Investigation of salicylate hepatic responses in comparison with chemical analogues of the drug

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1862, Issue 8, 2016, Pages 1412-1422

  Cameron, Amy R ^a   Logie, Lisa ^a   Patel, Kashyap ^a,b   Bacon, Sandra ^a,c,h   Forteath, Calum ^a   Harthill, Jean ^a   Roberts, Adam ^a   Sutherland, Calum ^a   Stewart, Derek ^c,d   Viollet, Benoit ^e,f   Sakamoto, Kei ^b,g   McDougall, Gordon ^c   Foretz, Marc ^e,f   Rena, Graham ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^d HERIOT WATT UNIVERSITY   (United Kingdom)

^e INSTITUT COCHIN   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g NESTLÉ RESEARCH CENTER   (Switzerland)

^h UNIVERSITY OF EXETER MEDICAL SCHOOL   (United Kingdom)

Author keywords

AMPK; Gluconeogenesis; MTOR signalling; NF B signalling; Salicylate

Indexed keywords

GAMMA RESORCYLIC ACID; GLUCOSE; GLUCOSE 6 PHOSPHATASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; SALICYLIC ACID; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; DRUG MECHANISM; ENZYME DEGRADATION; GLUCONEOGENESIS; HUMAN; HUMAN CELL; LIVER CELL; PRIORITY JOURNAL;

EID: 84966440558     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2016.04.015     Document Type: Article

References (55)

