The transcription factor CREB enhances interleukin-17A production and inflammation in a mouse model of atherosclerosis

Science Signaling

Volumn 6, Issue 293, 2013, Pages

  Kotla, Sivareddy ^a   Singh, Nikhlesh K ^a   Heckle, Mark R ^a   Tigyi, Gabor J ^a   Rao, Gadiparthi N ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

15 HYDROXYICOSATETRAENOIC ACID; APOLIPOPROTEIN E; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FOCAL ADHESION KINASE 2; INTERLEUKIN 17; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE SYK; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; XANTHINE OXIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ARCH; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CELL ADHESION; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INFLAMMATION; LEUKOCYTE MIGRATION; LIPID DIET; LIPID STORAGE; MONOCYTE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ANIMALS; AORTA, THORACIC; APOLIPOPROTEINS E; ARACHIDONATE 15-LIPOXYGENASE; ATHEROSCLEROSIS; AZO COMPOUNDS; BLOTTING, WESTERN; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL LINE; CELL MOVEMENT; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DIET, HIGH-FAT; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE; HUMANS; HYDROXYEICOSATETRAENOIC ACIDS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-17; MICE; MICE, KNOCKOUT; MONOCYTES; NADPH OXIDASE; OLIGONUCLEOTIDES, ANTISENSE; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; XANTHINE OXIDASE;

EID: 84885805852     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004214     Document Type: Article

References (55)

