Evaluation of antihyperglycemia and antihypertension potential of native Peruvian fruits using in vitro models

Journal of Medicinal Food

Volumn 12, Issue 2, 2009, Pages 278-291

  Pinto, Marcia Da Silva ^a   Ranilla, Lena Galvez ^a   Apostolidis, Emmanouil ^b   Lajolo, Franco Maria ^a   Genovese, Maria Inés ^a   Shetty, Kalidas ^b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

amylase; glucosidase; Angiotensin converting enzyme; Antioxidant activity; Enzyme inhibition; Hyperglycemia; Hypertension; Peruvian fruits; Phenolic phytochemicals; Type 2 diabetes

Indexed keywords

1,1 DIPHENYL 2 PICRYLHYDRAZYL; ALPHA GLUCOSIDASE; AMYLASE; ANTIHYPERTENSIVE AGENT; CARICA PUBESCENS EXTRACT; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; HYPERGLYCEMIC AGENT; INGA FEUILLE EXTRACT; PHYSALIS PERUVIANA EXTRACT; PLANT EXTRACT; POUTERIA LUCUMA EXTRACT; PROSOPIS PALLIDA EXTRACT; PRUNUS CAPULI EXTRACT; UNCLASSIFIED DRUG;

ANTIOXIDANT ACTIVITY; ARTICLE; CARICA PUBESCENS; DRUG ACTIVITY; DRY WEIGHT; FRUIT; HYPERGLYCEMIA; HYPERTENSION; IN VITRO STUDY; INGA FEUILLE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PAPAYA; PHYSALIS; PHYSALIS PERUVIANA; POUTERIA; POUTERIA LUCUMA; PRIORITY JOURNAL; PROSOPIS; PROSOPIS PALLIDA; PRUNUS; PRUNUS CAPULI;

ALPHA-GLUCOSIDASES; ANGIOSPERMS; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANTIHYPERTENSIVE AGENTS; ANTIOXIDANTS; BIPHENYL COMPOUNDS; DIABETES MELLITUS, TYPE 2; FREE RADICAL SCAVENGERS; FRUIT; HYPOGLYCEMIC AGENTS; INDICATORS AND REAGENTS; MEDICINE, TRADITIONAL; PERU; PHENOLS; PICRATES; PLANT EXTRACTS; PLANTS, MEDICINAL;

ANIMALIA; INGA; PHYSALIS PERUVIANA; PHYSALIS PUBESCENS; POUTERIA LUCUMA; PROSOPIS PALLIDA; PRUNUS CAPULI; VASCONCELLEA CUNDINAMARCENSIS;

EID: 67649559457     PISSN: 1096620X     EISSN: None     Source Type: Journal    
DOI: 10.1089/jmf.2008.0113     Document Type: Article

References (92)

