxia. Am J Hum Genet. 2000; 66: 1531-1539. PMID: 10762541
9. Kapoor A, Satishchandra P, Ratnapriya R, Reddy R, Kadandale J, Shankar SK, et al. An idiopathic epilepsy syndrome linked to 3q13.3-q21 and missense mutations in the extracellular calcium sensing receptor gene. Ann Neurol. 2008; 64: 158-167. doi: 10.1002/ana.21428 PMID: 18756473
10. Cossette P, Liu L, Brisebois K, Dong H, Lortie A, Vanasse M, et al. Mutation of GABRA1 in an autosomal dominant form of juvenile myoclonic epilepsy. Nat Genet. 2002; 31: 184-189. PMID: 11992121
11. Dibbens LM, Feng HJ, Richards MC, Harkin LA, Hodgson BL, Scott D, et al. GABRD encoding a protein for extra- or peri-synaptic GABAA receptors is a susceptibility locus for generalized epilepsies. Hum Mol Genet. 2004; 13: 1315-1319. PMID: 15115768
12. Suzuki T, Delgado-Escueta AV, Aguan K, Alonso ME, Shi J, Hara Y, et al. Mutations in EFHC1 cause juvenile myoclonic epilepsy. Nat Genet. 2004; 36: 842-849. PMID: 15258581
13. de Nijs L, Wolkoff N, Grisar T, Lakaye B. Juvenile myoclonic epilepsy as a possible neurodevelopmental disease: role of EFHC1 or Myoclonin1. Epilepsy Behav. 2013; 28 Suppl 1: S58-60. doi: 10.1016/j. yebeh.2012.06.034 PMID: 23756481
14. Grisar T, Lakaye B, de Nijs L, LoTurco J, Daga A, Delgado-Escueta AV. Myoclonin1/EFHC1 in cell division, neuroblast migration, synapse/dendrite formation in juvenile myoclonic epilepsy. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV, editors. Jasper's Basic Mechanisms of the Epilepsies. 4th ed. Bethesda (MD); 2012. PMID: 22787666
15. Delgado-Escueta AV. Advances in genetics of juvenile myoclonic epilepsies. Epilepsy Curr. 2007; 7: 61-67. PMID: 17520076
16. Gardiner M. Genetics of idiopathic generalized epilepsies. Epilepsia. 2005; 46 Suppl 9: 15-20. PMID: 16302872
17. Pal DK, Evgrafov OV, Tabares P, Zhang F, Durner M, Greenberg DA. BRD2 (RING3) is a probable major susceptibility gene for common juvenile myoclonic epilepsy. Am J Hum Genet. 2003; 73: 261-270. PMID: 12830434
18. Mas C, Taske N, Deutsch S, Guipponi M, Thomas P, Covanis A, et al. Association of the connexin36 gene with juvenile myoclonic epilepsy. J Med Genet. 2004; 41: e93. PMID: 15235036
19. Greenberg DA, Cayanis E, Strug L, Marathe S, Durner M, Pal DK, et al. Malic enzyme 2 may underlie susceptibility to adolescent-onset idiopathic generalized epilepsy. Am J Hum Genet. 2005; 76: 139-146. PMID: 15532013
20. Helbig I, Hartmann C, Mefford HC. The unexpected role of copy number variations in juvenile myoclonic epilepsy. Epilepsy Behav. 2013; 28 Suppl 1: S66-68. doi: 10.1016/j.yebeh.2012.07.005 PMID: 23756484
21. Stogmann E, Lichtner P, Baumgartner C, Bonelli S, Assem-Hilger E, Leutmezer F, et al. Idiopathic generalized epilepsy phenotypes associated with different EFHC1 mutations. Neurology. 2006; 67: 2029-2031. PMID: 17159113
22. Salzmann A, Guipponi M, Lyons PJ, Fricker LD, Sapio M, Lambercy C, et al. 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. 2012; 33: 124-135. doi: 10.1002/humu.21613 PMID: 21922598
23. Sapio MR, Salzmann A, Vessaz M, Crespel A, Lyons PJ, Malafosse A, et al. Naturally occurring carboxypeptidase A6 mutations: effect on enzyme function and association with epilepsy. J Biol Chem. 2012; 287: 42900-42909. doi: 10.1074/jbc.M112.414094 PMID: 23105115
