Raphanus sativus cv. Sango sprout juice decreases diet-induced obesity in sprague dawley rats and ameliorates related disorders

PLoS ONE

Volumn 11, Issue 3, 2016, Pages

  Vivarelli, Fabio ^a   Canistro, Donatella ^a   Sapone, Andrea ^a   De Nicola, Gina Rosalinda ^b   Marquillas, Clara Babot ^a   Iori, Renato ^b   Antonazzo, Ippazio Cosimo ^a   Gentilini, Fabio ^a   Paolini, Moreno ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTILIPEMIC AGENT; ANTIOBESITY AGENT; ANTIOXIDANT; CATALASE; CHOLESTEROL; FATTY ACID; GLUCURONOSYLTRANSFERASE; GLUTATHIONE REDUCTASE; PLANT EXTRACT; RAPHANUS SATIVUS EXTRACT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (QUINONE); SUPEROXIDE DISMUTASE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOBESITY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BODY WEIGHT; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIET INDUCED OBESITY; DOWN REGULATION; DRUG ACTIVITY; ENZYME ACTIVITY; FATTY ACID BLOOD LEVEL; FOOD INTAKE; HYPOLIPIDEMIC ACTIVITY; LIMIT OF QUANTITATION; LIPID DIET; LIVER WEIGHT; MALE; NONHUMAN; RADISH; RAT; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; ANALYSIS; ANIMAL; BLOOD; BODY WEIGHT GAIN; CHEMISTRY; ENZYMOLOGY; FRUIT AND VEGETABLE JUICE; FUNCTIONAL FOOD; LIVER; OBESITY; PATHOLOGY; RAPHANUS; SPRAGUE DAWLEY RAT;

ANIMALS; BODY WEIGHT; DIET, HIGH-FAT; FRUIT AND VEGETABLE JUICES; FUNCTIONAL FOOD; LIVER; MALE; OBESITY; RAPHANUS; RATS, SPRAGUE-DAWLEY; WEIGHT GAIN;

EID: 84978732393     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0150913     Document Type: Article

References (79)

1. World Health Organization Obesity: preventing and managing the global epidemic-report of a WHO consultation on obesity. Geneva: WHO; 1998.
2. Tsai AG, Abbo ED, Ogden LG. The time burden of overweight and obesity in primary care. BMC Health Serv Res 2011; 11: 191. doi: 10.1186/1472-6963-11-191 PMID: 21846407
3. Fontaine KR, McCubrey R, Mehta T, Pajewski NM, Keith SW, Bangalore SS, et al. Body mass index and mortality rate among Hispanic adults: a pooled analysis of multiple epidemiologic data sets. Int J Obes (Lond) 2012; 36: 1121-1126.
4. Singla P, Bardoloi A, Parkash AA. Metabolic effects of obesity: A review. World J Diabetes 2010; 1: 76-88. doi: 10.4239/wjd.v1.i3.76 PMID: 21537431
5. Marinou K, Tousoulis D, Antonopoulos AS Stefanadi E, Stefanadis C. Obesity and cardiovascular disease: from pathophysiology to risk stratification. Int J Cardiol 2012; 138: 3-8.
6. Finucane MM, Stevens GA, Cowan MJ, Danaei G, Lin JK, Paciorek CJ, Singh GM, et al. (2011) National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9!1 million participants. The Lancet 2011; 377: 557-67.
7. Kolotkin RL, Zunker C, Østbye T. Sexual functioning and obesity: a review. Obesity (Silver Spring) 2012; 20: 2325-2333.
8. Gupta D, Krueger CB, Lastra G. (2012) Over-nutrition, obesity and insulin resistance in the development of β-cell dysfunction. Expert Rev Cardiovasc Ther 2012; 10: 379-385.
9. Derosa G, Maffioli P. (2012) Anti-obesity drugs: a review about their effects and their safety. Expert Opin Drug Saf 2012; 11: 459-741. doi: 10.1517/14740338.2012.675326 PMID: 22439841
10. Crujeiras AB, Díaz-Lagares A, Carreira MC Amil M, Casanueva FF. Oxidative stress associated to dysfunctional adipose tissue: a potential link between obesity, type 2 diabetes mellitus and breast cancer. Free Radic Res 2013; 47: 243-256. doi: 10.3109/10715762.2013.772604 PMID: 23409968
11. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004; 114: 1752-1761. PMID: 15599400
12. Finer N. Weight Management: Approaches. In: Caballero editor. Encyclopedia of Human Nutrition, Walthampp: Academic Press; 2013. pp. 404-409.
