Glabridin, an isoflavan from licorice root, downregulates iNOS expression and activity under high-glucose stress and inflammation

Molecular Nutrition and Food Research

Volumn 59, Issue 6, 2015, Pages 1041-1052

  Yehuda, Itamar ^a,b   Madar, Zecharia ^b   Leikin Frenkel, Alicia ^c,d   Tamir, Snait ^a,e  

^a MIGAL GALILEE TECHNOLOGY CENTER   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

^d SHEBA MEDICAL CENTER   (Israel)

^e TEL HAI COLLEGE   (Israel)

Author keywords

Chronic glucose stress; Glabridin; Inducible nitric oxide synthase; Inflammation; Oxidative stress

Indexed keywords

GLYCYRRHIZA;

3-NITROTYROSINE; ANTIINFLAMMATORY AGENT; GLABRIDIN; GLUCOSE BLOOD LEVEL; INDUCIBLE NITRIC OXIDE SYNTHASE; ISOFLAVONE DERIVATIVE; LIPOPOLYSACCHARIDE; MESSENGER RNA; NITRIC OXIDE; NOS2 PROTEIN, MOUSE; PHENOL DERIVATIVE; TUMOR NECROSIS FACTOR ALPHA; TYROSINE;

ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CHEMICALLY INDUCED; CHEMISTRY; DISEASE MODEL; DOWN REGULATION; DRUG EFFECTS; FEMALE; GENETICS; GLUCOSE BLOOD LEVEL; GLYCYRRHIZA; HYPERGLYCEMIA; INFLAMMATION; LIPID DIET; LIVER; MACROPHAGE; METABOLISM; MOUSE; OXIDATIVE STRESS; PHYSIOLOGICAL STRESS; PLANT ROOT; SECRETION (PROCESS); UPREGULATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BLOOD GLUCOSE; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; GLYCYRRHIZA; HYPERGLYCEMIA; INFLAMMATION; ISOFLAVONES; LIPOPOLYSACCHARIDES; LIVER; MACROPHAGES; MICE; MICE, INBRED C57BL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; PHENOLS; PLANT ROOTS; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; TUMOR NECROSIS FACTOR-ALPHA; TYROSINE; UP-REGULATION;

EID: 84930181123     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201400876     Document Type: Article

References (41)

