Phosphorylation of Janus kinase 1 (JAK1) by AMP-activated protein kinase (AMPK) links energy sensing to anti-inflammatory signaling

Science Signaling

Volumn 9, Issue 453, 2016, Pages

  Rutherford, Claire ^a   Speirs, Claire ^a   Williams, Jamie J L ^b   Ewart, Marie Ann ^a,h   Mancini, Sarah J ^a   Hawley, Simon A ^c   Delles, Christian ^a   Viollet, Benoit ^d,e,f   Costa Pereira, Ana P ^g   Baillie, George S ^a   Salt, Ian P ^a   Palmer, Timothy M ^b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF BRADFORD   (United Kingdom)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d INSTITUT COCHIN   (France)

^e CNRS   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g HAMMERSMITH HOSPITAL   (United Kingdom)

^h AvantiCell Science Ltd   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; 6,7 DIHYDRO 4 HYDROXY 3 (2' HYDROXY 1,1' BIPHENYL 4 YL) 6 OXOTHIENO[2,3 B]PYRIDINE 5 CARBONITRILE; CCAAT ENHANCER BINDING PROTEIN EPSILON; GLYCOPROTEIN GP 130; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INTERLEUKIN 6; JANUS KINASE 1; MAMMALIAN TARGET OF RAPAMYCIN; METFORMIN; MITOGEN ACTIVATED PROTEIN KINASE 1; NITRIC OXIDE; ONCOSTATIN M; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN 14 3 3; SALICYLIC ACID; SERINE; STAT1 PROTEIN; STAT3 PROTEIN; JAK1 PROTEIN, MOUSE; STAT3 PROTEIN, MOUSE;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CATALYSIS; CELL CULTURE; ENZYME ACTIVATION; ENZYME INHIBITION; FIBROBLAST; FIBROSARCOMA CELL; GENE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; KINASE ASSAY; METABOLIC STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; VASCULAR ENDOTHELIAL CELL; AMINO ACID SUBSTITUTION; ANIMAL; CYTOLOGY; ENDOTHELIUM CELL; GENETICS; KNOCKOUT MOUSE; METABOLISM; MISSENSE MUTATION; MOUSE; PHOSPHORYLATION; PHYSIOLOGY;

14-3-3 PROTEINS; AMINO ACID SUBSTITUTION; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ENDOTHELIAL CELLS; ENZYME ACTIVATION; JANUS KINASE 1; MICE; MICE, KNOCKOUT; MUTATION, MISSENSE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84994908860     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aaf8566     Document Type: Article

References (74)

1. J. J. O'Shea, D. M. Schwartz, A. V. Villarino, M. Gadina, I. B. McInnes, A. Laurence, The JAK-STAT pathway: Impact on human disease and therapeutic intervention. Annu. Rev. Med. 66, 311-328 (2015).
2. C. Garbers, H. M. Hermanns, F. Schaper, G. Müller-Newen, J. Grötzinger, S. Rose-John, J. Scheller, Plasticity and cross-talk of interleukin 6-type cytokines. Cytokine Growth Factor Rev. 23, 85-97 (2012).
3. S. A. Jones, J. Scheller, S. Rose-John, Therapeutic strategies for the clinical blockade of IL-6/gp130 signaling. J. Clin. Invest. 121, 3375-3383 (2011).
4. R. Eulenfeld, A. Dittrich, C. Khouri, P. J. Müller, B. Mütze, A. Wolf, F. Schaper, Interleukin-6 signalling: More than Jaks and STATs. Eur. J. Cell Biol. 91, 486-495 (2012).
5. D. G. Hardie, AMP-activated protein kinase: Maintaining energy homeostasis at the cellular and whole-body levels. Annu. Rev. Nutr. 34, 31-55 (2014).
6. G. R. Steinberg, B. E. Kemp, AMPK in health and disease. Physiol. Rev. 89, 1025-1078 (2009).
7. L. Tong, Structure and function of biotin-dependent carboxylases. Cell. Mol. Life Sci. 70, 863-891 (2013).
8. K. Marcinko, G. R. Steinberg, The role of AMPK in controlling metabolism and mitochondrial biogenesis during exercise. Exp. Physiol. 99, 1581-1585 (2014).