13. Le Lay S, Simard G, Martinez MC, Andriantsitohaina R. Oxidative stress and metabolic pathologies: from an adipocentric point of view. Oxid Med Cell Longev Published online: 20 July 2014. doi: 10.1155/ 2014/908539
14. Curtis JM, Grimsrud PA, Wright WS, Xu X, Foncea RE, Graham DW. et al. Downregulation of adipose glutathione S-transferase A4 leads to increased protein carbonylation, oxidative stress, and mitochondrial dysfunction. Diabetes 2010; 59: 1132-1142. doi: 10.2337/db09-1105 PMID: 20150287
15. González-Castejón M, Rodriguez-Casado A. Dietary phytochemicals and their potential effects on obesity: a review. Pharmacol Res 2011; 64: 438-455. doi: 10.1016/j.phrs.2011.07.004 PMID: 21798349
16. Hursel R, Westerterp-Plantenga MS. Catechin- and caffeine-rich teas for control of body weight in humans. Am J Clin Nutr 2013; 98 Suppl. 6: 1682S-1693S.
17. Dinkova-Kostova AT, Kostov RV. Glucosinolates and isothiocyanates in health and disease. Trends Mol Med 2012; 18: 337-347. doi: 10.1016/j.molmed.2012.04.003 PMID: 22578879
18. Canistro D, Croce CD, Iori R, Barillari J, Bronzetti G, Poi G, et al. Genetic and metabolic effects of gluconasturtiin, a glucosinolate derived from cruciferae. Mutat Res 2004; 545: 23-35. PMID: 14698414
19. Valgimigli L, Iori R. Antioxidant and pro-oxidant capacities of ITCs. Environ Mol Mutagen 2009; 50: 222-237. doi: 10.1002/em.20468 PMID: 19197991
20. Canistro D, Barillari J, Melega S, Sapone A, Iori R, Speroni E, et al. Black cabbage seed extract affects rat Cyp-mediated biotransformation: organ and sex related differences. Food Chem Toxicol 2012; 50: 2612-2621. doi: 10.1016/j.fct.2012.05.030 PMID: 22634264
21. Melega S, Canistro D, Pagnotta E, Iori R, Sapone A, Paolini M. Effect of sprout extract from Tuscan black cabbage on xenobiotic-metabolizing and antioxidant enzymes in rat liver. Mutat Res 2013; 751: 45-51. doi: 10.1016/j.mrgentox.2012.10.013 PMID: 23183052
22. Raunio H, Kuusisto M, Juvonen RO, Pentikäinen OT. Modeling of interactions between xenobiotics and cytochrome P450 (CYP) enzymes. Front Pharmacol. 2015; 6:123. doi: 10.3389/fphar.2015.00123 PMID: 26124721
23. Abdelmegeed MA, Banerjee A, Yoo SH, Jang S, Gonzalez FJ, Song BJ. Critical role of cytochrome P450 2E1 (CYP2E1) in the development of high fat-induced non-alcoholic steatohepatitis. J Hepatol. 2012; 57: 860-866. doi: 10.1016/j.jhep.2012.05.019 PMID: 22668639
24. Guengerich FP. Cytochrome p450 and chemical toxicology. Chem Res Toxicol 2008; 21: 70-78. PMID: 18052394
25. Bast A. Is formation of reactive oxygen by cytochrome P450 perilous and predictable? Trends Pharmacol. Sci. 1986; 7: 226-227.
26. Paolini M, Pozzetti L, Pedulli GF, Cipollone M, Mesirca R, Cantelli-Forti G. Paramagnetic resonance in detecting carcinogenic risk from cytochrome P450 overexpression. J Investig Med. 1996; 44: 470-473. PMID: 8952228
27. Wu T, Tang Q, Yu Z, Gao Z, Hu H, Chen W, et al. Inhibitory effects of sweet cherry anthocyanins on the obesity development in C57BL/6 mice. Int J Food Sci Nutr 2014; 65: 351-359. doi: 10.3109/09637486. 2013.854749 PMID: 24224922
28. Xiao Z, Mi L, Chung FL, Veenstra TD. Proteomic analysis of covalent modifications of tubulins by isothiocyanates. J Nutr 2012; 142 Suppl. 7: 1377S-1381S.