1. Shoelson, S. E., Lee, J., Goldfine, A. B., Inflammation and insulin resistance. J. Clin. Invest. 2006, 116, 1793-1801.
2. Tabit, C. E., Chung, W. B., Hamburg, N. M., Vita, J. A., Endothelial dysfunction in diabetes mellitus: molecular mechanisms and clinical implications. Rev. Endocr. Metab. Disord. 2010, 11, 61-74.
3. Jay, D., Hitomi, H., Griendling, K. K., Oxidative stress and diabetic cardiovascular complications. Free Radic. Biol. Med. 2006, 40, 183-192.
4. Wellen, K. E., Hotamisligil, G. S., Inflammation, stress, and diabetes. J. Clin. Invest. 2005, 115, 1111-1119.
5. Forstermann, U., Nitric oxide and oxidative stress in vascular disease. Pflugers Arch. 2010, 459, 923-939.
6. Pitocco, D., Zaccardi, F., Di Stasio, E., Romitelli, F. et al., Oxidative stress, nitric oxide, and diabetes. Rev. Diabet. Stud. 2010, 7, 15-25.
7. Pacher, P., Beckman, J. S., Liaudet, L., Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 2007, 87, 315-424.
8. Naseem, K. M., The role of nitric oxide in cardiovascular diseases. Mol. Aspects Med. 2005, 26, 33-65.
9. Sharov, V. S., Pal, R., Dremina, E. S., Michaelis, E. K. et al., Fluorogenic tagging of protein 3-nitrotyrosine with 4-(aminomethyl)benzene sulfonate in tissues: a useful alternative to immunohistochemistry for fluorescence microscopy imaging of protein nitration. Free Radic. Biol. Med. 2012, 53, 1877-1885.
10. Beckman, J. S., Koppenol, W. H., Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am. J. Physiol. 1996, 271, C1424-C1437.
11. Du, Y., Smith, M. A., Miller, C. M., Kern, T. S., Diabetes-induced nitrative stress in the retina, and correction by aminoguanidine. J. Neurochem. 2002, 80, 771-779.
12. Gong, L., Liu, F. Q., Wang, J., Wang, X. P. et al., Hyperglycemia induces apoptosis of pancreatic islet endothelial cells via reactive nitrogen species-mediated Jun N-terminal kinase activation. Biochim. Biophys. Acta 2011, 1813, 1211-1219.
13. Zou, M. H., Shi, C., Cohen, R. A., High glucose via peroxynitrite causes tyrosine nitration and inactivation of prostacyclin synthase that is associated with thromboxane/prostaglandin H(2) receptor-mediated apoptosis and adhesion molecule expression in cultured human aortic endothelial cells. Diabetes 2002, 51, 198-203.
14. Stevens, M. J., Oxidative-nitrosative stress as a contributing factor to cardiovascular disease in subjects with diabetes. Curr. Vasc. Pharmacol. 2005, 3, 253-266.
15. Bolego, C., Cignarella, A., Zancan, V., Pinna, C. et al., Diabetes abolishes the vascular protective effects of estrogen in female rats. Life Sci. 1999, 64, 741-749.
16. Maggi, A., Cignarella, A., Brusadelli, A., Bolego, C. et al., Diabetes undermines estrogen control of inducible nitric oxide synthase function in rat aortic smooth muscle cells through overexpression of estrogen receptor-beta. Circulation 2003, 108, 211-217.
17. Barrett-Connor, E., Giardina, E. G., Gitt, A. K., Gudat, U. et al., Women and heart disease: the role of diabetes and hyperglycemia. Arch. Intern. Med. 2004, 164, 934-942.
18. Chakrabarti, S., Morton, J. S., Davidge, S. T., Mechanisms of estrogen effects on the endothelium: an overview. Can. J. Cardiol. 2014, 30, 705-712.
19. Cignarella, A., Kratz, M., Bolego, C., Emerging role of estrogen in the control of cardiometabolic disease. Trends Pharmacol. Sci. 2010, 31, 183-189.
20. Mukhopadhyay, S., Mukherjee, T. K., Bridging advanced glycation end product, receptor for advanced glycation end product and nitric oxide with hormonal replacement/estrogen therapy in healthy versus diabetic postmenopausal women: a perspective. Biochim. Biophys. Acta 2005, 1745, 145-155.
21. Sztejnsznajd, C., Silva, M. E., Nussbacher, A., Gebara, O. E. et al., Estrogen treatment improves arterial distensibility, fibrinolysis, and metabolic profile in postmenopausal women with type 2 diabetes mellitus. Metabolism 2006, 55, 953-959.