1. G. K. Hansson, A. Hermansson, The immune system in atherosclerosis. Nat. Immunol. 12, 204-212 (2011).
2. P. Libby, P. M. Ridker, G. K. Hansson, Progress and challenges in translating the biology of atherosclerosis. Nature 473, 317-325 (2011).
3. H. C. Stary, A. B. Chandler, R. E. Dinsmore, V. Fuster, S. Glagov, W. Insull Jr., M. E. Rosenfeld, C. J. Schwartz, W. D. Wagner, R. W. Wissler, A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation 92, 1355-1374 (1995).
4. S. M. Sendobry, J. A. Cornicelli, K. Welch, T. Bocan, B. Tait, B. K. Trivedi, N. Colbry, R. D. Dyer, S. J. Feinmark, A. Daugherty, Attenuation of diet-induced atherosclerosis in rabbits with a highly selective 15-lipoxygenase inhibitor lacking significant antioxidant properties. Br. J. Pharmacol. 120, 1199-1206 (1997).
5. T. Cyrus, J. L. Witztum, D. J. Rader, R. Tangirala, S. Fazio, M. F. Linton, C. D. Funk, Disruption of the 12/15-lipoxygenase gene diminishes atherosclerosis in apo E-deficient mice. J. Clin. Invest. 103, 1597-1604 (1999).
6. D. Harats, A. Shaish, J. George, M. Mulkins, H. Kurihara, H. Levkovitz, E. Sigal, Over-expression of 15-lipoxygenase in vascular endothelium accelerates early atherosclerosis in LDL receptor - deficient mice. Arterioscler. Thromb. Vasc. Biol. 20, 2100-2105 (2000).
7. M. Mehrabian, H. Allayee, J. Wong, W. Shi, X. P. Wang, Z. Shaposhnik, C. D. Funk, A. J. Lusis, Identification of 5-lipoxygenase as a major gene contributing to atherosclerosis susceptibility in mice. Circ. Res. 91, 120-126 (2002).
8. S. Ylä-Herttuala, W. Palinski, M. E. Rosenfeld, S. Parthasarathy, T. E. Carew, S. Butler, J. L. Witztum, D. Steinberg, Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J. Clin. Invest. 84, 1086-1095 (1989).
9. S. Ylä-Herttuala, J. Luoma, H. Viita, T. Hiltunen, T. Sisto, T. Nikkari, Transfer of 15-lipoxygenase gene into rabbit iliac arteries results in the appearance of oxidation-specific lipid-protein adducts characteristic of oxidized low density lipoprotein. J. Clin. Invest. 95, 2692-2698 (1995).
10. T. Cyrus, D. Praticò, L. Zhao, J. L. Witztum, D. J. Rader, J. Rokach, G. A. FitzGerald, C. D. Funk, Absence of 12/15-lipoxygenase expression decreases lipid peroxidation and atherogenesis in apolipoprotein E - deficient mice. Circulation 103, 2277-2282 (2001).
11. D. J. Benz, M. Mol, M. Ezaki, N. Mori-Ito, I. Zelán, A. Miyanohara, T. Friedmann, S. Parthasarathy, D. Steinberg, J. L. Witztum, Enhanced levels of lipoperoxides in low density lipoprotein incubated with murine fibroblast expressing high levels of human 15-lipoxygenase. J. Biol. Chem. 270, 5191-5197 (1995).
12. A. R. Brash, Lipoxygenases: Occurrence, functions, catalysis, and acquisition of substrate. J. Biol. Chem. 274, 23679-23682 (1999).
13. H. Kühn, J. Barnett, D. Grunberger, P. Baecker, J. Chow, B. Nguyen, H. Bursztyn-Pettegrew, H. Chan, E. Sigal, Overexpression, purification and characterization of human recombinant 15-lipoxygenase. Biochim. Biophys. Acta 1169, 80-89 (1993).
14. H. S. Potula, D. Wang, D. V. Quyen, N. K. Singh, V. Kundumani-Sridharan, M. Karpurapu, E. A. Park, W. C. Glasgow, G. N. Rao, Src-dependent STAT-3-mediated expression of monocyte chemoattractant protein-1 is required for 15(S)-hydroxyeicosatetraenoic acid-induced vascular smooth muscle cell migration. J. Biol. Chem. 284, 31142-31155 (2009).
15. K. R. Chava, M. Karpurapu, D. Wang, M. Bhanoori, V. Kundumani-Sridharan, Q. Zhang, T. Ichiki, W. C. Glasgow, G. N. Rao, CREB-mediated IL-6 expression is required for 15(S)-hydroxyeicosatetraenoic acid - induced vascular smooth muscle cell migration. Arterioscler. Thromb. Vasc. Biol. 29, 809-815 (2009).
16. P. Henriksson, M. Hamberg, U. Diczfalusy, Formation of 15-HETE as a major hydroxyeicosatetraenoic acid in the atherosclerotic vessel wall. Biochim. Biophys. Acta 834, 272-274 (1985).
17. T. C. Simon, A. N. Makheja, J. M. Bailey, Formation of 15-hydroxyeicosatetraenoic acid (15-HETE) as the predominant eicosanoid in aortas from Watanabe Heritable Hyperlipidemic and cholesterol-fed rabbits. Atherosclerosis 75, 31-38 (1989).
18. T. Hiltunen, J. Luoma, T. Nikkari, S. Ylä-Herttuala, Induction of 15-lipoxygenase mRNA and protein in early atherosclerotic lesions. Circulation 92, 3297-3303 (1995).
