Transgenic overexpression of human DMPK accumulates into hypertrophic cardiomyopathy, myotonic myophaty and hypotension traits of myotonic dystrophy

Human Molecular Genetics

Volumn 13, Issue 20, 2004, Pages 2505-2518

  O'Cochlain, D Fearghas ^a   Perez Terzic, Carmen ^a   Reyes, Santiago ^a   Kane, Garvan C ^a   Behfar, Atta ^a   Hodgson, Denice M ^a   Strommen, Jeffrey A ^a   Liu, Xiao Ke ^a   van den Broek, Walther ^b   Wansink, Derick G ^b   Wieringa, Bé ^b   Terzic, Andre ^a  

^a Mayo Clinic   (United States)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CHLORIDE; CHLORIDE CHANNEL; GENE PRODUCT; MESSENGER RNA; PROTEIN KINASE; RHO KINASE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY MUSCLE; ARTICLE; CELL DEGENERATION; CELL TYPE; CELL VIABILITY; CONTROLLED STUDY; CYTOARCHITECTURE; DISEASE ASSOCIATION; ENDURANCE; EXERCISE; EXON; FEMALE; FIBROSING ALVEOLITIS; GENE OVEREXPRESSION; GENE TRANSLOCATION; HEART ARRHYTHMIA; HEART MUSCLE; HEART MUSCLE EXCITABILITY; HEART VENTRICLE HYPERTROPHY; HEART WORK; HYPERTROPHIC CARDIOMYOPATHY; HYPOTENSION; MALE; MOUSE; MULTIGENE FAMILY; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE FUNCTION; MYOTONIA; MYOTONIC DYSTROPHY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROMOTER REGION; RISK ASSESSMENT; SARCOLEMMA; SARCOMERE; SKELETAL MUSCLE; SMOOTH MUSCLE; SMOOTH MUSCLE TONE; TRANSGENE; TRANSGENIC MOUSE; WILD TYPE;

AGING; ANIMALS; CARDIOMYOPATHY, HYPERTROPHIC; ECHOCARDIOGRAPHY; EXERCISE TEST; GENE DOSAGE; GENE EXPRESSION; HUMANS; HYPOTENSION; MICE; MICE, TRANSGENIC; MUSCLE, SKELETAL; MUSCLE, SMOOTH, VASCULAR; MYOCARDIUM; MYOTONIC DYSTROPHY; PROTEIN-SERINE-THREONINE KINASES; TRANSGENES;

MURINAE;

EID: 19544367095     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddh266     Document Type: Article

References (64)

