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Drug Res (Stuttg) 2020; 70(11): 503-511
DOI: 10.1055/a-1221-4733
Review

Protective Effect of Grape and Apple Juices against Cadmium Intoxication in the Kidney of Rats

Bianca Andrade Handan
1   Department of Biosciences, Federal University of São Paulo, UNIFESP, SP, Brazil
,
Carolina Foot Gomes De Moura
1   Department of Biosciences, Federal University of São Paulo, UNIFESP, SP, Brazil
,
Caroline Margonato Cardoso
1   Department of Biosciences, Federal University of São Paulo, UNIFESP, SP, Brazil
,
Aline Boveto Santamarina
1   Department of Biosciences, Federal University of São Paulo, UNIFESP, SP, Brazil
,
Luciana Pellegrini Pisani
1   Department of Biosciences, Federal University of São Paulo, UNIFESP, SP, Brazil
,
Daniel Araki Ribeiro
1   Department of Biosciences, Federal University of São Paulo, UNIFESP, SP, Brazil
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Abstract

Background The objective of this study was to evaluate protective effect of grape and apple juices against toxicity induced by cadmium in the kidney of rats.

Methods A total of 20 male-Wistar rats were distributed into four groups (n=5): Control group: animals received an intraperitoneal (i.p.) injection of 0.9% saline solution and after 15 days, 1 mL of water was administered for 15 days, via gavage; Cadmium group: animals received an intraperitoneal injection of cadmium chloride (1.2 mg/kg) and after 15 days, 1 mL of water was administered for 15 days via gavage; Cadmium+Grape Juice: animals received an i.p. injection of cadmium chloride (1.2 mg/kg), and after 15 days, 0.8 mL of grape juice was administered for 15 days, via gavage; Cadmium+Apple Juice: animals received i.p. injection of cadmium chloride (1.2 mg/kg) and after 15 days, 1.0 mL of apple juice was administered for 15 days, via gavage.

Results Histopathological analysis revealed severe tubular lesion and necrosis in the group exposed to cadmium, while animals exposed to grape or apple juices showed a significant reduction of tissue injury. 8-OHdG immunoexpression, DNA damage, cytochrome C and catalase gene expressions and Toll like signaling pathway (TLR2, and pIKKα/β) decreased in animals treated with grape juice when compared to cadmium group.

Conclusion Taken together, we conclude that grape and apple juices had a protective effect by means of antioxidant, antigenotoxic actions and for promoting tissue regeneration in the kidney of rats following cadmium intoxication.

