Lemon verbena (Lippia citriodora) polyphenols alleviate obesity-related disturbances in hypertrophic adipocytes through AMPK-dependent mechanisms

Phytomedicine

Volumn 22, Issue 6, 2015, Pages 605-614

  Herranz López, María ^a   Barrajón Catalán, Enrique ^a   Segura Carretero, Antonio ^b   Menéndez, Javier A ^c   Joven, Jorge ^d   Micol, Vicente ^a,e  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

^c CATALAN INSTITUTE OF ONCOLOGY   (Spain)

^d HOSPITAL UNIVERSITARI SANT JOAN DE REUS   (Spain)

^e INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Adipocyte; Adiponectin; AMPK; Fat metabolism; Lippia citriodora; Verbascoside

Indexed keywords

ACTEOSIDE; ADENYLATE KINASE; ADIPONECTIN; FATTY ACID SYNTHASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; POLYPHENOL; REACTIVE OXYGEN METABOLITE; TRIACYLGLYCEROL; PLANT EXTRACT;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FATTY ACID OXIDATION; GENE EXPRESSION; IMMUNOFLUORESCENCE; INFLAMMATION; LEMON; LIPID METABOLISM; LIPPIA CITRIODORA; MALE; METABOLIC DISORDER; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; 3T3 CELL LINE; ANIMAL; C57BL MOUSE; CHEMISTRY; DRUG EFFECTS; HUMAN; KNOCKOUT MOUSE; LIPPIA; METABOLISM; PATHOPHYSIOLOGY; PROMOTER REGION;

ALOYSIA TRIPHYLLA; CITRUS LIMON; MURINAE; MUS; VERBENA;

3T3-L1 CELLS; ADIPOCYTES; ADIPONECTIN; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; FATTY ACID SYNTHASE, TYPE I; HUMANS; LIPID METABOLISM; LIPPIA; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; OBESITY; PLANT EXTRACTS; POLYPHENOLS; PPAR GAMMA; PROMOTER REGIONS, GENETIC; REACTIVE OXYGEN SPECIES;

EID: 84928896553     PISSN: 09447113     EISSN: 1618095X     Source Type: Journal    
DOI: 10.1016/j.phymed.2015.03.015     Document Type: Article

References (46)

