Laminar flow activation of ERK5 protein in vascular endothelium leads to atheroprotective effect via NF-E2-related factor 2 (Nrf2) activation

Journal of Biological Chemistry

Volumn 287, Issue 48, 2012, Pages 40722-40731

  Kim, Miso ^a   Kim, Suji ^a   Lim, Jae Hyang ^b   Lee, ChuHee ^a   Choi, Hyoung Chul ^a   Woo, Chang Hoon ^a  

^a Yeungnam University College of Medicine   (South Korea)

^b Ewha Womans University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-INFLAMMATORIES; BLOOD FLOW; DISTURBED FLOW; EXTRACELLULAR SIGNAL-REGULATED KINASE; FLOW ACTIVATION; IN-VIVO; NUCLEAR LOCALIZATION; NUCLEAR TRANSLOCATIONS; SIGNAL PATHWAYS; SPECIFIC INHIBITORS; STRESS-INDUCED; TRANSCRIPTIONAL ACTIVITY; TRANSCRIPTIONAL FACTORS; UP-REGULATION; VASCULAR ENDOTHELIUM; VASCULAR FUNCTIONS;

CHEMICAL COMPOUNDS; DISEASES; ENDOTHELIAL CELLS; GENE EXPRESSION;

LAMINAR FLOW;

KRUPPEL LIKE FACTOR 2; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 7; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF2;

APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; BLOOD FLOW; ENDOTHELIUM CELL; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LAMINAR FLOW; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; UPREGULATION; VASCULAR ENDOTHELIUM;

ANIMALS; ATHEROSCLEROSIS; ENDOTHELIUM, VASCULAR; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE 7; NF-E2-RELATED FACTOR 2; REGIONAL BLOOD FLOW; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

MUS;

EID: 84870015805     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.381509     Document Type: Article

References (36)

