Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014, Article ID 898045, 7 pages
http://dx.doi.org/10.1155/2014/898045
Review Article

Bioactive Compounds Derived from the Yeast Metabolism of Aromatic Amino Acids during Alcoholic Fermentation

1Facultad de Enología, Universitat Rovira i Virgili, Marcel·lí Domingo s/n, 43003 Tarragona, Spain
2Departamento de Biotecnologia de Alimentos, Instituto de Agroquímica y Tecnología de los Alimentos (CSIC), Agustín Escardino, 7, 46980 Valencia, Spain
3Facultad de Farmacia, Universidad de Sevilla, Profesor García González, 2, 41012 Sevilla, Spain

Received 20 February 2014; Accepted 16 April 2014; Published 5 May 2014

Academic Editor: You-Lin Tain

Copyright © 2014 Albert Mas et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. Varela, F. Pizarro, and E. Agosin, “Biomass content governs fermentation rate in nitrogen-deficient wine musts,” Applied and Environmental Microbiology, vol. 70, no. 6, pp. 3392–3400, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. L. F. Bisson, “Stuck and sluggish fermentations,” The American Journal of Enology and Viticulture, vol. 50, no. 1, pp. 107–119, 1999. View at Google Scholar · View at Scopus
  3. P. Taillandier, F. Ramon Portugal, A. Fuster, and P. Strehaiano, “Effect of ammonium concentration on alcoholic fermentation kinetics by wine yeasts for high sugar content,” Food Microbiology, vol. 24, no. 1, pp. 95–100, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. E. Albers, C. Larsson, G. Lidén, C. Niklasson, and L. Gustafsson, “Influence of the nitrogen source on Saccharomyces cerevisiae anaerobic growth and product formation,” Applied and Environmental Microbiology, vol. 62, no. 9, pp. 3187–3195, 1996. View at Google Scholar · View at Scopus
  5. F. Radler, “Yeasts—metabolism of organic acids,” in Wine Microbiology and Biotechnology, G. H. Fleet, Ed., pp. 165–182, Harwood Academic Publishers, Singapore, 1993. View at Google Scholar
  6. C. Camarasa, J.-P. Grivet, and S. Dequin, “Investigation by 13C-NMR and tricarboxylic acid (TCA) deletion mutant analysis of pathways of succinate formation in Saccharomyces cerevisiae during anaerobic fermentation,” Microbiology, vol. 149, no. 9, pp. 2669–2678, 2003. View at Google Scholar · View at Scopus
  7. A. Gutiérrez, G. Beltran, J. Warringer, and J. M. Guillamon, “Genetic basis of variations in nitrogen source utilization in four wine commercial yeast strains,” PLoS ONE, vol. 8, no. 6, Article ID E67166, 2013. View at Google Scholar
  8. A. Rapp and G. Versini, “Influence of nitrogen compounds in grapes on aroma compounds of wines,” Developments in Food Science, vol. 37, pp. 1659–1694, 1995. View at Publisher · View at Google Scholar · View at Scopus
  9. P. A. Henschke and V. Jiranek, “Yeasts-metabolism of nitrogen compounds,” in Wine Microbiology and Biotechnology, G. H. Fleet, Ed., pp. 77–164, Harwood Academic Publishers, Chur, Switzerland, 1993. View at Google Scholar
  10. J. H. Swiegers, E. J. Bartowsky, P. A. Henschke, and I. S. Pretorius, “Yeast and bacterial modulation of wine aroma and flavour,” Australian Journal of Grape and Wine Research, vol. 11, no. 2, pp. 139–173, 2005. View at Google Scholar · View at Scopus
  11. S.-J. Bell and P. A. Henschke, “Implications of nitrogen nutrition for grapes, fermentation and wine,” Australian Journal of Grape and Wine Research, vol. 11, no. 3, pp. 242–295, 2005. View at Google Scholar · View at Scopus
  12. P. Ribéreau-Gayon, D. Dubourdieu, B. Donèche, and A. Lonvaud, Handbook of Enology, John Wiley & Sons, 2nd edition, 2006.
