Protein kinase D2 is an essential regulator of murine myoblast differentiation

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Kleger, Alexander ^a   Loebnitz, Christiane ^a   Pusapati, Ganesh V ^a   Armacki, Milena ^c   ller, Martin Mü ^a   Tümpel, Stefan ^a   Illing, Anett ^a   Hartmann, Daniel ^a,b   Brunner, Cornelia ^a   Liebau, Stefan ^a   Rudolph, Karl L ^a   Adler, Guido ^a   Seufferlein, Thomas ^c  

^a UNIVERSITY OF ULM   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MYOCYTE ENHANCER FACTOR 2; PROTEIN KINASE C; PROTEIN KINASE D; PROTEIN KINASE D1; PROTEIN KINASE D2; PROTEIN KINASE D3; SHORT HAIRPIN RNA; SOMATOMEDIN; SPHINGOSINE 1 PHOSPHATE; TRANSCRIPTION FACTOR PAX3; UNCLASSIFIED DRUG; ISOPROTEIN; PROTEIN KINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FUSION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REPRESSION; IN VITRO STUDY; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SATELLITE CELL; TRANSCRIPTION INITIATION; ANIMAL; CELL CULTURE; CYTOLOGY; GENETICS; MUSCLE; PHOSPHORYLATION; PHYSIOLOGY; REGENERATION; SKELETAL MUSCLE; SKELETAL MUSCLE SATELLITE CELL;

MURINAE;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; MICE; MUSCLE DEVELOPMENT; MUSCLE FIBERS, SKELETAL; MUSCLES; MYOBLASTS; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN KINASES; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 79551512439     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014599     Document Type: Article

References (60)

