P38 mapks regulate the expression of genes in the dopamine synthesis pathway through phosphorylation of NR4A nuclear receptors

Journal of Cell Science

Volumn 124, Issue 17, 2011, Pages 3006-3016

  Sekine, Yusuke ^a   Takagahara, Shuichi ^a   Hatanaka, Ryo ^a   Watanabe, Takeshi ^a   Oguchi, Haruka ^a   Noguchi, Takuya ^a   Naguro, Isao ^a   Kobayashi, Kazuto ^b   Tsunoda, Makoto ^a   Funatsu, Takashi ^a   Nomura, Hiroshi ^a   Toyoda, Takeshi ^a   Matsuki, Norio ^a   Kuranaga, Erina ^a,c   Miura, Masayuki ^a   Takeda, Kohsuke ^a   Ichijo, Hidenori ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

^c RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

NR4A nuclear receptor; P38 mapk; Stress response; Tyrosine hydroxylase

Indexed keywords

AROMATIC LEVO AMINO ACID DECARBOXYLASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NUCLEAR RECEPTOR NR4A3; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CUTICLE; DOPAMINE METABOLISM; DROSOPHILA; FEMALE; GENE EXPRESSION; GENE INDUCTION; GENE SILENCING; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSACTIVATION; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; DOPA DECARBOXYLASE; DOPAMINE; DROSOPHILA; FEMALE; GENE EXPRESSION REGULATION; MALE; MOLECULAR SEQUENCE DATA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SEQUENCE ALIGNMENT; TRANSFECTION;

BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 80054050110     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.085902     Document Type: Article

References (63)

