Skip to main content

Advertisement

Log in

Phytochemical uptake following human consumption of Montmorency tart cherry (L. Prunus cerasus) and influence of phenolic acids on vascular smooth muscle cells in vitro

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

To investigate the phytochemical uptake following human consumption of Montmorency tart cherry (L. Prunus cerasus) and influence of selected phenolic acids on vascular smooth muscle cells in vitro.

Methods

In a randomised, double-blinded, crossover design, 12 healthy males consumed either 30 or 60 mL of Montmorency tart cherry concentrate. Following analysis of the juice composition, venous blood samples were taken before and 1, 2, 3, 5 and 8 h post-consumption of the beverage. In addition to examining some aspects of the concentrate contents, plasma concentrations of protocatechuic acid (PCA), vanillic acid (VA) and chlorogenic (CHL) acid were analysed by reversed-phase high-performance liquid chromatography (HPLC) with diode array for quantitation and mass spectrometry detection (LCMS) for qualitative purposes. Vascular smooth muscle cell migration and proliferation were also assessed in vitro.

Results

Both the 30 and 60 mL doses of Montmorency cherry concentrate contained high amounts of total phenolics (71.37 ± 0.11; 142.73 ± 0.22 mg/L) and total anthocyanins (62.47 ± 0.31; 31.24 ± 0.16 mg/L), as well as large quantities of CHL (0.205 ± 0.24; 0.410 ± 0.48 mg/L) and VA (0.253 ± 0.84; 0.506 ± 1.68 mg/L). HPLC/LCMS identified two dihydroxybenzoic acids (PCA and VA) in plasma following MC concentrate consumption. Both compounds were most abundant 1–2 h post-initial ingestion with traces detectable at 8 h post-ingestion. Cell migration was significantly influenced by the combination of PCA and VA, but not in isolation. There was no effect of the compounds on cell proliferation.

Conclusions

These data show new information that phenolic compounds thought to exert vasoactive properties are bioavailable in vivo following MC consumption and subsequently can influence cell behaviour. These data may be useful for the design and interpretation of intervention studies investigating the health effects of Montmorency cherries.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Habauzit V, Morand C (2012) Evidence for a protective effect of polyphenols-containing foods on cardiovascular health: an update for clinicians. Ther Adv Chronic Dis 3(2):87–106. doi:10.1177/2040622311430006

    Article  CAS  Google Scholar 

  2. Arranz S, Chiva-Blanch G, Valderas-Martinez P, Medina-Remon A, Lamuela-Raventos RM, Estruch R (2012) Wine, beer, alcohol and polyphenols on cardiovascular disease and cancer. Nutrients 4(7):759–781. doi:10.3390/nu4070759

    Article  CAS  Google Scholar 

  3. Vinson JA, Su XH, Zubik L, Bose P (2001) Phenol antioxidant quantity and quality in foods: fruits. J Agric Food Chem 49(11):5315–5321. doi:10.1021/jf0009293

    Article  CAS  Google Scholar 

  4. Wang H, Nair MG, Strasburg GM, Chang Y-C, Booren AM, Gray JI, DeWitt DL (1999) Antioxidant and antiinflammatory activities of anthocyanins and their aglycon, cyanidin, from tart cherries. J Nat Prod 62(2):294–296. doi:10.1021/np980501m

    Article  CAS  Google Scholar 

  5. Seeram NP, Momin RA, Nair MG, Bourquin LD (2001) Cyclooxygenase inhibitory and antioxidant cyanidin glycosides in cherries and berries. Phytomedicine 8(5):362–369. doi:10.1078/0944-7113-00053

    Article  CAS  Google Scholar 

  6. Kirakosyan A, Seymour EM, Llanes DEU, Kaufman PB, Bolling SF (2009) Chemical profile and antioxidant capacities of tart cherry products. Food Chem 115(1):20–25. doi:10.1016/j.foodchem.2008.11.042

    Article  CAS  Google Scholar 

  7. Bell PG, McHugh MP, Stevenson E, Howatson G (2013) The role of cherries in exercise and health. Scand J Med Sci Sports. doi:10.1111/sms.12085

