Mitogen-activated protein kinase phosphatase (mkp)-1 as a neuroprotective agent: Promotion of the morphological development of midbrain dopaminergic neurons

NeuroMolecular Medicine

Volumn 15, Issue 2, 2013, Pages 435-446

  Collins, Louise M ^a   O'Keeffe, Gerard W ^a   Long Smith, Caitriona M ^a   Wyatt, Sean L ^b   Sullivan, Aideen M ^a   Toulouse, André ^a   Nolan, Yvonne M ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

6 OHDA; Development; Dopaminergic neuron; Growth; MKP 1; p38

Indexed keywords

MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; OXIDOPAMINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; CYTOARCHITECTURE; DOPAMINERGIC NERVE CELL; EMBRYO; GENE EXPRESSION; GROWTH REGULATION; MESENCEPHALON; NERVE FIBER GROWTH; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; VENTRAL MESENCEPHALON;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; CORPUS STRIATUM; DOPAMINERGIC NEURONS; DUAL SPECIFICITY PHOSPHATASE 1; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMIDAZOLES; MESENCEPHALON; NERVE TISSUE PROTEINS; NEURITES; NEUROPROTECTIVE AGENTS; OXIDOPAMINE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PARKINSON DISEASE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION;

RATTUS;

EID: 84877759836     PISSN: 15351084     EISSN: 15591174     Source Type: Journal    
DOI: 10.1007/s12017-013-8230-5     Document Type: Article

References (56)