29. De Nicola GR, Bagatta M, Pagnotta E, Angelino D, Gennari L, Ninfali P, et al. Comparison of bioactive phytochemical content and release of isothiocyanates in selected brassica sprouts. Food Chem 2013; 141: 297-303. doi: 10.1016/j.foodchem.2013.02.102 PMID: 23768361
30. Matera R, Gabbanini S, De Nicola GR, Iori R, Petrillo G, Valgimigli L. Identification and analysis of isothiocyanates and new acylated anthocyanins in the juice of Raphanus sativus cv. Sango sprouts. Food Chem 2012; 133: 563-572. doi: 10.1016/j.foodchem.2012.01.050 PMID: 25683434
31. He J, Giusti MM. Anthocyanins: natural colorants with health-promoting properties. Annu Rev Food Sci Technol 2010; 1:163-187. doi: 10.1146/annurev.food.080708.100754 PMID: 22129334
32. Soriano Sancho RA, Pastore GM. Evaluation of the effects of anthocyanins in type 2 diabetes. Food Res Int 2012; 46: 378-386.
33. Wu T, Yu Z, Tang Q, Song H, Gao Z, Chen W, Honeysuckle anthocyanin supplementation prevents diet-induced obesity in C57BL/6 mice. Food Funct 2013; 4: 1654-1661. doi: 10.1039/c3fo60251f PMID: 24081320
34. de Pascual-Teresa S, Moreno DA, García-Viguera C. Flavanols and anthocyanins in cardiovascular health: a review of current evidence. Int J Mol Sci 2010; 11: 1679-1703. doi: 10.3390/ijms11041679 PMID: 20480037
35. Cimino F, Speciale A, Anwar S, Canali R, Ricciardi E, Virgili F, et al. Anthocyanins protect human endothelial cells from mild hyperoxia damage through modulation of Nrf2 pathway. Genes Nutr 2013; 8: 391-399. doi: 10.1007/s12263-012-0324-4 PMID: 23229494
36. Anwar S, Speciale A, Fratantonio D, Chirafisi J, Saija A, Virgili F, et al. Cyanidin-3-O-glucoside modulates intracellular redox status and prevents HIF-1 stabilization in endothelial cells in vitro exposed to chronic hypoxia. Toxicol Lett 2014; 226: 206-213. doi: 10.1016/j.toxlet.2014.01.048 PMID: 24518827
37. Bauer C, Corsi C, Paolini M. Stability of microsomal monooxygenases in murine liver S9 fractions derived from phenobarbital and beta-naphthoflavone induced animals under various long-term conditions of storage. Teratog Carcinog Mutagen 1995; 14: 13-22.
38. Lowry OH, Rosenbrough HJ, Farr AL, Randall RJ. Protein measurement with folin phenol reagent. J Biol Chem 1951; 193: 265-275. PMID: 14907713
39. Bailey YL. Techniques in Protein Chemistry. Amsterdam: Elsevier; 1967.
40. Melega S, Canistro D, De Nicola GR, Lazzeri L, Sapone A, Paolini M. Protective effect of Tuscan black cabbage sprout extract against serum lipid increase and perturbations of liver antioxidant and detoxifying enzymes in rats fed a high-fat diet. Br J Nutr 2013; 110: 988-997. doi: 10.1017/ S0007114513000068 PMID: 23433361
41. Sapone A, Canistro D, Melega S, Moles R, Vivarelli F, Paolini M. On enzyme-based anticancer molecular dietary manipulations. J Biomed Biotechnol. 2012;790987. doi: 10.1155/2012/790987 PMID: 23049243
42. Bruce M. Microsomal NADPH cytochrome c-reductase. Meth Enzymol 1967; 10: 551-553.
43. Mazel P. Experiments illustrating drug metabolism in vitro. In: BN LaDu, Mandel HG, & Way EL, editors. Fundamentals of Drug Metabolism and Drug Disposition, Baltimore MD: The Williams & Wilkins Company, 1971; pp. 546-555.
44. Nash T. Colorimetric estimation of formaldehyde by means of Hantzsch reaction. Biochem J 1953; 55: 416-421. PMID: 13105648
45. Barillari J, Iori R, Broccoli M, Pozzetti L, Canistro D, Sapone A, et al. Glucoraphasatin and glucoraphenin, a redox pair of glucosinolates of brassicaceae, differently affect metabolizing enzymes in rats. J. Agric. Food Chem. 2007; 55: 5505-5511. PMID: 17579433
46. Reinke LA, Mayer ML. p-Nitrophenol hydroxylation. A microsomal oxidation which is highly inducible by ethanol. Drugs Metab Disp 1985; 13: 548-52.
