The Journal of Nutritional Biochemistry
Volume 20, Issue 11 , Pages 882-893 , November 2009

Apolipoprotein E determines the hepatic transcriptional profile of dietary maslinic acid in mice

  • Natalia Guillen

      Affiliations

    • Departamento de Bioquímica y Biología Molecular y Celular, Instituto Aragonés de Ciencias de la Salud (Universidad de Zaragoza–Dirección Salud del Gobierno de Aragón), E-50013 Zaragoza, Spain
    • CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, E-28029 Madrid, Spain
  • ,
  • Sergio Acín

      Affiliations

    • Departamento de Bioquímica y Biología Molecular y Celular, Instituto Aragonés de Ciencias de la Salud (Universidad de Zaragoza–Dirección Salud del Gobierno de Aragón), E-50013 Zaragoza, Spain
  • ,
  • Joaquín C. Surra

      Affiliations

    • Departamento de Bioquímica y Biología Molecular y Celular, Instituto Aragonés de Ciencias de la Salud (Universidad de Zaragoza–Dirección Salud del Gobierno de Aragón), E-50013 Zaragoza, Spain
    • CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, E-28029 Madrid, Spain
  • ,
  • Carmen Arnal

      Affiliations

    • CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, E-28029 Madrid, Spain
    • Departamento de Patología Animal, Facultad de Veterinaria, Universidad de Zaragoza, E-50013 Zaragoza, Spain
  • ,
  • Javier Godino

      Affiliations

    • Departamento de Bioquímica y Biología Molecular y Celular, Instituto Aragonés de Ciencias de la Salud (Universidad de Zaragoza–Dirección Salud del Gobierno de Aragón), E-50013 Zaragoza, Spain
  • ,
  • Andrés García-Granados

      Affiliations

    • Departamento de Química Orgánica, Facultad de Ciencias, Universidad de Granada, E-18071 Granada, Spain
  • ,
  • Pedro Muniesa

      Affiliations

    • CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, E-28029 Madrid, Spain
    • Departamento de Anatomía y Embriología y Genética Animal, Facultad de Veterinaria, Universidad de Zaragoza, E-50013 Zaragoza, Spain
  • ,
  • Valentina Ruiz-Gutiérrez

      Affiliations

    • Group of Nutrition and Lipid Metabolism, Instituto de la Grasa, CSIC, E-41012 Sevilla, Spain
  • ,
  • Jesús Osada

      Affiliations

    • Departamento de Bioquímica y Biología Molecular y Celular, Instituto Aragonés de Ciencias de la Salud (Universidad de Zaragoza–Dirección Salud del Gobierno de Aragón), E-50013 Zaragoza, Spain
    • CIBER de Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, E-28029 Madrid, Spain
    • Corresponding Author InformationCorresponding author. Department of Biochemistry and Molecular Biology, Veterinary School, University of Zaragoza, E-50013 Zaragoza, Spain. Tel.: +34 976 761 644; fax: +34 976 761 612.

Received 1 April 2008 ,Revised 8 August 2008 ,Accepted 11 August 2008.

