Characterization of a novel BCHE "silent" allele: Point mutation (p.Val204Asp) causes loss of activity and prolonged apnea with suxamethonium

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Delacour, Herve ^a   Lushchekina, Sofya ^b   Mabboux, Isabelle ^a   Bousquet, Aurore ^a,c   Ceppa, Franck ^a,c   Schopfer, Lawrence M ^d   Lockridge, Oksana ^d   Masson, Patrick ^d,e  

^a Military Hospital Begin   (France)

^b EMANUEL INSTITUTE OF BIOCHEMICAL PHYSICS   (Russian Federation)

^c Val de Grace School of Military Medicine   (France)

^d UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^e INSTITUT DE BIOLOGIE STRUCTURALE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; BENZOYLCHOLINE; BUTYRYLTHIOCHOLINE; CHOLINESTERASE; CINCHOCAINE; FLUORIDE; GLUTAMINE; GLYCINE; HISTIDINE; SERINE; SUXAMETHONIUM; THREONINE; VALINE; ISOQUINOLINE DERIVATIVE; MIVACURIUM; NEUROMUSCULAR DEPOLARIZING AGENT;

ALLELE; APNEA; ARTICLE; BCHE GENE; CATALYSIS; ELECTROPHORESIS; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; ENZYME INHIBITION; ENZYME KINETICS; ENZYME SUBSTRATE; FEMALE; GENETIC VARIABILITY; GENOTYPE; HUMAN; HYDROGEN BOND; INFANT; MALE; MOLECULAR DYNAMICS; NEUROMUSCULAR BLOCKING; PHENOTYPE; POINT MUTATION; BIOCATALYSIS; CASE REPORT; CHEMICALLY INDUCED; CHEMISTRY; ENZYMOLOGY; FAMILY HEALTH; GENETICS; KINETICS; METABOLISM; MISSENSE MUTATION; NEWBORN; NUCLEOTIDE SEQUENCE; PEDIGREE;

ALLELES; APNEA; BASE SEQUENCE; BIOCATALYSIS; BUTYRYLCHOLINESTERASE; DNA MUTATIONAL ANALYSIS; FAMILY HEALTH; FEMALE; HUMANS; INFANT, NEWBORN; ISOQUINOLINES; KINETICS; MALE; MOLECULAR DYNAMICS SIMULATION; MUTATION, MISSENSE; NEUROMUSCULAR DEPOLARIZING AGENTS; PEDIGREE; SUCCINYLCHOLINE;

EID: 84904609510     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101552     Document Type: Article

References (30)