    Google Scholar 

  8. Bell PG, Walshe IH, Davison GW, Stevenson E, Howatson G (2014) Montmorency cherries reduce the oxidative stress and inflammatory responses to repeated days high-intensity stochastic cycling. Nutrients 6(2):829–843. doi:10.3390/nu6020829

    Article  Google Scholar 

  9. Howatson G, McHugh MP, Hill JA, Brouner J, Jewell AP, Van Someren KA, Shave RE, Howatson SA (2010) Influence of tart cherry juice on indices of recovery following marathon running. Scand J Med Sci Sports 20(6):843–852. doi:10.1111/j.1600-0838.2009.01005.x

    Article  CAS  Google Scholar 

  10. Pigeon WR, Carr M, Gorman C, Perlis ML (2010) Effects of a tart cherry juice beverage on the sleep of older adults with insomnia: a pilot study. J Med Food 13(3):579–583. doi:10.1089/jmf.2009.0096

    Article  Google Scholar 

  11. Howatson G, Bell PG, Tallent J, Middleton B, McHugh MP, Ellis J (2012) Effect of tart cherry juice (Prunus cerasus) on melatonin levels and enhanced sleep quality. Eur J Nutr 51(8):909–916. doi:10.1007/s00394-011-0263-7

    Article  CAS  Google Scholar 

  12. Bell PG, Gaze DC, Davison GW, George TW, Scotter MJ, Howatson G (2014) Montmorency tart cherry (Prunus cerasus L.) concentrate lowers uric acid, independent of plasma cyanidin-3-O-glucosiderutinoside. J Funct Foods 11:82–90. doi:10.1016/j.jff.2014.09.004

    Article  CAS  Google Scholar 

  13. Seymour EM, Warber SM, Kirakosyan A, Noon KR, Gillespie B, Uhley VE, Wunder J, Urcuyo DE, Kaufman PB, Bolling SF (2014) Anthocyanin pharmacokinetics and dose-dependent plasma antioxidant pharmacodynamics following whole tart cherry intake in healthy humans. J Funct Foods 11:509–516. doi:10.1016/j.jff.2014.08.007

    Article  CAS  Google Scholar 

  14. Lila MA, Raskin I (2005) Health-related interactions of phytochemicals. J Food Sci 70(1):R20–R27

    Article  CAS  Google Scholar 

  15. Patras A, Brunton NP, O’Donnell C, Tiwari BK (2010) Effect of thermal processing on anthocyanin stability in foods; mechanisms and kinetics of degradation. Trends Food Sci Technol 21(1):3–11. doi:10.1016/j.tifs.2009.07.004

    Article  CAS  Google Scholar 

  16. Tomas-Barberan F, Espin JC (2001) Phenolic compounds and related enzymes as determinants of quality in fruits and vegetables. J Sci Food Agric 81(9):853–876. doi:10.1002/jsfa.885

    Article  CAS  Google Scholar 

  17. Vitaglione P, Donnarumma G, Napolitano A, Galvano F, Gallo A, Scalfi L, Fogliano V (2007) Protocatechuic acid is the major human metabolite of cyanidin-glucosides. J Nutr 137(9):2043–2048

    CAS  Google Scholar 

  18. de Ferrars RM, Czank C, Zhang Q, Botting NP, Kroon PA, Cassidy A, Kay CD (2014) The pharmacokinetics of anthocyanins and their metabolites in humans. Br J Pharmacol 171(13):3268–3282. doi:10.1111/bph.12676

    Article  Google Scholar 

  19. Nurmi T, Mursu J, Heinonen M, Nurmi A, Hiltunen R, Voutilainen S (2009) Metabolism of berry anthocyanins to phenolic acids in humans. J Agric Food Chem 57(6):2274–2281. doi:10.1021/jf8035116

