MLK3 is part of a feedback mechanism that regulates different cellular responses to reactive oxygen species

Science Signaling

Volumn 7, Issue 328, 2014, Pages

  Lee, Ho Sung ^a   Hwang, Chae Young ^a,b   Shin, Sung Young ^a   Kwon, Ki Sun ^b   Cho, Kwang Hyun ^a  

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

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

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MIXED LINEAGE KINASE 3; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; 2-(4-IODOPHENYL)-3-(4-NITROPHENYL)-5-(2,4-DISULFOPHENYL)-2H-TETRAZOLIUM; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; MITOGEN-ACTIVATED PROTEIN KINASE KINASE KINASE 11; SMALL INTERFERING RNA; TETRAZOLIUM;

ARTICLE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; POSITIVE FEEDBACK; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; BIOLOGICAL MODEL; CELL LINE; CELL SURVIVAL; COMPUTER SIMULATION; FEEDBACK SYSTEM; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PLASMID; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL LINE; CELL SURVIVAL; COMPUTER SIMULATION; FEEDBACK, PHYSIOLOGICAL; HUMANS; MAP KINASE KINASE KINASES; MODELS, BIOLOGICAL; PHOSPHORYLATION; PLASMIDS; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TETRAZOLIUM SALTS;

EID: 84901820554     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2005260     Document Type: Article

References (141)

1. V. J. Thannickal, B. L. Fanburg, Reactive oxygen species in cell signaling. Am. J. Physiol. Lung Cell. Mol. Physiol. 279, L1005-L1028 (2000).
2. K. Irani, Oxidant signaling in vascular cell growth, death, and survival: A review of the roles of reactive oxygen species in smooth muscle and endothelial cell mitogenic and apoptotic signaling. Circ. Res. 87, 179-183 (2000).
3. M. Giorgio, M. Trinei, E. Migliaccio, P. G. Pelicci, Hydrogen peroxide: A metabolic by-product or a common mediator of ageing signals? Nat. Rev. Mol. Cell Biol. 8, 722-728 (2007).
4. E. A. Veal, A. M. Day, B. A. Morgan, Hydrogen peroxide sensing and signaling. Mol. Cell 26, 1-14 (2007).
5. K. R. Martin, J. C. Barrett, Reactive oxygen species as double-edged swords in cellular processes: Low-dose cell signaling versus high-dose toxicity. Hum. Exp. Toxicol. 21, 71-75 (2002).
6. L. A. Jiménez, C. Zanella, H. Fung, Y. M. Janssen, P. Vacek, C. Charland, J. Goldberg, B. T. Mossman, Role of extracellular signal-regulated protein kinases in apoptosis by asbestos and H2O2. Am. J. Physiol. 273, L1029-L1035 (1997).
7. R. Aikawa, I. Komuro, T. Yamazaki, Y. Zou, S. Kudoh, M. Tanaka, I. Shiojima, Y. Hiroi, Y. Yazaki, Oxidative stress activates extracellular signal-regulated kinases through Src and Ras in cultured cardiac myocytes of neonatal rats. J. Clin. Invest. 100, 1813-1821 (1997).
8. J. W. Ramos, The regulation of extracellular signal-regulated kinase (ERK) in mammalian cells. Int. J. Biochem. Cell Biol. 40, 2707-2719 (2008).
9. M. J. Robinson, M. H. Cobb, Mitogen-activated protein kinase pathways. Curr. Opin. Cell Biol. 9, 180-186 (1997).
10. C. Y. Hwang, C. Lee, K. S. Kwon, Extracellular signal-regulated kinase 2-dependent phosphorylation induces cytoplasmic localization and degradation of p21Cip1. Mol. Cell. Biol. 29, 3379-3389 (2009).
11. A. Clerk, S. J. Fuller, A. Michael, P. H. Sugden, Stimulation of "stress-regulated" mitogen-activated protein kinases (stress-activated protein kinases/c-Jun N-terminal kinases and p38-mitogen-activated protein kinases) in perfused rat hearts by oxidative and other stresses. J. Biol. Chem. 273, 7228-7234 (1998).
12. R. Derynck, X. H. Feng, TGF-b receptor signaling. Biochim. Biophys. Acta 1333, F105-F150 (1997).
13. H. M. Shen, Z. G. Liu, JNK signaling pathway is a key modulator in cell death mediated by reactive oxygen and nitrogen species. Free Radic. Biol. Med. 40, 928-939 (2006).
14. M. Saitoh, H. Nishitoh, M. Fujii, K. Takeda, K. Tobiume, Y. Sawada, M. Kawabata, K. Miyazono, H. Ichijo, Mammalian thioredoxin is a direct inhibitor of apoptosis signalregulating kinase (ASK) 1. EMBO J. 17, 2596-2606 (1998).
