30
Views
43
CrossRef citations to date
0
Altmetric
Cell Growth and Development

Alternative Splicing Controls Myotonic Dystrophy Protein Kinase Structure, Enzymatic Activity, and Subcellular Localization

, , , , &
Pages 5489-5501 | Received 07 Feb 2003, Accepted 20 May 2003, Published online: 27 Mar 2023

REFERENCES

  • Alessi, D. R., M. Andjelkovic, B. Caudwell, P. Cron, N. Morrice, P. Cohen, and B. A. Hemmings. 1996. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15: 6541–6551.
  • Alessi, D. R., F. B. Caudwell, M. Andjelkovic, B. A. Hemmings, and P. Cohen. 1996. Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett. 399: 333–338.
  • Amano, M., K. Chihara, N. Nakamura, T. Kaneko, Y. Matsuura, and K. Kaibuchi. 1999. The COOH terminus of Rho-kinase negatively regulates Rho-kinase activity. J. Biol. Chem. 274: 32418–32424.
  • Amano, M., Y. Fukata, and K. Kaibuchi. 2000. Regulation and functions of Rho-associated kinase. Exp. Cell Res. 261: 44–51.
  • Benders, A. G. M., P. J. T. A. Groenen, F. T. J. J. Oerlemans, J. H. Veerkamp, and B. Wieringa. 1997. Myotonic dystrophy protein kinase is involved in the modulation of the Ca2+ homeostasis in skeletal muscle cells. J. Clin. Investig. 100: 1440–1447.
  • Berul, C. I., C. T. Maguire, M. J. Aronovitz, J. Greenwood, C. Miller, J. Gehrmann, D. Housman, M. E. Mendelsohn, and S. Reddy. 1999. DMPK dosage alterations result in atrioventricular conduction abnormalities in a mouse myotonic dystrophy model. J. Clin. Investig. 103: R1–R7.
  • Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254.
  • Brazil, D. P., and B. A. Hemmings. 2001. Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem. Sci. 26: 657–664.
  • Brodbeck, D., M. M. Hill, and B. A. Hemmings. 2001. Two splice variants of protein kinase Bγ have different regulatory capacity depending on the presence or absence of the regulatory phosphorylation site serine 472 in the carboxy-terminal hydrophobic domain. J. Biol. Chem. 276: 29550–29558.
  • Brook, J. D., M. E. McCurrach, H. G. Harley, A. J. Buckler, D. Church, H. Aburatani, K. Hunter, V. P. Stanton, J.-P. Thirion, T. Hudson, R. Sohn, B. Zemelman, R. G. Snell, S. A. Rundle, S. Crow, J. Davies, P. Shelbourne, J. Buxton, C. Jones, V. Juvonen, K. Johnson, P. S. Harper, D. J. Shaw, and D. E. Housman. 1992. Molecular basis of myotonic dystrophy: expansion of a trinucleotide (CTG) repeat at the 3′ end of a transcript encoding a protein kinase family member. Cell 68: 799–808.
  • Burgess, H. A., and O. Reiner. 2002. Alternative splice variants of doublecortin-like kinase are differentially expressed and have different kinase activities. J. Biol. Chem. 277: 17696–17705.
  • Bush, E. W., S. M. Helmke, R. A. Birnbaum, and M. B. Perryman. 2000. Myotonic dystrophy protein kinase domains mediate localization, oligomerization, novel catalytic activity, and autoinhibition. Biochemistry 39: 8480–8490.
  • Caceres, J. F., and A. R. Kornblihtt. 2002. Alternative splicing: multiple control mechanisms and involvement in human disease. Trends Genet. 18: 186–193.
  • Chalfant, C. E., H. Mischak, J. E. Watson, B. C. Winkler, J. Goodnight, R. V. Farese, and D. R. Cooper. 1995. Regulation of alternative splicing of protein kinase C beta by insulin. J. Biol. Chem. 270: 13326–13332.
  • Charlet-B., N., R. S. Savkur, G. Singh, A. V. Philips, E. A. Grice, and T. A. Cooper. 2002. Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol. Cell 10: 45–53.
  • Davis, B. M., M. E. McCurrach, K. L. Taneja, R. H. Singer, and D. E. Housman. 1997. Expansion of a CUG trinucleotide repeat in the 3′ untranslated region of myotonic dystrophy protein kinase transcripts results in nuclear retention of transcripts. Proc. Natl. Acad. Sci. USA 94: 7388–7393.
  • Di Cunto, F., E. Calautti, J. Hsiao, L. Ong, G. Topley, E. Turco, and G. P. Dotto. 1998. Citron Rho-interacting kinase, a novel tissue-specific ser/thr kinase encompassing the Rho-Rac-binding protein Citron. J. Biol. Chem. 273: 29706–29711.
  • Dunne, P. W., E. T. Walch, and H. F. Epstein. 1994. Phosphorylation reactions of recombinant human myotonic dystrophy protein kinase and their inhibition. Biochemistry. 33: 10809–10814.
