Transforming growth factor-β-activated kinase 1 regulates angiogenesis via AMP-activated protein kinase-α1 and redox balance in endothelial cells

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 12, 2013, Pages 2792-2799

  Zippel, Nina ^a   Malik, Randa Abdel ^a   Frömel, Timo ^a   Popp, Rüdiger ^a   Bess, Elke ^a   Strilic, Boris ^b   Wettschureck, Nina ^b   Fleming, Ingrid ^a   Fisslthaler, Beate ^a  

^a GOETHE UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

Author keywords

AMPK kinase; Angiogenesis modulators; MAP kinase kinase kinase 7; Redox

Indexed keywords

HYDROGEN PEROXIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MACROGOL; MANGANESE SUPEROXIDE DISMUTASE; MITOGEN ACTIVATED PROTEIN KINASE 1; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; SUPEROXIDE; SYNAPTOPHYSIN; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VASCULAR RING;

AMPK KINASE; ANGIOGENESIS MODULATORS; MAP KINASE KINASE KINASE 7; REDOX;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTIOXIDANTS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYDROGEN PEROXIDE; INTERLEUKIN-1BETA; MAP KINASE KINASE KINASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; NEOVASCULARIZATION, PHYSIOLOGIC; OXIDATION-REDUCTION; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; RECEPTORS, LDL; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; TIME FACTORS; TRANSFECTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84888199803     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.301848     Document Type: Article

References (43)

