Accumulation in fetal muscle and localization to the neuromuscular junction of cAMP-dependent protein kinase A regulatory and catalytic subunits RIα and Cα

Journal of Cell Biology

Volumn 134, Issue 5, 1996, Pages 1241-1254

  Imaizumi Scherrer, Tereza ^a   Faust, Daniela M ^a   Bénichou, Jean Claude ^a   Hellio, Raymond ^b   Weiss, Mary C ^a,b  

^a CNRS   (France)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINESTERASE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVE SITE; FETUS; IN SITU HYBRIDIZATION; INTERCOSTAL MUSCLE; MOUSE; MUSCLE DENERVATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE;

ANIMALIA;

EID: 0029758857     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.134.5.1241     Document Type: Article

References (67)

1. Altiok, N., J.L. Bessereau, and J.P. Changeux. 1995. ErbB3 and ErbB2/neu mediate the effect of heregulin on acetylcholine receptor gene expression in muscle: differential expression at the endplate. EMBO (Eur. Mol. Biol. Organ.) J. 14:4258-4266.
2. Beebe, S.J., O. Oyen, M. Sandberg, A. Froysa, V. Hansson, and T. Jahnsen. 1990. Molecular cloning of a tissue-specific protein kinase (Cγ) from human testis - representing a third isoform for the catalytic subunit of cAMP-dependent protein kinase. Mol. Endocrinol. 4: 465-475.
3. Boshart, M., F. Weih, M. Nichols, and G. Schütz. 1991. The tissue-specific extinguisher locus TSE1 encodes a regulatory subunit of cAMP-dependent protein kinase. Cell. 66:849-859.
4. Brenner, H.R., V. Witzemann, and B. Sakmann. 1990. Imprinting of acetylcholine receptor messenger RNA accumulation in mammalian neuromuscular synapses. Nature (Lond.). 344:544-547.
5. Cadd, G., and G.S. McKnight. 1989. Distinct patterns of cAMP-dependent protein kinase gene expression in mouse brain. Neuron. 3:71-79.
6. Chahine, K.G., E. Baracchini, and D. Goldman. 1993. Coupling muscle electrical activity to gene expression via a cAMP-dependent second messenger system. J. Biol. Chem. 268:2893-2898.
7. Chu, G.C., M.A. Velleca, and J.P. Merlie. 1995. Synapse-specific gene expression. Sem. Dev. Biol. 6:175-183.
8. Duclert, A., N. Savatier, and J.-P. Changeux. 1993. An 83-nucleotide promoter of the acetylcholine receptor ε-subunit gene confers preferential synaptic expressin in mouse muscle. Proc. Natl. Acad. Sci. USA. 90:3043-3047.
9. Duclert, A., and J.P. Changeux. 1995. Acetylcholine receptor gene expression at the developing neuromuscular junction. Physiol. Rev. 75:339-368.
10. Dürr, I., M. Numberger, C. Berberich, and V. Witzemann. 1994. Characterization of the functional role of E-box elements for the transcriptional activity of rat acetylcholine receptor ε-subunit and γ-subunit gene promoters in primary muscle cell cultures. Eur. J. Biochem. 224:353-364.
11. Fan, C-M., J.A. Porter, C. Chiang, D.T. Chang, P.A. Beachy, and M. Tessier-Lavigne. 1995. Long-range sclerotome induction by sonic hedgehog: direct role of the amino-terminal cleavage product and modulation by the cyclic AMP signaling pathway. Cell. 81:457-465.
12. Fontaine, B., A. Klarsfeld, and J.P. Changeux. 1987. Calcitonin gene-related peptide and muscle activity regulate acetylcholine receptor α-subunit mRNA levels by distinct intracellular pathways. J. Cell Biol. 105:1337-1342.
13. Fontaine, B., D. Sassoon, M. Buckingham, and J.P. Changeux. 1988. Detection of the nicotinic acetylcholine receptor α-subunit mRNA by in situ hybridization at neuromuscular junctions of 15-day-old chick striated muscles. EMBO (Eur. Mol. Biol Organ.) J. 7:603-609.