  • Feng, J., M. Ito, K. Ichikawa, N. Isaka, M. Nishikawa, D. J. Hartshorne, and T. Nakano. 1999. Inhibitory phosphorylation site for Rho-associated kinase on smooth muscle myosin phosphatase. J. Biol. Chem. 274: 37385–37390.
  • Fu, Y.-H., A. Pizzuti, R. G. Fenwick Jr., J. King, S. Rajnarayan, P. W. Dunne, J. Dubel, G. A. Nasser, T. Ashizawa, P. de Jong, B. Wieringa, R. G. Korneluk, M. B. Perryman, H. F. Epstein, and C. T. Caskey. 1992. An unstable triplet repeat in a gene related to myotonic muscular dystrophy. Science 255: 1256–1258.
  • Groenen, P., and B. Wieringa. 1998. Expanding complexity in myotonic dystrophy. BioEssays 20: 901–912.
  • Groenen, P. J. T. A., D. G. Wansink, M. Coerwinkel, W. van den Broek, G. Jansen, and B. Wieringa. 2000. Constitutive and regulated modes of splicing produce six major myotonic dystrophy protein kinase (DMPK) isoforms with distinct properties. Hum. Mol. Genet. 9: 605–616.
  • Harper, P. S. 2001. Myotonic dystrophy, 3rd ed., vol. 37. W. B. Saunders, London, United Kingdom.
  • Hill, M. M., and B. A. Hemmings. 2002. Analysis of protein kinase B/Akt. Methods Enzymol. 345: 448–463.
  • Jansen, G., P. J. Groenen, D. Bachner, P. H. Jap, M. Coerwinkel, F. Oerlemans, W. van den Broek, B. Gohlsch, D. Pette, J. J. Plomp, P. C. Molenaar, M. G. Nederhoff, C. J. van Echteld, M. Dekker, A. Berns, H. Hameister, and B. Wieringa. 1996. Abnormal myotonic dystrophy protein kinase levels produce only mild myopathy in mice. Nat. Genet. 13: 316–324.
  • Justice, R. W., O. Zilian, D. F. Woods, M. Noll, and P. J. Bryant. 1995. The Drosophila tumor suppressor gene warts encodes a homolog of human myotonic dystrophy kinase and is required for the control of cell shape and proliferation. Genes Dev. 9: 534–546.
  • Kawano, Y., Y. Fukata, N. Oshiro, M. Amano, T. Nakamura, M. Ito, F. Matsumura, M. Inagaki, and K. Kaibuchi. 1999. Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J. Cell Biol. 147: 1023–1038.
  • Leung, T., X.-Q. Chen, I. Tan, E. Manser, and L. Lim. 1998. Myotonic dystrophy kinase-related Cdc42-binding kinase acts as a Cdc42 effector in promoting cytoskeletal reorganization. Mol. Cell. Biol. 18: 130–140.
  • Mahadevan, M., C. Amemiya, G. Jansen, L. Sabourin, S. Baird, C. Neville, N. Wormskamp, B. Segers, M. Batzer, J. Lamerdin, P. de Jong, B. Wieringa, and R. Korneluk. 1993. Structure and genomic sequence of the myotonic dystrophy (DM kinase) gene. Hum. Mol. Genet. 2: 299–304.
  • Mankodi, A., M. P. Takahashi, H. Jiang, C. L. Beck, W. J. Bowers, R. T. Moxley, S. C. Cannon, and C. A. Thornton. 2002. Expanded CUG repeats trigger aberrant splicing of ClC-1 chloride channel pre-mRNA and hyperexcitability of skeletal muscle in myotonic dystrophy. Mol. Cell 10: 35–44.
  • Manning, G., G. D. Plowman, T. Hunter, and S. Sudarsanam. 2002. Evolution of protein kinase signaling from yeast to man. Trends Biochem. Sci. 27: 514–520.
  • Millward, T., P. Cron, and B. A. Hemmings. 1995. Molecular cloning and characterization of a conserved nuclear serine(threonine) protein kinase. Proc. Natl. Acad. Sci. 92: 5022–5026.
  • Millward, T. A., C. W. Heizmann, B. W. Schafer, and B. A. Hemmings. 1998. Calcium regulation of Ndr protein kinase mediated by S100 calcium-binding proteins. EMBO J. 17: 5913–5922.
  • Millward, T. A., D. Hess, and B. A. Hemmings. 1999. Ndr protein kinase is regulated by phosphorylation on two conserved sequence motifs. J. Biol. Chem. 274: 33847–33850.
  • Mounsey, J. P., D. J. Mistry, C. W. Ai, S. Reddy, and J. R. Moorman. 2000. Skeletal muscle sodium channel gating in mice deficient in myotonic dystrophy protein kinase. Hum. Mol. Genet. 9: 2313–2320.
  • Mounsey, J. P., P. Xu, J. E. John, 3rd, L. T. Horne, J. Gilbert, A. D. Roses, and J. R. Moorman. 1995. Modulation of skeletal muscle sodium channels by human myotonin protein kinase. J. Clin. Investig. 95: 2379–2384.
