Skip to main content
SpringerLink
Log in

Effects of oral administration of common antioxidant supplements on the energy metabolism of red blood cells. Attenuation of oxidative stress-induced changes in Rett syndrome erythrocytes by CoQ10

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Nutritional supplements are traditionally employed for overall health and for managing some health conditions, although controversies are found concerning the role of antioxidants‐mediated benefits in vivo. Consistently with its critical role in systemic redox buffering, red blood cell (RBC) is recognized as a biologically relevant target to investigate the effects of oxidative stress. In RBC, reduction of the ATP levels and adenylate energy charge brings to disturbance in intracellular redox status. In the present work, several popular antioxidant supplements were orally administrated to healthy adults and examined for their ability to induce changes on the energy metabolism and oxidative status in RBC. Fifteen volunteers (3 per group) were treated for 30 days per os with epigallocatechin gallate (EGCG) (1 g green tea extract containing 50% EGCG), resveratrol (325 mg), coenzyme Q10 (CoQ10) (300 mg), vitamin C (1 g), and vitamin E (400 U.I.). Changes in the cellular levels of high-energy compounds (i.e., ATP and its catabolites, NAD and GTP), GSH, GSSG, and malondialdehyde (MDA) were simultaneously analyzed by ion-pairing HPLC. Response to oxidative stress was further investigated through the oxygen radical absorptive capacity (ORAC) assay. According to our experimental approach, (i) CoQ10 appeared to be the most effective antioxidant inducing a high increase in ATP/ADP, ATP/AMP, GSH/GSSG ratio and ORAC value and, in turn, a reduction of NAD concentration, (ii) EGCG modestly modulated the intracellular energy charge potential, while (iii) Vitamin E, vitamin C, and resveratrol exhibited very weak effects. Given that, the antioxidant potential of CoQ10 was additionally assessed in a pilot study which considered individuals suffering from Rett syndrome (RTT), a severe X-linked neuro-developmental disorder in which RBC oxidative damages provide biological markers for redox imbalance and chronic hypoxemia. RTT patients (n = 11), with the typical clinical form, were supplemented for 12 months with CoQ10 (300 mg, once daily). Level of lipid peroxidation (MDA production) and energy state of RBCs were analyzed at 2 and 12 months. Our data suggest that CoQ10 may significantly attenuate the oxidative stress-induced damage in RTT erythrocytes.

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

Access this article

Log in via an institution

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
Fig. 5

Similar content being viewed by others

References

  1. Dandekar A, Mendez R, Zhang K (2015) Cross talk between er stress, oxidative stress, and inflammation in health and disease. Methods Mol Biol 1292:205–214. https://doi.org/10.1007/978-1-4939-2522-3_15

    Article  CAS  PubMed  Google Scholar 

  2. Pizzino G, Irrera N, Cucinotta M, Pallio G, Mannino F, Arcoraci V, Squadrito F, Altavilla D, Bitto A (2017) Oxidative stress: harms and benefits for human health, oxidative medicine and cellular longevity. Oxid Med Cell Longev 2017:8416763. https://doi.org/10.1155/2017/8416763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Jackson MJ (1999) An overview of methods for assessment of free radical activity in biology. Proc Nutr Soc 58:1001–1006. https://doi.org/10.1017/S0029665199001317

    Article  CAS  PubMed  Google Scholar 

  4. Fraga CG, Oteiza PI, Galleano M (2014) In vitro measurements and interpretation of total antioxidant capacity. Biochim Biophys Acta 1840:931–934. https://doi.org/10.1016/j.bbagen.2013.06.030

    Article  CAS  PubMed  Google Scholar 

  5. López-Alarcón C, Denicola A (2013) Evaluating the antioxidant capacity of natural products: a review on chemical and cellular-based assays. Anal Chim Acta 763:1–10. https://doi.org/10.1016/j.aca.2012.11.051