1. Logie L., Harthill J., Patel K., Bacon S., McDougall G., Hamilton D.L., Macrae K., Wang H.-H., Xue L., Jiang H., Sakamoto K., Prescott A.R., Rena G. Cellular responses to the metal-binding properties of metformin. Diabetes 2012, 61:1423-1433.
2. Rena G., Pearson E.R., Sakamoto K. Molecular action and pharmacogenetics of metformin: current understanding of an old drug. Diabetes Manag. 2012, 2:439-452.
3. Rena G., Pearson E.R., Sakamoto K. Molecular mechanism of action of metformin: old or new insights?. Diabetologia 2013, 56:1898-1906.
4. Mitchell J.A., Saunders M., Barnes P.J., Newton R., Belvisi M.G. Sodium salicylate inhibits cyclo-oxygenase-2 activity independently of transcription factor (nuclear factor κB) activation: role of arachidonic acid. Mol. Pharmacol. 1997, 51:907-912.
5. Zhou G., Myers R., Li Y., Chen Y., Shen X., Fenyl-Melody J., Wu M., Ventre J., Doebber T., Fujii N., Musi N., Hirshman M.F., Goodyear L.J., Moller D.E. Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest. 2001, 108:1167-1174.
6. Hawley S.A., Gadalla A.E., Olsen G.S., Hardie D.G. The antidiabetic drug metformin activates the AMP-activated protein kinase cascade via an adenine nucleotide-independent mechanism. Diabetes 2002, 51:2420-2425.
7. Fryer L.G.D., Parbu-Patel A., Carling D. The anti-diabetic drugs rosiglitazone and metformin stimulate AMP-activated protein kinase through distinct signaling pathways. J. Biol. Chem. 2002, 277:25226-25232.
8. Boyle J.G., Logan P.J., Ewart M.A., Reihill J.A., Ritchie S.A., Connell J.M.C., Cleland S.J., Salt I.P. Rosiglitazone stimulates nitric oxide synthesis in human aortic endothelial cells via AMP-activated protein kinase. J. Biol. Chem. 2008, 283:11210-11217. (17, 11210-11217).
9. Rena G., Sakamoto K. Salicylic acid: old and new implications for the treatment of type 2 diabetes?. Diabetol. Int. 2014, 1-7.
10. Hardie D.G., Ross F.A., Hawley S.A. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 2012, 13:251-262.
11. Hardie D.G., Sakamoto K. AMPK: a key sensor of fuel and energy status in skeletal muscle. Physiology (Bethesda, Md) 2006, 21:48-60.
12. Hawley S.A., Fullerton M.D., Ross F.A., Schertzer J.D., Chevtzoff C., Walker K.J., Peggie M.W., Zibrova D., Green K.A., Mustard K.J., Kemp B.E., Sakamoto K., Steinberg G.R., Hardie D.G. The ancient drug salicylate directly activates AMP-activated protein kinase. Science 2012, 918-922.
13. Brody T. Action of sodium salicylate and related compounds on tissue metabolism in vitro. J. Pharmacol. Exp. Ther. 1956, 117:39-51.
14. Smith M.J.H., Meade B.W. The effect of salicylate on glycosuria, blood glucose and liver glycogen of the alloxan-diabetic rat. Biochem. J. 1952, 51:18-20.
15. Mahler R.F. Chemistry of hypoglycaemic substances other than insulin. Br. Med. Bull. 1960, 16:250-254.
16. Meade B.W. Effect of certain hydroxybenzoic acids on the oxygen consumption of Wistar rats. Ann. Rheum. Dis. 1954, 13:60-62.
17. Woods H.F., Stubbs W.A., Johnson G., Alberti K.G.M.M. Inhibition by salicylate of gluconeogenesis in the isolated perfused rat liver. Clin. Exp. Pharmacol. Physiol. 1974, 1:535-540.
18. Schwenger P., Alpert D., Skolnik E.Y., Vilcek J. Activation of p38 mitogen-activate protein kinase by sodium salicylate leads to inhibition of tumour necrosis factor-induced I kappa B alpha phosphorylation and degradation. Mol. Cell. Biol. 1998, 18:78-84.
19. Yin M.-J., Yamamoto Y., Gaynor R.B. The anti-inflammatory agents aspirin and salicylate inhibit the activity of I kappa B kinase-beta. Nature 1998, 396:77-80.
20. Yuan M., Konstantopoulos N., Lee J., Hansen L., Li Z.-W., Karin M., Shoelson S. Reversal of obesity and diet-induced insulin resistance with salicylates or targeted disruption of Ikk beta. Science 2001, 293:1673-1677.
21. Grempler R., Kienitz A., Werner T., Meyer M., Barthel A., Ailett F., Sutherland C., Walther R., Schmoll D. Tumour necrosis factor alpha decreases glucose 6-phosphatase gene expression by activation of nuclear factor kappa B. Biochem. J. 2004, 382:471-479.
22. Foretz M., Hébrard S., Leclerc J., Zarrinpashneh E., Soty M., Mithieux G., Sakamoto K., Andreelli F., Viollet B. Metformin inhibits hepatic gluconeogenesis in mice independently of the LKB1/AMPK pathway via a decrease in hepatic energy state. J. Clin. Invest. 2010, 120:2355-2369.
23. Cameron A.R., Anil S., Sutherland E., Harthill J., Rena G. Zinc-dependent effects of small molecules on the insulin-sensitive transcription factor FOXO1a and gluconeogenic genes. Metallomics 2010, 2:195-203.
24. Cameron A.R., Anton S., Melville L., Houston N.P., Dayal S., McDougall G.J., Stewart D., Rena G. Black tea polyphenols mimic insulin/IGF-1 signalling to the longevity factor FOXO1a. Aging Cell 2008, 7:69-77.
25. Cameron A.R., Wallace K., Logie L., Prescott A.R., Unterman T.G., Harthill J., Rena G. The antineurodegenerative agent clioquinol regulates the transcription factor FOXO1a. Biochem. J. 2012, 443:57-64.
26. Rena G., Guo S.D., Cichy S.C., Unterman T.G., Cohen P. Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J. Biol. Chem. 1999, 274:17179-17183.
27. Rena G., Prescott A.R., Guo S.D., Cohen P., Unterman T.G. Roles of the forkhead in rhabdomyosarcoma (FKHR) phosphorylation sites in regulating 14-3-3 binding, transactivation and nuclear targetting. Biochem. J. 2001, 354:605-612.
28. Hunter R.W., Treebak J.T., Wojtaszewski J.F.P., Sakamoto K. Molecular mechanism by which AMP-activated protein kinase activation promotes glycogen accumulation in muscle. Diabetes 2011, 60:766-774.
