Dorsomorphin stimulates neurite outgrowth in PC12 cells via activation of a protein kinase A-dependent MEK-ERK1/2 signaling pathway

Genes to Cells

Volumn 16, Issue 11, 2011, Pages 1121-1132

  Kudo, Tada Aki ^a   Kanetaka, Hiroyasu ^a   Mizuno, Kazutoshi ^a   Ryu, Yasuhiro ^a   Miyamoto, Yoshiyuki ^a   Nunome, Shoko ^a   Zhang, Ye ^a   Kano, Mitsuhiro ^a   Shimizu, Yoshinaka ^a   Hayashi, Haruhide ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; BONE MORPHOGENETIC PROTEIN 2; CYCLIC AMP DEPENDENT PROTEIN KINASE; DORSOMORPHIN; GW 441756; LDL 193189; LDN 193189; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; NERVE GROWTH FACTOR; PHOSPHOTRANSFERASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEURITE; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; BUTADIENES; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION, DEVELOPMENTAL; ISOQUINOLINES; MAP KINASE KINASE KINASES; MAP KINASE SIGNALING SYSTEM; NEURITES; NITRILES; PC12 CELLS; PROTEIN KINASES; PYRAZOLES; PYRIMIDINES; RATS; SIGNAL TRANSDUCTION; SULFONAMIDES; TRANSCRIPTIONAL ACTIVATION;

RATTUS;

EID: 80054954520     PISSN: 13569597     EISSN: 13652443     Source Type: Journal    
DOI: 10.1111/j.1365-2443.2011.01556.x     Document Type: Article

References (51)