    Article  CAS  Google Scholar 

  20. Ross R (1993) The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362(6423):801–809. doi:10.1038/362801a0

    Article  CAS  Google Scholar 

  21. Owens G (1995) Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 75(3):487–517

    CAS  Google Scholar 

  22. Buckow R, Kastell A, Terefe NS, Versteeg C (2010) Pressure and temperature effects on degradation kinetics and storage stability of total anthocyanins in blueberry juice. J Agric Food Chem 58(18):10076–10084. doi:10.1021/jf1015347

    Article  CAS  Google Scholar 

  23. Shahidi F HCT (2007) Antioxidant measurement and applications. In: ACS Symposium Series 956 American Chemical Society, Washington, DC

  24. Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. Lebenson Wiss Technol 28(1):25–30. doi:10.1016/s0023-6438(95)80008-5

    Article  CAS  Google Scholar 

  25. Ou B, Bosak KN, Brickner PR, Iezzoni DG, Seymour EM (2012) Processed tart cherry products-comparative phytochemical content, in vitro antioxidant capacity and in vitro anti-inflammatory activity. J Food Sci 77(5):H105–H112. doi:10.1111/j.1750-3841.2012.02681.x

    Article  CAS  Google Scholar 

  26. Wang HB, Nair MG, Iezzoni AF, Strasburg GM, Booren AM, Gray JI (1997) Quantification and characterization of anthocyanins in Balaton tart cherries. J Agric Food Chem 45(7):2556–2560. doi:10.1021/jf960896k

    Article  CAS  Google Scholar 

  27. Kamat JP, Ghosh A, Devasagayam TPA (2000) Vanillin as an antioxidant in rat liver mitochondria: inhibition of protein oxidation and lipid peroxidation induced by photosensitization. Mol Cell Biochem 209(1–2):47–53. doi:10.1023/a:1007048313556

    Article  CAS  Google Scholar 

  28. Chiang LC, Ng LT, Chiang W, Chang MY, Lin CC (2003) Immunomodulatory activities of flavonoids, monoterpenoids, triterpenoids, iridoid glycosides and phenolic compounds of plantago species. Planta Med 69(7):600–604

    Article  CAS  Google Scholar 

  29. Fang J (2014) Bioavailability of anthocyanins. Drug Metab Rev 46(4):508–520. doi:10.3109/03602532.2014.978080

    Article  CAS  Google Scholar 

  30. Azzini E, Vitaglione P, Intorre F, Napolitano A, Durazzo A, Foddai MS, Fumagalli A, Catasta G, Rossi L, Venneria E, Raguzzini A, Palomba L, Fogliano V, Maiani G (2010) Bioavailability of strawberry antioxidants in human subjects. Br J Nutr 104(8):1165–1173. doi:10.1017/s000711451000187x

    Article  CAS  Google Scholar 

  31. Kirakosyan A, Seymour EM, Wolforth J, McNish R, Kaufman PB, Bolling SF (2015) Tissue bioavailability of anthocyanins from whole tart cherry in healthy rats. Food Chem 171:26–31. doi:10.1016/j.foodchem.2014.08.114

    Article  CAS  Google Scholar 

  32. Kakkar S, Bais S (2014) A review on protocatechuic acid and its pharmacological potential. ISRN Pharmacol 2014:952943. doi:10.1155/2014/952943

    Article  Google Scholar 

  33. Stalmach A, Williamson G, Crozier A (2014) Impact of dose on the bioavailability of coffee chlorogenic acids in humans. Food Funct 5(8):1727–1737. doi:10.1039/c4fo00316k

    Article  CAS  Google Scholar 

  34. Stalmach A, Mullen W, Barron D, Uchida K, Yokota T, Cavin C, Steiling H, Williamson G, Crozier A (2009) Metabolite profiling of hydroxycinnamate derivatives in plasma and urine after the ingestion of coffee by humans: identification of biomarkers of coffee consumption. Drug Metab Dispos 37(8):1749–1758. doi:10.1124/dmd.109.028019

    Article  CAS  Google Scholar 

  35. Azuma K, Ippoushi K, Nakayama M, Ito H, Higashio H, Terao J (2000) Absorption of chlorogenic acid and caffeic acid in rats after oral administration. J Agric Food Chem 48(11):5496–5500. doi:10.1021/jf000483q

