Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2015, Article ID 836301, 12 pages
http://dx.doi.org/10.1155/2015/836301
Research Article

Quercetin Affects Erythropoiesis and Heart Mitochondrial Function in Mice

1Center of Biomedical Research, Faculty of Health Sciences, Universidad Autónoma de Chile, Ricardo Morales 3369, 8910132 Santiago, Chile
2Center for Biomedical Research, Faculty of Biological Sciences and Faculty of Medicine, Universidad Andres Bello, República 217, 8370146 Santiago, Chile
3iEng Solutions Ltd., London N12 0DR, UK
4Department of Chemical Sciences, Faculty of Exact Sciences, Universidad Andres Bello, República 275, 8370146 Santiago, Chile
5Millennium Institute of Immunology and Immunotherapy, Santiago, Chile

Received 30 January 2015; Revised 8 May 2015; Accepted 11 May 2015

Academic Editor: Victor M. Gonzalez

Copyright © 2015 Lina M. Ruiz 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. J. A. Ross and C. M. Kasum, “Dietary flavonoids: bioavailability, metabolic effects, and safety,” Annual Review of Nutrition, vol. 22, pp. 19–34, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. K. B. Pandey and S. I. Rizvi, “Plant polyphenols as dietary antioxidants in human health and disease,” Oxidative Medicine and Cellular Longevity, vol. 2, no. 5, pp. 270–278, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. E. Osorio, E. G. Pérez, C. Areche et al., “Why is quercetin a better antioxidant than taxifolin? Theoretical study of mechanisms involving activated forms,” Journal of Molecular Modeling, vol. 19, no. 5, pp. 2165–2172, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. F. Arredondo, C. Echeverry, J. A. Abin-Carriquiry et al., “After cellular internalization, quercetin causes Nrf2 nuclear translocation, increases glutathione levels, and prevents neuronal death against an oxidative insult,” Free Radical Biology and Medicine, vol. 49, no. 5, pp. 738–747, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. R. J. Nijveldt, E. van Nood, D. E. C. van Hoorn, P. G. Boelens, K. van Norren, and P. A. M. van Leeuwen, “Flavonoids: a review of probable mechanisms of action and potential applications,” The American Journal of Clinical Nutrition, vol. 74, no. 4, pp. 418–425, 2001. View at Google Scholar · View at Scopus
  6. A. W. Boots, G. R. M. M. Haenen, and A. Bast, “Health effects of quercetin: from antioxidant to nutraceutical,” European Journal of Pharmacology, vol. 585, no. 2-3, pp. 325–337, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. F. Perez-Vizcaino, D. Bishop-Bailley, F. Lodi et al., “The flavonoid quercetin induces apoptosis and inhibits JNK activation in intimal vascular smooth muscle cells,” Biochemical and Biophysical Research Communications, vol. 346, no. 3, pp. 919–925, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. R. Bucki, T. J. J. Pastore, F. Giraud, J.-C. Sulpicejand, and P. A. Janmey, “Flavonoid inhibition of platelet procoagulant activity and phosphoinositide synthesis,” Journal of Thrombosis and Haemostasis, vol. 1, no. 8, pp. 1820–1828, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. T. P. T. Cushnie and A. J. Lamb, “Antimicrobial activity of flavonoids,” International Journal of Antimicrobial Agents, vol. 26, no. 5, pp. 343–356, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. N. Gulati, B. Laudet, V. M. Zohrabian, R. Murali, and M. Jhanwar-Uniyal, “The antiproliferative effect of Quercetin in cancer cells is mediated via inhibition of the PI3K-Akt/PKB pathway,” Anticancer Research, vol. 26, no. 2, pp. 1177–1181, 2006. View at Google Scholar · View at Scopus
  11. A. W. Boots, H. Li, R. P. F. Schins et al., “The quercetin paradox,” Toxicology and Applied Pharmacology, vol. 222, no. 1, pp. 89–96, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. S.-F. Xia, Z.-X. Xie, Y. Qiao et al., “Differential effects of quercetin on hippocampus-dependent learning and memory in mice fed with different diets related with oxidative stress,” Physiology & Behavior, vol. 138, pp. 325–331, 2015. View at Publisher · View at Google Scholar