24. Belhedi N, Perroud N, Karege F, Vessaz M, Malafosse A, Salzmann A. Increased CPA6 promoter methylation in focal epilepsy and in febrile seizures. Epilepsy Res. 2014; 108: 144-148. doi: 10.1016/j. eplepsyres.2013.10.007 PMID: 24290490
25. Escayg A, Goldin AL. Sodium channel SCN1A and epilepsy: mutations and mechanisms. Epilepsia. 2010; 51: 1650-1658. doi: 10.1111/j.1528-1167.2010.02640.x PMID: 20831750
26. Sapio MR, Fricker LD. Carboxypeptidases in disease: insights from peptidomic studies. Proteomics Clin Appl. 2014; 8: 327-337. doi: 10.1002/prca.201300090 PMID: 24470285
27. Wei S, Segura S, Vendrell J, Aviles FX, Lanoue E, Day R, et al. Identification and characterization of three members of the human metallocarboxypeptidase gene family. J Biol Chem. 2002; 277: 14954-14964. PMID: 11836249
28. Lyons PJ, Callaway MB, Fricker LD. Characterization of carboxypeptidase A6, an extracellular matrix peptidase. J Biol Chem. 2008; 283: 7054-7063. doi: 10.1074/jbc.M707680200 PMID: 18178555
29. Reznik SE, Fricker LD. Carboxypeptidases from A to z: implications in embryonic development and Wnt binding. Cell Mol Life Sci. 2001; 58: 1790-1804. PMID: 11766880
30. Lyons PJ, Fricker LD. Substrate specificity of human carboxypeptidase A6. J Biol Chem. 2010; 285: 38234-38242. doi: 10.1074/jbc.M110.158626 PMID: 20855895
31. Fontenele-Neto JD, Kalinina E, Feng Y, Fricker LD. Identification and distribution of mouse carboxypeptidase A-6. Brain Res Mol Brain Res. 2005; 137: 132-142. PMID: 15950771
32. Guipponi M, Thomas P, Girard-Reydet C, Feingold J, Baldy-Moulinier M, Malafosse A. Lack of association between juvenile myoclonic epilepsy and GABRA5 and GABRB3 genes. Am J Med Genet. 1997; 74: 150-153. PMID: 9129713
33. Proposal for revised classification of epilepsies and epileptic syndromes. Commission on Classification and Terminology of the International League Against Epilepsy. Epilepsia. 1989; 30: 389-399. PMID: 2502382
34. Dudbridge F. Pedigree disequilibrium tests for multilocus haplotypes. Genet Epidemiol. 2003; 25: 115-121. PMID: 12916020
35. Schrodinger, LLC (2010) The PyMOL Molecular Graphics System, Version 1.3r1.
36. Stern C. The Hardy-Weinberg Law. Science. 1943; 97: 137-138. PMID: 17788516
37. Thusberg J, Olatubosun A, Vihinen M. Performance of mutation pathogenicity prediction methods on missense variants. Hum Mutat. 2011; 32: 358-368. doi: 10.1002/humu.21445 PMID: 21412949
38. Gomis-Ruth FX. Structure and mechanism of metallocarboxypeptidases. Crit Rev Biochem Mol Biol. 2008; 43: 319-345. doi: 10.1080/10409230802376375 PMID: 18937105
39. Garcia-Saez I, Reverter D, Vendrell J, Aviles FX, Coll M. The three-dimensional structure of human procarboxypeptidase A2. Deciphering the basis of the inhibition, activation and intrinsic activity of the zymogen. EMBO J. 1997; 16: 6906-6913. PMID: 9384570
40. Varlamov O, Leiter EH, Fricker L. Induced and spontaneous mutations at Ser202 of carboxypeptidase E. Effect on enzyme expression, activity, and intracellular routing. J Biol Chem. 1996; 271: 13981-13986. PMID: 8662840
41. Song L, Fricker LD. The pro region is not required for the expression or intracellular routeing of carboxypeptidase E. The Biochemical journal. 1997; 323 (Pt 1): 265-271. PMID: 9173892
42. Novikova EG, Reznik SE, Varlamov O, Fricker LD. Carboxypeptidase Z is present in the regulated secretory pathway and extracellular matrix in cultured cells and in human tissues. J Biol Chem. 2000; 275: 4865-4870. PMID: 10671522
