Cholinesterases: the opinion of neurophysiologist



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Abstract

The review addresses issues of structure and functions of acetyl- and butyrylcholinesterases. Authors consider these enzymes not only as limiters of the neurotransmitter acetylcholine life span in synaptic cleft but also accounting for their putative non-synaptic functions. Particular emphasis has been placed on the possibility of correction of nerve system pathologies by way of modification of the activity of these enzymes.

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About the authors

K. A Petrov

A.E. Arbuzov Institute of Organic and Physical Chemistry; Kazan (Volga Region) Federal University; Kazan Institute of Biochemistry and Biophysics

A. D Kharlamova

A.E. Arbuzov Institute of Organic and Physical Chemistry; Kazan (Volga Region) Federal University; Kazan Institute of Biochemistry and Biophysics

E. E Nikolsky

A.E. Arbuzov Institute of Organic and Physical Chemistry; Kazan (Volga Region) Federal University; Kazan Institute of Biochemistry and Biophysics

References

  1. Massouli J., Perrier N., Noureddine H. et al. Old and new questions about cholinesterases. Chem Biol Interact. 2008; 75(1-3): 30-44.
  2. Silman I., Sussman J.L. Acetylcholinesterase: how is structure related to function? Chem. Biol. Interact. 2008; 175(1-3): 3-10.
  3. Моралев С.М., Розенгарт Е.В. Современные представления о структуре и каталитических свойствах холинэстераз позвоночных и беспозвоночных (обзор). Журнал эволюционной биохимии и физиологии 1999; 35(1): 3-14.
  4. Lawler H.C. Turnover time of acetylcholinesterase. J. Biol. Chem. 1961; 236: 2296-301.
  5. Kaplan D., Ordentlich A., Barak D. et al. Does "butyrylization" of acetylcholinesterase through substitution of the six divergent aromatic amino acids in the active center gorge generate an enzyme mimic of butyrylcholinesterase? Biochemistry 2001; 40(25): 7433-45.
  6. Chatonnet A., Lockridge O. Comparison of butyrylcholinesterase and acetylcholinesterase. Biochem. J. 1989; 260(3): 625-34.
  7. Loewi O., Navratil E. Pflug. Arch. Ges. Physiol. 1926; 214: 678.
  8. Wood S.J., Slater C.R. Safety factor at the neuromuscular junction. Prog. Neurobiol. 2000; 64(4): 393-429.
  9. Hobbiger F. Pharmacology of anticholinesterase drugs. Handbook of exp. pharmacol. Berlin: Springer-Verlag, N.Y.: Heidelberg, 1976; 42(4): 486-581.
  10. Adler M., Manley H.A., Purcell A.L. et al. Reduced acetylcholine receptor density, morphological remodeling, and butyrylcholinesterase activity can sustain muscle function in acetylcholinesterase knockout mice. Muscle Nerve 2004; 30(3): 317-27.
  11. Girard E., Bernard V., Minic J. et al. Butyrylcholinesterase and the control of synaptic responses in acetylcholinesterase knockout mice. Life Sci. 2007; 80(24-25): 2380-5.
  12. Chatonnet F., Boudinot E., Chatonnet A. et al. Breathing without acetylcholinesterase. Adv. Exp. Med. Biol. 2004; 551: 165-70.
  13. Katz B., Miledi R. The binding of acetylcholine to receptors and its removal from the synaptic cleft. J. Physiol. 1973; 231: 549-74.
  14. Garcia-Carrasco M., Escarcega R.O., Fuentes-Alexandro S. et al. Therapeutic options in autoimmune myasthenia gravis. Autoimmun. Rev. 2007; 6(6): 373-8.
