Advertisement

European Journal of Nutrition

, Volume 57, Issue 2, pp 817–832 | Cite as

Euterpe oleracea Mart. seed extract protects against renal injury in diabetic and spontaneously hypertensive rats: role of inflammation and oxidative stress

  • Viviane da Silva Cristino Cordeiro
  • Graziele Freitas de Bem
  • Cristiane Aguiar da Costa
  • Izabelle Barcellos Santos
  • Lenize Costa Reis Marins de Carvalho
  • Dayane Teixeira Ognibene
  • Ana Paula Machado da Rocha
  • Jorge José de Carvalho
  • Roberto Soares de Moura
  • Angela Castro Resende
Original Contribution

Abstract

Purpose

Euterpe oleracea Mart. (açaí) seed extract (ASE), through its anti-hypertensive, antioxidant and anti-inflammatory properties, may be useful to treat or prevent human diseases. Several evidences suggest that oxidative stress and inflammation contribute to the pathogenesis of diabetic nephropathy; therefore, we tested the hypothesis that ASE (200 mg/kg−1day−1) prevents diabetes and hypertension-related oxidative stress and inflammation, attenuating renal injury.

Methods

Male rats with streptozotocin (STZ)-induced diabetes (D), and spontaneously hypertensive rats with STZ-induced diabetes (DH) were treated daily with tap water or ASE (D + ASE and DH + ASE, respectively) for 45 days. The control (C) and hypertensive (H) animals received water.

Results

The elevated serum levels of urea and creatinine in D and DH, and increased albumin excretion in HD were reduced by ASE. Total glomeruli number in D and DH, were increased by ASE that also reduced renal fibrosis in both groups by decreasing collagen IV and TGF-β1 expression. ASE improved biomarkers of renal filtration barrier (podocin and nephrin) in D and DH groups and prevented the increased expression of caspase-3, IL-6, TNF-α and MCP-1 in both groups. ASE reduced oxidative damage markers (TBARS, carbonyl levels and 8-isoprostane) in D and DH associated with a decrease in Nox 4 and p47 subunit expression and increase in antioxidant enzyme activity in both groups (SOD, catalase and GPx).

Conclusion

ASE substantially reduced renal injury and prevented renal dysfunction by reducing inflammation, oxidative stress and improving the renal filtration barrier, providing a nutritional resource for prevention of diabetic and hypertensive-related nephropathy.

Keywords

Euterpe oleracea Mart Diabetes Hypertension Nephropathy Oxidative stress Inflammation 

Notes

Acknowledgements

This work was conducted with grants from National Council of Scientific and Technological Development (CNPq, No. 304974/2013-7) and Rio de Janeiro State Research Agency (FAPERJ, No. E-26/111.784/2013).

Compliance with ethical standards

Conflict of interest

Roberto Soares de Moura is the inventor of a patent (PCT/BR02/00038) that supported the development of a new patent application (PCT/BR2007/000178). The other authors state no conflicts of interest.

Ethical standards

The manuscript does not contain clinical studies or patient data.

