Distinct localization of collagen Q and PRiMA forms of acetylcholinesterase at the neuromuscular junction

Molecular and Cellular Neuroscience

Volumn 46, Issue 1, 2011, Pages 272-281

  Bernard, Véronique ^a,b   Girard, Emmanuelle ^a,b   Hrabovska, Anna ^a,b   Camp, Shelley ^c   Taylor, Palmer ^c   Plaud, Benoit ^b,d   Krejci, Eric ^a,b  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b CNRS   (France)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITÉ PARIS EST CRÉTEIL   (France)

Author keywords

Acetylcholine; Acetylcholinesterase; Collagen Q; Electron microscopy; Muscle activity; PRiMA; Synapse structure

Indexed keywords

ACETYLCHOLINESTERASE; COLLAGEN; COLLAGEN Q; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CELL MEMBRANE; MOTONEURON; MOUSE; MUSCLE CELL; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION;

ACETYLCHOLINE; ACETYLCHOLINESTERASE; ANIMALS; BUNGAROTOXINS; COLLAGEN; IMMUNOHISTOCHEMISTRY; ISOENZYMES; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; SYNAPSES;

EID: 78650887862     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2010.09.010     Document Type: Article

References (48)

1. Anglister L. Acetylcholinesterase from the motor nerve terminal accumulates on the synaptic basal lamina of the myofiber. J. Cell Biol. 1991, 115:755-764.
2. Anglister L., Eichler J., Szabo M., Haesaert B., Salpeter M.M. 125I-labeled fasciculin 2: a new tool for quantitation of acetylcholinesterase densities at synaptic sites by EM-autoradiography. J. Neurosci. Methods 1998, 81:63-71.
3. Bernard V., Levey A.I., Bloch B. Regulation of the subcellular distribution of m4 muscarinic acetylcholine receptors in striatal neurons in vivo by the cholinergic environment: evidence for regulation of cell surface receptors by endogenous and exogenous stimulation. J. Neurosci. 1999, 19:10237-10249.
4. Bon S., Coussen F., Massoulié J. Quaternary associations of acetylcholinesterase. II. The polyproline attachment domain of the collagen tail. J. Biol. Chem. 1997, 272:3016-3021.
5. Boudreau-Larivière C., Gisiger V., Michel R.N., Hubatsch D.A., Jasmin B.J. Fast and slow skeletal muscles express a common basic profile of acetylcholinesterase molecular forms. Am. J. Physiol. 1997, 272:C68-C76.
6. Camp S., De Jaco A., Zhang L., Marquez M., De la Torre B., Taylor P. Acetylcholinesterase expression in muscle is specifically controlled by a promoter-selective enhanceosome in the first intron. J. Neurosci. 2008, 28:2459-2470.
7. Cartaud A., Strochlic L., Guerra M., Blanchard B.t., Lambergeon M., Krejci E., Cartaud J., Legay C. MuSK is required for anchoring acetylcholinesterase at the neuromuscular junction. J. Cell Biol. 2004, 165:505-515.
8. Couteaux R., Taxi J. Recherches histochimiques sur la distribution des activités cholinestérasiques au niveau de la synapse myoneurale. Arch. Anat. Microsc. Morphol. Exp. 1952, 352-392.
9. Deprez P., Inestrosa N.C., Krejci E. Two different heparin-binding domains in the triple-helical domain of ColQ, the collagen tail subunit of synaptic acetylcholinesterase. J. Biol. Chem. 2003, 278:23233-23242.
10. Di Giamberardino L., Couraud J.Y. Rapid accumulation of high molecular weight acetylcholinesterase in transected sciatic nerve. Nature 1978, 271:170-172.
11. Dobbertin A., Hrabovska A., Dembele K., Camp S., Taylor P., Krejci E., Bernard V.r. Targeting of acetylcholinesterase in neurons in vivo: a dual processing function for the proline-rich membrane anchor subunit and the attachment domain on the catalytic subunit. J. Neurosci. 2009, 4519-4530.
12. Donger C., Krejci E., Serradell A.P., Eymard B., Bon S., Nicole S., Chateau D., Gary F., Fardeau M., Massoulié J., Guicheney P. Mutation in the human acetylcholinesterase-associated collagen gene, COLQ, is responsible for congenital myasthenic syndrome with end-plate acetylcholinesterase deficiency (Type Ic). Am. J. Hum. Genet. 1998, 63:967-975.
