Calcineurin-NFAT signaling, together with GABP and peroxisome PGC-1α, drives utrophin gene expression at the neuromuscular junction

American Journal of Physiology - Cell Physiology

Volumn 289, Issue 4 58-4, 2005, Pages

  Angus, Lindsay M ^a   Chakkalakal, Joe V ^a   Méjat, Alexandre ^b   Eibl, Joe K ^c   Bélanger, Guy ^a   Megeney, Lynn A ^a,d   Chin, Eva R ^e   Schaeffer, Laurent ^b   Michel, Robin N ^c,f   Jasmin, Bernard J ^a,d  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITÉ DE LYON   (France)

^c LAURENTIAN UNIVERSITY   (Canada)

^d OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^e PFIZER INC   (United States)

^f Gina Cody School of Engineering and Computer Science   (Canada)

Author keywords

Duchenne muscular dystrophy; Nuclear respiratory factor 2; Synaptic gene expression

Indexed keywords

ACETYLCHOLINESTERASE; BETA GALACTOSIDASE; CALCINEURIN; CHOLINERGIC RECEPTOR; CYCLOSPORIN A; CYTOCHROME C; GA BINDING PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; TACROLIMUS; TRANSCRIPTION FACTOR ETS; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; UTROPHIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; GENE EXPRESSION; GENE TRANSFER; IMMUNOFLUORESCENCE; MOUSE; MUTATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PEROXISOME; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STATISTICAL ANALYSIS; TRANSACTIVATION;

ANIMALS; CALCINEURIN; CYCLOSPORINE; DNA-BINDING PROTEINS; GA-BINDING PROTEIN TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; IMMUNOSUPPRESSIVE AGENTS; MICE; MUSCLE, SKELETAL; NEUROMUSCULAR JUNCTION; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; SIGNAL TRANSDUCTION; TACROLIMUS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; UTROPHIN;

EID: 25444500449     PISSN: 03636143     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.00196.2005     Document Type: Article

References (62)

