AGE

, Volume 34, Issue 2, pp 341–358

Dietary oil modifies the plasma proteome during aging in the rat

  • Mónica Santos-González
  • José López-Miranda
  • Francisco Pérez-Jiménez
  • Plácido Navas
  • José M. Villalba
Article

Abstract

Fatty acids and other components of the diet may modulate, among others, mechanisms involved in homeostasis, aging, and age-related diseases. Using a proteomic approach, we have studied how dietary oil affected plasma proteins in young (6 months) or old (24 months) rats fed lifelong with two experimental diets enriched in either sunflower or virgin olive oil. After the depletion of the most abundant proteins, levels of less abundant proteins were studied using two-dimensional electrophoresis and mass spectrometry. Our results showed that compared with the sunflower oil diet, the virgin olive oil diet induced significant decreases of plasma levels of acute phase proteins such as inter-alpha inhibitor H4P heavy chain (at 6 months), hemopexin precursor (at 6 and 24 months), preprohaptoglobin precursor (at 6 and 24 months), and α-2-HS glycoprotein (at 6 and 24 months); antioxidant proteins such as type II peroxiredoxin (at 24 months); proteins related with coagulation such as fibrinogen γ-chain precursor (at 24 months), T-kininogen 1 precursor (at 6 and 24 months), and apolipoprotein H (at 6 and 24 months); or with lipid metabolism and transport such as apolipoprotein E (at 6 and 24 months) and apolipoprotein A-IV (at 24 months). The same diet increased the levels of apolipoprotein A-1 (at 6 and 24 months), diminishing in general the changes that occurred with age. Our unbiased analysis reinforces the beneficial role of a diet rich in virgin olive oil compared with a diet rich in sunflower oil, modulating inflammation, homeostasis, oxidative stress, and cardiovascular risk during aging.