  13. R. Casuso, E. Martínez-López, F. Hita-Contreras et al., “The combination of oral quercetin supplementation and exercise prevents brain mitochondrial biogenesis,” Genes & Nutrition, vol. 9, pp. 1–8, 2014. View at Google Scholar
  14. E. J. Choi, K.-M. Chee, and B. H. Lee, “Anti- and prooxidant effects of chronic quercetin administration in rats,” European Journal of Pharmacology, vol. 482, no. 1–3, pp. 281–285, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. D. J. Dorta, A. A. Pigoso, F. E. Mingatto et al., “The interaction of flavonoids with mitochondria: effects on energetic processes,” Chemico-Biological Interactions, vol. 152, no. 2-3, pp. 67–78, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. D. J. Dorta, A. A. Pigoso, F. E. Mingatto et al., “Antioxidant activity of flavonoids in isolated mitochondria,” Phytotherapy Research, vol. 22, no. 9, pp. 1213–1218, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. U. De Marchi, L. Biasutto, S. Garbisa, A. Toninello, and M. Zoratti, “Quercetin can act either as an inhibitor or an inducer of the mitochondrial permeability transition pore: a demonstration of the ambivalent redox character of polyphenols,” Biochimica et Biophysica Acta, vol. 1787, no. 12, pp. 1425–1432, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Lesjak, R. Hoque, S. Balesaria et al., “Quercetin inhibits intestinal iron absorption and ferroportin transporter expression in vivo and in vitro,” PLoS ONE, vol. 9, no. 7, Article ID e102900, 2014. View at Publisher · View at Google Scholar
  19. R. Hoque, The effects of quercetin on iron metabolism [Doctoral thesis], Diabetes & Nutritional Sciences Division, School of Medicine, King's College London, University of London, 2014.
  20. R. Lill, B. Hoffmann, S. Molik et al., “The role of mitochondria in cellular iron-sulfur protein biogenesis and iron metabolism,” Biochimica et Biophysica Acta: Molecular Cell Research, vol. 1823, no. 9, pp. 1491–1508, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. J. L. Spivak, “The anaemia of cancer: death by a thousand cuts,” Nature Reviews Cancer, vol. 5, no. 7, pp. 543–555, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Fontenay, S. Cathelin, M. Amiot, E. Gyan, and E. Solary, “Mitochondria in hematopoiesis and hematological diseases,” Oncogene, vol. 25, no. 34, pp. 4757–4767, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. A. D. Sheftel, A.-S. Zhang, C. Brown, O. S. Shirihai, and P. Ponka, “Direct interorganellar transfer of iron from endosome to mitochondrion,” Blood, vol. 110, no. 1, pp. 125–132, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. N. Hegde, M. W. Rich, and C. Gayomali, “The cardiomyopathy of iron deficiency,” Texas Heart Institute Journal, vol. 33, no. 3, pp. 340–344, 2006. View at Google Scholar · View at Scopus
  25. J. Marín-García and M. J. Goldenthal, “The mitochondrial organelle and the heart,” Revista Española de Cardiología, vol. 55, no. 12, pp. 1293–1310, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. G. Karamanlidis, C. F. Lee, L. Garcia-Menendez et al., “Mitochondrial complex i deficiency increases protein acetylation and accelerates heart failure,” Cell Metabolism, vol. 18, no. 2, pp. 239–250, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Maranzana, G. Barbero, A. I. Falasca, G. Lenaz, and M. L. Genova, “Mitochondrial respiratory supercomplex association limits production of reactive oxygen species from complex i,” Antioxidants and Redox Signaling, vol. 19, no. 13, pp. 1469–1480, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Acín-Pérez, P. Fernández-Silva, M. L. Peleato, A. Pérez-Martos, and J. A. Enriquez, “Respiratory active mitochondrial supercomplexes,” Molecular Cell, vol. 32, no. 4, pp. 529–539, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Acin-Perez and J. A. Enriquez, “The function of the respiratory supercomplexes: the plasticity model,” Biochimica et Biophysica Acta: Bioenergetics, vol. 1837, no. 4, pp. 444–450, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. L. M. Ruiz, E. L. Jensen, R. I. Bustos et al., “Adaptive responses of mitochondria to mild copper deprivation involve changes in morphology, OXPHOS remodeling and