13. Dvir H., Harel M., Bon S., Liu W.-Q., Vidal M., Garbay C., Sussman J.L., Massoulié J., Silman I. The synaptic acetylcholinesterase tetramer assembles around a polyproline II helix. EMBO J. 2004, 23:4394-4405.
14. Feng G., Krejci E., Molgo J., Cunningham J.M., Massoulié J., Sanes J.R. Genetic analysis of collagen Q: roles in acetylcholinesterase and butyrylcholinesterase assembly and in synaptic structure and function. J. Cell Biol. 1999, 144:1349-1360.
15. Ferguson S.M., Savchenko V., Apparsundaram S., Zwick M., Wright J., Heilman C.J., Yi H., Levey A.I., Blakely R.D. Vesicular localization and activity-dependent trafficking of presynaptic choline transporters. J. Neurosci. 2003, 23:9697-9709.
16. Fernandez H.L., Duell M.J., Festoff B.W. Bidirectional axonal transport of 16S acetylcholinesterase in rat sciatic nerve. J. Neurobiol. 1980, 11:31-39.
17. Ferry C.B., Kelly S.S. The nature of the presynaptic effects of d-tubocurarine at the mouse neuromuscular junction. J. Physiol. 1988, 403:425-437.
18. Gisiger V., Stephens H.R. Localization of the pool of G4 acetylcholinesterase characterizing fast muscles and its alteration in murine muscular dystrophy. J. Neurosci. Res. 1988, 19:62-78.
19. Gisiger V., Bélisle M., Gardiner P.F. Acetylcholinesterase adaptation to voluntary wheel running is proportional to the volume of activity in fast, but not slow, rat hindlimb muscles. Eur. J. Neurosci. 1994, 6:673-680.
20. Jasmin B.J., Gisiger V. Regulation by exercise of the pool of G4 acetylcholinesterase characterizing fast muscles: opposite effect of running training in antagonist muscles. J. Neurosci. 1990, 10:1444-1454.
21. Jennings L.L., Malecki M., Komives E.A., Taylor P. Direct analysis of the kinetic profiles of organophosphate-acetylcholinesterase adducts by MALDI-TOF mass spectrometry. Biochemistry 2003, 42:11083-11091.
22. Jevsek M., Mars T., Mis K., Grubic Z. Origin of acetylcholinesterase in the neuromuscular junction formed in the in vitro innervated human muscle. Eur. J. Neurosci. 2004, 20:2865-2871.
23. Kasprzak H., Salpeter M.M. Recovery of acetylcholinesterase at intact neuromuscular junctions after in vivo inactivation with di-isopropylfluorophosphate. J. Neurosci. 1985, 5:951-955.
24. Katz B., Miledi R. The binding of acetylcholine to receptors and its removal from the synaptic cleft. J. Physiol. 1973, 231:549-574.
25. Katz B., Miledi R. Transmitter leakage from motor nerve endings. Proc. R. Soc. Lond. B Biol. Sci. 1977, 196:59-72.
26. Krejci E., Thomine S., Boschetti N., Legay C., Sketelj J., Massoulié J. The mammalian gene of acetylcholinesterase-associated collagen. J. Biol. Chem. 1997, 272:22840-22847.
27. Krejci E., Martinez-Pena y Valenzuela I., Ameziane R., Akaaboune M. Acetylcholinesterase dynamics at the neuromuscular junction of live animals. J. Biol. Chem. 2006, 281:10347-10354.
28. Leung K.W., Xie H.Q., Chen V.P., Mok M.K.W., Chu G.K.Y., Choi R.C.Y., Tsim K.W.K. Restricted localization of proline-rich membrane anchor (PRiMA) of globular form acetylcholinesterase at the neuromuscular junctions-contribution and expression from motor neurons. FEBS J. 2009, 276:3031-3042.
29. Lomo T., Massoulié J., Vigny M. Stimulation of denervated rat soleus muscle with fast and slow activity patterns induces different expression of acetylcholinesterase molecular forms. J. Neurosci. 1985, 5:1180-1187.
30. Magleby K.L., Terrar D.A. Factors affecting the time course of decay of end-plate currents: a possible cooperative action of acetylcholine on receptors at the frog neuromuscular junction. J. Physiol. 1975, 244:467-495.