15. G. Y. Kim, S. E. Mercer, D. Z. Ewton, Z. Yan, K. Jin, E. Friedman, The stress-activated protein kinases p38α and JNK1 stabilize p21Cip1 by phosphorylation. J. Biol. Chem. 277, 29792-29802 (2002).
16. K. A. Gallo, G. L. Johnson, Mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat. Rev. Mol. Cell Biol. 3, 663-672 (2002).
17. A. C. Maroney, J. P. Finn, T. J. Connors, J. T. Durkin, T. Angeles, G. Gessner, Z. Xu, S. L. Meyer, M. J. Savage, L. A. Greene, R. W. Scott, J. L. Vaught, Cep-1347 (KT7515), a semisynthetic inhibitor of the mixed lineage kinase family. J. Biol. Chem. 276, 25302-25308 (2001).
18. L. A. Tibbles, Y. L. Ing, F. Kiefer, J. Chan, N. Iscove, J. R. Woodgett, N. J. Lassam, MLK-3 activates the SAPK/JNK and p38/RK pathways via SEK1 and MKK3/6. EMBO J. 15, 7026-7035 (1996).
19. D. N. Chadee, J. M. Kyriakis, MLK3 is required for mitogen activation of B-Raf, ERK and cell proliferation. Nat. Cell Biol. 6, 770-776 (2004).
20. D. N. Chadee, D. Xu, G. Hung, A. Andalibi, D. J. Lim, Z. Luo, D. H. Gutmann, J. M. Kyriakis, Mixed-lineage kinase 3 regulates B-Raf through maintenance of the B-Raf/Raf-1 complex and inhibition by the NF2 tumor suppressor protein. Proc. Natl. Acad. Sci. U.S.A. 103, 4463-4468 (2006).
21. Y. H. Shen, J. Godlewski, J. Zhu, P. Sathyanarayana, V. Leaner, M. J. Birrer, A. Rana, G. Tzivion, Cross-talk between JNK/SAPK and ERK/MAPK pathways: Sustained activation of JNK blocks ERK activation by mitogenic factors. J. Biol. Chem. 278, 26715-26721 (2003).
22. T. Finkel, Redox-dependent signal transduction. FEBS Lett. 476, 52-54 (2000).
23. J. A. McCubrey, M. M. Lahair, R. A. Franklin, Reactive oxygen species-induced activation of the MAP kinase signaling pathways. Antioxid. Redox Signal. 8, 1775-1789 (2006).
24. Y. Xiong, G. J. Hannon, H. Zhang, D. Casso, R. Kobayashi, D. Beach, p21 is a universal inhibitor of cyclin kinases. Nature 366, 701-704 (1993).
25. A. L. Gartel, S. K. Radhakrishnan, Lost in transcription: p21 repression, mechanisms, and consequences. Cancer Res. 65, 3980-3985 (2005).
26. C. Y. Hwang, I. Y. Kim, K. S. Kwon, Cytoplasmic localization and ubiquitination of p21Cip1 by reactive oxygen species. Biochem. Biophys. Res. Commun. 358, 219-225 (2007).
27. M. F. Favata, K. Y. Horiuchi, E. J. Manos, A. J. Daulerio, D. A. Stradley, W. S. Feeser, D. E. Van Dyk, W. J. Pitts, R. A. Earl, F. Hobbs, R. A. Copeland, R. L. Magolda, P. A. Scherle, J. M. Trzaskos, Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273, 18623-18632 (1998).
28. B. L. Bennett, D. T. Sasaki, B. W. Murray, E. C. O'Leary, S. T. Sakata, W. Xu, J. C. Leisten, A. Motiwala, S. Pierce, Y. Satoh, S. S. Bhagwat, A. M. Manning, D. W. Anderson, SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. U.S.A. 98, 13681-13686 (2001).
29. T. C. Meng, T. Fukada, N. K. Tonks, Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol. Cell 9, 387-399 (2002).
30. Y. W. Lou, Y. Y. Chen, S. F. Hsu, R. K. Chen, C. L. Lee, K. H. Khoo, N. K. Tonks, T. C. Meng, Redox regulation of the protein tyrosine phosphatase PTP1B in cancer cells. FEBS J. 275, 69-88 (2008).
31. S. Zhu, J. D. Bjorge, D. J. Fujita, PTP1B contributes to the oncogenic properties of colon cancer cells through Src activation. Cancer Res. 67, 10129-10137 (2007).
32. J. D. Bjorge, A. Pang, D. J. Fujita, Identification of protein-tyrosine phosphatase 1B as the major tyrosine phosphatase activity capable of dephosphorylating and activating c-Src in several human breast cancer cell lines. J. Biol. Chem. 275, 41439-41446 (2000).