1. Adachi-Yamada, T., Nakamura, M., Irie, K., Tomoyasu, Y., Sano, Y., Mori, E., Goto, S., Ueno, N., Nishida, Y. and Matsumoto, K. (1999). p38 mitogen-activated protein kinase can be involved in transforming growth factor beta superfamily signal transduction in Drosophila wing morphogenesis. Mol. Cell. Biol. 19, 2322-2329.
2. Baker, K. D., Shewchuk, L. M., Kozlova, T., Makishima, M., Hassell, A., Wisely, B., Caravella, J. A., Lambert, M. H., Reinking, J. L., Krause, H. et al. (2003). The Drosophila orphan nuclear receptor DHR38 mediates an atypical ecdysteroid signaling pathway. Cell 113, 731-742.
3. Calleja, M., Herranz, H., Estella, C., Casal, J., Lawrence, P., Simpson, P. and Morata, G. (2000). Generation of medial and lateral dorsal body domains by the pannier gene of Drosophila. Development 127, 3971-3980.
4. Cerenius, L. and Soderhall, K. (2004). The prophenoloxidase-activating system in invertebrates. Immunol. Rev. 198, 116-126.
5. Chen, J., Xie, C., Tian, L., Hong, L., Wu, X. and Han, J. (2010). Participation of the p38 pathway in Drosophila host defense against pathogenic bacteria and fungi. Proc. Natl. Acad. Sci. USA 107, 20774-20779.
6. Craig, C. R., Fink, J. L., Yagi, Y., Ip, Y. T. and Cagan, R. L. (2004). A Drosophila p38 orthologue is required for environmental stress responses. EMBO Rep. 5, 1058-1063.
7. Cully, M., Genevet, A., Warne, P., Treins, C., Liu, T., Bastien, J., Baum, B., Tapon, N., Leevers, S. J. and Downward, J. (2010). A role for p38 stress-activated protein kinase in regulation of cell growth via TORC1. Mol. Cell. Biol. 30, 481-495.
8. Davis, M. M., O'Keefe, S. L., Primrose, D. A. and Hodgetts, R. B. (2007a). A neuropeptide hormone cascade controls the precise onset of post-eclosion cuticular tanning in Drosophila melanogaster. Development 134, 4395-4404.
9. Davis, M. M., Yang, P., Chen, L., O'Keefe, S. L. and Hodgetts, R. B. (2007b). The orphan nuclear receptor DHR38 influences transcription of the DOPA decarboxylase gene in epidermal and neural tissues of Drosophila melanogaster. Genome 50, 1049-1060.
10. Davis, M. M., Primrose, D. A. and Hodgetts, R. B. (2008). A member of the p38 mitogen-activated protein kinase family is responsible for transcriptional induction of Dopa decarboxylase in the epidermis of Drosophila melanogaster during the innate immune response. Mol. Cell. Biol. 28, 4883-4895.
11. De Gregorio, E., Spellman, P. T., Rubin, G. M. and Lemaitre, B. (2001). Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc. Natl. Acad. Sci. USA 98, 12590-12595.
12. Fisk, G. J. and Thummel, C. S. (1995). Isolation, regulation, and DNA-binding properties of three Drosophila nuclear hormone receptor superfamily members. Proc. Natl. Acad. Sci. USA 92, 10604-10608.
13. Friggi-Grelin, F., Iche, M. and Birman, S. (2003). Tissue-specific developmental requirements of Drosophila tyrosine hydroxylase isoforms. Genesis 35, 175-184.
14. Gibert, J. M., Peronnet, F. and Schlotterer, C. (2007). Phenotypic plasticity in Drosophila pigmentation caused by temperature sensitivity of a chromatin regulator network. PLoS Genet. 3, e30.
15. Glise, B., Bourbon, H. and Noselli, S. (1995). hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell 83, 451-461.
16. Gorman, M. J., An, C. and Kanost, M. R. (2007). Characterization of tyrosine hydroxylase from Manduca sexta. Insect Biochem. Mol. Biol. 37, 1327-1337.
17. Ha, E. M., Lee, K. A., Seo, Y. Y., Kim, S. H., Lim, J. H., Oh, B. H., Kim, J. and Lee, W. J. (2009). Coordination of multiple dual oxidase-regulatory pathways in responses to commensal and infectious microbes in drosophila gut. Nat. Immunol. 10, 949-957.
18. Han, S. J., Choi, K. Y., Brey, P. T. and Lee, W. J. (1998a). Molecular cloning and characterization of a Drosophila p38 mitogen-activated protein kinase. J. Biol. Chem. 273, 369-374.
19. Han, Z. S., Enslen, H., Hu, X., Meng, X., Wu, I. H., Barrett, T., Davis, R. J. and Ip, Y. T. (1998b). A conserved p38 mitogen-activated protein kinase pathway regulates Drosophila immunity gene expression. Mol. Cell. Biol. 18, 3527-3539.
