Abnormal actomyosin assembly in proliferating and differentiating myoblasts upon expression of a cytosolic DMPK isoform

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 5, 2011, Pages 867-877

  Mulders, Susan A M ^a   van Horssen, Remco ^a   Gerrits, Lieke ^a   Bennink, Miranda B ^a   Pluk, Helma ^a   de Boer van Huizen, Roelie T ^a   Croes, Huib J E ^a   Wijers, Mietske ^a   van de Loo, Fons A J ^a   Fransen, Jack ^a   Wieringa, Bé ^a   Wansink, Derick G ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Actomyosin cytoskeleton; Alternative splicing; Myogenesis; Myotonic dystrophy protein kinase; Rho kinase; ROCK; Stress fiber

Indexed keywords

ADENOVIRUS VECTOR; MYOSIN LIGHT CHAIN 2; MYOTONIC DYSTROPHY PROTEIN KINASE; MYOTONIC DYSTROPHY PROTEIN KINASE A; MYOTONIC DYSTROPHY PROTEIN KINASE C; MYOTONIC DYSTROPHY PROTEIN KINASE E; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CELL MOTILITY; CELL PROLIFERATION; CELL SHAPE; CONTROLLED STUDY; CYTOSKELETON; CYTOSOL; EMBRYO; MOUSE; MUSCLE DEVELOPMENT; MUTANT; MYOBLAST; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SKELETAL MUSCLE; STRESS FIBER;

ACTINS; ACTOMYOSIN; ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL POLARITY; CELL PROLIFERATION; CELL SHAPE; CYTOSOL; ISOENZYMES; MICE; MUSCLE DEVELOPMENT; MYOBLASTS; MYOSIN TYPE II; PHOSPHORYLATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; STRESS FIBERS; SUBCELLULAR FRACTIONS;

EID: 79955657623     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2011.01.024     Document Type: Article

References (57)

