Partial rescue of Rett syndrome by ω-3 polyunsaturated fatty acids (PUFAs) oil

Genes and Nutrition

Volumn 7, Issue 3, 2012, Pages 447-458

  De Felice, Claudio ^a   Signorini, Cinzia ^b   Durand, Thierry ^c   Ciccoli, Lucia ^b   Leoncini, Silvia ^b   D'Esposito, Maurizio ^d,e   Filosa, Stefania ^d,e   Oger, Camille ^c   Guy, Alexandre ^c   Bultel Poncé, Valérie ^c   Galano, Jean Marie ^c   Pecorelli, Alessandra ^c   De Felice, Laura ^f   Valacchi, Giuseppe ^g,h   Hayek, Joussef ^a  

^a UNIVERSITY HOSPITAL OF SIENA   (Italy)

^b UNIVERSITY OF SIENA   (Italy)

^c UNIVERSITÉ DE MONTPELLIER   (France)

^d INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^e IRCCS NEUROMED   (Italy)

^f UNIVERSITY OF FLORENCE   (Italy)

^g UNIVERSITY OF FERRARA   (Italy)

^h Kyung Hee University   (South Korea)

Author keywords

3 polyunsaturated fatty acids; Antioxidants; Isoprostanes; MeCP2; Nonprotein bound iron; Oxidative Stress; Rett syndrome

Indexed keywords

FISH OIL; OMEGA 3 FATTY ACID;

ARTICLE; CLINICAL ARTICLE; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; DIET SUPPLEMENTATION; DISEASE COURSE; DISEASE SEVERITY; FEMALE; HUMAN; LIPID PEROXIDATION; OXIDATIVE STRESS; RANDOMIZED CONTROLLED TRIAL; RETT SYNDROME; THERAPY EFFECT; TREATMENT OUTCOME; TREATMENT RESPONSE;

EID: 84866006373     PISSN: 15558932     EISSN: 18653499     Source Type: Journal    
DOI: 10.1007/s12263-012-0285-7     Document Type: Article

References (86)

