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Dietary rice protein isolate attenuates atherosclerosis in apoE-deficient mice by upregulating antioxidant enzymes

  • Ramona L. Burris
    Affiliations
    Arkansas Children's Nutrition Center, University of Arkansas for Medical Sciences, Little Rock, AR 72202, USA

    Arkansas Children's Hospital Research Institute, University of Arkansas for Medical Sciences, Little Rock, AR 72202, USA
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  • Cheng-Hui Xie
    Affiliations
    Arkansas Children's Nutrition Center, University of Arkansas for Medical Sciences, Little Rock, AR 72202, USA

    Department of Physiology and Biophysics, University of Arkansas for Medical Sciences, Little Rock, AR 72202, USA
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  • Author Footnotes
    1 Present address: Department of Anatomy and Cell Biology, University of Florida, Gainesville, FL, USA.
    Prajitha Thampi
    Footnotes
    1 Present address: Department of Anatomy and Cell Biology, University of Florida, Gainesville, FL, USA.
    Affiliations
    Arkansas Children's Nutrition Center, University of Arkansas for Medical Sciences, Little Rock, AR 72202, USA

    Arkansas Children's Hospital Research Institute, University of Arkansas for Medical Sciences, Little Rock, AR 72202, USA

    Department of Microbiology and Immunology, University of Arkansas for Medical Sciences, Little Rock, AR 72202, USA
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  • Xianli Wu
    Affiliations
    Arkansas Children's Nutrition Center, University of Arkansas for Medical Sciences, Little Rock, AR 72202, USA

    Department of Physiology and Biophysics, University of Arkansas for Medical Sciences, Little Rock, AR 72202, USA
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  • Stepan B. Melnyk
    Affiliations
    Department of Pediatrics, University of Arkansas for Medical Sciences, Little Rock, AR 72202, USA
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  • Shanmugam Nagarajan
    Correspondence
    Corresponding author at: Arkansas Children's Nutrition Center, 15 Children's Way, Little Rock, AR, USA. Tel.: +1 501 364 2814; fax: +1 501 364 3161.
    Affiliations
    Arkansas Children's Nutrition Center, University of Arkansas for Medical Sciences, Little Rock, AR 72202, USA

    Arkansas Children's Hospital Research Institute, University of Arkansas for Medical Sciences, Little Rock, AR 72202, USA

    Department of Microbiology and Immunology, University of Arkansas for Medical Sciences, Little Rock, AR 72202, USA
    Search for articles by this author
  • Author Footnotes
    1 Present address: Department of Anatomy and Cell Biology, University of Florida, Gainesville, FL, USA.

      Abstract

      Rice-based diets may have been reported to protect against the development of atherosclerosis; however, the underlying mechanism(s) for this protection remains unknown. In this report, the mechanism(s) contributing to the atheroprotective effects of rice-based diet was addressed using the apolipoprotein E knockout (apoE−/−) mice fed rice protein isolate (RPI) or casein (CAS). Reduced atherosclerotic lesions were observed in aortic sinus and enface analyses of the descending aorta in RPI-fed apoE−/− mice compared with CAS-fed mice. Plasma total- and HDL-cholesterol levels were not different amongst the two groups, suggesting alternative mechanism(s) could have contributed to the atheroprotective effect of rice-based diets. Plasma oxLDL and anti-oxLDL IgG levels were significantly decreased in RPI-fed compared to CAS-fed animals. Plasma and aortic tissue GSH levels and GSH:GSSG ratio were higher in RPI-fed mice compared to CAS-fed group. Interestingly, RPI feeding increased mRNA and protein expression of superoxide dismutase, and mRNA expression of catalase, glutathione peroxidase and glutathione reductase, key antioxidant enzymes implicated inhibiting oxidative stress leading to atherosclerosis. In conclusion, these findings suggest that the reduction in atherosclerotic lesions observed in mice fed the rice-based diet is mediated in part by inhibiting oxidative stress and subsequent oxLDL generation that could result in reduced foam cell formation, an early event during atherogenesis.

      Abbreviations:

      ApoE−/− (apolipoprotein E knockout), CAS (casein), LOX-1 (lectin-like oxidized LDL binding protein-1), ORAC (Oxygen Radical Absorbance Capacity), oxLDL (oxidized low-density lipoprotein), RPI (rice protein isolate)

