Protein kinase C isoforms at the neuromuscular junction: Localization and specific roles in neurotransmission and development

Journal of Anatomy

Volumn 224, Issue 1, 2014, Pages 61-73

  Lanuza, Maria A ^a   Santafe, Manel M ^a   Garcia, Neus ^a   Besalduch, Núria ^a   Tomàs, Marta ^a   Obis, Teresa ^a   Priego, Mercedes ^a   Nelson, Phillip G ^b   Tomàs, Josep ^a  

^a FACULTAT DE MEDICINA I CIÈNCIES DE LA SALUT   (Spain)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Electrical stimulation; Immunofluorescence; Isoforms; Neuromuscular junction; Neurotransmission; Protein kinase C; Synapse elimination

Indexed keywords

ACETYLCHOLINE; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM CHANNEL; CALCIUM ION; CALPHOSTIN C; CHOLINERGIC RECEPTOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUCOSE; INSULIN; MUSCARINIC RECEPTOR; NEUROTRANSMITTER; NEUROTROPHIN; NEUROTROPHIN 3; NEUROTROPHIN 4; NEUROTROPHIN RECEPTOR P75; OMEGA AGATOXIN IVA; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE C BETA1; PROTEIN KINASE C BETAII; PROTEIN KINASE C DELTA; PROTEIN KINASE C EPSILON; PROTEIN KINASE C GAMMA; PROTEIN SERINE KINASE; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; VOLTAGE DEPENDENT CALCIUM CHANNEL;

CELL MATURATION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; ELECTROSTIMULATION; ENDPLATE POTENTIAL; ENZYME ACTIVITY; EX VIVO STUDY; GLUCOSE TRANSPORT; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; MYOTUBE; NERVE CELL DIFFERENTIATION; NERVE FIBER; NEUROANATOMY; NEUROMODULATION; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RECEPTOR DOWN REGULATION; REVIEW; RODENT; SCHWANN CELL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SPINAL CORD; SYNAPTIC MEMBRANE; SYNAPTOSOME; TRANSVERSE TUBULAR SYSTEM;

ELECTRICAL STIMULATION; IMMUNOFLUORESCENCE; ISOFORMS; NEUROMUSCULAR JUNCTION; NEUROTRANSMISSION; PROTEIN KINASE C; SYNAPSE ELIMINATION;

ADULT; HUMANS; NEUROMUSCULAR JUNCTION; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN KINASE C; SYNAPTIC TRANSMISSION;

EID: 84890148207     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/joa.12106     Document Type: Review

References (94)

