Rapamycin induces Mitogen-activated protein (MAP) kinase phosphatase-1 (MKP-1) expression through activation of protein kinase B and Mitogen-activated protein kinase kinase pathways

Journal of Biological Chemistry

Volumn 288, Issue 47, 2013, Pages 33966-33977

  Rastogi, Ruchi ^a   Jiang, Zhongliang ^a   Ahmad, Nisar ^a   Rosati, Rita ^a   Liu, Yusen ^b   Beuret, Laurent ^c   Monks, Robert ^d   Charron, Jean ^c   Birnbaum, Morris J ^d   Samavati, Lobelia ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONWIDE CHILDREN S HOSPITAL   (United States)

^c LAVAL UNIVERSITY   (Canada)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; CHEMICAL ACTIVATION; MAMMALS; NITRIC OXIDE; PHOSPHATASES; TRANSCRIPTION; TRANSCRIPTION FACTORS;

BONE MARROW; MECHANISM OF ACTION; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN-ACTIVATED PROTEIN KINASE KINASE; PRE-TREATMENT; PROTEIN KINASE B; RAPAMYCIN TREATMENT; RAPID ACTIVATION;

IMMUNOLOGY;

ACTIVATING TRANSCRIPTION FACTOR 1; ACTIVATING TRANSCRIPTION FACTOR 2; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; INTERLEUKIN 6; ISOENZYME; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; NITRIC OXIDE; PROTEIN KINASE B; RAPAMYCIN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE; MKP 1 GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

MUS;

EID: 84888326401     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.492702     Document Type: Article

References (58)