29. Sutherland C. Analysis of signal transduction pathways using molecular biological manipulations. Protein Phosphorylation: A Practical Approach 1999, Oxford University Press, London, New York. D.G. Hardie (Ed.).
30. Patel S., Lochhead P., Rena G., Sutherland C. Antagonistic effects of phorbol esters on insulin regulation of insulin-like growth factor-binding protein-1 (IGFBP-1) but not glucose-6-phosphatase gene expression. Biochem. J. 2001, 359:611-619.
31. Patel S., Lochhead P.A., Rena G., Fumagalli S., Pende M., Kozma S.C., Thomas G., Sutherland C. Insulin regulation of insulin-like growth factor-binding protein-1 gene expression is dependent on the mammalian target of rapamycin, but independent of ribosomal S6 kinase activity. J. Biol. Chem. 2002, 277:9889-9895.
32. Patel S., Lipina C., Sutherland C. Different mechanisms are used by insulin to repress three genes that contain homologous thymine-rich insulin response elements. FEBS Lett. 2003, 549:72-76.
33. Kalender A., Selvaraj A., Kim S.Y., Gulati P., Brule S., Viollet B., Kemp B.E., Bardeesy N., Dennis P., Schlager J.J., Marette A., Kozma S.C., Thomas G. Metformin, independent of AMPK, inhibits mTORC1 in a rag GTPase-dependent manner. Cell Metab. 2010, 11:390-401.
34. Kickstein E., Krauss S., Thornhill P., Rutschow D., Zeller R., Sharkey J., Williamson R., Fuchs M., Kohler A., Glossmann H., Schneider R., Sutherland C., Scheweiger S. Biguanide metformin acts on tau phosphorylation via mTOR/protein phosphatase (PP2A) signaling. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:21830-21835.
35. Dowling R.J.O., Zakikhani M., Fantus I.G., Pollak M., Sonenberg N. Metformin inhibits mammalian target of rapamycin-dependent translation initiation in breast cancer cells. Cancer Res. 2007, 67:10804-10812.
36. Reid J., Watson R.D., Cochran J.B., Sproull D.H. Sodium gamma-resorcylate in rheumatic fever. Br. Med. J. 1951, 2:321-326.
37. Clarke N.E., Mosher R.E., Clarke C.N. Phenolic compounds in the treatment of rheumatic fever. I. A study of gentisic acid derivatives. Circulation 1953, 7:247-257.
38. Schaefer L.E., Rashkoff I.A., Megibow R.S. Sodium gentisate in the treatment of acute rheumatic fever. Circulation 1950, 2:265-270.
39. Whitehouse M.W., Dean P.D.G. Biochemical properties of anti-inflammatory drugs-V. Biochem. Pharmacol. 1965, 14:557-567.
40. Fang V., Foye W.O., Robinson S.M., Jenkins H.J. Hypoglycemic activity and chemical structure of the salicylates. J. Pharm. Sci. 1968, 57:2111-2116.
41. Clark K., Peggie M., Plater L., Sorcek R.J., Young E.R.R., Madwed J.B., Hough J., McIver E.G., Cohen P. Novel cross-talk within the IKK family controls innate immunity. Biochem. J. 2011, 434:93-104.
42. Goransson O., McBride A., Hawley S.A., Ross F.A., Shpiro N., Foretz M., Viollet B., Hardie D.G., Sakamoto K. Mechanism of action of A-769662, a valuable tool for activation of AMP-activated protein kinase. J. Biol. Chem. 2007, 282:32549-32560.
43. Reid J. Dinitrophenol and diabetes mellitus: a comparison with salicylate. Br. Med. J. 1958, 2:724-727.
44. Suzaki T., Iyanagi T., Kobayashi S. Effect of 2,4-dinitrophenol on the oxidative metabolism of hexobarbital by cytochrome P-450 in perfused rat liver. J. Biochem. 1983, 94:361-371.
45. Sibille B., Keriel C., Fontaine E., Catelloni F., Rigoulet M., Leverve X.M. Octanoate affects 2,4-dinitrophenol uncoupling in intact isolated rat hepatocytes. Eur. J. Biochem. 1995, 231:498-502.
46. Salminen A., Hyttinen J.M.T., Kaarniranta K. AMP-activated protein kinase inhibits NF-κB signaling and inflammation: impact on healthspan and lifespan. J. Mol. Med. 2011, 89:667-676.
47. Hundal R.S., Peterson K.F., Mayerson A.B., Randhawa P.S., Inzucchi S., Shoelson S., Shulman G.I. Mechanism by which high-dose aspirin improves glucose metabolism in type 2 diabetes. J. Clin. Invest. 2002, 109:1321-1326.
48. Brune K., Rainsford K.D., Schweitzer A. Biodistribution of mild analgesics. Br. J. Clin. Pharmacol. 1980, 10:279S-284S.
49. Rainsford K.D., Schweitzer A., Brune K. Distribution of the acetyl compared with the salicyl moiety of acetylsalicylic acid: acetylation of macromolecules in organs wherein side-effects are manifest. Biochem. Pharmacol. 1983, 32:1301-1308.
50. Wolff J., Austen F.K. Salicylates and thyroid function. II. The Effect on the Thyroid-Pituitary Interrelation. J. Clin. Invest. 1958, 37:1144-1152.
51. Koska J., Ortega E., Bunt J.C., Gasser A., Impson J., Hanson R.L., Forbes J., de Courten B., Krakoff J. The effect of salsalate on insulin action and glucose tolerance in obese non-diabetic patients: results of a randomised double-blind placebo-controlled study. Diabetologia 2009, 52:385-393.
52. Brunmair B., Staniek K., Gras F., Scharf N., Althaym A., Clara R., Roden M., Gnaiger E., Nohl H., Waldhausl W., Furnsinn C. Thiazolidinediones, like metformin, inhibit respiratory complex I: a common mechanism contributing to their antidiabetic actions?. Diabetes 2004, 53:1052-1059.
53. Andrews M.M. The glycogenolytic activity of some substituted salicylic acids. Biochem. J. 1960, 75:298-303.
54. Kim J.K., Kim Y.-J., Fillmore J.J., Chen Y., Moore I., Lee J., Yuan M., Li Z.W., Karin M., Perret P., Shoelson S.E., Shulman G.I. Prevention of fat-induced insulin resistance by salicylate. J. Clin. Invest. 2001, 108:437-446.
55. Arkan M.C., Hevener A.L., Greten F.R., Maeda S., Li Z.-W., Long J.M., Wynshaw-Boris A., Poli G., Olefsky J., Karin M. IKK-[beta] links inflammation to obesity-induced insulin resistance. Nat. Med. 2005, 11:191-198.