  13. D. Torrea, C. Varela, M. Ugliano, C. Ancin-Azpilicueta, I. Leigh Francis, and P. A. Henschke, “Comparison of inorganic and organic nitrogen supplementation of grape juice—effect on volatile composition and aroma profile of a Chardonnay wine fermented with Saccharomyces cerevisiae yeast,” Food Chemistry, vol. 127, no. 3, pp. 1072–1083, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Hua and P. Xu, “Recent advances in biotechnological production of 2-phenylethanol,” Biotechnology Advances, vol. 29, no. 6, pp. 654–660, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. J. R. Dickinson, “Filament formation in Saccharomyces cerevisiae—a review,” Folia Microbiologica, vol. 53, no. 1, pp. 3–14, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. G. F. Sprague Jr. and S. C. Winans, “Eukaryotes learn how to count: Quorum sensing by yeast,” Genes and Development, vol. 20, no. 9, pp. 1045–1049, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. J. M. Hornby, E. C. Jensen, A. D. Lisec et al., “Quorum sensing in the dimorphic fungus candida albicans is mediated by farnesol,” Applied and Environmental Microbiology, vol. 67, no. 7, pp. 2982–2992, 2001. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Chen, M. Fujita, Q. Feng, J. Clardy, and G. R. Fink, “Tyrosol is a quorum-sensing molecule in Candida albicans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 14, pp. 5048–5052, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. H. Chen and G. R. Fink, “Feedback control of morphogenesis in fungi by aromatic alcohols,” Genes and Development, vol. 20, no. 9, pp. 1150–1161, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. D. van Dyk, I. S. Pretorius, and F. F. Bauer, “Mss11p is a central element of the regulatory network that controls FLO11 expression and invasive growth in Saccharomyces cerevisiae,” Genetics, vol. 169, no. 1, pp. 91–106, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. C. Giovannini, E. Straface, D. Modesti et al., “Tyrosol, the major olive oil biophenol, protects against oxidized-LDL- induced injury in Caco-2 cells,” Journal of Nutrition, vol. 129, no. 7, pp. 1269–1277, 1999. View at Google Scholar · View at Scopus
  22. S. M. Samuel, M. Thirunavukkarasu, S. V. Penumathsa, D. Paul, and N. Maulik, “Akt/FOXO3a/SIRT1-mediated cardioprotection by n-tyrosol against ischemic stress in rat in vivo model of myocardial infarction: switching gears toward survival and longevity,” Journal of Agricultural and Food Chemistry, vol. 56, no. 20, pp. 9692–9698, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Vitalini, C. Gardana, A. Zanzotto et al., “From vineyard to glass: agrochemicals enhance the melatonin and total polyphenol contents and antiradical activity of red wines,” Journal of Pineal Research, vol. 51, no. 3, pp. 278–285, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. E. M. Cornford, P. D. Crane, L. D. Braun, W. D. Bocash, A. M. Nyerges, and W. H. Oldendorf, “Reduction in brain glucose utilization rate after tryptophol (3-indole ethanol) treatment,” Journal of Neurochemistry, vol. 36, no. 5, pp. 1758–1765, 1981. View at Google Scholar · View at Scopus
  25. M. I. Rodriguez-Naranjo, M. J. Torija, A. Mas, E. Cantos-Villar, and M. D. C. Garcia-Parrilla, “Production of melatonin by Saccharomyces strains under growth and fermentation conditions,” Journal of Pineal Research, vol. 53, no. 3, pp. 219–224, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Arevalo-Villena, E. J. Bartowsky, D. Capone, and M. A. Sefton, “Production of indole by wine-associated microorganisms under oenological conditions,” Food Microbiology, vol. 27, no. 5, pp. 685–690, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. D.-X. Tan, R. Hardeland, L. C. Manchester et al., “Functional roles of melatonin in plants, and perspectives in nutritional and agricultural science,” Journal of Experimental Botany, vol. 63, no. 2, pp. 577–597, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Sprenger, R. Hardeland, B. Fuhrberg, and S.-Z. Han, “Melatonin and other 5-methoxylated indoles in yeast: presence in high concentrations and dependence on tryptophan availability,” Cytologia, vol. 64, no. 2, pp. 209–213, 1999. View at Google Scholar · View at Scopus