33. S. Q. Zhang, W. Yang, M. I. Kontaridis, T. G. Bivona, G. Wen, T. Araki, J. Luo, J. A. Thompson, B. L. Schraven, M. R. Philips, B. G. Neel, Shp2 regulates Src family kinase activity and Ras/Erk activation by controlling Csk recruitment. Mol. Cell 13, 341-355 (2004).
34. R. Roskoski Jr., Src kinase regulation by phosphorylation and dephosphorylation. Biochem. Biophys. Res. Commun. 331, 1-14 (2005).
35. M. Z. Mehdi, N. R. Pandey, S. K. Pandey, A. K. Srivastava, H2O2-induced phosphorylation of ERK1/2 and PKB requires tyrosine kinase activity of insulin receptor and c-Src. Antioxid. Redox Signal. 7, 1014-1020 (2005).
36. J. Abe, M. Takahashi, M. Ishida, J. D. Lee, B. C. Berk, c-Src is required for oxidative stress-mediated activation of big mitogen-activated protein kinase 1 (BMK1). J. Biol. Chem. 272, 20389-20394 (1997).
37. E. Giannoni, F. Buricchi, G. Raugei, G. Ramponi, P. Chiarugi, Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth. Mol. Cell. Biol. 25, 6391-6403 (2005).
38. D. A. Tice, J. S. Biscardi, A. L. Nickles, S. J. Parsons, Mechanism of biological synergy between cellular Src and epidermal growth factor receptor. Proc. Natl. Acad. Sci. U.S.A. 96, 1415-1420 (1999).
39. J. S. Biscardi, M. C. Maa, D. A. Tice, M. E. Cox, T. H. Leu, S. J. Parsons, c-Src-mediated phosphorylation of the epidermal growth factor receptor on Tyr845 and Tyr1101 is associated with modulation of receptor function. J. Biol. Chem. 274, 8335-8343 (1999).
40. V. G. Brunton, B. W. Ozanne, C. Paraskeva, M. C. Frame, A role for epidermal growth factor receptor, c-Src and focal adhesion kinase in an in vitro model for the progression of colon cancer. Oncogene 14, 283-293 (1997).
41. L. Moro, L. Dolce, S. Cabodi, E. Bergatto, E. Boeri Erba, M. Smeriglio, E. Turco, S. F. Retta, M. G. Giuffrida, M. Venturino, J. Godovac-Zimmermann, A. Conti, E. Schaefer, L. Beguinot, C. Tacchetti, P. Gaggini, L. Silengo, G. Tarone, P. Defilippi, Integrin-induced epidermal growth factor (EGF) receptor activation requires c-Src and p130Cas and leads to phosphorylation of specific EGF receptor tyrosines. J. Biol. Chem. 277, 9405-9414 (2002).
42. G. N. Rao, Hydrogen peroxide induces complex formation of SHC-Grb2-SOS with receptor tyrosine kinase and activates Ras and extracellular signal-regulated protein kinases group of mitogen-activated protein kinases. Oncogene 13, 713-719 (1996).
43. S. Sebastian, J. Settleman, S. J. Reshkin, A. Azzariti, A. Bellizzi, A. Paradiso, The complexity of targeting EGFR signalling in cancer: From expression to turnover. Biochim. Biophys. Acta 1766, 120-139 (2006).
44. M. Holgado-Madruga, A. J. Wong, Gab1 is an integrator of cell death versus cell survival signals in oxidative stress. Mol. Cell. Biol. 23, 4471-4484 (2003).
45. P. C. Chan, J. N. Sudhakar, C. C. Lai, H. C. Chen, Differential phosphorylation of the docking protein Gab1 by c-Src and the hepatocyte growth factor receptor regulates different aspects of cell functions. Oncogene 29, 698-710 (2010).
46. N. Li, A. Batzer, R. Daly, V. Yajnik, E. Skolnik, P. Chardin, D. Bar-Sagi, B. Margolis, J. Schlessinger, Guanine-nucleotide-releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling. Nature 363, 85-88 (1993).
47. P. Chardin, J. H. Camonis, N. W. Gale, L. van Aelst, J. Schlessinger, M. H. Wigler, D. Bar-Sagi, Human Sos1: A guanine nucleotide exchange factor for Ras that binds to GRB2. Science 260, 1338-1343 (1993).
48. U. Schaeper, N. H. Gehring, K. P. Fuchs, M. Sachs, B. Kempkes, W. Birchmeier, Coupling of Gab1 to c-Met, Grb2, and Shp2 mediates biological responses. J. Cell Biol. 149, 1419-1432 (2000).