1. 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 (Pubitemid 29455390)
2. Anderson BM, Ma DWL (2009) Are all n-3 polyunsaturated fatty acids created equal? Lipids Health Dis 8:33
3. Ariani F, Hayek G, Rondinella D, Artuso R, Mencarelli MA, Spanhol-Rosseto A, Pollazzon M, Buoni S, Spiga O, Ricciardi S, Meloni I, Longo I, Mari F, Broccoli V, Zappella M, Renieri A (2008) FOXG1 is responsible for the congenital variant of Rett syndrome. Am J Hum Genet 83:89-93
4. Arnold C, Markovic M, Blossey K, Wallukat G, Fischer R, Dechend R, Konkel A, von Schacky C, Luft FC, Muller DN, Rothe M, Schunck WH (2010) Arachidonic acid-metabolizing cytochrome P450 enzymes are targets of 3 fatty acids. J Biol Chem285:32720-32733
5. Ballas N, Lioy DT, Grunseich C, Mandel G (2009) Non-cell autonomous influence of MeCP2-deficient glia on neuronal dendritic morphology. Nat Neurosci 12:311-317
6. Bazan NG (2007) Omega-3 fatty acids, pro-inflammatory signaling and neuroprotection. Curr Opin Clin Nutr Metab Care 10:136-141 (Pubitemid 46220304)
7. Belayev L, Marcheselli VL, Khoutorova L, Rodriguez de Turco EB, Busto R, Ginsberg MD, Bazan NG (2005) Docosahexaenoic acid complexed to albumin elicits high-grade ischemic neuroprotection. Stroke 36:118-123 (Pubitemid 40054186)
8. Belayev L, Khoutorova L, Atkins KD, Bazan NG (2009) Robust docosahexaenoic acid-mediated neuroprotection in a rat model of transient, focal cerebral ischemia. Stroke 40:3121-3126
9. Ben-Shachar S, Chahrour M, Thaller C, Shaw CA, Zoghbi HY (2009) Mouse models of MeCP2 disorders share gene expression changes in the cerebellum and hypothalamus. Hum Mol Genet 18:2431-2442
10. Calder PC (2006) n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 83:1505S-1519S (Pubitemid 44713092)
11. Calder PC, Yaqoob P (2009) Understanding omega-3 polyunsaturated fatty acids. Postgrad Med 121:148-157
12. Cappa M, Bizzarri C, Vollono C, Petroni A, Banni S (2011) Adrenoleukodystrophy. Endocr Dev 20:149-160
13. Chahrour M, Zoghbi HY (2007) The story of Rett syndrome: from clinic to neurobiology. Neuron 56:422-437 (Pubitemid 350026269)
14. Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST, Qin J, Zoghbi HY (2008) MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320:1224-1229 (Pubitemid 351929512)
15. Chang CY, Ke DS, Chen JY (2009) Essential fatty acids and human brain. Acta Neurol Taiwan 18:231-241
16. Chao HT, Chen H, Samaco RC, Xue M, Chahrour M, Yoo J, Neul JL, Gong S, Lu HC, Heintz N, Ekker M, Rubenstein JL, Noebels JL, Rosenmund C, Zoghbi HY (2010) Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 468:263-269
17. Chapkin RS, McMurray DN, Davidso LA, Patil BS, Fan YY, Lupton JR (2008) Bioactive dietary long-chain fatty acids: emerging mechanisms of action. Br J Nutr 100:1152-1157
18. Chen J, Chua KW, Chua CC, Yu H, Pei A, Chua BH, Hamdy RC, Xu X, Liu CF (2011) Antioxidant activity of 7,8-dihydroxyflavone provides neuroprotection against glutamate-induced toxicity. Neurosci Lett 499:181-185
19. Cobb S, Guy J, Bird A (2010) Reversibility of functional deficits in experimental models of Rett syndrome. Biochem Soc Trans 38:498-506
20. Collins AL, Levenson JM, Vilaythong AP, Richman R, Armstrong DL, Noebels JL, David Sweatt J, Zoghbi HY (2004) Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum Mol Genet 13:2679-2689 (Pubitemid 39485416)
21. Comporti M, Signorini C, Buonocore G, Ciccoli L (2002) Iron release, oxidative stress and erythrocyte ageing. Free Radic Biol Med 32:568-576 (Pubitemid 34241489)
22. Comporti M, Signorini C, Arezzini B, Vecchio D, Monaco B, Gardi C (2008) F2-isoprostanes are not just markers of oxidative stress. Free Radic Biol Med 44:247-256
23. de Assis AM, Rech A, Longoni A, Rotta LN, Denardin CC, Pasquali MA, Souza DO, Perry ML, Moreira JC (2012) X3-Polyunsaturated fatty acids prevent lipoperoxidation, modulate antioxidant enzymes, and reduce lipid content but do not alter glycogen metabolism in the livers of diabetic rats fed on a high fat thermolyzed diet. Mol Cell Biochem 361:151-160
