Targeting PKCθ in skeletal muscle and muscle diseases: Good or bad?

Biochemical Society Transactions

Volumn 42, Issue 6, 2014, Pages 1550-1555

  Marrocco, Valeria ^a   Fiore, Piera ^a   Madaro, Luca ^b   Crupi, Annunziata ^a   Lozanoska Ochser, Biliana ^a   Bouché, Marina ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

Muscle development; Muscle maintenance; Muscular dystrophy; Protein kinase C (PKC ); Skeletal muscle

Indexed keywords

PROTEIN KINASE C THETA; ISOENZYME; PRKCQ PROTEIN, HUMAN; PROTEIN KINASE C;

ARTICLE; CELL FUNCTION; HOMEOSTASIS; IN VITRO STUDY; IN VIVO STUDY; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE DISEASE; MUSCLE GROWTH; MUSCULAR DYSTROPHY; MYOPATHY; NONHUMAN; PROTEIN TARGETING; SKELETAL MUSCLE; ENZYMOLOGY; HUMAN; METABOLISM;

HOMEOSTASIS; HUMANS; ISOENZYMES; MUSCLE, SKELETAL; MUSCULAR DISEASES; PROTEIN KINASE C;

EID: 84911908641     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20140207     Document Type: Article

References (54)

1. Osada, S., Mizuno, K., Saido, T.C., Suzuki, K., Kuroki, T. and Ohno, S. (1992) A new member of the protein kinase C family, nPKCe, predominantly expressed in skeletal muscle. Mol. Cell. Biol. 12, 3930-3938 PubMed
2. Baier, G. (2007) PKC isotype functions in T lymphocytes. Ernst Schering Found Symp. Proc. 3, 29-41 PubMed
3. Wang, X., Chuang, H.C., Li, J.P. and Tan, T.H. (2012) Regulation of PKC-0 function by phosphorylation in T cell receptor signaling. Front. Immunol. 3, 197 PubMed
4. Cohen, S., Braiman, A., Shubinsky, G., Ohayon, A., Altman, A. and Isakov, N. (2009) PKC0 is required for hemostasis and positive regulation of thrombin-induced platelet aggregation and a-granule secretion. Biochem. Biophys. Res. Commun. 385, 22-27 CrossRef PubMed
5. Liu, Y., Graham, C, Parravicini, V., Brown, M.J., Rivera, J. and Shaw, S. (2001) Protein kinase C0 is expressed in mast cells and is functionally involved in Fce receptor I signaling. J. Leukoc. Biol. 69, 831-840 PubMed
6. Tassi, I., Cella, M., Presti, R., Colucci, A., Gilfillan, S., Littman, D.R. and Colonna, M. (2008) NK cell-activating receptors require PKC-0 for sustained signaling, transcriptional activation, and IFN-y secretion. Blood 112, 4109-4116 CrossRef PubMed
7. Hilgenberg, L and Miles, K. (1995) Developmental regulation of a protein kinase C isoform localized in the neuromuscular junction. J. Cell Sci. 108, 51-61 PubMed
8. Lanuza, M.A., Besalduch, N., Gonzalez, C, Santafe, M.M., Garcia, N., Tamas, M., Nelson, P.G. and Tamas, J. (2010) Decreased phosphorylation of S and s subunits of the acetylcholine receptor coincides with delayed postsynaptic maturation in PKC0 deficient mouse. Exp. Neurol. 225, 183-195 CrossRef PubMed
9. Li, M.X., Jia, M., Yang, L.X., Jiang, H., Lanuza, M.A., Gonzalez, CM. and Nelson, P.G. (2004) The role of the 0 isoform of protein kinase C (PKC) in activity-dependent synapse elimination: evidence from the PKC0 knock-out mouse in vivo and in vitro. J. Neurosci. 24, 3762-3769 CrossRef PubMed
10. Hilgenberg, L, Yearwood, S., Milstein, S. and Miles, K. (1996) Neural influence on protein kinase C isoform expression in skeletal muscle. J. Neurosci. 16, 4994-5003 PubMed
11. Serra, C, Federici, M., Buongiorno, A., Senni, M.I., Morelli, S., Segratella, E., Pascuccio, M., Tiveron, C, Mattei, E., Tatangelo, L. et al. (2003) Transgenic mice with dominant negative PKC-0 in skeletal muscle: a new model of insulin resistance and obesity. J. Cell. Physiol. 196, 89-97 CrossRef PubMed
12. 2+ mobilization and NFAT cell activation in primary mouse T cells. J. Exp. Med. 197, 1525-1535 CrossRef PubMed