9. E. Bess, B. Fisslthaler, T. Frömel, I. Fleming, Nitric oxide-induced activation of the AMP-activated protein kinase a2 subunit attenuates IkB kinase activity and inflammatory responses in endothelial cells. PLOS ONE 6, e20848 (2011).
10. B. Gongol, T. Marin, I.-C. Peng, B. Woo, M. Martin, S. King, W. Sun, D. A. Johnson, S. Chien, J. Y.-J. Shyy, AMPKa2 exerts its anti-inflammatory effects through PARP-1 and Bcl-6. Proc. Natl. Acad. Sci. U.S.A. 110, 3161-3166 (2013).
11. F. S. Gaskin, K. Kamada, M. Y. Zuidema, A. W. Jones, L. J. Rubin, R. J. Korthuis, Isoform-selective 5′-AMP-activated protein kinase-dependent preconditioning mechanisms to prevent postischemic leukocyte-endothelial cell adhesive interactions. Am. J. Physiol. Heart Circ. Physiol. 300, H1352-H1360 (2011).
12. S. Schuhmacher, M. Foretz, M. Knorr, T. Jansen, M. Hortmann, P. Wenzel, M. Oelze, A. L. Kleschyov, A. Daiber, J. F. Keaney, G. Wegener, K. Lackner, T. Münzel, B. Viollet, E. Schulz, a1AMP-activated protein kinase preserves endothelial function during chronic angiotensin II treatment by limiting Nox2 upregulation. Arterioscler. Thromb. Vasc. Biol. 31, 560-566 (2011).
13. A. Bai, M. Yong, A. G. Ma, Y. Ma, C. R. Weiss, Q. Guan, C. N. Bernstein, Z. Peng, Novel anti-inflammatory action of 5-aminoimidazole-4-carboxamide ribonucleoside with protective effect in dextran sulfate sodium-induced acute and chronic colitis. J. Pharmacol. Exp. Ther. 333, 717-725 (2010).
14. X. Zhao, J. W. Zmijewski, E. Lorne, G. Liu, Y.-J. Park, Y. Tsuruta, E. Abraham, Activation of AMPK attenuates neutrophil proinflammatory activity and decreases the severity of acute lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 295, L497-L504 (2008).
15. R. Prasad, S. Giri, N. Nath, I. Singh, A. K. Singh, 5-aminoimidazole-4-carboxamide-1-beta-4-ribofuranoside attenuates experimental autoimmune encephalomyelitis via modulation of endothelial-monocyte interaction. J. Neurosci. Res. 84, 614-625 (2006).
16. S. Galic, M. D. Fullerton, J. D. Schertzer, S. Sikkema, K. Marcinko, C. R. Walkley, D. Izon, J. Honeyman, Z.-P. Chen, B. J. van Denderen, B. E. Kemp, G. R. Steinberg, Hematopoietic AMPK b1 reduces mouse adipose tissue macrophage inflammation and insulin resistance in obesity. J. Clin. Invest. 121, 4903-4915 (2011).
17. Y. Zhang, J. Qiu, X. Wang, Y. Zhang, M. Xia, AMP-activated protein kinase suppresses endothelial cell inflammation through phosphorylation of transcriptional coactivator p300. Arterioscler. Thromb. Vasc. Biol. 31, 2897-2908 (2011).
18. H. Yu, H. Lee, A. Herrmann, R. Buettner, R. Jove, Revisiting STAT3 signalling in cancer: New and unexpected biological functions. Nat. Rev. Cancer 14, 736-746 (2014).
19. W. Vainchenker, S. N. Constantinescu, JAK/STAT signaling in hematological malignancies. Oncogene 32, 2601-2613 (2013).
20. G. Ortiz-Muñoz, J. L. Martin-Ventura, P. Hernandez-Vargas, B. Mallavia, V. Lopez-Parra, O. Lopez-Franco, B. Muñoz-Garcia, P. Fernandez-Vizarra, L. Ortega, J. Egido, C. Gomez-Guerrero, Suppressors of cytokine signaling modulate JAK/STAT-mediated cell responses during atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 29, 525-531 (2009).
