Acetylcholinesterase deficiency contributes to neuromuscular junction dysfunction in type 1 diabetic neuropathy

American Journal of Physiology - Endocrinology and Metabolism

Volumn 303, Issue 4, 2012, Pages

  Garcia, Carmen C ^a   Potian, Joseph G ^a   Hognason, Kormakur ^a   Thyagarajan, Baskaran ^a   Sultatos, Lester G ^a   Souayah, Nizar ^a   Routh, Vanessa H ^a   McArdle, Joseph J ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Butyrylcholinesterase; Streptozotocin; Type 1 diabetes

Indexed keywords

ACETYLCHOLINESTERASE; CHOLINERGIC RECEPTOR; CHOLINESTERASE; CHOLINESTERASE INHIBITOR; STREPTOZOCIN;

ACETYLCHOLINESTERASE DEFICIENCY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC NEUROPATHY; DISEASE SEVERITY; ENZYME DEFICIENCY; EVOKED MUSCLE RESPONSE; EXTENSOR DIGITORUM LONGUS MUSCLE; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MINIATURE ENDPLATE POTENTIAL; MOUSE; MUSCLE TONE; MUSCLE TWITCH; MUSCLE WEAKNESS; NERVE STIMULATION; NEUROMUSCULAR JUNCTION DISORDER; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STREPTOZOCIN DIABETES; SWISS WEBSTER MOUSE;

ACETYLCHOLINESTERASE; ANIMALS; BUTYRYLCHOLINESTERASE; CHOLINESTERASE INHIBITORS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETIC NEUROPATHIES; GPI-LINKED PROTEINS; HYPERGLYCEMIA; MALE; MICE; MOTOR ENDPLATE; MUSCLE WEAKNESS; NEUROMUSCULAR JUNCTION DISEASES; PHYSOSTIGMINE;

EID: 84865134806     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00622.2011     Document Type: Article

References (76)