1. Arikawa-Hirasawa E, Rossi SG, Rotundo RL, and Yamada Y. Absence of acetylcholinesterase at the neuromuscular junctions of perlecan-null mice. Nat Neurosci 5: 119-123, 2002.
2. Au HC and Scheffler IE. Promoter analysis of the human succinate dehydrogenase iron-protein gene: both nuclear respiratory factors NRF-1 and NRF-2 are required. Eur J Biochem 251: 164-174, 1998.
3. Baar K. Involvement of PPARγ co-activator-1, nuclear respiratory factors 1 and 2, and PPARα in the adaptive response to endurance exercise. Proc Nutr Soc 63: 269-273, 2004.
4. Bassel-Duby R and Olson EN. Role of calcineurin in striated muscle: development, adaptation, and disease. Biochem Biophys Res Commun 311: 1133-1141, 2003.
5. Blake DJ, Weir A, Newey SE, and Davies KE. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 82: 291-329, 2002.
6. Burden SJ. Building the vertebrate neuromuscular synapse. J Neurobiol 53: 501-511, 2002.
7. Cantó C, Suárez E, Lizcano JM, Griñó E, Shepherd PR, Fryer LGD, Carling D, Bertran J, Palacín M, Zorzano A, and Gumà A. Neuregulin signaling on glucose transport in muscle cells. J Biol Chem 279: 12260-12268, 2004.
8. Carrasco MA, Riveros N, Ríos J, Müller M, Torres F, Pineda J, Lantadilla S, and Jaimovich E. Depolarization-induced slow calcium transients activate early genes in skeletal muscle cells. Am J Physiol Cell Physiol 284: C1438-C1447, 2003.
9. Chakkalakal JV, Harrison MA, Carbonetto S, Chin E, Michel RN, and Jasmin BJ. Stimulation of calcineurin signaling attenuates the dystrophic pathology in mdx mice. Hum Mol Genet 13: 379-388, 2004.
10. Chakkalakal JV, Stocksley MA, Harrison MA, Angus LM, Deschênes- Furry J, St-Pierre S, Megeney LA, Chin ER, Michel RN, and Jasmin BJ. Expression of utrophin A mRNA correlates with the oxidative capacity of skeletal muscle fiber types and is regulated by calcineurin/NFAT signaling. Proc Natl Acad Sci USA 100: 7791-7796, 2003.
11. 1 receptors to stimulate acetylcholinesterase and acetylcholine receptor expression: transduction and transcription control. J Neurosci 23: 4445-4456, 2003.
12. Cohen TV and Randall WR. NFATc1 activates the acetylcholinesterase promoter in rat muscle. J Neurochem 90: 1059-1067, 2004.
13. De Kerchove d'Exaerde A, Cartaud J, Ravel-Chapuis A, Seroz T, Pasteau F, Angus LM, Jasmin BJ, Changeux JP, and Schaeffer L. Expression of mutant Ets protein at the neuromuscular synapse causes alterations in morphology and gene expression. EMBO Rep 3: 1075-1081, 2002.
14. 2+ (RAMIC) mobilization operated by postsynaptic neuronal nicotinic receptor regulates synaptic function at the mouse neuromuscular junction [Article in Japanese]. Nippon Yakurigaku Zasshi 110, Suppl 1: 114P-119P, 1997.
15. Duclert A, Savatier N, Schaeffer L, and Changeux JP. Identification of an element crucial for the sub-synaptic expression of the acetylcholine receptor ε-subunit gene. J Biol Chem 271: 17433-17438, 1996.
16. Dunn SE, Burns JL, and Michel RN. Calcineurin is required for skeletal muscle hypertrophy. J Biol Chem 274: 21908-21912, 1999.
17. Dunn SE, Chin ER, and Michel RN. Matching of calcineurin activity to upstream effectors is critical for skeletal muscle fiber growth. J Cell Biol 151: 663-672, 2000.
18. Fromm L and Burden SJ. Neuregulin-1-stimulated phosphorylation of GABP in skeletal muscle cells. Biochemistry 40: 5306-5312, 2001.
19. Gramolini AO, Angus LM, Schaeffer L, Burton EA, Tinsley JM, Davies KE, Changeux JP, and Jasmin BJ. Induction of utrophin gene expression by heregulin in skeletal muscle cells: role of the N-box motif and GA binding protein. Proc Natl Acad Sci USA 96: 3223-3227, 1999.
20. Gramolini AO, Bélanger G, Thompson JM, Chakkalakal JV, and Jasmin BJ. Increased expression of utrophin in a slow vs. a fast muscle involves posttranscriptional events. Am J Physiol Cell Physiol 281: C1300-C1309, 2001.
21. Gramolini AO, Burton EA, Tinsley JM, Ferns MJ, Cartaud A, Cartaud J, Davies KE, Lunde JA, and Jasmin BJ. Muscle and neural isoforms of agrin increase utrophin expression in cultured myotubes via a transcriptional regulatory mechanism. J Biol Chem 273: 736-743, 1998.
22. Gramolini AO, Dennis CL, Tinsley JM, Robertson GS, Cartaud J, Davies KE, and Jasmin BJ. Local transcriptional control of utrophin expression at the neuromuscular synapse. J Biol Chem 272: 8117-8120, 1997.
23. Jasmin BJ, Angus LM, Bélanger G, Chakkalakal JV, Gramolini AO, Lunde JA, Stocksley MA, and Thompson J. Multiple regulatory events controlling the expression and localization of utrophin in skeletal muscle fibers: insights into a therapeutic strategy for Duchenne muscular dystrophy. J Physiol Paris 96: 31-42, 2002.
24. Jasmin BJ, Campbell MJ, and Michel RN. Nerve-dependent regulation of succinate dehydrogenase in junctional and extrajunctional compartments of rat muscle fibres. J Physiol 484: 155-164, 1995.
25. Karnovsky MJ and Roots L. A "direct-coloring" thiocholine method for cholinesterases. J Histochem Cytochem 12: 219-221, 1964.
26. Kelly DP and Scarpulla RC. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev 18: 357-368, 2004.
27. Khurana TS, Rosmarin AG, Shang J, Krag TO, Das S, and Gammeltoft S. Activation of utrophin promoter by heregulin via the ets-related transcription factor complex GA-binding protein α/β. Mol Biol Cell 10: 2075-2086, 1999.
28. Kim CH, Xiong WC, and Mei L. Regulation of MuSK expression by a novel signaling pathway. J Biol Chem 278: 38522-38527, 2003.
29. Knutti D, Kaul A, and Kralli A. A tissue-specific coactivator of steroid receptors, identified in a functional genetic screen. Mol Cell Biol 20: 2411-2422, 2000.