24. De Felice C, Ciccoli L, Leoncini S, Signorini C, Rossi M, Vannuccini L, Guazzi G, Latini G, Comporti M, Valacchi G, Hayek J (2009) Systemic oxidative stress in classic Rett syndrome. Free Radic Biol Med 47:440-448
25. De Felice C, Signorini C, Durand T, Oger C, Guy A, Bultel-Poncé V, Galano JM, Ciccoli L, Leoncini S, D'Esposito M, Filosa S, Pecorelli A, Valacchi G, Hayek J (2011) F2-dihomo-isoprostanes as potential early biomarkers of lipid oxidative damage in Rett syndrome. J Lipid Res 52:2287-2297
26. Deckelbaum RJ, Worgall TS, Seo T (2006) n-3 fatty acids and gene expression. Am J Clin Nutr 83:1520S-1525S (Pubitemid 44713093)
27. El-Ansary AK, Al-Daihan SK, El-Gezeery AR (2011) On the protective effect of omega-3 against propionic acid-induced neurotoxicity in rat pups. Lipids Health Dis 10:142
28. Fourcade S, López-Erauskin J, Galino J, Duval C, Naudi A, Jove M, Kemp S, Villarroya F, Ferrer I, Pamplona R, Portero-Otin M, Pujol A (2008) Early oxidative damage underlying neurodegeneration in X- adrenoleukodystrophy. Hum Mol Genet 17:1762-1773 (Pubitemid 351791502)
29. Galino J, Ruiz M, Fourcade S, Schlüter A, López-Erauskin J, Guilera C, Jove M, Naudi A, García-Arumí E, Andreu AL, Starkov AA, Pamplona R, Ferrer I, Portero-Otin M, Pujol A (2011) Oxidative damage compromises energy metabolism in the axonal degeneration mouse model of X-adrenoleukodystrophy. Antioxid Redox Signal 15:2095-2107
30. Gamoh S, Hashimoto M, Sugioka K, Shahdat Hossain M, Hata N, Misawa Y, Masumura S (1999) Chronic administration of docosahexaenoic acid improves reference memory-related learning ability in young rats. Neuroscience 93:237-241 (Pubitemid 29290703)
31. Guy J, Gan J, Selfridge J, Cobb S, Bird A (2007) Reversal of neurological defects in a mouse model of Rett syndrome. Science 315:1143-1147 (Pubitemid 46328028)
32. Guy J, Cheval H, Selfridge J, Bird A (2011) The role of MeCP2 in the brain. Annu Rev Cell Dev Biol 27:631-652
33. Hagberg B, Aicardi J, Dias K, Ramos O (1983) A progressive syndrome of autism, dementia, ataxia, and loss of purposeful hand use in girls: Rett's syndrome: report of 35 cases. Ann Neurol 14:471-479 (Pubitemid 13010048)
34. Halliwell B, Gutteridge J (1999) Free radicals, other reactive species and disease. In: Halliwell B, Gutteridge J (eds) Free radicals in biology and medicine. Clarendon Press, Oxford, pp 617-783
35. Johnson RA, Lam M, Punzo AM, Li H, Lin BR, Ye K, Mitchell GS, Chang Q (2011) 7,8-dihydroxyflavone (7,8-DHF) exhibits therapeutic efficacy in a mouse model of Rett syndrome. J Appl Physiol. doi:10.1152/japplphysiol.01361
36. Jump DB (2002) The biochemistry of n-3 polyunsaturated fatty acids. J Biol Chem 277:8755-8758 (Pubitemid 34952937)
37. Kadiiska MB, Gladen BC, Baird DD, Germolec D, Graham LB, Parker CE, Nyska A, Wachsman JT, Ames BN, Basu S, Brot N, Fitzgerald GA, Floyd RA, George M, Heinecke JW, Hatch GE, Hensley K, Lawson JA, Marnett LJ, Morrow JD, Murray DM, Plastaras J, Roberts LJ, Rokach J, Shigenaga MK, Sohal RS, Sun J, Tice RR, Van Thiel DH, Wellner D, Walter PB, Tomer KB, Mason RP, Barrett JC (2005) Biomarkers of oxidative stress study II: are oxidation products of lipids, proteins, and DNA markers of CCl4 poisoning? Free Radic Biol Med 38:698-710 (Pubitemid 40249740)
38. Kawashima H, Nishimata S, Ishii C, Yamanaka G, Kashiwagi Y, Takekuma K, Hoshika A, Watanabe Y (2011) New treatment of free-radical scavenger in adrenoleukodystrophy. J Clin Pharm Ther 36:412-415
39. Kris-Etherton PM, Harris WS, Appel LJ; American Heart Association. Nutrition Committee (2002) Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 106:2747-2757 (Pubitemid 35364932)
40. Kron M, Müller M (2010) Impaired hippocampal Ca2? homeostasis and concomitant K? channel dysfunction in a mouse model of Rett syndrome during anoxia. Neuroscience 171:300-315
41. Leoncini S, De Felice C, Signorini C, Pecorelli A, Durand T, Valacchi G, Ciccoli L, Hayek J (2011) Oxidative stress in Rett syndrome: natural history, genotype, and variants. Redox Rep 16:145-153
42. Lien EL (2009) Toxicology and safety of DHA. Prostaglandins Leukot Essent Fatty Acids 81:125-132