13. Sun, Z., Arendt, C.W., Ellmeier, W., Schaeffer, E.M., Sunshine, M.J., Gandhi, L., Annes, J., Petrzilka, D., Kupfer, A., Schwartzberg, P.L and Littman, D.R. (2000) PKC-0 is required for TCR-induced NF-KB activation in mature but not immature T lymphocytes. Nature 404, 402-407 CrossRef PubMed
14. Baier, G. and Wagner, J. (2009) PKC inhibitors: potential in T cell-dependent immune diseases. Curr. Opin. Cell Biol. 21, 262-267 CrossRef PubMed
15. Boschelli, D.H., Subrath, J., Niu, C, Wu, B., Wang, Y., Lee, J., Brennan, A., Ho, M., Deng, B., Yang, X. et al. (2010) Optimization of 5-vinylaryl-3-pyridinecarbonitriles as PKC0 inhibitors. Bioorg. Med. Chem. Lett. 20, 1965-1968 CrossRef PubMed
16. Cywin, C.L, Dahmann, G., Prokopowicz, III, A.S., Young, E.R., Magolda, R.L, Cardozo, M.G., Cogan, D.A., Disalvo, D., Ginn, J.D., Kashem, M.A. et al. (2007) Discovery of potent and selective PKC-0 inhibitors. Bioorg. Med. Chem. Lett. 17, 225-230 CrossRef PubMed
17. Griffin, M.E., Marcucci, M.J., Cline, G.W., Bell, K., Barucci, N., Lee, D., Goodyear, L.J., Kraegen, E.W., White, M.F. and Shulman, G.I. (1999) Free fatty acid-induced insulin resistance is associated with activation of protein kinase C0 and alterations in the insulin signaling cascade. Diabetes 48, 1270-1274 CrossRef PubMed
18. Kim, J.K., Fillmore, J.J., Sunshine, M.J., Albrecht, B., Higashimori, T., Kim, D.W., Liu, Z.X., Soos, T.J., Cline, G.W., O'Brien, W.R. et al. (2004) PKC-0 knockout mice are protected from fat-induced insulin resistance. J. Clin. Invest. 114, 823-827 CrossRef PubMed
19. Gao, Z., Wang, Z., Zhang, X., Butler, A.A., Zuberi, A., Gawronska-Kozak, B., Lefevre, M., York, D., Ravussin, E., Berthoud, H.R. et al. (2007) Inactivation of PKC0 leads to increased susceptibility to obesity and dietary insulin resistance in mice. Am. J. Physiol. Endocrinol. Metab. 292, E84-E91 CrossRef PubMed
20. Biressi, S., Tagliafico, E., Lamorte, G., Monteverde, S., Tenedini, E., Roncaglia, E., Ferrari, S., Ferrari, S., Cusella-De Angelis, M.G., Tajbakhsh, S. and Cossu, G. (2007) Intrinsic phenotypic diversity of embryonic and fetal myoblasts is revealed by genome-wide gene expression analysis on purified cells. Dev. Biol. 304, 633-651 CrossRef PubMed
21. Cusella-De Angelis, M.G., Molinari, S., Le Donne, A., Coletta, M., Vivarelli, E., Bouche, M., Molinaro, M., Ferrari, S. and Cossu, G. (1994) Differential response of embryonic and fetal myoblasts to TGF: a possible regulatory mechanism of skeletal muscle histogenesis. Development 120, 925-933 PubMed
22. Zappelli, F., Willems, D., Osada, S., Ohno, S., Wetsel, W.C., Molinaro, M., Cossu, G. and Bouché, M. (1996) The inhibition of differentiation caused by TGFβ in fetal myoblasts is dependent upon selective expression of PKCθ: a possible molecular basis for myoblast diversification during limb histogenesis. Dev. Biol. 180, 156-164 CrossRef PubMed
23. Messina, G., Biressi, S., Monteverde, S., Magli, A., Cassano, M., Perani, L., Roncaglia, E., Tagliafico, E., Starnes, L., Campbell, C.E. et al. (2010) Nfix regulates fetal-specific transcription in developing skeletal muscle. Cell 140, 554-566 CrossRef PubMed
24. D'Andrea, M., Pisaniello, A., Serra, C., Senni, M.I., Castaldi, L., Molinaro, M. and Bouché, M. (2006) Protein kinase Cθ co-operates with calcineurin in the activation of slow muscle genes in cultured myogenic cells. J. Cell. Physiol. 207, 379-388 CrossRef PubMed
25. Parra, M., Kasler, H., McKinsey, T.A., Olson, E.N. and Verdin, E. (2005) Protein kinase D1 phosphorylates HDAC7 and induces its nuclear export after T-cell receptor activation. J. Biol. Chem. 280, 13762-13770 CrossRef PubMed