49. M. Lewitzky, C. Kardinal, N. H. Gehring, E. K. Schmidt, B. Konkol, M. Eulitz, W. Birchmeier, U. Schaeper, S. M. Feller, The C-terminal SH3 domain of the adapter protein Grb2 binds with high affinity to sequences in Gab1 and SLP-76 which lack the SH3-typical P-x-x-P core motif. Oncogene 20, 1052-1062 (2001).
50. A. Montagner, A. Yart, M. Dance, B. Perret, J. P. Salles, P. Raynal, A novel role for Gab1 and SHP2 in epidermal growth factor-induced Ras activation. J. Biol. Chem. 280, 5350-5360 (2005).
51. H. Gu, B. G. Neel, The "Gab" in signal transduction. Trends Cell Biol. 13, 122-130 (2003).
52. M. Yu, J. Luo, W. Yang, Y. Wang, M. Mizuki, Y. Kanakura, P. Besmer, B. G. Neel, H. Gu, The scaffolding adapter Gab2, via Shp-2, regulates kit-evoked mast cell proliferation by activating the Rac/JNK pathway. J. Biol. Chem. 281, 28615-28626 (2006).
53. D. Wang, B. C. Paria, Q. Zhang, M. Karpurapu, Q. Li, W. T. Gerthoffer, Y. Nakaoka, G. N. Rao, A role for Gab1/SHP2 in thrombin activation of PAK1: Gene transfer of kinase-dead PAK1 inhibits injury-induced restenosis. Circ. Res. 104, 1066-1075 (2009).
54. D. T. Denhardt, Signal-transducing protein phosphorylation cascades mediated by Ras/Rho proteins in the mammalian cell: The potential for multiplex signalling. Biochem. J. 318 (Pt. 3), 729-747 (1996).
55. Y. M. Agazie, M. J. Hayman, Molecular mechanism for a role of SHP2 in epidermal growth factor receptor signaling. Mol. Cell. Biol. 23, 7875-7886 (2003).
56. L. K. Rushworth, A. D. Hindley, E. O'Neill, W. Kolch, Regulation and role of Raf-1/B-Raf heterodimerization. Mol. Cell. Biol. 26, 2262-2272 (2006).
57. K. L. Guan, C. Figueroa, T. R. Brtva, T. Zhu, J. Taylor, T. D. Barber, A. B. Vojtek, Negative regulation of the serine/threonine kinase B-Raf by Akt. J. Biol. Chem. 275, 27354-27359 (2000).
58. K. Moelling, K. Schad, M. Bosse, S. Zimmermann, M. Schweneker, Regulation of Raf-Akt cross-talk. J. Biol. Chem. 277, 31099-31106 (2002).
59. L. R. Howe, S. J. Leevers, N. Gómez, S. Nakielny, P. Cohen, C. J. Marshall, Activation of the MAP kinase pathway by the protein kinase raf. Cell 71, 335-342 (1992).
60. J. M. Kyriakis, H. App, X. F. Zhang, P. Banerjee, D. L. Brautigan, U. R. Rapp, J. Avruch, Raf-1 activates MAP kinase-kinase. Nature 358, 417-421 (1992).
61. C. F. Zheng, K. L. Guan, Activation of MEK family kinases requires phosphorylation of two conserved Ser/Thr residues. EMBO J. 13, 1123-1131 (1994).
62. D. R. Alessi, Y. Saito, D. G. Campbell, P. Cohen, G. Sithanandam, U. Rapp, A. Ashworth, C. J. Marshall, S. Cowley, Identification of the sites in MAP kinase kinase-1 phosphorylated by p74raf-1. EMBO J. 13, 1610-1619 (1994).
63. M. Yan, D. J. Templeton, Identification of 2 serine residues of MEK-1 that are differentially phosphorylated during activation by raf and MEK kinase. J. Biol. Chem. 269, 19067-19073 (1994).
64. R. K. Jaiswal, S. A. Moodie, A. Wolfman, G. E. Landreth, The mitogen-activated protein kinase cascade is activated by B-Raf in response to nerve growth factor through interaction with p21ras. Mol. Cell. Biol. 14, 6944-6953 (1994).
65. C. W. Reuter, A. D. Catling, T. Jelinek, M. J. Weber, Biochemical analysis of MEK activation in NIH3T3 fibroblasts. Identification of B-Raf and other activators. J. Biol. Chem. 270, 7644-7655 (1995).
66. S. L. Campbell, R. Khosravi-Far, K. L. Rossman, G. J. Clark, C. J. Der, Increasing complexity of Ras signaling. Oncogene 17, 1395-1413 (1998).
67. Y. Kim, A. E. Rice, J. M. Denu, Intramolecular dephosphorylation of ERK by MKP3. Biochemistry 42, 15197-15207 (2003).