References

  1. 1.
    Elmarakby AA, Faulkner J, Baban B, Saleh MA, Sullivan JC (2012) Induction of hemeoxygenase-1 reduces glomerular injury and apoptosis in diabetic spontaneously hypertensive rats. Am J Physiol Renal Physiol 302(7):F791–F800CrossRefGoogle Scholar
  2. 2.
    Rivero A, Mora C, Muros M, García J, Herrera H, Navarro-González JF (2009) Pathogenic perspectives for the role of inflammation in diabetic nephropathy. Clin Sci (Lond) 116(6):479–492CrossRefGoogle Scholar
  3. 3.
    Saleh MA, Boesen EI, Pollock JS, Savin VJ, Pollock DM (2011) Endothelin receptor A-specific stimulation of glomerular inflammation and injury in a streptozotocin-induced rat model of diabetes. Diabetologia 54(4):979–988CrossRefGoogle Scholar
  4. 4.
    Langham RG, Kelly DJ, Cox AJ, Thomson NM, Holthöfer H, Zaoui P, Pinel N, Cordonnier DJ, Gilbert RE (2002) Proteinuria and the expression of the podocyte slit diaphragm protein, nephrin, in diabetic nephropathy: effects of angiotensin converting enzyme inhibition. Diabetologia 45(11):1572–1576CrossRefGoogle Scholar
  5. 5.
    Lee SC, Han SH, Li JJ, Lee SH, Jung DS, Kwak SJ, Kim SH, Kim DK, Yoo TH, Kim JH, Chang SH, Han DS, Kang SW (2009) Induction of heme oxygenase-1 protects against podocyte apoptosis under diabetic conditions. Kidney Int 76(8):838–848CrossRefGoogle Scholar
  6. 6.
    Susztak K, Raff AC, Schiffer M, Bottinger EP (2006) Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes 55(1):225–233CrossRefGoogle Scholar
  7. 7.
    Bhatia K, Elmarakby AA, El- Remessey A, Sullivan JC (2012) Oxidative stress contributes to sex differences in angiotensin II-mediated hypertension in spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol 302:R274–R282CrossRefGoogle Scholar
  8. 8.
    Pradhan A, Umezu M, Fukagawa M (2006) Heme-oxygenase upregulation ameliorates angiotensin II-induced tubulointerstitial injury and salt-sensitive hypertension. Am J Nephrol 26(6):552–561CrossRefGoogle Scholar
  9. 9.
    Chow KM, Szeto CC (2004) Leflunomide and anti-glomerular basement membrane glomerulonephritis: comment on the letter by Bruyn et al. Arthritis Rheum 50(1):336–337CrossRefGoogle Scholar
  10. 10.
    Nguyen G (2006) Increased cyclooxygenase-2, hyperfiltration, glomerulosclerosis, and diabetic nephropathy: put the blame on the (pro)renin receptor? Kidney Int 70(4):618–620CrossRefGoogle Scholar
  11. 11.
    Tesch GH (2010) Review: Serum and urine biomarkers of kidney disease: a pathophysiological perspective. Nephrology (Carlton) 15(6):609–616CrossRefGoogle Scholar
  12. 12.
    Elmarakby AA, Faulkner J, Baban B, Sullivan JC (2012) Induction of hemeoxygenase-1 reduces renal oxidative stress and inflammation in diabetic spontaneously hypertensive rats. Int J Hypertens 2012:957235Google Scholar
  13. 13.
    Jaimes EA, Hua P, Tian RX, Raij L (2010) Human glomerular endothelium: interplay among glucose, free fatty acids, angiotensin II, and oxidative stress. Am J Physiol Renal Physiol 298(1):F125–F132CrossRefGoogle Scholar
  14. 14.
    Biswas SK, Lopes de Faria JB (2007) Pre-pubertal induction of experimental diabetes protects against early renal macrophage infiltration. Pediatr Nephrol 22(7):1045–1049CrossRefGoogle Scholar
  15. 15.
    Biswas SK, Peixoto EB, Souza DS, de Faria JB (2008) Hypertension increases pro-oxidant generation and decreases antioxidant defense in the kidney in early diabetes. Am J Nephrol 28(1):133–142CrossRefGoogle Scholar
  16. 16.
    Erejuwa OO, Sulaiman SA, Wahab MS, Sirajudeen KN, Salleh MS, Gurtu S (2011) Differential responses to blood pressure and oxidative stress in streptozotocin-induced diabetic wistar-kyoto rats and spontaneously hypertensive rats: effects of antioxidant (honey) treatment. Int J Mol Sci 12(3):1888–1907CrossRefGoogle Scholar
  17. 17.
    Ahmad J (2015) Management of diabetic nephropathy: recent progress and future perspective. Diabetes Metab Syndr 9(4):343–358CrossRefGoogle Scholar
  18. 18.
    Schauss AG, Wu X, Prior RL, Ou B, Huang D, Owens J et al (2006) Antioxidant capacity and other bioactivities of the freeze-dried Amazonian palm berry, Euterpe oleraceae mart. (acai). J Agric Food Chem 54(22):8604–8610CrossRefGoogle Scholar