20. Iwawaki, T., Kohno, K. and Kobayashi, K. (2000). Identification of a potential nurr1 response element that activates the tyrosine hydroxylase gene promoter in cultured cells. Biochem. Biophys. Res. Commun. 274, 590-595.
21. Jankovic, J., Chen, S. and Le, W. D. (2005). The role of Nurr1 in the development of dopaminergic neurons and Parkinson's disease. Prog. Neurobiol. 77, 128-138.
22. Jürgens, G., Wieschaus, E., Nüsslein-Volhard, C. and Kluding, H. (1984). Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. Roux's Arch. Dev. Biol. 193, 283-295.
23. Kennerdell, J. R. and Carthew, R. W. (2000). Heritable gene silencing in Drosophila using double-stranded RNA. Nat. Biotechnol. 18, 896-898.
24. Kim, D. H., Feinbaum, R., Alloing, G., Emerson, F. E., Garsin, D. A., Inoue, H., Tanaka-Hino, M., Hisamoto, N., Matsumoto, K., Tan, M. W. et al. (2002). A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297, 623-626.
25. Kolluri, S. K., Bruey-Sedano, N., Cao, X., Lin, B., Lin, F., Han, Y. H., Dawson, M. I. and Zhang, X. K. (2003). Mitogenic effect of orphan receptor TR3 and its regulation by MEKK1 in lung cancer cells. Mol. Cell. Biol. 23, 8651-8667.
26. Kozlova, T., Pokholkova, G. V., Tzertzinis, G., Sutherland, J. D., Zhimulev, I. F. and Kafatos, F. C. (1998). Drosophila hormone receptor 38 functions in metamorphosis: a role in adult cuticle formation. Genetics 149, 1465-1475.
27. Kozlova, T., Lam, G. and Thummel, C. S. (2009). Drosophila DHR38 nuclear receptor is required for adult cuticle integrity at eclosion. Dev. Dyn. 238, 701-707.
28. Kumakura, K., Nomura, H., Toyoda, T., Hashikawa, K., Noguchi, T., Takeda, K., Ichijo, H., Tsunoda, M., Funatsu, T., Ikegami, D. et al. (2010). Hyperactivity in novel environment with increased dopamine and impaired novelty preference in apoptosis signal-regulating kinase 1 (ASK1)-deficient mice. Neurosci. Res. 66, 313-320.
29. Kuranaga, E., Kanuka, H., Igaki, T., Sawamoto, K., Ichijo, H., Okano, H. and Miura, M. (2002). Reaper-mediated inhibition of DIAP1-induced DTRAF1 degradation results in activation of JNK in Drosophila. Nat. Cell Biol. 4, 705-710.
30. Kyriakis, J. M. and Avruch, J. (2001). Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81, 807-869.
31. Le, W. D., Xu, P., Jankovic, J., Jiang, H., Appel, S. H., Smith, R. G. and Vassilatis, D. K. (2003). Mutations in NR4A2 associated with familial Parkinson disease. Nat. Genet. 33, 85-89.
32. Mace, K. A., Pearson, J. C. and McGinnis, W. (2005). An epidermal barrier wound repair pathway in Drosophila is mediated by grainy head. Science 308, 381-385.
33. Masuyama, N., Oishi, K., Mori, Y., Ueno, T., Takahama, Y. and Gotoh, Y. (2001). Akt inhibits the orphan nuclear receptor Nur77 and T-cell apoptosis. J. Biol. Chem. 276, 32799-32805.
34. Matsuzawa, A., Saegusa, K., Noguchi, T., Sadamitsu, C., Nishitoh, H., Nagai, S., Koyasu, S., Matsumoto, K., Takeda, K. and Ichijo, H. (2005). ROS-dependent activation of the TRAF6-ASK1-p38 pathway is selectively required for TLR4- mediated innate immunity. Nat. Immunol. 6, 587-592.
35. Maxwell, M. A. and Muscat, G. E. (2006). The NR4A subgroup: immediate early response genes with pleiotropic physiological roles. Nucl. Recept. Signal. 4, e002.
36. Mizumura, K., Takeda, K., Hashimoto, S., Horie, T. and Ichijo, H. (2006). Identification of Op18/stathmin as a potential target of ASK1-p38 MAP kinase cascade. J. Cell. Physiol. 206, 363-370.
37. Nappi, A. J. and Vass, E. (1993). Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigment Cell Res. 6, 117-126.
38. Neckameyer, W. S. and White, K. (1993). Drosophila tyrosine hydroxylase is encoded by the pale locus. J. Neurogenet. 8, 189-199.
39. Nishitoh, H., Saitoh, M., Mochida, Y., Takeda, K., Nakano, H., Rothe, M., Miyazono, K. and Ichijo, H. (1998). ASK1 is essential for JNK/SAPK activation by TRAF2. Mol. Cell 2, 389-395.
40. Pearson, J. C., Juarez, M. T., Kim, M., Drivenes, O. and McGinnis, W. (2009). Multiple transcription factor codes activate epidermal wound-response genes in Drosophila. Proc. Natl. Acad. Sci. USA 106, 2224-2229.