1. Wild S, Roglic G, Green A, Sicree R, King H: Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004;27:1047-1053.
2. Daar AS, Singer PA, Persad DL, Pramming SK, Matthews DR, Beaglehole R, Bernstein A, Borysiewicz LK, Colagiuri S, Ganguly N, Glass RI, Finegood DT, Koplan J, Nabel EG, Sarna G, Sarrafzadegan N, Smith R, Yach D, Bell J: Grand challenges in chronic non-communicable diseases. Nature 2007;450:494-496.
3. Hung HC, Joshipura KJ, Jiang R, Hu FB, Hunter D, Smith-Warner SA, Colditz GA, Rosner B, Spiegelman D, Willett WC: Fruit and vegetable intake and risk of major chronic disease. J Natl Cancer Inst 2004;96:1577-1584.
4. Costacou T, Mayer-Davis EJ: Nutrition and prevention of type 2 diabetes. Innu Rev Nutr 2003;23:147-170.
5. Esposito K, Nappo F, Marfella R, Giugliano G, Giugliano F, Ciotola M, Quagliaro L, Ceriello A, Giugliano D: Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: role of oxidative stress. Circulation 2002;106: 2067-2072.
6. Joshipura KJ, Hu FB, Manson JE, Stampfer MJ, Rimm EB, Speizer FE, Colditz G, Ascherio A, Rosner B, Spiegelman D, Willett WC: The effect of fruit and vegetable intake on risk for coronary heart disease. Ann Intern Med 2001;132:1106-1114.
7. Nöthlings U, Schulze MB, Weikert C, Boeing H, Van der Schouw YT, Bamia C, Benetou V, Lagiou P, Krogh V, Beulens JWJ, Peeters PHM, Halkjër J, Tjønneland A, Tumino R, Panico S, Masala G, Clavel-Chapelon F, De Lauzon B, Boutron-Ruault MC, Vercambre MN, Kaaks R, Linseisen J, Overvad K, Arriola L, Ardanaz E, Gonzalez CA, Tormo MJ, Bingham S, Khaw KT, Key TJA, Vineis P, Riboli E, Ferrari P, Boffetta P, Bueno-de-Mesquita HB, Van der A DL, Berglund G, Wirfält E, Hallmans G, Johansson I, Lund E, Trichopoulo A: Intake of vegetables, legumes, and fruit, and risk for all-cause, cardiovascular, and cancer mortality in a European diabetic population. J Nutr 2008;138:775-781.
8. Matsui T, Ueda T, Oki T, Sugita K, Terahara N, Matsumoto K: α-Glucosidase inhibitory action of natural acylated anthocyanins. 1. Survey of natural pigments with potent inhibitory activity. J Agric Food Chem 2001;49:1948-1951.
9. Kwon YI, Vattem DV, Shetty K: Evaluation of clonal herbs of Lamiaceae species for management of diabetes and hypertension. Asia Pac J Clin Nutr 2006;15:107-118.
10. McDougall GJ, Shpiro F, Doboson P, Smith P, Black A, Stewart D: Different polyphenolic compounds of soft fruits inhibit α-amylase and α-glucosidase. J Agric Food Chem 2005;53:2760-2766.
11. Khan A, Bryden NA, Polansky MM, Anderson RA: Insulin potentiating factor and chromium content of selected foods and spices. Biol Trace Elem Res 1990;24:183-188.
12. Kotowaroo MI, Mahomoodally MF, Gurib-Fakim A, Subratty AH: Screening of traditional antidiabetic medicinal plants of Mauritius for possible α-amylase inhibitory effects in vitro. Phytother Res 2006;20:228-231.
13. Gao H, Huang YN, Xu PY, Kawabata J: Inhibitory effect on α-glucosidase by the fruits of Terminalia chebula Retz. Food Chem 2007;105:628-634.
14. Bhandari MR, Jong-Anurakkun N, Hong G, Kawabata J: α-Glucosidase and α-amylase inhibitory activities of Nepalese medicinal herb Pakhanbhed (Bergenia ciliata, Haw.). Food Chem 2008;106:247-252.
15. Ali H, Houghton PJ, Soumyanath A: α-Amylase inhibitory activity of some Malaysian plants used to treat diabetes; with particular reference to Phyllanthus amarus. J Ethnopharmacol 2006; 107:449-455.
16. nd ed. NIH Publication Number 95-1468. U.S. Government Printing Office, Washington, DC, 1995, pp. 1-14.