1. Abbott CA, Mackness MI, Kumar S, Olukoga AO, Gordon C, Arrol S, Bhatnagar D, Boulton AJ, Durrington PN. Relationship between serum butyrylcholinesterase activity, hypertriglyceridaemia and insulin sensitivity in diabetes mellitus. Clin Sci (Lond) 85: 77-81, 1993.
2. Adler M, Filbert MG. Role of butyrylcholinesterase in canine tracheal smooth muscle function. FEBS Lett 267: 107-110, 1990.
3. Adler M, Manley HA, Purcell AL, Deshpande SS, Hamilton TA, Kan RK, Oyler G, Lockridge O, Duysen EG, Sheridan RE. Reduced acetylcholine receptor density, morphological remodeling, and butyrylcholinesterase activity can sustain muscle function in acetylcholinesterase knockout mice. Muscle Nerve 30: 317-327, 2004.
4. Andersen H. Motor function in diabetic neuropathy. Acta Neurol Scand 100: 211-220, 1999.
5. Arendt T, Bruckner MK, Lange M, Bigl V. Changes in acetylcholinesterase and butyrylcholinesterase in Alzheimer's disease resemble embryonic development-a study of molecular forms. Neurochem Int 21: 381-396, 1992.
6. Argentieri TM, Aiken SP, Laxminarayan S, McArdle JJ. Characteristics of synaptic transmission in reinnervating rat skeletal muscle. Pflugers Arch 421: 256-261, 1992.
7. Ashokkumar N, Pari L, Ramkumar KM. N-Benzoyl-D-phenylalanine attenuates brain acetylcholinesterase in neonatal streptozotocin-diabetic rats. Basic Clin Pharmacol Toxicol 99: 246-250, 2006.
8. Biessels GJ, Deary IJ, Ryan CM. Cognition and diabetes: a lifespan perspective. Lancet Neurol 7: 184-190, 2008.
9. Buonanno A, Mudd J, Merlie JP. Isolation and characterization of the beta and epsilon subunit genes of mouse muscle acetylcholine receptor. J Biol Chem 264: 7611-7616, 1989.
10. Calcutt NA, Cooper ME, Kern TS, Schmidt AM. Therapies for hyperglycaemia-induced diabetic complications: from animal models to clinical trials. Nat Rev Drug Discov 8: 417-429, 2009.
11. Chevessier F, Peter C, Mersdorf U, Girard E, Krejci E, McArdle JJ, Witzemann V. A new mouse model for the slow-channel congenital myasthenic syndrome induced by the AChR epsilonL221F mutation. Neurobiol Dis 45: 851-861, 2012.
12. Constantini S, Schiller Y, Cohen AM, Rahamimoff R. Pathophysiology of the neuromuscular junction in diabetic rats. Isr J Med Sci 23: 101-106, 1987.
13. Cresnar B, Crne-Finderle N, Breskvar K, Sketelj J. Neural regulation of muscle acetylcholinesterase is exerted on the level of its mRNA. J Neurosci Res 38: 294-299, 1994.
14. Dash NK, Azam M, Gupta G, Baquer NZ. Effect of hyperglycemia on acetylcholinesterase and catecholamine levels in rat brain and heart. Biochem Int 23: 261-269, 1991.
15. Dave KR, Katyare SS. Effect of alloxan-induced diabetes on serum and cardiac butyrylcholinesterases in the rat. J Endocrinol 175: 241-250, 2002.
16. Duysen EG, Li B, Xie W, Schopfer LM, Anderson RS, Broomfield CA, Lockridge O. Evidence for nonacetylcholinesterase targets of organophosphorus nerve agent: supersensitivity of acetylcholinesterase knockout mouse to VX lethality. J Pharmacol Exp Ther 299: 528-535, 2001.
17. Fahim MA, el-Sabban F, Davidson N. Muscle contractility decrement and correlated morphology during the pathogenesis of streptozotocindiabetic mice. Anat Rec 251: 240-244, 1998.
18. Fahim MA, Hasan MY, Alshuaib WB. Cadmium modulates diabetesinduced alterations in murine neuromuscular junction. Endocr Res 26: 205-217, 2000.
19. Fahim MA, Hasan MY, Alshuaib WB. Early morphological remodeling of neuromuscular junction in a murine model of diabetes. J Appl Physiol 89: 2235-2240, 2000.
20. Fischbach GD, Schuetze SM. A post-natal decrease in acetylcholine channel open time at rat end-plates. J Physiol 303: 125-137, 1980.