  15. Osborn G.G., Saunders A.V. Current treatments for patients with Alzheimer disease. J. Am. Osteopath. Assoc. 2010; 110 (9 Suppl
  16. : 16-26.
  17. Кривой И.И., Кулешов В.И., Матюшин Д.Л. Нервно-мышечный синапс и антихолинэстеразные вещества. Л.: Изд-во ЛГУ им. А.А. Жданова; 1987.
  18. Anglister L., Stiles J.R., Salpeter M.M. Acetylcholinesterase density and turnover number at frog neuromuscular junctions, with modeling of their role in synaptic function. Neuron1994; 12(4): 783-94.
  19. Rotundo R.L., Rossi S.G., Kimbell L.M. et al. Targeting acetylcholinesterase to the neuromuscular synapse. Chem. Biol. Interact. 2005; 157-158: 15-21.
  20. Rotundo R.L., Ruiz C.A., Marrero E. et al. Assembly and regulation of acetylcholinesterase at the vertebrate neuromuscular junction. Chem. Biol. Interact. 2008; 175(1-3): 26-9.
  21. Grifman M., Arbel A., Ginzberg D. et al. In vitro phosphorylation of acetylcholinesterase at non-consensus protein kinase A sites enhances the rate of acetylcholine hydrolysis. Brain Res. Mol. Brain. Res. 1997; 51(1-2): 179-87.
  22. Udayabanu M., Kumaran D., Nair R.U. et al. Nitric oxide associated with iNOS expression inhibits acetylcholinesterase activity and induces memory impairment during acute hypobaric hypoxia. Brain Res. 2008; 1230: 138-49.
  23. Malomouzh A.I., Nurullin L.F., Arkhipova S.S. et al. NMDA receptors at the endplate of rat skeletal muscles: precise postsynaptic localization. Muscle Nerve 2011; 44(6): 987-9.
  24. Petrov K.A., Malomouzh A.I., Kovyazina I.V. et al. Regulation of acetylcholinesterase activity by nitric oxide in rat neuromuscular junction via N-methyl-D-aspartate receptor activation. Eur. J. Neurosci. 2013; 37(2): 181-9.
  25. Vigny M., Gisiger V., Massouli J. «Nonspecific» cholinesterase and acetylcholinesterase in rat tissues: molecular forms, structural and catalytic properties, and significance of the two enzyme systems. PNAS USA 1978; 75: 2588-92.
  26. Sikorav J.L. Krejci E., Massoulie J. cDNA sequences of Torpedo marmorata acetylcholinesterase: primary structure of the precursor of a catalytic subunit; existence of multiple 5'-untranslated regions. EMBO J. 1987; 6: 1865-73.
  27. Rotundo R.L., Gomez A.M., Fernandez-Valle C. et al. Allelic variants of acetylcholinesterase: genetic evidence that all acetylcholinesterase forms in avian nerves and muscles are encoded by a single gene. PNAS USA 1988; 85(20): 7805-9.
  28. Maulet Y., Camp S., Gibney G. et al. Single gene encodes glycophospholipid-anchored and asymmetric acetylcholinesterase forms: Alternate coding exons contain inverted repeat sequences. Neuron 1990; 4: 289-301.
  29. Sikorav J.-L., Duval N., Anselmet A. et al. Complex alternative splicing of acetylcholinesterase transcripts in Torpedo electric organ; Primary structure of the precursor of the glycolipid-anchored dimeric form. EMBO J. 1988; 7: 2983-93.
  30. Soreq H., Ben-Aziz R., Prody C.A. et al. Molecular cloning and construction of the coding region for human acytlcholinesterase reveals a G+C-rich attenuation structure. PNAS USA 1990; 87: 9688-92.
  31. Maulet Y., Camp S., Gibney G. et al. Single gene encodes glycophospholipid-anchored and asymmetric acetylcholinesterase forms: alternative coding exons contain inverted repeat sequences. Neuron 1990; 4(2): 289-301.