  19. 19.
    de Oliveira PR, da Costa CA, de Bem GF, Cordeiro VS, Santos IB, de Carvalho LC, da Conceição EP, Lisboa PC, Ognibene DT, Sousa PJ, Martins GR, da Silva AJ, de Moura RS, Resende AC (2015) Euterpe oleracea Mart.-derived polyphenols protect mice from diet-induced obesity and fatty liver by regulating hepatic lipogenesis and cholesterol excretion. PLoS One 10(12):e0143721CrossRefGoogle Scholar
  20. 20.
    Rocha AP, Carvalho LC, Sousa MA, Madeira SV, Sousa PJ, Tano T, Schini-Kerth VB, Resende AC, Soares de Moura R (2007) Endothelium-dependent vasodilator effect of Euterpe oleracea Mart. (Acai) extracts in mesenteric vascular bed of the rat. Vascul Pharmacol 46(2):97–104CrossRefGoogle Scholar
  21. 21.
    da Costa CA, de Oliveira PR, de Bem GF, de Cavalho LC, Ognibene DT, da Silva AF, Dos Santos Valença S, Pires KM, da Cunha Sousa PJ, de Moura RS, Resende AC (2012) Euterpe oleracea Mart.-derived polyphenols prevent endothelial dysfunction and vascular structural changes in renovascular hypertensive rats: role of oxidative stress. Naunyn Schmiedebergs Arch Pharmacol 385(12):1199–1209CrossRefGoogle Scholar
  22. 22.
    de Bem GF, da Costa CA, de Oliveira PR, Cordeiro VSC, Santos IB, Carvalho LRM, Souza MA, Ognibene DT, Daleprane JB, Sousa PJ, Resende AC, de Moura RS (2014) Protective effect of Euterpe oleracea Mart (acai) extract on programmed changes in the adult rat offspring caused by maternal protein restriction during pregnancy. J Pharm Pharmacol 66(9):1328–1338CrossRefGoogle Scholar
  23. 23.
    de Oliveira PR, da Costa CA, de Bem GF, de Cavalho LC, de Souza MA, de Lemos Neto M, da Cunha Sousa PJ, de Moura RS, Resende AC (2010) Effects of an extract obtained from fruits of Euterpe oleracea Mart. in the components of metabolic syndrome induced in C57BL/6 J mice fed a high-fat diet. J Cardiovasc Pharmacol 56(6):619–626CrossRefGoogle Scholar
  24. 24.
    Moura RS, Ferreira TS, Lopes AA, Pires KM, Nesi RT, Resende AC, Souza PJ, Silva AJ, Borges RM, Porto LC, Valenca SS (2012) Effects of Euterpe oleracea Mart. (ACAI) extract in acute lung inflammation induced by cigarette smoke in the mouse. Phytomedicine 19(3–4):262–269CrossRefGoogle Scholar
  25. 25.
    Ribaldo PD, Souza DS, Biswas SK, Block K, Lopes de Faria JM, Lopes de Faria JB (2009) Green tea (Camellia sinensis) attenuates nephropathy by downregulating Nox4 NADPH oxidase in diabetic spontaneously hypertensive rats. J Nutr 139(1):96–100CrossRefGoogle Scholar
  26. 26.
    Cordeiro VSC, Carvalho LCRM, de Bem GF, da Costa CA, Souza MAV, Sousa PJC, Rocha VN, Carvalho J, Soares de Moura R, Resende AC (2015) Euterpe oleracea Mart. extract prevents vascular remodeling and endothelial dysfunction in spontaneously hypertensive rats. Int J Appl Res Nat Prod 8(3):6–16Google Scholar
  27. 27.
    Draper HH, Squires EJ, Mahmoodi H, Agarwal S, Hadley M (1993) A comparative evaluation of thiobarbituric acid methods for the determination of malondialdehyde in biological materials. Free Radic Biol Med 15(4):353–363CrossRefGoogle Scholar
  28. 28.
    Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG et al (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478CrossRefGoogle Scholar
  29. 29.
    Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  30. 30.
    Mandarim-de-Lacerda CA (2003) Stereological tools in biomedical research. An Acad Bras Cienc 75(4):469–486CrossRefGoogle Scholar
  31. 31.
    Bertram JF, Soosaipillai MC, Ricardo SD, Ryan GB (1992) Total numbers of glomeruli and individual glomerular cell types in the normal rat kidney. Cell Tissue Res 270(1):37–45CrossRefGoogle Scholar
  32. 32.
    Aritomi S, Niinuma K, Ogawa T, Konda T, Nitta K (2013) Additive effects of cilnidipine and angiotensin II receptor blocker in preventing the progression of diabetic nephropathy in diabetic spontaneously hypertensive rats. Clin Exp Nephrol 17(1):41–50CrossRefGoogle Scholar
  33. 33.
    Srinivasan PS, Hakim ZS, Santani DD, Goyal RK (1997) Effects of chronic treatment with amlodipine in streptozotocin-diabetic and spontaneously hypertensive rats. Pharmacol Res 35(5):423–428CrossRefGoogle Scholar