1. 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., Sohn R., Zemelman B., Snell R.G., Rundle S.A., Crow S., Davies J., Shelbourne P., Buxton J., Jones C., Juvonen V., Johnson K., Harper P.S., Shaw D.J., Housman D.E. 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 1992, 68:799-808.
2. Mulders S.A., van Engelen B.G., Wieringa B., Wansink D.G. Molecular therapy in myotonic dystrophy: focus on RNA gain-of-function. Hum. Mol. Genet. 2010, 19:R90-97.
3. Caenepeel S., Charydczak G., Sudarsanam S., Hunter T., Manning G. The mouse kinome: discovery and comparative genomics of all mouse protein kinases. Proc. Natl. Acad. Sci. USA 2004, 101:11707-11712.
4. Manning G., Plowman G.D., Hunter T., Sudarsanam S. Evolution of protein kinase signaling from yeast to man. Trends Biochem. Sci. 2002, 27:514-520.
5. Groenen P.J.T.A., Wansink D.G., Coerwinkel M., van den Broek W., Jansen G., Wieringa B. Constitutive and regulated modes of splicing produce six major myotonic dystrophy protein kinase (DMPK) isoforms with distinct properties. Hum. Mol. Genet. 2000, 9:605-616.
6. Wansink D.G., van Herpen R.E.M.A., Coerwinkel-Driessen M.M., Groenen P.J.T.A., Hemmings B.A., Wieringa B. Alternative splicing controls myotonic dystrophy protein kinase structure, enzymatic activity and subcellular localization. Mol. Cell. Biol. 2003, 23:5489-5501.
7. van Herpen R.E., Oude Ophuis R.J., Wijers M., Bennink M.B., van de Loo F.A., Fransen J., Wieringa B., Wansink D.G. Divergent mitochondrial and endoplasmic reticulum association of DMPK splice isoforms depends on unique sequence arrangements in tail anchors. Mol. Cell. Biol. 2005, 25:1402-1414.
8. Oude Ophuis R.J., Mulders S.A., van Herpen R.E., van de Vorstenbosch R., Wieringa B., Wansink D.G. DMPK protein isoforms are differentially expressed in myogenic and neural cell lineages. Muscle Nerve 2009, 40:545-555.
9. Amano M., Nakayama M., Kaibuchi K. Rho-kinase/ROCK: a key regulator of the cytoskeleton and cell polarity. Cytoskeleton (Hoboken) 2010, 67:545-554.
10. Zhao Z.S., Manser E. PAK and other Rho-associated kinases-effectors with surprisingly diverse mechanisms of regulation. Biochem. J. 2005, 386:201-214.
11. Tan I., Yong J., Dong J.M., Lim L., Leung T. A tripartite complex containing MRCK modulates lamellar actomyosin retrograde flow. Cell 2008, 135:123-136.
12. Pollard T.D., Cooper J.A. Actin, a central player in cell shape and movement. Science 2009, 326:1208-1212.
13. Peckham M. Engineering a multi-nucleated myotube, the role of the actin cytoskeleton. J. Microsc. 2008, 231:486-493.
14. Sparrow J.C., Schock F. The initial steps of myofibril assembly: integrins pave the way. Nat. Rev. Mol. Cell Biol. 2009, 10:293-298.
15. Swailes N.T., Colegrave M., Knight P.J., Peckham M. Non-muscle myosins 2A and 2B drive changes in cell morphology that occur as myoblasts align and fuse. J. Cell Sci. 2006, 119:3561-3570.
16. Epstein H.F., Fischman D.A. Molecular analysis of protein assembly in muscle development. Science 1991, 251:1039-1044.
17. Jansen G., Groenen P.J., Bachner D., Jap P.H., Coerwinkel M., Oerlemans F., van den Broek W., Gohlsch B., Pette D., Plomp J.J., Molenaar P.C., Nederhoff M.G., van Echteld C.J., Dekker M., Berns A., Hameister H., Wieringa B. Abnormal myotonic dystrophy protein kinase levels produce only mild myopathy in mice. Nat. Genet. 1996, 13:316-324.
18. Reddy S., Smith D.B.J., Rich M.M., Leferovich J.M., Reilly P., Davis B.M., Tran K., Rayburn H., Bronson R., Cros D., Balice-Gordon R.J., Housman D. Mice lacking the myotonic dystrophy protein kinase develop a late onset progressive myopathy. Nat. Genet. 1996, 13:325-335.
19. Morgan J.E., Beauchamp J.R., Pagel C.N., Peckham M., Ataliotis P., Jat P.S., Noble M.D., Farmer K., Partridge T.A. Myogenic cell lines derived from transgenic mice carrying a thermolabile T antigen: a model system for the derivation of tissue-specific and mutation-specific cell lines. Dev. Biol. 1994, 162:486-498.
20. Schiedner G., Hertel S., Kochanek S. Efficient transformation of primary human amniocytes by E1 functions of Ad5: generation of new cell lines for adenoviral vector production. Hum. Gene Ther. 2000, 11:2105-2116.
21. Chartier C., Degryse E., Gantzer M., Dieterle A., Pavirani A., Mehtali M. Efficient generation of recombinant adenovirus vectors by homologous recombination in Escherichia coli. J. Virol. 1996, 70:4805-4810.
22. Meberg P.J., Ono S., Minamide L.S., Takahashi M., Bamburg J.R. Actin depolymerizing factor and cofilin phosphorylation dynamics: response to signals that regulate neurite extension. Cell Motil. Cytoskeleton 1998, 39:172-190.
23. Wallimann T., Moser H., Eppenberger H.M. Isoenzyme-specific localization of M-line bound creatine kinase in myogenic cells. J. Muscle Res. Cell Motil. 1983, 4:429-441.
24. Seto M., Sasaki Y., Sasaki Y. Alteration in the myosin phosphorylation pattern of smooth muscle by phorbol ester. Am. J. Physiol. 1990, 259:C769-C774.
25. Talmadge R.J., Roy R.R. Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J. Appl. Physiol. 1993, 75:2337-2340.
26. van Horssen R., Janssen E., Peters W., van de Pasch L., Lindert M.M., van Dommelen M.M., Linssen P.C., Hagen T.L., Fransen J.A., Wieringa B. Modulation of cell motility by spatial repositioning of enzymatic ATP/ADP exchange capacity. J. Biol. Chem. 2009, 284:1620-1627.
27. Totsukawa G., Yamakita Y., Yamashiro S., Hartshorne D.J., Sasaki Y., Matsumura F. Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J. Cell Biol. 2000, 150:797-806.
28. Naumanen P., Lappalainen P., Hotulainen P. Mechanisms of actin stress fibre assembly. J. Microsc. 2008, 231:446-454.