  32. Li Y., Camp S., Rachinsky T.L. et al. Gene structure of mammalian acetylcholinesterase. Alternative exons dictate tissue-specific expression. J. Biol. Chem. 1991; 266: 23083-90.
  33. Li Y., Camp S., Rachinsky T.L. et al. Promoter elements and transcriptional control of the mouse acetylcholinesterase gene. J. Biol. Chem. 1993а; 268:3563-72.
  34. Li Y., Camp S., Taylor P. Tissue-specific expression and alternate mRNA processing of the mammalian acetylcholinesterase gene. J. Bio. Chem. 1993b; 268: 5790-97.
  35. Ekstrom T.J., Klump W.M., Getman D. et al. Promoter elements and transcriptional regulation of the acetylcholinesterase gene. DNA Cell Biol. 1993; 12:63-72.
  36. Massoulie J. The origin of the molecular diversity and functional anchoring of cholinesterases. Neurosignals 2002; 11(3): 130-43.
  37. Kaufer D., Friedman A., Seidman S. et al. Acute stress facilitates long-lasting changes in cholinergic gene expression. Nature 1998; 393: 373-7.
  38. Perrier N.A., Salani M., Falasca C. et al. The readthrough variant of acetylcholinesterase remains very minor after heat shock, organophosphate inhibition and stress, in cell culture and in vivo. J. Neurochem. 2005; 94: 629-38.
  39. Atanasova E., Chiappa S., Wieben E. et al. Novel messenger RNA and alternative promoter for murine acetylcholinesterase. J. Biol. Chem. 1999; 274: 21078-84.
  40. Meshorer E., Toiber D., Zurel D. et al. Combinatorial complexity of 5' alternative acetylcholinesterase transcripts and protein products. J. Biol. Chem. 2004; 279: 29740-51.
  41. Camp S., De Jaco A., Zhang L. et al. Acetylcholinesterase expression in muscle is specifically controlled by a promoter-selective enhancesome in the first intron. J. Neurosci. 2008; 28: 2459-70.
  42. Arpagaus M., Kott M., Vatsis K.P. et al. Structure of the gene for human butyrylcholinesterase. Evidence for a single copy. Biochemistry 1990; 29: 124-131.
  43. Krejci E., Thomine S., Boschetti N. et al. The mammalian gene of acetylcholinesterase-associated collagen. J. Biol. Chem. 1997; 272(36): 22840-7.
  44. Ting A.L., Siow N.L., Kong L.W. et al. Transcriptional regulation of acetylcholinesterase-associated collagen ColQ in fast- and slow-twich muscle fibers. Chem. Biol. Interact. 2005; 15: 157-8.
  45. Perrier A.L., Massoulie J., Krejci E. PRiMA: The membrane anchor of acetylcholinesterase in the brain. Neuron 2002; 33: 275-85.
  46. Perrier N.A., Kherif S., Perrier A.L. et al. Expression of PRiMA in the mouse brain: membrane anchoring and accumulation of 'tailed' acetylcholinesterase. Eur. J. Neurosci. 2003; 18(7): 1837-47.
  47. Mok M.K., Leung K.W., Xie H.Q. et al. A new variant of proline-rich membrane anchor (PRiMA) of acetylcholinesterase in chicken: expression in different muscle fiber types. Neurosci. Lett. 2009; 461(2): 202-6.
  48. Grassi J. Vigny M., Massoulie J. Molecular forms of acetylcholinesterase in bovine caudate nucleus and superior cervical ganglion: solubility properties and hydrophobic character. J. Neurochem. 1982; 38:457-69.
  49. Rakonczay Z., Vincendon G., Zanetta J.P. Heterogeneity of rat brain acetylcholinesterase: a study by gel filtration and gradient centrifugation. J. Neurochem. 1981; 37:662-69.
  50. Xie H.Q., Liang D., Leung K.W. et al. Targeting acetylcholinesterase to membrane rafts: a function mediated by the proline-rich membrane anchor (Prima) in neurons. J. Biol. Chem. 2010; 285: 11537-46.
