Myosin Va cooperates with PKA RIα to mediate maintenance of the endplate in vivo

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 5, 2010, Pages 2031-2036

  Röder, Ira V ^a   Choi, Kyeong Rock ^a   Reischl, Markus ^a   Petersen, Yvonne ^a   Diefenbacher, Markus E ^a   Zaccolo, Manuela ^b   Pozzan, Tullio ^c,d   Rudolf, Rüdiger ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^d UNIVERSITY OF PADOVA   (Italy)

Author keywords

cAMP; Microdomain; Muscle; Neuromuscular junction; Synaptic plasticity

Indexed keywords

ACTIN; CALCITONIN GENE RELATED PEPTIDE; CHOLINERGIC RECEPTOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IIALPHA; MYOSIN VA;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; DENERVATION; IN VIVO STUDY; MOUSE; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM;

A KINASE ANCHOR PROTEINS; ACTINS; ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASE RIALPHA SUBUNIT; DENERVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MOLECULAR MOTOR PROTEINS; MOTOR ENDPLATE; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; NEURONAL PLASTICITY; RECEPTORS, CHOLINERGIC; SIGNAL TRANSDUCTION;

EID: 76649121881     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0914087107     Document Type: Article

References (46)

1. Lisé MF, et al. (2006) Involvement of myosin Vb in glutamate receptor trafficking. J Biol Chem 281:3669-3678.
2. Correia SS, et al. (2008) Motor protein-dependent transport of AMPA receptors into spines during long-term potentiation. Nat Neurosci 11:457-466.
3. Wang Z, et al. (2008) Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 135:535-548.
4. Röder IV, et al. (2008) Role of Myosin Va in the plasticity of the vertebrate neuromuscular junction in vivo. PLoS One 3:e3871.
5. Lichtman JW, Magrassi L, Purves D (1987) Visualization of neuromuscular junctions over periods of several months in living mice. J Neurosci 7:1215-1222.
6. Levitt TA, Salpeter MM (1981) Denervated endplates have a dual population of junctional acetylcholine receptors. Nature 291:239-241.
7. Akaaboune M, Culican SM, Turney SG, Lichtman JW (1999) Rapid and reversible effects of activity on acetylcholine receptor density at the neuromuscular junction in vivo. Science 286:503-507.
8. Bruneau E, Sutter D, Hume RI, Akaaboune M (2005) Identification of nicotinic acetylcholine receptor recycling and its role in maintaining receptor density at the neuromuscular junction in vivo. J Neurosci 25:9949-9959.
9. Bruneau EG, Akaaboune M (2006) The dynamics of recycled acetylcholine receptors at the neuromuscular junction in vivo. Development 133:4485-4493.
10. 2+ influx associated with muscle activity. Nature 349:337-339.
11. Rotzler S, Brenner HR (1990) Metabolic stabilization of acetylcholine receptors in vertebrate neuromuscular junction by muscle activity. J Cell Biol 111:655-661.
12. Shyng SL, Xu R, Salpeter MM (1991) Cyclic AMP stabilizes the degradation of original junctional acetylcholine receptors in denervated muscle. Neuron 6:469-475.
13. Andreose JS, Xu R, Lømo T, Salpeter MM, Fumagalli G (1993) Degradation of two AChR populations at rat neuromuscular junctions: regulation in vivo by electrical stimulation. J Neurosci 13:3433-3438.
14. Xu R, Salpeter MM (1997) Acetylcholine receptors in innervated muscles of dystrophic mdx mice degrade as after denervation. J Neurosci 17:8194-8200.
15. Marques MJ, Conchello JA, Lichtman JW (2000) From plaque to pretzel: fold formation and acetylcholine receptor loss at the developing neuromuscular junction. J Neurosci 20:3663-3675.
16. Labovitz SS, Robbins N, Fahim MA (1984) Endplate topography of denervated and disused rat neuromuscular junctions: comparison by scanning and light microscopy. Neuroscience 11:963-971.
17. Wilson MH, Deschenes MR (2005) The neuromuscular junction: anatomical features and adaptations to various forms of increased, or decreased neuromuscular activity. Int J Neurosci 115:803-828.
18. Li MX, Jia M, Jiang H, Dunlap V, Nelson PG (2001) Opposing actions of protein kinase A and C mediate Hebbian synaptic plasticity. Nat Neurosci 4:871-872.
19. Caroni P, Rotzler S, Britt JC, Brenner HR (1993) Calcium influx and protein phosphorylation mediate the metabolic stabilization of synaptic acetylcholine receptors in muscle. J Neurosci 13:1315-1325.