      Keywords

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      References

        • Adlercreutz H.
        Western diet and Western diseases: some hormonal and biochemical mechanisms and associations.
        Scand J Clin Lab Invest. 1990; 50: 3-23
        • Kolonel L.N.
        Variability in diet and its relation to risk in ethnic and migration groups.
        Basic Life Sci. 1988; 43: 129-135
        • Mikkola T.S.
        • Clarkson T.B.
        Estrogen replacement therapy, atherosclerosis, and vascular function.
        Cardiovasc Res. 2002; 53: 605-619
        • Qureshi A.A.
        • Salser W.A.
        • Parmar R.
        • Emeson E.E.
        Novel tocotrienols of rice bran inhibit atherosclerotic lesions in C57BL/6 ApoE-deficient mice.
        J Nutr. 2001; 131: 2606-2618
        • Seetharamaiah G.S.
        • Chandrasekhara N.
        Studies on hypocholesterolemic activity of rice bran oil.
        Atherosclerosis. 1989; 78: 219-223
        • Ling W.H.
        • Cheng Q.X.
        • Ma J.
        • Wang T.
        Red and black rice decrease atherosclerotic plaque formation and increase antioxidant status in rabbits.
        J Nutr. 2001; 131: 1421-1426
        • Xia X.
        • Ling W.
        • Ma J.
        • et al.
        An anthocyanin-rich extract from black rice enhances atherosclerotic plaque stabilization in apolipoprotein E-deficient mice.
        J Nutr. 2006; 136: 2220-2225
        • Ni W.
        • Tsuda Y.
        • Takashima S.
        • Sato H.
        • Sato M.
        • Imaizumi K.
        Anti-atherogenic effect of soya and rice-protein isolate, compared with casein, in apolipoprotein E-deficient mice.
        Br J Nutr. 2003; 90: 13-20
        • Libby P.
        Inflammation in atherosclerosis.
        Nature. 2002; 420: 868-874
        • Steinberg D.
        Low density lipoprotein oxidation and its pathobiological significance.
        J Biol Chem. 1997; 272: 20963-20966
        • Hsiai T.
        • Berliner J.A.
        Oxidative stress as a regulator of murine atherosclerosis.
        Curr Drug Targets. 2007; 8: 1222-1229
        • Oliveira H.C.
        • Cosso R.G.
        • Alberici L.C.
        • et al.
        Oxidative stress in atherosclerosis-prone mouse is due to low antioxidant capacity of mitochondria.
        FASEB J. 2005; 19: 278-280
        • Harrison D.
        • Griendling K.K.
        • Landmesser U.
        • Hornig B.
        • Drexler H.
        Role of oxidative stress in atherosclerosis.
        Am J Cardiol. 2003; 91: 7A-11A
        • Greaves D.R.
        • Gordon S.
        Thematic review series: the immune system and atherogenesis. Recent insights into the biology of macrophage scavenger receptors.
        J Lipid Res. 2005; 46: 11-20
        • Zhang S.H.
        • Reddick R.L.
        • Piedrahita J.A.
        • Maeda N.
        Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E.
        Science. 1992; 258: 468-471
        • Caligiuri G.
        • Nicoletti A.
        • Zhou X.
        • Tornberg I.
        • Hansson G.K.
        Effects of sex and age on atherosclerosis and autoimmunity in apoE-deficient mice.
        Atherosclerosis. 1999; 145: 301-308
        • Reeves P.G.
        • Rossow K.L.
        • Lindlauf J.
        Development and testing of the AIN-93 purified diets for rodents: results on growth, kidney calcification and bone mineralization in rats and mice.
        J Nutr. 1993; 123: 1923-1931
        • Morita T.
        • Oh-hashi A.
        • Takei K.
        • Ikai M.
        • Kasaoka S.
        • Kiriyama S.
        Cholesterol-lowering effects of soybean, potato and rice proteins depend on their low methionine contents in rats fed a cholesterol-free purified diet.
        J Nutr. 1997; 127: 470-477
        • Paigen B.
        • Holmes P.A.
        • Mitchell D.
        • Albee D.
        Comparison of atherosclerotic lesions and HDL-lipid levels in male, female, and testosterone-treated female mice from strains C57BL/6, BALB/c and C3H.
        Atherosclerosis. 1987; 64: 215-221
        • Nagarajan S.
        • Burris R.L.
        • Stewart B.W.
        • Wilkerson J.E.
        • Badger T.M.
        Dietary soy protein isolate ameliorates atherosclerotic lesions in apolipoprotein E-deficient mice potentially by inhibiting monocyte chemoattractant protein-1 expression.
        J Nutr. 2008; 138: 332-337
        • Friedewald W.T.
        • Levy R.I.
        • Fredrickson D.S.
        Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of preparative ultracentrifuge.