21. M.-A. Ewart, C. F. Kohlhaas, I. P. Salt, Inhibition of tumor necrosis factor a-stimulated monocyte adhesion to human aortic endothelial cells by AMP-activated protein kinase. Arterioscler. Thromb. Vasc. Biol. 28, 2255-2257 (2008).
22. B. Enkhjargal, S. Godo, A. Sawada, N. Suvd, H. Saito, K. Noda, K. Satoh, H. Shimokawa, Endothelial AMP-activated protein kinase regulates blood pressure and coronary flow responses through hyperpolarization mechanism in mice. Arterioscler. Thromb. Vasc. Biol. 34, 1505-1513 (2014).
23. J. M. Corton, J. G. Gillespie, S. A. Hawley, D. G. Hardie, 5-Aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells? Eur. J. Biochem. 229, 558-565 (1995).
24. J. W. Scott, B. J. W. van Denderen, S. B. Jorgensen, J. E. Honeyman, G. R. Steinberg, J. S. Oakhill, T. J. Iseli, A. Koay, P. R. Gooley, D. Stapleton, B. E. Kemp, Thienopyridone drugs are selective activators of AMP-activated protein kinase b1-containing complexes. Chem. Biol. 15, 1220-1230 (2008).
25. M. R. Owen, E. Doran, A. P. Halestrap, Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem. J. 348, 607-614 (2000).
26. S. A. Hawley, M. D. Fullerton, F. A. Ross, J. D. Schertzer, C. Chevtzoff, K. J. Walker, M. W. Peggie, D. Zibrova, K. A. Green, K. J. Mustard, B. E. Kemp, K. Sakamoto, G. R. Steinberg, D. G. Hardie, The ancient drug salicylate directly activates AMP-activated protein kinase. Science 336, 918-922 (2012).
27. R. J. Ford, M. D. Fullerton, S. L. Pinkosky, E. A. Day, J. W. Scott, J. S. Oakhill, A. L. Bujak, B. K. Smith, J. D. Crane, R. M. Blümer, K. Marcinko, B. E. Kemp, H. C. Gerstein, G. R. Steinberg, Metformin and salicylate synergistically activate liver AMPK, inhibit lipogenesis and improve insulin sensitivity. Biochem. J. 468, 125-132 (2015).
28. A. Woods, D. Azzout-Marniche, M. Foretz, S. C. Stein, P. Lemarchand, P. Ferré, F. Foufelle, D. Carling, Characterization of the role of AMP-activated protein kinase in the regulation of glucose-activated gene expression using constitutively active and dominant negative forms of the kinase. Mol. Cell. Biol. 20, 6704-6711 (2000).
29. J. Yang, J. Huang, M. Dasgupta, N. Sears, M. Miyagi, B. Wang, M. R. Chance, X. Chen, Y. Du, Y. Wang, L. An, Q. Wang, T. Lu, X. Zhang, Z. Wang, G. R. Stark, Reversible methylation of promoter-bound STAT3 by histone-modifying enzymes. Proc. Natl. Acad. Sci. U.S.A. 107, 21499-21504 (2010).
30. C. A. Cantwell, E. Sterneck, P. F. Johnson, Interleukin-6-specific activation of the C/EBPd gene in hepatocytes is mediated by Stat3 and Sp1. Mol. Cell. Biol. 18, 2108-2117 (1998).
31. M. Jougasaki, T. Ichiki, Y. Takenoshita, M. Setoguchi, Statins suppress interleukin-6-induced monocyte chemo-attractant protein-1 by inhibiting Janus kinase/signal transducers and activators of transcription pathways in human vascular endothelial cells. Br. J. Pharmacol. 159, 1294-1303 (2010).
32. M. Romano, M. Sironi, C. Toniatti, N. Polentarutti, P. Fruscella, P. Ghezzi, R. Faggioni, W. Luini, V. van Hinsbergh, S. Sozzani, F. Bussolino, V. Poli, G. Ciliberto, A. Mantovani, Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity 6, 315-325 (1997).
33. E. C. Borden, G. C. Sen, G. Uze, R. H. Silverman, R. M. Ransohoff, G. R. Foster, G. R. Stark, Interferons at age 50: Past, current and future impact on biomedicine. Nat. Rev. Drug Discov. 6, 975-990 (2007).