68. D. W. Chan, V. W. Liu, G. S. Tsao, K. M. Yao, T. Furukawa, K. K. Chan, H. Y. Ngan, Loss of MKP3 mediated by oxidative stress enhances tumorigenicity and chemoresistance of ovarian cancer cells. Carcinogenesis 29, 1742-1750 (2008).
69. M. Muda, A. Theodosiou, N. Rodrigues, U. Boschert, M. Camps, C. Gillieron, K. Davies, A. Ashworth, S. Arkinstall, The dual specificity phosphatases M3/6 and MKP-3 are highly selective for inactivation of distinct mitogen-activated protein kinases. J. Biol. Chem. 271, 27205-27208 (1996).
70. Y. Hu, D. D. Bowtell, Sos1 rapidly associates with Grb2 and is hypophosphorylated when complexed with the EGF receptor after EGF stimulation. Oncogene 12, 1865-1872 (1996).
71. A. D. Cherniack, J. K. Klarlund, B. R. Conway, M. P. Czech, Disassembly of Son-of-sevenless proteins from Grb2 during p21ras desensitization by insulin. J. Biol. Chem. 270, 1485-1488 (1995).
72. W. J. Langlois, T. Sasaoka, A. R. Saltiel, J. M. Olefsky, Negative feedback regulation and desensitization of insulin- and epidermal growth factor-stimulated p21ras activation. J. Biol. Chem. 270, 25320-25323 (1995).
73. S. R. Lee, K. S. Yang, J. Kwon, C. Lee, W. Jeong, S. G. Rhee, Reversible inactivation of the tumor suppressor PTEN by H2O2. J. Biol. Chem. 277, 20336-20342 (2002).
74. M. Holgado-Madruga, D. R. Emlet, D. K. Moscatello, A. K. Godwin, A. J. Wong, A Grb2-associated docking protein in EGF- and insulin-receptor signalling. Nature 379, 560-564 (1996).
75. D. R. Mattoon, B. Lamothe, I. Lax, J. Schlessinger, The docking protein Gab1 is the primary mediator of EGF-stimulated activation of the PI-3K/Akt cell survival pathway. BMC Biol. 2, 24 (2004).
76. S. Q. Zhang, W. G. Tsiaras, T. Araki, G. Wen, L. Minichiello, R. Klein, B. G. Neel, Receptor-specific regulation of phosphatidylinositol 3?-kinase activation by the protein tyrosine phosphatase Shp2. Mol. Cell. Biol. 22, 4062-4072 (2002).
77. T. Kodaki, R. Woscholski, B. Hallberg, P. Rodriguez-Viciana, J. Downward, P. J. Parker, The activation of phosphatidylinositol 3-kinase by Ras. Curr. Biol. 4, 798-806 (1994).
78. T. D. Bunney, M. Katan, Phosphoinositide signalling in cancer: Beyond PI3K and PTEN. Nat. Rev. Cancer 10, 342-352 (2010).
79. X. Wang, K. D. McCullough, T. F. Franke, N. J. Holbrook, Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J. Biol. Chem. 275, 14624-14631 (2000).
80. H. A. Seong, H. Jung, H. Ichijo, H. Ha, Reciprocal negative regulation of PDK1 and ASK1 signaling by direct interaction and phosphorylation. J. Biol. Chem. 285, 2397-2414 (2010).
81. A. Toker, A. C. Newton, Cellular signaling: Pivoting around PDK-1. Cell 103, 185-188 (2000).
82. K. Datta, A. Bellacosa, T. O. Chan, P. N. Tsichlis, Akt is a direct target of the phosphatidylinositol 3-kinase. Activation by growth factors, v-src and v-Ha-ras, in Sf9 and mammalian cells. J. Biol. Chem. 271, 30835-30839 (1996).
83. E. H. Goldman, L. Chen, H. Fu, Activation of apoptosis signal-regulating kinase 1 by reactive oxygen species through dephosphorylation at serine 967 and 14-3-3 dissociation. J. Biol. Chem. 279, 10442-10449 (2004).
84. D. Mustacich, G. Powis, Thioredoxin reductase. Biochem. J. 346 (Pt. 1), 1-8 (2000).
85. G. Bunkoczi, E. Salah, P. Filippakopoulos, O. Fedorov, S. Müller, F. Sobott, S. A. Parker, H. Zhang, W. Min, B. E. Turk, S. Knapp, Structural and functional characterization of the human protein kinase ASK1. Structure 15, 1215-1226 (2007).
86. K. Morita, M. Saitoh, K. Tobiume, H. Matsuura, S. Enomoto, H. Nishitoh, H. Ichijo, Negative feedback regulation of ASK1 by protein phosphatase 5 (PP5) in response to oxidative stress. EMBO J. 20, 6028-6036 (2001).