        Clin Chem. 1972; 18: 499-502
        • Enkhmaa B.
        • Shiwaku K.
        • Katsube T.
        • et al.
        Mulberry (Morus alba L.) leaves and their major flavonol quercetin 3-(6-malonylglucoside) attenuate atherosclerotic lesion development in LDL receptor-deficient mice.
        J Nutr. 2005; 135: 729-734
        • Wu X.
        • Beecher G.R.
        • Holden J.M.
        • Haytowitz D.B.
        • Gebhardt S.E.
        • Prior R.L.
        Lipophilic and hydrophilic antioxidant capacities of common foods in the United States.
        J Agric Food Chem. 2004; 52: 4026-4037
        • Melnyk S.
        • Pogribna M.
        • Pogribny I.
        • Hine R.J.
        • James S.J.
        A new HPLC method for the simultaneous determination of oxidized and reduced plasma aminothiols using coulometric electrochemical detection.
        J Nutr Biochem. 1999; 10: 490-497
        • Thampi P.
        • Stewart B.W.
        • Joseph L.
        • Melnyk S.B.
        • Hennings L.J.
        • Nagarajan S.
        Dietary homocysteine promotes atherosclerosis in apoE-deficient mice by inducing scavenger receptors expression.
        Atherosclerosis. 2008; 197: 620-629
        • Zhou X.
        • Paulsson G.
        • Stemme S.
        • Hansson G.K.
        Hypercholesterolemia is associated with a T helper (Th) 1/Th2 switch of the autoimmune response in atherosclerotic apo E-knockout mice.
        J Clin Invest. 1998; 101: 1717-1725
        • Stewart B.W.
        • Nagarajan S.
        Recombinant CD36 inhibits oxLDL-induced ICAM-1-dependent monocyte adhesion.
        Mol Immunol. 2006; 43: 255-267
        • Lin S.J.
        • Shyue S.K.
        • Liu P.L.
        • et al.
        Adenovirus-mediated overexpression of catalase attenuates oxLDL-induced apoptosis in human aortic endothelial cells via AP-1 and C-Jun N-terminal kinase/extracellular signal-regulated kinase mitogen-activated protein kinase pathways.
        J Mol Cell Cardiol. 2004; 36: 129-139
        • Shatrov V.A.
        • Brune B.
        Induced expression of manganese superoxide dismutase by non-toxic concentrations of oxidized low-density lipoprotein (oxLDL) protects against oxLDL-mediated cytotoxicity.
        Biochem J. 2003; 374: 505-511
        • Van Tits L.
        • De Graaf J.
        • Hak-Lemmers H.
        • et al.
        Increased levels of low-density lipoprotein oxidation in patients with familial hypercholesterolemia and in end-stage renal disease patients on hemodialysis.
        Lab Invest. 2003; 83: 13-21
        • Tabuchi M.
        • Inoue K.
        • Usui-Kataoka H.
        • et al.
        The association of C-reactive protein with an oxidative metabolite of LDL and its implication in atherosclerosis.
        J Lipid Res. 2007; 48: 768-781
        • Kato R.
        • Mori C.
        • Kitazato K.
        • et al.
        Transient increase in plasma oxidized LDL during the progression of atherosclerosis in apolipoprotein E knockout mice.
        Arterioscler Thromb Vasc Biol. 2009; 29: 33-39
        • Stocker R.
        • Keaney Jr., J.F.
        Role of oxidative modifications in atherosclerosis.
        Physiol Rev. 2004; 84: 1381-1478
        • Yu S.
        • Fang N.
        • Li Q.
        • et al.
        In vitro actions on human cancer cells and the liquid chromatography–mass spectrometry/mass spectrometry fingerprint of phytochemicals in rice protein isolate.
        J Agric Food Chem. 2006; 54: 4482-4492
        • Rosenblat M.
        • Aviram M.
        Macrophage glutathione content and glutathione peroxidase activity are inversely related to cell-mediated oxidation of LDL: in vitro and in vivo studies.
        Free Radic Biol Med. 1998; 24: 305-317
        • Rosenblat M.
        • Coleman R.
        • Aviram M.
        Increased macrophage glutathione content reduces cell-mediated oxidation of LDL and atherosclerosis in apolipoprotein E-deficient mice.
        Atherosclerosis. 2002; 163: 17-28
        • Faruqi R.M.
        • Poptic E.J.
        • Faruqi T.R.
        • De La Motte C.
        • DiCorleto P.E.
        Distinct mechanisms for N-acetylcysteine inhibition of cytokine-induced E-selectin and VCAM-1 expression.
        Am J Physiol. 1997; 273: H817-H826
        • Dedoussis G.V.
        • Kaliora A.C.
        • Psarras S.
        • et al.
        Antiatherogenic effect of Pistacia lentiscus via GSH restoration and downregulation of CD36 mRNA expression.
        Atherosclerosis. 2004; 174: 293-303
        • Ashfaq S.
        • Abramson J.L.
        • Jones D.P.
        • et al.