bioenergetics,” Journal of Cellular Physiology, vol. 229, no. 5, pp. 607–619, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. J. D. Wikstrom, K. Mahdaviani, M. Liesa et al., “Hormone-induced mitochondrial fission is utilized by brown adipocytes as an amplification pathway for energy expenditure,” The EMBO Journal, vol. 33, no. 5, pp. 418–436, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. R. I. Bustos, E. L. Jensen, L. M. Ruiz et al., “Copper deficiency alters cell bioenergetics and induces mitochondrial fusion through up-regulation of MFN2 and OPA1 in erythropoietic cells,” Biochemical and Biophysical Research Communications, vol. 437, no. 3, pp. 426–432, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Vazquez-Martin, B. Corominas-Faja, S. Cufi et al., “The mitochondrial H+-ATP synthase and the lipogenic switch New core components of metabolic reprogramming in induced pluripotent stem (iPS) cells,” Cell Cycle, vol. 12, no. 2, pp. 207–218, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Pich, D. Bach, P. Briones et al., “The Charcot-Marie-Tooth type 2A gene product, Mfn2, up-regulates fuel oxidation through expression of OXPHOS system,” Human Molecular Genetics, vol. 14, no. 11, pp. 1405–1415, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Picard, O. S. Shirihai, B. J. Gentil, and Y. Burelle, “Mitochondrial morphology transitions and functions: implications for retrograde signaling?” American Journal of Physiology—Regulatory, Integrative and Comparative Physiology, vol. 304, no. 6, pp. R393–R406, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Liesa, M. Palacín, and A. Zorzano, “Mitochondrial dynamics in mammalian health and disease,” Physiological Reviews, vol. 89, no. 3, pp. 799–845, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Liesa and O. S. Shirihai, “Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure,” Cell Metabolism, vol. 17, no. 4, pp. 491–506, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. D. Bach, S. Pich, F. X. Soriano et al., “Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism: a novel regulatory mechanism altered in obesity,” Journal of Biological Chemistry, vol. 278, no. 19, pp. 17190–17197, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Zorzano, “Regulation of mitofusin-2 expression in skeletal muscleThis paper is one of a selection of papers published in this Special Issue, entitled 14th International Biochemistry of Exercise Conference—Muscles as Molecular and Metabolic Machines, and has undergone the Journal’s usual peer review process,” Applied Physiology, Nutrition, and Metabolism, vol. 34, no. 3, pp. 433–439, 2009. View at Publisher · View at Google Scholar
  40. B. N. Finck and D. P. Kelly, “Peroxisome proliferator-activated receptor γ coactivator-1 (PGC-1) regulatory cascade in cardiac physiology and disease,” Circulation, vol. 115, no. 19, pp. 2540–2548, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. Z. Wu, P. Puigserver, U. Andersson et al., “Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1,” Cell, vol. 98, no. 1, pp. 115–124, 1999. View at Publisher · View at Google Scholar · View at Scopus
  42. K. Vanhees, L. de Bock, R. W. L. Godschalk, F. J. van Schooten, and S. B. van Waalwijk van Doorn-Khosrovani, “Prenatal exposure to flavonoids: implication for cancer risk,” Toxicological Sciences, vol. 120, no. 1, pp. 59–67, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. A. M. Sabogal-Guáqueta, J. I. Muñoz-Manco, J. R. Ramírez-Pineda, M. Lamprea-Rodriguez, E. Osorio, and G. P. Cardona-Gómez, “The flavonoid quercetin ameliorates Alzheimer's disease pathology and protects cognitive and emotional function in aged triple transgenic Alzheimer's disease model mice,” Neuropharmacology, vol. 93, pp. 134–145, 2015. View at Publisher · View at Google Scholar