34. M. C. Gauzzi, L. Velazquez, R. McKendry, K. E. Mogensen, M. Fellous, S. Pellegrini, Interferon-a-dependent activation of Tyk2 requires phosphorylation of positive regulatory tyrosines by another kinase. J. Biol. Chem. 271, 20494-20500 (1996).
35. S. A. Hawley, M. Davison, A. Woods, S. P. Davies, R. K. Beri, D. Carling, D. G. Hardie, Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMPactivated protein kinase. J. Biol. Chem. 271, 27879-27887 (1996).
36. K. M. Brown, L. C. Y. Lee, J. E. Findlay, J. P. Day, G. S. Baillie, Cyclic AMP-specific phosphodiesterase, PDE8A1, is activated by protein kinase A-mediated phosphorylation. FEBS Lett. 586, 1631-1637 (2012).
37. J. W. Scott, D. G. Norman, S. A. Hawley, L. Kontogiannis, D. G. Hardie, Protein kinase substrate recognition studied using the recombinant catalytic domain of AMP-activated protein kinase and a model substrate. J. Mol. Biol. 317, 309-323 (2002).
38. D. M. Gwinn, D. B. Shackelford, D. F. Egan, M. M. Mihaylova, A. Mery, D. S. Vasquez, B. E. Turk, R. J. Shaw, AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell 30, 214-226 (2008).
39. R. Ferrao, H. J. A. Wallweber, H. Ho, C. Tam, Y. Franke, J. Quinn, P. J. Lupardus, The structural basis for class II cytokine receptor recognition by JAK1. Structure 24, 897-905 (2016).
40. R. McNally, A. V. Toms, M. J. Eck, T. J. Boggon, Crystal structure of the FERM-SH2 module of human Jak2. PLOS ONE 11, e0156218 (2016).
41. H. J. A. Wallweber, C. Tam, Y. Franke, M. A. Starovasnik, P. J. Lupardus, Structural basis of recognition of interferon-a receptor by tyrosine kinase 2. Nat. Struct. Mol. Biol. 21, 443-448 (2014).
42. Z. Chen, I.-C. Peng, W. Sun, M.-I. Su, P.-H. Hsu, Y. Fu, Y. Zhu, K. DeFea, S. Pan, M.-D. Tsai, J. Y.-J. Shyy, AMP-activated protein kinase functionally phosphorylates endothelial nitric oxide synthase Ser633. Circ. Res. 104, 496-505 (2009).
43. D. Bridges, G. B. G. Moorhead, 14-3-3 proteins: A number of functions for a numbered protein. Sci. Signal. 2005, re10 (2005).
44. V. K. Weerasekara, D. J. Panek, D. G. Broadbent, J. B. Mortenson, A. D. Mathis, G. N. Logan, J. T. Prince, D. M. Thomson, J. W. Thompson, J. L. Andersen, Metabolic-stress-induced rearrangement of the 14-3-3z interactome promotes autophagy via a ULK1- and AMPKregulated 14-3-3z interaction with phosphorylated Atg9. Mol. Cell. Biol. 34, 4379-4388 (2014).
45. H. I. D. Mack, B. Zheng, J. M. Asara, S. M. Thomas, AMPK-dependent phosphorylation of ULK1 regulates ATG9 localization. Autophagy 8, 1197-1214 (2012).
46. M. Müller, J. Briscoe, C. Laxton, D. Guschin, A. Ziemiecki, O. Silvennoinen, A. G. Harpur, G. Barbieri, B. A. Witthuhn, C. Schindler, The protein tyrosine kinase JAK1 complements defects in interferon-a/b and -g signal transduction. Nature 366, 129-135 (1993).
47. D. Guschin, N. Rogers, J. Briscoe, B. Witthuhn, D. Watling, F. Horn, S. Pellegrini, K. Yasukawa, P. Heinrich, G. R. Stark, A major role for the protein tyrosine kinase JAK1 in the JAK/STAT signal transduction pathway in response to interleukin-6. EMBO J. 14, 1421-1429 (1995).
48. K. R. Laderoute, K. Amin, J. M. Calaoagan, M. Knapp, T. Le, J. Orduna, M. Foretz, B. Viollet, 5′-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments. Mol. Cell. Biol. 26, 5336-5347 (2006).