Key words

biologics - apoptosis - inflammation


Publication History

Received: 01 April 2020

Accepted: 18 May 2020

Article published online:
20 August 2020

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Hectors TL, Vanparys C, van der Ven K. et al. Environmental pollutants and type 2 diabetes: A review of mechanisms that can disrupt beta cell function. Diabetologia 2011; 54: 1273-1290
    CrossrefPubMedGoogle Scholar
  • 2 Yi Y, Yang Z, Zhang S. Ecological risk assessment of heavy metals in sediment and human health risk assessment of heavy metals in fishes in the middle and lower reaches of the Yangtze River basin. Environ Pollut 2011; 159: 2575-2585
    CrossrefPubMedGoogle Scholar
  • 3 de Moura CFG, Ribeiro FAP, Lucke G. et al. Apple juice attenuates genotoxicity and oxidative stress induced by cadmium exposure in multiple organs of rats. J Trace Elem Med Biol 2015; 32: 7-12
    CrossrefPubMedGoogle Scholar
  • 4 Panjehpour M, Bayesteh M. The cytotoxic effects of cadmium chloride on the human lung carcinoma: Calu-6: Cell line. Res Phamaceut Sci 2008; 3: 113-117
    PubMedGoogle Scholar
  • 5 Engström A, Michaëlsson K, Suwazono Y. et al. Long-term cadmium exposure and the association with bone mineral density and fractures in a population-based study among women. J Bone Miner Res 2011; 26: 486-495
    CrossrefPubMedGoogle Scholar
  • 6 Akerstrom M, Barregard L, Lundh T. et al. The relationship between cadmium in kidney and cadmium in urine and blood in an environmentally exposed population. Toxicol Appl Pharmacol 2013; 268: 286-293
    CrossrefPubMedGoogle Scholar
  • 7 Arora M, Weuve J, Schwartz J. et al. Association of environmental cadmium exposure with pediatric dental caries. Environ Health Perspect 2008; 116: 821-825
    CrossrefPubMedGoogle Scholar
  • 8 Borges LP, Brandão R, Godoi B. et al. Oral administration of diphenyl diselenide protects against cadmium-induced liver damage in rats. Chem Biol Interact 2008; 171: 15-25
    CrossrefPubMedGoogle Scholar
  • 9 Hamada T, Tanimoto A, Sasaguri Y. Apoptosis induced by cadmium. Apoptosis 1997; 2: 359-367
    CrossrefPubMedGoogle Scholar
  • 10 Bertin G, Averbeck D. Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences: A review. Biochimie 2006; 88: 1549-1559
    CrossrefPubMedGoogle Scholar
  • 11 Ramesh B, Satakopan VN. Antioxidant activities of hydroalcoholic extract of Ocimum sanctum against cadmium induced toxicity in rats. Indian J Clin Biochem 2010; 25: 307-310
    CrossrefPubMedGoogle Scholar
  • 12 Liu RH. Dietary bioactive compounds and their health implications. J Food Sci 2013; 1: A18-A25
    CrossrefPubMedGoogle Scholar
  • 13 Georgiev V, Ananga A, Tsolova V. Recent advances and uses of grape flavonoids as nutraceuticals. Nutrient 2014; 6: 391-415
    CrossrefPubMedGoogle Scholar
  • 14 de Moura CF, Ribeiro FA, Handan BA. et al. Grape juice concentrate protects rat liver against cadmium intoxication: Histopathology, cytochrome c and metalloproteinases expression. Drug Res 2016; 66: 339-344
    Article in Thieme ConnectPubMedGoogle Scholar
  • 15 Luna C, Li G, Liton PB. et al. Resveratrol prevents the expression of glaucoma markers induced by chronic oxidative stress in trabecular meshwork cells. Food Chem Toxicol 2009; 47: 198-204
    CrossrefPubMedGoogle Scholar
  • 16 Boyer J, Liu RH. Apple phytochemicals and their health benefits. Nutr J 2004; 3: 5
    CrossrefPubMedGoogle Scholar
  • 17 Gerhauser C. Cancer chemopreventive potential of apples, apple juice, and apple componentes. Planta Med 2008; 74: 1608-1624
    Article in Thieme ConnectPubMedGoogle Scholar
  • 18 Ribeiro FAP, de Moura CFG, Aguiar-Jr O. et al. The chemopreventive activity of apple against carcinogenesis: antioxidante activity and cell cycle control. Eur J Cancer Prev 2014; 23: 477-480
    CrossrefPubMedGoogle Scholar
  • 19 Bouayed J, Hoffmann L, Bohn T. Antioxidative mechanisms of whole-apple antioxidants employing different varieties from Luxembourg. J Med Food 2011; 14: 1631-1637 2011
    CrossrefPubMedGoogle Scholar
  • 20 Claudio SR, Gollucke AP, Yamamura H. et al. Purple carrot extract protects against cadmium intoxication in multiple organs of rats: Genotoxicity, oxidative stress and tissue morphology analyses. J Trace Elem Biol Med 2016; 33: 37-47
    CrossrefPubMedGoogle Scholar
  • 21 Hasler CM, Bloch AS, Thomson CA. et al. Position of the American Dietetic Association: Functional foods. J Am Diet Assoc 2004; 104: 814-826
    CrossrefPubMedGoogle Scholar
  • 22 de Moura CFG, Ribeiro FAP, de Jesus GPP. et al. Antimutagenic and antigenotoxic potential of grape juice concentrate in blood and liver of rats exposed to cadmium. Environ Sci Pollut Res 2014; 21: 13118-13126
    CrossrefPubMedGoogle Scholar
