Heterogeneity of neuromuscular junctions in striated muscle of human esophagus demonstrated by triple staining for the vesicular acetylcholine transporter, α-bungarotoxin, and acetylcholinesterase

Cell and Tissue Research

Volumn 324, Issue 2, 2006, Pages 181-188

  Kallmünzer, Bernd ^a   Sörensen, Björn ^a   Neuhuber, Winfried L ^a   Wörl, Jürgen ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Neurotoxin; Binding site; Esophagus; Human; Motor endplate; Nicotinic acetylcholine receptor; Synaptic vesicle

Indexed keywords

ACETYLCHOLINE; ACETYLCHOLINESTERASE; ALPHA BUNGAROTOXIN; NICOTINIC RECEPTOR; VESICULAR ACETYLCHOLINE TRANSPORTER;

AGED; ARTICLE; CADAVER; ESOPHAGUS; FEMALE; HISTOCHEMISTRY; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; NERVE ENDING; NEUROMUSCULAR SYNAPSE; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RELIABILITY; SENSITIVITY ANALYSIS; SKELETAL MUSCLE; STAINING; TRANSPORT KINETICS;

ACETYLCHOLINESTERASE; AGED; BUNGAROTOXINS; ESOPHAGUS; FEMALE; HISTOCYTOCHEMISTRY; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; MOTOR ENDPLATE; MUSCLE, SKELETAL; NEUROMUSCULAR JUNCTION; RECEPTORS, NICOTINIC; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

EID: 33645799724     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-005-0154-4     Document Type: Article

References (43)