31. Marsh D., Grassi J., Vigny M., Massoulié J. An immunological study of rat acetylcholinesterase: comparison with acetylcholinesterases from other vertebrates. J. Neurochem. 1984, 43:204-213.
32. Martinez-Pena y Valenzuela I., Akaaboune M. Acetylcholinesterase mobility and stability at the neuromuscular junction of living mice. Mol. Biol. Cell 2007, 18:2904-2911.
33. Massoulié J., Millard C.B. Cholinesterases and the basal lamina at vertebrate neuromuscular junctions. Curr. Opin. Pharmacol. 2009, 9:316-325.
34. McMahan U.J., Sanes J.R., Marshall L.M. Cholinesterase is associated with the basal lamina at the neuromuscular junction. Nature 1978, 271:172-174.
35. Ohno K., Brengman J., Tsujino A., Engel A.G. Human endplate acetylcholinesterase deficiency caused by mutations in the collagen-like tail subunit (ColQ) of the asymmetric enzyme. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:9654-9659.
36. Perrier A.L., Massoulié J., Krejci E. PRiMA: the membrane anchor of acetylcholinesterase in the brain. Neuron 2002, 33:275-285.
37. Rogers A.W., Darzynkiewicz Z., Salpeter M.M., Ostrowski K., Barnard E.A. Quantitative studies on enzymes in structures in striated muscles by labeled inhibitor methods. I. The number of acetylcholinesterase molecules and of other DFP-reactive sites at motor endplates, measured by radioautography. J. Cell Biol. 1969, 41:665-685.
38. Salpeter M.M. Electron microscope radioautography as a quantitative tool in enzyme cytochemistry. II. The distribution of DFP-reactive sties at motor endplates of a vertebrate twitch muscle. J. Cell Biol. 1969, 42:122-134.
39. Schatz C.R., Veh R.W. High-resolution localization of acetylcholinesterase at the rat neuromuscular junction. J. Histochem. Cytochem. 1987, 35:1299-1307.
40. Tago H., Kimura H., Maeda T. Visualization of detailed acetylcholinesterase fiber and neuron staining in rat brain by a sensitive histochemical procedure. J. Histochem. Cytochem. 1986, 34:1431-1438.
41. Tsim K., Leung K., Mok K., Chen V., Zhu K., Zhu J., Guo A., Bi C., Zheng K., Lau D., Xie H., Choi R. Expression and localization of PRiMA-linked globular form acetylcholinesterase in vertebrate neuromuscular junctions. J. Mol. Neurosci. 2010, 40:40-46.
42. Vallette F.M., De la Porte S., Koenig J., Massoulié J., Vigny M. Acetylcholinesterase in cocultures of rat myotubes and spinal cord neurons: effects of collagenase and cis-hydroxyproline on molecular forms, intra- and extracellular distribution, and formation of patches at neuromuscular contacts. J. Neurochem. 1990, 54:915-923.
43. Vyskocil F., Illés P. Non-quantal release of transmitter at mouse neuromuscular junction and its dependence on the activity of Na+-K+ ATP-ase. Pflugers Arch. 1977, 370:295-297.
44. Vyskocil F., Malomouzh A.I., Nikolsky E.E. Non-quantal acetylcholine release at the neuromuscular junction. Physiol. Res. 2009, 58:763-784.
45. Xie W., Stribley J.A., Chatonnet A., Wilder P.J., Rizzino A., McComb R.D., Taylor P., Hinrichs S.H., Lockridge O. Postnatal developmental delay and supersensitivity to organophosphate in gene-targeted mice lacking acetylcholinesterase. J. Pharmacol. Exp. Ther. 2000, 293:896-902.
46. Xie H.Q., Leung K.W., Chen V.P., Lau F.T.C., Liu L.S., Choi R.C.Y., Tsim K.W.K. The promoter activity of proline-rich membrane anchor (PRiMA) of globular form acetylcholinesterase in muscle: suppressive roles of myogenesis and innervating nerve. Chem. Biol. Interact 2008, 175:79-82.
47. Younkin S.G., Rosenstein C., Collins P.L., Rosenberry T.L. Cellular localization of the molecular forms of acetylcholinesterase in rat diaphragm. J. Biol. Chem. 1982, 257:13630-13637.
48. Zemkova H., Vyskocil F., Edwards C. The effects of nerve terminal activity on non-quantal release of acetylcholine at the mouse neuromuscular junction. J. Physiol. 1990, 423:631-640.