14. Fontaine, B., and J.P. Changeux. 1989. Localization of nicotinic acetylcholine receptor α-subunit transcripts during myogenesis and motor endplate development in the chick. J. Cell Biol 108: 1025-1037.
15. Gauthier-Rouvière, C., M. Vandromme, N. Lautredou, Q.Q. Cai, F. Girard, A. Fernandez, and N. Lamb. 1995. The serum response factor nuclear localization signal: general implications for cyclic AMP-dependent protein kinase activity in control of nuclear translocation. Mol. Cell. Biol. 15:433-444.
16. Goldman, D., H.R. Brenner, and S. Heinemann. 1988. Acetylcholine receptor, alpha-, beta-, gamma-, and delta-subunit mRNA levels are regulated by muscle activity. Neuron. 1:329-335.
17. Goldman, D., and J. Staple. 1989. Spatial and temporal expression of acetylcholine receptor RNAs in innervated and denervated rat soleus muscle. Neuron. 3:219-228.
18. Gundersen, K., J.R. Sanes, and J.P. Merlie. 1993. Neural regulation of muscle acetylcholine receptor ε- and α-subunit gene promoters in transgenic mice. J. Cell Biol. 123:1535-1544.
19. Hall, Z. W., and E. Ralston. 1989. Nuclear domains in muscle cells. Cell. 59:771-772.
20. Hall, Z.W., and J.R. Sanes. 1993. Synaptic structure and development: the neuromuscular junction. Cell. 72:99-121.
21. Hammerschmidt, M., M.J. Bitgood, and A.P. McMahon. 1996. Protein kinase A is a common negative regulator of hedgehog signaling in the vertebrate embryo. Genes & Dev. 10:647-658.
22. Huganir, R.L., A.H. Delcour, P. Greengard, and G.P. Hess. 1986. Phosphorylation of the nicotinic acetylcholine receptor regulates its rate of desensitization. Nature (Lond.). 321:774-776.
23. Huganir, R.L., and P. Greengard. 1983. cAMP-dependent protein kinase phosphorylates the nicotinic acetylcholine receptor. Proc. Natl. Acad. Sci. USA. 80:1130-1134.
24. Jiang, J., and G. Struhl. 1995. Protein kinase A and hedgehog signaling in Drosophila limb development. Cell. 80:563-572.
25. Jo, S.A., X. Zhu, M.A. Marchionni, and S.J. Burden. 1995. Neuregulins are concentrated at nerve-muscle synapses and activate ACh-receptor gene expression. Nature (Lond.). 373:158-161.
26. Jones, K.W., M.H. Shapero, M. Chevrette, and R.E.K. Fournier. 1991. Subtractive hybridization cloning of a tissue-specific extinguisher: TSE1 encodes a regulatory subunit of protein kinase A. Cell. 66:861-872.
27. Klarsfeld, A., J.-L. Bessereau, A.-M. Salmon, A. Triller, C. Babinet, and J.-P. Changeux. 1991. An acetylcholine receptor α-subunit promoter conferring preferential synaptic expression in muscle of transgenic mice. EMBO (Eur. Mol. Biol. Organ.) J. 10:625-632.
28. Koelle, G.B., and J.S. Friedenwald. 1949. A histochemical method for localizing cholinesterase activity. Proc. Soc. Biol. Med. 70:617-622.
29. Kues, W.A., H.R. Brenner, B. Sakmann, and V. Witzemann. 1995. Local neurotrophic repression of gene transcripts encoding fetal AChRs at rat neuromuscular synapses. J. Cell Biol. 130:949-957.
30. Lalli, E., and P. Sassone-Corsi. 1994. Signal transduction and gene regulation: the nuclear response to cAMP. J. Biol. Chem. 269:17359-17362.
31. Lepage, T., S.M. Cohen, F.J. Diaz-Benjumea, and S.M. Parkhurst. 1995. Signal transduction by cAMP-dependent protein kinase A in Drosophila limb patterning. Nature (Lond.). 373:711-715.