Keywords

Fatty acids Olive oil Plasma proteome Rat Sunflower oil 

References

  1. Anderson L (2005) Candidate-based proteomics in the search for biomarkers of cardiovascular disease. J Physiol 563:23–60PubMedCrossRefGoogle Scholar
  2. Asakura S, Hurley RW, Skorstengaard K, Ohkubo I, Mosher DF (1992) Inhibition of cell adhesion by high molecular weight kininogen. J Cell Biol 116:465–476PubMedCrossRefGoogle Scholar
  3. Babio N, Bullo M, Salas-Salvado J (2009) Mediterranean diet and metabolic syndrome: the evidence. Public Health Nutr 12:1607–1617PubMedCrossRefGoogle Scholar
  4. Bello RI, Alcaín FJ, Gómez-Díaz C, López-Lluch G, Navas P, Villalba JM (2003) Hydrogen peroxide- and cell-density-regulated expression of NADH-cytochrome b 5 reductase in HeLa cells. J Bioenerg Biomembr 35:169–179PubMedCrossRefGoogle Scholar
  5. Bello RI, Gómez-Díaz C, Burón MI, Navas P, Villalba JM (2006) Differential regulation of hepatic apoptotic pathways by dietary olive and sunflower oils in the aging rat. Exp Gerontol 41:1174–1184PubMedCrossRefGoogle Scholar
  6. Binkert C, Demetriou M, Sukhu B, Szweras M, Tenenbaum HC, Dennis JW (1999) Regulation of osteogenesis by fetuin. J Biol Chem 274:28514–28520PubMedCrossRefGoogle Scholar
  7. Calder PC (2009) Polyunsaturated fatty acids and inflammatory processes: new twists in an old tale. Biochimie 91:791–795PubMedCrossRefGoogle Scholar
  8. Chan CD, Watts GF (2006) Apolipoproteins as markers and managers of coronary risk. QJM 99:277–287PubMedCrossRefGoogle Scholar
  9. Chavakis T, Boeckel N, Santoso S, Voss R, Isordia-Salas I, Pixley RA, Morgenstern E, Colman RW, Preissner KT (2002) Inhibition of platelet adhesion and aggregation by a defined region (Gly-486-Lys-502) of high molecular weight kininogen. J Biol Chem 277:23157–23164PubMedCrossRefGoogle Scholar
  10. Chlebovska K, Chlebovsky O (1999) Favourable effect of K, Mg aspartate on serum proteins in aging rats. Mech Ageing Dev 108:127–138PubMedCrossRefGoogle Scholar
  11. Colman RW, Schmaier AH (1997) Contact system: a vascular biology modulator with anticoagulant, profibrinolytic, antiadhesive, and proinflammatory attributes. Blood 90:3819–3843PubMedGoogle Scholar
  12. Cooke NE (1986) Rat vitamin D binding protein. Determination of the full-length primary structure from cloned cDNA. J Biol Chem 261:3441–3450PubMedGoogle Scholar
  13. Daimon M, Oizumi T, Karasawa S, Kaino W, Takase K, Tada K, Jimbu Y, Wada K, Kameda W, Susa S, Muramatsu M, Kubota I, Kawata S, Kato T (2011) Association of the clusterin gene polymorphisms with type 2 diabetes mellitus. Metabolism PMID: 20850846 (in press)Google Scholar
  14. Danesh J, Lewington S, Thompson SG, Lowe GD, Collins R, Kostis JB, Wilson AC, Folsom AR, Wu K, Benderly M, Goldbourt U, Willeit J, Kiechl S, Yarnell JW, Sweetnam PM, Elwood PC, Cushman M, Psaty BM, Tracy RP, Tybjaerg-Hansen A, Haverkate F, de Maat MP, Fowkes FG, Lee AJ, Smith FB, Salomaa V, Harald K, Rasi R, Vahtera E, Jousilahti P, Pekkanen J, D'Agostino R, Kannel WB, Wilson PW, Tofler G, Arocha-Pinango CL, Rodriguez-Larralde A, Nagy E, Mijares M, Espinosa R, Rodriquez-Roa E, Ryder E, Diez-Ewald MP, Campos G, Fernandez V, Torres E, Marchioli R, Valagussa F, Rosengren A, Wilhelmsen L, Lappas G, Eriksson H, Cremer P, Nagel D, Curb JD, Rodriguez B, Yano K, Salonen JT, Nyyssonen K, Tuomainen TP, Hedblad B, Lind P, Loewel H, Koenig W, Meade TW, Cooper JA, De Stavola B, Knottenbelt C, Miller GJ, Cooper JA, Bauer KA, Rosenberg RD, Sato S, Kitamura A, Naito Y, Palosuo T, Ducimetiere P, Amouyel P, Arveiler D, Evans AE, Ferrieres J, Juhan-Vague I, Bingham A, Schulte H, Assmann