Quercetin Affects Erythropoiesis and Heart Mitochondrial Function in Mice

Oxidative Medicine and Cellular Longevity

Volumn 2015, Issue , 2015, Pages

  Ruiz, Lina M ^a   Salazar, Celia ^a   Jensen, Erik ^b   Ruiz, Paula A ^c   Tiznado, William ^b   Quintanilla, Rodrigo A ^a   Barreto, Marlen ^a   Elorza, Alvaro A ^b,d  

^a UNIVERSIDAD AUTÓNOMA DE CHILE   (Chile)

^b UNIVERSIDAD ANDRÉS BELLO   (Chile)

^c IEng Solutions Ltd   (United Kingdom)

^d Pontificia Universidad Católica de Chile   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANTS; DIETARY SUPPLEMENTS; FLAVONOIDS; MAMMALS; MITOCHONDRIA; MOBILE SECURITY; PROTEINS;

ANTIOXIDANT CAPACITY; ANTIOXIDANT EFFECT; CELLULAR MODEL; FOOD SUPPLEMENTS; MITOCHONDRIAL FUNCTION; PROTEIN EXPRESSION LEVELS; PROTEIN OXIDATION; RESPIRATORY CHAINS;

PHENOLS;

CERULOPLASMIN; INSULIN; MITOFUSIN 2; QUERCETIN; VOLTAGE DEPENDENT ANION CHANNEL; ANTIOXIDANT; FERRITIN; GUANOSINE TRIPHOSPHATASE; MFN2 PROTEIN, MOUSE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PPARGC1A PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ERYTHROPOIESIS; HEART MITOCHONDRION; IN VIVO STUDY; INSULIN BLOOD LEVEL; MALE; METABOLISM; MITOCHONDRIAL DYNAMICS; MOUSE; NONHUMAN; OXIDATION; PROTEIN EXPRESSION; ANIMAL; BLOOD; BONE MARROW CELL; C57BL MOUSE; CARDIAC MUSCLE; CYTOLOGY; DRUG EFFECTS; MITOCHONDRION;

MAMMALIA; MUS;

ANIMALS; ANTIOXIDANTS; BODY WEIGHT; BONE MARROW CELLS; CERULOPLASMIN; ERYTHROPOIESIS; FERRITINS; GTP PHOSPHOHYDROLASES; INSULIN; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MYOCARDIUM; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA COACTIVATOR 1-ALPHA; QUERCETIN; TRANSCRIPTION FACTORS;

EID: 84935917504     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2015/836301     Document Type: Article

References (75)