1. Malek, A. M., Alper, S. L., and Izumo, S. (1999) Hemodynamic shear stress and its role in atherosclerosis. JAMA 282, 2035-2042
2. Dai, G., Kaazempur-Mofrad, M. R., Natarajan, S., Zhang, Y., Vaughn, S., Blackman, B. R., Kamm, R. D., García-Cardeña, G., and Gimbrone, M. A., Jr. (2004) Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and -resistant regions of human vasculature. Proc. Natl. Acad. Sci. U.S.A. 101, 14871-14876 (Pubitemid 39410767)
3. Warabi, E., Wada, Y., Kajiwara, H., Kobayashi, M., Koshiba, N., Hisada, T., Shibata, M., Ando, J., Tsuchiya, M., Kodama, T., and Noguchi, N. (2004) Effect on endothelial cell gene expression of shear stress, oxygen concentration, and low-density lipoprotein as studied by a novel flow cell culture system. Free Radic. Biol. Med. 37, 682-694 (Pubitemid 38993514)
4. Takabe, W., Jen, N., Ai, L., Hamilton, R., Wang, S., Holmes, K., Dharbandi, F., Khalsa, B., Bressler, S., Barr, M. L., Li, R., and Hsiai, T. K. (2011) Oscillatory shear stress induces mitochondrial superoxide production: implication of NADPH oxidase and c-Jun NH2-terminal kinase signaling. Antioxid. Redox. Signal. 15, 1379-1388
5. Warabi, E., Takabe, W., Minami, T., Inoue, K., Itoh, K., Yamamoto, M., Ishii, T., Kodama, T., and Noguchi, N. (2007) Shear stress stabilizes NF-E2-related factor 2 and induces antioxidant genes in endothelial cells: role of reactive oxygen/nitrogen species. Free Radic. Biol. Med. 42, 260-269 (Pubitemid 44959746)
6. Hosoya, T., Maruyama, A., Kang, M. I., Kawatani, Y., Shibata, T., Uchida, K., Warabi, E., Noguchi, N., Itoh, K., and Yamamoto, M. (2005) Differential responses of the Nrf2-Keap1 system to laminar and oscillatory shear stresses in endothelial cells. J. Biol. Chem. 280, 27244-27250 (Pubitemid 41040764)
7. Kobayashi, A., Kang, M. I., Okawa, H., Ohtsuji, M., Zenke, Y., Chiba, T., Igarashi, K., and Yamamoto, M. (2004) Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol. 24, 7130-7139 (Pubitemid 39014439)
8. Furukawa, M., and Xiong, Y. (2005) BTB protein Keap1 targets antioxidant transcription factor Nrf2 for ubiquitination by the Cullin 3-Roc1 ligase. Mol. Cell. Biol. 25, 162-171 (Pubitemid 40039808)
9. Maher, J., and Yamamoto, M. (2010) The rise of antioxidant signaling - the evolution and hormetic actions of Nrf2. Toxicol. Appl. Pharmacol. 244, 4-15
10. Osburn, W. O., and Kensler, T. W. (2008) Nrf2 signaling: an adaptive response pathway for protection against environmental toxic insults. Mutat. Res. 659, 31-39
11. Zakkar, M., Van der Heiden, K., Luong le, A., Chaudhury, H., Cuhlmann, S., Hamdulay, S. S., Krams, R., Edirisinghe, I., Rahman, I., Carlsen, H., Haskard, D. O., Mason, J. C., and Evans, P. C. (2009) Activation of Nrf2 in endothelial cells protects arteries from exhibiting a proinflammatory state. Arterioscler. Thromb. Vasc. Biol. 29, 1851-1857
12. Dekker, R. J., Boon, R. A., Rondaij, M. G., Kragt, A., Volger, O. L., Elderkamp, Y. W., Meijers, J. C., Voorberg, J., Pannekoek, H., and Horrevoets, A. J. (2006) KLF2 provokes a gene expression pattern that establishes functional quiescent differentiation of the endothelium. Blood 107, 4354-4363 (Pubitemid 43801361)
13. Parmar, K. M., Larman, H. B., Dai, G., Zhang, Y., Wang, E. T., Moorthy, S. N., Kratz, J. R., Lin, Z., Jain, M. K., Gimbrone, M. A., Jr., and García-Cardeña, G. (2006) Integration of flow-dependent endothelial phenotypes by Kruppel-like factor 2. J. Clin. Invest. 116, 49-58 (Pubitemid 43121790)
14. Woo, C. H., Shishido, T., McClain, C., Lim, J. H., Li, J. D., Yang, J., Yan, C., and Abe, J. (2008) Extracellular signal-regulated kinase 5 SUMOylation antagonizes shear stress-induced antiinflammatory response and endothelial nitric oxide synthase expression in endothelial cells. Circ. Res. 102, 538-545 (Pubitemid 351416753)
15. Ohnesorge, N., Viemann, D., Schmidt, N., Czymai, T., Spiering, D., Schmolke, M., Ludwig, S., Roth, J., Goebeler, M., and Schmidt, M. (2010) Erk5 activation elicits a vasoprotective endothelial phenotype via induction of Kruppel-like factor 4 (KLF4). J. Biol. Chem. 285, 26199-26210
16. Clark, P. R., Jensen, T. J., Kluger, M. S., Morelock, M., Hanidu, A., Qi, Z., Tatake, R. J., and Pober, J. S. (2011) MEK5 is activated by shear stress, activates ERK5, and induces KLF4 to modulate TNF responses in human dermal microvascular endothelial cells. Microcirculation 18, 102-117
17. Wang, X., and Tournier, C. (2006) Regulation of cellular functions by the ERK5 signalling pathway. Cell. Signal. 18, 753-760 (Pubitemid 43208930)
18. Buschbeck, M., and Ullrich, A. (2005) The unique C-terminal tail of the mitogen-activated protein kinase ERK5 regulates its activation and nuclear shuttling. J. Biol. Chem. 280, 2659-2667 (Pubitemid 40189370)