1. Masson P, Lockridge O (2010) Butyrylcholinesterase for protection from organophosphorus poisons: catalytic complexities and hysteretic behavior. Arch Biochem Biophys 494: 107-120.
2. Johnson G, Moore SW (2012) Why has butyrylcholinesterase been retained? Structural and functional diversification in a duplicated gene. Neurochem Int 61: 783-797.
3. Forbat A, Lehmann H, Silk E (1953) Prolonged apnoea following injection of succinylcholine. Lancet 265: 1067-1068.
4. Kalow W, Genest K (1957) A method for the detection of atypical forms of human serum cholinesterase; determination of dicucaine number. Can J Biochem Physiol 35: 339-346.
5. Souza RL, Mikami LR, Maegawa RO, Chautard-Freire-Maia EA (2005) Four new mutations in the BCHE gene of human butyrylcholinesterase in a Brazilian blood donor sample. Mol Genet Metab 84: 349-353. (Pubitemid 40386882)
6. Zsigmond EK, Downs JR (1971) Plasma cholinesterase activity in newborns and infants. Canad Anaest Soc J 18: 278-285.
7. Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7: 88-95.
8. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, et al. (2010) A method and server for predicting damaging missense mutations. Nat Methods 7: 248-249.
9. Schwarz JM, Rödelsperger C, Schuelke M, Seelow D (2010) MutationTaster evaluates disease-causing potential of sequence alterations. Nat Methods 7: 575-576.
10. Harris H, Whittaker M (1961) Differential inhibition of human serum cholinesterase with fluoride: recognition of two new phenotypes. Nature 191: 556-562.
11. Radić Z, Pickering NA, Vellom DC, Camp S, Taylor P (1993) Three distinct domains in the cholinesterase molecule confer selectivity for acetyl- and butyrylcholinesterase inhibitors. Biochemistry 32: 12074-12084. (Pubitemid 23353646)
12. Masson P, Legrand P, Bartels CF, Froment MT, Schopfer LM, et al. (1997) Role of aspartate 70 and tryptophane 82 in binding of succinydithiocholine to human butyrylcholinesterase. Biochemistry 36: 2266-2277. (Pubitemid 27104721)
13. Li B, Sedlacek M, Manoharan I, Boopathy R, Duysen EG, et al. (2005) Butyrylcholinesterase, paraoxonase, and albumin esterase, but not carboxylesterase, are present in human plasma. Biochem Pharmacol 70: 1673-16784.
14. Karnovsky MJ, Roots LA (1964) A "direct-coloring" thiocholine method for cholinesterases. J Histochem Cytochem 12: 219-221.
15. Checler F, Grassi J, Masson P, Vincent JP (1990) Monoclonal antibodies allow precipitation of esterasic but not peptidasic activities associated with butyrylcholinesterase. J Neurochem 55: 750-5.
16. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
17. Nicolet Y, Lockridge O, Masson P, Fontecilla-Camps JC, Nachon F (2003) Crystal structure of human butyrylcholinesterase and of its complexes with substrate and products. J Biol Chem 278: 41141-41147. (Pubitemid 37280939)
18. Masson P, Lushchekina S, Schopfer LM, Lockridge O (2013) Effects of viscosity and osmotic stress on the reaction of human butyrylcholinesterase with cresyl saligenin phosphate, a toxicant related to the aerotoxic syndrome: Kinetic and molecular dynamics studies. Biochem J 454: 387-399.
19. Lushchekina SV, Nemukhin AV, Varfolomeev SD, Masson P (2014) Molecular modeling evidence for His 438 flip in the mechanism of BuChE hysteretic behavior. J Mol Neurosci 52: 434-445.
20. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802. (Pubitemid 43078511)
21. Best RB, Zhu X, Shim J, Lopes PEM, Mittal J, et al. (2012) Optimization of the Additive CHARMM All-Atom Protein Force Field Targeting Improved Sampling of the Backbone Q, y and Side-Chain x 1 and x2 Dihedral Angles. J Chem Theor Comput 8: 3257-3273.
22. Sadovnichy V, Tikhonravov A, Voevodin V, Opanasenko V (2013) "Lomonosov": Supercomputing at Moscow State University. In Contemporary High Performance Computing: From Petascale toward Exascale, J.S. Vetter, ed. (Boca Raton, USA, CRC Press), pp 283-307.
23. Bakan A, Meireles LM, Bahar I (2011) ProDy: Protein Dynamics Inferred from Theory and Experiments. Bioinformatics 27: 1575-1577.
24. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38. (Pubitemid 26152973)
25. Sakamoto N, Hidaka K, Fujisawa T, Maeda M, Iuchi I (1998) Identification of a point mutation associated with a silent phenotype of human serum butyrylcho-linesterase- a case of familial cholinesterasemia. Clin Chim Acta 274: 159-166. (Pubitemid 28269298)
26. Primo-Parmo SL, Bartels CF, Wiersema B, van der Spek AFL, Innis JW, et al. (1996) Characterization of 12 silent alleles of the human butyrylcholinesterase (BCHE) gene. Am J Hum Genet 58: 52-64.
27. Hidaka K, Watanabe Y, Tomita M, Ueda N, Higashi M, et al. (2001) Gene analysis of genomic DNA from stored serum by polymerase chain reaction: identification of three missense mutations in patients with cholinesterasemia and ABO genotyping. Clin Chim Acta 303: 61-67. (Pubitemid 32121806)
28. Varkey Altamirano C, Bartels CF, Lockridge O (2000) The butyrylcholinesterase K-variant shows similar protein turnover and quaternary interaction to the wild-type enzyme. J Neurochem 74: 869-877. (Pubitemid 30053761)
29. Varkey Altamirano C, Lockridge O (1999) Conserved aromatic residue of the Cterminus of human butyrylcholinesterase mediate the association of tetramers. Biochemistry 38: 13414-13412.
30. Podoly E, Hanin G, Soreq H (2010) Alanine-to-threonine substitutions and amyloid disease: butyrylcholinesterase as a case study. Chem Biol Interact 187: 64-71.