32. Li, L., R. Heller-Harrison, M. Czech, and E.N. Olson. 1992. Cyclic AMP-dependent protein kinase inhibits the activity of myogenic helix-loop-helix proteins. Mol. Cell Biol. 12:4478-4485.
33. Li, W., J.T. Ohlmeyer, M.E. Lane, and D. Kalderon. 1995. Function of protein kinase A in hedgehog signal transduction and Drosophila imaginal disc development. Cell. 80:553-562.
34. McCartney, S., B.M. Little, L.K. Langeberg, and J.D. Scott. 1995. Cloning and characterization of A-kinase anchor protein 100 (AKAP 100). A protein that targets A-kinase to the sarcoplasmic reticulum. J. Biol. Chem. 270:9327-9333.
35. McKnight, G.S. 1991. Cyclic AMP second messenger systems. Current Opin. Cell Biol. 3:213-217.
36. Merlie, J.P., and J.R. Sanes. 1985. Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibers. Nature (Lond.). 317:66-68.
37. Mishina M., T. Takai, K. Imoto, M. Noda, T. Takahashi, S. Numa, C. Methfessel, and B. Sakmann. 1986. Molecular distinction between fetal and adult forms of muscle acetylcholine receptor. Nature (Lond.). 321:406-411.
38. Morita, N., K. Namikawa, and H. Kiyama. 1995. Up-regulation of PKA R1α subunit mRNA in rat skeletal muscle after nerve injury. NeuroReport. 6: 1050-1052.
39. Moscoso, L., G.C. Chu, M. Gautam, P.G. Noakes, J.P. Merlie, and J.R. Sanes. 1995. Synapse-associated expression of an acetylcholine receptor-inducing protein, ARIA/heregulin, and its putative receptors ErbB2 and ErhB3. in developing mammalian muscle. Dev. Biol. 172:158-169.
40. Mulle, C., P. Benoit, C. Pinset, M. Roa, and J.P. Changeux. 1988. Calcitonin gene-related peptide enhances the rate of desensitization of the nicotinic acetylcholine receptor in cultured mouse muscle cells. Proc. Natl. Acad. Sci. USA. 85:5728-5732.
41. Pan, D., and G.M. Rubin. 1995. cAMP-dependent protein kinase and hedgehog act antagonistically in regulating decapentaplegic transcription in Drosophila imaginal dises. Cell. 80:543-552.
42. Pavlath, G.K., K. Rich, S.G. Webster, and H.M. Blau. 1989. Localization of muscle gene products in nuclear domains. Nature (Lond.). 337:570-573.
43. Piette, J., J.L. Bessereau, M. Huchet, and J.P. Changeux. 1990. Two adjacent MyoD1-binding sites regulate the expression of the acetylcholine receptor α-subunit gene. Nature (Lond.). 345:353-355.
44. Piette, J., M. Huchet, D. Houzelstein, and J.P. Changeux. 1993. Compartmentalized expression of the α- and γ-subunits of the acetylcholine receptor in recently fused myofibers. Dev. Biol. 157:205-213.
45. Sanes, J.R., V.R. Johnson, P.T. Kotzbauer, J. Mudd, T. Hanley, J.C. Martinou, and J.P. Merlie. 1991. Selective expression of an acetylcholine receptor-lacZ transgene in synaptic nuclei of adult muscle fibers. Development (Camb.). 113:1181-1191.
46. Sassoon, D. 1993. Myogenic regulatory factors: dissecting their role and regulation during vertebrate embryogenesis. Dev. Biol. 156:11-23.
47. Sassoon, D., and N. Rosenthal. 1993. Detection of messenger RNA by in situ hybridization. Methods Enzymol. 225:384-404.
48. Schulman, H. 1995. Protein phosphorylation in neuronal plasticity and gene expression. Curr. Opin. Neurobiol. 5:375-381.
49. Scott, J.D. 1993. Cyclic nucelotide-dependent protein kinases. In Intracellular Messengers. C.W. Taylor, editor. Pergamon Press. Oxford, UK. 137-166.
50. Scott, J.D., and S. McCartney. 1994. Localization of A-kinase through anchoring proteins. Mol. Endocrinol. 8:5-11.