19. N. T. Aggarwal, S. L. Pfister, W. B. Campbell, Hypercholesterolemia enhances 15-lipoxygenase - mediated vasorelaxation and acetylcholine-induced hypotension. Arterioscler. Thromb. Vasc. Biol. 28, 2209-2215 (2008).
20. M. E. Hatley, S. Srinivasan, K. B. Reilly, D. T. Bolick, C. C. Hedrick, Increased production of 12/15 lipoxygenase eicosanoids accelerates monocyte/endothelial interactions in diabetic db/db mice. J. Biol. Chem. 278, 25369-25375 (2003).
21. S. K. Chakrabarti, B. K. Cole, Y. Wen, S. R. Keller, J. L. Nadler, 12/15-lipoxygenase products induce inflammation and impair insulin signaling in 3T3-L1 adipocytes. Obesity 17, 1657-1663 (2009).
22. H. Yoshida, K. Sasaki, Y. Hirowatari, H. Kurosawa, N. Sato, N. Furutani, N. Tada, Increased serum iron may contribute to enhanced oxidation of low-density lipoprotein in smokers in part through changes in lipoxygenase and catalase. Clin. Chim. Acta 345, 161-170 (2004).
23. V. J. O'Leary, V. M. Darley-Usmar, L. J. Russell, D. Stone, Pro-oxidant effects of lipoxygenase-derived peroxides on the copper-initiated oxidation of low-density lipoprotein. Biochem. J. 282 (pt. 3), 631-634 (1992).
24. J. A. Leopold, J. Loscalzo, Oxidative risk for atherothrombotic cardiovascular disease. Free Radic. Biol. Med. 47, 1673-1706 (2009).
25. J. D. Lambeth, Nox enzymes, ROS, and chronic disease: An example of antagonistic pleiotropy. Free Radic. Biol. Med. 43, 332-347 (2007).
26. E. Galkina, K. Ley, Immune and inflammatory mechanisms of atherosclerosis. Annu. Rev. Immunol. 27, 165-197 (2009).
27. I. Tabas, C. K. Glass, Anti-inflammatory therapy in chronic disease: Challenges and opportunities. Science 339, 166-172 (2013).
28. G. R. Drummond, S. Selemidis, K. K. Griendling, C. G. Sobey, Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat. Rev. Drug Discov. 10, 453-471 (2011).
29. C. E. Berry, J. M. Hare, Xanthine oxidoreductase and cardiovascular disease: Molecular mechanisms and pathophysiological implications. J. Physiol. 555, 589-606 (2004).
30. R. A. Oeckler, P. M. Kaminski, M. S. Wolin, Stretch enhances contraction of bovine coronary arteries via an NAD(P)H oxidase - mediated activation of the extracellular signal - regulated kinase mitogen-activated protein kinase cascade. Circ. Res. 92, 23-31 (2003).
31. N. K. Tonks, Redox redux: Revisiting PTPs and the control of cell signaling. Cell 121, 667-670 (2005).
32. I. Nakashima, K. Takeda, Y. Kawamoto, Y. Okuno, M. Kato, H. Suzuki, Redox control of catalytic activities of membrane-associated protein tyrosine kinases. Arch. Biochem. Biophys. 434, 3-10 (2005).
33. N. Yamamoto, K. Takeshita, M. Shichijo, T. Kokubo, M. Sato, K. Nakashima, M. Ishimori, H. Nagai, Y. F. Li, T. Yura, K. B. Bacon, The orally available spleen tyrosine kinase inhibitor 2-[7-(3,4-dimethoxyphenyl)-imidazo[1,2- c]pyrimidin-5-ylamino]nicotinamide dihydrochloride (BAY 61-3606) blocks antigen-induced airway inflammation in rodents. J. Pharmacol. Exp. Ther. 306, 1174-1181 (2003).
34. L. Buckbinder, D. T. Crawford, H. Qi, H. Z. Ke, L. M. Olson, K. R. Long, P. C. Bonnette, A. P. Baumann, J. E. Hambor, W. A. Grasser, L. C. Pan, T. A. Owen, M. J. Luzzio, C. A. Hulford, D. F. Gebhard, V. M. Paralkar, H. A. Simmons, J. C. Kath, W. G. Roberts, S. L. Smock, A. Guzman-Perez, T. A. Brown, M. Li, Proline-rich tyrosine kinase 2 regulates osteoprogenitor cells and bone formation, and offers an anabolic treatment approach for osteoporosis. Proc. Natl. Acad. Sci. U.S.A. 104, 10619-10624 (2007).
35. A. K. Bajpai, E. Blaskova, S. B. Pakala, T. Zhao, W. C. Glasgow, J. S. Penn, D. A. Johnson, G. N. Rao, 15(S)-HETE production in human retinal microvascular endothelial cells by hypoxia: Novel role for MEK1 in 15(S)-HETE - induced angiogenesis. Invest. Ophthalmol. Vis. Sci. 48, 4930-4938 (2007).
36. T. Zhao, D. Wang, S. Y. Cheranov, M. Karpurapu, K. R. Chava, V. Kundumani-Sridharan, D. A. Johnson, J. S. Penn, G. N. Rao, A novel role for activating transcription factor-2 in 15(S)-hydroxyeicosatetraenoic acid-induced angiogenesis. J. Lipid Res. 50, 521-533 (2009).
37. R. Ross, Atherosclerosis-An inflammatory disease. N. Engl. J. Med. 340, 115-126 (1999).
