Antidiabetic effect of Achillea millefollium through multitarget interactions: α-glucosidases inhibition, insulin sensitization and insulin secretagogue activities

Journal of Ethnopharmacology

Volumn 212, Issue , 2018, Pages 1-7

  Chávez Silva, Fabiola ^a   Cerón Romero, Litzia ^a   Arias Durán, Luis ^a   Navarrete Vázquez, Gabriel ^a   Almanza Pérez, Julio ^b   Román Ramos, Rubén ^b   Ramírez Ávila, Guillermo ^c   Perea Arango, Irene ^a   Villalobos Molina, Rafael ^d   Estrada Soto, Samuel ^a  

^a UNIVERSIDAD AUTÓNOMA DEL ESTADO DE MORELOS   (Mexico)

^b DEPARTAMENTO DE QUÍMICA   (Mexico)

^c INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^d UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Achillea millefollium; Antidiabetic; Calcium mobilization; Insulin secretion; Insulin sensitization; PPAR

Indexed keywords

ACARBOSE; ACHILLEA MILLEFOLIUM EXTRACT; ADIPONECTIN; ALCOHOL; ALPHA GLUCOSIDASE; GELATINASE B; GLIBENCLAMIDE; GLUCOSE; GLUCOSE TRANSPORTER 2; GLUCOSE TRANSPORTER 4; INSULIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RESISTIN; SCAVENGER RECEPTOR A; SODIUM GLUCOSE COTRANSPORTER 1; TUMOR NECROSIS FACTOR; ANTIDIABETIC AGENT; GLYCOSIDASE INHIBITOR; PLANT EXTRACT;

3T3-L1 CELL LINE; ACHILLEA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIDIABETIC ACTIVITY; ARTICLE; CALCIUM MOBILIZATION; CLINICAL EVALUATION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME INHIBITION; IN VITRO STUDY; IN VIVO STUDY; INSULIN RELEASE; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PROTEIN EXPRESSION; RIN-M5F CELL LINE; ANIMAL; CHEMISTRY; EXPERIMENTAL DIABETES MELLITUS; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; METABOLISM; PHYTOTHERAPY;

ACHILLEA; ALPHA-GLUCOSIDASES; ANIMALS; BLOOD GLUCOSE; DIABETES MELLITUS, EXPERIMENTAL; GLUCOSE TOLERANCE TEST; GLYCOSIDE HYDROLASE INHIBITORS; HYPOGLYCEMIC AGENTS; MALE; MICE; PHYTOTHERAPY; PLANT EXTRACTS;

EID: 85031796873     PISSN: 03788741     EISSN: 18727573     Source Type: Journal    
DOI: 10.1016/j.jep.2017.10.005     Document Type: Article

References (50)