  34. 34.
    Chen ZY, Jiao R, Ma KY (2008) Cholesterol-lowering nutraceuticals and functional foods. J Agric Food Chem 56(19):8761–8773CrossRefGoogle Scholar
  35. 35.
    Chen S, Jim B, Ziyadeh FN (2003) Diabetic nephropathy and transforming growth factor-beta: transforming our view of glomerulosclerosis and fibrosis build-up. Semin Nephrol 23(6):532–543CrossRefGoogle Scholar
  36. 36.
    Krag S, Nyengaard JR, Wogensen L (2007) Combined effects of moderately elevated blood glucose and locally produced TGF-beta1 on glomerular morphology and renal collagen production. Nephrol Dial Transplant 22(9):2485–2496CrossRefGoogle Scholar
  37. 37.
    Satchell SC, Tooke JE (2008) What is the mechanism of microalbuminuria in diabetes: a role for the glomerular endothelium? Diabetologia 51(5):714–725CrossRefGoogle Scholar
  38. 38.
    Wang Y, Wang DH (2011) Protective effect of TRPV1 against renal fibrosis via inhibition of TGF-beta/Smad signaling in DOCA-salt hypertension. Mol Med 17(11–12):1204–1212Google Scholar
  39. 39.
    Chen S, Chen H, Liu Q, Ma Q (2015) Effect of simvastatin on the expression of nephrin, podocin, and vascular endothelial growth factor (VEGF) in podocytes of diabetic rat. Int J Clin Exp Med 8(10):18225–18234.&nbspGoogle Scholar
  40. 40.
    de Moura RS, Pires KM, Santos FT, Lopes AA, Nesi RT, Resende AC, Sousa PJ, da Silva AJ, Porto LC, Valenca SS (2011) Addition of acai (Euterpe oleracea) to cigarettes has a protective effect against emphysema in mice. Food Chem Toxicol 49(4):855–863CrossRefGoogle Scholar
  41. 41.
    Galkina E, Ley K (2006) Leukocyte recruitment and vascular injury in diabetic nephropathy. J Am Soc Nephrol 17(2):368–377CrossRefGoogle Scholar
  42. 42.
    Schmid H, Boucherot A, Yasuda Y, Henger A, Brunner B, Eichinger F et al (2006) Modular activation of nuclear factor-kappaB transcriptional programs in human diabetic nephropathy. Diabetes 55(11):2993–3003CrossRefGoogle Scholar
  43. 43.
    Elsherbiny NM, Al-Gayyar MM, Abd El Galil KH (2015) Nephroprotective role of dipyridamole in diabetic nephropathy: effect on inflammation and apoptosis. Life Sci 143:8–17CrossRefGoogle Scholar
  44. 44.
    Kanamori H, Matsubara T, Mima A, Sumi E, Nagai K, Takahashi T et al (2007) Inhibition of MCP-1/CCR2 pathway ameliorates the development of diabetic nephropathy. Biochem Biophys Res Commun 360(4):772–777CrossRefGoogle Scholar
  45. 45.
    Li D, Peng C, Xie X, Mao Y, Li M, Cao Z et al (2014) Antidiabetic effect of flavonoids from Malus toringoides (Rehd.) Hughes leaves in diabetic mice and rats. J Ethnopharmacol 153(3):561–567CrossRefGoogle Scholar
  46. 46.
    Pessôa BS, Peixoto EB, Papadimitriou A, Lopes de Faria JM, Lopes de Faria JB (2012) Spironolactone improves nephropathy by enhancing glucose-6-phosphate dehydrogenase activity and reducing oxidative stress in diabetic hypertensive rat. J Renin Angiotensin Aldosterone Syst 13(1):56–66CrossRefGoogle Scholar
  47. 47.
    Gorin Y, Block K, Hernandez J, Bhandari B, Wagner B, Barnes JL et al (2005) Nox4 NAD(P)H oxidase mediates hypertrophy and fibronectin expression in the diabetic kidney. J Biol Chem 280(47):39616–39626CrossRefGoogle Scholar
  48. 48.
    Patinha D, Afonso J, Sousa T, Morato M, Albino-Teixeira A (2014) Activation of adenosine receptors improves renal antioxidant status in diabetic Wistar but not SHR rats. Ups J Med Sci 119(1):10–18CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Viviane da Silva Cristino Cordeiro
    • 1
  • Graziele Freitas de Bem
    • 1
  • Cristiane Aguiar da Costa
    • 1
  • Izabelle Barcellos Santos
    • 1
  • Lenize Costa Reis Marins de Carvalho
    • 1
  • Dayane Teixeira Ognibene
    • 1
  • Ana Paula Machado da Rocha
    • 1
  • Jorge José de Carvalho
    • 2
  • Roberto Soares de Moura
    • 1
  • Angela Castro Resende
    • 1
  1. 1.Department of Pharmacology, Institute of BiologyState University of Rio de JaneiroRio de JaneiroBrazil
  2. 2.Department of Histology and Embryology, Institute of BiologyState University of Rio de JaneiroRio de JaneiroBrazil

Personalised recommendations