1. Arnold HH, Braun T (2000) Genetics of muscle determination and development. Curr Top Dev Biol 48: 129-164.
2. Du M, Perry RL, Nowacki NB, Gordon JW, Salma J, et al. (2008) Protein kinase A represses skeletal myogenesis by targeting myocyte enhancer factor 2D. Mol Cell Biol 28: 2952-2970.
3. Nebbioso A, Manzo F, Miceli M, Conte M, Manente L, et al. (2009) Selective class II HDAC inhibitors impair myogenesis by modulating the stability and activity of HDAC-MEF2 complexes. EMBO Rep 10: 776-782.
4. Ohkawa Y, Marfella CG, Imbalzano AN (2006) Skeletal muscle specification by myogenin and Mef2D via the SWI/SNF ATPase Brg1. Embo J 25: 490-501.
5. Olson EN, Perry M, Schulz RA (1995) Regulation of muscle differentiation by the MEF2 family of MADS box transcription factors. Dev Biol 172: 2-14.
6. Molkentin JD, Olson EN (1996) Defining the regulatory networks for muscle development. Curr Opin Genet Dev 6: 445-453.
7. Wang H, Xu Q, Xiao F, Jiang Y, Wu Z (2008) Involvement of the p38 mitogenactivated protein kinase alpha, beta, and gamma isoforms in myogenic differentiation. Mol Biol Cell 19: 1519-1528.
8. Yoon MS, Chen J (2008) PLD regulates myoblast differentiation through the mTOR-IGF2 pathway. J Cell Sci 121: 282-289.
9. Czifra G, Toth IB, Marincsak R, Juhasz I, Kovacs I, et al. (2006) Insulin-like growth factor-I-coupled mitogenic signaling in primary cultured human skeletal muscle cells and in C2C12 myoblasts. A central role of protein kinase Cdelta. Cell Signal 18: 1461-1472.
10. Ramazzotti G, Bavelloni A, Piazzi M, Fiume R, et al. (2010) A role for PKCepsilon during C2C12 myogenic differentiation. Cell Signal 22: 629-635.
11. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S (2002) The protein kinase complement of the human genome. Science 298: 1912-1934.
12. Rykx A, De Kimpe L, Mikhalap S, Vantus T, Seufferlein T, et al. (2003) Protein kinase D: a family affair. FEBS Lett 546: 81-86.
13. Storz P, Doppler H, Toker A (2005) Protein kinase D mediates mitochondrionto- nucleus signaling and detoxification from mitochondrial reactive oxygen species. Mol Cell Biol 25: 8520-8530.
14. von Blume J, Knippschild U, Dequiedt F, Giamas G, Beck A, et al. (2007) Phosphorylation at Ser244 by CK1 determines nuclear localization and substrate targeting of PKD2. Embo J 26: 4619-4633.
15. Waldron RT, Rey O, Iglesias T, Tugal T, Cantrell D, et al. (2001) Activation loop Ser744 and Ser748 in protein kinase D are transphosphorylated in vivo. J Biol Chem 276: 32606-32615.
16. Zugaza JL, Sinnett-Smith J, Van Lint J, Rozengurt E (1996) Protein kinase D (PKD) activation in intact cells through a protein kinase C-dependent signal transduction pathway. Embo J 15: 6220-6230.
17. Baron CL, Malhotra V (2002) Role of diacylglycerol in PKD recruitment to the TGN and protein transport to the plasma membrane. Science 295: 325-328.
18. Eiseler T, Doppler H, Yan IK, Kitatani K, Mizuno K, et al. (2009) Protein kinase D1 regulates cofilin-mediated F-actin reorganization and cell motility through slingshot. Nat Cell Biol 11: 545-556.
19. Prigozhina NL, Waterman-Storer CM (2004) Protein kinase D-mediated anterograde membrane trafficking is required for fibroblast motility. Curr Biol 14: 88-98.
20. von Wichert G, Edenfeld T, von Blume J, Krisp H, Krndija D, et al. (2008) Protein kinase D2 regulates chromogranin A secretion in human BON neuroendocrine tumour cells. Cell Signal 20: 925-934.
21. Yeaman C, Ayala MI, Wright JR, Bard F, Bossard C, et al. (2004) Protein kinase D regulates basolateral membrane protein exit from trans-Golgi network. Nat Cell Biol 6: 106-112.
22. Fielitz J, Kim MS, Shelton JM, Qi X, Hill JA, et al. (2008) Requirement of protein kinase D1 for pathological cardiac remodeling. Proc Natl Acad Sci U S A 105: 3059-3063.
23. Kim M, Jang HR, Kim JH, Noh SM, Song KS, et al. (2008) Epigenetic inactivation of protein kinase D1 in gastric cancer and its role in gastric cancer cell migration and invasion. Carcinogenesis 29: 629-637.
24. Geng J, Zhao Z, Kang W, Wang W, Liu G, et al. (2009) Hypertrophic response to angiotensin II is mediated by protein kinase D-extracellular signal-regulated kinase 5 pathway in human aortic smooth muscle cells. Biochem Biophys Res Commun 388: 517-522.
25. Yaffe D, Saxel O (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270: 725-727.
26. Oster H, Abraham D, Leitges M (2006) Expression of the protein kinase D (PKD) family during mouse embryogenesis. Gene Expr Patterns 6: 400-408.
27. Fanzani A, Colombo F, Giuliani R, Preti A, Marchesini S (2006) Insulin-like growth factor 1 signaling regulates cytosolic sialidase Neu2 expression during myoblast differentiation and hypertrophy. Febs J 273: 3709-3721.
28. Gentile MA, Nantermet PV, Vogel RL, Phillips R, Holder D, et al. Androgenmediated improvement of body composition and muscle function involves a novel early transcriptional program including IGF1, mechano growth factor, and induction of {beta}-catenin. J Mol Endocrinol 44: 55-73.
29. Prelle K, Wobus AM, Krebs O, Blum WF, Wolf E (2000) Overexpression of insulin- like growth factor-II in mouse embryonic stem cells promotes myogenic differentiation. Biochem Biophys Res Commun 277: 631-638.
30. Qiang YW, Yao L, Tosato G, Rudikoff S (2004) Insulin-like growth factor I induces migration and invasion of human multiple myeloma cells. Blood 103: 301-308.
31. Donati C, Meacci E, Nuti F, Becciolini L, Farnararo M, et al. (2005) Sphingosine 1-phosphate regulates myogenic differentiation: a major role for S1P2 receptor. Faseb J 19: 449-451.