19. Akaike, M., Che, W., Marmarosh, N. L., Ohta, S., Osawa, M., Ding, B., Berk, B. C., Yan, C., and Abe, J. (2004) The hinge-helix 1 region of peroxisome proliferator-activated receptor γ1 (PPARγ1) mediates interaction with extracellular signal-regulated kinase 5 and PPARγ1 transcriptional activation: involvement in flow-induced PPARγ activation in endothelial cells. Mol. Cell. Biol. 24, 8691-8704 (Pubitemid 39245088)
20. Pi, X., Yan, C., and Berk, B. C. (2004) Big mitogen-activated protein kinase (BMK1)/ERK5 protects endothelial cells from apoptosis. Circ. Res. 94, 362-369 (Pubitemid 38240728)
21. 2+-independent activation of the endothelial nitric oxide synthase in response to tyrosine phosphatase inhibitors and fluid shear stress. Circ. Res. 82, 686-695
22. Chen, X. L., Varner, S. E., Rao, A. S., Grey, J. Y., Thomas, S., Cook, C. K., Wasserman, M. A., Medford, R. M., Jaiswal, A. K., and Kunsch, C. (2003) Laminar flow induction of antioxidant response element-mediated genes in endothelial cells: a novel anti-inflammatory mechanism. J. Biol. Chem. 278, 703-711 (Pubitemid 36790739)
23. Yan, C., Luo, H., Lee, J. D., Abe, J., and Berk, B. C. (2001) Molecular cloning of mouse ERK5/BMK1 splice variants and characterization of ERK5 functional domains. J. Biol. Chem. 276, 10870-10878 (Pubitemid 38089264)
24. Woo, C. H., Massett, M. P., Shishido, T., Itoh, S., Ding, B., McClain, C., Che, W., Vulapalli, S. R., Yan, C., and Abe, J. (2006) ERK5 activation inhibits inflammatory responses via peroxisome proliferator-activated receptor δ (PPARδ) stimulation. J. Biol. Chem. 281, 32164-32174 (Pubitemid 46036771)
25. Lee, H. H., Park, S. A., Almazari, I., Kim, E. H., Na, H. K., and Surh, Y. J. (2010) Piceatannol induces heme oxygenase-1 expression in human mammary epithelial cells through activation of ARE-driven Nrf2 signaling. Arch. Biochem. Biophys. 501, 142-150
26. Young, A., Wu, W., Sun, W., Benjamin Larman, H., Wang, N., Li, Y. S., Shyy, J. Y., Chien, S., and García-Cardeña, G. (2009) Flow activation of AMP-activated protein kinase in vascular endothelium leads to Krüppel-like factor 2 expression. Arterioscler. Thromb. Vasc. Biol. 29, 1902-1908
27. Nigro, P., Abe, J., Woo, C. H., Satoh, K., McClain, C., O'Dell, M. R., Lee, H., Lim, J. H., Li, J. D., Heo, K. S., Fujiwara, K., and Berk, B. C. (2010) PKCζdecreases eNOS protein stability via inhibitory phosphorylation of ERK5. Blood 116, 1971-1979
28. E, G., Cao, Y., Bhattacharya, S., Dutta, S., Wang, E., and Mukhopadhyay, D. (2012) Endogenous vascular endothelial growth factor-A (VEGF-A) maintains endothelial cell homeostasis by regulating VEGF receptor-2 transcription. J. Biol. Chem. 287, 3029-3041
29. Lim, J. H., Jono, H., Komatsu, K., Woo, C. H., Lee, J., Miyata, M., Matsuno, T., Xu, X., Huang, Y., Zhang, W., Park, S. H., Kim, Y. I., Choi, Y. D., Shen, H., Heo, K. S., Xu, H., Bourne, P., Koga, T., Xu, H., Yan, C., Wang, B., Chen, L. F., Feng, X. H., and Li, J. D. (2012) CYLD negatively regulates transforming growth factor-β-signalling via deubiquitinating Akt. Nat. Commun. 3, 771
30. Ali, F., Zakkar, M., Karu, K., Lidington, E. A., Hamdulay, S. S., Boyle, J. J., Zloh, M., Bauer, A., Haskard, D. O., Evans, P. C., and Mason, J. C. (2009) Induction of the cytoprotective enzyme heme oxygenase-1 by statins is enhanced in vascular endothelium exposed to laminar shear stress and impaired by disturbed flow. J. Biol. Chem. 284, 18882-18892
31. Dai, G., Vaughn, S., Zhang, Y., Wang, E. T., Garcia-Cardena, G., and Gimbrone, M. A., Jr. (2007) Biomechanical forces in atherosclerosis-resistant vascular regions regulate endothelial redox balance via phosphoinositol 3-kinase/Akt-dependent activation of Nrf2. Circ. Res. 101, 723-733 (Pubitemid 47494103)
32. Huang, H. C., Nguyen, T., and Pickett, C. B. (2002) Phosphorylation of Nrf2 at Ser-40 by protein kinase C regulates antioxidant response element-mediated transcription. J. Biol. Chem. 277, 42769-42774 (Pubitemid 35285650)
33. Sun, Z., Huang, Z., and Zhang, D. D. (2009) Phosphorylation of Nrf2 at multiple sites by MAP kinases has a limited contribution in modulating the Nrf2-dependent antioxidant response. PLoS One 4, e6588
34. Shen, G., Hebbar, V., Nair, S., Xu, C., Li, W., Lin, W., Keum, Y. S., Han, J., Gallo, M. A., and Kong, A. N. (2004) Regulation of Nrf2 transactivation domain activity: the differential effects of mitogen-activated protein kinase cascades and synergistic stimulatory effect of Raf and CREB-binding protein. J. Biol. Chem. 279, 23052-23060 (Pubitemid 38685609)
35. Hayashi, M., Kim, S. W., Imanaka-Yoshida, K., Yoshida, T., Abel, E. D., Eliceiri, B., Yang, Y., Ulevitch, R. J., and Lee, J. D. (2004) Targeted deletion of BMK1/ERK5 in adult mice perturbs vascular integrity and leads to endothelial failure. J. Clin. Invest. 113, 1138-1148 (Pubitemid 38544099)
36. Yan, L., Carr, J., Ashby, P. R., Murry-Tait, V., Thompson, C., and Arthur, J. S. (2003) Knockout of ERK5 causes multiple defects in placental and embryonic development. BMC Dev. Biol. 3, 11