17. Johnston JI, Franz V: Renin-angiotensin system: a dual tissue and hormonal system for cardiovascular control. J Hypertens 1992; 10:13-26.
18. Bussmann RW, Sharon D: Traditional medicinal plant use in Northern Peru: tracking two thousand years of healing culture. J Ethnobiol Ethnomed 2006;2:47.
19. Bussmann RW, Sharon D, Vandebroek I, Jones A, Revene Z: Health for sale: the medicinal plant markets in Trujillo and Chiclayo, Northern Peru. J Ethnobiol Ethnomed 2007;3:37.
20. National Research Council: Fruits. In: Lost Crops of the Incas: Little Known Plants of the Andes with Promise for Worldwide Cultivation. National Academy Press, Washington, DC, 1989, pp. 210-316.
21. Jacobsen SE, Mujica A, Ortiz R: The global potential for quinoa and other Andean crops Food Rev Int 2003;19:139-148.
22. Shetty K, Curtis OF, Levin RE, Wikowsky R, Ang W: Prevention of vitrification associated with in vitro shoot culture of oregano (Origanum vulgare) by Pseudomonas spp. J Plant Physiol 1995;147:447-451.
23. Worthington V, ed.: Alpha amylase. In: Worthington Enzyme Manual. Worthington Biochemical Corp., Freehold, NJ, 1993, pp. 36-41.
24. Worthington V, ed.: Maltase-α-glucosidase. In: Worthington Enzyme Manual. Worthington Biochemical Corp., Freehold, NJ, 1993, p. 261.
25. McCue P, Kwon YI, Shetty K: Anti-amylase, anti-glucosidase and anti-angiotensin I-converting enzyme potential of selected foods. J Food Biotechnol 2005;29:278-294.
26. Ramadan MF, Moersel JT: Impact of enzymatic treatment on chemical composition, physicochemical properties and radical scavenging activity of goldenberry (Physalis peruviana L.) juice. J Sci Food Agric 2007;87:452-460.
27. Morton JF: Cape gooseberry. In: Fruits of Warm Climates (Morton JF, ed.). Creative Resource Systems, Winterville, NC, 1987, pp. 430-434.
28. Popenoe H, King SR, Leon J, Kalinowski LS: Goldenberry (cape gooseberry). In: Lost Crops of the Incas: Little Known Plants of the Andes with Promise for Worldwide Cultivation. National Academy Press, Washington, DC, 1990, pp. 241-252.
29. Ramadan MF, Morsel JT: Oil goldenberry (Physalis peruviana L.). J Agric Food Chem 2003;51:969-974.
30. Wu SJ, Ng LT, Lin DL, Huang SN, Wang SS, Lin CC: Physalis peruviana extract induces apoptosis in human Hep G2 cells through CD95/CD95L system and the mitochondrial signaling transduction pathway. Cancer Lett 2004;215:199-208.
31. Wu SJ, Tsai JY, Chang SP, Lin DL, Wang SS, Huang SN, Ng LT: Supercritical carbon dioxide extract exhibits enhanced antioxidant and anti-inflammatory activities of Physalis peruviana. J Ethnopharmacol 2006;108:407-413.
32. Arun M, Asha VV: Preliminary studies on antihepatotoxic effect of Physalis peruviana Linn. (Solanaceae) against carbon tetrachloride induced acute liver injury in rats. J Ethnopharmacol 2007;111:110-114.
33. Franco LA, Matiz GE, Calle J, Pinzon R, Ospina LF: Actividad antinflamatoria de extractos y fracciones obtenidas de calices de Physalis peruviana L. Biomedica 2007;27:110-115.
34. Wu SJ, Ng LT, Huang YM, Lin DL, Wang SS, Huang SN, Lin CC: Antioxidant activities of Physalis peruviana. Biol Pharm Bull 2005;28:963-966.
35. Bravo L, Grados N, Saura-Calixto F: Composition and potential uses of mesquite pods (Prosopis pallida L.): comparison with carob pods (Ceratonia siliqua L.). J Sci Food Agric 1994;65: 303-306.
36. Becker R, Sayre RN, Saunders RM: Semiarid legume crops as protein resources. J Am Oil Chem Soc 1984;61:931-938.
