DUSP4 regulates neuronal differentiation and calcium homeostasis by modulating ERK1/2 phosphorylation

Stem Cells and Development

Volumn 24, Issue 6, 2015, Pages 686-700

  Kim, Sun Young ^a,b   Han, Yong Mahn ^a   Oh, Mihee ^b   Kim, Won Kon ^b   Oh, Kyoung Jin ^b   Lee, Sang Chul ^b,c   Bae, Kwang Hee ^b,c   Han, Baek Soo ^b,c  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^c University of Science and Technology (UST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE I; CALCIUM ION; DUAL SPECIFICITY PHOSPHATASE 4; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATASE; UNCLASSIFIED DRUG; CACNA1C PROTEIN, MOUSE; CALCIUM CHANNEL L TYPE; MKP2 PROTEIN, MOUSE; PROTEIN TYROSINE PHOSPHATASE;

ANIMAL CELL; ARTICLE; CALCIUM BALANCE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CELL FUNCTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE SILENCING; IN VITRO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEUROMODULATION; NEURULATION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; GENETICS; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; PHOSPHORYLATION;

ANIMALS; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; CELLS, CULTURED; EMBRYONIC STEM CELLS; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASES;

EID: 84924365613     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0434     Document Type: Article

References (56)

1. Arregui CO, J Balsamo and J Lilien. (2000). Regulation of signaling by protein-tyrosine phosphatases: potential roles in the nervous system. Neurochem Res 25:95-105.
2. Paul S and PJ Lombroso. (2003). Receptor and nonreceptor protein tyrosine phosphatases in the nervous system. Cell Mol Life Sci 60:2465-2482.
3. Keyse SM. (1995). An emerging family of dual specificity MAP kinase phosphatases. Biochim Biophys Acta 1265: 152-160.
4. Chu Y, PA Solski, R Khosravi-Far, CJ Der and K Kelly. (1996). The mitogen-activated protein kinase phosphatases PAC1, MKP-1, and MKP-2 have unique substrate specificities and reduced activity in vivo toward the ERK2 sevenmaker mutation. J Biol Chem 271:6497-6501.
5. Guan KL and E Butch. (1995). Isolation and characterization of a novel dual specific phosphatase, HVH2, which selectively dephosphorylates the mitogen-activated protein kinase. J Biol Chem 270:7197-7203.
6. Cadalbert L, CM Sloss, P Cameron and R Plevin. (2005). Conditional expression of MAP kinase phosphatase-2 protects against genotoxic stress-induced apoptosis by binding and selective dephosphorylation of nuclear activated c-jun N-terminal kinase. Cell Signal 17:1254-1264.
7. Berasi SP, C Huard, D Li, HH Shih, Y Sun, W Zhong, JE Paulsen, EL Brown, RE Gimeno and RV Martinez. (2006). Inhibition of gluconeogenesis through transcriptional activation of EGR1 and DUSP4 by AMP-activated kinase. J Biol Chem 281:27167-27177.
8. Hasegawa T, A Enomoto, T Kato, K Kawai, R Miyamoto, M Jijiwa, M Ichihara, M Ishida, N Asai, et al. (2008). Roles of induced expression of MAPK phosphatase-2 in tumor development in RET-MEN2A transgenic mice. Oncogene 27:5684-5695.
9. Sieben NL, J Oosting, AM Flanagan, J Prat, GM Roemen, SM Kolkman-Uljee, R van Eijk, CJ Cornelisse, GJ Fleuren and M van Engeland. (2005). Differential gene expression in ovarian tumors reveals Dusp 4 and Serpina 5 as key regulators for benign behavior of serous borderline tumors. J Clin Oncol 23:7257-7264.
10. Wang H, Y Lu, W Huang, ET Papoutsakis, P Fuhrken and EA Eklund. (2007). HoxA10 activates transcription of the gene encoding mitogen-activated protein kinase phosphatase 2 (Mkp2) in myeloid cells. J Biol Chem 282:16164-16176.
11. Venter DJ, SJ Ramus, FM Hammet, M de Silva, AM Hutchins, V Petrovic, G Price and JE Armes. (2005). Complex CGH alterations on chromosome arm 8p at candidate tumor suppressor gene loci in breast cancer cell lines. Cancer Genet Cytogenet 160:134-140.
12. Brown JL, M Snir, H Noushmehr, M Kirby, SK Hong, AG Elkahloun and B Feldman. (2008). Transcriptional profiling of endogenous germ layer precursor cells identifies dusp4 as an essential gene in zebrafish endoderm specification. Proc Natl Acad Sci U S A 105:12337-12342.