51. Simon, A.M., P. Hoppe, and S.J. Burden. 1992. Spatial restriction of AChR gene expression to subsynaptic nuclei. Development (Camb.). 114:545-553.
52. Simon, A.M., and S.J. Burden. 1993. An E box mediates activation and repression of the acetylcholine receptor δ-subunit gene during myogenesis. Mol. Cell. Biol. 13:5133-5140.
53. Tang, J., S.A. Jo, and S.J. Burden. 1994. Separate pathways for synapse-specific and electrical activity-dependent gene expression in skeletal muscle. Development (Camb.). 120:1799-1804.
54. Taylor, S.S., J.A. Buechler, and W. Yonemoto. 1990. cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu. Rev. Biochem. 59:971-1005.
55. Uhler, M.D., J.C. Chrivia, and G.S. McKinght. 1986. Evidence for a second isoform of the catalytic subunit of cAMP-dependent protein kinase. J. Biol. Chem. 261:15360-15363.
56. Valenzuela, D.M., T.N. Stitt, P.S. DiStefano, E. Rojas, K. Mattsson, D.L. Compton, L. Nunez, J.S. Park, J.L. Stark, D.R. Gies, et al. 1995. Receptor tyrosine kinase specific for the skeletal muscle lineage: expression in embryonic muscle, at the neuromuscular junction, and after injury. Neuron. 15: 573-584.
57. Vandromme, M., G. Carnac, C. Gauthier-Rouvière, D. Fesquet, N. Lamb, and A. Fernandez. 1994. Nuclear import of the myogenic factor MyoD requires cAMP-dependent protein kinase activity but not the direct phosphorylation of MyoD. J. Cell Sci. 107:613-620.
58. Vandromme, M., J.C. Cavadore, A. Bonnieu, A. Froeschlé, N. Lamb, and A. Fernandez. 1995. Two nuclear localization signals present in the basic-helix 1 domains of MyoD promote its active nuclear translocation and can function independently. Proc. Natl. Acad. Sci. USA. 92:4646-4650.
59. Van Patten, S.M., P. Howard, D.A. Walsh, and R.A. Maurer. 1992. The α- and β-isoforms of the inhibitor protein of the 3′,5′-cyclic adenosine monophosphate-dependent protein kinase: characteristics and tissue- and developmental-specific expression. Mol. Endocrinol. 6:2114-2121.
60. Walke, W., J. Staple, L. Adams, M. Gnegy, K. Chahine, and D. Goldman. 1994. Calcium-dependent regulation of rat and chick muscle nicotinic acetycholine receptor (nAChR) gene expression. J. Biol. Chem. 269:19447-19456.
61. Watkins, S. 1989. Cryosectionning. In Current Protocols in Molecular Biology. F.A. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl, editors. John Wiley & Sons. Inc., New York. 14.2.1-14.2.8.
62. Wen, W., J. Meinkoth, R.Y. Tsien, and S.S. Taylor. 1995. Identification of a signal for rapid export of proteins from the nucleus. Cell. 82:463-473.
63. Wilkinson, D.G., and M.A. Nieto. 1993. Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Methods Enzymol. 225: 361-373.
64. Winter, B., T. Braun, and H.H. Arnold. 1993. cAMP-dependent protein kinase represses myogenic differentiation and the activity of the muscle-specific helix-loop-helix transcription factors Myf-5 and MyoD. J. Biol. Chem. 268: 9869-9878.
65. Witzemann, V., B. Barg, Y. Nishikawa, B. Sakmann, and S. Numa. 1987. Differential regulation of muscle acetylcholine receptor γ- and ε-subunit mRNAs. FEBS Lett. 223:104-112.
66. Witzemann, V., H.R. Brenner, and B. Sakmann. 1991. Neural factors regulate AChR subunit mRNAs at rat neuromuscular synapses. J. Cell Biol. 114: 125-141.
67. Zhu, X., C. Lai, S. Thomas, and S.J. Burden. 1995. Neuregulin receptors, erbB3 and erbB4, are localized at neuromuscular synapses. EMBO (Eur. Mol. Biol. Organ.) J. 14:5842-5848.