References 

  1. Keys A. Mediterranean diet and public health: personal reflections. Am J Clin Nutr. 1995;61(Suppl):1321S–1323S
  2. Visioli F, Galli C, Plasmati E, Viappiani S, Hernandez A, Colombo C, et al. Olive phenol hydroxytyrosol prevents passive smoking-induced oxidative stress. Circulation. 2000;102:2169–2171
  3. de la Puerta R, Martinez Dominguez ME, Ruiz-Gutierrez V, Flavill JA, Hoult JR. Effects of virgin olive oil phenolics on scavenging of reactive nitrogen species and upon nitrergic neurotransmission. Life Sci. 2001;69:1213–1222
  4. de la Puerta-Vazquez R, Martinez-Dominguez E, Sanchez Perona J, Ruiz-Gutierrez V. Effects of different dietary oils on inflammatory mediator generation and fatty acid composition in rat neutrophils. Metabolism. 2004;53:59–65
  5. Kris-Etherton PM. Monounsaturated fatty acids and risk of cardiovascular disease. Circulation. 1999;100:1253–1258
  6. Perona JS, Cabello-Moruno R, Ruiz-Gutiérrez V. The role of virgin olive oil components in the modulation of endothelial function. Journal of Nutritional Biochemistry. 2006;17:429–445
  7. Perona JS, Canizares J, Montero E, Sanchez-Dominguez JM, Ruiz-Gutierrez V. Plasma lipid modifications in elderly people after administration of two virgin olive oils of the same variety (Olea europaea var. hojiblanca) with different triacylglycerol composition. Br J Nutr. 2003;89:819–826
  8. Calleja L, Paris MA, Paul A, Vilella E, Joven J, Jimenez A, et al. Low-cholesterol and high-fat diets reduce atherosclerotic lesion development in ApoE-knockout mice. Arterioscler Thromb Vasc Biol. 1999;19:2368–2375
  9. Herrera MD, Perez-Guerrero C, Marhuenda E, Ruiz-Gutierrez V. Effects of dietary oleic-rich oils (virgin olive and high-oleic-acid sunflower) on vascular reactivity in Wistar–Kyoto and spontaneously hypertensive rats. Br J Nutr. 2001;86:349–357
  10. Sanchez Perona J, Martínez-González J, Sánchez-Domínguez JM, Badimon L, Ruiz-Gutierrez V. The unsaponifiable fraction of virgin olive oil in chylomicrons from men improves the balance between vasoprotective and pro-thrombotic factors released by endothelial cells. J Nutr. 2004;134:3284–3289
  11. Rodriguez-Rodriguez R, Perona JS, Herrera MD, Ruiz-Gutierrez V. Triterpenic compounds from “orujo” olive oil elicit vasorelaxation in aorta from spontaneously hypertensive rats. J Agric Food Chem. 2006;54:2096–2102
  12. Acín S, Navarro MA, Perona JS, Surra JC, Guillen N, Arnal C, et al. Microarray analysis of hepatic genes differentially expressed in the presence of the unsaponifiable fraction of olive oil in apolipoprotein E-deficient mice. Br J Nutr. 2007;97:628–638
  13. Montilla MP, Agil A, Navarro MC, Jimenez MI, Garcia-Granados A, Parra A, et al. Antioxidant activity of maslinic acid, a triterpene derivative obtained from Olea europaea. Planta Med. 2003;69:472–474
  14. Wang R, Wei W, Wang L, Liu R, Yi D, Du L. Constituents of the flowers of Punica granatum. Fitoterapia. 2006;77:534–537
  15. Marquez Martin A, de la Puerta Vazquez R, Fernandez-Arche A, Ruiz-Gutierrez V. Suppressive effect of maslinic acid from pomace olive oil on oxidative stress and cytokine production in stimulated murine macrophages. Free Radic Res. 2006;40:295–302
  16. Yang ZG, Li HR, Wang LY, Li YH, Lu SG, Wen XF, et al. Triterpenoids from Hippophae rhamnoides L. and their nitric oxide production-inhibitory and DPPH radical-scavenging activities. Chem Pharm Bull (Tokyo). 2007;55:15–18