1. Al-Awwadi, N.A.J., Antidiabetics effect of Achillea santolina aqueous leaves extract. Int. J. Med. Plants Res. 4 (2013), 151–156.
2. Al-Rowais, N.A., Herbal medicine in the treatment of diabetes mellitus. Saudi Med. J. 23 (2002), 1327–1331.
3. Anandharajan, R., Jaiganesh, S., Shankernarayanan, N.P., Viswakarma, R.A., Balakrishnan, A., In vitro glucose uptake activity of Aegles marmelos and Syzygium cumini by activation of GLUT4, PI3 kinase and PPARγ in L6 myotubes. Phytomedicine 13 (2005), 434–441.
4. Akram, M., Minireview on Achillea millefolium Linn. J. Membr. Biol. 246 (2013), 661–663.
5. Baggio, C., Otofuji, G.M., Freitas, C.S., Mayer, B., Marques, M.C., Mesia-Vela, S., Modulation of antioxidant systems by subchronic exposure to the aqueous extract of leaves from Achillea millefolium L. in rats. Nat. Prod. Res. 30 (2016), 613–615.
6. Baretta, I.P., Felizardo, R.A., Bimbato, V.F., dos Santos, M.G., Kassuya, A.C., Gasparotto Junior, A., da Silva, C.R., de Oliveira, S.M., Ferreira, J., Andreatini, R., Anxiolytic-like effects of acute and chronic treatment with Achillea millefolium L. extract. J. Ethnopharmacol. 140 (2012), 46–54.
7. Bellomo, G., Jewell, S.A., Thor, H., Orrenius, S., Regulation of intracellular calcium compartmentation: studies with isolated hepatocytes and t-butyl hydroperoxide. Proc. Natl. Acad. Sci. USA 79 (1982), 6842–6846.
8. Benedek, B., Gjoncaj, N., Saukel, J., Kopp, B., Distribution of phenolic compounds in Middleeuropean taxa of the Achillea millefolium L. aggregate. Chem. Biodivers., 2007, 4.
9. Benedek, B., Kopp, B., Melzig, M.F., Achillea millefolium L. s.l. – Is the anti-inflammatory activity mediated by protease inhibition?. J. Ethnopharmacol. 113 (2007), 312–317.
10. Candan, F., Unlu, M., Tepe, B., Daferera, D., Polissiou, M., Sökmen, A., Akpulat, H., Antioxidant and antimicrobial activity of the essential oil and methanol extracts of Achillea millefolium subsp. Millefolium Afan. (Asteraceae). J. Ethnopharmacol. 87 (2003), 215–220.
11. Cavalcanti, A.M., Baggio, C.H., Freitas, C.S., Rieck, L., de Sousa, R.S., Da Silva-Santos, J.E., Mesia-Vela, S., Marques, M.C., Safety and antiulcer efficacy studies of Achillea millefolium L. after chronic treatment in Wistar rats. J. Ethnopharmacol. 107 (2006), 277–284.
12. Chaudhury, A., Duvoor, C., Dendi, V.S., Kraleti, S., Chada, A., Ravilla, R., Marco, A., Shekhawat, N.S., Montales, M.T., Kuriakose, K., Sasapu, A., Beebe, A., Patil, N., Musham, C.K., Lohani, G.P., Mirza, W., Clinical review of antidiabetic drugs: implications for Type 2 diabetes mellitus management. Front. Endocrinol. 8 (2017), 1–12.
13. Clark, R.B., The role of PPARs in inflammation and immunity. J. Leukoc. Biol. 71 (2002), 388–400.
14. Chou, S.T., Peng, H.Y., Hsu, J.C., Lin, C.C., Shih, Y., Achillea millefolium L. essential oil inhibits lps-induced oxidative stress and nitric oxide production in RAW 264.7 macrophages. Int. J. Mol. Sci. 14 (2013), 12978–12993.
15. Dall'Acqua, S., Bolego, C., Cignarella, A., Gaion, R.M., Innocenti, G., Vasoprotective activity of standardized Achillea millefolium extract. Phytomedicine 18 (2011), 1031–1036.
16. de Souza, P., Crestani, S., Vilhena da Silva, R., de, C., Gasparotto, F., Leite Kassuya, C.A., da Silva-Santos, J.E., Arquimedes Gasparotto, J., Involvement of bradykinin and prostaglandins in the diuretic effects of Achillea millefolium L. (Asteraceae). J. Ethnopharmacol. 149 (2013), 157–161.
17. Fernyhough, M.E., Okine, E., Hausmanc, G., Vierck, J.L., Dodsona, M.V., PPARγ and GLUT4 expression as developmental regulators/markers for preadipocyte differentiation into an adipocyte. Domest. Anim. Endocrinol. 33 (2007), 367–378.
18. García-Díaz, J.A., Navarrete-Vázquez, G., García-Jiménez, S., Hidalgo-Figueroa, S., Almanza-Pérez, J.C., Alarcón-Aguilar, F.J., Gómez-Zamudio, J., Cruz, M., Ibarra-Barajas, M., Estrada-Soto, S., Antidiabetic, antihyperlipidemic and anti-inflammatory effects of tilianin in streptozotocin-nicotinamide diabetic rats. Biomed. Pharmacother. 83 (2016), 667–675.