21. Gattenlohner S, Schneider C, Thamer C, Klein R, Roggendorf W, Gohlke F, Niethammer C, Czub S, Vincent A, Muller-Hermelink HK, Marx A. Expression of foetal type acetylcholine receptor is restricted to type 1 muscle fibres in human neuromuscular disorders. Brain 125: 1309-1319, 2002.
22. Gautron J. Ultrastructural localization of acetylcholinesterase. A direct method for light and electron microscopy. Histochemistry 76: 469-478, 1982.
23. Ghareeb DA, Hussen HM. Vanadium improves brain acetylcholinesterase activity on early stage alloxan-diabetic rats. Neurosci Lett 436: 44-47, 2008.
24. Girard E, Bernard V, Minic J, Chatonnet A, Krejci E, Molgo J. Butyrylcholinesterase and the control of synaptic responses in acetylcholinesterase knockout mice. Life Sci 80: 2380-2385, 2007.
25. Glisovic S, Trinkaus M, Pregelj P, Sketelj J. The asymmetric molecular forms of AChE and the expression of collagen Q in mature and immature fast and slow rat muscles. Chem Biol Interact 187: 90-95, 2010.
26. Gomez CM, Maselli RA, Groshong J, Zayas R, Wollmann RL, Cens T, Charnet P. Active calcium accumulation underlies severe weakness in a panel of mice with slow-channel syndrome. J Neurosci 22: 6447-6457, 2002.
27. Greig NH, Utsuki T, Ingram DK, Wang Y, Pepeu G, Scali C, Yu QS, Mamczarz J, Holloway HW, Giordano T, Chen D, Furukawa K, Sambamurti K, Brossi A, Lahiri DK. Selective butyrylcholinesterase inhibition elevates brain acetylcholine, augments learning and lowers Alzheimer beta-amyloid peptide in rodent. Proc Natl Acad Sci USA 102: 17213-17218, 2005.
28. Homs J, Ariza L, Pagès G, Verdú E, Casals L, Udina E, Chillón M, Bosch A, Navarro X. Comparative study of peripheral neuropathy and nerve regeneration in NOD and ICR diabetic mice. J Peripher Nerv Syst 16: 213-227, 2011.
29. Jayawardane P, Senanayake N, Dawson A. Electrophysiological correlates of intermediate syndrome following acute organophosphate poisoning. Clin Toxicol (Phila) 47: 193-205, 2009.
30. John M, Oommen A, Zachariah A. Muscle injury in organophosphorous poisoning and its role in the development of intermediate syndrome. Neurotoxicology 24: 43-53, 2003.
31. Kerschensteiner M, Reuter MS, Lichtman JW, Misgeld T. Ex vivo imaging of motor axon dynamics in murine triangularis sterni explants. Nat Protoc 3: 1645-1653, 2008.
32. Kiauta T, Brzin M, Dettbarn WD. Synthesis of neuromuscular cholinesterases in innervated and denervated rat diaphragm. Exp Neurol 56: 281-288, 1977.
33. Kimura I, Okazaki M, Kimura M. Streptozocin-diabetes modifies acetylcholine release from mouse phrenic nerve terminal and presynaptic sensitivity to succinylcholine. Jpn J Pharmacol 62: 35-41, 1993.
34. Kiss G, Somogyi J, Csermely P, Szelenyi J, Ver A. Streptozotocininduced diabetes alters the oligomerization pattern of acetylcholinesterase in rat skeletal muscle. Diabetologia 44: 220-223, 2001.
35. Koelle GB, Horn RS. Acetyl disulfide, (CH3COS)2, a major active component in the thiolacetic acid histochemical method for acetylcholinesterase. J Histochem Cytochem 16: 743-753, 1968.
36. Kong L, Wang X, Choe DW, Polley M, Burnett BG, Bosch-Marcé M, Griffin JW, Rich MM, Sumner CJ. Impaired synaptic vesicle release and immaturity of neuromuscular junctions in spinal muscular atrophy mice. J Neurosci 29: 842-851, 2009.
37. Krejci E, Legay C, Thomine S, Sketelj J, Massoulie J. Differences in expression of acetylcholinesterase and collagen Q control the distribution and oligomerization of the collagen-tailed forms in fast and slow muscles. J Neurosci 19: 10672-10679, 1999.
38. Krejci E, Thomine S, Boschetti N, Legay C, Sketelj J, Massoulie J. The mammalian gene of acetylcholinesterase-associated collagen. J Biol Chem 272: 22840-22847, 1997.
39. Kuhad A, Chopra K. Curcumin attenuates diabetic encephalopathy in rats: behavioral and biochemical evidences. Eur J Pharmacol 576: 34-42, 2007.