  29. E. Serrano, C. Venegas, G. Escames et al., “Antioxidant defence and inflammatory response in professional road cyclists during a 4-day competition,” Journal of Sports Sciences, vol. 28, no. 10, pp. 1047–1056, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Chahbouni, G. Escames, C. Venegas et al., “Melatonin treatment normalizes plasma pro-inflammatory cytokines and nitrosative/oxidative stress in patients suffering from Duchenne muscular dystrophy,” Journal of Pineal Research, vol. 48, no. 3, pp. 282–289, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. A. López, J. A. García, G. Escames et al., “Melatonin protects the mitochondria from oxidative damage reducing oxygen consumption, membrane potential, and superoxide anion production,” Journal of Pineal Research, vol. 46, no. 2, pp. 188–198, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. G. A. Bubenik, “Gastrointestinal melatonin: localization, function, and clinical relevance,” Digestive Diseases and Sciences, vol. 47, no. 10, pp. 2336–2348, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. D.-X. Tan, L. C. Manchester, R. J. Reiter, W.-B. Qi, M. Karbownik, and J. R. Calvo, “Significance of melatonin in antioxidative defense system: reactions and products,” Biological Signals and Receptors, vol. 9, no. 3-4, pp. 137–159, 2000. View at Google Scholar · View at Scopus
  34. D.-X. Tan, L. C. Manchester, M. P. Terron, L. J. Flores, and R. J. Reiter, “One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species?” Journal of Pineal Research, vol. 42, no. 1, pp. 28–42, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Oaknin-Bendahan, Y. Anis, I. Nir, and N. Zisapel, “Effects of long-term administration of melatonin and a putative antagonist on the ageing rat,” NeuroReport, vol. 6, no. 5, pp. 785–788, 1995. View at Google Scholar · View at Scopus
  36. M. Karbownik, R. J. Reiter, S. Burkhardt, E. Gitto, D.-X. Tan, and A. Lewiñski, “Melatonin attenuates estradiol-induced oxidative damage to DNA: relevance for cancer prevention,” Experimental Biology and Medicine, vol. 226, no. 7, pp. 707–712, 2001. View at Google Scholar · View at Scopus
  37. V. Vijayalaxmi, R. J. Reiter, T. S. Herman, and M. L. Meltz, “Melatonin and radioprotection from genetic damage: in vivo/in vitro studies with human volunteers,” Mutation Research—Genetic Toxicology, vol. 371, no. 3-4, pp. 221–228, 1996. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Carrillo-Vico, J. M. Guerrero, P. J. Lardone, and R. J. Reiter, “A review of the multiple actions of melatonin on the immune system,” Endocrine, vol. 27, no. 2, pp. 189–200, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Larson, R. E. Jessen, T. Uz et al., “Impaired hippocampal long-term potentiation in melatonin MT2 receptor-deficient mice,” Neuroscience Letters, vol. 393, no. 1, pp. 23–26, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. M. A. Pappolla, M. Sos, R. A. Omar et al., “Melatonin prevents death of neuroblastoma cells exposed to the Alzheimer amyloid peptide,” Journal of Neuroscience, vol. 17, no. 5, pp. 1683–1690, 1997. View at Google Scholar · View at Scopus
  41. M. Pohanka, “Alzheimer's disease and related neurodegenerative disorders: implication and counteracting of melatonin,” Journal of Applied Biomedicine, vol. 9, no. 4, pp. 185–196, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Jacob, B. Poeggeler, J. H. Weishaupt et al., “Melatonin as a candidate compound for neuroprotection in amyotrophic lateral sclerosis (ALS): high tolerability of daily oral melatonin administration in ALS patients,” Journal of Pineal Research, vol. 33, no. 3, pp. 186–187, 2002. View at Publisher · View at Google Scholar · View at Scopus
  43. D. W. Dodick and D. J. Capobianco, “Treatment and management of cluster headache,” Current Pain and Headache Reports, vol. 5, no. 1, pp. 83–91, 2001. View at Google Scholar · View at Scopus