    Article  CAS  PubMed  Google Scholar 

  6. Niki E (2010) Assessment of antioxidant capacity in vitro and in vivo. Free Radic Biol Med 49:503–515. https://doi.org/10.1016/j.freeradbiomed.2010.04.016

    Article  CAS  PubMed  Google Scholar 

  7. Carocho M, Ferreira IC (2013) A review on antioxidants, prooxidants and related controversy: natural and synthetic compounds, screening and analysis methodologies and future perspectives. Food and Chemical Toxicology 51:15–25. https://doi.org/10.1016/j.fct.2012.09.021

    Article  CAS  PubMed  Google Scholar 

  8. Pandey KB, Rizvi SI (2010) Markers of oxidative stress in erythrocytes and plasma during aging in humans. Oxid Med Cell Longev 3:2–12. https://doi.org/10.4161/oxim.3.1.10476

    Article  PubMed  PubMed Central  Google Scholar 

  9. Rodríguez J, Di Pierro D, Gioia M, Monaco S, Delgado R, Coletta M, Marini S (2006) Effects of a natural extract from Mangifera indica L, and its active compound, mangiferin, on energy state and lipid peroxidation of red blood cells. Biochim Biophys Acta 1760:1333–1342. https://doi.org/10.1016/j.bbagen.2006.04.005

    Article  CAS  PubMed  Google Scholar 

  10. Arbos KA, Claro LM, Borges L, Santos CA, Weffort-Santos AM (2008) Human erythrocytes as a system for evaluating the antioxidant capacity of vegetable extracts. Nutr Res 28:457–463. https://doi.org/10.1016/j.nutres.2008.04.004

    Article  CAS  PubMed  Google Scholar 

  11. Alvarez-Suarez JM, Giampieri F, González-Paramás AM, Damiani E, Astolfi P, Martinez-Sanchez G, Bompadre S, Quiles JL, Santos-Buelga C, Battino M (2012) Phenolics from monofloral honeys protect human erythrocyte membranes against oxidative damage. Food Chem Toxicol 50:1508–1516. https://doi.org/10.1016/j.fct.2012.01.042

    Article  CAS  PubMed  Google Scholar 

  12. Kosenko EA, Aliev G, Tikhonova LA, Li Y, Poghosyan AC, Kaminsky YG (2012) Antioxidant status and energy state of erythrocytes in Alzheimer dementia: probing for markers. CNS Neurol Disord 11:926–932. https://doi.org/10.1007/978-3-642-30018-9_202

    Article  CAS  Google Scholar 

  13. Della Rovere F, Granata A, Broccio M, Zirilli A, Broccio G (1995) Hemoglobin oxidative stress in cancer. Anticancer Res 15:2089–2095

    CAS  PubMed  Google Scholar 

  14. Chakraborty D, Bhattacharyya M (2001) Antioxidant defense status of red blood cells of patients with beta-thalassemia and Ebeta-thalassemia. Clin Chim Acta 305:123–129. https://doi.org/10.1016/S0009-8981(00)00428-9

    Article  CAS  PubMed  Google Scholar 

  15. Mohanty JG, Nagababu E, Rifkind JM (2014) Red blood cell oxidative stress impairs oxygen delivery and induces red blood cell aging. Front Physiol. 5:84. https://doi.org/10.3389/fphys.2014.00084

    Article  PubMed  PubMed Central  Google Scholar 

  16. Kuhn V, Diederich L, Keller STC IV, Kramer CM, Lückstädt W, Panknin C, Suvorava T, Isakson BE, Kelm M, Cortese-Krott MM (2017) Red blood cell function and dysfunction: redox regulation, nitric oxide metabolism, Anemia. Antioxid Redox Signal 26:718–742. https://doi.org/10.1089/ars.2016.6954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Kennett EC, Kuchel PW (2003) Redox reactions and electron transfer across the red cell membrane. IUBMB Life 55:375–385. https://doi.org/10.1080/15216540310001592843