49. C. G. Mullighan, J. Zhang, R. C. Harvey, J. R. Collins-Underwood, B. A. Schulman, L. A. Phillips, S. K. Tasian, M. L. Loh, X. Su, W. Liu, M. Devidas, S. R. Atlas, I.-M. Chen, R. J. Clifford, D. S. Gerhard, W. L. Carroll, G. H. Reaman, M. Smith, J. R. Downing, S. P. Hunger, C. L. Willman, JAK mutations in high-risk childhood acute lymphoblastic leukemia. Proc. Natl. Acad. Sci. U.S.A. 106, 9414-9418 (2009).
50. O. Silvennoinen, S. R. Hubbard, Molecular insights into regulation of JAK2 in myeloproliferative neoplasms. Blood 125, 3388-3392 (2015).
51. L. A. J. O'Neill, D. G. Hardie, Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature 493, 346-355 (2013).
52. M. Dandapani, D. G. Hardie, AMPK: Opposing the metabolic changes in both tumour cells and inflammatory cells? Biochem. Soc. Trans. 41, 687-693 (2013).
53. Y. D. Kim, Y. H. Kim, Y. M. Cho, D. K. Kim, S. W. Ahn, J. M. Lee, D. Chanda, M. Shong, C. H. Lee, H. S. Choi, Metformin ameliorates IL-6-induced hepatic insulin resistance via induction of orphan nuclear receptor small heterodimer partner (SHP) in mouse models. Diabetologia 55, 1482-1494 (2012).
54. Y. D. Kim, Y.-H. Kim, S. Tadi, J. H. Yu, Y.-H. Yim, N. H. Jeoung, M. Shong, L. Hennighausen, R. A. Harris, I.-K. Lee, C.-H. Lee, H.-S. Choi, Metformin inhibits growth hormone-mediated hepatic PDK4 gene expression through induction of orphan nuclear receptor small heterodimer partner. Diabetes 61, 2484-2494 (2012).
55. A. Nerstedt, E. Cansby, M. Amrutkar, U. Smith, M. Mahlapuu, Pharmacological activation of AMPK suppresses inflammatory response evoked by IL-6 signalling in mouse liver and in human hepatocytes. Mol. Cell. Endocrinol. 375, 68-78 (2013).
56. A. Nerstedt, A. Johansson, C. X. Andersson, E. Cansby, U. Smith, M. Mahlapuu, AMPactivated protein kinase inhibits IL-6-stimulated inflammatory response in human liver cells by suppressing phosphorylation of signal transducer and activator of transcription 3 (STAT3). Diabetologia 53, 2406-2416 (2010).
57. C. He, H. Li, B. Viollet, M.-H. Zou, Z. Xie, AMP suppresses vascular inflammation in vivo by inhibiting signal transducer and activator of transcription-1. Diabetes 64, 4285-4297 (2015).
58. K. Inoki, T. Zhu, K.-L. Guan, TSC2 mediates cellular energy response to control cell growth and survival. Cell 115, 577-590 (2003).
59. R. J. Shaw, N. Bardeesy, B. D. Manning, L. Lopez, M. Kosmatka, R. A. DePinho, L. C. Cantley, The LKB1 tumor suppressor negatively regulates mTOR signaling. Cancer Cell 6, 91-99 (2004).
60. A. Mukhopadhyay, K. C. Berrett, U. Kc, P. M. Clair, S. M. Pop, S. R. Carr, B. L. Witt, T. G. Oliver, Sox2 cooperates with Lkb1 loss in a mouse model of squamous cell lung cancer. Cell Rep. 8, 40-49 (2014).
61. Y. Q. Wang, W. M. Dai, X. Y. Chu, B. Yang, M. Zhao, Y. Sun, Downregulation of LKB1 suppresses Stat3 activity to promote the proliferation of esophageal carcinoma cells. Mol. Med. Rep. 9, 2400-2404 (2014).
62. D. W. Kim, H. K. Chung, K. C. Park, J. H. Hwang, Y. S. Jo, J. Chung, D. V. Kalvakolanu, N. Resta, M. Shong, Tumor suppressor LKB1 inhibits activation of signal transducer and activator of transcription 3 (STAT3) by thyroid oncogenic tyrosine kinase rearranged in transformation (RET)/papillary thyroid carcinoma (PTC). Mol. Endocrinol. 21, 3039-3049 (2007).