G, Cantin B, Lamarche B, Despres JP, Dagenais GR, Tunstall-Pedoe H, Woodward M, Ben-Shlomo Y, Davey Smith G, Palmieri V, Yeh JL, Rudnicka A, Ridker P, Rodeghiero F, Tosetto A, Shepherd J, Ford I, Robertson M, Brunner E, Shipley M, Feskens EJ, Kromhout D, Dickinson A, Ireland B, Juzwishin K, Kaptoge S, Lewington S, Memon A, Sarwar N, Walker M, Wheeler J, White I, Wood A (2005) Plasma fibrinogen level and the risk of major cardiovascular diseases and nonvascular mortality: an individual participant meta-analysis. JAMA 294:1799–1809PubMedCrossRefGoogle Scholar
  15. Daveau M, Jean L, Soury E, Olivier E, Masson S, Lyoumi S, Chan P, Hiron M, Lebreton JP, Husson A, Jegou S, Vaudry H, Salier JP (1998) Hepatic and extra-hepatic transcription of inter-alpha-inhibitor family genes under normal or acute inflammatory conditions in rat. Arch Biochem Biophys 350:315–323PubMedCrossRefGoogle Scholar
  16. Duverger N, Kruth H, Emmanuel F, Caillaud JM, Viglietta C, Castro G, Tailleux A, Fievet C, Fruchart JC, Houdebine LM, Denefle P (1996a) Inhibition of atherosclerosis development in cholesterol-fed human apolipoprotein A-I-transgenic rabbits. Circulation 94:713–717PubMedGoogle Scholar
  17. Duverger N, Tremp G, Caillaud JM, Emmanuel F, Castro G, Fruchart JC, Steinmetz A, Denefle P (1996b) Protection against atherogenesis in mice mediated by human apolipoprotein A-IV. Science 273:966–968PubMedCrossRefGoogle Scholar
  18. Echan LA, Tang HY, Ali-Khan N, Lee K, Speicher DW (2005) Depletion of multiple high-abundance proteins improves protein profiling capacities of human serum and plasma. Proteomics 5:3292–3303PubMedCrossRefGoogle Scholar
  19. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247PubMedCrossRefGoogle Scholar
  20. French LE, Chonn A, Ducrest D, Baumann B, Belin D, Wohlwend A, Kiss JZ, Sappino AP, Tschopp J, Schifferli JA (1993) Murine clusterin: molecular cloning and mRNA localization of a gene associated with epithelial differentiation processes during embryogenesis. J Cell Biol 122:1119–1130PubMedCrossRefGoogle Scholar
  21. Gomaraschi M, Putt WE, Pozzi S, Iametti S, Barbiroli A, Bonomi F, Favari E, Bernini F, Franceschini G, Talmud PJ, Calabresi L (2010) Structure and function of the apoA-IV T347S and Q360H common variants. Biochem Biophys Res Commun 393:126–130PubMedCrossRefGoogle Scholar
  22. Haddad JG (1995) Plasma vitamin D-binding protein (Gc-globulin): multiple tasks. J Steroid Biochem Mol Biol 53:579–582PubMedCrossRefGoogle Scholar
  23. Hanley JM, Haugen TH, Heath EC (1983) Biosynthesis and processing of rat haptoglobin. J Biol Chem 258:7858–7869PubMedGoogle Scholar
  24. Ix JH, Shlipak MG, Brandenburg VM, Ali S, Ketteler M, Whooley MA (2006) Association between human fetuin-A and the metabolic syndrome: data from the Heart and Soul Study. Circulation 113:1760–1767PubMedCrossRefGoogle Scholar
  25. Jenne DE, Lowin B, Peitsch MC, Bottcher A, Schmitz G, Tschopp J (1991) Clusterin (complement lysis inhibitor) forms a high density lipoprotein complex with apolipoprotein A-I in human plasma. J Biol Chem 266:11030–11036PubMedGoogle Scholar
  26. Jiménez-Gémez Y, López-Miranda J, Blanco-Colio LM, Marín C, Pérez-Martínez P, Ruano J, Paniagua JA, Rodríguez F, Egido J, Pérez-Jiménez F (2009) Olive oil and walnut breakfasts reduce the postprandial inflammatory response in mononuclear cells compared with a butter breakfast in healthy men. Atherosclerosis 204:e70–e76CrossRefGoogle Scholar
  27. Kim JW, No JK, Ikeno Y, Yu BP, Choi JS, Yokozawa T, Chung HY (2002) Age-related changes in redox status of rat serum. Arch Gerontol Geriatr 34:9–17PubMedCrossRefGoogle Scholar