  44. P. Galindo, S. González-Manzano, M. J. Zarzuelo et al., “Different cardiovascular protective effects of quercetin administered orally or intraperitoneally in spontaneously hypertensive rats,” Food & Function, vol. 3, no. 6, pp. 643–650, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. E. Schültke, R. W. Griebel, and B. H. J. Juurlink, “Quercetin administration after spinal cord trauma changes S-100β levels,” Canadian Journal of Neurological Sciences, vol. 37, no. 2, pp. 223–228, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. S.-T. Chan, Y.-C. Lin, C.-H. Chuang, R.-J. Shiau, J.-W. Liao, and S.-L. Yeh, “Oral and intraperitoneal administration of quercetin decreased lymphocyte DNA damage and plasma lipid peroxidation induced by TSA in vivo,” BioMed Research International, vol. 2014, Article ID 580626, 9 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. H. K. Park, S. J. Kim, D. Y. Kwon, J. H. Park, and Y. C. Kim, “Protective effect of quercetin against paraquat-induced lung injury in rats,” Life Sciences, vol. 87, no. 5-6, pp. 181–186, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. G. H. Heeba and M. E. Mahmoud, “Dual effects of quercetin in doxorubicin-induced nephrotoxicity in rats and its modulation of the cytotoxic activity of doxorubicin on human carcinoma cells,” Environmental Toxicology, 2014. View at Publisher · View at Google Scholar
  49. J. Renugadevi and S. M. Prabu, “Quercetin protects against oxidative stress-related renal dysfunction by cadmium in rats,” Experimental and Toxicologic Pathology, vol. 62, no. 5, pp. 471–481, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. S. K. Richetti, M. Blank, K. M. Capiotti et al., “Quercetin and rutin prevent scopolamine-induced memory impairment in zebrafish,” Behavioural Brain Research, vol. 217, no. 1, pp. 10–15, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. R. M. J. Deacon, “Measuring the strength of mice,” Journal of Visualized Experiments, no. 76, p. e2610, 2013. View at Google Scholar · View at Scopus
  52. A. Elorza, B. Hyde, H. K. Mikkola, S. Collins, and O. S. Shirihai, “UCP2 modulates cell proliferation through the MAPK/ERK pathway during erythropoiesis and has no effect on heme biosynthesis,” The Journal of Biological Chemistry, vol. 283, no. 45, pp. 30461–30470, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. W. Duan, Z. Guo, H. Jiang, M. Ware, X.-J. Li, and M. P. Mattson, “Dietary restriction normalizes glucose metabolism and BDNF levels, slows disease progression, and increases survival in huntingtin mutant mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 5, pp. 2911–2916, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. C. Jung, C. M. J. Higgins, and Z. Xu, “Measuring the quantity and activity of mitochondrial electron transport chain complexes in tissues of central nervous system using blue native polyacrylamide gel electrophoresis,” Analytical Biochemistry, vol. 286, no. 2, pp. 214–223, 2000. View at Publisher · View at Google Scholar · View at Scopus
  55. L. I. Grad and B. D. Lemire, “Riboflavin enhances the assembly of mitochondrial cytochrome c oxidase in C. elegans NADH-ubiquinone oxidoreductase mutants,” Biochimica et Biophysica Acta: Bioenergetics, vol. 1757, no. 2, pp. 115–122, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. I. Wittig, R. Carrozzo, F. M. Santorelli, and H. Schägger, “Functional assays in high-resolution clear native gels to quantify mitochondrial complexes in human biopsies and cell lines,” Electrophoresis, vol. 28, no. 21, pp. 3811–3820, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. J.-M. Li, W. Wang, C.-Y. Fan et al., “Quercetin preserves β-cell mass and function in fructose-induced hyperinsulinemia through modulating pancreatic Akt/FoxO1 activation,” Evidence-Based Complementary and Alternative Medicine, vol. 2013, Article ID 303902, 12 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Khurana, K. Venkataraman, A. Hollingsworth, M. Piche, and T. C. Tai, “Polyphenols: benefits to the cardiovascular system in health and in aging,” Nutrients, vol. 5, no. 10, pp. 3779–3827, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. M. J. Ryan, G. R. McLemore Jr., and S. T. Hendrix, “Insulin resistance and obesity in a mouse model of systemic lupus erythematosus,” Hypertension, vol. 48, no. 5, pp. 988–993, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. C. Thomas and L. Thomas, “Biochemical markers and hematologic indices in the diagnosis of functional iron deficiency,” Clinical Chemistry, vol. 48, no. 7, pp. 1066–1076, 2002. View at Google Scholar · View at Scopus