1. Wullschleger, S., Loewith, R., and Hall, M. N. (2006) TOR signaling in growth and metabolism. Cell 124, 471-484
2. Zoncu, R., Efeyan, A., and Sabatini, D. M. (2011) mTOR. From growth signal integration to cancer, diabetes, and ageing. Nat. Rev. Mol. Cell Biol. 12, 21-35
3. Guertin, D. A., Stevens, D. M., Thoreen, C. C, Burds, A. A., Kalaany, N. Y., Moffat, J., Brown, M., Fitzgerald, K. J., and Sabatini, D. M. (2006) Ablation in mice of the mTORC components raptor, rictor, or mLST8 reveals that mTORC2 is required for signaling to Akt-FOXO and PKCa, but not S6K1. Devcell 11, 859-871
4. Sarbassov, D. D., Guertin, D. A., Ali, S. M., and Sabatini, D. M. (2005) Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307, 1098-1101
5. Janes, M. R., and Fruman, D. A. (2009) Immune regulation by rapamycin. Moving beyond T cells. Sci Signal 2, pe25
6. Cao, W., Manicassamy, S., Tang, H., Kasturi, S. P., Pirani, A., Murthy, N, and Pulendran, B. (2008) Toll-like receptor-mediated induction of type I interferon in plasmacytoid dendritic cells requires the rapamycin-sensitive PI3K-mTOR-p70S6K pathway. Nat Immunol. 9, 1157-1164
7. Weichhart, T., Costantino, G., Poglitsch, M., Rosner, M., Zeyda, M., Stuhlmeier, K. M., Kolbe, T., Stulnig, T. M., Hörl, W. H, Hengstschläger, M., Müller, M., and Säemann, M. D. (2008) The TSC-mTOR signaling pathway regulates the innate inflammatory response. Immunity 29, 565-577
8. Delgoffe, G. M., Pollizzi, K. N, Waickman, A. T., Heikamp, E., Meyers, D. J., Horton, M. R., Xiao, B., Worley, P. F., and Powell, J. D. (2011) The kinase mTOR regulates the differentiation of helper T cells through the selective activation of signaling by mTORC1 and mTORC2. Nat Immunol 12, 295-303
9. Dong, C., Davis, R. J., and Flavell, R. A. (2002) MAP kinases in the immune response. Annu Rev Immunol 20, 55-72
10. Jeffrey, K. L., Camps, M., Rommel, C., and Mackay, C. R. (2007) Targeting dual-specificity phosphatases. Manipulating MAP kinase signalling and immune responses. Nat. Rev. Drug Discov. 6, 391-403
11. Rastogi, R., Du, W., Ju, D., Pirockinaite, G., Liu, Y., Nunez, G., and Samavati, L. (2011) Dysregulation of p38 and MKP-1 in response to NOD1/TLR4 stimulation in sarcoid bronchoalveolar cells. Am. J. Resp. Crit. Care Med. 183, 500-510
12. Liu, Y., Shepherd, E. G., and Nelin, L. D. (2007) MAPK phosphatases. Regulating the immune response. Nat. Rev. Immunol. 7, 202-212
13. Chi, H., Barry, S. P., Roth, R. J., Wu, J. J., Jones, E. A., Bennett, A. M., and Flavell, R. A. (2006) Dynamic regulation of pro- and anti-inflammatory cytokines by MAPK phosphatase 1 (MKP-1) in innate immune responses. Proc. Natl. Acad. Sci. U. S. A. 103, 2274-2279
14. Wang, X., Meng, X., Kuhlman, J. R., Nelin, L. D., Nicol, K. K., English, B. K., and Liu, Y. (2007) Knockout of Mkp-1 enhances the host inflammatory responses to gram-positive bacteria. J. Immunol. 178, 5312-5320
15. Kristiansen, M., Hughes, R., Patel, P., Jacques, T. S., Clark, A. R., and Ham, J. (2010) Mkp1 is a c-Jun. target gene that antagonizes JNK-dependent apoptosis in sympathetic neurons. JNeurosci 30, 10820-10832
16. Wang, J., Zhou, J. Y., and Wu, G. S. (2007) ERK-dependent MKP-1-mediated cisplatin resistance in human ovarian cancer cells. Cancer Res. 67, 11933-11941
17. Wang, X., Nelin, L. D., Kuhlman, J. R., Meng, X., Welty, S. E., and Liu, Y. (2008) The role of MAP kinase phosphatase-1 in the protective mechanism of dexamethasone against endotoxemia. Life Sci. 83, 671-680
18. Abraham, S. M., Lawrence, T., Kleiman, A., Warden, P., Medghalchi, M., Tuckermann, J., Saklatvala, J., and Clark, A. R. (2006) Antiinflammatory effects of dexamethasone are partly dependent on induction of dual specificity phosphatase 1. J. Exp. Med. 203, 1883-1889
19. Hammer, M., Mages, J., Dietrich, H., Schmitz, F., Striebel, F., Murray, P. J., Wagner, H., and Lang, R. (2005) Control of dual-specificity phosphatase-1 expression in activated macrophages by IL-10. Eur. J. Immunol. 35, 2991-3001
20. Xiao, Y. Q., Malcolm, K., Worthen, G. S., Gardai, S., Schiemann, W. P., Fadok, V. A., Bratton, D. L., and Henson, P. M. (2002) Cross-talk between ERK and p38 MAPK mediates selective suppression of pro-inflammatory cytokines by transforming growth factor-/3. J. Biol. Chem. 277, 14884-14893
21. Zhang, Y., Reynolds, J. M., Chang, S. H, Martin-Orozco, N, Chung, Y., Nurieva, R. I., and Dong, C (2009) MAP kinase phosphatase 1 is necessary for T cell activation and function. J. Biol. Chem. 284, 30815-30824