1. Abbs ET, Joseph DN (1981) The effects of atropine and oxotremorine on acetylcholine release in rat phrenic nerve diaphragm preparations. Br J Pharmacol 73, 481-483.
2. Antipenko A, Frías JA, Parra J, et al. (1999) Effect of chronic electrostimulation of rabbit skeletal muscle on calmodulin level and protein kinase activity. Int J Biochem Cell Biol 31, 303-310.
3. Anwyl R (2009) Metabotropic glutamate receptor-dependent long-term potentiation. Neuropharmacology 56, 735-740.
4. Arakawa M, Mizoguchi A, Masutani M, et al. (1993) Ultrastructural localization of protein kinase C beta-subspecies in the axon terminal of rat neuromuscular junction. Neurosci Res 16, 125-130.
5. Arenson MS (1989) Muscarinic inhibition of quantal transmitter release from the magnesium-paralysed frog sartorius muscle. Neuroscience 30, 827-836.
6. Balice-Gordon RJ, Lichtman JW (1993) In vivo observations of pre- and postsynaptic changes during the transition from multiple to single innervation at developing neuromuscular junctions. J Neurosci 13, 834-855.
7. Barde YA, Edgar D, Thoenen H (1982) Purification of a new neurotrophic factor from mammalian brain. EMBO J 1, 549-553.
8. Besalduch N, Tomàs M, Santafe MM, et al. (2010) Synaptic activity-related classical protein kinase C isoform localization in the adult rat neuromuscular synapse. J Comp Neurol 518, 211-228.
9. Besalduch N, Santafe MM, Garcia N, et al. (2011) Transmitter release in the neuromuscular synapse of the protein kinase C theta-deficient adult mouse. J Comp Neurol 519, 849-855.
10. Brandt DT, Goerke A, Heuer M, et al. (2003) Protein kinase C delta induces Src kinase activity via activation of the protein tyrosine phosphatase PTP alpha. J Biol Chem 278, 34073-34078.
11. Buffelli M, Busetto G, Bidoia C, et al. (2004) Activity-dependent synaptic competition at mammalian neuromuscular junctions. News Physiol Sci 19, 85-91.
12. Bursztajn S, Schneider LW, Jong YJ, et al. (1988) Phorbol esters inhibit the synthesis of acetylcholine receptors in cultured muscle cells. Biol Cell 63, 57-65.
13. Byrne JH, Kandel ER (1996) Presynaptic facilitation revisited: state and time dependence. J Neurosci 16, 425-435.
14. Canto C, Suarez E, Lizcano JM, et al. (2004) Neuregulin signaling on glucose transport in muscle cells. J Biol Chem 279, 12260-12268.
15. 2+ channels and snare proteins in neurotransmitter release. Ann NY Acad Sci 868, 144-159.
16. Caulfield MP (1993) Muscarinic receptors - characterization, coupling and function. Pharmacol Ther 58, 319-379.
17. Chang Q, Balice-Gordon RJ (1997) Nip and tuck at the neuromuscular junction: a role for proteases in developmental synapse elimination. BioEssays 19, 271-275.
18. Cleland PJ, Appleby GJ, Rattigan S, et al. (1989) Exercise-induced translocation of protein kinase C and production of diacylglycerol and phosphatidic acid in rat skeletal muscle in vivo. Relationship to changes in glucose transport. J Biol Chem 264, 17704-17711.
19. Ekström PA, Bergstrand H, Edström A (1992) Effects of protein kinase inhibitors on regeneration in vitro of adult frog sciatic sensory axons. J Neurosci Res 31, 462-469.
20. Ganguly DK, Das M (1979) Effects of oxotremorine demonstrate presynaptic muscarinic and dopaminergic receptors on motor nerve terminals. Nature 278, 645-646.
21. Garcia N, Santafe MM, Tomas M, et al. (2010a) The interaction between tropomyosin-related kinase B receptors and presynaptic muscarinic receptors modulates transmitter release in adult rodent motor nerve terminals. J Neurosci 30, 16514-16522.
22. Garcia N, Santafe MM, Tomas M, et al. (2010b) Involvement of Brain-derived neurotrophic factor (BDNF) in the functional elimination of synaptic contacts at polyinnervated neuromuscular synapses during development. J Neurosci Res 88, 1406-1419.
23. Garcia N, Santafe MM, Tomas M, et al. (2010c) Neurotrophin-4 couples to locally modulated ACh release at the end of neuromuscular synapse maturation. Neurosci Lett 468, 72-74.