37. Bravo L, Grados N, Saura-Calixto F: Characterization of syrups and dietary fiber obtained from mesquite pods (Prosopis pallida L.). J Agric Food Chem 1998;46:1727-1733.
38. Rababah TM, Hettiarachchy NS, Horax R: Total phenolics and antioxidant activities of fenugreek, green tea, black tea, grape seed, ginger, rosemary, Gotu kola, and Ginkgo extracts, vitamin E, and tert-butylhydroquinone. J Agric Food Chem 2004;52: 5183-5186.
39. Shahidi F, Marian N: Phenolics in Food and Nutraceuticals, Vol. 1. CRC Press, Boca Raton, FL, 2003, pp. 144-150.
40. Prior RL, Cao G, Martin A, Sofic E, McEwan J, O'Brien C, Lischner N, Ehlenfeldt M, Kalt W, Krewer G, Mainland CM: Antioxidant capacity as influenced by total phenolic and anthocyanin content, maturity, and variety of Vaccinium species. J Agric Food Chem 1998;46:2686-2693.
41. Deighton N, Brennan R, Finn C, Davies HV: Antioxidat properties of domesticated and wild Rubus species. J Sci Food Agric 2000;80:1307-1313.
42. Pinto MS, Lajolo FM, Genovese MI: Bioactive compounds and quantification of total ellagic acid in strawberries (Fragaria × ananassa Duch.). Food Chem 2008;107:1629-1635.
43. Lovelock CE, Clough BF, Woodrow IE: Distribution and accumulation of ultraviolet-radiation-absorbing compounds in leaves of tropical mangroves. Planta 1992;188:143-154.
44. Chaves N, Escudero JC, Gutierrez-Merino C: Role of ecological variables in the seasonal variation of flavonoid content of Cistus ladanifer. J Chem Ecol 1997;23:579-604.
45. Alonso-Amelot ME, Oliveros A, Calcagano-Pisarelli MP: Phenolics and condensed tannins in relation to altitude in neotropical Pteridium spp. A field study in the Venezuelan Andes. Biochem System Ecol 2004;32:969-981.
46. Sullivan JH, Teramura AH, Ziska LH: Variation in UV-B sensitivity in plants from a 3000 m elevational gradient in Hawaii. Am J Botany 1992;79:737-743.
47. Alonso-Amelot ME, Oliveros-Bastidas A, Arellano E: Extraction efficiency of phenolics and tannins from some sun-exposed neotropical forbs and shrubs in a mountain habitat. Ciencia 2005;13:429-439.
48. Spitaler R, Winkler A, Lins I, Yanar S, Stuppner H, Zidorn C: Altitudinal variation of phenolic contents in flowering heads of Arnica montana cv. ARBO: a 3-year comparison. J Chem Ecol 2008;34:369-375.
49. Alonso-Amelot ME, Oliveros-Bastidas A, Calcagno-Pisarelli MP: Phenolics and condensed tannins of high altitude Pteridium arachnoideum in relation to sunlight exposure, elevation, and rain regime. Biochem Syst Ecol 2007;35:1-10.
50. Zidorn C, Schubert B, Stuppner H: Altitudinal differences in the contents of phenolics in flowering heads of three members of the tribe Lactuceae (Asteraceae) occurring as introduced species in New Zealand. Biochem Syst Ecol 2005;33:855-872.
51. Prior RL, Gu L, Wu X, Jacob RA, Sotoudeh G, Kader AA, Cook RA: Plasma antioxidant capacity changes following a meal as a measure of the ability of a food to alter in vivo antioxidant status. J Am Coll Nutr 2007;26:170-181.
52. Seeram NP: Berry fruits for cancer prevention: current status and future prospects. J Agric Food Chem 2008;56:630-635.
53. Tsuda T, Horio F, Osawa T: Absorption and metabolism of cyanidin 3-O-beta-D-glucoside in rats. FEBS Lett 1999;23:179-182.
54. Mohsen MA, Marks J, Kuhnle G, Moore K, Debnam E, Srai SK, Rice-Evans C, Spencer JP: Absorption, tissue distribution and excretion of pelargonidin and its metabolites following oral administration to rats. Br J Nutr 2006;95:51-58.