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.
2. K. B. Pand ey 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.
3. E. Osorio, E. G. Perez, C. Areche, et al., "Why is quercetin a better antioxidant than taxifolin? Theoretical study ofmechanisms involving activated forms, " Journal of Molecular Modeling, vol. 19, no. 5, pp. 2165-2172, 2013.
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.
5. R. J. Nijveldt, E. vanNood, D. E. C. vanHoorn, 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.
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.
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.
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.
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.
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.
11. A. W. Boots, H. Li, R. P. F. Schins, et al., "Thequercetin paradox, " Toxicology and Applied Pharmacology, vol. 222, no. 1, pp. 89-96, 2007.
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.
13. R. Casuso, E. Martinez-Lopez, 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.
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.
15. D. J. Dorta, A. A. Pigoso, F. E. Mingatto, et al., "The interaction of flavonoidswithmitochondria: effects on energetic processes, " Chemico-Biological Interactions, vol. 152, no. 2-3, pp. 67-78, 2005.
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.
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, " Biochimicaet Biophysica Acta, vol. 1787, no. 12, pp. 1425-1432, 2009.
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.
19. R. Hoque, The effects of quercetin on iron metabolism Doctoral thesis, Diabetes & Nutritional Sciences Division, School of Medicine, Kings 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, " Biochimicaet BiophysicaActa:Molecular Cell Research, vol. 1823, no. 9, pp. 1491-1508, 2012.
21. J. L. Spivak, "The anaemia of cancer: death by a thousand cuts, " Nature Reviews Cancer, vol. 5, no. 7, pp. 543-555, 2005.
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.
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.
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.
25. J. Marin-Garcia and M. J. Goldenthal, "The mitochondrial organelle and the heart, " Revista Espanola de Cardiologa, vol. 55, no. 12, pp. 1293-1310, 2002.
26. G. Karamanlidis, C. F. Lee, L. Garcia-Menendez, et al., "Mitochondrial complex i deficiency increases protein acetylation and accelerates heart failure, " CellMetabolism, vol. 18, no. 2, pp. 239-250, 2013.
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.
28. R. Acin-Perez, P. Fernand ez-Silva, M. L. Peleato, A. Perez-Martos, and J. A. Enriquez, "Respiratory active mitochondrial supercomplexes, " Molecular Cell, vol. 32, no. 4, pp. 529-539, 2008.
29. R. Acin-Perez and J. A. Enriquez, "The function of the respiratory supercomplexes: the plasticity model, " Biochimicaet Biophysica Acta: Bioenergetics, vol. 1837, no. 4, pp. 444-450, 2014.
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.
31. J. D. Wikstrom, K. Mahdaviani, M. Liesa, et al., "Hormoneinduced mitochondrial fission is utilized by brown adipocytes as an amplification pathway for energy expenditure, "TheEMBO Journal, vol. 33, no. 5, pp. 418-436, 2014.
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.
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.
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.
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 ComparativePhysiology, vol. 304, no. 6, pp. R393-R406, 2013.
36. M. Liesa, M. PalaCn, and A. Zorzano, "Mitochondrial dynamics in mammalian health and disease, " Physiological Reviews, vol. 89, no. 3, pp. 799-845, 2009.
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.
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.
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 Journals usual peer review process, " Applied Physiology, Nutrition, and Metabolism, vol. 34, no. 3, pp. 433-439, 2009.
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.
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.
42. K. Vanhees, L. de Bock, R. W. L. Godschalk, F. J. van Schooten, and S. B. vanWaalwijk van Doorn-Khosrovani, "Prenatal exposure to flavonoids: implication for cancer risk, " Toxicological Sciences, vol. 120, no. 1, pp. 59-67, 2011.
43. A. M. Sabogal-Guaqueta, J. I. Munoz-Manco, J. R. Ramirez-Pineda, M. Lamprea-Rodriguez, E. Osorio, and G. P. Cardona-Gomez, "The flavonoid quercetin ameliorates Alzheimers disease pathology and protects cognitive and emotional function in aged triple transgenic Alzheimers disease model mice, " Neuropharmacology, vol. 93, pp. 134-145, 2015.
44. P. Galindo, S. Gonzalez-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.
45. E. Schultke, R. W. Griebel, and B. H. J. Juurlink, "Quercetin administration after spinal cord trauma changes S-100β levels, " Canadian Journal ofNeurological Sciences, vol. 37, no. 2, pp. 223-228, 2010.
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.
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.
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.
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.
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.
51. R. M. J. Deacon, "Measuring the strength of mice, " Journal of Visualized Experiments, no. 76, p. e2610, 2013.
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.
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.
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.
55. L. I. Grad and B. D. Lemire, "Riboflavin enhances the assembly of mitochondrial cytochrome c oxidase in C. elegans NADHubiquinone oxidoreductase mutants, " Biochimicaet Biophysica Acta: Bioenergetics, vol. 1757, no. 2, pp. 115-122, 2006.
56. I. Wittig, R. Carrozzo, F. M. Santorelli, and H. Schagger, "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.
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.
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.
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.
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.
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.
62. N. E. Hellman and J. D. Gitlin, "Ceruloplasmin metabolism and function, " Annual Review of Nutrition, vol. 22, pp. 439-458, 2002.
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, "TheJournal ofNeuroscience, vol. 22, no. 15, pp. 6578-6586, 2002.
64. A. Raghavan, T. Sheiko, B. H. Graham, and W. J. Craigen, "Voltage-dependant anion channels: novel insights into isoform function through genetic models, " Biochimicaet Biophysica Acta: Biomembranes, vol. 1818, no. 6, pp. 1477-1485, 2012.
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.
66. M. M. Baccan, O. Chiarelli-Neto, R. M. S. Pereira, and B. P. Esposito, "Quercetin as a shuttle for labile iron, " Journal of Inorganic Biochemistry, vol. 107, no. 1, pp. 34-39, 2012.
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, " Biochimicaet Biophysica Acta-Bioenergetics, vol. 1556, no. 2-3, pp. 187-196, 2002.
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.
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.
70. S. A. Bakheet, "Assessment of anti-cytogenotoxic effects of quercetin in animals treated with topotecan, " Oxidative Medicine and Cellular Longevity, vol. 2011, Article ID824597, 8 pages, 2011.
71. A. Pekal, 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.
72. A. C. Mot, 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.
73. G. Galati, O. Sabzevari, J. X. Wilson, and P. J. OBrien, "Prooxidant activity and cellular effects of the phenoxyl radicals of dietary flavonoids and other polyphenolics, " Toxicology, vol. 177, no. 1, pp. 91-104, 2002.
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.
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.