24. Garcia N, Santafe MM, Tomàs M, et al. (2010d) Involvement of neurotrophin-3 (NT-3) in the functional elimination of synaptic contacts during neuromuscular development. Neurosci Lett 473, 141-145.
25. Garcia N, Tomàs M, Santafe MM, et al. (2011) Blocking p75 (NTR) receptors alters polyinnervation of neuromuscular synapses during development. J Neurosci Res 89, 1331-1341.
26. Herrera AA, Zeng Y (2003) Activity-dependent switch from synapse formation to synapse elimination during development of neuromuscular junctions. J Neurocytol 32, 817-833.
27. Hilgenberg L, Miles K (1995) Developmental regulation of a protein kinase C isoform localized in the neuromuscular junction. J Cell Sci 108, 51-61.
28. Hilgenberg L, Yearwood S, Milstein S, et al. (1996) Neural influence on protein kinase C expression in skeletal muscle. J Neurosci 16, 4994-5003.
29. Jansen JK, Van Essen DC, Brown MC (1976) Formation and elimination of synapses in skeletal muscles of rat. Cold Spring Harb Symp Quant Biol 40, 425-434.
30. Jia M, Li M, Dunlap V, et al. (1999) The thrombin receptor mediates functional activity-dependent neuromuscular synapse reduction via protein kinase C activation in vitro. J Neurobiol 38, 369-381.
31. Kim S, Bondeva T, Nelson PG (2002) Activation of protein kinase C isozymes in primary mouse myotubes by carbachol. Brain Res Dev Brain Res 137, 13-21.
32. Kotecha SA, MacDonald JF (2003) Signaling molecules and receptor transduction cascades that regulate NMDA receptor-mediated synaptic transmission. Int Rev Neurobiol 54, 51-106.
33. 2+, phospholipid-dependent protein kinase associated with plasma membrane. Nature 301, 621-623.
34. Kraft AS, Anderson WB, Cooper HL, et al. (1982) Decrease in cytosolic calcium/phospholipid-dependent protein kinase activity following phorbol ester treatment of EL4 thymoma cells. J Biol Chem 257, 13193-13196.
35. Lanuza MA, Li MX, Jia M, et al. (2000) Protein kinase C-mediated changes in synaptic efficacy at the neuromuscular junction in vitro: the role of postsynaptic acetylcholine receptors. J Neurosci Res 61, 616-625.
36. Lanuza MA, Garcia N, Santafe M, et al. (2001) Pertussis toxin-sensitive G-protein and protein kinase C activity are involved in normal synapse elimination in the neonatal rat muscle. J Neurosci Res 63, 330-340.
37. Lanuza MA, Garcia N, Santafe M, et al. (2002) Pre- and postsynaptic maturation of the neuromuscular junction during neonatal synapse elimination depends on protein kinase C. J Neurosci Res 67, 607-617.
38. Lanuza MA, Gizaw R, Viloria A, et al. (2006a) Phosphorylation of the nicotinic acetylcholine receptor in myotube-cholinergic neuron cocultures. J Neurosci Res 83, 1407-1414.
39. Lanuza MA, Besalduch N, Garcia N, et al. (2006b) PKA and PKC localization at the adult rat neuromuscular junction. FENS Forum Abstracts. Vol. 3, A048.2.240. The Federation of European Neuroscience Societies. www.fns.org
40. Lanuza MA, Besalduch N, Garcia N, et al. (2007) Plastic embedded semithin cross-sections as a tool for high-resolution immunofluorescence analysis of the neuromuscular junction molecules: specific cellular location of protease-activated receptor-1. J Neurosci Res 85, 748-756.
41. Lanuza MA, Besalduch N, González C, et al. (2010) Decreased phosphorylation of δ and ε subunits of the acetylcholine receptor coincides with delayed postsynaptic maturation in PKC θ deficient mouse. Exp Neurol 225, 183-195.
42. Lanuza MA, Besalduch N, Obis T, et al. (2012) Exclusive presynaptic location and coupling to ACh release of the novel protein kinase C epsilon isoform in the adult rat neuromuscular synapse. Program No. 137.11. 2012 Neuroscience Meeting Planner. New Orleans, LA: Society for Neuroscience. Online.
43. Li MX, Jia M, Jiang H, et al. (2001) Opposing actions of protein kinase A and C mediate Hebbian synaptic plasticity. Nat Neurosci 4, 871-872.
44. Li MX, Jia M, Yang LX, et al. (2004) The role of the theta isoform of protein kinase C (PKC) in activity-dependent synapse elimination: evidence from the PKC theta knock-out mouse in vivo and in vitro. J Neurosci 24, 3762-3769.