1. Manning, G., Whyte, D.B., Martinez, R., Hunter, T. and Sudarsanam, S. (2002) The protein kinase complement ofthe human genome. Science, 298, 1912-1934.
2. Harper, P.S. (2001) Myotonic Dystrophy. WB Saunders Co Ltd, London, UK.
3. Riento, K. and Ridley, A.J. (2003) Rocks: multifunctional kinases in cell behaviour. Nat. Rev. Mol. Cell. Biol., 4, 446-456.
4. Ueda, H., Ohno, S. and Kobayashi T. (2000) Myotonic dystrophy and myotonic dystrophy protein kinase. Prog. Histochem. Cytochem., 35, 187-251.
5. Wansink, D.G., van Herpen, R.E.M.A., Coerwinkel-Driessen, M.M., Groenen, P.J.T.A., Hemmings, B.A. and Wieringa, B. (2003) Alternative splicing controls myotonic dystrophy protein kinase structure, enzymatic activity and subcellular localization. Mol. Cell. Biol., 23, 5489-5501.
6. Wansink, D.G. and Wieringa, B. (2003) Transgenic mouse models for myotonic dystrophy type 1 (DM1). Cytogenet. Genome Res., 100 230-242.
7. Groenen, P.J.T.A., Wansink, D.G., Coerwinkel, M., van den Broek, W., Jansen, G. and Wieringa, B. (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.
8. Jansen, G., Mahadevan, M., Amemiya, C., Wormskamp, N.G., Segers, B., Hendriks, W., O'Hoy, K., Baird, S., Sabourin, L., Lennon, G. et al. (1992) Characterization of the myotonic dystrophy region predicts multiple protein isoforms-encoding mRNAs. Nat. Genet., 1, 261-266.
9. Jansen, G., Groenen, P.J.T.A., Bachner, D., Jap, P.H., Coerwinkel, M., Oerlemans, F., van den Brock, W., Gohlsch, B., Pette, D., Plomp, J.J. et al. (1996) Abnormal myotonic dystrophy protein kinase levels produce only mild myopathy in mice. Nat. Genet., 13, 316-324.
10. Berul, C.I., Maguire, C.T., Aronovitz, M.J., Greenwood, J., Miller, C., Gehrmann, J., Housman, D., Mendelsohn, M.E. and Reddy, S. (1999) DMPK dosage alterations result in atrioventricular conduction abnormalities in a mouse myotonic dystrophy model. J. Clin. Invest. 103, R1-R7.
11. Mounsey, J.P., Mistry, D.J., Ai, C.W., Reddy, S. and Moorman, J.R. (2000) Skeletal muscle sodium channel gating in mice deficient in myotonic dystrophy protein kinase. Hum. Mol. Genet., 9, 2313-2320.
12. Pall, G.S., Johnson, K.J. and Smith, G.L. (2003) Abnormal contractile activity and calcium cycling in cardiac myocytes from DMPK-KO mice. Physiol. Genomics, 13, 139-146.
13. Lee, H.C., Patel, M.K., Mistry, D.J., Wang, Q., Reddy, S., Moorman, J.R. and Mounsey, J.P. (2003) Abnormal Na channel gating in murine cardiac myocytes deficient in myotonic dystrophy protein kinase. Physiol. Genomics, 12, 1471-1475.
14. Steinmeyer, K., Klocke, R., Ortland, C., Gronemeier, M., Jockusch, H., Grunder, S. and Jentsch, T.J. (1991) Inactivation of muscle chloride channel by transposon insertion in myotonic mice. Nature, 354, 304-308.
15. Mounsey, J.P., Xu, P., John, J.E., III, Horne, L.T., Gilbert, J., Roses, A.D. and Moorman, J.R. (1995) Modulation of skeletal muscle sodium channels by human myotonin protein kinase. J. Clin. Invest., 95, 2379-2384.
16. 2+ homeostasis in skeletal muscle cells. J. Clin. Invest., 100, 1440-1447.
17. Kimura, T., Takahashi, M.P., Okuda, Y., Kaido, M., Fujimura, H., Yanagihara, T. and Sakoda, S. (2000) The expression of ion channel mRNAs in skeletal muscles from patients with myotonic muscular dystrophy. Neurosci. Lett., 295, 93-96.
18. Mankodi, A., Takahashi, M.P., Jiang, H., Beck, C.L., Bowers, W.J., Moxley, R.T., Cannon, S.C. and Thornton C.A. (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.
19. Jin, S., Shimizu, M., Balasubramanyam, A. and Epstein, H.F. (2000) Myotonic dystrophy protein kinase (DMPK) induces actin cytoskeletal reorganization and apoptotic-like blebbing in lens cells. Cell Motil. Cytoskeleton, 45, 133-148.
20. Muranyi, A., Zhang, R., Liu, F., Hirano, K., Ito, M., Epstein, H.F. and Hartshorne, D.J. (2001) Myotonic dystrophy protein kinase phosphorylates the myosin phosphatase targeting subunit and inhibits myosin phosphatase activity. FEBS Lett., 493, 80-84.