30. Krag TOB, Gyrd-Hansen M, and Khurana TS. Harnessing the potential of dystrophin-related proteins for ameliorating Duchenne's muscular dystrophy. Acta Physiol Scand 171: 349-358, 2001.
31. Krejci E, Legay C, Thomine S, Sketelj J, and Massoulié 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.
32. Kues WA, Sakmann B, and Witzemann V. Differential expression patterns of five acetylcholine receptor subunit genes in rat muscle during development. Eur J Neurosci 7: 1376-1385, 1995.
33. Lee HH, Choi RC, Ting AK, Siow NL, Jiang JX, Massoulié J, and Tsim KW. Transcriptional regulation of acetylcholinesterase-associated collagen ColQ: differential expression in fast and slow twitch muscle fibers is driven by distinct promoters. J Biol Chem 279: 27098-27107, 2004.
34. Lehman JJ, Barger PM, Kovacs A, Saffitz JE, Medeiros DM, and Kelly DP. Peroxisome proliferator-activated receptor γ coactivator-1 promotes cardiac mitochondrial biogenesis. J Clin Invest 106: 847-856, 2000.
35. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, and Spiegelman BM. Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres. Nature 418: 797-801, 2002.
36. Lin J, Wu PH, Tarr PT, Lindenberg KS, St-Pierre J, Zhang C, Mootha VK, Jäger S, Vianna CR, Reznick RM, Cui L, Manieri M, Donovan MX, Wu Z, Cooper MP, Fan MC, Rohas LM, Zavacki AM, Cinti S, Shulman GI, Lowell BB, Krainc D, and Spiegelman BM. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1α null mice. Cell 119: 121-135, 2004.
37. Madhavan R, Zhao XT, Chan F, Wu Z, and Peng HB. The involvement of calcineurin in acetylcholine receptor redistribution in muscle. Mol Cell Neurosci 23: 587-599, 2003.
38. Megeath LJ and Fallon JR. Intracellular calcium regulates agrin-induced acetylcholine receptor clustering. J Neurosci 18: 672-678, 1998.
39. Méjat A, Ravel-Chapuis A, Vandromme M, and Schaeffer L. Synapse-specific gene expression at the neuromuscular junction. Ann NY Acad Sci 998: 53-65, 2003.
40. Michel RN, Dunn SE, and Chin ER. Calcineurin and skeletal muscle growth. Proc Nutr Soc 63: 341-349, 2004.
41. Michel RN, Vu CQ, Tetzlaff W, and Jasmin BJ. Neural regulation of acetylcholinesterase mRNAs at mammalian neuromuscular synapses. J Cell Biol 127: 1061-1069, 1994.
42. Mootha VK, Handschin C, Arlow D, Xie X, St-Pierre J, Sihag S, Yang W, Altshuler D, Puigserver P, Patterson N, Willy PJ, Schulman IG, Heyman RA, Lander ES, and Spiegelman BM. Errα and Gabpa/b specify PGC-1α-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc Natl Acad Sci USA 101: 6570-6575, 2004.
43. Olson EN and Williams RS. Remodeling muscles with calcineurin. Bioessays 22: 510-519, 2000.
44. 2+ signals localize to satellite cells and to components of the neuromuscular junction in skeletal muscle. J Neurosci 23: 8185-8192, 2003.
45. Puigserver P and Spiegelman BM. Peroxisome proliferator-activated receptor-γ coactivator 1α (PGC-1α): transcriptional coactivator and metabolic regulator. Endocr Rev 24: 78-90, 2003.
46. Puigserver P, Wu Z, Park CW, Graves R, Wright M, and Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92: 829-839, 1998.
47. Rodova M, Kelly KF, VanSaun M, Daniel JM, and Werle MJ. Regulation of the rapsyn promoter by Kaiso and δ-catenin. Mol Cell Biol 24: 7188-7196, 2004.
48. Rothermel BA, Vega RB, and Williams RS. The role of modulatory calcineurin-interacting proteins in calcineurin signaling. Trends Cardiovasc Med 13: 15-21, 2003.
49. Sanes JR and Lichtman JW. Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2: 791-805, 2001.
50. Scarpulla RC. Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim Biophys Acta 1576: 1-14, 2002.
51. Scarpulla RC. Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene 286: 81-89, 2002.
52. Schaeffer L, Duclert N, Huchet-Dymanus M, and Changeux JP. Implication of a multisubunit Ets-related transcription factor in synaptic expression of the nicotinic acetylcholine receptor. EMBO J 17: 3078-3090, 1998.
53. Schiaffino S and Serrano A. Calcineurin signaling and neural control of skeletal muscle fiber type and size. Trends Pharmacol Sci 23: 569-575, 2002.
54. Schulz RA and Yutzey KE. Calcineurin signaling and NFAT activation in cardiovascular and skeletal muscle development. Dev Biol 266: 1-16, 2004.
55. Sunesen M and Changeux JP. Transcription in neuromuscular junction formation: who turns on whom? J Neurocytol 32: 677-684, 2003.
56. Sunesen M, Huchet-Dymanus M, Christensen MO, and Changeux JP. Phosphorylation-elicited quaternary changes of GA binding protein in transcriptional activation. Mol Cell Biol 23: 8008-8018, 2003.
57. Tsim KW, Choi RC, Siow NL, Cheng AW, Ling KK, Jiang JX, Tung EK, Lee HH, Xie QH, Simon J, and Barnard EA. ATP induces post-synaptic gene expressions in vertebrate skeletal neuromuscular junctions. J Neurocytol 32: 603-617, 2003.
58. Tung EK, Choi RC, Siow NL, Jiang JX, Ling KK, Simon J, Barnard EA, and Tsim KW. P2Y2 receptor activation regulates the expression of acetylcholinesterase and acetylcholine receptor genes at vertebrate neuromuscular junctions. Mol Pharmacol 66: 794-806, 2004.
59. Virbasius JV and Scarpulla RC. Transcriptional activation through ETS domain binding sites in the cytochrome c oxidase subunit IV gene. Mol Cell Biol 11: 5631-5638, 1991.
60. Virbasius JV and Scarpulla RC. Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc Natl Acad Sci USA 91: 1309-1313, 1994.
61. Virbasius JV, Virbasius CA, and Scarpulla RC. Identity of GABP with NRF-2, a multisubunit activator of cytochrome oxidase expression, reveals a cellular role for an ETS domain activator of viral promoters. Genes Dev 7: 380-392, 1993.
62. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, and Spiegelman BM. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124, 1999.