38. C. Morgantini, S. Imaizumi, V. Grijalva, M. Navab, A. M. Fogelman, S. T. Reddy, Apolipoprotein A-I mimetic peptides prevent atherosclerosis development and reduce plaque inflammation in a murine model of diabetes. Diabetes 59, 3223-3228 (2010).
39. D. Poeckel, K. A. Zemski Berry, R. C. Murphy, C. D. Funk, Dual 12/15- and 5-lipoxygenase deficiency in macrophages alters arachidonic acid metabolism and attenuates peritonitis and atherosclerosis in ApoE knock-out mice. J. Biol. Chem. 284, 21077-21089 (2009).
40. M. Okigaki, C. Davis, M. Falasca, S. Harroch, D. P. Felsenfeld, M. P. Sheetz, J. Schlessinger, Pyk2 regulates multiple signaling events crucial for macrophage morphology and migration. Proc. Natl. Acad. Sci. U.S.A. 100, 10740-10745 (2003).
41. Cip1 / Ets-1/p300 system. Arterioscler. Thromb. Vasc. Biol. 31, 1084-1092 (2011).
42. P. Andre, T. Morooka, D. Sim, K. Abe, C. Lowell, N. Nanda, S. Delaney, G. Siu, Y. Yan, S. Hollenbach, A. Pandey, H. Gao, Y. Wang, K. Nakajima, S. A. Parikh, C. Shi, D. Phillips, W. Owen, U. Sinha, D. I. Simon, Critical role for Syk in responses to vascular injury. Blood 118, 5000-5010 (2011).
43. R. Gadepalli, N. K. Singh, V. Kundumani-Sridharan, M. R. Heckle, G. N. Rao, Novel role of proline-rich nonreceptor tyrosine kinase 2 in vascular wall remodeling after balloon injury. Arterioscler. Thromb. Vasc. Biol. 32, 2652-2661 (2012).
44. J. M. Kyriakis, J. Avruch, Mammalian MAPK signal transduction pathways activated by stress and inflammation: A 10-year update. Physiol. Rev. 92, 689-737 (2012).
45. J. Y. Altarejos, M. Montminy, CREB and the CRTC co-activators: Sensors for hormonal and metabolic signals. Nat. Rev. Mol. Cell Biol. 12, 141-151 (2011).
46. E. Benito, A. Barco, CREB 's control of intrinsic and synaptic plasticity: Implications for CREB-dependent memory models. Trends Neurosci. 33, 230-240 (2010).
47. B. V. Khan, S. S. Parthasarathy, R. W. Alexander, R. M. Medford, Modified low density lipoprotein and its constituents augment cytokine-activated vascular cell adhesion molecule-1 gene expression in human vascular endothelial cells. J. Clin. Invest. 95, 1262-1270 (1995).
48. Y. Huo, L. Zhao, M. C. Hyman, P. Shashkin, B. L. Harry, T. Burcin, S. B. Forlow, M. A. Stark, D. F. Smith, S. Clarke, S. Srinivasan, C. C. Hedrick, D. Praticò, J. L. Witztum, J. L. Nadler, C. D. Funk, K. Ley, Critical role of macrophage 12/15-lipoxygenase for atherosclerosis in apolipoprotein E - deficient mice. Circulation 110, 2024-2031 (2004).
49. S. Taleb, M. Romain, B. Ramkhelawon, C. Uyttenhove, G. Pasterkamp, O. Herbin, B. Esposito, N. Perez, H. Yasukawa, J. Van Snick, A. Yoshimura, A. Tedgui, Z. Mallat, Loss of SOCS3 expression in T cells reveals a regulatory role for interleukin-17 in atherosclerosis. J. Exp. Med. 206, 2067-2077 (2009).
50. E. Smith, K. M. Prasad, M. Butcher, A. Dobrian, J. K. Kolls, K. Ley, E. Galkina, Blockade of interleukin-17A results in reduced atherosclerosis in apolipoprotein E - deficient mice. Circulation 121, 1746-1755 (2010).
51. M. S. Madhur, S. A. Funt, L. Li, A. Vinh, W. Chen, H. E. Lob, Y. Iwakura, Y. Blinder, A. Rahman, A. A. Quyyumi, D. G. Harrison, Role of interleukin 17 in inflammation, atherosclerosis, and vascular function in apolipoprotein E - deficient mice. Arterioscler. Thromb. Vasc. Biol. 31, 1565-1572 (2011).
52. K. Fogh, C. G. Larsen, L. Iversen, K. Kragballe, Interleukin-8 stimulates the formation of 15-hydroxy-eicosatetraenoic acid by human neutrophils in vitro. Agents Actions 35, 227-231 (1992).
53. L. H. Zhang, V. S. Kamanna, S. H. Ganji, X. M. Xiong, M. L. Kashyap, Pioglitazone increases apolipoprotein A-I production by directly enhancing PPRE-dependent transcription in HepG2 cells. J. Lipid Res. 51, 2211-2222 (2010).
54. N. K. Singh, D. Wang, V. Kundumani-Sridharan, D. Van Quyen, J. Niu, G. N. Rao, 15-Lipoxygenase-1-enhanced Src-Janus kinase 2-signal transducer and activator of transcription 3 stimulation and monocyte chemoattractant protein-1 expression require redox-sensitive activation of epidermal growth factor receptor in vascular wall remodeling. J. Biol. Chem. 286, 22478-22488 (2011).
55. X. Y. Tian, W. T. Wong, A. Xu, Y. Lu, Y. Zhang, L. Wang, W. S. Cheang, Y. Wang, X. Yao, Y. Huang, Uncoupling protein-2 protects endothelial function in diet-induced obese mice. Circ. Res. 110, 1211-1216 (2012).