1. Aldunate R, Casar JC, Brandan E, Inestrosa NC (2004) Structural and functional organization of synaptic acetylcholinesterase. Brain Res Brain Res Rev 47:96-104
2. Arias HR (2000) Localization of agonist and competitive antagonist binding sites on nicotinic acetylcholine receptors. Neurochem Int 36:595-645
3. Arvidsson U, Riedl M, Elde R, Meister B (1997) Vesicular acetylcholine transporter (VAChT) protein: a novel and unique marker for cholinergic neurons in the central and peripheral nervous systems. J Comp Neurol 378:454-467
4. Assadi M, Müntener M (2005) Utrophin is lacking at the neuromuscular junctions in the extraocular muscles of normal cat: artefact or true? Histochem Cell Biol 123:189-194
5. Barchan D, Kachalsky S, Neumann D, Vogel Z, Ovadia M, Kochva E, Fuchs S (1992) How the mongoose can fight the snake: the binding site of the mongoose acetylcholine receptor. Proc Natl Acad Sci USA 89:7717-7721
6. Barchan D, Ovadia M, Kochva E, Fuchs S (1995) The binding site of the nicotinic acetylcholine receptor in animal species resistant to alpha-bungarotoxin. Biochemistry 34:9172-9176
7. Bravo D, Parsons SM (2002) Microscopic kinetics and structure-function analysis in the vesicular acetylcholine transporter. Neurochem Int 41:285-289
8. Breuer C, Neuhuber WL, Wörl J (2004) Development of neuromuscular junctions in the mouse esophagus: morphology suggests a role for enteric co-innervation during maturation of vagal myoneural contacts. J Comp Neurol 475:47-69
9. Chang CC, Lee CY (1963) Isolation of neurotoxins from the venom of Bungarus multicinctus and their modes of neuromuscular blocking action. Arch Int Pharmacodyn Ther 144:241-257
10. Gasnier B (2000) The loading of neurotransmitters into synaptic vesicles. Biochimie 82:327-337
11. Griesmann GE, McCormick DJ, De Aizpurua HJ, Lennon VA (1990) Alpha-bungarotoxin binds to human acetylcholine receptor alpha-subunit peptide 185-199 in solution and solid phase but not to peptides 125-147 and 389-409. J Neurochem 54:1541-1547
12. Gruber H, Zenker W (1978) Acetylcholinesterase activity in motor nerve fibres in correlation to muscle fibre types in rat. Brain Res 141:325-334
13. Ishikawa Y, Kano M, Tamiya N, Shimada Y (1985) Acetylcholine receptors of human skeletal muscle: a species difference detected by snake neurotoxins. Brain Res 346:82-88
14. Kachalsky SG, Jensen BS, Barchan D, Fuchs S (1995) Two subsites in the binding domain of the acetylcholine receptor: an aromatic subsite and a proline subsite. Proc Natl Acad Sci USA 92:10801-10805
15. Karlin A (2002) Emerging structure of the nicotinic acetylcholine receptors. Nat Rev Neurosci 3:102-114
16. Karnovsky MJ, Roots L (1964) A "direct-coloring" thiocholine method for cholinesterases. J Histochem Cytochem 12:219-221
17. Kreienkamp HJ, Sine SM, Maeda RK, Taylor P (1994) Glycosylation sites selectively interfere with alpha-toxin binding to the nicotinic acetylcholine receptor. J Biol Chem 269:8108-8114
18. Le Novère N, Corringer P-J, Changeux J-P (2002) The diversity of subunit composition in nAChRs: evolutionary origins, physiologic and pharmacologic consequences. J Neurobiol 53:447-456
19. Legay C (2000) Why so many forms of acetylcholinesterase? Microsc Res Tech 49:56-72
20. Lindstrom JM (2003) Nicotinic acetylcholine receptors of muscles and nerves: comparison of their structures, functional roles, and vulnerability to pathology. Ann NY Acad Sci 998:41-52
21. Lips KS, Pfeil U, Haberberger RV, Kummer W (2002) Localisation of the high-affinity choline transporter-1 in the rat skeletal motor unit. Cell Tissue Res 307:275-280
22. Marshall IG, Parsons SM (1987) The vesicular acetylcholine transport system. Trends Neurosci 10:174-177
23. Neuhuber WL, Eichhorn U, Wörl J (2001) Enteric co-innervation of striated muscle fibers in the esophagus: just a "hangover"? Anat Rec 262:41-46
24. Nguyen ML, Parsons SM (1995) Effects of internal pH on the acetylcholine transporter of synaptic vesicles. J Neurochem 64:1137-1142
25. Nguyen ML, Parsons SM (1996) Interactions of protons with the acetylcholine transporter of synaptic vesicles. Prog Brain Res 109:97-103
26. Nirthanan S, Gwee MCE (2004) Three-finger alpha-neurotoxins and the nicotinic acetylcholine receptor, forty years on. J Pharmacol Sci 94:1-17
27. Prado MAM, Reis RAM, Prado VF, Mello MC de, Gomez MV, Mello FG de (2002) Regulation of acetylcholine synthesis and storage. Neurochem Int 41:291-299
28. Prior C, Marshall IG, Parsons SM (1992) The pharmacology of vesamicol: an inhibitor of the vesicular acetylcholine transporter. Gen Pharmacol 23:1017-1022
29. Ravdin P, Axelrod D (1977) Fluorescent tetramethyl rhodamine derivatives of alpha-bungarotoxin: preparation, separation, and characterization. Anal Biochem 80:585-592
30. Roghani A, Carroll PT (2002) Analysis of uptake and release of newly synthesized acetylcholine in PC12 cells overexpressing the rat vesicular acetylcholine transporter (VAChT). Brain Res Mol Brain Res 100:21-30
31. Rotundo RL (2003) Expression and localization of acetylcholinesterase at the neuromuscular junction. J Neurocytol 32:743-766
32. Sang Q, Young HM (1997) Development of nicotinic receptor clusters and innervation accompanying the change in muscle phenotype in the mouse esophagus. J Comp Neurol 386:119-136
33. Sang Q, Ciampoli D, Greferath U, Sommer L, Young HM (1999) Innervation of the esophagus in mice that lack Mash-1. J Comp Neurol 408:1-10
34. Schäfer MK-H, Weihe E, Erickson JD, Eiden LE (1995) Human and monkey cholinergic neurons visualized in paraffin-embedded tissues by immunoreactivity for VAChT, the vesicular acetylcholine transporter. J Mol Neurosci 6:225-235
35. Schäfer MK, Eiden LE, Weihe E (1998) Cholinergic neurons and terminal fields revealed by immunohistochemistry for the vesicular acetylcholine transporter. I. Central nervous system. Neuroscience 84:331-359
36. Searl T, Prior C, Marshall IG (1991) Acetylcholine recycling and release at rat motor nerve terminals studied using (-)-vesamicol and troxpyrrolium. J Physiol (Lond) 444:99-116
37. Song HJ, Ming GL, Fon E, Bellocchio E, Edwards RH, Poo MM (1997) Expression of a putative vesicular acetylcholine transporter facilitates quantal transmitter packaging. Neuron 18:815-826
38. Usdin TB, Eiden LE, Bonner TI, Erickson JD (1995) Molecular biology of the vesicular ACh transporter. Trends Neurosci 18:218-224
39. Van der Kloot W (2003) Loading and recycling of synaptic vesicles in the Torpedo electric organ and the vertebrate neuromuscular junction. Prog Neurobiol 71:269-303
40. Weihe E, Tao-Cheng JH, Schäfer MK, Erickson JD, Eiden LE (1996) Visualization of the vesicular acetylcholine transporter in cholinergic nerve terminals and its targeting to a specific population of small synaptic vesicles. Proc Natl Acad Sci USA 93:3547-3552
41. Wörl J, Neuhuber WL (2005) Enteric co-innervation of motor endplates in the esophagus: state of the art ten years after. Histochem Cell Biol 123:117-130
42. Wörl J, Dütsch F, Neuhuber WL (2002) Development of neuromuscular junctions in the mouse esophagus: focus on establishment and reduction of enteric co-innervation. Anat Embryol 205:141-152
43. Wu M, Majewski M, Wojtkiewicz J, Vanderwinden JM, Adriaensen D, Timmermans JP (2003) Anatomical and neurochemical features of the extrinsic and intrinsic innervation of the striated muscle in the porcine esophagus: evidence for regional and species differences. Cell Tissue Res 311:289-297