1. Bennett, B. L.; Sasaki, D. T.; Murray, B. W.; O'Leary, E. C.; Sakata, S. T.; Xu, W.; et al. (2001). SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proceedings of the National Academy of Sciences of the United States of America, 98(24), 13681-13686.
2. Blandini, F.; Porter, R. H.; & Greenamyre, J. T. (1996). Glutamate and Parkinson's disease. Molecular Neurobiology, 12(1), 73-94.
3. Blum, D.; Torch, S.; Lambeng, N.; Nissou, M.; Benabid, A. L.; Sadoul, R.; et al. (2001). Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: Contribution to the apoptotic theory in Parkinson's disease. Progress in Neurobiology, 65(2), 135-172.
4. Camps, M.; Nichols, A.; & Arkinstall, S. (2000). Dual specificity phosphatases: A gene family for control of MAP kinase function. FASEB journal, 14(1), 6-16.
5. Chambers, J. W.; Pachori, A.; Howard, S.; Iqbal, S.; & Lograsso, P. V. (2013). Inhibition of JNK mitochondrial localization and signaling is protective against ischemia/reperfusion injury in rats. The Journal of biological chemistry, 288(6), 4000-4011.
6. Che, W.; Manetsch, M.; Quante, T.; Rahman, M. M.; Patel, B. S.; Ge, Q.; et al. (2012). Sphingosine 1-phosphate induces MKP-1 expression via p38 MAPK- and CREB-mediated pathways in airway smooth muscle cells. Biochimica et Biophysica Acta, 1823(10), 1658-1665.
7. Choi, W. S.; Eom, D. S.; Han, B. S.; Kim, W. K.; Han, B. H.; Choi, E. J.; et al. (2004). Phosphorylation of p38 MAPK induced by oxidative stress is linked to activation of both caspase-8- and -9-mediated apoptotic pathways in dopaminergic neurons. The Journal of biological chemistry, 279(19), 20451-20460.
8. Choi, B. H.; Hur, E. M.; Lee, J. H.; Jun, D. J.; & Kim, K. T. (2006). Protein kinase Cdelta-mediated proteasomal degradation of MAP kinase phosphatase-1 contributes to glutamate-induced neuronal cell death. Journal of Cell Science, 119(Pt 7), 1329-1340.
9. Chu, J. M.; Chan, Y. S.; Chen, L. W.; & Yung, K. K. (2012). Neurokinin receptor 3 peptide exacerbates 6-hydroxydopamine-induced dopaminergic degeneration in rats through JNK pathway. Journal of Neurochemistry, 123(3), 417-427.
10. Coleman, M. (2005). Axon degeneration mechanisms: Commonality amid diversity. Nature Reviews Neuroscience, 6(11), 889-898.
11. Collins, L. M.; Toulouse, A.; Connor, T. J.; & Nolan, Y. M. (2012). Contributions of central and systemic inflammation to the pathophysiology of Parkinson's disease. Neuropharmacology, 62(7), 2154-2168.
12. Crampton, S. J.; Collins, L. M.; Toulouse, A.; Nolan, Y. M.; & O'Keeffe, G. W. (2012). Exposure of foetal neural progenitor cells to IL-1beta impairs their proliferation and alters their differentiation - a role for maternal inflammation? Journal of Neurochemistry, 120(6), 964-973.
13. Crocker, C. E.; Khan, S.; Cameron, M. D.; Robertson, H. A.; Robertson, G. S.; & Lograsso, P. (2011). JNK inhibition protects dopamine neurons and provides behavioral improvement in a rat 6-hydroxydopamine model of Parkinson's disease. ACS chemical neuroscience, 2(4), 207-212.
14. Crotty, S.; Fitzgerald, P.; Tuohy, E.; Harris, D. M.; Fisher, A.; Mandel, A.; et al. (2008). Neuroprotective effects of novel phosphatidylglycerol-based phospholipids in the 6-hydroxydopamine model of Parkinson's disease. European Journal of Neuroscience, 27(2), 294-300.
15. Davis, S.; Vanhoutte, P.; Pages, C.; Caboche, J.; & Laroche, S. (2000). The MAPK/ERK cascade targets both Elk-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. The Journal of neuroscience, 20(12), 4563-4572.
16. Ding, Y. M.; Jaumotte, J. D.; Signore, A. P.; & Zigmond, M. J. (2004). Effects of 6-hydroxydopamine on primary cultures of substantia nigra: Specific damage to dopamine neurons and the impact of glial cell line-derived neurotrophic factor. Journal of Neurochemistry, 89(3), 776-787.
17. Doddareddy, M.; Rawling, T.; & Ammit, A. J. (2012). Targeting mitogen-activated protein kinase phosphatase-1 (MKP-1): structure-based design of MKP-1 inhibitors and upregulators. Current Medicinal Chemistry, 19(2), 163-173.
18. Eljaschewitsch, E.; Witting, A.; Mawrin, C.; Lee, T.; Schmidt, P. M.; Wolf, S.; et al. (2006). The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells. Neuron, 49(1), 67-79.