45. Liu Y, Fields RD, Fitzgerald S, et al. (1994) Proteolytic activity, synapse elimination, and the Hebb synapse. J Neurobiol 25, 325-335.
46. MacDonald JF, Kotecha SA, Lu WY, et al. (2001) Convergence of PKC-dependent kinase signal cascades on NMDA receptors. Curr Drug Targets 2, 299-312.
47. Miles K, Wagner M (2003) Overexpression of nPKC theta is inhibitory for agrin-induced nicotinic acetylcholine receptor clustering in C2C12 myotubes. J Neurosci Res 71, 188-195.
48. Mochly-Rosen D (1995) Localization of protein kinases by anchoring proteins: a theme in signal transduction. Science 268, 247-251.
49. Mochly-Rosen D, Gordon AS (1998) Anchoring proteins for protein kinase C: a means for isozyme selectivity. FASEB J 12, 35-42.
50. Mochly-Rosen D, Khaner H, Lopez J, et al. (1991a) Intracellular receptors for activated protein kinase C. Identification of a binding site for the enzyme. J Biol Chem 266, 14866-14868.
51. Mochly-Rosen D, Khaner H, Lopez J (1991b) Identification of intracellular receptor proteins for activated protein kinase C. Proc Natl Acad Sci USA 88, 3997-4000.
52. Moraczewski J, Nowotniak A, Wrobel E, et al. (2002) Differential changes in protein kinase C associated with regeneration of rat extensor digitorum longus and soleus muscles. Int J Biochem Cell Biol 34, 938-949.
53. Nakano S, Shimohama S, Saitoh T, et al. (1992) Localization of protein kinase C in human skeletal muscle. Muscle Nerve 15, 496-499.
54. Nelson PG, Lanuza MA, Jia M, et al. (2003) Phosphorylation reactions in activity-dependent synapse modification at the neuromuscular junction during development. J Neurocytol 32, 803-816.
55. Nguyen QT, Lichtman JW (1996) Mechanism of synapse disassembly at the developing neuromuscular junction. Curr Opin Neurobiol 6, 104-112.
56. Nimnual AS, Chang W, Chang NS, et al. (1998) Identification of phosphorylation sites on AChR-subunit associated with dispersal of AChR clusters on the surface of muscle cells. Biochemistry 37, 14823-14832.
57. 2+ signalling pathway at the endplate provided by the gamma to epsilon subunit switch in ACh receptors. Brain Res Mol Brain Res 24, 341-345.
58. Nishizuka Y (1995) Protein kinase C and lipid signaling for sustained cellular responses. FASEB J 9, 484-496.
59. Numann R, Hauschka SD, Catterall WA, et al. (1994) Modulation of skeletal muscle sodium channels in a satellite cell line by protein kinase C. J Neurosci 14, 4226-4236.
60. Oancea E, Meyer T (1998) Protein kinase C as a molecular machine for decoding calcium and diacylglycerol signals. Cell 95, 307-318.
61. Perkins GA, Wang L, Huang LJ, et al. (2001) PKA, PKC, and AKAP localization in and around the neuromuscular junction. BMC Neurosci 2, 17.
62. Perrini S, Henriksson J, Zierath JR, et al. (2004) Exercise-induced protein kinase C isoform-specific activation in human skeletal muscle. Diabetes 53, 21-24.
63. Poo MM (2001) Neurotrophins as synaptic modulators. Nat Rev Neurosci 2, 24-32.
64. Ren SQ, Yan JZ, Zhang XY, et al. (2013) PKCλ is critical in AMPA receptor phosphorylation and synaptic incorporation during LTP. EMBO J 32, 1365-1380.
65. Richter EA, Cleland PJ, Rattigan S, et al. (1987) Contraction-associated translocation of protein kinase C in rat skeletal muscle. FEBS Lett 217, 232-236.
66. Roberts RE, McLean WG (1997) Protein kinase C isozyme expression in sciatic nerves and spinal cords of experimentally diabetic rats. Brain Res 754, 147-156.
67. Roche KW, Tingley WG, Huganir RL (1994) Glutamate receptor phosphorylation and synaptic plasticity. Curr Opin Neurobiol 4, 383-388.
68. Rose AJ, Michell BJ, Kemp BE, et al. (2004) Effect of exercise on protein kinase C activity and localization in human skeletal muscle. J Physiol 561, 861-870.
69. Ross A, Rapuano M, Prives J (1988) Induction of phosphorylation and cell surface redistribution of acetylcholine receptors by phorbol ester and carbamylcholine in cultured chick muscle cells. J Cell Biol 107, 1139-1145.
70. Sacktor TC (2008) PKMzeta, LTP maintenance, and the dynamic molecular biology of memory storage. Prog Brain Res 169, 27-40.