  17. Wen X, Sun H, Liu J, Wu G, Zhang L, Wu X, et al. Pentacyclic triterpenes: Part 1. The first examples of naturally occurring pentacyclic triterpenes as a new class of inhibitors of glycogen phosphorylases. Bioorg Med Chem Lett. 2005;15:4944–4948
  18. Xu HX, Zeng FQ, Wan M, Sim KY. Anti-HIV triterpene acids from Geum japonicum. J Nat Prod. 1996;59:643–645
  19. Reyes FJ, Centelles JJ, Lupianez JA, Cascante M. (2Alpha,3beta)-2,3-dihydroxyolean-12-en-28-oic acid, a new natural triterpene from Olea europea, induces caspase dependent apoptosis selectively in colon adenocarcinoma cells. FEBS Lett. 2006;580:6302–6310
  20. Juan ME, Wenzel U, Ruiz-Gutierrez V, Daniel H, Planas JM. Olive fruit extracts inhibit proliferation and induce apoptosis in HT-29 human colon cancer cells. J Nutr. 2006;136:2553–2557
  21. Martin R, Carvalho J, Ibeas E, Hernandez M, Ruiz-Gutierrez V, Nieto ML. Acidic triterpenes compromise growth and survival of astrocytoma cell lines by regulating reactive oxygen species accumulation. Cancer Res. 2007;67:3741–3751
  22. Alba-Mendoza J, Hidalgo-Casado F, Ruiz-Gómez MA, Martínez Román F, Moyano-Pérez MJ, Cert-Ventulá A, et al. Características de los aceites de oliva de primera y segunda centrifugación. Grasas Aceites. 1996;47:163–181
  23. Garcia-Granados A, Martinez A, Moliz JN, Parra A, Rivas F. 2-α,3-β-Dihydroxyolean-12-en-28-oic acid (maslinic acid). Molecules. 1998;3:M88
  24. European Commission Regulation (EEC) No. 2568/91 of 11 July 1991 on the characteristics of olive oil and olive-residue oil and on the relevant methods of analysis. Off J Comm Eur Communities. 1991;L 248:1–83
  25. Canales RD, Luo Y, Willey JC, Austermiller B, Barbacioru CC, Boysen C, et al. Evaluation of DNA microarray results with quantitative gene expression platforms. Nat Biotechnol. 2006;24:1115–1122
  26. Gilsbach R, Kouta M, Bönisch H, Brüss M. Comparison of in vitro and in vivo reference genes for internal standardization of real-time PCR data. Biotechniques. 2006;40:173–177
  27. Arbonés-Mainar JM, Navarro MA, Acín S, Guzmán MA, Arnal C, Surra JC, et al. Trans-10, cis-12- and cis-9, trans-11-conjugated linoleic acid isomers selectively modify HDL-apolipoprotein composition in apolipoprotein E knockout mice. J Nutr. 2006;136:353–359
  28. Guillen N, Acin S, Navarro MA, Perona JS, Arbones-Mainar JM, Arnal C, et al. Squalene in a sex-dependent manner modulates atherosclerotic lesion which correlates with hepatic fat content in apoE-knockout male mice. Atherosclerosis. 2008;196:558–564
  29. Acin S, Navarro MA, Arbones-Mainar JM, Guillen N, Sarria AJ, Carnicer R, et al. Hydroxytyrosol administration enhances atherosclerotic lesion development in apo E deficient mice. J Biochem (Tokyo). 2006;140:383–391
  30. Lofgren S, Hagbjork AL, Ekman S, Fransson-Steen R, Terelius Y. Metabolism of human cytochrome P450 marker substrates in mouse: a strain and gender comparison. Xenobiotica. 2004;34:811–834
  31. Ando M, Tomoyori H, Imaizumi K. Dietary cholesterol-oxidation products accumulate in serum and liver in apolipoprotein E-deficient mice, but do not accelerate atherosclerosis. Br J Nutr. 2002;88:339–345
  32. Upmacis RK, Crabtree MJ, Deeb RS, Shen H, Lane PB, Benguigui LE, et al. Profound biopterin oxidation and protein tyrosine nitration in tissues of ApoE-null mice on an atherogenic diet: contribution of inducible nitric oxide synthase. Am J Physiol Heart Circ Physiol. 2007;293:H2878–H2887