29. Pellegrin S., Mellor H. Actin stress fibres. J. Cell Sci. 2007, 120:3491-3499.
30. Vicente-Manzanares M., Ma X., Adelstein R.S., Horwitz A.R. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 2009, 10:778-790.
31. Langanger G., Moeremans M., Daneels G., Sobieszek A., De Brabander M., De Mey J. The molecular organization of myosin in stress fibers of cultured cells. J. Cell Biol. 1986, 102:200-209.
32. Pollard T.D., Borisy G.G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003, 112:453-465.
33. Vicente-Manzanares M., Horwitz A.R. Myosin light chain mono- and di-phosphorylation differentially regulate adhesion and polarity in migrating cells. Biochem. Biophys. Res. Commun. 2010, 402:537-542.
34. Chamberlain J.S., Jaynes J.B., Hauschka S.D. Regulation of creatine kinase induction in differentiating mouse myoblasts. Mol. Cell. Biol. 1985, 5:484-492.
35. Kitzmann M., Fernandez A. Crosstalk between cell cycle regulators and the myogenic factor MyoD in skeletal myoblasts. Cell Mol. Life. Sci. 2001, 58:571-579.
36. Kitzmann M., Carnac G., Vandromme M., Primig M., Lamb N.J., Fernandez A. The muscle regulatory factors MyoD and myf-5 undergo distinct cell cycle-specific expression in muscle cells. J. Cell Biol. 1998, 142:1447-1459.
37. Pin C.L., Merrifield P.A. Embryonic and fetal rat myoblasts express different phenotypes following differentiation in vitro. Dev. Genet. 1993, 14:356-368.
38. Sutherland C.J., Esser K.A., Elsom V.L., Gordon M.L., Hardeman E.C. Identification of a program of contractile protein gene expression initiated upon skeletal muscle differentiation. Dev. Dyn. 1993, 196:25-36.
39. McGrath M.J., Cottle D.L., Nguyen M.A., Dyson J.M., Coghill I.D., Robinson P.A., Holdsworth M., Cowling B.S., Hardeman E.C., Mitchell C.A., Brown S. Four and a half LIM protein 1 binds myosin-binding protein C and regulates myosin filament formation and sarcomere assembly. J. Biol. Chem. 2006, 281:7666-7683.
40. van Herpen R.E., Tjeertes J.V., Mulders S.A., Oude Ophuis R.J., Wieringa B., Wansink D.G. Coiled-coil interactions modulate multimerization, mitochondrial binding and kinase activity of myotonic dystrophy protein kinase splice isoforms. FEBS J. 2006, 273:1124-1136.
41. Kaliman P., Llagostera E. Myotonic dystrophy protein kinase (DMPK) and its role in the pathogenesis of myotonic dystrophy 1. Cell. Signal. 2008, 20:1935-1941.
42. O'Cochlain D.F., Perez-Terzic C., Reyes S., Kane G.C., Behfar A., Hodgson D.M., Strommen J.A., Liu X.K., van den Broek W., Wansink D.G., Wieringa B., Terzic A. Transgenic overexpression of human DMPK accumulates into hypertrophic cardiomyopathy, myotonic myopathy and hypotension traits of myotonic dystrophy. Hum. Mol. Genet. 2004, 13:2505-2518.
43. Eddinger T.J. Myosin heavy chain isoforms and dynamic contractile properties: skeletal versus smooth muscle. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 1998, 119:425-434.
44. Muranyi A., Zhang R., Liu F., Hirano K., Ito M., Epstein H.F., Hartshorne D.J. Myotonic dystrophy protein kinase phosphorylates the myosin phosphatase targeting subunit and inhibits myosin phosphatase activity. FEBS Lett. 2001, 493:80-84.
45. Matsumura F., Hartshorne D.J. Myosin phosphatase target subunit: many roles in cell function. Biochem. Biophys. Res. Commun. 2008, 369:149-156.
46. Wilkinson S., Paterson H.F., Marshall C.J. Cdc42-MRCK and Rho-ROCK signalling cooperate in myosin phosphorylation and cell invasion. Nat. Cell Biol. 2005, 7:255-261.
47. Follonier Castella L., Buscemi L., Godbout C., Meister J.J., Hinz B. A new lock-step mechanism of matrix remodelling based on subcellular contractile events. J. Cell Sci. 2010, 123:1751-1760.
48. Leung T., Chen X.-Q., Manser E., Lim L. The p160 RhoA-binding kinase ROKα is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol. Cell. Biol. 1996, 16:5313-5327.
49. Amano M., Chihara K., Kimura K., Fukata Y., Nakamura N., Matsuura Y., Kaibuchi K. Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 1997, 275:1308-1311.
50. Ishizaki T., Naito M., Fujisawa K., Maekawa M., Watanabe N., Saito Y., Narumiya S. p160ROCK, a Rho-associated coiled-coil forming protein kinase, works downstream of Rho and induces focal adhesions. FEBS Lett. 1997, 404:118-124.
51. Nakano K., Takaishi K., Kodama A., Mammoto A., Shiozaki H., Monden M., Takai Y. Distinct actions and cooperative roles of ROCK and mDia in Rho small G protein-induced reorganization of the actin cytoskeleton in Madin-Darby canine kidney cells. Mol. Biol. Cell 1999, 10:2481-2491.
52. Yamashiro S., Totsukawa G., Yamakita Y., Sasaki Y., Madaule P., Ishizaki T., Narumiya S., Matsumura F. Citron kinase, a Rho-dependent kinase, induces di-phosphorylation of regulatory light chain of myosin II. Mol. Biol. Cell 2003, 14:1745-1756.
53. Houle F., Rousseau S., Morrice N., Luc M., Mongrain S., Turner C.E., Tanaka S., Moreau P., Huot J. Extracellular signal-regulated kinase mediates phosphorylation of tropomyosin-1 to promote cytoskeleton remodeling in response to oxidative stress: impact on membrane blebbing. Mol. Biol. Cell 2003, 14:1418-1432.
54. Richardson B.E., Nowak S.J., Baylies M.K. Myoblast fusion in fly and vertebrates: new genes, new processes and new perspectives. Traffic 2008, 9:1050-1059.
55. Berendse M., Grounds M.D., Lloyd C.M. Myoblast structure affects subsequent skeletal myotube morphology and sarcomere assembly. Exp. Cell Res. 2003, 291:435-450.
56. Quach N.L., Rando T.A. Focal adhesion kinase is essential for costamerogenesis in cultured skeletal muscle cells. Dev. Biol. 2006, 293:38-52.
57. Duan R., Gallagher P.J. Dependence of myoblast fusion on a cortical actin wall and nonmuscle myosin IIA. Dev. Biol. 2009, 325:374-385.