Skip to main content
×
Home
    • Aa
    • Aa

Absorption and metabolism of olive oil secoiridoids in the small intestine

  • Joana Pinto (a1) (a2), Fátima Paiva-Martins (a1), Giulia Corona (a2), Edward S. Debnam (a3), Maria Jose Oruna-Concha (a2), David Vauzour (a2), Michael H. Gordon (a2) and Jeremy P. E. Spencer (a2)...
Abstract

The secoiridoids 3,4-dihydroxyphenylethanol-elenolic acid (3,4-DHPEA-EA) and 3,4-dihydroxyphenylethanol-elenolic acid dialdehyde (3,4-DHPEA-EDA) account for approximately 55 % of the phenolic content of olive oil and may be partly responsible for its reported human health benefits. We have investigated the absorption and metabolism of these secoiridoids in the upper gastrointestinal tract. Both 3,4-DHPEA-EDA and 3,4-DHPEA-EA were relatively stable under gastric conditions, only undergoing limited hydrolysis. Both secoiridoids were transferred across a human cellular model of the small intestine (Caco-2 cells). However, no glucuronide conjugation was observed for either secoiridoid during transfer, although some hydroxytyrosol and homovanillic alcohol were formed. As Caco-2 cells are known to express only limited metabolic activity, we also investigated the absorption and metabolism of secoiridoids in isolated, perfused segments of the jejunum and ileum. Here, both secoiridoids underwent extensive metabolism, most notably a two-electron reduction and glucuronidation during the transfer across both the ileum and jejunum. Unlike Caco-2 cells, the intact small-intestinal segments contain NADPH-dependent aldo-keto reductases, which reduce the aldehyde carbonyl group of 3,4-DHPEA-EA and one of the two aldeydic carbonyl groups present on 3,4-DHPEA-EDA. These reduced forms are then glucuronidated and represent the major in vivo small-intestinal metabolites of the secoiridoids. In agreement with the cell studies, perfusion of the jejunum and ileum also yielded hydroxytyrosol and homovanillic alcohol and their respective glucuronides. We suggest that the reduced and glucuronidated forms represent novel physiological metabolites of the secoiridoids that should be pursued in vivo and investigated for their biological activity.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Absorption and metabolism of olive oil secoiridoids in the small intestine
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about sending content to Dropbox.

      Absorption and metabolism of olive oil secoiridoids in the small intestine
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about sending content to Google Drive.