21. Fu, Y.H., Pizzuti, A., Fenwick, Jr, R.G., King, J., Rajnarayan, S., Dunne, P.W., Dubel, J., Nasser, G.A., Ashizawa, T., de Jong, P. et al. (1992) An unstable triplet repeat in a gene related to myotonic muscular dystrophy. Science, 255, 1256-1258.
22. Brook, J.D., McCurrach, M.E., Harley, H.G., Buckler, A.J, Church, D., Aburatani, H., Hunter, K., Stanton, V.P., Thirion, J.P., Hudson, T. et al. (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.
23. Mahadevan, M., Tsilfidis, C., Sabourin, L., Shuder, G., Amemiya, C., Jansen, G., Neville, C., Narang, M., Barcelo, J., O'Hoy, K. et al. (1992) Myotonic dystrophy mutation: an unstable CTG repeat in the 3′ untranslated region of the gene. Science, 255, 1253-1255.
24. Aslanidis, C., Jansen, G., Amemiya, C., Shutler, G., Mahadevan, M., Tsilfidis, C., Chen, C., Alleman, J., Wormskamp, N.G., Vooijs, M. et al. (1992) Cloning of the essential myotonic dystrophy region and mapping of the putative defect. Nature, 355 548-551.
25. Sabourin, L.A., Tamai, K., Narang, M.A. and Korneluk, R.G. (1997) Overexpression of 3′-untranslated region of the myotonic dystrophy protein kinase cDNA inhibits myoblast differentiation in vitro. J Biol. Chem., 272, 29626-29635.
26. Furling, D., Lam le, T., Agbulut, O., Butler-Browne, G.S. and Morris, G.E. (2003) Changes in myotonic dystrophy protein kinase levels and muscle development in congenital myotonic dystrophy. Am. J. Pathol., 162, 1001-1009.
27. Storbeck, C.J., Drmanic, S., Daniel, K., Waring, J.D., Jirik, F.R., Parry, D.J., Ahmed, N., Sabourin, L.A., Ikeda, J. and Korneluk, R.G. (2004) Inhibition of myogenesis in transgenic mice expressing the human DMPK 3′-UTR. Hum. Mol. Genet., 13, 589-600.
28. Amack, J.D. and Mahadevan, M.S. (2004) Myogenic defects in myotonic dystrophy. Dev. Biol., 265, 294-301.
29. Ebralidze, A., Wang, Y., Petkova, V., Ebralidse, K. and Junghans, R.P. (2004) RNA leaching of transcription factors disrupts transcription in myotonic dystrophy. Science, 303, 383-387.
30. Ranum, L.P. and Day, J.W. (2004) Myotonic dystrophy: RNA pathogenesis comes into focus. Am. J Hum. Genet., 74, 793-804.
31. La Spada, A.R., Richards, R.I. and Wieringa, B. (2004) Dynamic mutations on the move in Banff. Nat. Genet., 36, 667-670.
32. Storbeck, C.J., Sabourin, L.A., Waring, J.D. and Korneluk, R.G. (1998) Definition of regulatory sequence elements in the promoter region and the first intron of the myotonic dystrophy protein kinase gene. J. Biol. Chem., 273, 9139-9147.
33. Lam, L.T., Pham, Y.C., Nguyen, T.M. and Morris, G.E. (2000) Characterization of a monoclonal antibody panel shows that the myotonic dystrophy protein kinase, DMPK, is expressed almost exclusively in muscle and heart. Hum. Mol. Genet., 9, 2167-2173.
34. ATP channel knockout compromises the metabolic benefit of exercise training resulting in cardiac deficits. Diabetes, in press.
35. Chien, K.R. (1999) Stress pathways and heart failure. Cell 98, 555-558.
36. Frey, N. and Olson, E.N. (2003) Cardiac hypertrophy: the good, the bad, and the ugly. Annu. Rev. Physiol., 65, 45-79.
37. Chien, K.R. and Olson, E.N. (2002) Converging pathways and principles in heart development and disease. Cell, 110, 153-162.
38. Wieringa, B. (1994) Myotonic dystrophy reviewed: back to the future? Hum. Mol. Genet., 3, 1-7.
39. Gurnett, C.A., Kahl, S.D., Anderson, R.D. and Campbell, K.P. (1995) Absence of the skeletal muscle sarcolemma chloride channel ClC-1 in myotonic mice. J. Biol. Chem., 270, 9035-9038.
40. Charlet-B., N., Savkur, R.S., Singh, G., Philips, A.V., Grice, E.A. and Cooper, T.A. (2002) Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol. Cell., 1, 45-53.
41. Kanadia, R.N., Johnstone, K.A., Mankodi, A., Lungu, C., Thornton, C.A., Esson, D., Timmers, A.M., Hauswirth, W.W. and Swanson, M.S. (2003) A muscleblind knockout model for myotonic dystrophy. Science, 302, 1978-1980.