1. Ahn, N.G. & Tolwinski, N.S. (1999) U0126: an inhibitor of MKK/ERK signal transduction in mammalian cells. Promega Notes 71, 4-8.
2. Boergermann, J.H., Kopf, J., Yu, P.B. & Knaus, P. (2010) Dorsomorphin and LDN-193189 inhibit BMP-mediated Smad, p38 and Akt signalling in C2C12 cells. Int. J. Biochem. Cell Biol. 42, 1802-1807.
3. Burry, R.W. (2001) p21(ras) stimulates pathways in addition to ERK, p38, and Akt to induce elongation of neurites in PC12 cells. J. Neurosci. Res. 63, 45-53.
4. Charles, M.P., Adamski, D., Kholler, B., Pelletier, L., Berger, F. & Wion, D. (2003) Induction of neurite outgrowth in PC12 cells by the bacterial nucleoside N6-methyldeoxyadenosine is mediated through adenosine A2a receptors and via cAMP and MAPK signaling pathways. Biochem. Biophys. Res. Commun. 304, 795-800.
5. Cuny, G.D., Yu, P.B., Laha, J.K., Xing, X., Liu, J.F., Lai, C.S., Deng, D.Y., Sachidanandan, C., Bloch, K.D. & Peterson, R.T. (2008) Structure-activity relationship study of bone morphogenetic protein (BMP) signaling inhibitors. Bioorg. Med. Chem. Lett. 18, 4388-4392.
6. Deutsch, P.J. & Sun, Y. (1992) The 38-amino acid form of pituitary adenylate cyclase-activating polypeptide stimulates dual signaling cascades in PC12 cells and promotes neurite outgrowth. J. Biol. Chem. 267, 5108-5113.
7. Evangelopoulos, M.E., Weis, J. & Krüttgen, A. (2009) Mevastatin-induced neurite outgrowth of neuroblastoma cells via activation of EGFR. J. Neurosci. Res. 87, 2138-2144.
8. Freeland, K., Liu, Y.Z. & Latchman, D.S. (2000) Distinct signalling pathways mediate the cAMP response element (CRE)-dependent activation of the calcitonin gene-related peptide gene promoter by cAMP and nerve growth factor. Biochem. J. 345, 233-238.
9. Frödin, M., Peraldi, P. & Van Obberghen, E. (1994) Cyclic AMP activates the mitogen-activated protein kinase cascade in PC12 cells. J. Biol. Chem. 269, 6207-6214.
10. Ghayor, C., Ehrbar, M., San Miguel, B., Gratz, K.W. & Weber, F.E. (2009) cAMP enhances BMP2-signaling through PKA and MKP1-dependent mechanisms. Biochem. Biophys. Res. Commun. 381, 247-252.
11. Greene, L.A. & Tischler, A.S. (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl Acad. Sci. USA 73, 2424-2428.
12. Grewal, S.S., Fass, D.M., Yao, H., Ellig, C.L., Goodman, R.H. & Stork, P.J. (2000) Calcium and cAMP signals differentially regulate cAMP-responsive element-binding protein function via a Rap1-extracellular signal-regulated kinase pathway. J. Biol. Chem. 275, 34433-34441.
13. Hansen, T.O., Rehfeld, J.F. & Nielsen, F.C. (2003) KCl potentiates forskolin-induced PC12 cell neurite outgrowth via protein kinase A and extracellular signal-regulated kinase signaling pathways. Neurosci. Lett. 347, 57-61.
14. Hao, J., Daleo, M.A., Murphy, C.K., Yu, P.B., Ho, J.N., Hu, J., Peterson, R.T., Hatzopoulos, A.K. & Hong, C.C. (2008) Dorsomorphin, a selective small molecule inhibitor of BMP signaling, promotes cardiomyogenesis in embryonic stem cells. PLoS ONE 3, e2904.
15. Hao, J., Ho, J.N., Lewis, J.A., Karim, K.A., Daniels, R.N., Gentry, P.R., Hopkins, C.R., Lindsley, C.W. & Hong, C.C. (2010) In vivo structure-activity relationship study of dorsomorphin analogues identifies selective VEGF and BMP inhibitors. ACS Chem. Biol. 5, 245-253.
16. Hayashi, H., Ishisaki, A., Suzuki, M. & Imamura, T. (2001) BMP-2 augments FGF-induced differentiation of PC12 cells through upregulation of FGF receptor-1 expression. J. Cell Sci. 114, 1387-1395.
17. Heldin, C.H., Miyazono, K. & ten Dijke, P. (1997) TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390, 465-471.
18. Hogan, B.L. (1996) Bone morphogenetic proteins in development. Curr. Opin. Genet. Dev. 6, 432-438.
19. Iwasaki, S., Hattori, A., Sato, M., Tsujimoto, M. & Kohno, M. (1996) Characterization of the bone morphogenetic protein-2 as a neurotrophic factor. Induction of neuronal differentiation of PC12 cells in the absence of mitogen-activated protein kinase activation. J. Biol. Chem. 271, 17360-17365.
20. Iwasaki, S., Iguchi, M., Watanabe, K., Hoshino, R., Tsujimoto, M. & Kohno, M. (1999) Specific activation of the p38 mitogen-activated protein kinase signaling pathway and induction of neurite outgrowth in PC12 cells by bone morphogenetic protein-2. J. Biol. Chem. 274, 26503-26510.
21. Jung, E.J., Kim, C.W. & Kim, D.R. (2008) Cytosolic accumulation of gammaH2AX is associated with tropomyosin-related kinase A-induced cell death in U2OS cells. Exp. Mol. Med. 40, 276-285.
22. Kao, S., Jaiswal, R.K., Kolch, W. & Landreth, G.E. (2001) Identification of the mechanisms regulating the differential activation of the MAPK cascade by epidermal growth factor and nerve growth factor in PC12 cells. J. Biol. Chem. 276, 18169-18177.
23. Kim, D.S., Lee, J.S., Leem, J.W., Huh, Y.J., Kim, J.Y., Kim, H.S., Park, I.H., Daley, G.Q., Hwang, D.Y. & Kim, D.W. (2010) Robust enhancement of neural differentiation from human ES and iPS cells regardless of their innate difference in differentiation propensity. Stem Cell Rev. 6, 270-281.
24. Kimura, N., Matsuo, R., Shibuya, H., Nakashima, K. & Taga, T. (2000) BMP2-induced apoptosis is mediated by activation of the TAK1-p38 kinase pathway that is negatively regulated by Smad6. J. Biol. Chem. 275, 17647-17652.
25. Koike, T., Uno, S., Ishizawa, M., Takahashi, H., Ikeda, K., Yokota, S. & Makishima, M. (2006) The heat shock protein inhibitor KNK437 induces neurite outgrowth in PC12 cells. Neurosci. Lett. 410, 212-217.