26. Vega, R.B., Harrison, B.C., Meadows, E., Roberts, C.R., Papst, P.J., Olson, E.N. and McKinsey, T.A. (2004) Protein kinases C and D mediate agonist-dependent cardiac hypertrophy through nuclear export of histone deacetylase 5. Mol. Cell Biol. 24, 8374-8385 CrossRef PubMed
27. Kim, M.S., Fielitz, J., McAnally, J., Shelton, J.M., Lemon, D.D., McKinsey, T.A., Richardson, J.A., Bassel-Duby, R. and Olson, E.N. (2008) Protein kinase D1 stimulates MEF2 activity in skeletal muscle and enhances muscle performance. Mol. Cell. Biol. 28, 3600-3609 CrossRef PubMed
28. Madaro, L., Marrocco, V., Fiore, P., Aulino, P., Smeriglio, P., Adamo, S., Molinaro, M. and Bouché, M. (2011) PKCθ signaling is required for myoblast fusion by regulating the expression of caveolin-3 and β1D integrin upstream focal adhesion kinase. Mol. Biol. Cell 22, 1409-1419 CrossRef PubMed
29. Le, G.F. and Rudnicki, M.A. (2007) Skeletal muscle satellite cells and adult myogenesis. Curr. Opin. Cell Biol. 19, 628-633 CrossRef PubMed
30. Moraczewski, J., Nowotniak, A., Wróbel, E., Castagna, M., Gautron, J. and Martelly, I. (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 CrossRef PubMed
31. Tokugawa, S., Sakuma, K., Fujiwara, H., Hirata, M., Oda, R., Morisaki, S., Yasuhara, M. and Kubo, T. (2009) The expression pattern of PKCθ in satellite cells of normal and regenerating muscle in the rat. Neuropathology 29, 211-218 CrossRef PubMed
32. Boczán, J., Boros, S., Mechler, F., Kovács, L. and Bíró, T. (2000) Differential expressions of protein kinase C isozymes during proliferation and differentiation of human skeletal muscle cells in vitro. Acta Neuropathol. 99, 96-104 CrossRef PubMed
33. Marino, J.S., Hinds, Jr, T.D., Potter, R.A., Ondrus, E., Onion, J.L., Dowling, A., McLoughlin, T.J., Sanchez, E.R. and Hill, J.W. (2013) Suppression of protein kinase Cθ contributes to enhanced myogenesis in vitro via IRS1 and ERK1/2 phosphorylation. BMC Cell Biol. 14, 39 CrossRef PubMed
34. Besalduch, N., Santafé, M.M., Garcia, N., Gonzalez, C., Tomás, M., Tomás, J. and Lanuza, M.A. (2011) Transmitter release in the neuromuscular synapse of the protein kinase Cθ-deficient adult mouse. J. Comp. Neurol. 519, 849-855 CrossRef PubMed
35. Rayavarapu, S., Coley, W. and Nagaraju, K. (2012) Endoplasmic reticulum stress in skeletal muscle homeostasis and disease. Curr. Rheumatol. Rep. 14, 238-243 CrossRef PubMed
36. Nagaraju, K., Casciola-Rosen, L., Lundberg, I., Rawat, R., Cutting, S., Thapliyal, R., Chang, J., Dwivedi, S., Mitsak, M., Chen, Y. W. et al. (2005) Activation of the endoplasmic reticulum stress response in autoimmune myositis: potential role in muscle fiber damage and dysfunction. Arthritis Rheum. 52, 1824-1835 PubMed
37. Fujita, E., Kouroku, Y., Isoai, A., Kumagai, H., Misutani, A., Matsuda, C., Hayashi, Y. K. and Momoi, T. (2007) Two endoplasmic reticulum-associated degradation (ERAD) systems for the novel variant of the mutant dysferlin: ubiquitin/proteasome ERAD(I) and autophagy/lysosome ERAD(II). Hum. Mol. Genet. 16, 618-629 PubMed
38. Sakaki, K., Wu, J. and Kaufman, R.J. (2008) Protein kinase Cθ is required for autophagy in response to stress in the endoplasmic reticulum. J. Biol. Chem. 283, 15370-15380 CrossRef PubMed
39. Madaro, L., Marrocco, V., Carnio, S., Sandri, M. and Bouché, M. (2013) Intracellular signaling in ER stress-induced autophagy in skeletal muscle cells. FASEB J. 27, 1990-2000 CrossRef PubMed
40. Paoletti, R., Maffei, A., Madaro, L., Notte, A., Stanganello, E., Cifelli, G., Carullo, P., Molinaro, M., Lembo, G. and Bouché, M. (2010) Protein kinase Cθ is required for cardiomyocyte survival and cardiac remodeling. Cell Death Dis. 1, e45 CrossRef PubMed