87. A. H. Kim, G. Khursigara, X. Sun, T. F. Franke, M. V. Chao, Akt phosphorylates and negatively regulates apoptosis signal-regulating kinase 1. Mol. Cell. Biol. 21, 893-901 (2001).
88. K. A. Schachter, Y. Du, A. Lin, K. A. Gallo, Dynamic positive feedback phosphorylation of mixed lineage kinase 3 by JNK reversibly regulates its distribution to Triton-soluble domains. J. Biol. Chem. 281, 19134-19144 (2006).
89. H. Ichijo, E. Nishida, K. Irie, P. ten Dijke, M. Saitoh, T. Moriguchi, M. Takagi, K. Matsumoto, K. Miyazono, Y. Gotoh, Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 275, 90-94 (1997).
90. Z. Xu, N. V. Kukekov, L. A. Greene, Regulation of apoptotic c-Jun N-terminal kinase signaling by a stabilization-based feed-forward loop. Mol. Cell. Biol. 25, 9949-9959 (2005).
91. J. J. Song, Y. J. Lee, Cross-talk between JIP3 and JIP1 during glucose deprivation: SEK1-JNK2 and Akt1 act as mediators. J. Biol. Chem. 280, 26845-26855 (2005).
92. H. S. Park, M. S. Kim, S. H. Huh, J. Park, J. Chung, S. S. Kang, E. J. Choi, Akt (protein kinase B) negatively regulates SEK1 by means of protein phosphorylation. J. Biol. Chem. 277, 2573-2578 (2002).
93. B. Dérijard, J. Raingeaud, T. Barrett, I. H. Wu, J. Han, R. J. Ulevitch, R. J. Davis, Independent human MAP-kinase signal transduction pathways defined by MEK and MKK isoforms. Science 267, 682-685 (1995).
94. X. Lu, S. Nemoto, A. Lin, Identification of c-Jun NH2-terminal protein kinase (JNK)-activating kinase 2 as an activator of JNK but not p38. J. Biol. Chem. 272, 24751-24754 (1997).
95. C. P. Bagowski, J. Besser, C. R. Frey, J. E. Ferrell Jr., The JNK cascade as a biochemical switch in mammalian cells: Ultrasensitive and all-or-none responses. Curr. Biol. 13, 315-320 (2003).
96. M. K. Barthwal, P. Sathyanarayana, C. N. Kundu, B. Rana, A. Pradeep, C. Sharma, J. R. Woodgett, A. Rana, Negative regulation of mixed lineage kinase 3 by protein kinase B/AKT leads to cell survival. J. Biol. Chem. 278, 3897-3902 (2003).
97. I. W. Leung, N. Lassam, Dimerization via tandem leucine zippers is essential for the activation of the mitogen-activated protein kinase kinase kinase, MLK-3. J. Biol. Chem. 273, 32408-32415 (1998).
98. N. Tapon, K. Nagata, N. Lamarche, A. Hall, A new Rac target POSH is an SH3-containing scaffold protein involved in the JNK and NF-κB signalling pathways. EMBO J. 17, 1395-1404 (1998).
99. T. D. Prickett, D. L. Brautigan, Cytokine activation of p38 mitogen-activated protein kinase and apoptosis is opposed by alpha-4 targeting of protein phosphatase 2A for site-specific dephosphorylation of MEK3. Mol. Cell. Biol. 27, 4217-4227 (2007).
100. W. Wang, J. X. Chen, R. Liao, Q. Deng, J. J. Zhou, S. Huang, P. Sun, Sequential activation of the MEK-extracellular signal-regulated kinase and MKK3/6-p38 mitogen-activated protein kinase pathways mediates oncogenic ras-induced premature senescence. Mol. Cell. Biol. 22, 3389-3403 (2002).
101. S. Grethe, M. I. Pörn-Ares, p38 MAPK regulates phosphorylation of Bad via PP2A-dependent suppression of the MEK1/2-ERK1/2 survival pathway in TNF-α induced endothelial apoptosis. Cell. Signal. 18, 531-540 (2006).
102. S. P. Li, M. R. Junttila, J. Han, V. M. Kähäri, J. Westermarck, p38 mitogen-activated protein kinase pathway suppresses cell survival by inducing dephosphorylation of mitogen-activated protein/extracellular signal-regulated kinase kinase1,2. Cancer Res. 63, 3473-3477 (2003).
103. M. Camps, A. Nichols, C. Gillieron, B. Antonsson, M. Muda, C. Chabert, U. Boschert, S. Arkinstall, Catalytic activation of the phosphatase MKP-3 by ERK2 mitogen-activated protein kinase. Science 280, 1262-1265 (1998).