  28. Kirkwood TB, Austad SN (2000) Why do we age? Nature 408:233–238PubMedCrossRefGoogle Scholar
  29. Kordula T, Travis J (1995) Activation of the rat serine proteinase inhibitor 3 gene by interferon gamma via the interleukin 6-responsive element. Biochem J 309:63–67PubMedGoogle Scholar
  30. Kruskal JB, Commerford PJ, Franks JJ, Kirsch RE (1987) Fibrin and fibrinogen-related antigens in patients with stable and unstable coronary artery disease. New Engl J Med 317:1361–1365PubMedCrossRefGoogle Scholar
  31. Lebreton JP, Joisel F, Raoult JP, Lannuzel B, Rogez JP, Humbert G (1979) Serum concentration of human alpha 2 HS glycoprotein during the inflammatory process: evidence that alpha 2 HS glycoprotein is a negative acute-phase reactant. J Clin Invest 64:1118–1129PubMedCrossRefGoogle Scholar
  32. Lovely RS, Kazmierczak SC, Massaro JM, D'Agostino RB Sr, O'Donnell CJ, Farrell DH (2010) Gamma' fibrinogen: evaluation of a new assay for study of associations with cardiovascular disease. Clin Chem 56:781–788PubMedCrossRefGoogle Scholar
  33. Mahley RW, Rall SC Jr (2000) Apolipoprotein E: far more than a lipid transport protein. Annu Rev Genomics Hum Genet 1:507–537PubMedCrossRefGoogle Scholar
  34. Martinez-Pinna R, Barbas C, Blanco-Colio LM, Tunon J, Ramos-Mozo P, Lopez JA, Meilhac O, Michel JB, Egido J, Martin-Ventura JL (2010) Proteomic and metabolomic profiles in atherothrombotic vascular disease. Curr Atheroscl Rep 12:202–208CrossRefGoogle Scholar
  35. Mataix J (ed) (2002) Lípidos, vol I. Nutrición y alimentación humana. Ergon, MadridGoogle Scholar
  36. Materljan E, Materljan M, Materljan B, Vlacic H, Baricev-Novakovic Z, Sepcic J (2009) Multiple sclerosis and cancers in Croatia—a possible protective role of the “Mediterranean diet”. Coll Antropol 33:539–545PubMedGoogle Scholar
  37. Matsuura E, Kobayashi K, Tabuchi M, Lopez LR (2006) Oxidative modification of low-density lipoprotein and immune regulation of atherosclerosis. Prog Lipid Res 45:466–486PubMedCrossRefGoogle Scholar
  38. Melamed-Frank M, Lache O, Enav BI, Szafranek T, Levy NS, Ricklis RM, Levy AP (2001) Structure–function analysis of the antioxidant properties of haptoglobin. Blood 98:3693–3698PubMedCrossRefGoogle Scholar
  39. Meydani M (2001) Nutrition interventions in aging and age-associated disease. Ann NY Acad Sci 928:226–235PubMedCrossRefGoogle Scholar
  40. Miyakis S, Giannakopoulos B, Krilis SA (2004) Beta 2 glycoprotein I—function in health and disease. Thromb Res 114:335–346PubMedCrossRefGoogle Scholar
  41. Miyata M, Biro S, Kaieda H, Eto H, Orihara K, Kihara T, Obata H, Matsushita N, Matsuyama T, Tei C (2001) Apolipoprotein J/clusterin is induced in vascular smooth muscle cells after vascular injury. Circulation 104:1407–1412PubMedCrossRefGoogle Scholar
  42. Muller-Eberhard HJ, Schreiber RD (1980) Molecular biology and chemistry of the alternative pathway of complement. Adv Immunol 29:1–53PubMedCrossRefGoogle Scholar
  43. Ostos MA, Conconi M, Vergnes L, Baroukh N, Ribalta J, Girona J, Caillaud JM, Ochoa A, Zakin MM (2001) Antioxidative and antiatherosclerotic effects of human apolipoprotein A-IV in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 21:1023–1028PubMedCrossRefGoogle Scholar
  44. Owen RW, Giacosa A, Hull WE, Haubner R, Wurtele G, Spiegelhalder B, Bartsch H (2000) Olive-oil consumption and health: the possible role of antioxidants. Lancet Oncol 1:107–112PubMedCrossRefGoogle Scholar
  45. Pérez-Jiménez F, Ruano J, Pérez-Martínez P, López-Segura F, López-Miranda J (2007) The influence of olive oil on human health: not a question of fat alone. Mol Nutr Food Res 51:1199–1208PubMedCrossRefGoogle Scholar