    Article  CAS  PubMed  Google Scholar 

  18. Buehler P, Alayash AI (2005) Redox biology of blood revisited: the role of red blood cells in maintaining circulatory reductive capacity. Antioxid Redox Signaling 7:1755–1760. https://doi.org/10.1089/ars.2005.7.1755

    Article  CAS  Google Scholar 

  19. Agalakova NI, Gusev GP (2012) Fluoride induces oxidative stress and ATP depletion in the rat erythrocytes in vitro. Environ Toxicol Pharmacol. 34:334–337. https://doi.org/10.1016/j.etap.2012.05.006

    Article  CAS  PubMed  Google Scholar 

  20. Tavazzi B, Di Pierro D, Amorini AM, Fazzina G, Tuttobene M, Giardina B, Lazzarino G (2000) Energy metabolism and lipid peroxidation of human erythrocytes as a function of increased oxidative stress. Eur J Biochem 267:684–689. https://doi.org/10.1046/j.1432-1327.2000.01042.x

    Article  CAS  PubMed  Google Scholar 

  21. Tavazzi B, Amorini AM, Fazzina G, Di Pierro D, Tuttobene M, Giardina B, Lazzarino G (2001) Oxidative stress induces impairment of human erythrocyte energy metabolism through the oxygen radical-mediated direct activation of AMP-deaminase. J Biol Chem 276:48083–48092. https://doi.org/10.1074/jbc.M101715200

    Article  CAS  PubMed  Google Scholar 

  22. Lazzarino G, Di Pierro D, Tavazzi B, Cerroni L, Giardina B (1991) Simultaneous separation of malondialdehyde, ascorbic acid and adenite nucleotide derivatives from biological samples by ion pairing high- performance liquid chromatography. Anal. Biochem. 19:191–196. https://doi.org/10.1016/0003-2697(91)90378-7

    Article  Google Scholar 

  23. Di Pierro D, Tavazzi B, Perno CP, Bartolini M, Balestra E, Calio R, Giardina B, Lazzarino G (1995) An ion pairing high performance liquid chromatography method for the simulateneous determination of Nucleotides, deoxynucleotides, nicotinic coenzymes, oxypurines, nucleosides and bases. Anal Biochem 231:407–412. https://doi.org/10.1006/abio.1995.0071

    Article  PubMed  Google Scholar 

  24. Cao G, Alessio HM, Cutler RG (1993) Oxygen-radical absorbance capacity assay for antioxidants. Free Radic Biol Med 14:303–331. https://doi.org/10.1016/0891-5849(93)90027-R

    Article  CAS  PubMed  Google Scholar 

  25. Ciccoli L, De Felice C, Paccagnini E, Leoncini S, Pecorelli A, Signorini C, Belmonte G, Valacchi G, Rossi M, Hayek J (2012) Morphological changes and oxidative damage in Rett Syndrome erythrocytes. Biochim Biophys Acta. 1820:511–520. https://doi.org/10.1016/j.bbagen.2011.12.002

    Article  CAS  PubMed  Google Scholar 

  26. De Felice C, Signorini C, Leoncini S, Pecorelli A, Durand T, Valacchi G, Ciccoli L, Hayek J (2012) The role of oxidative stress in Rett syndrome: an overview. Ann N Y Acad Sci 1259:121–135. https://doi.org/10.1111/j.1749-6632.2012.06611.x

    Article  CAS  PubMed  Google Scholar 

  27. De Felice C, Della Ragione F, Signorini C, Leoncini S, Pecorelli A et al (2014) Oxidative brain damage in Mecp2-mutant murine models of Rett syndrome. Neurobiol Dis 68:66–77. https://doi.org/10.1016/j.nbd.2014.04.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY (1999) Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23:185–188. https://doi.org/10.1038/13810

    Article  CAS  PubMed  Google Scholar 

  29. Ciaccio C, Di Pierro D, Sbardella D, Tundo GR, Curatolo P, Galasso C et al (2017) Oxygen exchange and energy metabolism in erythrocytes of Rett syndrome and their relationships with respiratory alterations. Mol Cell Biochem 426:205–213. https://doi.org/10.1007/s11010-016-2893-9