63. M. Momcilovic, D. B. Shackelford, Targeting LKB1 in cancer - exposing and exploiting vulnerabilities. Br. J. Cancer 113, 574-584 (2015).
64. D. F. Egan, D. B. Shackelford, M. M. Mihaylova, S. Gelino, R. A. Kohnz, W. Mair, D. S. Vasquez, A. Joshi, D. M. Gwinn, R. Taylor, J. M. Asara, J. Fitzpatrick, A. Dillin, B. Viollet, M. Kundu, M. Hansen, R. J. Shaw, Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331, 456-461 (2011).
65. E. Flex, V. Petrangeli, L. Stella, S. Chiaretti, T. Hornakova, L. Knoops, C. Ariola, V. Fodale, E. Clappier, F. Paoloni, S. Martinelli, A. Fragale, M. Sanchez, S. Tavolaro, M. Messina, G. Cazzaniga, A. Camera, G. Pizzolo, A. Tornesello, M. Vignetti, A. Battistini, H. Cavé, B. D. Gelb, J.-C. Renauld, A. Biondi, S. N. Constantinescu, R. Foà, M. Tartaglia, Somatically acquired JAK1 mutations in adult acute lymphoblastic leukemia. J. Exp. Med. 205, 751-758 (2008).
66. W. A. Sands, H. D. Woolson, S. J. Yarwood, T. M. Palmer, Exchange protein directly activated by cyclic AMP-1-regulated recruitment of CCAAT/enhancer-binding proteins to the suppressor of cytokine signaling-3 promoter. Methods Mol. Biol. 809, 201-214 (2012).
67. S. J. Yarwood, G. Borland, W. A. Sands, T. M. Palmer, Identification of CCAAT/enhancerbinding proteins as exchange protein activated by cAMP-activated transcription factors that mediate the induction of the SOCS-3 gene. J. Biol. Chem. 283, 6843-6853 (2008).
68. M. M. A. Safhi, C. Rutherford, C. Ledent, W. A. Sands, T. M. Palmer, Priming of signal transducer and activator of transcription proteins for cytokine-triggered polyubiquitylation and degradation by the A2A adenosine receptor. Mol. Pharmacol. 77, 968-978 (2010).
69. J. A. Reihill, M.-A. Ewart, I. P. Salt, The role of AMP-activated protein kinase in the functional effects of vascular endothelial growth factor-A and -B in human aortic endothelial cells. Vascular Cell 3, 9 (2011).
70. W. A. Sands, A. F. Martin, E. W. Strong, T. M. Palmer, Specific inhibition of nuclear factor-kB-dependent inflammatory responses by cell type-specific mechanisms upon A2A adenosine receptor gene transfer. Mol. Pharmacol. 66, 1147-1159 (2004).
71. H. D. Woolson, V. S. Thomson, C. Rutherford, S. J. Yarwood, T. M. Palmer, Selective inhibition of cytokine-activated extracellular signal-regulated kinase by cyclic AMP via Epac1-dependent induction of suppressor of cytokine signalling-3. Cell. Signal. 21, 1706-1715 (2009).
72. C. Rutherford, S. Childs, J. Ohotski, L. McGlynn, M. Riddick, S. MacFarlane, D. Tasker, S. Pyne, N. J. Pyne, J. Edwards, T. M. Palmer, Regulation of cell survival by sphingosine-1-phosphates receptor S1P1 via reciprocal ERK-dependent suppression of Bim and PI-3-kinase/protein kinase C-mediated upregulation of Mcl-1. Cell Death Dis. 4, e927 (2013).
73. Y. Y. Sin, T. P. Martin, L. Wills, S. Currie, G. S. Baillie, Small heat shock protein 20 (Hsp20) facilitates nuclear import of protein kinase D 1 (PKD1) during cardiac hypertrophy. Cells Commun. Signal 13, 16 (2015).
74. B. Wang, H. Yang, Y.-C. Liu, T. Jelinek, L. Zhang, E. Ruoslahti, H. Fu, Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. Biochemistry 38, 12499-12504-12504 (1999).