  46. Perona JS, Cabello-Moruno R, Ruíz-Gutiérrez V (2006) The role of virgin olive oil components in the modulation of endothelial function. J Nutr Biochem 17:429–445PubMedCrossRefGoogle Scholar
  47. Price PA, Williamson MK, Nguyen TM, Than TN (2004) Serum levels of the fetuin–mineral complex correlate with artery calcification in the rat. J Biol Chem 279:1594–1600PubMedCrossRefGoogle Scholar
  48. Quiles JL, Pamplona R, Ramirez-Tortosa MC, Naudi A, Portero-Otin M, Araujo-Nepomuceno E, Lopez-Frias M, Battino M, Ochoa JJ (2010) Coenzyme Q addition to an n-6 PUFA-rich diet resembles benefits on age-related mitochondrial DNA deletion and oxidative stress of a MUFA-rich diet in rat heart. Mech Ageing Dev 131:38–47PubMedCrossRefGoogle Scholar
  49. Rosenberg ME, Silkensen J (1995) Clusterin: physiologic and pathophysiologic considerations. Int J Biochem Cell Biol 27:633–645PubMedCrossRefGoogle Scholar
  50. Sandford AJ, Chagani T, Spinelli JJ, Pare PD (1999) alpha1-Antitrypsin genotypes and the acute-phase response to open heart surgery. Am J Respir Crit Care Med 159:1624–1628PubMedGoogle Scholar
  51. Santos-González M, Gómez Díaz C, Navas P, Villalba JM (2007) Modifications of plasma proteome in long-lived rats fed on a coenzyme Q10-supplemented diet. Exp Gerontol 42:798–806PubMedCrossRefGoogle Scholar
  52. Schroeder F, Petrescu AD, Huang H, Atshaves BP, McIntosh AL, Martin GG, Hostetler HA, Vespa A, Landrock D, Landrock KK, Payne HR, Kier AB (2008) Role of fatty acid binding proteins and long chain fatty acids in modulating nuclear receptors and gene transcription. Lipids 43:1–17PubMedCrossRefGoogle Scholar
  53. Silkensen JR, Schwochau GB, Rosenberg ME (1994) The role of clusterin in tissue injury. Biochem Cell Biol 72:483–488PubMedCrossRefGoogle Scholar
  54. Srinivas PR, Wagner AS, Reddy LV, Deutsch DD, Leon MA, Goustin AS, Grunberger G (1993) Serum alpha 2-HS-glycoprotein is an inhibitor of the human insulin receptor at the tyrosine kinase level. Mol Endocrinol 7:1445–1455PubMedCrossRefGoogle Scholar
  55. Stoscheck CM (1990) Quantitation of protein. Methods Enzymol 182:50–68PubMedCrossRefGoogle Scholar
  56. Sueyoshi T, Enjyoji K, Shimada T, Kato H, Iwanaga S, Bando Y, Kominami E, Katunuma N (1985) A new function of kininogens as thiol-proteinase inhibitors: inhibition of papain and cathepsins B, H and L by bovine, rat and human plasma kininogens. FEBS Lett 182:193–195PubMedCrossRefGoogle Scholar
  57. Thambisetty M, Simmons A, Velayudhan L, Hye A, Campbell J, Zhang Y, Wahlund LO, Westman E, Kinsey A, Guntert A, Proitsi P, Powell J, Causevic M, Killick R, Lunnon K, Lynham S, Broadstock M, Choudhry F, Howlett DR, Williams RJ, Sharp SI, Mitchelmore C, Tunnard C, Leung R, Foy C, O'Brien D, Breen G, Furney SJ, Ward M, Kloszewska I, Mecocci P, Soininen H, Tsolaki M, Vellas B, Hodges A, Murphy DG, Parkins S, Richardson JC, Resnick SM, Ferrucci L, Wong DF, Zhou Y, Muehlboeck S, Evans A, Francis PT, Spenger C, Lovestone S (2010) Association of plasma clusterin concentration with severity, pathology, and progression in Alzheimer disease. Arch Gen Psychiatry 67:739–748PubMedCrossRefGoogle Scholar
  58. Tolle A, Schlame M, Charlier N, Guthmann F, Rustow B (2005) Vitamin E differentially regulates the expression of peroxiredoxin-1 and -6 in alveolar type II cells. Free Radic Biol Med 38:1401–1408PubMedCrossRefGoogle Scholar
  59. Tolosano E, Hirsch E, Patrucco E, Camaschella C, Navone R, Silengo L, Altruda F (1999) Defective recovery and severe renal damage after acute hemolysis in hemopexin-deficient mice. Blood 94:3906–3914PubMedGoogle Scholar