1. Alipieva K., Korkina L., Orhan I.E., Georgiev M.I. Verbascoside - a review of its occurrence, (bio)synthesis and pharmacological significance Biotechnol. Adv. 32 2014 1065 1076
2. Baker R.G., Hayden M.S., Ghosh S. NF-kappaB, inflammation, and metabolic disease Cell Metab. 13 2011 11 22
3. Beltran-Debon R., Alonso-Villaverde C., Aragones G., Rodriguez-Medina I., Rull A., Micol V., Segura-Carretero A., Fernandez-Gutierrez A., Camps J., Joven J. The aqueous extract of Hibiscus sabdariffa calices modulates the production of monocyte chemoattractant protein-1 in humans Phytomedicine 17 2010 186 191
4. Beltrán-Debón R., Rull A., Rodríguez-Sanabria F., Iswaldi I., Herranz-López M., Aragonés G., Camps J., Alonso-Villaverde C., Menéndez J.A., Micol V., Segura-Carretero A., Joven J. Continuous administration of polyphenols from aqueous rooibos (Aspalathus linearis) extract ameliorates dietary-induced metabolic disturbances in hyperlipidemic mice Phytomedicine 18 2011 414 424
5. Bouskila M., Pajvani U.B., Scherer P.E. Adiponectin: a relevant player in PPARgamma-agonist-mediated improvements in hepatic insulin sensitivity? Int. J. Obes. (Lond.) 29 Suppl. 1 2005 S17 S23
6. Burke L.E., Wang J. Treatment strategies for overweight and obesity J. Nurs. Sch. 43 2011 368 375
7. Carrera-Quintanar L., Funes L., Vicente-Salar N., Blasco-Lafarga C., Pons A., Micol V., Roche E. Effect of polyphenol supplements on redox status of blood cells: a randomized controlled exercise training trial Eur. J. Nutr. 2014 DOI: 10.1007/s00394-00014-00785-x
8. Carrera-Quintanar L., Funes L., Viudes E., Tur J., Micol V., Roche E., Pons A. Antioxidant effect of lemon verbena extracts in lymphocytes of university students performing aerobic training program Scand. J. Med. Sci. Sports 22 2012 454 461
9. Caturla N., Funes L., Perez-Fons L., Micol V. A randomized, double-blinded, placebo-controlled study of the effect of a combination of lemon verbena extract and fish oil omega-3 fatty acid on joint management J. Altern. Complement. Med. 17 2011 1051 1063
10. Chung S., Yao H., Caito S., Hwang J.W., Arunachalam G., Rahman I. Regulation of SIRT1 in cellular functions: role of polyphenols Arch. Biochem. Biophys 501 2010 79 90
11. Fang X., Palanivel R., Cresser J., Schram K., Ganguly R., Thong F.S., Tuinei J., Xu A., Abel E.D., Sweeney G. An APPL1-AMPK signaling axis mediates beneficial metabolic effects of adiponectin in the heart Am. J. Physiol. Endocrinol. Metab. 299 2010 E721 E729
12. Fernandez-Arroyo S., Herranz-Lopez M., Beltran-Debon R., Borras-Linares I., Barrajon-Catalan E., Joven J., Fernandez-Gutierrez A., Segura-Carretero A., Micol V. Bioavailability study of a polyphenol-enriched extract from Hibiscus sabdariffa in rats and associated antioxidant status Mol. Nutr. Food Res. 56 2012 1590 1595
13. Funes L., Carrera-Quintanar L., Cerdan-Calero M., Ferrer M.D., Drobnic F., Pons A., Roche E., Micol V. Effect of lemon verbena supplementation on muscular damage markers, proinflammatory cytokines release and neutrophils' oxidative stress in chronic exercise Eur. J. Appl. Physiol 111 2011 695 705
14. Funes L., Fernández-Arroyo S., Laporta O., Pons A., Roche E., Segura-Carretero A., Fernández-Gutiérrez A., Micol V. Correlation between plasma antioxidant capacity and verbascoside levels in rats after oral administration of lemon verbena extract Food Chem. 117 2009 589 598
15. Funes L., Laporta O., Cerdán-Calero M., Micol V. Effects of verbascoside, a phenylpropanoid glycoside from lemon verbena, on phospholipid model membranes Chem. Phys. Lipids 163 2010 190 199