    Article  CAS  PubMed  Google Scholar 

  30. Sbardella D, Tundo GR, Campagnolo L, Valacchi G, Orlandi A, Curatolo P, Borsellino G, D’Esposito M, Ciaccio C, Cesare SD, Pierro DD, Galasso C, Santarone ME, Hayek J, Coletta M, Marini S (2017) Retention of mitochondria in mature human red blood cells as the result of autophagy impairment in rett syndrome. Sci Rep 7:12297. https://doi.org/10.1038/s41598-017-12069-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Neul JL, Kaufmann WE, Glaze DG, Christodoulou J, Clarke AJ, Bahi-Buisson N, Leonard H, Bailey ME, Schanen NC, Zappella M, Renieri A, Huppke P, Percy AK (2010) Rett syndrome: recise diagnostic criteria and nomenclature. Ann. Neurol 68:944–950. https://doi.org/10.1002/ana.22124

    Article  PubMed  PubMed Central  Google Scholar 

  32. Atkinson DE (1968) The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry. 7:4030–4034. https://doi.org/10.1021/bi00851a033

    Article  CAS  PubMed  Google Scholar 

  33. Amorini AM, Lazzarino G, Galvano F, Fazzina G, Tavazzi B, Galvano G (2003) Cyanidin-3-O-β-glucopyranoside protects myocardium and erythrocytes from oxygen radical-mediated damages. Free Radic Res. 37:453–460. https://doi.org/10.1080/1071576021000055253

    Article  CAS  PubMed  Google Scholar 

  34. Littarru GP, Tiano L (2007) Bioenergetic and antioxidant properties of coenzyme Q10: recent developments. Mol Biotechnol 37:31–37. https://doi.org/10.1007/s12033-007-0052-y

    Article  CAS  PubMed  Google Scholar 

  35. Kalèn A, Norling B, Appelkvist EL, Dallner G (1987) Ubiquinone synthesis in the microsomal fraction of rat liver. Biochim Biophys Acta 926:70–78. https://doi.org/10.1016/0304-4165(87)90183-8

    Article  PubMed  Google Scholar 

  36. Forsmark-Andrée P, Ernster L (1994) Evidence for a protective effect of endogenous ubiquinol against oxidative damage to mitochondrial protein and DNA during lipid peroxidation. Mol Aspects Med 15:73–81. https://doi.org/10.1016/0098-2997(94)90015-9

    Article  Google Scholar 

  37. Littarru GP, Battino M, Tomasetti M, Mordente A, Santini S, Oradei A, Manto A, Ghirlanda G (1994) Metabolic implications of coenzyme Q10 in red blood cells and plasma lipoproteins. Mol Aspects Med 15:67–72. https://doi.org/10.1016/0098-2997(94)90014-0

    Article  Google Scholar 

  38. Stocker R, Suarna C (1993) Extracellular reduction of ubiquinone-1 and -10 by human Hep G2 and blood cells. Biochim Biophys Acta 1158:15–22

    Article  CAS  Google Scholar 

  39. Garrido-Maraver J, Cordero MD, Oropesa-Avila M, Oropesa-Avila M, Vega AF, de la Mata M, Pavon AD, Alcocer-Gomez E, Calero CP, Paz MV et al (2014) Clinical applications of coenzyme Q10. Front Biosci 19:619–633

    Article  CAS  Google Scholar 

  40. Acosta MJ, Vazquez Fonseca L, Desbats MA, Cerqua C, Zordan R, Trevisson E, Salviati L (2016) Coenzyme Q biosynthesis in health and disease. Biochim Biophys Acta 1857:1079–1085. https://doi.org/10.1016/j.bbabio.2016.03.036