22. Moreira, A. C., Silva, A. M., Santos, M. S., Sardao, V. A., Phytoestrogens as alternative hormone replacement therapy in menopause: what is real, what is unknown. J. Steroid Biochem. Mol. Biol. 2014, 143, 61-71.
23. Cederroth, C. R., Vinciguerra, M., Gjinovci, A., Kuhne, F. et al., Dietary phytoestrogens activate AMP-activated protein kinase with improvement in lipid and glucose metabolism. Diabetes 2008, 57, 1176-1185.
24. Sacks, F. M., Lichtenstein, A., VanHorn, L., Harris, W. et al., Soy protein, isoflavones, and cardiovascular health: an American Heart Association Science Advisory for professionals from the Nutrition Committee. Circulation 2006, 113, 1034-1044.
25. Simmler, C., Pauli, G. F., Chen, S. N., Phytochemistry and biological properties of glabridin. Fitoterapia 2013, 90, 160-184.
26. Kang, J. S., Yoon, Y. D., Cho, I. J., Han, M. H. et al., Glabridin, an isoflavan from licorice root, inhibits inducible nitric-oxide synthase expression and improves survival of mice in experimental model of septic shock. J. Pharmacol. Exp. Ther. 2005, 312, 1187-1194.
27. Somjen, D., Knoll, E., Vaya, J., Stern, N. et al., Estrogen-like activity of licorice root constituents: glabridin and glabrene, in vascular tissues in vitro and in vivo. J. Steroid Biochem. Mol. Biol. 2004, 91, 147-155.
28. Yehuda, I., Madar, Z., Szuchman-Sapir, A., Tamir, S., Glabridin, a phytoestrogen from licorice root, up-regulates manganese superoxide dismutase, catalase and paraoxonase 2 under glucose stress. Phytother. Res. 2011, 25, 659-667.
29. Park, E. K., Jung, H. S., Yang, H. I., Yoo, M. C. et al., Optimized THP-1 differentiation is required for the detection of responses to weak stimuli. Inflamm. Res. 2007, 56, 45-50.
30. Hollander, K. S., Tempel Brami, C., Konikoff, F. M., Fainaru, M. et al., Dietary enrichment with alpha-linolenic acid during pregnancy attenuates insulin resistance in adult offspring in mice. Arch. Physiol. Biochem. 2014, 120, 99-111.
31. Hayek, T., Kaplan, M., Kerry, R., Aviram, M., Macrophage NADPH oxidase activation, impaired cholesterol fluxes, and increased cholesterol biosynthesis in diabetic mice: a stimulatory role for D-glucose. Atherosclerosis 2007, 195, 277-286.
32. Ceriello, A., Quagliaro, L., D'Amico, M., Di Filippo, C. et al., Acute hyperglycemia induces nitrotyrosine formation and apoptosis in perfused heart from rat. Diabetes 2002, 51, 1076-1082.
33. Cignarella, A., Bolego, C., Pelosi, V., Meda, C. et al., Distinct roles of estrogen receptor-alpha and beta in the modulation of vascular inducible nitric-oxide synthase in diabetes. J. Pharmacol. Exp. Ther. 2009, 328, 174-182.
34. Vegeto, E., Pollio, G., Pellicciari, C., Maggi, A., Estrogen and progesterone induction of survival of monoblastoid cells undergoing TNF-alpha-induced apoptosis. FASEB J. 1999, 13, 793-803.
35. Pare, G., Krust, A., Karas, R. H., Dupont, S. et al., Estrogen receptor-alpha mediates the protective effects of estrogen against vascular injury. Circ. Res. 2002, 90, 1087-1092.
36. Chang, K., Lee, S. J., Cheong, I., Billiar, T. R. et al., Nitric oxide suppresses inducible nitric oxide synthase expression by inhibiting post-translational modification of IkappaB. Exp. Mol. Med. 2004, 36, 311-324.
37. Manach, C., Scalbert, A., Morand, C., Remesy, C. et al., Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 2004, 79, 727-747.
38. Cao, J., Chen, X., Liang, J., Yu, X. Q. et al., Role of P-glycoprotein in the intestinal absorption of glabridin, an active flavonoid from the root of Glycyrrhiza glabra. Drug Metab. Dispos. 2007, 35, 539-553.
39. Ito, C., Oi, N., Hashimoto, T., Nakabayashi, H. et al., Absorption of dietary licorice isoflavan glabridin to blood circulation in rats. J. Nutr. Sci. Vitaminol. 2007, 53, 358-365.
40. Mladenka, P., Zatloukalova, L., Filipsky, T., Hrdina, R., Cardiovascular effects of flavonoids are not caused only by direct antioxidant activity. Free Radic. Biol. Med. 2010, 49, 963-975.
41. Duarte, J., Francisco, V., Perez-Vizcaino, F., Modulation of nitric oxide by flavonoids. Food Funct. 2014, 5, 1653-1668.