    Article  CAS  Google Scholar 

  36. Farah A, Donangelo CM (2006) Phenolic compounds in coffee. Braz J Plant Physiol 18(1):23–36

    Article  CAS  Google Scholar 

  37. Farah A, Monteiro M, Donangelo CM, Lafay S (2008) Chlorogenic acids from green coffee extract are highly bioavailable in humans. J Nutr 138(12):2309–2315. doi:10.3945/jn.108.095554

    Article  CAS  Google Scholar 

  38. Mountzouris KC, Tsirtsikos P, Kalamara E, Nitsch S, Schatzmayr G, Fegeros K (2007) Evaluation of the efficacy of a probiotic containing lactobacillus, bifidobacterium, enterococcus, and pediococcus strains in promoting broiler performance and modulating cecal microflora composition and metabolic activities. Poult Sci 86(2):309–317

    Article  CAS  Google Scholar 

  39. Louis SF, Zahradka P (2010) Vascular smooth muscle cell motility: from migration to invasion. Exp Clin Cardiol 15(4):E75–E85

    CAS  Google Scholar 

  40. Wang H, Liu T-Q, Guan S, Zhu Y-X, Cui Z-F (2008) Protocatechuic acid from Alpinia oxyphylla promotes migration of human adipose tissue-derived stromal cells in vitro. Eur J Pharmacol 599(1–3):24–31. doi:10.1016/j.ejphar.2008.09.030

    Article  CAS  Google Scholar 

  41. Lin H, Chen JH, Chou FP, Wang CJ (2011) Protocatechuic acid inhibits cancer cell metastasis involving the down-regulation of Ras/Akt/NF-κB pathway and MMP-2 production by targeting RhoB activation. Br J Pharmacol 162(1):237–254

    Article  CAS  Google Scholar 

  42. Lirdprapamongkol K, Kramb J-P, Suthiphongchai T, Surarit R, Srisomsap C, Dannhardt G, Svasti J (2009) Vanillin suppresses metastatic potential of human cancer cells through PI3K inhibition and decreases angiogenesis in vivo. J Agric Food Chem 57(8):3055–3063. doi:10.1021/jf803366f

    Article  CAS  Google Scholar 

  43. Mudnic I, Budimir D, Modun D, Gunjaca G, Generalic I, Skroza D, Katalinic V, Ljubenkov I, Boban M (2012) Antioxidant and vasodilatory effects of blackberry and grape wines. J Med Food 15(3):315–321. doi:10.1089/jmf.2011.0129

    Article  CAS  Google Scholar 

  44. Broncel M, Kozirog M, Duchnowicz P, Koter-Michalak M, Sikora J, Chojnowska-Jezierska J (2010) Aronia melanocarpa extract reduces blood pressure, serum endothelin, lipid, and oxidative stress marker levels in patients with metabolic syndrome. Med Sci Monit 16(1):CR28–CR34

    Google Scholar 

Download references

Acknowledgments

The authors would like to thank their participants in this investigation. K.M.K., G.H., J.L. and P.G.B. conceived and designed the research; K.M.K., P.G.B., S.E.J. conducted the research; K.M.K., G.H., C.L.C., S. E. J., R.B. analysed and interpreted the data; K.M.K. and G.H. drafted the paper. G.H. and K.M.K. had primary responsibility for final content. All authors read, edited and approved the final manuscript. The Cherry Research Committee of the Cherry Marketing Institute (Lansing, MI, USA), a not for profit organisation, provided financial support for a PhD studentship to make this work possible. S. E. J. was supported by Grant PG/12/45/29672 from the British Heart Foundation to R. B. All other elements of the study were funded by Northumbria University. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Glyn Howatson.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 26 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Keane, K.M., Bell, P.G., Lodge, J.K. et al. Phytochemical uptake following human consumption of Montmorency tart cherry (L. Prunus cerasus) and influence of phenolic acids on vascular smooth muscle cells in vitro. Eur J Nutr 55, 1695–1705 (2016). https://doi.org/10.1007/s00394-015-0988-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-015-0988-9

Keywords

Navigation