22. Bauerfeld, C P., Rastogi, R., Pirockinaite, G., Lee, I., Hüttemann, M., Monks, B., Birnbaum, M. J., Franchi, L., Nuñez, G., and Samavati, L. (2012) TLR4-mediated AKT activation is MyD88/TRIF-dependent and critical for induction of oxidative phosphorylation and mitochondrial transcription factor A in murine macrophages. J. Immunol. 188, 2847-2857
23. Bélanger, L. F., Roy, S., Tremblay, M., Brott, B., Steff, A. M., Mourad, W., Hugo, P., Erikson, R., and Charron, J. (2003) Mek2 is dispensable for mouse growth and development. Mol. Cell. Biol. 23, 4778-4787
24. Bissonauth, V., Roy, S., Gravel, M., Guillemette, S., and Charron, J. (2006) Requirement for Map2k1 (Mek1) in extra-embryonic ectoderm during placentogenesis. Development 133, 3429-3440
25. Cho, H., Mu, J., Kim, J. K., Thorvaldsen, J. L., Chu, Q., Crenshaw, E. B., 3rd, Kaestner, K. H, Bartolomei, M. S., Shulman, G. I., and Birnbaum, M. J. (2001) Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB/3). Science 292, 1728-1731
26. Cho, H., Thorvaldsen, J. L., Chu, Q., Feng, F., and Birnbaum, M. J. (2001) Akt1/PKBa is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J. Biol. Chem. 276, 38349-38352
27. Samavati, L., Rastogi, R., Du, W., Hüttemann, M., Fite, A., and Franchi, L. (2009) STAT3 tyrosine phosphorylation is critical for interleukin 1/3 and interleukin-6 production in response to lipopolysaccharide and live bacteria. Mol. Immunol. 46, 1867-1877
28. Liu, R. M., Choi, J., Wu, J. H, GastonPravia, K. A., Lewis, K. M., Brand, J. D., Mochel, N. S., Krzywanski, D. M., Lambeth, J. D., Hagood, J. S., Forman, H. J., Thannickal, V. J., and Postlethwait, E. M. (2010) Oxidative modification of nuclear mitogen-activated protein kinase phosphatase 1 is involved in transforming growth factor/31-induced expression of plasminogen activator inhibitor 1 in fibroblasts. J. Biol. Chem. 285, 16239-16247
29. Kuwano, Y., Kim, H. H, Abdelmohsen, K., Pullmann, R., Jr., Martindale, J. L., Yang, X., and Gorospe, M. (2008) MKP-1 mRNA stabilization and translational control by RNA-binding proteins HuR and NF90. Mol. Cell. Biol. 28, 4562-4575
30. Chen, X. G., Liu, F., Song, X. F., Wang, Z. H, Dong, Z. Q., Hu, Z. Q., Lan, R. Z., Guan, W., Zhou, T. G., Xu, X. M., Lei, H, Ye, Z. Q., Peng, E. J., Du, L. H, and Zhuang, Q. Y. (2010) Rapamycin regulates Akt and ERK phosphorylation through mTORC1 and mTORC2 signaling pathways. Mol. Carcinog 49, 603-610
31. Carracedo, A., Ma, L., Teruya-Feldstein, J., Rojo, F., Salmena, L., Alimonti, A., Egia, A., Sasaki, A. T., Thomas, G., Kozma, S. C, Papa, A., Nardella, C, Cantley, L. C, Baselga, J., and Pandolfi, P. P. (2008) Inhibition of mTORC1 leads to MAPK pathway activation through a PI3K-dependent feedback loop in human cancer. J. Clin. Invest. 118, 3065-3074
32. Sun, S. Y., Rosenberg, L. M., Wang, X., Zhou, Z., Yue, P., Fu, H., and Khuri, F. R. (2005) Activation of Akt and eIF4E survival pathways by rapamycinmediated mammalian target of rapamycin inhibition. Cancer Res. 65, 7052-7058
33. Chang, F., Steelman, L. S., Lee, J. T., Shelton, J. G., Navolanic, P. M., Blalock, W. L., Franklin, R. A., and McCubrey, J. A. (2003) Signal transduction mediated by the Ras/Raf/MEK/ERK pathway from cytokine receptors to transcription factors. Potential targeting for therapeutic intervention. Leukemia 17, 1263-1293
34. Sánchez-Tilló, E., Comalada, M., Farrera, C, Valledor, A. F., Lloberas, J., and Celada, A. (2006) Macrophage-colony-stimulating factor-induced proliferation and lipopolysaccharide-dependent activation of macrophages requires Raf-1 phosphorylation to induce mitogen kinase phosphatase-1 expression. J. Immunol. 176, 6594-6602
35. Ananieva, O., Darragh, J., Johansen, C, Carr, J. M., McIlrath, J., Park, J. M., Wingate, A., Monk, C. E., Toth, R., Santos, S. G., Iversen, L., and Arthur, J. S. (2008) The kinases MSK1 and MSK2 act as negative regulators of Toll-like receptor signaling. Nat. Immunol. 9, 1028-1036
36. Deak, M., Clifton, A. D., Lucocq, L. M., and Alessi, D. R. (1998) Mitogenand stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J. 17, 4426-4441
37. Shimada, M., Nakadai, T., Fukuda, A., and Hisatake, K. (2010) cAMP-response element-binding protein (CREB) controls MSK1-mediated phosphorylation of histone H3 at the c-fos promoter in vitro. J. Biol. Chem. 285, 9390-9401
38. Lau, E., and Ronai, Z. A. (2012) ATF2. At the crossroad of nuclear and cytosolic functions. J. Cell Sci. 125, 2815-2824
39. Johansson-Haque, K., Palanichamy, E., and Okret, S. (2008) Stimulation of MAPK-phosphatase 1 gene expression by glucocorticoids occurs through a tethering mechanism involving C/EBP. J. Mol. Endocrinol. 41, 239-249