13. Liu Y, M Asakura, H Inoue, T Nakamura, M Sano, Z Niu, M Chen, RJ Schwartz and MD Schneider. (2007). Sox17 is essential for the specification of cardiac mesoderm in embryonic stem cells. Proc Natl Acad Sci U S A 104:3859-3864.
14. Torres C, MK Francis, A Lorenzini, M Tresini and VJ Cristofalo. (2003). Metabolic stabilization of MAP kinase phosphatase-2 in senescence of human fibroblasts. Exp Cell Res 290:195-206.
15. Shen WH, J Wang, J Wu, VB Zhurkin and Y Yin. (2006). Mitogen-activated protein kinase phosphatase 2: a novel transcription target of p53 in apoptosis. Cancer Res 66:6033-6039.
16. Rosenberg SS and NC Spitzer. (2011). Calcium signaling in neuronal development. Cold Spring Harb Perspect Biol 3:a004259.
17. Gomez TM and JQ Zheng. (2006). The molecular basis for calcium-dependent axon pathfinding. Nat Rev Neurosci 7:115-125.
18. Kater SB, MP Mattson, C Cohan and J Connor. (1988). Calcium regulation of the neuronal growth cone. Trends Neurosci 11:315-321.
19. D'Ascenzo M, R Piacentini, P Casalbore, M Budoni, R Pallini, GB Azzena and C Grassi. (2006). Role of L-type Ca2 + channels in neural stem/progenitor cell differentiation. Eur J Neurosci 23:935-944.
20. Soderling TR and JT Stull. (2001). Structure and regulation of calcium/calmodulin-dependent protein kinases. Chem Rev 101:2341-2352.
21. Wayman GA, S Kaech, WF Grant, M Davare, S Impey, H Tokumitsu, N Nozaki, G Banker and TR Soderling. (2004). Regulation of axonal extension and growth cone motility by calmodulin-dependent protein kinase I. J Neurosci 24: 3786-3794.
22. Kasahara J, K Fukunaga and E Miyamoto. (2000). Activation of CA(2+)/calmodulin-dependent protein kinase IV in cultured rat hippocampal neurons. J Neurosci Res 59: 594-600.
23. Schmitt JM, GA Wayman, N Nozaki and TR Soderling. (2004). Calcium activation of ERK mediated by calmodulin kinase I. J Biol Chem 279:24064-24072.
24. Wayman GA, S Impey, D Marks, T Saneyoshi, WF Grant, V Derkach and TR Soderling. (2006). Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 50:897-909.
25. Malmersjo S, I Liste, O Dyachok, A Tengholm, E Arenas and P Uhlen. (2010). Ca2 + and cAMP signaling in human embryonic stem cell-derived dopamine neurons. Stem Cells Dev 19:1355-1364.
26. Deisseroth K, S Singla, H Toda, M Monje, TD Palmer and RC Malenka. (2004). Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42:535-552.
27. Bibel M, J Richter, E Lacroix and YA Barde. (2007). Generation of a defined and uniform population of CNS progenitors and neurons from mouse embryonic stem cells. Nat Protoc 2:1034-1043.
28. Milosevic J, P Bulau, E Mortz and O Eickelberg. (2009). Subcellular fractionation of TGF-beta1-stimulated lung epithelial cells: a novel proteomic approach for identifying signaling intermediates. Proteomics 9:1230-1240.
29. Zhong D, X Liu, FR Khuri, SY Sun, PM Vertino and W Zhou. (2008). LKB1 is necessary for Akt-mediated phosphorylation of proapoptotic proteins. Cancer Res 68:7270-7277.
30. Levy S, O Beharier, Y Etzion, M Mor, L Buzaglo, L Shaltiel, LA Gheber, J Kahn, AJ Muslin, et al. (2009). Molecular basis for zinc transporter 1 action as an endogenous inhibitor of L-type calcium channels. J Biol Chem 284:32434-32443.
31. Chen P, D Hutter, X Yang, M Gorospe, RJ Davis and Y Liu. (2001). Discordance between the binding affinity of mitogen-activated protein kinase subfamily members for MAP kinase phosphatase-2 and their ability to activate the phosphatase catalytically. J Biol Chem 276:29440-29449.
32. Bluthgen N, S Legewie, SM Kielbasa, A Schramme, O Tchernitsa, J Keil, A Solf, M Vingron, R Schafer, H Herzel and C Sers. (2009). A systems biological approach suggests that transcriptional feedback regulation by dual-specificity phosphatase 6 shapes extracellular signal-related kinase activity in RAS-transformed fibroblasts. FEBS J 276:1024-1035.
33. Naito Y, Y Watanabe, H Yokokura, R Sugita, M Nishio and H Hidaka. (1997). Isoform-specific activation and structural diversity of calmodulin kinase I. J Biol Chem 272:32704-32708.
34. Uboha NV, M Flajolet, AC Nairn and MR Picciotto. (2007). A calcium- and calmodulin-dependent kinase Ialpha/microtubule affinity regulating kinase 2 signaling cascade mediates calcium-dependent neurite outgrowth. J Neurosci 27:4413-4423.