55. Vitaglione P, Donnarumma G, Napolitano A, Galvano F, Gallo A, Scalfi L, Fogliano V: Protocatechuic acid is the major human metabolite of cyanidin-glucosides. J Nutr 2007;137:2043-2048.
56. Clifford MN: Chlorogenic acids and other cinnamates - nature, occurrence, dietary burden, absorption and metabolism. J Sci Food Agric 2000;80:1033-1042.
57. Shetty K, Wahlqvist ML: A model for the role of the proline-linked pentose-phosphate pathway in phenolic phytochemical biosynthesis and mechanism of action for human health and environmental applications. Asia Pac J Clin Nutr 2004;13:1-24.
58. Apostolidis E, Kwon YI, Shetty K: Potential of cranberry-based herbal synergies for diabetes and hypertension management. Asia Pac J Clin Nutr 2006;15:433-441.
59. Zhao Z, Moghadasian MH: Chemistry, natural sources, dietary intake and pharmacokinetic properties of ferulic acid: a review. Food Chem 2008;109:691-702.
60. Clifford MN: Chlorogenic acids and other cinnamates - nature, occurrence and dietary burden. J Sci Food Agric 1999;79:362-372.
61. Graf E: Antioxidant potential of ferulic acid. Free Radic Biol Med 1992;13:435-448.
62. World Health Organization: Diabetes. Fact Sheet 2006; 312. http://www.who.int/mediacentre/factsheets/fs312/en/print.html (accessed April 21, 2008).
63. Yeh GY, Eisenberg DM, Kaptchuk TJ, Phillips RS: Systematic review of herbs and dietary supplements for glycemic control in diabetes. Diabetes Care 2003;26:1277-1294.
64. Jia W, Gao W, Tang L: Antidiabetic herbal drugs officially approved in China. Phytother Res 2003;17:1127-1134.
65. Bnouham M, Ziyyat A, Mekhfi H, Tahri A, Legssyer A: Medicinal plants with potential antidiabetic activity - a review of ten years of herbal medicine research (1990-2000). Int J Diabetes Metab 2006;14:1-25.
66. rd ed. (Pickup JC, William G, eds.). Blackwell Science Ltd., Oxford, UK, 2003, pp. 73.1-73.21.
67. Broadhurst CL: Nutrition and non-insulin dependent diabetes from an anthropological perspective. Altern Med Rev 1997;2: 378-399.
68. Cheplick S, Kwon Y, Bhowmik P, Shetty K: Clonal variation in raspberry fruit phenolics and relevance for diabetes and hypertension management. J Food Biochem 2007;31:656-679.
69. Greenberg JA, Boozer CN, Geliebter A: Coffee, diabetes, and weight control. Am J Clin Nutr 2006;84:682-693.
70. McCarty MF: Nutraceutical resources for diabetes prevention - an update. Med Hypotheses 2005;64:151-158.
71. +-dependent D-glucose uptake in rat intestinal brush border membrane vesicles. J Nutr 1989;119: 1698-1704.
72. Johnston KL, Clifford MN, Morgan LM: Coffee acutely modifies gastrointestinal hormone secretion and glucose tolerance in humans: glycemic effects of chlorogenic acid and caffeine. Am J Clin Nutr 2003;78:728-733.
73. Bassoli BK, Cassolla P, Borba-Murad GR, Constantin J, Salgueiro-Pagadigorria CL, Bazotte RB, Silva RSSF, Souza HM: Chlorogenic acid reduces the plasma glucose peak in the oral glucose tolerance test: effects on hepatic glucose release and glycaemia. Cell Biochem Funct 2008;26:320-328.
74. Rohn S, Rawel HM, Kroll J: Inhibitory effects of plant phenols on the activity of selected enzymes. J Agric Food Chem 2002;50:3566-3571.
75. Kwon Y-I, Apostolidis E, Kim Y-C, Shetty K: Health benefits of traditional corn, beans, and pumpkin: in vitro studies for hyperglycemia and hypertension management. J Med Food 2007;10: 266-275.