16. Grahame Hardie D. AMP-activated protein kinase: a key regulator of energy balance with many roles in human disease J. Intern. Med. 276 6 2014 543 559
17. Green H., Kehinde O. An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion Cell 5 1975 19 27
18. Gustafson B., Gogg S., Hedjazifar S., Jenndahl L., Hammarstedt A., Smith U. Inflammation and impaired adipogenesis in hypertrophic obesity in man Am. J. Physiol. Endocrinol. Metab. 297 2009 E999 E1003
19. Han C.Y., Subramanian S., Chan C.K., Omer M., Chiba T., Wight T.N., Chait A. Adipocyte-derived serum amyloid A3 and hyaluronan play a role in monocyte recruitment and adhesion Diabetes 56 2007 2260 2273
20. Hardie D.G., Ross F.A., Hawley S.A. AMP-activated protein kinase: a target for drugs both ancient and modern Chem. Biol. 19 2012 1222 1236
21. Hattori Y., Nakano Y., Hattori S., Tomizawa A., Inukai K., Kasai K. High molecular weight adiponectin activates AMPK and suppresses cytokine-induced NF-κB activation in vascular endothelial cells FEBS Lett. 582 2008 1719 1724
22. Herranz-Lopez M., Fernandez-Arroyo S., Perez-Sanchez A., Barrajon-Catalan E., Beltran-Debon R., Menendez J.A., Alonso-Villaverde C., Segura-Carretero A., Joven J., Micol V. Synergism of plant-derived polyphenols in adipogenesis: perspectives and implications Phytomedicine 19 2012 253 261
23. 2+ and AMPK/SIRT1 Nature 464 2010 1313 1319
24. Iwaki M., Matsuda M., Maeda N., Funahashi T., Matsuzawa Y., Makishima M., Shimomura I. Induction of adiponectin, a fat-derived antidiabetic and antiatherogenic factor, by nuclear receptors Diabetes 52 2003 1655 1663
25. Ji E., Jung M.Y., Park J.H., Kim S., Seo C.R., Park K.W., Lee E.K., Yeom C.H., Lee S. Inhibition of adipogenesis in 3T3-L1 cells and suppression of abdominal fat accumulation in high-fat diet-feeding C57BL/6J mice after downregulation of hyaluronic acid Int. J. Obes. (Lond.) 38 2014 1035 1043
26. Jiang F., Zhang Y., Dusting G.J. NADPH oxidase-mediated redox signaling: roles in cellular stress response, stress tolerance, and tissue repair Pharmacol. Rev. 63 2011 218 242
27. Joven J., Espinel E., Rull A., Aragones G., Rodriguez-Gallego E., Camps J., Micol V., Herranz-Lopez M., Menendez J.A., Borras I., Segura-Carretero A., Alonso-Villaverde C., Beltran-Debon R. Plant-derived polyphenols regulate expression of miRNA paralogs miR-103/107 and miR-122 and prevent diet-induced fatty liver disease in hyperlipidemic mice Biochim. Biophys. Acta 1820 2012 894 899
28. Joven J., Rull A., Ferre N., Escola-Gil J.C., Marsillach J., Coll B., Alonso-Villaverde C., Aragones G., Claria J., Camps J. The results in rodent models of atherosclerosis are not interchangeable: the influence of diet and strain Atherosclerosis 195 2007 e85 e92
29. Joven J., Rull A., Rodriguez-Gallego E., Camps J., Riera-Borrull M., Hernández-Aguilera A., Martin-Paredero V., Segura-Carretero A., Micol V., Alonso-Villaverde C., Menéndez J.A. Multifunctional targets of dietary polyphenols in disease: a case for the chemokine network and energy metabolism Food Chem. Toxicol. 51 2012 267 279
30. Koh E.H., Park J.Y., Park H.S., Jeon M.J., Ryu J.W., Kim M., Kim S.Y., Kim M.S., Kim S.W., Park I.S., Youn J.H., Lee K.U. Essential role of mitochondrial function in adiponectin synthesis in adipocytes Diabetes 56 2007 2973 2981
31. Kwon H., Pessin J.E. Adipokines mediate inflammation and insulin resistance Front Endocrinol. 4 2013 71
32. Li N., Karin M. Is NF-κB the sensor of oxidative stress? FASEB J. 13 1999 1137 1143
33. Lu K, Han M, Ting HL, Liu Z, Zhang D Scutellarin from Scutellaria baicalensis suppresses adipogenesis by upregulating PPARα in 3T3-L1 cells J. Nat. Prod. 76 2013 672 678