19. Guillausseau, P.J., Meas, T., Virally, M., Laloi-Michelin, M., Medeau, V., Kevorkian, J.-P., Abnormalities in insulin secretion in type 2 diabetes mellitus. Diabetes Metab. 34 (2008), S43–S48.
20. Hayashi, K., Kojima, R., Ito, M., Strain differences in the diabetogenic activity of streptozotocin in mice. Biol. Pharm. Bull. 29 (2006), 1110–1119.
21. Hidalgo-Figueroa, S., Ramírez-Espinosa, J.J., Estrada-Soto, S., Almanza-Pérez, J.C., Román-Ramos, R., Alarcón-Aguilar, F.J., Hernández-Rosado, J.V., Moreno-Díaz, H., Díaz-Coutiño, D., Navarrete-Vázquez, G., Discovery of thiazolidine-2,4-dione/biphenylcarbonitrile hybrid as dual PPAR α/γ modulator with antidiabetic effect: in vitro, in silico and in vivo approaches. Chem. Biol. Drug. Des. 81 (2013), 474–483.
22. IDF Diabetes Atlas, 2015. seventh edition. 〈http://www.diabetesatlas.org/〉 (Accessed 3 April 2017).
23. Innocenti, L.G., Vegeto, E., Dall'Acqua, S., Ciana, P., Giorgetti, M., Agradi, E., Sozzi, A., Fico, G., Tome, F., In vitro estrogenic activity of Achillea millefolium. Phytomedicine 14 (2007), 147–152.
24. Joshi, S.R., Parikh, R.M., Das, A.K., Insulin history, biochemistry, physiology and pharmacology. J. Assoc. Physicians India 55 (2007), 19–25.
25. Kellett, G.L., Brot-Laroche, E., Mace, O.J., Leturque, A., Sugar absorption in the intestine: the role of GLUT2. Annu. Rev. Nutr. 28 (2008), 35–54.
26. Koushyar, H., Koushyar, M.M., ByramI, G., Feizpour, A., Golamnezhad, Z., Boskabady, M.H., The effect of hydroethanol extract of Achillea millefolium on β‑adrenoceptors of guinea pig tracheal smooth muscle. Indian. J. Pharm. Sci., 2013, 400–405.
27. Larsen, T.M., Toubro, S., Astrup, A., PPARgamma agonists in the treatment of type II diabetes: is increased fatness commensurate with long-term efficacy?. Int. J. Obes. Relat. Metab. Disord. 27 (2003), 147–161.
28. Li, Y., Zhang, M.L., Cong, B., Wang, S.M., Dong, M., Sauriol, F., Huo, C.H., Shi, Q.W., Gu, Y.C., Kiyota, H., Achillinin A, a cytotoxic guaianolide from the flower of Yarrow, Achillea millefolium. Biosci. Biotechnol. Biochem. 75 (2011), 1554–1556.
29. Li, Y., Zhu, M.C., Zhang, M.L., Wang, Y.F., Dong, M., Shi, Q.W., Huo, C.H., Sauriol, F., Kiyota, H., Gu, Y.C., Cong, B., Achillinin B and C, new sesquiterpene dimers isolated from Achillea millefolium. Tetrahedron Lett. 53 (2012), 2601–2603.
30. Martínez, S.M., Mecanismos moleculares queue intervienen en la regulación de la síntesis de insulina por glucosa. Rev. Hosp. General. Dr. Man. Gea González 3 (2000), 118–120 (In Spanish).
31. 2+ from the endoplasmic reticulum. J. Ethnopharmacol. 188 (2016), 159–166.
32. Mustafa, K.G., Ganai, B.A., Akbar, S., Dar, M.Y., Masood, A.,. β-cell protective efficacy, hypoglycemic and hypolipidemic effects of extracts of Achillea millifolium in diabetic rats. Chin. J. Nat. Med. 10 (2012), 185–189.
33. Nathan, D.M., Buse, J.B., Davidson, M.B., Ferrannini, E., Holman, R.R., Sherwin, R., Zinman, B., Medical management of hyperglycemia in type 2 diabetes: a consensus algorithm for the initiation and adjustment of therapy. Diabetes Care 32 (2009), 193–203.
34. Nurul, I., Hyun, A.J., Hee, S.S., Hye, M.K., Jae, S.C., Potent α-glucosidase and protein tyrosine phosphatase 1B inhibitors from Artemisia capillaris. Arch. Pharm. Res. 36 (2013), 542–552.
35. Ortiz-Andrade, R.R., Sánchez-Salgado, J.C., Navarrete-Vázquez, G., Webster, S.P., Binnie, M., García-Jiménez, S., León-Rivera, I., Cigarroa-Vázquez, P., Villalobos-Molina, R., Estrada-Soto, S., Antidiabetic and toxicological evaluations of naringenin in normoglycaemic and NIDDM rats. Diabetes Obes. Metab. 10 (2008), 1097–1104.