      Absorption and metabolism of olive oil secoiridoids in the small intestine
      Available formats
      ×
Copyright
Corresponding author
*Corresponding author: Dr J. P. E. Spencer, email j.p.e.spencer@rdg.ac.uk
References
Hide All
1 Sofi F, Abbate R, Gensini GF, et al. (2010) Accruing evidence about benefits of adherence to the Mediterranean diet on health: an updated systematic review and meta-analysis. Am J Clin Nutr 92, 11891196.
2 Braga C, La Vecchia C, Franceschi S, et al. (1998) Olive oil, other seasoning fats, and the risk of colorectal carcinoma. Cancer 82, 448453.
3 Keys A (1995) Mediterranean diet and public health: personal reflections. Am J Clin Nutr 61, 1321S1323S.
4 Lopez-Miranda J, Perez-Jimenez F, Ros E, et al. (2010) Olive oil and health: summary of the II international conference on olive oil and health consensus report, Jaen and Cordoba (Spain) 2008. Nutr Metab Cardiovasc Dis 20, 284294.
5 Owen RW, Giacosa A, Hull WE, et al. (2000) The antioxidant/anticancer potential of phenolic compounds isolated from olive oil. Eur J Cancer 36, 12351247.
6 Owen RW, Haubner R, Wurtele G, et al. (2004) Olives and olive oil in cancer prevention. Eur J Cancer Prev 13, 319326.
7 Montedoro G, Servili M, Baldioli M, et al. (1993) Simple and hydrolyzable phenolic compounds in virgin olive oil. 3. Spectroscopic Characterizations of the Secoiridoid Derivatives. J Agric Food Chem 41, 22282234.
8 Brenes M, Garcia A, Garcia P, et al. (2001) Acid hydrolysis of secoiridoid aglycons during storage of virgin olive oil. J Agric Food Chem 49, 56095614.
9 Garcia A, Brenes M, Martinez F, et al. (2001) High-performance liquid chromatography evaluation of phenols in virgin olive oil during extraction at laboratory and industrial scale. J Am Oil Chem Soc 78, 625629.
10 Tovar MJ, Motilva MJ & Romero MP (2001) Changes in the phenolic composition of virgin olive oil from young trees (Olea europaea L. cv. Arbequina) grown under linear irrigation strategies. J Agric Food Chem 49, 55025508.
11 Paiva-Martins F, Fernandes J, Rocha S, et al. (2009) Effects of olive oil polyphenols on erythrocyte oxidative damage. Mol Nutr Food Res 53, 609616.
12 Paiva-Martins F, Fernandes J, Santos V, et al. (2010) Powerful protective role of 3,4-dihydroxyphenylethanol-elenolic acid dialdehyde against erythrocyte oxidative-induced hemolysis. J Agric Food Chem 58, 135140.
13 Fabiani R, Rosignoli P, De Bartolomeo A, et al. (2008) Oxidative DNA damage is prevented by extracts of olive oil, hydroxytyrosol, and other olive phenolic compounds in human blood mononuclear cells and HL60 cells. J Nutr 138, 14111416.
14 Garcia-Villalba R, Carrasco-Pancorbo A, Oliveras-Ferraros C, et al. (3000) Characterization and quantification of phenolic compounds of extra-virgin olive oils with anticancer properties by a rapid and resolutive LC-ESI-TOF MS method. J Pharm Biomed Anal 51, 416429.
15 Menendez JA, Vazquez-Martin A, Garcia-Villalba R, et al. (2008) tabAnti-HER2 (erbB-2) oncogene effects of phenolic compounds directly isolated from commercial extra-virgin olive oil (EVOO). BMC Cancer 8, 377.
16 Menendez JA, Vazquez-Martin A, Oliveras-Ferraros C, et al. (2009) Extra-virgin olive oil polyphenols inhibit HER2 (erbB-2)-induced malignant transformation in human breast epithelial cells: relationship between the chemical structures of extra-virgin olive oil secoiridoids and lignans and their inhibitory activities on the tyrosine kinase activity of HER2. Int J Oncol 34, 4351.
17 D'Angelo S, Manna C, Migliardi V, et al. (2001) Pharmacokinetics and metabolism of hydroxytyrosol, a natural antioxidant from olive oil. Drug Metab Dispos 29, 14921498.
18 Miro-Casas E, Covas MI, Farre M, et al. (2003) Hydroxytyrosol disposition in humans. Clin Chem 49, 945952.
19 Miro-Casas E, Covas MI, Fito M, et al. (2003) Tyrosol and hydroxytyrosol are absorbed from moderate and sustained doses of virgin olive oil in humans. Eur J Clin Nutr 57, 186190.
20 Visioli F, Galli C, Bornet F, et al. (2000) Olive oil phenolics are dose-dependently absorbed in humans. FEBS Lett 468, 159160.
21 Vissers MN, Zock PL, Roodenburg AJ, et al. (2002) Olive oil phenols are absorbed in humans. J Nutr 132, 409417.