  51. Hicks D., John D., Makova N.Z. et al. Membrane Targeting, Shedding and Protein Interactions of Brain Acetylcholinesterase. J. Neurochem. 2011; 116: 742-6.
  52. Golub T., Wacha S., Caroni P. Spatial and temporal control of signaling through lipid rafts. Curr. Opin. Neurobiol. 2004; 14(5): 542-50.
  53. Dart C. Lipid microdomains and the regulation of ion channel function. J Physiol. 2010; 588(17): 3169-78.
  54. Neumann A.K., Itano M.S., Jacobson K. Understanding lipid rafts and other related membrane domains. F1000 Biol. Rep. 2010; 2:31.
  55. Ohno-Iwashita Y., Shimada Y., Hayashi M. et al. Cholesterolbinding toxins and anti-cholesterol antibodies as structural probes for cholesterol localization. Subcell. Biochem. 2010; 51: 597-621.
  56. Slutsky I., Silman I., Parnas I. et al. Presynaptic M(2) muscarinic receptors are involved in controlling the kinetics of ACh release at the frog neuromuscular junction. J. Physiol. 2001; 536(Pt 3): 717-25.
  57. Oliveira L., Timoteo M.A., Correia-de-Sa P. Modulation by adenosine of both muscarinic M1-facilitation and M2-inhibition of [3H]-acetylcholine release from the rat motor nerve terminals. Eur J Neurosci. 2002; 15(11): 1728-36.
  58. Oliveira L, Timoteo MA, Correia-de-Sa P. Negative crosstalk between M1 and M2 muscarinic autoreceptors involves endogenous adenosine activating A1 receptors at the rat motor endplate. Neurosci. Lett. 2009; 459(3): 127-31.
  59. Dudel J. The time course of transmitter release in mouse motor nerve terminals is differentially affected by activation of muscarinic M1 or M2 receptors. Eur. J. Neurosci. 2007; 26(8): 2160-8.
  60. Vizi E.S., Lendvai B. Modulatory role of presynaptic nicotinic receptors in synaptic and non-synaptic chemical communication in the central nervous system. Brain Res. Brain Res. Rev. 1999; 30(3): 219-35.
  61. Bruses J.L., Chauvet N., Rutishauser U. Membrane lipid rafts are necessary for the maintenance of the (alpha)7 nicotinic acetylcholine receptor in somatic spines of ciliary neurons. J. Neurosci. 2001; 21(2): 504-12.
  62. Delint-Ramirez I., Fernandez E., Bayes A. et al. In vivo composition of NMDA receptor signaling complexes differs between membrane subdomains and is modulated by PSD-95 and PSD-93. J. Neurosci. 2010; 30(24): 8162-70.
  63. Stetzkowski-Marden F., Recouvreur M., Camus G. et al. Rafts are required for acetylcholine receptor clustering. J Mol Neurosci. 2006;30(1-2):37-8.
  64. Pato C., Stetzkowski-Marden F., Gaus K. et al. Role of lipid rafts in agrin-elicited acetylcholine receptor clustering. Chem. Biol. Interact. 2008; 175(1-3): 64-7.
  65. Allen J.A., Halverson-Tamboli R.A., Rasenick M.M. Lipid raft microdomains and neurotransmitter signalling. Nat. Rev. Neurosci. 2007; 8(2): 128-40.
  66. Bowen D.M., Smith C.B., White P. et al. Neurotransmitter-related enzymes and indices of hypoxia in senile dementia and other abiotrophies. Brain 1976; 99: 459-96
  67. Davies P., Maloney A.J.F. Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 1976; 2: 1403.
  68. Perry E.K., Perry R.H., Blessed G. et al. Necropsy evidence of central cholinergic deficits in senile dementia. Lancet 1977; 1: 189.