47. Lubet RA, Mayer RT, Cameron JW, Nims RW, Burke MD, Wolff T, pentoxyresorufin: a rapid and sensitive assay for measuring induction of cytochrome(s) P-450 by phenobarbital and other xenobiotics in the rat. Arch Biochem Biophys. 1985; 238: 43-48. PMID: 3985627
48. Burke MD, Thompson S, Elcombe CR, Halpert J, Haaparanta T, Mayer RT. Ethoxy-, pentoxy- and benzyloxyphenoxazones and homologues: a series of substrates to distinguish between different induced cytochromes P-450. Biochem Pharmacol 1985; 34: 3337-3345. PMID: 3929792
49. Aitio A. A simple and sensitive assay of 7-ethoxycoumarin deethylation. Anal Biochem 1978; 85: 488-491. PMID: 565602
50. Canistro D, Bonamassa B, Pozzetti L, Sapone A, Abdel-Rahman SZ, Biagi GL, et al. Alteration of xenobiotic metabolizing enzymes by resveratrol in liver and lung of CD1 mice. Food Chem. Toxicol. 2009; 47: 454-61. doi: 10.1016/j.fct.2008.11.040 PMID: 19101601
51. Sheweita SA. Drug-metabolizing enzymes: mechanisms and functions. Curr Drug Metab. 2000; 1: 107-132. PMID: 11465078
52. Habig WH, Pabst MJ & Jakoby WB. Glutathione S-transferase AA from rat liver. J Biol Chem 1974; 249: 7130-7139. PMID: 4436300
53. Barillari J, Iori R, Broccoli M, Pozzetti L, Canistro D, Sapone A, et al. Glucoraphasatin and glucoraphenin, a redox pair of glucosinolates of brassicaceae, differently affect metabolizing enzymes in rats. J Agric Food Chem. 2007; 55: 5505-5511. PMID: 17579433
54. Paolini M, Sapigni E, Hrelia P, Scotti M, Morotti M, Cantelli-Forti G. Wide spectrum detection of precarcinogens in short-term bioassays by simultaneous superinduction of multiple forms of cytochrome P450 isoenzymes. Carcinogenesis 1991; 12: 759-766. PMID: 1903089
55. Wheeler CR, Salzman JA, Elsayed NM, Omaye ST, Korte DW Jr. Automated assays for superoxide dismutase, catalase, glutathione peroxidase, and glutathione reductase activity. Anal Biochem 1990; 184: 193-199. PMID: 2327564
56. Ernster L, Danielson L, Junggren M. DT diaphorase. I. Purification from the soluble fraction of rat-liver cytoplasm, and properties. Biochim Biophys Acta. 1962; 58: 171-188. PMID: 13890666
57. Misra HP & Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972; 247: 3170-3175. PMID: 4623845
58. Box P, Hunter WG. Statistics for Experiments. New York: Wiley; 1978.
59. Kim KH, Park Y. Food components with anti-obesity effect. Annu Rev Food Sci Technol 2011; 2: 237-257. doi: 10.1146/annurev-food-022510-133656 PMID: 22129382
60. Calabrese, Mattson MP, Calabrese V. Resveratrol commonly displays hormesis: occurrence and biomedical significance. Hum Exp Toxicol. 2010; 29: 980-1015. doi: 10.1177/0960327110383625 PMID: 21115559
61. Salamone F, Li Volti G, Titta L, Puzzo L, Barbagallo I, La Delia F, et al. Moro orange juice prevents fatty liver in mice. World J Gastroenterol 2012; 18: 3862-3868. doi: 10.3748/wjg.v18.i29.3862 PMID: 22876038
62. Choi KM, Lee YS, Sin DM, Lee S, Lee MK, Lee YM, et al. Sulforaphane inhibits mitotic clonal expansion during adipogenesis through cell cycle arrest. Obesity (Silver Spring) 2012; 20: 1365-1371.