20. Fontaine B, Klarsfeld A, Changeux JP (1987) Calcitonin gene-related peptide and muscle activity regulate acetylcholine receptor alpha-subunit mRNA levels by distinct intracellular pathways. J Cell Biol 105:1337-1342.
21. Lanuza MA, et al. (2006) Phosphorylation of the nicotinic acetylcholine receptor in myotube-cholinergic neuron cocultures. J Neurosci Res 83:1407-1414.
22. Poyner DR (1992) Calcitonin gene-related peptide: multiple actions, multiple receptors. Pharmacol Ther 56 (1):23-51.
23. Miles K, Greengard P, Huganir RL (1989) Calcitonin gene-related peptide regulates phosphorylation of the nicotinic acetylcholine receptor in rat myotubes. Neuron 2:1517-1524.
24. New HV, Mudge AW (1986) Calcitonin gene-related peptide regulates muscle acetylcholine receptor synthesis. Nature 323:809-811.
25. Boudreau-Larivière C, Jasmin BJ (1999) Calcitonin gene-related peptide decreases expression of acetylcholinesterase in mammalian myotubes. FEBS Lett 444 (1):22-26.
26. Rossi SG, Dickerson IM, Rotundo RL (2003) Localization of the calcitonin gene-related peptide receptor complex at the vertebrate neuromuscular junction and its role in regulating acetylcholinesterase expression. J Biol Chem 278:24994-25000.
27. Lu B, Fu WM, Greengard P, Poo MM (1993) Calcitonin gene-related peptide potentiates synaptic responses at developing neuromuscular junction. Nature 363:76-79.
28. Zaccolo M, et al. (2006) Restricted diffusion of a freely diffusible second messenger: mechanisms underlying compartmentalized cAMP signalling. Biochem Soc Trans 34:495-497.
29. Imaizumi-Scherrer T, Faust DM, Bénichou JC, Hellio R, Weiss MC (1996) Accumulation in fetal muscle and localization to the neuromuscular junction of cAMP-dependent protein kinase A regulatory and catalytic subunits RI alpha and C alpha. J Cell Biol 134:1241-1254.
30. Perkins GA, et al. (2001) PKA, PKC, and AKAP localization in and around the neuromuscular junction. BMC Neurosci 2:17.
31. Barradeau S, Imaizumi-Scherrer T, Weiss MC, Faust DM (2001) Muscle-regulated expression and determinants for neuromuscular junctional localization of the mouse RIalpha regulatory subunit of cAMP-dependent protein kinase. Proc Natl Acad Sci USA 98:5037-5042.
32. Wong W, Scott JD (2004) AKAP signalling complexes: focal points in space and time. Nat Rev Mol Cell Biol 5:959-970.
33. Carlson CR, et al. (2006) Delineation of type I protein kinase A-selective signaling events using an RI anchoring disruptor. J Biol Chem 281:21535-21545.
34. Di Benedetto G, et al. (2008) Protein kinase A type I and type II define distinct intracellular signaling compartments. Circ Res 103:836-844.
35. Röder IV, et al. (2009) PKA microdomain organisation and cAMP handling in healthy and dystrophic muscle in vivo. Cell Signal 21:819-826.
36. Nikolaev VO, Bünemann M, Hein L, Hannawacker A, Lohse MJ (2004) Novel single chain cAMP sensors for receptor-induced signal propagation. J Biol Chem 279:37215-37218.
37. Hu CD, Chinenov Y, Kerppola TK (2002) Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol Cell 9:789-798.
38. Wu X, Bowers B, Rao K, Wei Q, Hammer JA, 3rd (1998) Visualization of melanosome dynamics within wild-type and dilute melanocytes suggests a paradigm for myosin V function in vivo. J Cell Biol 143:1899-1918.
39. De Corte V, et al. (2002) Gelsolin-induced epithelial cell invasion is dependent on Ras-Rac signaling. EMBO J 21:6781-6790.
40. Day RN, Walder JA, Maurer RA (1989) A protein kinase inhibitor gene reduces both basal and multihormone-stimulated prolactin gene transcription. J Biol Chem 264:431-436.
41. 2+ and cytosolic cAMP dynamics in mouse skeletal muscle. J Cell Biol 173:187-193.
42. Brown MC, Ironton R (1977) Motor neurone sprouting induced by prolonged tetrodotoxin block of nerve action potentials. Nature 265:459-461.
43. Coers C, Woolf AL (1959) The Innervation of Muscle: A Biopsy Study (Blackwell Scientific Publications, Oxford).
44. Balice-Gordon RJ, Breedlove SM, Bernstein S, Lichtman JW (1990) Neuromuscular junctions shrink and expand as muscle fiber size is manipulated: in vivo observations in the androgen-sensitive bulbocavernosus muscle of mice. J Neurosci 10:2660-2671.
45. Rudolf R, et al. (2003) Myosin Va facilitates the distribution of secretory granules in the F-actin rich cortex of PC12 cells. J Cell Sci 116:1339-1348.
46. Donà M, et al. (2003) Functional in vivo gene transfer into the myofibers of adult skeletal muscle. Biochem Biophys Res Commun 312:1132-1138.