    Article  CAS  PubMed  Google Scholar 

  41. Niklowitz P, Sonnenschein A, Janetzky B, Andler W, Menke T (2007) Enrichment of coenzyme Q10 in plasma and blood cells: defense against oxidative damage. Int J Biol Sci 3:257–262. https://doi.org/10.7150/ijbs.3.257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Littarru GP, Tiano L (2007) Bioenergetic and antioxidant properties of coenzyme Q10: recent developments. Mol Biotechnol 37:31–37. https://doi.org/10.1007/s12033-007-0052-y

    Article  CAS  PubMed  Google Scholar 

  43. Niklowitz P, Menke T, Andler W, Okun JG (2004) Simultaneous analysis of coenzyme Q10 in plasma, erythrocytes and platelets: comparison of the antioxidant level in blood cells and their environment in healthy children and after oral supplementation in adults. Clin Chim Acta. 342:219–226. https://doi.org/10.1016/j.cccn.2003.12.020

    Article  CAS  PubMed  Google Scholar 

  44. Niki E (2014) Role of vitamin E as a lipid-soluble peroxyl radical scavenger: in vitro and in vivo evidence. Free Radic Biol Med 66:3–12. https://doi.org/10.1016/j.freeradbiomed.2013.03.022

    Article  CAS  PubMed  Google Scholar 

  45. May JM, Qu ZC, Mendiratta S (1998) Protection and recycling of a-tocopherol in human erythrocytes by intracellular ascorbic acid. Arch Biochem Biophys 349:281–289. https://doi.org/10.1006/abbi.1997.0473

    Article  CAS  PubMed  Google Scholar 

  46. Armutcu F, Coskun O, Gürel A, Sahin S, Kanter M, Cihan A, Numanoglu KV, Altinyazar C (2005) Vitamin E protects against acetone-induced oxidative stress in rat red blood cells. Cell Biol Toxicol 21:53–60. https://doi.org/10.1007/s10565-005-1781-y

    Article  CAS  PubMed  Google Scholar 

  47. Tesoriere L, D’Arpa D, Butera D, Allegra M, Renda D, Maggio A, Bongiorno A, Livrea MA (2001) Oral supplements of vitamin E improve measures of oxidative stress in plasma and reduce oxidative damage to LDL and erythrocytes in beta-thalassemia intermedia patients. Free Radic Res 34:529–540. https://doi.org/10.1080/10715760100300461

    Article  CAS  PubMed  Google Scholar 

  48. Vrolijk MF, Opperhuizen A, Jansen EH, Godschalk RW, Van Schooten FJ, Bast A, Haenen GR (2015) The shifting perception on antioxidants: the case of vitamin E and β-carotene. Redox Biol 4:272–478. https://doi.org/10.1016/j.redox.2014.12.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Nakamura YK, Omaye ST (2009) Vitamin E-modulated gene expression associated with ROS generation. J Funct Foods 1:241–252. https://doi.org/10.1016/j.jff.2009.02.002

    Article  CAS  Google Scholar 

  50. Rigotti A (2007) Absorption, transport, and tissue delivery of vitamin E. Mol Aspects Med 2:423–436. https://doi.org/10.1016/j.mam.2007.01.002

    Article  CAS  Google Scholar 

  51. Saito Y, Fukuhara A, Nishio K, Hayakawa M, Ogawa Y, Sakamoto H, Fujii K, Yoshida Y, Niki E (2009) Characterization of cellular uptake and distribution of coenzyme Q10 and vitamin E in PC12 cells. J Nutr Biochem 20:350–357. https://doi.org/10.1016/j.jnutbio.2008.04.005

    Article  CAS  PubMed  Google Scholar 

  52. Tu H, Li H, Wang Y, Niyyati M, Wang Y, Leshin J, Levine M (2015) Low red blood cell vitamin C concentrations induce red blood cell fragility: a link to diabetes via glucose, glucose transporters, and dehydroascorbic acid. EBioMedicine 2:1735–1750. https://doi.org/10.1016/j.ebiom.2015.09.049