  69. Weinstock M. The pharmacotherapy of Alzheimer's disease based on the cholinergic hypothesis: an update. Neurodegeneration 1995; 4(4): 349-56.
  70. Eagger S.A., Levy R., Sahakian B.J. Tacrine in Alzheimer's disease, Lancet 1991; 337: 989-92.
  71. Greenfield S.A. A noncholinergic action of acetylcholinesterase (AChE) in the brain: from neuronal secretion to the generation of movement. Cell. Mol. Neurobiol. 1991; 11(1): 55-77.
  72. Appleyard M., Jahnsen H. Actions of acetylcholinesterase in the guinea-pig cerebellar cortex in vitro. Neuroscience 1992; 47(2): 291-301.
  73. Dong H., Xiang Y.Y., Farchi N. et al. Excessive expression of acetylcholinesterase impairs glutamatergic synaptogenesis in hippocampal neurons. J. Neurosci. 2004; 24: 8950-60.
  74. Paraoanu L., Layer P. Acetylcholinesterase in cell adhesion, neurite growth and network formation. FEBS J. 2008; 275: 618-24.
  75. Zhang X.J., Yang L., Zhao Q. et al. Induction of acetylcholinesterase expression during apoptosis in various cell types. Cell Death Differ. 2002; 9: 790-800.
  76. Santos S.C., Vala I., Miguel C. et al. Expression and subcellular localization of a novel nuclear acetylcholinesterase protein. J. Biol. Chem. 2007; 282: 25597-603.
  77. Botti S.A., Felder C.E., Sussman J.L. et al. Electrotactins: a class of adhesion proteins with conserved electrostatic and structural motifs. Protein Eng.1998; 11: 415-20.
  78. Sharma K.V., Koenigsberger C., Brimijoin S. et al. Direct evidence for an adhesive function in the noncholinergic role of acetylcholinesterase in neurite outgrowth. J. Neurosci. Res. 2001; 63: 165-75.
  79. Inkson C.A., Brabbs A.C., Grewal T.S. et al. Characterization of acetylcholinesterase expression and secretion during osteoblast differentiation. Bone 2004; 35:819-27.
  80. Layer P.G., Weikert T., Alber R. Cholinesterases regulate neurite growth of chick nerve cells in vitro by means of a non-enzymatic mechanism. Cell Tissue Res. 1993; 273: 219-26
  81. Geula C., Mesulam M. Special properties of cholinesterases in the cerebral cortex of Alzheimer's disease. Brain Res. 1989; 498(1): 185-9.
  82. Inestrosa N.C., Alvarez A., Perez C.A. et al. Acetylcholinesterase accelerates assembly of amyloid-beta-peptides into Alzheimer's fibrils: possible role of the peripheral site of the enzyme. Neuron 1996; 16: 881-91.
  83. Inestrosa N.C., Urra S., Colombres M. Acetylcholinesterase (AChE) - amyloid-p-peptide complexes in Alzheimer's disease. the Wnt signaling pathway. Current Alzheimer Research 2004; 1: 249-54
  84. Wiebusch H., Poirier J., Sevigny P. et al. Further evidence for a synergistic association between APOE epsilon4 and BCHE-K in confirmed Alzheimer's disease. Hum. Genet. 1999; 104(2): 158-63.
  85. Lehmann D.J., Johnston C., Smith A.D. Synergy between the genes for butyrylcholinesterase K variant and apolipoprotein E4 in late-onset confirmed Alzheimer's disease. Hum. Mol. Genet. 1997; 6(11): 1933-6.
  86. Berson A., Soreq H. It all starts at the ends: multifaceted involvement of C- and N-terminally modified cholinesterases in Alzheimer's disease. Rambam. Maimonides Med. J. 2010; 1(2): e0014.
  87. Berson A., Knobloch M., Hanan M. et al. Changes in readthrough acetylcholinesterase expression modulate amyloid-beta pathology. Brain. 2008; 131: 109-19.

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