  60. Tolosano E, Fagoonee S, Hirsch E, Berger FG, Baumann H, Silengo L, Altruda F (2002) Enhanced splenomegaly and severe liver inflammation in haptoglobin/hemopexin double-null mice after acute hemolysis. Blood 100:4201–4208PubMedCrossRefGoogle Scholar
  61. Torres C, Li M, Walter R, Sierra F (2001) T-kininogen inhibits fibroblast proliferation in the G(1) phase of the cell cycle. Exp Cell Res 269:171–179PubMedCrossRefGoogle Scholar
  62. Triffitt JT (1976) Plasma proteins present in human cortical bone: enrichment of the alpha2HS-glycoprotein. Calcif Tissue Res 22:27–33PubMedGoogle Scholar
  63. Trougakos IP, Gonos ES (2002) Clusterin/apolipoprotein J in human aging and cancer. Int J Biochem Cell Biol 34:1430–1448PubMedCrossRefGoogle Scholar
  64. Trougakos IP, Gonos ES (2004) Functional analysis of clusterin/apolipoprotein J in cellular death induced by severe genotoxic stress. Ann NY Acad Sci 1019:206–210PubMedCrossRefGoogle Scholar
  65. Trougakos IP, Stathatos M, Chalikia A, Melidonis A, Gonos ES (2002) Serum levels of the senescence biomarker clusterin/apolipoprotein J increase significantly in diabetes type II and during development of coronary heart disease or at myocardial infarction. Exp Gerontol 37:1175–1187PubMedCrossRefGoogle Scholar
  66. Vanschoonbeek K, Feijge MA, Paquay M, Rosing J, Saris W, Kluft C, Giesen PL, de Maat MP, Heemskerk JW (2004) Variable hypocoagulant effect of fish oil intake in humans: modulation of fibrinogen level and thrombin generation. Arterioscler Thromb Vasc Biol 24:1734–1740PubMedCrossRefGoogle Scholar
  67. Visioli F, Poli A, Gall C (2002) Antioxidant and other biological activities of phenols from olives and olive oil. Med Res Rev 22:65–75PubMedCrossRefGoogle Scholar
  68. Walter R, Murasko DM, Sierra F (1998) T-kininogen is a biomarker of senescence in rats. Mech Ageing Dev 106:129–144PubMedCrossRefGoogle Scholar
  69. Waterman E, Lockwood B (2007) Active components and clinical applications of olive oil. Altern Med Rev 12:331–342PubMedGoogle Scholar
  70. Wong CM, Siu KL, Jin DY (2004) Peroxiredoxin-null yeast cells are hypersensitive to oxidative stress and are genomically unstable. J Biol Chem 279:23207–23213PubMedCrossRefGoogle Scholar
  71. Yasuda S, Atsumi T, Ieko M, Matsuura E, Kobayashi K, Inagaki J, Kato H, Tanaka H, Yamakado M, Akino M, Saitou H, Amasaki Y, Jodo S, Amengual O, Koike T (2004) Nicked beta2-glycoprotein I: a marker of cerebral infarct and a novel role in the negative feedback pathway of extrinsic fibrinolysis. Blood 103:3766–3772PubMedCrossRefGoogle Scholar
  72. Yoshida Y, Takahashi Y, Yoshikawa T, Nonomura A, Yoshioka A (2006) Suppressive effect of alpha2 Heremans–Schmid glycoprotein on in vitro calcification of osteogenesis. Pediatr Int 48:11–16PubMedCrossRefGoogle Scholar

Copyright information

© American Aging Association 2011

Authors and Affiliations

  • Mónica Santos-González
    • 1
  • José López-Miranda
    • 2
    • 3
  • Francisco Pérez-Jiménez
    • 2
    • 3
  • Plácido Navas
    • 4
    • 5
  • José M. Villalba
    • 1
  1. 1.Departamento de Biología Celular, Fisiología e InmunologíaUniversity of CórdobaCórdobaSpain
  2. 2.Lipid and Atherosclerosis UnitIMIBIC/Reina Sofía University Hospital, University of CórdobaCórdobaSpain
  3. 3.CIBER Fisiopatología Obesidad y Nutrición (CIBEROBN)Instituto de Salud Carlos IIICórdobaSpain
  4. 4.Centro Andaluz de Biología del Desarrollo (CABD)University Pablo de Olavide-CSICSevilleSpain
  5. 5.CIBER Enfermedades Raras (CIBERER)Instituto de Salud Carlos IIISevillaSpain

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