    Article  PubMed  PubMed Central  Google Scholar 

  53. Traber MG, Stevens JF (2011) Vitamins C and E: beneficial effects from a mechanistic perspective. Free Radic. Biol Med. 51:1000–1013. https://doi.org/10.1016/j.freeradbiomed.2011.05.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Johnston CS, Meyer CG, Srilakshmi JC (1993) Vitamin C elevates red blood cell glutathione in healthy adults. Am J Clin Nutr 58:103–105. https://doi.org/10.1093/ajcn/58.1.103

    Article  CAS  PubMed  Google Scholar 

  55. Park EJ, Pezzuto JM (2015) The pharmacology of resveratrol in animals and humans. Biochim Biophys Acta 1852:1071–1113. https://doi.org/10.1016/j.bbadis.2015.01.014

    Article  CAS  PubMed  Google Scholar 

  56. Xia N, Forstermann U, Li H (2014) Resveratrol as a gene regulator in the vasculature. Curr Pharm Biotechnol 15:401–408. https://doi.org/10.2174/1389201015666140711114450

    Article  CAS  PubMed  Google Scholar 

  57. Pandey KB, Rizvi SI (2010) Protective effect of resveratrol on markers of oxidative stress in human erythrocytes subjected to in vitro oxidative insult. Phytother Res 24:11–14. https://doi.org/10.1002/ptr.2853

    Article  Google Scholar 

  58. Berman AY, Motechin RA, Wiesenfeld MY, Holz MK (2017) The therapeutic potential of resveratrol: a review of clinical trials. NPJ Precis Oncol 1:35. https://doi.org/10.1038/s41698-017-0038-6

    Article  PubMed  PubMed Central  Google Scholar 

  59. Jigisha A, Nishant R, Navin K, Pankaj G (2012) Green tea: a magical herb with miraculous outcomes. Int Res J Pharm 3:139–148

    Google Scholar 

  60. Farzaei MH, Bahramsoltani R, Abbasabadi Z, Braidy N, Nabavi SM (2019) Role of green tea catechins in prevention of age-related cognitive decline: pharmacological targets and clinical perspective. J Cell Physiol 234:2447–2459. https://doi.org/10.1002/jcp.27289

    Article  CAS  PubMed  Google Scholar 

  61. Zaveri NT (2006) Green tea and its polyphenolic catechins: medicinal uses in cancer and noncancer applications. Life Sci 78:2073–2080. https://doi.org/10.1016/j.lfs.2005.12.006

    Article  CAS  PubMed  Google Scholar 

  62. Saffari Y, Sadrzadeh SM (2004) Green tea metabolite EGCG protects membranes against oxidative damage in vitro. Life Sci 74:1513–1518. https://doi.org/10.1016/j.lfs.2003.08.019

    Article  CAS  PubMed  Google Scholar 

  63. Kim HS, Quon MJ, Kim JA (2014) New insights into the mechanisms of polyphenols beyond antioxidant properties; lessons from the green tea polyphenol, epigallocatechin 3-gallate. Redox Biol 2:187–195. https://doi.org/10.1016/j.redox.2013.12.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Bernatoniene J, Kopustinskiene DM (2018) The role of catechins in cellular responses to oxidative stress. Molecules 23(4):965. https://doi.org/10.3390/molecules23040965

    Article  CAS  PubMed Central  Google Scholar 

  65. Mereles D, Hunstein W (2011) Epigallocatechin-3-gallate (EGCG) for clinical trials: more pitfalls than promises? Int J Mol Sci 12:5592. https://doi.org/10.3390/ijms12095592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Ciccoli L, De Felice C, Leoncini S, Signorini C, Cortelazzo A et al (2015) Red blood cells in Rett syndrome: oxidative stress, morphological changes and altered membrane organization. Biol Chem 396:1233–1240. https://doi.org/10.1515/hsz-2015-0117