1. Yamaguchi K, Shirakabe K, Shibuya H, Irie K, Oishi I, Ueno N, Taniguchi T, Nishida E, Matsumoto K. Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science. 1995;270:2008-2011
2. Ninomiya-Tsuji J, Kishimoto K, Hiyama A, Inoue J, Cao Z, Matsumoto K. The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature. 1999;398:252-256
3. Sakurai H. Targeting of TAK1 in inflammatory disorders and cancer. Trends Pharmacol Sci. 2012;33:522-530
4. Momcilovic M, Hong SP, Carlson M. Mammalian TAK1 activates Snf1 protein kinase in yeast and phosphorylates AMP-Activated protein kinase in vitro. J Biol Chem. 2006;281:25336-25343
5. Xie M, Zhang D, Dyck JR, Li Y, Zhang H, Morishima M, Mann DL, Taffet GE, Baldini A, Khoury DS, Schneider MD. A pivotal role for endogenous TGF-beta-Activated kinase-1 in the LKB1/AMP-Activated protein kinase energy-sensor pathway. Proc Natl Acad Sci USA. 2006;103:17378-17383
6. Kim SY, Jeong S, Jung E, Baik KH, Chang MH, Kim SA, Shim JH, Chun E, Lee KY. AMP-Activated protein kinase-α1 as an activating kinase of TGF-β-Activated kinase 1 has a key role in inflammatory signals. Cell Death Dis. 2012;3:e357
7. Chang MY, Ho FM, Wang JS, Kang HC, Chang Y, Ye ZX, Lin WW. AICAR induces cyclooxygenase-2 expression through AMP-Activated protein kinase-Transforming growth factor-beta-Activated kinase 1-p38 mitogen-Activated protein kinase signaling pathway. Biochem Pharmacol. 2010;80:1210-1220
8. Ouchi N, Shibata R, Walsh K. AMP-Activated protein kinase signaling stimulates VEGF expression and angiogenesis in skeletal muscle. Circ Res. 2005;96:838-846
9. Ouchi N, Kobayashi H, Kihara S, Kumada M, Sato K, Inoue T, Funahashi T, Walsh K. Adiponectin stimulates angiogenesis by promoting cross-Talk between AMP-Activated protein kinase and Akt signaling in endothelial cells. J Biol Chem. 2004;279:1304-1309
10. Nagata D, Mogi M, Walsh K. AMP-Activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J Biol Chem. 2003;278:31000-31006
11. Webler AC, Michaelis UR, Popp R, Barbosa-Sicard E, Murugan A, Falck JR, Fisslthaler B, Fleming I. Epoxyeicosatrienoic acids are part of the VEGF-Activated signaling cascaDe Leading to angiogenesis. Am J Physiol Cell Physiol. 2008;295:C1292-C1301
12. Xu MJ, Song P, Shirwany N, Liang B, Xing J, Viollet B, Wang X, Zhu Y, Zou MH. Impaired expression of uncoupling protein 2 causes defective postischemic angiogenesis in mice deficient in AMP-Activated protein kinase α subunits. Arterioscler Thromb Vasc Biol. 2011;31:1757-1765
13. Jadrich JL, O'Connor MB, Coucouvanis E. The TGF beta activated kinase TAK1 regulates vascular development in vivo. Development. 2006;133:1529-1541
14. Morioka S, Inagaki M, Komatsu Y, Mishina Y, Matsumoto K, Ninomiya-Tsuji J. TAK1 kinase signaling regulates embryonic angiogenesis by modulating endothelial cell survival and migration. Blood. 2012;120:3846-3857
15. Sato S, Sanjo H, Takeda K, Ninomiya-Tsuji J, Yamamoto M, Kawai T, Matsumoto K, Takeuchi O, Akira S. Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat Immunol. 2005;6:1087-1095
16. Morioka S, Omori E, Kajino T, Kajino-Sakamoto R, Matsumoto K, Ninomiya-Tsuji J. TAK1 kinase determines TRAIL sensitivity by modulating reactive oxygen species and cIAP. Oncogene. 2009;28:2257-2265
17. Voronov E, Shouval DS, Krelin Y, Cagnano E, Benharroch D, Iwakura Y, Dinarello CA, Apte RN. IL-1 is required for tumor invasiveness and angiogenesis. Proc Natl Acad Sci USA. 2003;100:2645-2650
18. Konisti S, Kiriakidis S, Paleolog EM. Hypoxia-A key regulator of angiogenesis and inflammation in rheumatoid arthritis. Nat Rev Rheumatol. 2012;8:153-162
19. Jagielska J, Kapopara PR, Salguero G, Scherr M, Schütt H, Grote K, Schieffer B, Bavendiek U. Interleukin-1 assembles a proangiogenic signaling module consisting of caveolin-1, tumor necrosis factor receptorassociated factor 6, p38-mitogen-Activated protein kinase (MAPK), and MAPK-Activated protein kinase 2 in endothelial cells. Arterioscler Thromb Vasc Biol. 2012;32:1280-1288
20. Evangelista AM, Thompson MD, Bolotina VM, Tong X, Cohen RA. Nox4-And Nox2-dependent oxidant production is required for VEGFinduced SERCA cysteine-674 S-glutathiolation and endothelial cell migration. Free Radic Biol Med. 2012;53:2327-2334
21. Fukai T, Ushio-Fukai M. Superoxide dismutases: Role in redox signaling, vascular function, and diseases. Antioxid Redox Signal. 2011;15: 1583-1606
22. Beckman JS, Minor RL Jr, White CW, Repine JE, Rosen GM, Freeman BA. Superoxide dismutase and catalase conjugated to polyethylene glycol increases endothelial enzyme activity and oxidant resistance. J Biol Chem. 1988;263:6884-6892