35. Zhang T, MW Wolfe and MS Roberson. (2001). An early growth response protein (Egr) 1 cis-element is required for gonadotropin-releasing hormone-induced mitogenactivated protein kinase phosphatase 2 gene expression. J Biol Chem 276:45604-45613.
36. Tonks NK. (2006). Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 7: 833-846.
37. Finelli MJ, KJ Murphy, L Chen and H Zou. (2013). Differential phosphorylation of Smad1 integrates BMP and neurotrophin pathways through Erk/Dusp in axon development. Cell Rep 3:1592-1606.
38. Jeanneteau F, K Deinhardt, G Miyoshi, AM Bennett and MV Chao. (2010). The MAP kinase phosphatase MKP-1 regulates BDNF-induced axon branching. Nat Neurosci 13:1373-1379.
39. Misra-Press A, CS Rim, H Yao, MS Roberson and PJ Stork. (1995). A novel mitogen-activated protein kinase phosphatase. Structure, expression, and regulation. J Biol Chem 270:14587-14596.
40. Shaul YD and R Seger. (2007). The MEK/ERK cascade: from signaling specificity to diverse functions. Biochim Biophys Acta 1773:1213-1226.
41. Peng DJ, JY Zhou and GS Wu. (2010). Post-translational regulation of mitogen-activated protein kinase phosphatase-2 (MKP-2) by ERK. Cell Cycle 9:4650-4655.
42. Ulrich H and P Majumder. (2006). Neurotransmitter receptor expression and activity during neuronal differentiation of embryonal carcinoma and stem cells: from basic research towards clinical applications. Cell Prolif 39:281-300.
43. Bito H, K Deisseroth and RW Tsien. (1997). Ca2 + -dependent regulation in neuronal gene expression. Curr Opin Neurobiol 7:419-429.
44. Grassi C, M D'Ascenzo, A Torsello, G Martinotti, F Wolf, A Cittadini and GB Azzena. (2004). Effects of 50 Hz electromagnetic fields on voltage-gated Ca2 + channels and their role in modulation of neuroendocrine cell proliferation and death. Cell Calcium 35:307-315.
45. Spitzer NC, X Gu and E Olson. (1994). Action potentials, calcium transients and the control of differentiation of excitable cells. Curr Opin Neurobiol 4:70-77.
46. Mor M, O Beharier, S Levy, J Kahn, S Dror, D Blumenthal, LA Gheber, A Peretz, A Katz, A Moran and Y Etzion. (2012). ZnT-1 enhances the activity and surface expression of T-type calcium channels through activation of Ras-ERK signaling. Am J Physiol Cell Physiol 303:C192-C203.
47. Woodall AJ, MA Richards, DJ Turner and EM Fitzgerald. (2008). Growth factors differentially regulate neuronal Cav channels via ERK-dependent signalling. Cell Calcium 43:562-575.
48. Subramanian J and A Morozov. (2011). Erk1/2 inhibit synaptic vesicle exocytosis through L-type calcium channels. J Neurosci 31:4755-4764.
49. Clegg J, A Gillott and J Jones. (2013). Conceptual issues in neurodevelopmental disorders: lives out of synch. Curr Opin Psychiatry 26:289-294.
50. Barkovich AJ, R Guerrini, RI Kuzniecky, GD Jackson and WB Dobyns. (2012). A developmental and genetic classification for malformations of cortical development: update 2012. Brain 135:1348-1369.
51. Yang K, AM Sheikh, M Malik, G Wen, H Zou, WT Brown and X Li. (2011). Upregulation of Ras/Raf/ERK1/2 signaling and ERK5 in the brain of autistic subjects. Genes Brain Behav 10:834-843.
52. Zou H, Y Yu, AM Sheikh, M Malik, K Yang, G Wen, KK Chadman, WT Brown and X Li. (2011). Association of upregulated Ras/Raf/ERK1/2 signaling with autism. Genes Brain Behav 10:615-624.
53. Dwivedi Y, HS Rizavi, RC Roberts, RC Conley, CA Tamminga and GN Pandey. (2001). Reduced activation and expression of ERK1/2 MAP kinase in the post-mortem brain of depressed suicide subjects. J Neurochem 77:916-928.
54. Mortensen OV. (2013). MKP3 eliminates depolarization dependent neurotransmitter release through downregulation of L-type calcium channel Cav1.2 expression. Cell Calcium 53:224-230.
55. Splawski I, KW Timothy, N Decher, P Kumar, FB Sachse, AH Beggs, MC Sanguinetti and MT Keating. (2005). Severe arrhythmia disorder caused by cardiac L-type calcium channel mutations. Proc Natl Acad Sci U S A 102:8089-8096; discussion 8086-8088.
56. Splawski I, KW Timothy, LM Sharpe, N Decher, P Kumar, R Bloise, C Napolitano, PJ Schwartz, RM Joseph, et al. (2004). Ca(V)1.2 calcium channel dysfunction causes a multisystem disorder including arrhythmia and autism. Cell 119:19-31.