76. Puls W, Keup U, Krause H, Thomas PG, Hoffmeister F: Glucosidase inhibition: a new approach to the treatment of diabetes, obesity, and hyperlipoproteinemia. Naturwissen Schaften 1977;64:536-537.
77. Medina-Lezama J, Zea-Diaz H, Morey-Vargas O, Bolaños-Salazar J, Muñoz-Atahualpa E, Postigo-MacDowall M, Corrales-Medina F, Valdivia-Ascuña Z, Cuba-Bustinza C, Paredes-Díaz S: Prevalence of the metabolic syndrome in Peruvian Andean Hispanics: the PREVENCION study. Diabetes Res Clin Pract 2007;78:270-281.
78. Goldstein J, Jacoby E, del Aguila R, Lopez A: Poverty is a predictor of non-communicable disease among adults in Peruvian cities. Prev Med 2005;41:800-806.
79. Medina-Lezama J, Chirinos JA, Zea-Diaz H, Morey-Vargas O, Bolanos JF, Muñoz-Atahualpa E, Chirinos-Pacheco J: Design of PREVENCION: a population-based study of cardiovascular disease in Peru. Int J Cardiol 2005;105:198-202.
80. Kearney PM, Whelton M, Reynolds K, Muntner P, Whelton PK, He J: Global burden of hypertension: analysis of worldwide data. Lancet 2005;365:217-223.
81. Menénde J, Guevara A, Arcia N, Díaz EML, Marín C, Alfonso JC: Enfermedades crónicas y limitación funcional en adultos mayores: estudio comparativo en siete ciudades de América Latina y Caribe. Rev Panam Salud Publica 2005;17:353-361.
82. Aschner P: Diabetes trends in Latin America. Diabetes Metab Res Rev 2002;18(Suppl 3):S27-S31.
83. Taubert D, Berkels R, Roesen R, Klaus W: Chocolate and blood pressure in elderly individuals with isolated systolic hypertension. JAMA 2003;290:1029-1030.
84. Negishi H, Xu JW, Ikeda K, Njelekela M, Nara Y, Yamori Y: Black and green tea polyphenols attenuate blood pressure increases in stroke-prone spontaneously hypertensive rats. J Nutr 2004;134:38-42.
85. Appel LJ, Moore TJ, Obarzanek E, Vollmer WM, Svetkey LP, Sacks FM, Bray GA, Vogt TM, Cutler JA, Windhauser MM, Lin PH, Karanja N: A clinical trial of the effects of dietary patterns on blood pressure. DASH Collaborative Research Group. N Engl J Med 1997;336:1117-1124.
86. Edwards RL, Lyon T, Litwin SE, Rabovsky A, Symons JD, Jalili T: Quercetin reduces blood pressure in hypertensive subjects. J Nutr 2007;137:2405-2411.
87. Lee J, Bae IY, Lee HG, Yang C: Tyr-Pro-Lys, an angiotensin-I-converting enzyme inhibitory peptide derived from broccoli (Brassica oleracea Italica). Food Chem 2006;99:143-148.
88. Gouda KGM, Gowda LR, Rao AGA, Prakash V: Angiotensin-I-converting enzyme inhibitory peptide derived from glycinin, the 11S globulin of soybean (Glycine max). J Agric Food Chem 2006;54:4568-4573.
89. Foltz M, Meynen EE, Bianco V, van Platerink C, Koning TMMG, Kloek J: Angiotensin converting enzyme inhibitory peptides from a lactotripeptide- enriched milk beverage are absorbed intact into the circulation. J Nutr 2007;137:953-958.
90. Papadimitriou CG, Vafopoulou-Mastrojiannaki A, Silva SV, Gomes AM, Malcata FX, Alichanidis E: Identification of peptides in traditional and probiotic sheep milk yogurt with angiotensin I-converting enzyme (ACE)-inhibitory activity. Food Chem 2007;105:647-656.
91. Parris N, Moreau RA, Johnston DB, Dickey LC, Aluko RE: Angiotensin I converting enzyme-inhibitory peptides from commercial wet- and dry-milled corn germ. J Agric Food Chem 2008;56: 2620-2623.
92. Genovese MI, Pinto MS, Gonçalves AESS, Lajolo FM: Bioactive compounds and antioxidant capacity of exotic fruits and commercial frozen pulps from Brazil. Food Sci Technol Int 2008;14: 207-214.