    Article  CAS  PubMed  Google Scholar 

  67. Sierra C, Vilaseca MA, Brandi N, Artuch R, Mira A et al (2001) Oxidative stress in Rett syndrome. Brain Dev 23:S236–S239. https://doi.org/10.1016/S0387-7604(01)00369-2

    Article  PubMed  Google Scholar 

  68. Maffei S, De Felice C, Cannarile P, Leoncini S, Signorini C, Pecorelli A, Montomoli B, Lunghetti S, Ciccoli L, Durand T, Favilli R, Hayek J (2014) Effects of ω-3 PUFAs supplementation on myocardial function and oxidative stress markers in typical Rett syndrome. Mediat Inflamm. https://doi.org/10.1155/2014/983178

    Article  Google Scholar 

  69. De Felice C, Signorini C, Durand T, Ciccoli L, Leoncini S, D’Esposito M, Filosa S, Oger C, Guy A, Bultel-Poncé V, Galano JM, Pecorelli A, De Felice L, Valacchi G, Hayek J (2012) Partial rescue of Rett syndrome by ω-3 polyunsaturated fatty acids (PUFAs) oil. Genes Nutr 7:447–458. https://doi.org/10.1007/s12263-012-0285-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Mancuso M, Orsucci D, Calsolaro V, Choub A, Siciliano G (2009) Coenzyme Q10 and neurological diseases. Pharmaceuticals (Basel) 2(3):134–149. https://doi.org/10.3390/ph203134

    Article  CAS  Google Scholar 

  71. Gold WA, Williamson SL, Kaur S, Hargreaves IP, Land JM, Pelka GJ, Tam PP, Christodoulou J (2014) Mitochondrial dysfunction in the skeletal muscle of a mouse model of Rett syndrome (RTT): implications for the disease phenotype. Mitochondrion 15:10–17. https://doi.org/10.1016/j.mito.2014.02.012

    Article  CAS  PubMed  Google Scholar 

  72. Cervellati C, Sticozzi C, Romani A, Belmonte G, De Rasmo D, Signorile A, Cervellati F, Milanese C, Mastroberardino PG, Pecorelli A, Savelli V, Forman HJ, Hayek J (1852) Valacchi G (2015) Impaired enzymatic defensive activity, mitochondrial dysfunction and proteasome activation are involved in RTT cell oxidative damage. Biochim Biophys Acta 10:2066–2074. https://doi.org/10.1016/j.bbadis.2015.07.014

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The Grant of MIUR (Legge 232/2016, Articolo 1, Comma 314-337) is gratefully acknowledged.

Author information

Author notes

  1. Donato Di Pierro and Chiara Ciaccio have contributed equally to this work.

Authors and Affiliations

  1. Department of Clinical Sciences and Translational Medicine, University of Rome Tor Vergata, Rome, Italy

    Donato Di Pierro, Chiara Ciaccio, Diego Sbardella, Grazia Raffaella Tundo, Massimiliano Coletta & Stefano Marini

  2. Centro di Servizi Interdipartimentale - STA, University of Rome Tor Vergata, Rome, Italy

    Roberta Bernardini

  3. Department of Systems Medicine, Division of Child Neurology and Psychiatry, University of Rome Tor Vergata, Rome, Italy

    Paolo Curatolo, Cinzia Galasso & Virginia Pironi

Authors
  1. Donato Di Pierro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chiara Ciaccio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Diego Sbardella
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Grazia Raffaella Tundo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Roberta Bernardini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Paolo Curatolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cinzia Galasso
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Virginia Pironi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Massimiliano Coletta
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Stefano Marini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stefano Marini.

Ethics declarations

Conflict of interest

The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Di Pierro, D., Ciaccio, C., Sbardella, D. et al. Effects of oral administration of common antioxidant supplements on the energy metabolism of red blood cells. Attenuation of oxidative stress-induced changes in Rett syndrome erythrocytes by CoQ10. Mol Cell Biochem 463, 101–113 (2020). https://doi.org/10.1007/s11010-019-03633-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-019-03633-5

Keywords

Search

Navigation