42. Engel, A.G. and Franzini-Armstrong, C. (eds) (2004) Myology. McGraw-Hill, Inc., New York, NY.
43. Schiavon, G., Furlan, S., Marin, O. and Salvatori, S. (2002) Myotonic dystrophy protein kinase of the cardiac muscle: evaluation using an immunochemical approach. Microsc. Res. Tech., 58, 404-411.
44. Schulz, P.E., McIntosh, A.D., Kasten, M.R., Wieringa, B. and Epstein, H.F. (2003) A role for myotonic dystrophy protein kinase in synaptic plasticity. J. Neurophysiol., 89, 1177-1186.
45. Harman, D. (1981) The aging process. Proc. Natl Acad. Sci. USA, 78, 7124-7128.
46. Johnson, F.B., Sinclair, D.A. and Guarente, L. (1999) Molecular biology of aging. Cell, 96, 291-302.
47. ATP channel-dependent stress tolerance. EMBO J., 22 1732-1742.
48. Zingman, L.V., Hodgson, D.M., Bast, P.H., Kane, G.C., Perez-Terzie, C., Gumina, R.J., Pucar, D., Bienengraeber, M., Dzeja, P.P., Miki, T., et al. (2002) Kir6.2 is required for adaptation to stress. Proc. Natl Acad. Sci. USA, 99, 13278-13283.
49. Nguyen, H.H., Wolfe, J.T., III, Holmes, D.R., Jr. and Edwards, W.D. (1988) Pathology of the cardiac conduction system in myotonic dystrophy: a study of 12 cases. J. Am. Coll. Cardiol., 11, 662-671.
50. Chien, K.R., Ross, J., Jr. and Hoshijima, R. (2003) Calcium and heart failure: the cycle game. Nat. Med., 9, 508-509.
51. Rüdel, R. and Lehmann-Horn, F. (1985) Membrane changes in cells from myotonia patients. Physiol. Rev., 65, 310-356.
52. Entrikin, R.K., Randall, W.R. and Wilson B.W. (1982) Myotonic electromyographic activity in complexus muscles of normal and dystrophic chicks. Muscle Nerve, 5, 396-398.
53. Evans, W. (1944) The heart in myotonia atrophica. Br. Heart J., 4, 41-47.
54. O'Brien, T., Harper, P.S. and Newcombe, R.G. (1983) Blood pressure and myotonic dystrophy. Clin. Genet., 23, 422-426.
55. Pineiro, E., Fernandez-Lopez, L., Gamez, J., Marcos, R., Surralles, J. and Velazquez, A. (2003) Mutagenic stress modulates the dynamics of CTG repeat instability associated with myotonic dystrophy type 1. Nucl. Acids Res., 31, 6733-6740.
56. Tian, B., White, R.J., Xia, T., Welle, S., Turner, D.H., Mathews, M.B. and Thornton, C.A. (2000) Expanded CUG repeat RNAs form hairpins that activate the double-stranded RNA-dependent protein kinase PKR. RNA, 6, 79-87.
57. Miller, J.W., Urbinati, C.R., Teng-Umnuay, P., Stenberg, M.G., Byrne, B.J., Thornton, C.A. and Swanson, M.S. (2000) Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J., 19, 4439-4448.
58. Gacy, M.A. and McMurray, C.T. (1998) Influence of hairpins on template reannealing at trinucleotide repeat duplexes: a model for slipped DNA. Biochemistry, 37, 9426-9434.
59. Sasagawa, N., Kino, Y., Takeshita, Y., Oma, Y. and Ishiura, S. (2003) Overexpression of human myotonic dystrophy protein kinase in Schizosaccharomyces pombe induces an abnormal polarized and swollen cell morphology. J. Biochem. (Tokyo), 134, 537-542.
60. Engel, W.K. and Cunningham, G.G. (1963) Rapid examination of muscle tissue. An improved trichrome method for fresh-frozen biopsy sections. Neurology, 13, 919-923.
61. Perez-Terzic, C., Behfar, A., Mery, A., van Deursen, J.M., Terzic, A. and Puceat, M. (2003) Structural adaptation of the nuclear pore complex in stem cell-derived cardiomyocytes. Circ. Res., 92 444-452.
62. Perez-Terzic, C., Gacy, A.M., Bortolon, R., Dzeja, P.P., Puceat, M., Jaconi, M., Prendegast, F.G. and Terzic, A. (2001) Directed inhibition of nuclear import in cellular hypertrophy. J. Biol. Chem. 276, 20566-20571.
63. Hodgson, D.M., Behfar, A., Zingman, L.V., Kane, G.C., Perez-Terzic, C., Alekseev, A.E., Pucéat, M. and Terzic, A. (2004) Stable benefit of embryonic stem cell therapy in myocardial infarction. Am. J. Physiol., 287, H471-H479.
64. ATP channels, predisposes to catecholamine-induced ventricular dysrhythmia. Diabetes, in press.