19. Farooq, A.; & Zhou, M.-M. (2004). Structure and regulation of MAPK phosphatases. Cellular Signalling, 16(7), 769-779.
20. Franklin, C. C.; & Kraft, A. S. (1997). Conditional expression of the mitogen-activated protein kinase (MAPK) phosphatase MKP-1 preferentially inhibits p38 MAPK and stress-activated protein kinase in U937 cells. The Journal of biological chemistry, 272(27), 16917-16923.
21. Gallo, G. (2011). The cytoskeletal and signaling mechanisms of axon collateral branching. Developmental neurobiology, 71(3), 201-220.
22. Gass, P.; Eckhardt, A.; Schroder, H.; Bravo, R.; & Herdegen, T. (1996). Transient expression of the mitogen-activated protein kinase phosphatase MKP-1 (3CH134/ERP1) in the rat brain after limbic epilepsy. Brain Research. Molecular Brain Research, 41(1-2), 74-80.
23. Gutierrez, H.; & Davies, A. (2007). A fast and accurate procedure for deriving the Sholl profile in quantitative studies of neuronal morphology. Journal of Neuroscience Methods, 163(1), 24-30.
24. Gutierrez, H.; O'Keeffe, G. W.; Gavalda, N.; Gallagher, D.; & Davies, A. M. (2008). Nuclear factor kappa B signaling either stimulates or inhibits neurite growth depending on the phosphorylation status of p65/RelA. Journal of Neuroscience, 28(33), 8246-8256.
25. Hutter, D.; Chen, P.; Barnes, J.; & Liu, Y. (2000). Catalytic activation of mitogen-activated protein (MAP) kinase phosphatase-1 by binding to p38 MAP kinase: Critical role of the p38 C-terminal domain in its negative regulation. Biochemical journal, 352(Pt 1), 155.
26. Jeanneteau, F.; & Deinhardt, K. (2011). Fine-tuning MAPK signaling in the brain: The role of MKP-1. Communicative and Integrative Biology, 4(3), 281-283.
27. Jeanneteau, F.; Deinhardt, K.; Miyoshi, G.; Bennett, A. M.; & Chao, M. V. (2010). The MAP kinase phosphatase MKP-1 regulates BDNF-induced axon branching. Nature Neuroscience, 13(11), 1373-1379.
28. Kim, H. J. (2011). Stem cell potential in Parkinson's disease and molecular factors for the generation of dopamine neurons. Biochimica et Biophysica Acta, 1812(1), 1-11.
29. Lawan, A.; Shi, H.; Gatzke, F.; & Bennett, A. M. (2012). Diversity and specificity of the mitogen-activated protein kinase phosphatase-1 functions. Cellular and Molecular Life Sciences, 70(2), 223-237.
30. Long-Smith, C. M.; Collins, L.; Toulouse, A.; Sullivan, A. M.; & Nolan, Y. M. (2010). Interleukin-1β contributes to dopaminergic neuronal death induced by lipopolysaccharide-stimulated rat glia in vitro. Journal of Neuroimmunology, 226(1-2), 20-26.
31. Mandel, S.; Grunblatt, E.; Riederer, P.; Gerlach, M.; Levites, Y.; & Youdim, M. B. (2003). Neuroprotective strategies in Parkinson's disease: An update on progress. CNS drugs, 17(10), 729-762.
32. Manetsch, M.; Che, W.; Seidel, P.; Chen, Y.; & Ammit, A. J. (2012). MKP-1: A negative feedback effector that represses MAPK-mediated pro-inflammatory signaling pathways and cytokine secretion in human airway smooth muscle cells. Cellular Signalling, 24(4), 907-913.
33. McKelvey, L.; Gutierrez, H.; Nocentini, G.; Crampton, S. J.; Davies, A. M.; Riccardi, C. R.; et al. (2012). The intracellular portion of GITR enhances NGF-promoted neurite growth through an inverse modulation of Erk and NF-kappaB signalling. Biology open, 1(10), 1016-1023.
34. Michel, P. P.; & Hefti, F. (1990). Toxicity of 6-hydroxydopamine and dopamine for dopaminergic neurons in culture. Journal of Neuroscience Research, 26(4), 428-435.
35. Mishra, O. P.; & Delivoria-Papadopoulos, M. (2004). Effect of hypoxia on the expression and activity of mitogen-activated protein (MAP) kinase-phosphatase-1 (MKP-1) and MKP-3 in neuronal nuclei of newborn piglets: The role of nitric oxide. Neuroscience, 129(3), 665-673.
36. Nolan, A. M.; Nolan, Y. M.; & O'Keeffe, G. W. (2011). IL-1beta inhibits axonal growth of developing sympathetic neurons. Molecular and cellular neurosciences, 48(2), 142-150.
37. Nolan, Y.; Vereker, E.; Lynch, A. M.; & Lynch, M. A. (2003). Evidence that lipopolysaccharide-induced cell death is mediated by accumulation of reactive oxygen species and activation of p38 in rat cortex and hippocampus. Experimental Neurology, 184(2), 794-804.
38. O'Keeffe, G. W.; Dockery, P.; & Sullivan, A. M. (2004). Effects of growth/differentiation factor 5 on the survival and morphology of embryonic rat midbrain dopaminergic neurones. Journal of Neurocytology, 33(5), 479-488.