36. Ortiz-Andrade, R.R., García-Jiménez, S., Castillo-España, P., Ramírez-Ávila, G., Villalobos-Molina, R., Estrada-Soto, S., α-Glucosidase inhibitory activity of the methanolic extract from Tournefortia hartwegiana: an anti-hyperglycemic agent. J. Ethnopharmacol. 109 (2007), 48–53.
37. Petlevski, R., Hadzija, M., Slijepcevic, M., Juretic, D., Effect of ‘antidiabetis’ herbal preparation on serum glucose and fructosamine in NOD mice. J. Ethnopharmacol. 75 (2001), 181–184.
38. Potrich, F.B., Allemand, A., da Silva, L.M., Dos Santos, A.C., Baggio, C.H., Freitas, C.S., Mendes, D.A., Andre, E., Werner, M.F., Marques, M.C., Antiulcerogenic activity of hydroalcoholic extract of Achillea millefolium L.: involvement of the antioxidant system. J. Ethnopharmacol. 130 (2010), 85–92.
39. Ramírez, G., Zavala, M., Pérez, J., Zamilpa, A., In vitro screening of medicinal plants used in México as antidiabetics with glucosidase and lipase inhibitory activities. Evid. Based Complement. Altern. Med., 2012, 1–6.
40. Ramírez-Espinosa, J.J., Rios, M.Y., López-Martínez, S., López-Vallejo, F., Medina-Franco, J.L., Paoli, P., Gamici, G., Navarrete-Vázquez, G., Ortiz-Andrade, R., Estrada-Soto, S., Antidiabetic activity of some pentacyclic acid triterpenoids, role of PTP-1B: in vitro, in silico and in vivo approaches. Eur. J. Med. Chem. 46 (2011), 2243–2251.
41. Rydén, L., Standl, E., Bartnik, M., Van den Berghe, G., Betteridge, J., de Boer, M.J., Cosentino, F., Jönsson, B., Laakso, M., Malmberg, K., Priori, S., Ostergren, J., Tuomilehto, J., Thrainsdottir, I., Vanhorebeek, I., Stramba-Badiale, M., Lindgren, P., Qiao, Q., Priori, S.G., Blanc, J.J., Budaj, A., Camm, J., Dean, V., Deckers, J., Dickstein, K., Lekakis, J., McGregor, K., Metra, M., Morais, J., Osterspey, A., Tamargo, J., Zamorano, J.L., Deckers, J.W., Bertrand, M., Charbonnel, B., Erdmann, E., Ferrannini, E., Flyvbjerg, A., Gohlke, H., Juanatey, J.R., Graham, I., Monteiro, P.F., Parhofer, K., Pyörälä, K., Raz, I., Schernthaner, G., Volpe, M., Wood, D., Guidelines on diabetes, pre-diabetes, and cardiovascular diseases: executive summary. ‎Eur. Heart J. 28 (2007), 88–136.
42. Shroff, G., Therapeutic potential of human embryonic stem cells in type 2 diabetes mellitus. World J. Stem Cells, 8, 2016, 223.
43. Trisha, Dunning, A.M., Brief overview of diabetes the disease. Diabetes Educ.: Art. Sci. Evid., 2013.
44. Torres-Piedra, M., Ortiz-Andrade, R., Villalobos-Molina, R., Singh, N., Medina-Franco, J.L., Webster, S.P., Binnie, M., Navarrete-Vázquez, G., Estrada-Soto, S., Comparative study of flavonoid analogues on streptozotocine nicotinamide induced diabetic rats: quercetin as a potential antidiabetic agent acting via 11β–Hydroxysteroid dehydrogenase type 1 inhibition. Eur. J. Med. Chem. 45 (2010), 2606–2612.
45. Venditti, A., Maggi, F., Vittori, S., Papa, F., Serrilli, A.M., Di Cecco, M., Ciaschetti, G., Mandrone, M., Poli, F., Bianco, A., Antioxidant and α-glucosidase inhibitory activities of Achillea tenorii. Pharm. Biol. 53 (2015), 1505–1510.
46. Wang, Y.X., PPARs: diverse regulators in energy metabolism and metabolic diseases. Cell. Res. 20 (2010), 124–137.
47. Yaeesh, S., Jamal, Q., Khan, A.U., Gilani, A.H., Studies on hepatoprotective, antispasmodic and calcium antagonist activities of the aqueous-methanol extract of Achillea millefolium. Phytother. Res. 20 (2006), 546–551.
48. Yan, J., Zhang, G., Pan, J., Wang, Y., α-glucosidase inhibition by luteolin: kinetics, interaction and molecular docking. Int. J. Biol. Macromol. 64 (2014), 213–223.
49. Yazdanparast, R., Ardestani, A., Jamshidi, S., Experimental diabetes treated with Achillea santolina: Effect on pancreatic oxidative parameters. J. Ethnopharmacol. 112 (2007), 13–18.
50. Zolghadri, Y., Fazeli, M., Kooshki, M., Shomali, T., Karimaghayee, N., Dehghani, M., Achillea millefolium L. hydro- alcoholic extract protects pancreatic cells by Down regulating IL- 1β and iNOS gene expression in diabetic rats. Int. J. Mol. Cell. Med. Autumn 3 (2014), 255–262.