        The relationship between plasma levels of oxidized and reduced thiols and early atherosclerosis in healthy adults.
        J Am Coll Cardiol. 2006; 47: 1005-1011
        • Qiao M.
        • Kisgati M.
        • Cholewa J.M.
        • et al.
        Increased expression of glutathione reductase in macrophages decreases atherosclerotic lesion formation in low-density lipoprotein receptor-deficient mice.
        Arterioscler Thromb Vasc Biol. 2007; 27: 1375-1382
        • Fang X.
        • Weintraub N.L.
        • Rios C.D.
        • et al.
        Overexpression of human superoxide dismutase inhibits oxidation of low-density lipoprotein by endothelial cells.
        Circ Res. 1998; 82: 1289-1297
        • Yang H.
        • Roberts L.J.
        • Shi M.J.
        • et al.
        Retardation of atherosclerosis by overexpression of catalase or both Cu/Zn-superoxide dismutase and catalase in mice lacking apolipoprotein E.
        Circ Res. 2004; 95: 1075-1081
        • Lewis P.
        • Stefanovic N.
        • Pete J.
        • et al.
        Lack of the antioxidant enzyme glutathione peroxidase-1 accelerates atherosclerosis in diabetic apolipoprotein E-deficient mice.
        Circulation. 2007; 115: 2178-2187
        • Torzewski M.
        • Ochsenhirt V.
        • Kleschyov A.L.
        • et al.
        Deficiency of glutathione peroxidase-1 accelerates the progression of atherosclerosis in apolipoprotein E-deficient mice.
        Arterioscler Thromb Vasc Biol. 2007; 27: 850-857
        • Guo Z.
        • Ran Q.
        • Roberts 2nd, L.J.
        • et al.
        Suppression of atherogenesis by overexpression of glutathione peroxidase-4 in apolipoprotein E-deficient mice.
        Free Radic Biol Med. 2008; 44: 343-352
        • Yang H.
        • Shi M.
        • Richardson A.
        • Vijg J.
        • Guo Z.
        Attenuation of leukocyte–endothelium interaction by antioxidant enzymes.
        Free Radic Biol Med. 2003; 35: 266-276
        • Kume N.
        • Cybulsky M.I.
        • Gimbrone Jr., M.A.
        Lysophosphatidylcholine, a component of atherogenic lipoproteins, induces mononuclear leukocyte adhesion molecules in cultured human and rabbit arterial endothelial cells.
        J Clin Invest. 1992; 90: 1138-1144
        • Murohara T.
        • Scalia R.
        • Lefer A.M.
        Lysophosphatidylcholine promotes P-selectin expression in platelets and endothelial cells. Possible involvement of protein kinase C activation and its inhibition by nitric oxide donors.
        Circ Res. 1996; 78: 780-789
        • Quinn M.T.
        • Parthasarathy S.
        • Steinberg D.
        Lysophosphatidylcholine: a chemotactic factor for human monocytes and its potential role in atherogenesis.
        Proc Natl Acad Sci USA. 1988; 85: 2805-2809
        • Liu-Wu Y.
        • Hurt-Camejo E.
        • Wiklund O.
        Lysophosphatidylcholine induces the production of IL-1beta by human monocytes.
        Atherosclerosis. 1998; 137: 351-357
        • Zembowicz A.
        • Tang J.L.
        • Wu K.K.
        Transcriptional induction of endothelial nitric oxide synthase type III by lysophosphatidylcholine.
        J Biol Chem. 1995; 270: 17006-17010
        • Hirata K.
        • Miki N.
        • Kuroda Y.
        • Sakoda T.
        • Kawashima S.
        • Yokoyama M.
        Low concentration of oxidized low-density lipoprotein and lysophosphatidylcholine upregulate constitutive nitric oxide synthase mRNA expression in bovine aortic endothelial cells.
        Circ Res. 1995; 76: 958-962
        • Sheikh A.M.
        • Ochi H.
        • Manabe A.
        • Masuda J.
        Lysophosphatidylcholine posttranscriptionally inhibits interferon-gamma-induced IP-10, Mig and I-Tac expression in endothelial cells.
        Cardiovasc Res. 2005; 65: 263-271
        • Hara S.
        • Shike T.
        • Takasu N.
        • Mizui T.
        Lysophosphatidylcholine promotes cholesterol efflux from mouse macrophage foam cells.
        Arterioscler Thromb Vasc Biol. 1997; 17: 1258-1266
        • Hou M.
        • Xia M.
        • Zhu H.
        • et al.
        Lysophosphatidylcholine promotes cholesterol efflux from mouse macrophage foam cells via PPARgamma-LXRalpha-ABCA1-dependent pathway associated with apoE.
        Cell Biochem Funct. 2007; 25: 33-44
        • Adams M.R.
        • Golden D.L.
        • Franke A.A.
        • Potter S.M.
        • Smith H.S.
        • Anthony M.S.
        Dietary soy beta-conglycinin (7S globulin) inhibits atherosclerosis in mice.
        J Nutr. 2004; 134: 511-516