22 Weinbrenner T, Fito M, Farre Albaladejo M, et al. (2004) Bioavailability of phenolic compounds from olive oil and oxidative/antioxidant status at postprandial state in healthy humans. Drugs Exp Clin Res 30, 207212.
23 Corona G, Tzounis X, Assunta Dessi M, et al. (2006) The fate of olive oil polyphenols in the gastrointestinal tract: implications of gastric and colonic microflora-dependent biotransformation. Free Radic Res 40, 647658.
24 Manna C, Galletti P, Maisto G, et al. (2000) Transport mechanism and metabolism of olive oil hydroxytyrosol in Caco-2 cells. FEBS Lett 470, 341344.
25 Tuck KL, Freeman MP, Hayball PJ, et al. (2001) The in vivo fate of hydroxytyrosol and tyrosol, antioxidant phenolic constituents of olive oil, after intravenous and oral dosing of labeled compounds to rats. J Nutr 131, 19931996.
26 Lipinski CA, Lombardo F, Dominy BW, et al. (1997) Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 23, 325.
27 Paiva-Martins F, Gordon MH & Gameiro P (2003) Activity and location of olive oil phenolic antioxidants in liposomes. Chem Phys Lipids 124, 2336.
28 Limiroli R, Consonni R, Ottolina G, et al. (1995) 1H NMR and 13C NMR characterization of new oleuropein aglycones. J Chem Soc Perkin Trans 1, 15191523.
29 Paiva-Martins F & Gordon MH (2001) Isolation and characterization of the antioxidant component 3,4-dihydroxyphenylethyl 4-formyl-3-formylmethyl-4-hexenoate from olive (Olea europaea) leaves. J Agric Food Chem 49, 42144219.
30 Fisher RB & Gardner ML (1974) A kinetic approach to the study of absorption of solutes by isolated perfused small intestine. J Physiol 241, 211234.
31 Spencer JP, Chowrimootoo G, Choudhury R, et al. (1999) The small intestine can both absorb and glucuronidate luminal flavonoids. FEBS Lett 458, 224230.
32 Paiva-Martins F & Gordon MH (2005) Interactions of ferric ions with olive oil phenolic compounds. J Agric Food Chem 53, 27042709.
33 Lenaerts K, Bouwman FG, Lamers WH, et al. (2007) Comparative proteomic analysis of cell lines and scrapings of the human intestinal epithelium. BMC Genomics 8, 91.
34 Meunier V, Bourrie M, Berger Y, et al. (1995) The human intestinal epithelial cell line Caco-2; pharmacological and pharmacokinetic applications. Cell Biol Toxicol 11, 187194.
35 Fisher MB, Paine MF, Strelevitz TJ, et al. (2001) The role of hepatic and extrahepatic UDP-glucuronosyltransferases in human drug metabolism. Drug Metab Rev 33, 273297.
36 Gregory PA, Lewinsky RH, Gardner-Stephen DA, et al. (2004) Regulation of UDP glucuronosyltransferases in the gastrointestinal tract. Toxicol Appl Pharmacol 199, 354363.
37 Walgren RA, Karnaky KJ Jr, Lindenmayer GE, et al. (2000) Efflux of dietary flavonoid quercetin 4′-beta-glucoside across human intestinal Caco-2 cell monolayers by apical multidrug resistance-associated protein-2. J Pharmacol Exp Ther 294, 830836.
38 Walgren RA, Lin JT, Kinne RK, et al. (2000) Cellular uptake of dietary flavonoid quercetin 4′-beta-glucoside by sodium-dependent glucose transporter SGLT1. J Pharmacol Exp Ther 294, 837843.
39 Walgren RA, Walle UK & Walle T (1998) Transport of quercetin and its glucosides across human intestinal epithelial Caco-2 cells. Biochem Pharmacol 55, 17211727.
40 Poquet L, Clifford MN & Williamson G (2008) Investigation of the metabolic fate of dihydrocaffeic acid. Biochem Pharmacol 75, 12181229.
41 Jez JM, Bennett MJ, Schlegel BP, et al. (1997) Comparative anatomy of the aldo-keto reductase superfamily. Biochem J 326, (Pt 3), 625636.
42 Crosas B, Hyndman DJ, Gallego O, et al. (2003) Human aldose reductase and human small intestine aldose reductase are efficient retinal reductases: consequences for retinoid metabolism. Biochem J 373, 973979.
43 Suarez M, Romero MP, Macia A, et al. (2009) Improved method for identifying and quantifying olive oil phenolic compounds and their metabolites in human plasma by microelution solid-phase extraction plate and liquid chromatography–tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 877, 40974106.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 12
Total number of PDF views: 103 *
Loading metrics...

Abstract views

Total abstract views: 231 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 20th October 2017. This data will be updated every 24 hours.