104. M. Ekerot, M. P. Stavridis, L. Delavaine, M. P. Mitchell, C. Staples, D. M. Owens, I. D. Keenan, R. J. Dickinson, K. G. Storey, S. M. Keyse, Negative-feedback regulation of FGF signalling by DUSP6/MKP-3 is driven by ERK1/2 and mediated by Ets factor binding to a conserved site within the DUSP6/MKP-3 gene promoter. Biochem. J. 412, 287-298 (2008).
105. T. Furukawa, E. Tanji, S. Xu, A. Horii, Feedback regulation of DUSP6 transcription responding to MAPK1 via ETS2 in human cells. Biochem. Biophys. Res. Commun. 377, 317-320 (2008).
106. M. Hatakeyama, S. Kimura, T. Naka, T. Kawasaki, N. Yumoto, M. Ichikawa, J. H. Kim, K. Saito, M. Saeki, M. Shirouzu, S. Yokoyama, A. Konagaya, A computational model on the modulation of mitogen-activated protein kinase (MAPK) and Akt pathways in heregulin-induced ErbB signalling. Biochem. J. 373, 451-463 (2003).
107. A. Fujioka, K. Terai, R. E. Itoh, K. Aoki, T. Nakamura, S. Kuroda, E. Nishida, M. Matsuda, Dynamics of the Ras/ERK MAPK cascade as monitored by fluorescent probes. J. Biol. Chem. 281, 8917-8926 (2006).
108. S. Sasagawa, Y. Ozaki, K. Fujita, S. Kuroda, Prediction and validation of the distinct dynamics of transient and sustained ERK activation. Nat. Cell Biol. 7, 365-373 (2005).
109. R. Paumelle, D. Tulasne, C. Leroy, J. Coll, B. Vandenbunder, V. Fafeur, Sequential activation of ERK and repression of JNK by scatter factor/hepatocyte growth factor in Madin-Darby canine kidney epithelial cells. Mol. Biol. Cell 11, 3751-3763 (2000).
110. M. M. Monick, L. S. Powers, T. J. Gross, D. M. Flaherty, C. W. Barrett, G. W. Hunninghake, Active ERK contributes to protein translation by preventing JNK-dependent inhibition of protein phosphatase 1. J. Immunol. 177, 1636-1645 (2006).
111. Y. Chu, P. A. Solski, R. Khosravi-Far, C. J. Der, K. Kelly, 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 (1996).
112. M. R. Junttila, S. P. Li, J. Westermarck, Phosphatase-mediated crosstalk between MAPK signaling pathways in the regulation of cell survival. FASEB J. 22, 954-965 (2008).
113. E. J. Black, M. Walker, W. Clark, A. MacLaren, D. A. Gillespie, Cell transformation by v-Jun deactivates ERK MAP kinase signalling. Oncogene 21, 6540-6548 (2002).
114. E. Stepniak, R. Ricci, R. Eferl, G. Sumara, I. Sumara, M. Rath, L. Hui, E. F. Wagner, c-Jun/AP-1 controls liver regeneration by repressing p53/p21 and p38 MAPK activity. Genes Dev. 20, 2306-2314 (2006).
115. T. Peng, T. Zhang, X. Lu, Q. Feng, JNK1/c-fos inhibits cardiomyocyte TNF-α expression via a negative crosstalk with ERK and p38 MAPK in endotoxaemia. Cardiovasc. Res. 81, 733-741 (2009).
116. C. J. Staples, D. M. Owens, J. V. Maier, A. C. Cato, S. M. Keyse, Cross-talk between the p38α and JNK MAPK pathways mediated by MAP kinase phosphatase-1 determines cellular sensitivity to UV radiation. J. Biol. Chem. 285, 25928-25940 (2010).
117. S. J. Park, H. Y. Kim, H. Kim, S. M. Park, E. H. Joe, I. Jou, Y. H. Choi, Oxidative stress induces lipid-raft-mediated activation of Src homology 2 domain-containing protein-tyrosine phosphatase 2 in astrocytes. Free Radic. Biol. Med. 46, 1694-1702 (2009).
118. J. Abe, B. C. Berk, Fyn and JAK2 mediate Ras activation by reactive oxygen species. J. Biol. Chem. 274, 21003-21010 (1999).
119. V. C. Tu, J. J. Bahl, Q. M. Chen, Signals of oxidant-induced cardiomyocyte hypertrophy: Key activation of p70 S6 kinase-1 and phosphoinositide 3-kinase. J. Pharmacol. Exp. Ther. 300, 1101-1110 (2002).