40. Lakhman SS, Kaur G. Effect of alloxan-induced diabetes on acetylcholinesterase activity from discrete areas of rat brain. Neurochem Int 24: 159-163, 1994.
41. Li B, Stribley JA, Ticu A, Xie W, Schopfer LM, Hammond P, Brimijoin S, Hinrichs SH, Lockridge O. Abundant tissue butyrylcholinesterase and its possible function in the acetylcholinesterase knockout mouse. J Neurochem 75: 1320-1331, 2000.
42. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta Delta C(T)] Method. Methods 25: 402-408, 2001.
43. Marques MJ, Santo Neto H. Acetylcholine receptors and nerve terminal distribution at the neuromuscular junction of non-obese diabetic mice. Anat Rec 267: 112-119, 2002.
44. Massoulié J, Anselmet A, Bon S, Krejci E, Legay C, Morel N, Simon S. Acetylcholinesterase: C-terminal domains, molecular forms and functional localization. J Physiol Paris 92: 183-190, 1998.
45. McArdle JJ, Angaut-Petit D, Mallart A, Bournaud R, Faille L, Brigant JL. Advantages of the triangularis sterni muscle of the mouse for investigations of synaptic phenomena. J Neurosci Methods 4: 109-115, 1981.
46. McArdle JJ, Lentz TL, Witzemann V, Schwarz H, Weinstein SA, Schmidt JJ. Waglerin-1 selectively blocks the epsilon form of the muscle nicotinic acetylcholine receptor. J Pharmacol Exp Ther 289: 543-550, 1999.
47. McArdle JJ, Sellin LC, Coakley KM, Potian JG, Quinones-Lopez MC, Rosenfeld CA, Sultatos LG, Hognason K. Mefloquine inhibits cholinesterases at the mouse neuromuscular junction. Neuropharmacology 49: 1132-1139, 2005.
48. McComas AJ, Fawcett PR, Campbell MJ, Sica RE. Electrophysiological estimation of the number of motor units within a human muscle. J Neurol Neurosurg Psychiatry 34: 121-131, 1971.
49. Miglietta O. Neuromuscular junction defect in diabetes. Diabetes 22: 719-723, 1973.
50. Minic J, Chatonnet A, Krejci E, Molgo J. Butyrylcholinesterase and acetylcholinesterase activity and quantal transmitter release at normal and acetylcholinesterase knockout mouse neuromuscular junctions. Br J Pharmacol 138: 177-187, 2003.
51. Mishina M, Takai T, Imoto K, Noda M, Takahashi T, Numa S, Methfessel C, Sakmann B. Molecular distinction between fetal and adult forms of muscle acetylcholine receptor. Nature 321: 406-411, 1986.
52. Nishi M, Komazaki S, Kurebayashi N, Ogawa Y, Noda T, Iino M, Takeshima H. Abnormal features in skeletal muscle from mice lacking mitsugumin29. J Cell Biol 147: 1473-1480, 1999.
53. Ohno K, Brengman J, Tsujino A, Engel AG. Human endplate acetylcholinesterase deficiency caused by mutations in the collagen-like tail subunit (ColQ) of the asymmetric enzyme. Proc Natl Acad Sci USA 95: 9654-9659, 1998.
54. Primo-Parmo SL, Bartels CF, Wiersema B, van der Spek AF, Innis JW, La Du BN. Characterization of 12 silent alleles of the human butyrylcholinesterase (BCHE) gene. Am J Hum Genet 58: 52-64, 1996.
55. Ramkumar KM, Latha M, Ashokkumar N, Pari L, Ananthan R. Modulation of impaired cholinesterase activity in experimental diabetes: effect of Gymnema montanum leaf extract. J Basic Clin Physiol Pharmacol 16: 17-35, 2005.
56. Reske-Nielsen E, Gregersen G, Harmsen A, Lundbaek K. Morphological abnormalities of the terminal neuromuscular apparatus in recent juvenile diabetes. Diabetologia 6: 104-109, 1970.
57. Reske-Nielsen E, Lundbaek K, Gregersen G, Harmsen A. Pathological changes in the central and peripheral nervous system of young long-term diabetics. The terminal neuro-muscular apparatus. Diabetologia 6: 98-103, 1970.
58. Said G. Diabetic neuropathy-a review. Nat Clin Pract Neurol 3: 331-340, 2007.
59. Sakmann B, Brenner HR. Change in synaptic channel gating during neuromuscular development. Nature 276: 401-402, 1978.