43. Eng FJ, Varlamov O, Fricker LD. Sequences within the cytoplasmic domain of gp180/carboxypeptidase D mediate localization to the trans-Golgi network. Mol Biol Cell. 1999; 10: 35-46. PMID: 9880325
44. Katano M, Numata T, Aguan K, Hara Y, Kiyonaka S, Yamamoto S, et al. The juvenilemyoclonic epilepsyrelated protein EFHC1 interacts with the redox-sensitive TRPM2 channel linked to cell death. Cell Calcium. 2012; 51: 179-185. doi: 10.1016/j.ceca.2011.12.011 PMID: 22226147
45. Rossetto MG, Zanarella E, Orso G, Scorzeto M, Megighian A, Kumar V, et al. Defhc1.1, a homologue of the juvenile myoclonic gene EFHC1, modulates architecture and basal activity of the neuromuscular junction in Drosophila. Hum Mol Genet. 2011; 20: 4248-4257. doi: 10.1093/hmg/ddr352 PMID: 21835885
46. Noebels JL. The biology of epilepsy genes. Annu Rev Neurosci. 2003; 26: 599-625. PMID: 14527270
47. Lyons PJ, Ma LH, Baker R, Fricker LD. Carboxypeptidase A6 in zebrafish development and implications for VIth cranial nerve pathfinding. PLoS One. 2010; 5: e12967. doi: 10.1371/journal.pone. 0012967 PMID: 20885977
48. Tanco S, Lorenzo J, Garcia-Pardo J, Degroeve S, Martens L, Aviles FX, et al. Proteome-derived peptide libraries to study the substrate specificity profiles of carboxypeptidases. Mol Cell Proteomics. 2013; 12: 2096-2110. doi: 10.1074/mcp.M112.023234 PMID: 23620545
49. Fialka F, Gruber RM, Hitt R, Opitz L, Brunner E, Schliephake H, et al. CPA6, FMO2, LGI1, SIAT1 and TNC are differentially expressed in early- and late-stage oral squamous cell carcinoma-a pilot study. Oral Oncol. 2008; 44: 941-948. doi: 10.1016/j.oraloncology.2007.10.011 PMID: 18234543
50. Pizzuti A, Calabrese G, Bozzali M, Telvi L, Morizio E, Guida V, et al. A peptidase gene in chromosome 8q is disrupted by a balanced translocation in a duane syndrome patient. Invest Ophthalmol Vis Sci. 2002; 43: 3609-3612. PMID: 12454025
51. Fricker LD, Snyder SH. Enkephalin convertase: purification and characterization of a specific enkephalin-synthesizing carboxypeptidase localized to adrenal chromaffin granules. Proc Natl Acad Sci U S A. 1982; 79: 3886-3890. PMID: 6808517
52. Che FY, Yan L, Li H, Mzhavia N, Devi LA, Fricker LD. Identification of peptides from brain and pituitary of Cpe(fat)/Cpe(fat) mice. Proc Natl Acad Sci U S A. 2001; 98: 9971-9976. PMID: 11481435
53. Bajzar L, Manuel R, Nesheim ME. Purification and characterization of TAFI, a thrombin-activable fibrinolysis inhibitor. J Biol Chem. 1995; 270: 14477-14484. PMID: 7782309
54. Berezniuk I, Vu HT, Lyons PJ, Sironi JJ, Xiao H, Burd B, et al. Cytosolic Carboxypeptidase 1 Is Involved in Processing alpha- and beta-Tubulin. J Biol Chem. 2012; 287: 6503-6517. doi: 10.1074/jbc.M111. 309138 PMID: 22170066
55. Rogowski K, van Dijk J, Magiera MM, Bosc C, Deloulme JC, Bosson A, et al. A family of proteindeglutamylating enzymes associated with neurodegeneration. Cell. 2010; 143: 564-578. doi: 10.1016/ j.cell.2010.10.014 PMID: 21074048
56. Rodriguez de la Vega Otazo M, Lorenzo J, Tort O, Aviles FX, Bautista JM. Functional segregation and emerging role of cilia-related cytosolic carboxypeptidases (CCPs). FASEB J. 2012;
57. Moeller C, Swindell EC, Kispert A, Eichele G. Carboxypeptidase Z (CPZ) modulates Wnt signaling and regulates the development of skeletal elements in the chicken. Development. 2003; 130: 5103-5111. PMID: 12944424