40. Schwartz, C, Beck, K., Mink, S., Schmolke, M., Budde, B., Wenning, D., and Klempnauer, K. H. (2003) Recruitment of p300 by C/EBP/3 triggers phosphorylation of p300 and modulates coactivator activity. EMBO J. 22, 882-892
41. Chaturvedi, D., Gao, X., Cohen, M. S., Taunton, J., and Patel, T. B. (2009) Rapamycin induces transactivation of the EGFR and increases cell survival. Oncogene 28, 1187-1196
42. Chen, C. C, and Wang, J. K. (1999) p38 but not p44/42 mitogen-activated protein kinase is required for nitric oxide synthase induction mediated by lipopolysaccharide in RAW 264.7 macrophages. Mol. Pharmacol. 55, 481-488
43. Arthur, J. S., Fong, A. L., Dwyer, J. M., Davare, M., Reese, E., Obrietan, K., and Impey, S. (2004) Mitogen- and stress-activated protein kinase 1 mediates cAMP response element-binding protein phosphorylation and activation by neurotrophins. J. Neurosci. 24, 4324-4332
44. Zhao, Q., Shepherd, E. G., Manson, M. E., Nelin, L. D., Sorokin, A., and Liu, Y. (2005) The role of mitogen-activated protein kinase phosphatase-1 in the response of alveolar macrophages to lipopolysaccharide. Attenuation of proinflammatory cytokine biosynthesis via feedback control of p38. J. Biol. Chem. 280, 8101-8108
45. Carloni, S., Girelli, S., Scopa, C, Buonocore, G., Longini, M., and Balduini, W. (2010) Activation of autophagy and Akt/CREB signaling play an equivalent role in the neuroprotective effect of rapamycin in neonatal hypoxiaischemia. Autophagy 6, 366-377
46. Buck, M., and Chojkier, M. (2007) C/EBP/3 phosphorylation rescues macrophage dysfunction and apoptosis induced by anthrax lethal toxin. Am. J. Physiol. Cell Physiol. 293, C1788-C1796
47. Moua, T., Olson, E. J., Jean, H. C, and Ryu, J. H. (2012) Resolution of chylous pulmonary congestion and respiratory failure in LAM with sirolimus therapy. Am. J. Resp. Crit. Care Med. 186, 389-390
48. Mushaben, E. M., Kramer, E. L., Brandt, E. B., KhuranaHershey, G. K., and Le Cras, T. D. (2011) Rapamycin attenuates airway hyperreactivity, goblet cells, and IgE in experimental allergic asthma. J. Immunol. 187, 5756-5763
49. O'Reilly, K. E., Rojo, F., She, Q. B., Solit, D., Mills, G. B., Smith, D., Lane, H., Hofmann, F., Hicklin, D. J., Ludwig, D. L., Baselga, J., and Rosen, N. (2006) mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res. 66, 1500-1508
50. Brunn, G. J., Williams, J., Sabers, C, Wiederrecht, G., Lawrence, J. C, Jr., and Abraham, R. T. (1996) Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin, and LY294002. EMBO J. 15, 5256-5267
51. Brown, J., Wang, H., Suttles, J., Graves, D. T., and Martin, M. (2011) Mammalian target of rapamycin complex 2 (mTORC2) negatively regulates Toll-like receptor 4-mediated inflammatory response via FoxO1. J. Biol. Chem. 286, 44295-44305
52. Günzl, P., Bauer, K., Hainzl, E., Matt, U., Dillinger, B., Mahr, B., Knapp, S., Binder, B. R., and Schabbauer, G. (2010) Anti-inflammatory properties of the PI3K pathway are mediated by IL-10/DUSP regulation. J. Leukoc. Biol. 88, 1259-1269
53. Medina, E. A., Morris, I. R., and Berton, M. T. (2010) Phosphatidylinositol 3-kinase activation attenuates the TLR2-mediated macrophage proinflammatory cytokine response to Francisella tularensis live vaccine strain. J. Immunol. 185, 7562-7572
54. Arranz, A., Doxaki, C, Vergadi, E., Martinez De La Torre, Y., Vaporidi, K., Lagoudaki, E. D., Ieronymaki, E., Androulidaki, A., Venihaki, M., Margioris, A. N., Stathopoulos, E. N., Tsichlis, P. N., and Tsatsanis, C. (2012) Akt1 and Akt2 protein kinases differentially contribute to macrophage polarization. Proc. Natl. Acad. Sci. U. S. A. 109, 9517-9522
55. Kim, J. S., Sklarz, T., Banks, L. B., Gohil, M., Waickman, A. T., Skuli, N., Krock, B. L., Luo, C. T., Hu, W., Pollizzi, K. N., Li, M. O., Rathmell, J. C, Birnbaum, M. J., Powell, J. D., Jordan, M. S., and Koretzky, G. A. (2013) Natural and inducible TH17 cells are regulated differently by Akt and mTOR pathways. Nat Immunol 14, 611-618
56. Catalanotti, F., Reyes, G., Jesenberger, V., Galabova-Kovacs, G., De MatosSimoes, R., Carugo, O., and Baccarini, M. (2009) A Mek1-Mek2 heterodimer determines the strength and duration of the Erk signal. Nat. Struct. Mol. Biol. 16, 294-303
57. Huang, J., Wang, H., Song, Z., Lin, X., and Zhang, C. (2011) Involvement of MAPK phosphatase-1 in dexamethasone-induced chemoresistance in lung cancer. J. Chemother. 23, 221-226
58. Staples, C. J., Owens, D. M., Maier, J. V., Cato, A. C, and Keyse, S. M. (2010) Cross-talk between the p38a and JNK MAPK pathways mediated by MAP kinase phosphatase-1 determines cellular sensitivity to UV radiation. J. Biol. Chem. 285, 25928-25940