23. Meneghini MD, Ishitani T, Carter JC, Hisamoto N, Ninomiya-Tsuji J, Thorpe CJ, Hamill DR, Matsumoto K, Bowerman B. MAP kinase and Wnt pathways converge to downregulate an HMG-domain repressor in Caenorhabditis elegans. Nature. 1999;399:793-797
24. Shang Y, Doan CN, Arnold TD, Lee S, Tang AA, Reichardt LF, Huang EJ. Transcriptional corepressors HIPK1 and HIPK2 control angiogenesis via TGF-β-TAK1-dependent mechanism. PLoS Biol. 2013;11:e1001527
25. Safina A, Ren MQ, Vandette E, Bakin AV. TAK1 is required for TGFbeta 1-mediated regulation of matrix metalloproteinase-9 and metastasis. Oncogene. 2008;27:1198-1207
26. Vanlangenakker N, Vanden Berghe T, Bogaert P, Laukens B, Zobel K, Deshayes K, Vucic D, Fulda S, Vandenabeele P, Bertrand MJ. cIAP1 and TAK1 protect cells from TNF-induced necrosis by preventing RIP1/ RIP3-dependent reactive oxygen species production. Cell Death Differ. 2011;18:656-665
27. Elmasri H, Karaaslan C, Teper Y, Ghelfi E, Weng M, Ince TA, Kozakewich H, Bischoff J, Cataltepe S. Fatty acid binding protein 4 is a target of VEGF and a regulator of cell proliferation in endothelial cells. FASEB J. 2009;23:3865-3873
28. Carling D, Thornton C, Woods A, Sanders MJ. AMP-Activated protein kinase: New regulation, new roles? Biochem J. 2012;445:11-27
29. Huang G, Shi LZ, Chi H. Regulation of JNK and p38 MAPK in the immune system: Signal integration, propagation and termination. Cytokine. 2009;48:161-169
30. Wang Y, Huang G, Vogel P, Neale G, Reizis B, Chi H. Transforming growth factor beta-Activated kinase 1 (TAK1)-dependent checkpoint in the survival of dendritic cells promotes immune homeostasis and function. Proc Natl Acad Sci USA. 2012;109:E343-E352
31. Bar D, Apte RN, Voronov E, Dinarello CA, Cohen S. A continuous delivery system of IL-1 receptor antagonist reduces angiogenesis and inhibits tumor development. FASEB J. 2004;18:161-163
32. Arbiser JL, Petros J, Klafter R, Govindajaran B, McLaughlin ER, Brown LF, Cohen C, Moses M, Kilroy S, Arnold RS, Lambeth JD. Reactive oxygen generated by Nox1 triggers the angiogenic switch. Proc Natl Acad Sci USA. 2002;99:715-720
33. Wang Y, Zang QS, Liu Z, Wu Q, Maass D, Dulan G, Shaul PW, Melito L, Frantz DE, Kilgore JA, Williams NS, Terada LS, Nwariaku FE. Regulation of VEGF-induced endothelial cell migration by mitochondrial reactive oxygen species. Am J Physiol Cell Physiol. 2011;301:C695-C704
34. Kim KH, Park JY, Jung HJ, Kwon HJ. Identification and biological activities of a new antiangiogenic small molecule that suppresses mitochondrial reactive oxygen species. Biochem Biophys Res Commun. 2011;404:541-545
35. Kim SA, Choi HC. Metformin inhibits inflammatory response via AMPKPTEN pathway in vascular smooth muscle cells. Biochem Biophys Res Commun. 2012;425:866-872
36. Denu JM, Tanner KG. Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: Evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry. 1998;37:5633-5642
37. Park S, Scheffler TL, Rossie SS, Gerrard DE. AMPK activity is regulated by calcium-mediated protein phosphatase 2A activity. Cell Calcium. 2013;53:217-223
38. Colombo SL, Moncada S. AMPKalpha1 regulates the antioxidant status of vascular endothelial cells. Biochem J. 2009;421:163-169
39. Teng RJ, Du J, Afolayan AJ, Eis A, Shi Y, Konduri GG. AMP kinase activation improves angiogenesis in pulmonary artery endothelial cells with in utero pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol. 2013;304:L29-L42
40. Wang XR, Zhang MW, Chen DD, Zhang Y, Chen AF. AMP-Activated protein kinase rescues the angiogenic functions of endothelial progenitor cells via manganese superoxide dismutase induction in type 1 diabetes. Am J Physiol Endocrinol Metab. 2011;300:E1135-E1145
41. Salminen A, Kaarniranta K. AMP-Activated protein kinase (AMPK) controls the aging process via an integrated signaling network. Ageing Res Rev. 2012;11:230-241
42. Connor KM, Subbaram S, Regan KJ, Nelson KK, Mazurkiewicz JE, Bartholomew PJ, Aplin AE, Tai YT, Aguirre-Ghiso J, Flores SC, Melendez JA. Mitochondrial H2O2 regulates the angiogenic phenotype via PTEN oxidation. J Biol Chem. 2005;280:16916-16924
43. Lakshmanan AP, Harima M, Sukumaran V, Soetikno V, Thandavarayan RA, Suzuki K, Kodama M, Nagata M, Takagi R, Watanabe K. Modulation of AT-1R/AMPK-MAPK cascade plays crucial role for the pathogenesis of diabetic cardiomyopathy in transgenic type 2 diabetic (Spontaneous Diabetic Torii) rats. Biochem Pharmacol. 2012;83:653-660