41. Pei, L., Castrillo, A., Chen, M., Hoffmann, A. and Tontonoz, P. (2005). Induction of NR4A orphan nuclear receptor expression in macrophages in response to inflammatory stimuli. J. Biol. Chem. 280, 29256-29262.
42. Pei, L., Castrillo, A. and Tontonoz, P. (2006). Regulation of macrophage inflammatory gene expression by the orphan nuclear receptor Nur77. Mol. Endocrinol. 20, 786-794.
43. Perlmann, T. and Wallen-Mackénzie, A. (2004). Nurr1, an orphan nuclear receptor with essential functions in developing dopamine cells. Cell Tissue Res. 318, 45-52.
44. Riesgo-Escovar, J. R., Jenni, M., Fritz, A. and Hafen, E. (1996). The Drosophila Jun-N-terminal kinase is required for cell morphogenesis but not for DJun-dependent cell fate specification in the eye. Genes Dev. 10, 2759-2768.
45. Saitoh, M., Nishitoh, H., Fujii, M., Takeda, K., Tobiume, K., Sawada, Y., Kawabata, M., Miyazono, K. and Ichijo, H. (1998). Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17, 2596-2606.
46. Shen, J., Beall, C. J. and Hirsh, J. (1993). Tissue-specific alternative splicing of the Drosophila dopa decarboxylase gene is affected by heat shock. Mol. Cell. Biol. 13, 4549-4555.
47. Shinzawa, N., Nelson, B., Aonuma, H., Okado, K., Fukumoto, S., Miura, M. and Kanuka, H. (2009). p38 MAPK-dependent phagocytic encapsulation confers infection tolerance in Drosophila. Cell Host Microbe 6, 244-252.
48. Slagsvold, H. H., Ostvold, A. C., Fallgren, A. B. and Paulsen, R. E. (2002). Nuclear receptor and apoptosis initiator NGFI-B is a substrate for kinase ERK2. Biochem. Biophys. Res. Commun. 291, 1146-1150.
49. Sluss, H. K., Han, Z., Barrett, T., Goberdhan, D. C., Wilson, C., Davis, R. J. and Ip, Y. T. (1996). A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes Dev. 10, 2745-2758.
50. Sugumaran, M. (2002). Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell Res. 15, 2-9.
51. Takeda, K. and Ichijo, H. (2002). Neuronal p38 MAPK signalling: an emerging regulator of cell fate and function in the nervous system. Genes Cells 7, 1099-1111.
52. Takeda, K., Hatai, T., Hamazaki, T. S., Nishitoh, H., Saitoh, M. and Ichijo, H. (2000). Apoptosis signal-regulating kinase 1 (ASK1) induces neuronal differentiation and survival of PC12 cells. J. Biol. Chem. 275, 9805-9813.
53. Takeda, K., Matsuzawa, A., Nishitoh, H., Tobiume, K., Kishida, S., Ninomiya-Tsuji, J., Matsumoto, K. and Ichijo, H. (2004). Involvement of ASK1 in Ca2+-induced p38 MAP kinase activation. EMBO Rep. 5, 161-166.
54. True, J. R. (2003). Insect melanism: the molecules matter. Trends Ecol. Evol. 18, 640-647.
55. True, J. R., Edwards, K. A., Yamamoto, D. and Carroll, S. B. (1999). Drosophila wing melanin patterns form by vein-dependent elaboration of enzymatic prepatterns. Curr. Biol. 9, 1382-1391.
56. Walter, M. F., Black, B. C., Afshar, G., Kermabon, A. Y., Wright, T. R. and Biessmann, H. (1991). Temporal and spatial expression of the yellow gene in correlation with cuticle formation and dopa decarboxylase activity in Drosophila development. Dev. Biol. 147, 32-45.
57. Wang, Z., Benoit, G., Liu, J., Prasad, S., Aarnisalo, P., Liu, X., Xu, H., Walker, N. P. and Perlmann, T. (2003). Structure and function of Nurr1 identifies a class of ligand-independent nuclear receptors. Nature 423, 555-560.
58. Widmann, C., Gibson, S., Jarpe, M. B. and Johnson, G. L. (1999). Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol. Rev. 79, 143-180.
59. Wingate, A. D., Campbell, D. G., Peggie, M. and Arthur, J. S. (2006). Nur77 is phosphorylated in cells by RSK in response to mitogenic stimulation. Biochem. J. 393, 715-724.
60. Wittkopp, P. J., True, J. R. and Carroll, S. B. (2002). Reciprocal functions of the Drosophila yellow and ebony proteins in the development and evolution of pigment patterns. Development 129, 1849-1858.
61. Wittkopp, P. J., Carroll, S. B. and Kopp, A. (2003). Evolution in black and white: genetic control of pigment patterns in Drosophila. Trends Genet. 19, 495-504.
62. Zarubin, T. and Han, J. (2005). Activation and signaling of the p38 MAP kinase pathway. Cell Res. 15, 11-18.
63. Zeitlinger, J. and Bohmann, D. (1999). Thorax closure in Drosophila: involvement of Fos and the JNK pathway. Development 126, 3947-3956.