  • Muranyi, A., R. Zhang, F. Liu, K. Hirano, M. Ito, H. F. Epstein, and D. J. Hartshorne. 2001. Myotonic dystrophy protein kinase phosphorylates the myosin phosphatase targeting subunit and inhibits myosin phosphatase activity. FEBS Lett. 493: 80–84.
  • Nissim-Rafinia, M., and B. Kerem. 2002. Splicing regulation as a potential genetic modifier. Trends Genet. 18: 123–127.
  • Obata, T., M. B. Yaffe, G. G. Leparc, E. T. Piro, H. Maegawa, A. Kashiwagi, R. Kikkawa, and L. C. Cantley. 2000. Peptide and protein library screening defines optimal substrate motifs for AKT/PKB. J. Biol. Chem. 275: 36108–36115.
  • Philips, A. V., L. T. Timchenko, and T. A. Cooper. 1998. Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science 280: 737–740.
  • Ranum, L. P. W., and J. W. Day. 2002. Dominantly inherited, non-coding microsatellite expansion disorders. Curr. Opin. Genet. Dev. 12: 266–271.
  • Reddy, S., D. B. J. Smith, M. M. Rich, J. M. Leferovich, P. Reilly, B. M. Davis, K. Tran, H. Rayburn, R. Bronson, D. Cros, R. J. Balice-Gordon, and D. Housman. 1996. Mice lacking the myotonic dystrophy protein kinase develop a late onset progressive myopathy. Nat. Genet. 13: 325–335.
  • Savkur, R. S., A. Philips, and T. A. Cooper. 2001. Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy. Nat. Genet. 29: 40–47.
  • Scorrano, L., S. A. Oakes, J. T. Opferman, E. H. Cheng, M. D. Sorcinelli, T. Pozzan, and S. J. Korsmeyer. 2003. BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science 300: 135–139.
  • Sergeant, N., B. Sablonniere, S. Schraen-Maschke, A. Ghestem, C. Maurage, A. Wattez, P. Vermersch, and A. Delacourte. 2001. Dysregulation of human brain microtubule-associated tau mRNA maturation in myotonic dystrophy type 1. Hum. Mol. Genet. 10: 2143–2155.
  • Seto, M., Y. Sasaki, and Y. Sasaki. 1990. Alteration in the myosin phosphorylation pattern of smooth muscle by phorbol ester. Am. J. Physiol. 259: C769–C774.
  • Stadhouders, A. M., P. H. Jap, H. P. Winkler, H. M. Eppenberger, and T. Wallimann. 1994. Mitochondrial creatine kinase: a major constituent of pathological inclusions seen in mitochondrial myopathies. Proc. Natl. Acad. Sci. USA 91: 5089–5093.
  • Tan, I., K. T. Seow, L. Lim, and T. Leung. 2001. Intermolecular and intramolecular interactions regulate catalytic activity of myotonic dystrophy kinase-related Cdc42-binding kinase α. Mol. Cell. Biol. 21: 2767–2778.
  • Timchenko, L., N. W., T. Schneider, B. Patel, F. Hofmann, and C. T. Caskey. 1995. Full-length myotonin protein kinase (72 kDa) displays serine kinase activity. Proc. Natl. Acad. Sci. USA 92: 5366–5370.
  • Tiscornia, G., and M. S. Mahadevan. 2000. Myotonic dystrophy: the role of the CUG triplet repeats in splicing of a novel DMPK exon and altered cytoplasmic DMPK mRNA isoform ratios. Mol. Cell 5: 959–967.
  • Turner, M. S., L. Fen Fen, J. W. Trauger, J. Stephens, and P. LoGrasso. 2002. Characterization and purification of truncated human Rho-kinase II expressed in Sf-21 cells. Arch. Biochem. Biophys. 405: 13–20.
  • Ueda, H., S. Ohno, and T. Kobayashi. 2000. Myotonic dystrophy and myotonic dystrophy protein kinase. Progr. Histochem. Cytochem. 35: 187–251.
  • Wansink, D. G., and B. Wieringa. Transgenic mouse models for myotonic dystrophy type 1 (DM1). Cytogenet. Genome Res., in press.
  • Waring, J. D., R. Haq, K. Tamai, L. A. Sabourin, J.-E. Ikeda, and R. G. Korneluk. 1996. Investigation of myotonic dystrophy kinase isoform translocation and membrane association. J. Biol. Chem. 271: 15187–15193.
  • Xu, T., W. Wang, S. Zhang, R. A. Stewart, and W. Yu. 1995. Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 121: 1053–1063.
  • Yang, J., P. Cron, V. Thompson, V. Good, D. Hess, B. Hemmings, and D. Barford. 2002. Molecular mechanism for the regulation of protein kinase B/Akt by hydrophobic motif phosphorylation. Mol. Cell 9: 1227–1240.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.