  44. M. I. Rodriguez-Naranjo, A. Gil-Izquierdo, A. M. Troncoso, E. Cantos-Villar, and M. C. Garcia-Parrilla, “Melatonin: a new bioactive compound in wine,” Journal of Food Composition and Analysis, vol. 24, no. 4-5, pp. 603–608, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. M. I. Rodriguez-Naranjo, A. Gil-Izquierdo, A. M. Troncoso, E. Cantos-Villar, and M. C. Garcia-Parrilla, “Melatonin is synthesised by yeast during alcoholic fermentation in wines,” Food Chemistry, vol. 126, no. 4, pp. 1608–1613, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. F. J. V. Gomez, J. Raba, S. Cerutti, and M. F. Silva, “Monitoring melatonin and its isomer in Vitis vinifera cv. Malbec by UHPLC-MS/MS from grape to bottle,” Journal of Pineal Research, vol. 52, no. 3, pp. 349–355, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. M. D. Maldonado, H. Moreno, and J. R. Calvo, “Melatonin present in beer contributes to increase the levels of melatonin and antioxidant capacity of the human serum,” Clinical Nutrition, vol. 28, no. 2, pp. 188–191, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Iriti, M. Rossoni, and F. Faoro, “Melatonin content in grape: myth or panacea?” Journal of the Science of Food and Agriculture, vol. 86, no. 10, pp. 1432–1438, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. S. J. Murch, B. A. Hall, C. H. Le, and P. K. Saxena, “Changes in the levels of indoleamine phytochemicals during véraison and ripening of wine grapes,” Journal of Pineal Research, vol. 49, no. 1, pp. 95–100, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Brzezinski, “Melatonin in humans,” The New England Journal of Medicine, vol. 336, no. 3, pp. 186–195, 1997. View at Publisher · View at Google Scholar · View at Scopus
  51. H. E. Boccalandro, C. V. González, D. A. Wunderlin, and M. F. Silva, “Melatonin levels, determined by LC-ESI-MS/MS, fluctuate during the day/night cycle in Vitis vinifera cv Malbec: evidence of its antioxidant role in fruits,” Journal of Pineal Research, vol. 51, no. 2, pp. 226–232, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. Z. Eelderink-Chen, G. Mazzotta, M. Sturre, J. Bosman, T. Roenneberg, and M. Merrow, “A circadian clock in Saccharomyces cerevisiae,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 5, pp. 2043–2047, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Merrow and M. Raven, “Finding time: a daily clock in yeast,” Cell Cycle, vol. 9, no. 9, pp. 1671–1672, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. G. Diamantini, G. Tarzia, G. Spadoni, M. D’Alpaos, and P. Traldi, “Metastable ion studies in the characterization of melatonin isomers,” Rapid Communications in Mass Spectrometry, vol. 12, no. 20, pp. 1538–1542, 1998. View at Google Scholar
  55. T. Kocadağli, C. Yilmaz, and V. Gökmen, “Determination of melatonin and its isomer in foods by liquid chromatography tandem mass spectrometry,” Food Chemistry, vol. 153, pp. 151–156, 2014. View at Google Scholar
  56. A. Ramakrishna, P. Giridhar, K. U. Sankar, and G. A. Ravishankar, “Melatonin and serotonin profiles in beans of Coffea species,” Journal of Pineal Research, vol. 52, no. 4, pp. 470–476, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. F. A. Badria, “Melatonin, serotonin, and tryptamine in some Egyptian food and medicinal plants,” Journal of Medicinal Food, vol. 5, no. 3, pp. 153–157, 2002. View at Google Scholar · View at Scopus
  58. R. Pelagio-Flores, R. Ortíz-Castro, A. Méndez-Bravo, L. MacÍas-Rodríguez, and J. López-Bucio, “Serotonin, a tryptophan-derived signal conserved in plants and animals, regulates root system architecture probably acting as a natural auxin inhibitor in arabidopsis thaliana,” Plant and Cell Physiology, vol. 52, no. 3, pp. 490–508, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. M. G. Strakhovskaia, A. M. Serdalina, and G. I. Fraǐkin, “Effect of the photo-induced synthesis of serotonin on the photoreactivation of Saccharomyces cerevisiae yeasts,” Nauchnye Doklady Vysshei Shkoly. Biologicheskie Nauki, no. 3, pp. 25–28, 1983. View at Google Scholar · View at Scopus
  60. R. Hardeland and B. Poeggeler, “Melatonin beyond its classical funtions,” The Open Physiology Journal, vol. 1, no. 1, pp. 1–22, 2008. View at Publisher · View at Google Scholar
  61. J. M. Landete, S. Ferrer, and I. Pardo, “Biogenic amine production by lactic acid bacteria, acetic bacteria and yeast isolated from wine,” Food Control, vol. 18, no. 12, pp. 1569–1574, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. L. Manfroi, P. H. A. Silva, L. A. Rizzon, P. S. Sabaini, and M. B. A. Glória, “Influence of alcoholic and malolactic starter cultures on bioactive amines in Merlot wines,” Food Chemistry, vol. 116, no. 1, pp. 208–213, 2009. View at Publisher · View at Google Scholar · View at Scopus