39. O'Keeffe, G. W.; Gutierrez, H.; Pandolfi, P. P.; Riccardi, C.; & Davies, A. M. (2008). NGF-promoted axon growth and target innervation requires GITRL-GITR signaling. Nature Neuroscience, 11(2), 135-142.
40. Owens, D. M.; & Keyse, S. M. (2007). Differential regulation of MAP kinase signalling by dual-specificity protein phosphatases. Oncogene, 26(22), 3203-3213.
41. Peinado-Ramon, P.; Wallen, A.; & Hallbook, F. (1998). MAP kinase phosphatase-1 mRNA is expressed in embryonic sympathetic neurons and is upregulated after NGF stimulation. Brain Research. Molecular Brain Research, 56(1-2), 256-267.
42. Pratt, P. F.; Bokemeyer, D.; Foschi, M.; Sorokin, A.; & Dunn, M. J. (2003). Alterations in subcellular localization of p38 MAPK potentiates endothelin-stimulated COX-2 expression in glomerular mesangial cells. The Journal of biological chemistry, 278(51), 51928-51936.
43. Raff, M. C.; Whitmore, A. V.; & Finn, J. T. (2002). Axonal self-destruction and neurodegeneration. Science, 296(5569), 868-871.
44. Rajadhyaksha, A.; Husson, I.; Satpute, S. S.; Küppenbender, K. D.; Ren, J. Q.; Guerriero, R. M.; et al. (2004). L-Type Ca2 + channels mediate adaptation of extracellular signal-regulated kinase 1/2 phosphorylation in the ventral tegmental area after chronic amphetamine treatment. The Journal of neuroscience, 24(34), 7464-7476.
45. Raman, M.; Chen, W.; & Cobb, M. H. (2007). Differential regulation and properties of MAPKs. Oncogene, 26(22), 3100-3112.
46. Rayport, S.; Sulzer, D.; Shi, W. X.; Sawasdikosol, S.; Monaco, J.; Batson, D.; et al. (1992). Identified postnatal mesolimbic dopamine neurons in culture: Morphology and electrophysiology. The Journal of neuroscience, 12(11), 4264-4280.
47. Ries, V.; Silva, R. M.; Oo, T. F.; Cheng, H. C.; Rzhetskaya, M.; Kholodilov, N.; et al. (2008). JNK2 and JNK3 combined are essential for apoptosis in dopamine neurons of the substantia nigra, but are not required for axon degeneration. Journal of Neurochemistry, 107(6), 1578-1588.
48. Slack, D. N.; Seternes, O. M.; Gabrielsen, M.; & Keyse, S. M. (2001). Distinct binding determinants for ERK2/p38alpha and JNK map kinases mediate catalytic activation and substrate selectivity of map kinase phosphatase-1. The Journal of biological chemistry, 276(19), 16491-16500.
49. Staples, C. J.; Owens, D. M.; Maier, J. V.; Cato, A. C.; & Keyse, S. M. (2010). Cross-talk between the p38alpha and JNK MAPK pathways mediated by MAP kinase phosphatase-1 determines cellular sensitivity to UV radiation. The Journal of biological chemistry, 285(34), 25928-25940.
50. Takaki, M.; Ujike, H.; Kodama, M.; Takehisa, Y.; Nakata, K.; & Kuroda, S. (2001). Two kinds of mitogen-activated protein kinase phosphatases, MKP-1 and MKP-3, are differentially activated by acute and chronic methamphetamine treatment in the rat brain. Journal of Neurochemistry, 79(3), 679-688.
51. Toulouse, A.; & Sullivan, A. M. (2008). Progress in Parkinson's disease-where do we stand? Progress in Neurobiology, 85(4), 376-392.
52. Valjent, E.; Caboche, J.; & Vanhoutte, P. (2001). Mitogen-activated protein kinase/extracellular signal-regulated kinase induced gene regulation in brain: A molecular substrate for learning and memory? Molecular Neurobiology, 23(2-3), 83-99.
53. Walsh, S.; Finn, D. P.; & Dowd, E. (2011). Time-course of nigrostriatal neurodegeneration and neuroinflammation in the 6-hydroxydopamine-induced axonal and terminal lesion models of Parkinson's disease in the rat. Neuroscience, 175, 251-261.
54. Wancket, L. M.; Frazier, W. J.; & Liu, Y. (2012). Mitogen-activated protein kinase phosphatase (MKP)-1 in immunology, physiology, and disease. Life Sciences, 90(7-8), 237-248.
55. Winter, C.; Schenkel, J.; Zimmermann, M.; & Herdegen, T. (1998). MAP kinase phosphatase 1 is expressed and enhanced by FK506 in surviving mamillary, but not degenerating nigral neurons following axotomy. Brain Research, 801(1-2), 198-205.
56. Wu, J. J.; Zhang, L.; & Bennett, A. M. (2005). The noncatalytic amino terminus of mitogen-activated protein kinase phosphatase 1 directs nuclear targeting and serum response element transcriptional regulation. Molecular and Cellular Biology, 25(11), 4792-4803.