120. M. F. Xu, F. Zhang, L. Da, T. P. Li, M. J. Zhao, Microspherule protein 2 associates with ASK1 and acts as a negative regulator of stress-induced ASK1 activation. FEBS Lett. 586, 1678-1686 (2012).
121. Y. Kuwano, H. H. Kim, K. Abdelmohsen, R. Pullmann, J. L. Martindale, X. L. Yang, M. Gorospe, MKP-1 mRNA stabilization and translational control by RNA-binding proteins HuR and NF90. Mol. Cell. Biol. 28, 4562- 4575 (2008).
122. J. E. Ferrell Jr., Self-perpetuating states in signal transduction: Positive feedback, double-negative feedback and bistability. Curr. Opin. Cell Biol. 14, 140-148 (2002).
123. B. N. Kholodenko, J. F. Hancock, W. Kolch, Signalling ballet in space and time. Nat. Rev. Mol. Cell Biol. 11, 414-426 (2010).
124. K. Tobiume, A. Matsuzawa, T. Takahashi, H. Nishitoh, K. Morita, K. Takeda, O. Minowa, K. Miyazono, T. Noda, H. Ichijo, ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep. 2, 222-228 (2001).
125. J. Matsukawa, A. Matsuzawa, K. Takeda, H. Ichijo, The ASK1-MAP kinase cascades in mammalian stress response. J. Biochem. 136, 261-265 (2004).
126. A. Matsuzawa, H. Ichijo, Stress-responsive protein kinases in redox-regulated apoptosis signaling. Antioxid. Redox Signal. 7, 472-481 (2005).
127. P. T. Schumacker, Reactive oxygen species in cancer cells: Live by the sword, die by the sword. Cancer Cell 10, 175-176 (2006).
128. E. Takimoto, D. A. Kass, Role of oxidative stress in cardiac hypertrophy and remodeling. Hypertension 49, 241-248 (2007).
129. H. Kadowaki, H. Nishitoh, F. Urano, C. Sadamitsu, A. Matsuzawa, K. Takeda, H. Masutani, J. Yodoi, Y. Urano, T. Nagano, H. Ichijo, Amyloid b induces neuronal cell death through ROS-mediated ASK1 activation. Cell Death Differ. 12, 19-24 (2005).
130. K. Imoto, D. Kukidome, T. Nishikawa, T. Matsuhisa, K. Sonoda, K. Fujisawa, M. Yano, H. Motoshima, T. Taguchi, K. Tsuruzoe, T. Matsumura, H. Ichijo, E. Araki, Impact of mitochondrial reactive oxygen species and apoptosis signal-regulating kinase 1 on insulin signaling. Diabetes 55, 1197-1204 (2006).
131. S. Mangan, U. Alon, Structure and function of the feed-forward loop network motif. Proc. Natl. Acad. Sci. U.S.A. 100, 11980-11985 (2003).
132. D. Kim, Y. K. Kwon, K. H. Cho, The biphasic behavior of incoherent feed-forward loops in biomolecular regulatory networks. BioEssays 30, 1204-1211 (2008).
133. J. E. Ferrell, W. Xiong, Bistability in cell signaling: How to make continuous processes discontinuous, and reversible processes irreversible. Chaos 11, 227-236 (2001).
134. A. Schneider, U. Klingmüller, M. Schilling, Short-term information processing, longterm responses: Insights by mathematical modeling of signal transduction. Early activation dynamics of key signaling mediators can be predictive for cell fate decisions. BioEssays 34, 542-550 (2012).
135. J. E. Ferrell Jr., Feedback regulation of opposing enzymes generates robust, all-or-none bistable responses. Curr. Biol. 18, R244-R245 (2008).
136. L. F. Shampine, M. W. Reichelt, The MATLAB ODE suite. SIAM J. Sci. Comput. 18, 1-22 (1997).
137. D. E. Goldberg, Genetic Algorithms in Search, Optimization, and Machine Learning (Addison Wesley Publishing Company, Reading, MA, 1989).
138. T. F. Coleman, M. A. Branch, A. Grace, Optimization Toolbox for Use with MATLAB: User's Guide (MathWorks Inc., Natick, MA, ed. 2, 1999).
139. R. N. Gutenkunst, J. J. Waterfall, F. P. Casey, K. S. Brown, C. R. Myers, J. P. Sethna, Universally sloppy parameter sensitivities in systems biology models. PLOS Comput. Biol. 3, 1871-1878 (2007).
140. T. J. Collins, ImageJ for microscopy. BioTechniques 43, 25-30 (2007).
141. C. Y. Hwang, S. M. Lee, S. S. Park, K. S. Kwon, CDK2 differentially controls normal cell senescence and cancer cell proliferation upon exposure to reactive oxygen species. Biochem. Biophys. Res. Commun. 425, 94-99 (2012).