60. Sánchez-Chávez G, Salceda R. Acetyl- and butyrylcholinesterase in normal and diabetic rat retina. Neurochem Res 26: 153-159, 2001.
61. Sánchez-Chávez G, Salceda R. Acetyl- and butyrylcholinesterase molecular forms in normal and streptozotocin-diabetic rat retinal pigment epithelium. Neurochem Int 39: 209-215, 2001.
62. Sánchez-Chávez G, Salceda R. Effect of streptozotocin-induced diabetes on activities of cholinesterases in the rat retina. IUBMB Life 49: 283-287, 2000.
63. Schiller Y, Rahamimoff R. Neuromuscular transmission in diabetes: response to high-frequency activation. J Neurosci 9: 3709-3719, 1989.
64. Schmatz R, Mazzanti CM, Spanevello R, Stefanello N, Gutierres J, Corrêa M, da Rosa MM, Rubin MA, Chitolina Schetinger MR, Morsch VM. Resveratrol prevents memory deficits and the increase in acetylcholinesterase activity in streptozotocin-induced diabetic rats. Eur J Pharmacol 610: 42-48, 2009.
65. Shefner JM. Motor unit number estimation in human neurological diseases and animal models. Clin Neurophysiol 112: 955-964, 2001.
66. Sketelj J, Crne-Finderle N, Strukelj B, Trontelj JV, Pette D. Acetylcholinesterase mRNA level and synaptic activity in rat muscles depend on nerve-induced pattern of muscle activation. J Neurosci 18: 1944-1952, 1998.
67. Souayah N, Potian JG, Garcia CC, Krivitskaya N, Boone C, Routh VH, McArdle JJ. Motor unit number estimate as a predictor of motor dysfunction in an animal model of type 1 diabetes. Am J Physiol Endocrinol Metab 297: E602-E608, 2009.
68. Stum M, Girard E, Bangratz M, Bernard V, Herbin M, Vignaud A, Ferry A, Davoine CS, Echaniz-Laguna A, Rene F, Marcel C, Molgo J, Fontaine B, Krejci E, Nicole S. Evidence of a dosage effect and a physiological endplate acetylcholinesterase deficiency in the first mouse models mimicking Schwartz-Jampel syndrome neuromyotonia. Hum Mol Genet 17: 3166-3179, 2008.
69. Suhail M, Rizvi SI. Regulation of red cell acetylcholinesterase activity in diabetes mellitus. Indian J Exp Biol 28: 234-236, 1990.
70. Sultatos LG, Kaushik R. Altered binding of thioflavin t to the peripheral anionic site of acetylcholinesterase after phosphorylation of the active site by chlorpyrifos oxon or dichlorvos. Toxicol Appl Pharmacol 230: 390-396, 2008.
71. Teichert RW, Garcia CC, Potian JG, Schmidt JJ, Witzemann V, Olivera BM, McArdle JJ. Peptide-toxin tools for probing the expression and function of fetal and adult subtypes of the nicotinic acetylcholine receptor. Ann NY Acad Sci 1132: 61-70, 2008.
72. Teichert RW, Rivier J, Torres J, Dykert J, Miller C, Olivera BM. A uniquely selective inhibitor of the mammalian fetal neuromuscular nicotinic acetylcholine receptor. J Neurosci 25: 732-736, 2005.
73. Wang X, Engisch KL, Teichert RW, Olivera BM, Pinter MJ, Rich MM. Prolongation of evoked and spontaneous synaptic currents at the neuromuscular junction after activity blockade is caused by the upregulation of fetal acetylcholine receptors. J Neurosci 26: 8983-8987, 2006.
74. Witzemann V, Barg B, Criado M, Stein E, Sakmann B. Developmental regulation of five subunit specific mRNAs encoding acetylcholine receptor subtypes in rat muscle. FEBS Lett 242: 419-424, 1989.
75. Witzemann V, Barg B, Nishikawa Y, Sakmann B, Numa S. Differential regulation of muscle acetylcholine receptor gamma- and epsilon-subunit mRNAs. FEBS Lett 223: 104-112, 1987.
76. Zarros A, Liapi C, Galanopoulou P, Marinou K, Mellios Z, Skandali N, Al-Humadi H, Anifantaki F, Gkrouzman E, Tsakiris S. Effects of adult-onset streptozotocin-induced diabetes on the rat brain antioxidant status and the activities of acetylcholinesterase, [Na(+),K (+)]- and Mg(2+)-ATPase: modulation by L-cysteine. Metab Brain Dis 24: 337-348, 2009.