43. López-Erauskin J, Fourcade S, Galino J, Ruiz M, Schlüter A, Naudi A, Jove M, Portero-Otin M, Pamplona R, Ferrer I, Pujol A (2011) Antioxidants halt axonal degeneration in a mouse model of X- adrenoleukodystrophy. Ann Neurol 70:84-92
44. Macdonald JL, Verster A, Berndt A, Roskams AJ (2010) MBD2 and MeCP2 regulate distinct transitions in the stage-specific differentiation of olfactory receptor neurons. Mol Cell Neurosci 44:55-67
45. Maezawa I, Swanberg S, Harvey D, LaSalle JM, Jin LW (2009) Rett syndrome astrocytes are abnormal and spread MeCP2 deficiency through gap junctions. J Neurosci 29:5051-5061
46. Mahmood A, Bibat G, Zhan AL, Izbudak I, Farage L, Horska A, Mori S, Naidu S (2010) White matter impairment in Rett syndrome: diffusion tensor imaging study with clinical correlations. AJNR Am J Neuroradiol 31:295-299
47. Marchetto MC, Carromeu C, Acab A, Yu D, Yeo GW, Mu Y, Chen G, Gage FH, Muotri AR (2010) A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 143:527-539
48. Mari F, Azimonti S, Bertani I, Bolognese F, Colombo E, Caselli R, Scala E, Longo I, Grosso S, Pescucci C, Ariani F, Hayek G, Balestri P, Bergo A, Badaracco G, Zappella M, Broccoli V, Renieri A, Kilstrup-Nielsen C, Landsberger N (2005) CDKL5 belongs to the same molecular pathway of MeCP2 and it is responsible for the early-onset seizure variant of Rett syndrome. Hum Mol Genet 14:1935-1946 (Pubitemid 41418030)
49. Mas E, Woodman RJ, Burke V, Puddey IB, Beilin LJ, Durand T, Mori TA (2010) The omega-3 fatty acids EPA and DHA decrease plasma F(2)-isoprostanes: Results from two placebo-controlled interventions. Free Radic Res 44:983-990
50. Mastroeni R, Bensadoun JC, Charvin D, Aebischer P, Pujol A, Raoul C (2009) Insulin-like growth factor-1 and neurotrophin-3 gene therapy prevents motor decline in an X-linked adrenoleukodystrophy mouse model. Ann Neurol 66:117-122
51. Matarazzo MR, De Bonis ML, Vacca M, Della Ragione F, D'Esposito M (2009) Lessons from two human chromatin diseases, ICF syndrome and Rett syndrome. Int J Biochem Cell Biol 41:117-126
52. McGahon BM, Martin DS, Horrobin DF, Lynch MA (1999) Agerelated changes in synaptic function: analysis of the effect of dietary supplementation with omega-3 fatty acids. Neuroscience 94:305-314 (Pubitemid 29457620)
53. McNamara RK (2010) DHA deficiency and prefrontal cortex neuropathology in recurrent affective disorders. J Nutr 140:864-868
54. Montine KS, Quinn JF, Zhang J, Fessel JP, Roberts LJ 2nd, Morrow JD, Montine TJ (2004) Isoprostanes and related products of lipid peroxidation in neurodegenerative diseases. Chem Phys Lipids 128:117-124 (Pubitemid 38167381)
55. Montuschi P, Barnes PJ, Roberts LJ (2004) Isoprostanes: markers and mediators of oxidative stress. FASEB J 18:1791-1800 (Pubitemid 39602265)
56. Morrow JD, Roberts LJ (1997) The isoprostanes: unique bioactive products of lipid peroxidation. Prog Lipid Res 36:1-21 (Pubitemid 27387112)
57. Morrow JD, Hill KE, Burk RF, Nammour TM, Badr KF, Roberts LJ (1990) A series of prostaglandin F2-like compounds are produced in vivo in humans by a non-cyclooxygenase, free radical-catalyzed mechanism. Proc Natl Acad Sci USA 87:9383-9387 (Pubitemid 120030630)
58. Naidu S, Johnston MV (2011) Neurodevelopmental disorders: clinical criteria for Rett syndrome. Nat Rev Neurol 7:312-314
59. Neul JL, Fang P, Barrish J, Lane J, Caeg EB, Smith EO, Zoghbi H, Percy A, Glaze DG (2008) Specific mutations in methyl-CpGbinding protein 2 confer different severity in Rett syndrome. Neurology 70:1313-1321 (Pubitemid 351550354)
60. 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: revised diagnostic criteria and nomenclature. Ann Neurol 68:944-950
61. Nourooz-Zadeh J (2008) Key issues in F2-isoprostane analysis. Biochem Soc Trans 36:1060-1065
62. Nourooz-Zadeh J, Gopaul NK, Barrow S, Mallet AI, Anggard EE (1995) Analysis of F2-isoprostanes as indicators of nonenzymatic lipid peroxidation in vivo by gas chromatographymass spectrometry: development of a solid-phase extraction procedure. J Chromatogr B Biomed Appl 667:199-208
63. Ogier M, Wang H, Hong E, Wang Q, Greenberg ME, Katz DM (2007) Brain-derived neurotrophic factor expression and respiratory function improve after ampakine treatment in a mouse model of Rett syndrome. J Neurosci 27:10912-10917 (Pubitemid 47535875)