26. Lazarovici, P., Jiang, H. & Fink, D. Jr (1998) The 38-amino-acid form of pituitary adenylate cyclase-activating polypeptide induces neurite outgrowth in PC12 cells that is dependent on protein kinase C and extracellular signal-regulated kinase but not on protein kinase A, nerve growth factor receptor tyrosine kinase, p21(ras) G protein, and pp60(c-src) cytoplasmic tyrosine kinase. Mol. Pharmacol. 54, 547-558.
27. Lin, C.W., Wu, M.J., Liu, I.Y., Su, J.D. & Yen, J.H. (2010) Neurotrophic and cytoprotective action of luteolin in PC12 cells through ERK-dependent induction of Nrf2-driven HO-1 expression. J. Agric. Food. Chem. 58, 4477-4486.
28. Marshall, C.J. (1998) Signal transduction. Taking the Rap. Nature 392, 553-554.
29. Obara, Y., Labudda, K., Dillon, T.J. & Stork, P.J. (2004) PKA phosphorylation of Src mediates Rap1 activation in NGF and cAMP signaling in PC12 cells. J. Cell Sci. 117, 6085-6094.
30. Pang, L., Sawada, T., Decker, S.J. & Saltiel, A.R. (1995) Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J. Biol. Chem. 270, 13585-13588.
31. Radio, N.M., Breier, J.M., Shafer, T.J. & Mundy, W.R. (2008) Assessment of chemical effects on neurite outgrowth in PC12 cells using high content screening. Toxicol. Sci. 105, 106-118.
32. Radio, N.M. & Mundy, W.R. (2008) Developmental neurotoxicity testing in vitro: models for assessing chemical effects on neurite outgrowth. Neurotoxicology 29, 361-376.
33. Rakhit, S., Pyne, S. & Pyne, N.J. (2001) Nerve growth factor stimulation of p42/p44 mitogen-activated protein kinase in PC12 cells: role of G(i/o), G protein-coupled receptor kinase 2, beta-arrestin I, and endocytic processing. Mol. Pharmacol. 60, 63-70.
34. Rydel, R.E. & Greene, L.A. (1987) Acidic and basic fibroblast growth factors promote stable neurite outgrowth and neuronal differentiation in cultures of PC12 cells. J. Neurosci. 7, 3639-3653.
35. Segal, R.A., Bhattacharyya, A., Rua, L.A., Alberta, J.A., Stephens, R.M., Kaplan, D.R. & Stiles, C.D. (1996) Differential utilization of Trk autophosphorylation sites. J. Biol. Chem. 271, 20175-20181.
36. Shinomiya, N. & Shinomiya, M. (2003) Dichlorodiphenyltrichloroethane suppresses neurite outgrowth and induces apoptosis in PC12 pheochromocytoma cells. Toxicol. Lett. 137, 175-183.
37. Stork, P.J. & Schmitt, J.M. (2002) Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol. 12, 258-266.
38. Tamura, H. & Ohkuma, S. (1991) Induction of neurite outgrowth of PC12 cells by an inhibitor of vacuolar H(+)-ATPase, bafilomycin A1. FEBS Lett. 294, 51-55.
39. Taylor, S.S., Buechler, J.A. & Yonemoto, W. (1990) cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu. Rev. Biochem. 59, 971-1005.
40. Tsuji, M., Inanami, O. & Kuwabara, M. (2001) Induction of neurite outgrowth in PC12 cells by alpha-phenyl-N-tert-butylnitron through activation of protein kinase C and the Ras-extracellular signal-regulated kinase pathway. J. Biol. Chem. 276, 32779-32785.
41. Vaudry, D., Stork, P.J., Lazarovici, P. & Eiden, L.E. (2002) Signaling pathways for PC12 cell differentiation: making the right connections. Science 296, 1648-1649.
42. Vossler, M.R., Yao, H., York, R.D., Pan, M.G., Rim, C.S. & Stork, P.J. (1997) cAMP activates MAP kinase and Elk-1 through a B-Raf- and Rap1-dependent pathway. Cell 89, 73-82.
43. Wrana, J.L., Attisano, L., Wieser, R., Ventura, F. & Massague, J. (1994) Mechanism of activation of the TGF-beta receptor. Nature 370, 341-347.
44. Yanagisawa, M., Nakashima, K., Takeda, K., Ochiai, W., Takizawa, T., Ueno, M., Takizawa, M., Shibuya, H. & Taga, T. (2001) Inhibition of BMP2-induced, TAK1 kinase-mediated neurite outgrowth by Smad6 and Smad7. Genes Cells 6, 1091-1099.
45. Yang, Y.J., Lee, H.J., Choi, D.H., Huang, H.S., Lim, S.C. & Lee, M.K. (2008) Effect of scoparone on neurite outgrowth in PC12 cells. Neurosci. Lett. 440, 14-18.
46. Yao, H., York, R.D., Misra-Press, A., Carr, D.W. & Stork, P.J. (1998) The cyclic adenosine monophosphate-dependent protein kinase (PKA) is required for the sustained activation of mitogen-activated kinases and gene expression by nerve growth factor. J. Biol. Chem. 273, 8240-8247.
47. Yasui, H., Ito, N., Yamamori, T., Nakamura, H., Okano, J., Asanuma, T., Nakajima, T., Kuwabara, M. & Inanami, O. (2010) Induction of neurite outgrowth by alpha-phenyl-N-tert-butylnitrone through nitric oxide release and Ras-ERK pathway in PC12 cells. Free Radic. Res. 44, 645-654.
48. Yu, P.B., Deng, D.Y., Lai, C.S., Hong, C.C., Cuny, G.D., Bouxsein, M.L., Hong, D.W., McManus, P.M., Katagiri, T., Sachidanandan, C., Kamiya, N., Fukuda, T., Mishina, Y., Peterson, R.T. & Bloch, K.D. (2008a) BMP type I receptor inhibition reduces heterotopic [corrected] ossification. Nat. Med. 14, 1363-1369.
49. Yu, P.B., Hong, C.C., Sachidanandan, C., Babitt, J.L., Deng, D.Y., Hoyng, S.A., Lin, H.Y., Bloch, K.D. & Peterson, R.T. (2008b) Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat. Chem. Biol. 4, 33-41.
50. Yung, L.Y., Tso, P.H., Wu, E.H., Yu, J.C., Ip, N.Y. & Wong, Y.H. (2008) Nerve growth factor-induced stimulation of p38 mitogen-activated protein kinase in PC12 cells is partially mediated via G(i/o) proteins. Cell. Signal. 20, 1538-1544.
51. Zhou, G., Myers, R., Li, Y., Chen, Y., Shen, X., Fenyk-Melody, J., Wu, M., Ventre, J., Doebber, T., Fujii, N., Musi, N., Hirshman, M.F., Goodyear, L.J. & Moller, D.E. (2001) Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest. 108, 1167-1174.