32. Cencetti F, Bernacchioni C, Nincheri P, Donati C, Bruni P Transforming growth factor-beta1 induces transdifferentiation of myoblasts into myofibroblasts via up-regulation of sphingosine kinase-1/S1P3 axis. Mol Biol Cell 21: 1111-1124.
33. Meacci E, Nuti F, Donati C, Cencetti F, Farnararo M, et al. (2008) Sphingosine kinase activity is required for myogenic differentiation of C2C12 myoblasts. J Cell Physiol 214: 210-220.
34. Gschwendt M, Dieterich S, Rennecke J, Kittstein W, Mueller HJ, et al. (1996) Inhibition of protein kinase C mu by various inhibitors. Differentiation from protein kinase c isoenzymes. FEBS Lett 392: 77-80.
35. Halevy O, Piestun Y, Allouh MZ, Rosser BW, Rinkevich Y, et al. (2004) Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev Dyn 231: 489-502.
36. Zammit PS, Relaix F, Nagata Y, Ruiz AP, Collins CA, et al. (2006) Pax7 and myogenic progression in skeletal muscle satellite cells. J Cell Sci 119: 1824-1832.
37. Diel P, Baadners D, Schlupmann K, Velders M, Schwarz JP (2008) C2C12 myoblastoma cell differentiation and proliferation is stimulated by androgens and associated with a modulation of myostatin and Pax7 expression. J Mol Endocrinol 40: 231-241.
38. Olguin HC, Olwin BB (2004) Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev Biol 275: 375-388.
39. Zhu S, Goldschmidt-Clermont PJ, Dong C (2004) Transforming growth factorbeta- induced inhibition of myogenesis is mediated through Smad pathway and is modulated by microtubule dynamic stability. Circ Res 94: 617-625.
40. Zhukova E, Sinnett-Smith J, Wong H, Chiu T, Rozengurt E (2001) CCK(B)/ gastrin receptor mediates synergistic stimulation of DNA synthesis and cyclin D1, D3, and E expression in Swiss 3T3 cells. J Cell Physiol 189: 291-305.
41. Cerletti M, Jurga S, Witczak CA, Hirshman MF, Shadrach JL, et al. (2008) Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 134: 37-47.
42. Collins CA, Gnocchi VF, White RB, Boldrin L, Perez-Ruiz A, et al. (2009) Integrated functions of Pax3 and Pax7 in the regulation of proliferation, cell size and myogenic differentiation. PLoS One 4: e4475.
43. Epstein JA, Lam P, Jepeal L, Maas RL, Shapiro DN (1995) Pax3 inhibits myogenic differentiation of cultured myoblast cells. J Biol Chem 270: 11719-11722.
44. Young AP, Wagers AJ Pax3 induces differentiation of juvenile skeletal muscle stem cells without transcriptional upregulation of canonical myogenic regulatory factors. J Cell Sci.
45. Faenza I, Ramazzotti G, Bavelloni A, Fiume R, Gaboardi GC, et al. (2007) Inositide-dependent phospholipase C signaling mimics insulin in skeletal muscle differentiation by affecting specific regions of the cyclin D3 promoter. Endocrinology 148: 1108-1117.
46. Lee SJ, Lee YH, Kim YS, Ryu SH, Suh PG (1995) Transcriptional regulation of phospholipase C-gamma 1 gene during muscle differentiation. Biochem Biophys Res Commun 206: 194-200.
47. Mirandola P, Gobbi G, Ponti C, Sponzilli I, Cocco L, et al. (2006) PKCepsilon controls protection against TRAIL in erythroid progenitors. Blood 107: 508-513.
48. Sturany S, Van Lint J, Muller F, Wilda M, Hameister H, et al. (2001) Molecular cloning and characterization of the human protein kinase D2. A novel memberof the protein kinase D family of serine threonine kinases. J Biol Chem 276: 3310-3318.
49. Van Lint J, Rykx A, Maeda Y, Vantus T, Sturany S, et al. (2002) P rotein kinaseD: an intracellular traffic regulator on the move. Trends Cell Biol 12: 193-200.
50. Bassel-Duby R, Olson EN (2006) Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 75: 19-37.
51. Braun T, Arnold HH (1996) Myf-5 and myoD genes are activated in distinct mesenchymal stem cells and determine different skeletal muscle cell lineages. Embo J 15: 310-318.
52. Liljedahl M, Maeda Y, Colanzi A, Ayala I, Van Lint J, et al. (2001) Protein kinase D regulates the fission of cell surface destined transport carriers from the trans-Golgi network. Cell 104: 409-420.
53. Pusapati GV, Krndija D, Armacki M, von Wichert G, von Blume J, et al. (2010) Role of the Second Cysteine-rich Domain and Pro275 in PKD2 Interaction with ARF1, TGN Recruitment and Protein Transport. Mol Biol Cell 21: 1011-1022.
54. Jamora C, Yamanouye N, Van Lint J, Laudenslager J, Vandenheede JR, et al. (1999) Gbetagamma-mediated regulation of Golgi organization is through the direct activation of protein kinase D. Cell 98: 59-68.
55. Sturany S, Van Lint J, Gilchrist A, Vandenheede JR, Adler G, et al. (2002) Mechanism of activation of protein kinase D2(PKD2) by the CCK(B)/gastrin receptor. J Biol Chem 277: 29431-29436.
56. Naidu PS, Ludolph DC, To RQ, Hinterberger TJ, Konieczny SF (1995) Myogenin and MEF2 function synergistically to activate the MRF4 promoter during myogenesis. Mol Cell Biol 15: 2707-2718.
57. Kuisk IR, Li H, Tran D, Capetanaki Y (1996) A single MEF2 site governs desmin transcription in both heart and skeletal muscle during mouse embryogenesis. Dev Biol 174: 1-13.
58. Young AP, Wagers AJ (2010) Pax3 induces differentiation of juvenile skeletal muscle stem cells without transcriptional upregulation of canonical myogenic regulatory factors. J Cell Sci 123: 2632-2639.
59. Kleger A, Busch T, Liebau S, Prelle K, Paschke S, et al. (2007) The bioactive lipid sphingosylphosphorylcholine induces differentiation of mouse embryonic stem cells and human promyelocytic leukaemia cells. Cell Signal 19: 367-377.
60. Auer A, von Blume J, Sturany S, von Wichert G, Van Lint J, et al. (2005) Role of the regulatory domain of protein kinase D2 in phorbol ester binding, catalytic activity, and nucleocytoplasmic shuttling. Mol Biol Cell 16: 4375-4385.