  33. Sehayek E, Shefer S, Nguyen LB, Ono JG, Merkel M, Breslow JL. Apolipoprotein E regulates dietary cholesterol absorption and biliary cholesterol excretion: studies in C57BL/6 apolipoprotein E knockout mice. Proc Natl Acad Sci U S A. 2000;97:3433–3437
  34. Acín S, Navarro MA, Carnicer R, Arbonés JM, Guzmán MA, Arnal C, et al. Dietary cholesterol suppresses the ability of olive oil to delay the development of atherosclerotic lesions in apolipoprotein E knockout mice. Atherosclerosis. 2005;182:17–28
  35. Fernandez-Navarro M, Peragon J, Esteban FJ, de la Higuera M, Lupianez JA. Maslinic acid as a feed additive to stimulate growth and hepatic protein-turnover rates in rainbow trout (Onchorhynchus mykiss). Comp Biochem Physiol C Toxicol Pharmacol. 2006;144:130–140
  36. Fernandez-Navarro M, Peragon J, Amores V, De La Higuera M, Lupianez JA. Maslinic acid added to the diet increases growth and protein-turnover rates in the white muscle of rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol C Toxicol Pharmacol. 2008;147:158–167
  37. Marquez-Martin A, De La Puerta R, Fernandez-Arche A, Ruiz-Gutierrez V, Yaqoob P. Modulation of cytokine secretion by pentacyclic triterpenes from olive pomace oil in human mononuclear cells. Cytokine. 2006;36:211–217
  38. Wen X, Zhang P, Liu J, Zhang L, Wu X, Ni P, et al. Pentacyclic triterpenes: Part 2. Synthesis and biological evaluation of maslinic acid derivatives as glycogen phosphorylase inhibitors. Bioorg Med Chem Lett. 2006;16:722–726
  39. Artieda M, Cenarro A, Junquera C, Lasierra P, Martinez-Lorenzo MJ, Pocovi M, et al. Tendon xanthomas in familial hypercholesterolemia are associated with a differential inflammatory response of macrophages to oxidized LDL. FEBS Lett. 2005;579:4503–4512
  40. Calpe-Berdiel L, Escola-Gil JC, Ribas V, Navarro-Sastre A, Garces-Garces J, Blanco-Vaca F. Changes in intestinal and liver global gene expression in response to a phytosterol-enriched diet. Atherosclerosis. 2005;181:75–85
  41. Dutta R, Singh U, Li TB, Fornage M, Teng BB. Hepatic gene expression profiling reveals perturbed calcium signaling in a mouse model lacking both LDL receptor and Apobec1 genes. Atherosclerosis. 2003;169:51–62
  42. Peng X, Wood CL, Blalock EM, Chen KC, Landfield PW, Stromberg AJ. Statistical implications of pooling RNA samples for microarray experiments. BMC Bioinformatics. 2003;4:1–9
  43. Kiela PR, Midura AJ, Kuscuoglu N, Jolad SD, Solyom AM, Besselsen DG, et al. Effects of Boswellia serrata in mouse models of chemically induced colitis. Am J Physiol Gastrointest Liver Physiol. 2005;288:G798–G808
  44. Dinkova-Kostova AT, Liby KT, Stephenson KK, Holtzclaw WD, Gao X, Suh N, et al. Extremely potent triterpenoid inducers of the phase 2 response: correlations of protection against oxidant and inflammatory stress. Proc Natl Acad Sci U S A. 2005;102:4584–4589
  45. Piedrahita JA, Zhang SH, Hagaman JR, Oliver PM, Maeda N. Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proc Natl Acad Sci U S A. 1992;89:4471–4475
  46. Schrem H, Klempnauer J, Borlak J. Liver-enriched transcription factors in liver function and development: Part II. The C/EBPs and D site-binding protein in cell cycle control, carcinogenesis, circadian gene regulation, liver regeneration, apoptosis, and liver-specific gene regulation. Pharmacol Rev. 2004;56:291–330

PII: S0955-2863(08)00180-0

doi: 10.1016/j.jnutbio.2008.08.003

The Journal of Nutritional Biochemistry
Volume 20, Issue 11 , Pages 882-893 , November 2009