63. Badshah H, Ullah I, Kim SE, Kim TH, Lee HY, Kim MO. Anthocyanins attenuate body weight gain via modulating neuropeptide Y and GABAB1 receptor in rats hypothalamus. Neuropeptides 2013; 47: 347-353. doi: 10.1016/j.npep.2013.06.001 PMID: 23830691
64. Arima H, Oiso Y. Positive effect of baclofen on body weight reduction in obese subjects: a pilot study. Intern Med 2010; 49: 2043-2047. PMID: 20930428
65. Kalra SP, Dube MG, Pu S, Xu B, Horvath TL, Kalra PS. Interacting appetite-regulating pathways in the hypothalamic regulation of body weight. Endocr Rev 1999; 20: 68-100. PMID: 10047974
66. Ho JN, Son ME, Lim WC, Lim ST, Cho HY. Anti-obesity effects of germinated brown rice extract through down-regulation of lipogenic genes in high fat diet-induced obese mice. Biosci Biotechnol Biochem 2012; 76: 1068-10674. PMID: 22790925
67. Sankhari JM, Thounaojam MC, Jadeja RN, Devkar RV, Ramachandran AV. Anthocyanin-rich red cabbage (Brassica oleracea L.) extract attenuates cardiac and hepatic oxidative stress in rats fed an atherogenic diet. J Sci Food Agric 2012; 92: 1688-1693. doi: 10.1002/jsfa.5532 PMID: 22228433
68. Bevilacqua L, Ramsey JJ, Hagopian K, Weindruch R, Harper ME. Effects of short- and medium-term calorie restriction on muscle mitochondrial proton leak and reactive oxygen species production. Am J Physiol Endocrinol Metab 2004; 286: E852-861. PMID: 14736705
69. Lee YM, Choi JS, Kim MH, Jung MH, Lee YS, Song J. Effects of dietary genistein on hepatic lipid metabolism and mitochondrial function in mice fed high-fat diets. Nutrition 2006; 22: 956-964. PMID: 16814985
70. Matera R, Gabbanini S, Berretti S, Amorati R, De Nicola GR, Iori R, et al. Acylated anthocyanins from sprouts of Raphanus sativus cv. Sango: isolation, structure elucidation and antioxidant activity. Food Chem. 2015; 166: 397-406. doi: 10.1016/j.foodchem.2014.06.056 PMID: 25053073
71. Wu T, Tang Q, Gao Z, Yu Z, Song H, Zheng X, et al. Blueberry and mulberry juice prevent obesity development in C57BL/6 mice. PLoS One 2013; 8: e77585. doi: 10.1371/journal.pone.0077585 PMID: 24143244
72. Matsuda M, Shimomura I. Roles of oxidative stress, adiponectin, and nuclear hormone receptors in obesity-associated insulin resistance and cardiovascular risk. Horm Mol Biol Clin Investig 2014; 19: 75-88. doi: 10.1515/hmbci-2014-0001 PMID: 25390017
73. Speciale A, Chirafisi J, Saija A, Cimino F. Nutritional antioxidants and adaptive cell responses: an update. Curr Mol Med 2011; 11: 770-789. PMID: 21999148
74. Ghose R, Omoluabi O, Gandhi A, Shah P, Strohacker K, Carpenter KC, et al. Role of high-fat diet in regulation of gene expression of drug metabolizing enzymes and transporters. Life Sci. 2011; 89: 57-64. doi: 10.1016/j.lfs.2011.05.005 PMID: 21620874
75. Forman HJ, Davies KJ, Ursini F. How do nutritional antioxidants really work: nucleophilic tone and para-hormesis versus free radical scavenging in vivo. Free Radic Biol Med 2014; 66: 24-35. doi: 10. 1016/j.freeradbiomed.2013.05.045 PMID: 23747930
76. Puccinelli E, Gervasi PG, Pelosi G, Puntoni M, Longo V. Modulation of cytochrome P450 enzymes in response to continuous or intermittent high-fat diet in pigs. Xenobiotica 2013; 43: 686-698. doi: 10. 3109/00498254.2012.756558 PMID: 23360109
77. Huang HL, Lin WY, Lee LT, Wang HH, Lee WJ, Huang KC. Metabolic syndrome is related to nonalcoholic steatohepatitis in severely obese subjects. Obes Surg 2007; 17: 1457-1463. PMID: 18219772
78. Fisher CD, Lickteig AJ, Augustine LM, Ranger-Moore J, Jackson JP, Ferguson SS, et al. Hepatic cytochrome P450 enzyme alterations in humans with progressive stages of nonalcoholic fatty liver disease. Drug Metab Dispos 2009; 37: 2087-2094. doi: 10.1124/dmd.109.027466 PMID: 19651758
79. Abdelmegeed MA, Banerjee A, Yoo SH, Jang S, Gonzalez FJ, Song BJ. Critical role of cytochrome P450 2E1 (CYP2E1) in the development of high fat-induced non-alcoholic steatohepatitis. J Hepatol. 2012; 57: 860-866. doi: 10.1016/j.jhep.2012.05.019 PMID: 22668639