  • 23 Gollücke APB, Claudio SR, Yamamura H. et al. Grape skin extract mitigates tissue degeneration, genotoxicity, and oxidative status in multiple organs of rats exposed to cadmium. Eur J Cancer Prev 2019; 28: 109-111
    CrossrefPubMedGoogle Scholar
  • 24 Jia P, Teng J, Zou J. et al. Intermittent exposure to xenon protects against gentamicin-induced nephrotoxicity. PLos One 2013; 8: e64329
    CrossrefPubMedGoogle Scholar
  • 25 Badiglian Filho L, Oshima CT, De Oliveira Lima F. et al. Canonical and noncanonical Wnt pathway: a comparison among normal ovary, benign ovarian tumor and ovarian cancer. Oncol Rep 2009; 21: 313-320
    PubMedGoogle Scholar
  • 26 Tice RR, Agurell E, Anderson D. et al. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 2000; 35: 206-221
    CrossrefPubMedGoogle Scholar
  • 27 Matović V, Buha A, Bulat Z. et al. Cadmium toxicity revisited: focus on oxidative stress induction and interactions with zinc and magnesium. Arh Hig Rada Toksikol 2011; 62: 65-76
    CrossrefPubMedGoogle Scholar
  • 28 Bernhoft RA. Cadmium toxicity and treatment. Scientific World Journal 2013; 394652
    PubMedGoogle Scholar
  • 29 Rani A, Kumar A, Lal A. et al. Cellular mechanisms of cadmium-induced toxicity: a review. Int J Environ Health Res 2014; 24: 378-399
    CrossrefPubMedGoogle Scholar
  • 30 Lawal AO, Ellis EM. The chemopreventive effects of aged garlic extract against cadmium-induced toxicity. Environ Toxicol Pharmacol 2011; 32: 266-274
    CrossrefPubMedGoogle Scholar
  • 31 Renugadevi J, Prabu SM. Quercetin protects against oxidative stress-related renal dysfunction by cadmium in rats. Exp Toxicol Pathol 2010; 62: 471-481
    CrossrefPubMedGoogle Scholar
  • 32 Ghonim A, Abdeen A, El-Shawarby R. et al. Protective effect of cinnamon against cadmium-induced hepatorenal oxidative damage in rats. Int J Pharmacol Toxicol 2017; 5: 17-22
    CrossrefPubMedGoogle Scholar
  • 33 Eidi A, Mortazavi P, Bazargan M. et al. Hepatoprotective activity of cinnamon ethanolic extract against CCI4-induced liver injury in rats. EXCLI J 2012; 11: 495-507
    PubMedGoogle Scholar
  • 34 Amara S, Douki T, Garrel C. et al. Effect of static magnetic field and cadmium on oxidative stress and DNA damage in rat cortex brain and hippo-campus. Toxicolology Indian Health 2011; 27: 99-106
    CrossrefPubMedGoogle Scholar
  • 35 Stohs SJ, Bagchi D, Hassoun E. et al. Oxidative mechanisms in the toxicity of chromium and cadmium ions. Journal of Environmental Pathology, Toxicology and Oncology 2000; 20: 77-88
    PubMedGoogle Scholar
  • 36 Hartwig A. Mechanisms in cadmium-induced carcinogenicity: Recent insights. Biometals 2010; 23: 951-960
    CrossrefPubMedGoogle Scholar
  • 37 Bashir N, Manoharan V, Miltonprabu S. Grape seed proanthocyanidins protects against cadmium induced oxidative pancreatitis in rats by attenuating oxidative stress, inflammation and apoptosis via Nrf-2/HO-1 signaling. J Nutr Biochem 2016; 32: 128-141
    CrossrefPubMedGoogle Scholar
  • 38 Nomoto K, Tsuneyama K, Takahashi H. et al. Cytoplasmic fine granular expression of 8-hydroxydeoxyguanosine reflects early mitochondrial oxidative DNA damage in nonalcoholic fatty liver disease. Appl Immunohistochem Mol Morphol 2008; 16: 71-75
    CrossrefPubMedGoogle Scholar
  • 39 Rho KA, Kim MK. Effects of different grape formulations on antioxidative capacity, lipid peroxidation and oxidative DNA damage in aged rats. J Nutr Sci Vitaminol 2006; 52: 33-46
    CrossrefPubMedGoogle Scholar
  • 40 Babaknejad N, Moshtaghie AA, Nayeri H. et al. Protective role of zinc and magnesium against cadmium nephrotoxicity in male Wistar rats. Biol Trace Elem Res 2016; 174: 112-120
    CrossrefPubMedGoogle Scholar
  • 41 Peraza MA, Ayala-Fierro F, Barber DS. et al. Effects of micronutrients on metal toxicity. Environmental Health Perspectives 1998; 106 (Suppl. 01) (01) 203-216
    PubMedGoogle Scholar
  • 42 Candas D, Li JJ. MnSOD in oxidative stress response-potential regulation via mitochondrial protein influx. Antioxid Redox Signal 2014; 20: 1599-1617
    CrossrefPubMedGoogle Scholar
  • 43 Wang C, Youle RJ. The role of mitochondria in apoptosis. Annu Rev Genet 2009; 43: 95-118
    CrossrefPubMedGoogle Scholar
  • 44 Ow YP, Green DR, Hao Z. et al. Cytochrome c: Functions beyond respiration. Nat Rev Mol Cell Biol 2008; 9: 532-542
    CrossrefPubMedGoogle Scholar
  • 45 Moraes DA, Venancio DP, Suchecki D. Sleep deprivation alters energy homeostasis through non-compensatory alterations in hypothalamic insulin receptors in Wistar rats. Horm Behav 2014; 66: 705-712
    CrossrefPubMedGoogle Scholar
  • 46 Takeda K, Akira S. Toll-like receptors. Curr Protoc Immunol 2015; 109: 1-10
    CrossrefPubMedGoogle Scholar