71. Saito N, Itouji A, Totani Y, et al. (1993) Cellular and intracellular localization of epsilon-subspecies of protein kinase C in the rat brain; presynaptic localization of the epsilon-subspecies. Brain Res 607, 241-248.
72. Salvatori S, Furlan S, Millikin B, et al. (1993) Localization of protein kinase C in skeletal muscle T-tubule membranes. Biochem Biophys Res Commun 196, 1073-1080.
73. Sanderson JL, Dell'Acqua ML (2011) AKAP signaling complexes in regulation of excitatory synaptic plasticity. Neuroscientist 17, 321-336.
74. Sanes JR, Lichtman JW (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22, 389-442.
75. Santafe MM, Garcia N, Lanuza MA, et al. (2001) Calcium channels coupled to neurotransmitter release at dually innervated neuromuscular junctions in the newborn rat. Neuroscience 102, 697-708.
76. Santafe MM, Garcia N, Lanuza MA, et al. (2002) Decreased calcium influx into the neonatal rat motor nerve terminals can recruit additional neuromuscular junctions during the synapse elimination period. Neuroscience 110, 147-154.
77. Santafe MM, Salon I, Garcia N, et al. (2003) Modulation of ACh release by presynaptic muscarinic autoreceptors in the neuromuscular junction of the newborn and adult rat. Eur J Neurosci 17, 119-127.
78. Santafe MM, Lanuza MA, Garcia N, et al. (2005) Calcium inflow-dependent protein kinase C activity is involved in the modulation of transmitter release in the neuromuscular junction of the adult rat. Synapse 57, 76-84.
79. Santafe MM, Lanuza MA, Garcia N, et al. (2006) Muscarinic autoreceptors modulate transmitter release through protein kinase C and protein kinase A in the rat motor nerve terminal. Eur J Neurosci 23, 2048-2056.
80. Santafe MM, Garcia N, Lanuza MA, et al. (2007) Protein kinase C activity affects neurotransmitter release at polyinnervated neuromuscular synapses. J Neurosci Res 85, 1449-1457.
81. Santafe MM, Garcia N, Lanuza MA, et al. (2009a) Interaction between protein kinase C and protein kinase A can modulate transmitter release at the rat neuromuscular synapse. J Neurosci Res 87, 683-690.
82. Santafe MM, Garcia N, Lanuza MA, et al. (2009b) Presynaptic muscarinic receptors, calcium channels, and protein kinase C modulate the functional disconnection of weak inputs at polyinnervated neonatal neuromuscular synapses. J Neurosci Res 87, 1195-1206.
83. Shirai Y, Adachi N, Saito N (2008) Protein kinase Cepsilon: function in neurons. FEBS J 275, 3988-3994.
84. Tanaka C, Nishizuka Y (1994) The protein kinase C family for neuronal signaling. Annu Rev Neurosci 17, 551-567.
85. Tomàs J, Santafe MM, Lanuza MA, et al. (2011) Silent synapses in neuromuscular junction development. J Neurosci Res 89, 3-12.
86. Tsuruno S, Hirano T (2007) Persistent activation of protein kinase Calpha is not necessary for expression of cerebellar long-term depression. Mol Cell Neurosci 35, 38-48.
87. Van Ginneken MM, Keizer HA, Wijnberg ID, et al. (2004) Immunohistochemical identification and fiber type specific localization of protein kinase C isoforms in equine skeletal muscle. Am J Vet Res 65, 69-73.
88. Vary TC, Goodman S, Kilpatrick LE, et al. (2005) Nutrient regulation of PKCepsilon is mediated by leucine, not insulin, in skeletal muscle. Am J Physiol Endocrinol Metab 289, 684-694.
89. 2+ and phorbol ester. J Cell Biol 107, 267-268.
90. Wang XH, Poo MM (1997) Potentiation of developing synapses by postsynaptic release of neurotrophin-4. Neuron 19, 825-835.
91. Wang T, Xie K, Lu B (1995) Neurotrophins promote maturation of developing neuromuscular synapses. J Neurosci 15, 4796-4805.
92. Wessler I, Karl M, Mai M, et al. (1987) Muscarine receptors on the rat phrenic nerve, evidence for positive and negative muscarinic feedback mechanisms. Naunyn-Schmiedeberg's Arch Pharmacol 335, 605-612.
93. + channel required for modulation by protein kinase C. Science 254, 866-868.
94. Wyatt RM, Balice-Gordon RJ (2003) Activity-dependent elimination of neuromuscular synapses. J Neurocytol 32, 777-794.