34. Menendez J.A., Joven J., Aragones G., Barrajon-Catalan E., Beltran-Debon R., Borras-Linares I., Camps J., Corominas-Faja B., Cufi S., Fernandez-Arroyo S., Garcia-Heredia A., Hernandez-Aguilera A., Herranz-Lopez M., Jimenez-Sanchez C., Lopez-Bonet E., Lozano-Sanchez J., Luciano-Mateo F., Martin-Castillo B., Martin-Paredero V., Perez-Sanchez A., Oliveras-Ferraros C., Riera-Borrull M., Rodriguez-Gallego E., Quirantes-Pine R., Rull A., Tomas-Menor L., Vazquez-Martin A., Alonso-Villaverde C., Micol V., Segura-Carretero A. Xenohormetic and anti-aging activity of secoiridoid polyphenols present in extra virgin olive oil: a new family of gerosuppressant agents Cell Cycle 12 2013 555 578
35. Okada-Iwabu M., Yamauchi T., Iwabu M., Honma T., Hamagami K., Matsuda K., Yamaguchi M., Tanabe H., Kimura-Someya T., Shirouzu M., Ogata H., Tokuyama K., Ueki K., Nagano T., Tanaka A., Yokoyama S., Kadowaki T. A small-molecule AdipoR agonist for type 2 diabetes and short life in obesity Nature 503 2013 493 499
36. Quirantes-Pine R., Herranz-Lopez M., Funes L., Borras-Linares I., Micol V., Segura-Carretero A., Fernandez-Gutierrez A. Phenylpropanoids and their metabolites are the major compounds responsible for blood-cell protection against oxidative stress after administration of Lippia citriodora in rats Phytomedicine 20 2013 1112 1118
37. Rezaee F., Dashty M. Role of adipose tissue in metabolic system disorders adipose tissue is the initiator of metabolic diseases J. Diabetes Metab. S13 2013 008 10.4172/2155-6156.S13-008
38. Rodriguez-Sanabria F., Rull A., Aragones G., Beltran-Debon R., Alonso-Villaverde C., Camps J., Joven J. Differential response of two models of genetically modified mice fed with high fat and cholesterol diets: relationship to the study of non-alcoholic steatohepatitis Mol. Cell. Biochem. 343 2010 59 66
39. Rull A., Camps J., Alonso-Villaverde C., Joven J. Insulin resistance, inflammation, and obesity: role of monocyte chemoattractant protein-1 (or CCL2) in the regulation of metabolism Mediators Inflamm. 2010 2010 326580
40. Rull A., Escola-Gil J.C., Julve J., Rotllan N., Calpe-Berdiel L., Coll B., Aragones G., Marsillach J., Alonso-Villaverde C., Camps J., Blanco-Vaca F., Joven J. Deficiency in monocyte chemoattractant protein-1 modifies lipid and glucose metabolism Exp. Mol. Pathol. 83 2007 361 366
41. Salminen A., Hyttinen J.T., Kaarniranta K. AMP-activated protein kinase inhibits NF-κB signaling and inflammation: impact on healthspan and lifespan J. Mol. Med. 89 2011 667 676
42. Salminen A., Kaarniranta K. AMP-activated protein kinase (AMPK) controls the aging process via an integrated signaling network Ageing Res. Rev. 11 2012 230 241
43. Snel M., Jonker J.T., Schoones J., Lamb H., de Roos A., Pijl H., Smit J.W., Meinders A.E., Jazet I.M. Ectopic fat and insulin resistance: pathophysiology and effect of diet and lifestyle interventions Int. J. Endocrinol. 2012 2012 983814
44. Yeop Han C., Kargi A.Y., Omer M., Chan C.K., Wabitsch M., O'Brien K.D., Wight T.N., Chait A. Differential effect of saturated and unsaturated free fatty acids on the generation of monocyte adhesion and chemotactic factors by adipocytes: dissociation of adipocyte hypertrophy from inflammation Diabetes 59 2010 386 396
45. Yoshizaki T., Kusunoki C., Kondo M., Yasuda M., Kume S., Morino K., Sekine O., Ugi S., Uzu T., Nishio Y., Kashiwagi A., Maegawa H. Autophagy regulates inflammation in adipocytes Biochem. Biophys. Res. Commun. 417 2012 352 357
46. Zebisch K., Voigt V., Wabitsch M., Brandsch M. Protocol for effective differentiation of 3T3-L1 cells to adipocytes Anal. Biochem. 425 2012 88 90