41. Camerino, G.M., Bouchè, M., De Bellis, M., Cannone, M., Liantonio, A., Musaraj, K., Romano, R., Smeriglio, P., Madaro, L., Giustino, A. et al. (2014) Protein kinase Cθ (PKCθ) modulates the ClC-1 chloride channel activity and skeletal muscle phenotype: a biophysical and gene expression study in mouse models lacking the PKCθ. Pflugers Arch., doi:10.1007/s00424-014-1495-1 PubMed
42. Lueck, J.D., Mankodi, A., Swanson, M.S., Thornton, C.A. and Dirksen, R.T. (2007) Muscle chloride channel dysfunction in two mouse models of myotonic dystrophy. J. Gen. Physiol. 129, 79-94 CrossRef PubMed
43. Pierno, S., Desaphy, J.F., Liantonio, A., De Luca, A., Zarrilli, A., Mastrofrancesco, L., Procino, G., Valenti, G. and Conte Camerino, D. (2007) Disuse of rat muscle in vivo reduces protein kinase C activity controlling the sarcolemma chloride conductance. J. Physiol. 584, 983-995 CrossRef PubMed
44. Zhang, E.Y., Kong, K.F. and Altman, A. (2013) The yin and yang of protein kinase C-θ (PKCθ): a novel drug target for selective immunosuppression. Adv. Pharmacol. 66, 267-312 CrossRef PubMed
45. Healy, A.M., Izmailova, E., Fitzgerald, M., Walker, R., Hattersley, M., Silva, M., Siebert, E., Terkelsen, J., Picarella, D., Pickard, M.D. et al. (2006) PKC-θ-deficient mice are protected from Th1-dependent antigen-induced arthritis. J. Immunol. 177, 1886-1893 CrossRef PubMed
46. Marsland, B.J., Soos, T.J., Späth, G., Littman, D.R. and Kopf, M. (2004) Protein kinase Cθ is critical for the development of in vivo T helper (Th)2 cell but not Th1 cell responses. J. Exp. Med. 200, 181-189 CrossRef PubMed
47. Zanin-Zhorov, A., Ding, Y., Kumari, S., Attur, M., Hippen, K.L., Brown, M., Blazar, B.R., Abramson, S.B., Lafaille, J.J. and Dustin, M.L. (2010) Protein kinase C-θ mediates negative feedback on regulatory T cell function. Science 328, 372-376 CrossRef PubMed
48. Evans, N.P., Misyak, S.A., Robertson, J.L., Bassaganya-Riera, J. and Grange, R.W. (2009) Dysregulated intracellular signaling and inflammatory gene expression during initial disease onset in Duchenne muscular dystrophy. Am. J. Phys. Med. Rehabil. 88, 502-522 CrossRef PubMed
49. Porter, J.D., Khanna, S., Kaminski, H.J., Rao, J.S., Merriam, A.P., Richmonds, C.R., Leahy, P., Li, J., Guo, W. and Andrade, F.H. (2002) A chronic inflammatory response dominates the skeletal muscle molecular signature in dystrophin-deficient mdx mice. Hum. Mol. Genet. 11, 263-272 CrossRef PubMed
50. Madaro, L. and Bouché, M. (2014) From innate to adaptive immune response in muscular dystrophies and skeletal muscle regeneration: the role of lymphocytes. Biomed. Res. Int. 2014, 438675 CrossRef PubMed
51. Morrison, J., Palmer, D.B., Cobbold, S., Partridge, T. and Bou-Gharios, G. (2005) Effects of T-lymphocyte depletion on muscle fibrosis in the mdx mouse. Am. J. Pathol. 166, 1701-1710 CrossRef PubMed
52. Vetrone, S.A., Montecino-Rodriguez, E., Kudryashova, E., Kramerova, I., Hoffman, E.P., Liu, S.D., Miceli, M.C. and Spencer, M.J. (2009) Osteopontin promotes fibrosis in dystrophic mouse muscle by modulating immune cell subsets and intramuscular TGF-β. J. Clin. Invest. 119, 1583-1594 CrossRef PubMed
53. Eghtesad, S., Jhunjhunwala, S., Little, S.R. and Clemens, P.R. (2011) Rapamycin ameliorates dystrophic phenotype in mdx mouse skeletal muscle. Mol. Med. 17, 917-924 CrossRef PubMed
54. Madaro, L., Pelle, A., Nicoletti, C., Crupi, A., Marrocco, V., Bossi, G., Soddu, S. and Bouché, M. (2012) PKCθ ablation improves healing in a mouse model of muscular dystrophy. PLoS ONE 7, e31515 CrossRef PubMed