  61. L. Viatte, J.-C. Lesbordes-Brion, D.-Q. Lou et al., “Deregulation of proteins involved in iron metabolism in hepcidin-deficient mice,” Blood, vol. 105, no. 12, pp. 4861–4864, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. N. E. Hellman and J. D. Gitlin, “Ceruloplasmin metabolism and function,” Annual Review of Nutrition, vol. 22, pp. 439–458, 2002. View at Publisher · View at Google Scholar · View at Scopus
  63. B. N. Patel, R. J. Dunn, S. Y. Jeong, Q. Zhu, J.-P. Julien, and S. David, “Ceruloplasmin regulates iron levels in the CNS and prevents free radical injury,” The Journal of Neuroscience, vol. 22, no. 15, pp. 6578–6586, 2002. View at Google Scholar · View at Scopus
  64. A. Raghavan, T. Sheiko, B. H. Graham, and W. J. Craigen, “Voltage-dependant anion channels: novel insights into isoform function through genetic models,” Biochimica et Biophysica Acta: Biomembranes, vol. 1818, no. 6, pp. 1477–1485, 2012. View at Publisher · View at Google Scholar · View at Scopus
  65. I. Dalle-Donne, M. Carini, M. Orioli et al., “Protein carbonylation: 2,4-dinitrophenylhydrazine reacts with both aldehydes/ketones and sulfenic acids,” Free Radical Biology and Medicine, vol. 46, no. 10, pp. 1411–1419, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. M. M. Baccan, O. Chiarelli-Neto, R. M. S. Pereira, and B. P. Espósito, “Quercetin as a shuttle for labile iron,” Journal of Inorganic Biochemistry, vol. 107, no. 1, pp. 34–39, 2012. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Salvi, A. M. Brunati, G. Clari, and A. Toninello, “Interaction of genistein with the mitochondrial electron transport chain results in opening of the membrane transition pore,” Biochimica et Biophysica Acta—Bioenergetics, vol. 1556, no. 2-3, pp. 187–196, 2002. View at Publisher · View at Google Scholar · View at Scopus
  68. H. S. Yoon, S. C. Moon, N. D. Kim, B. S. Park, M. H. Jeong, and Y. H. Yoo, “Genistein induces apoptosis of RPE-J cells by opening mitochondrial PTP,” Biochemical and Biophysical Research Communications, vol. 276, no. 1, pp. 151–156, 2000. View at Publisher · View at Google Scholar · View at Scopus
  69. L. M. Larocca, L. Teofili, G. Leone et al., “Antiproliferative activity of quercetin on normal bone marrow and leukaemic progenitors,” British Journal of Haematology, vol. 79, no. 4, pp. 562–566, 1991. View at Publisher · View at Google Scholar · View at Scopus
  70. S. A. Bakheet, “Assessment of anti-cytogenotoxic effects of quercetin in animals treated with topotecan,” Oxidative Medicine and Cellular Longevity, vol. 2011, Article ID 824597, 8 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. A. Pȩkal, M. Biesaga, and K. Pyrzynska, “Interaction of quercetin with copper ions: complexation, oxidation and reactivity towards radicals,” BioMetals, vol. 24, no. 1, pp. 41–49, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. A. C. Moţ, C. Coman, C. Miron, G. Damian, C. Sarbu, and R. Silaghi-Dumitrescu, “An assay for pro-oxidant reactivity based on phenoxyl radicals generated by laccase,” Food Chemistry, vol. 143, pp. 214–222, 2014. View at Publisher · View at Google Scholar · View at Scopus
  73. G. Galati, O. Sabzevari, J. X. Wilson, and P. J. O'Brien, “Prooxidant activity and cellular effects of the phenoxyl radicals of dietary flavonoids and other polyphenolics,” Toxicology, vol. 177, no. 1, pp. 91–104, 2002. View at Publisher · View at Google Scholar · View at Scopus
  74. J. M. Davis, E. A. Murphy, M. D. Carmichael, and B. Davis, “Quercetin increases brain and muscle mitochondrial biogenesis and exercise tolerance,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 296, no. 4, pp. R1071–R1077, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. M. Vessal, M. Hemmati, and M. Vasei, “Antidiabetic effects of quercetin in streptozocin-induced diabetic rats,” Comparative Biochemistry and Physiology C: Toxicology & Pharmacology, vol. 135, no. 3, pp. 357–364, 2003. View at Publisher · View at Google Scholar · View at Scopus