64. Pecorelli A, Ciccoli L, Signorini C, Leoncini S, Giardini A, D'Esposito M, Filosa S, Hayek J, De Felice C, Valacchi G (2011) Increased levels of 4HNE-protein plasma adducts in Rett syndrome. Clin Biochem 44:368-371
65. Rett A (1966) On a unusual brain atrophy syndrome in hyperammonemia in childhood. Wien Med Wochenschr 116:723-726
66. Roberts LJ, Montine TJ, Markesbery WR, Tapper AR, Hardy P, Chemtob S, Dettbarn WD, Morrow JD (1998) Formation of isoprostane-like compounds (neuroprostanes) in vivo from docosahexaenoic acid. J Biol Chem 273:13605-13612 (Pubitemid 28268404)
67. Roux JC, Dura E, Moncla A, Mancini J, Villard L (2007) Treatment with desipramine improbe breathing and survival in a mouse model for Rett syndrome. Eur J Neurosci 25:1915-1922 (Pubitemid 46581739)
68. Sastry PS (1985) Lipids of nervous tissue: composition and metabolism. Prog Lipid Res 24:69-176
69. Schmitz G, Ecker J (2008) The opposing effects of n-3 and n-6 fatty acids. Prog Lipid Res 47:147-155
70. Serhan CN, Gotlinger K, Hong S, Lu Y, Siegelman J, Baer T, Yang R, Colgan SP, Petasis NA (2006) Anti-inflammatory actions of neuroprotectin D1/protectin D1 and its natural stereoisomers: assignments of dihydroxy-containing docosatrienes. J Immunol 176:1848-1859 (Pubitemid 43134330)
71. Serhan CN, Chiang N, Van Dyke TE (2008) Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol 8:349-361 (Pubitemid 351595216)
72. Signorini C, Comporti M, Giorgi G (2003) Ion trap tandem mass spectrometric determination of F2-isoprostanes. J Mass Spectrom 38:1067-1074 (Pubitemid 37407701)
73. Signorini C, Ciccoli L, Leoncini S, Carloni S, Perrone S, Comporti M, Balduini W, Buonocore G (2009) Free iron, total F2-isoprostanes and total F4-neuroprostanes in a model of neonatal hypoxicischemic encephalopathy: neuroprotective effect of melatonin. J Pineal Res 46:148-154
74. Signorini C, De Felice C, Leoncini S, Giardini A, D'Esposito M, Filosa S, Della Ragione F, Rossi M, Pecorelli A, Valacchi G, Ciccoli L, Hayek J (2011) F4-neuroprostanes mediate neurological severity in Rett syndrome. Clin Chim Acta 412:1399-1406
75. Soderberg M, Edlund C, Kristensson K, Dallner G (1991) Fatty acid composition of brain phospholipids in aging and in Alzheimer's disease. Lipids 26:421-425
76. Sprecher H, VanRollins M, Sun F, Wyche A, Needleman P (1982) Dihomo-prostaglandins and -thromboxane. A prostaglandin family from adrenic acid that may be preferentially synthesized in the kidney. J Biol Chem 257:3912-3918 (Pubitemid 12083980)
77. Tropea D, Giacometti E, Wilson NR, Beard C, McCurry C, Fu DD, Flannery R, Jaenisch R, Sur M (2009) Partial reversal of Rett syndrome-like symptoms in MeCP2 mutant mice. Proc Natl Acad Sci USA 106:2029-2034
78. VanRollins M, Woltjer RL, Yin H, Morrow JD, Montine TJ (2008) F2-dihomo-isoprostanes arise from free radical attack on adrenic acid. J Lipid Res 49:995-1005
79. Viemari JC, Roux JC, Tryba AK, Saywell V, Burnet H, Pena F, Zanella S, Bevengut M, Barthelemy-Requin M, Herzing LB, Moncla A, Mancini J, Ramirez JM, Villard L, Hilaire G (2005) Mecp2 deficiency disrupts norepinephrine and respiratory systems in mice. J Neurosci 25:11521-11530 (Pubitemid 43098445)
80. Wada M, DeLong CJ, Hong YH, Rieke CJ, Song I, Sidhu RS, Yuan C, Warnock M, Schmaier AH, Yokoyama C, Smyth EM, Wilson SJ, FitzGerald GA, Garavito RM, de Sui X, Regan JW, Smith WL (2007) Enzymes and receptors of prostaglandin pathways with arachidonic acid-derived versus eicosapentaenoic acidderived substrates and products. J Biol Chem 282:22254-22266 (Pubitemid 47267340)
81. Wood LG, Gibson PG, Garg ML (2003) Biomarkers of lipid peroxidation, airway inflammation and asthma. Eur Respir J 21:177-186 (Pubitemid 36150317)
82. Xiao YF, Sigg DC, Leaf A (2005) The antiarrhythmic effect of n-3 polyunsaturated fatty acids: modulation of cardiac ion channels as a potential mechanism. J Membr Biol 206:141-154 (Pubitemid 43199147)
83. Yin H, Porter NA (2005) New insights regarding the autoxidation of polyunsaturated fatty acids. Antioxid Redox Signal 7:170-184 (Pubitemid 40187935)
84. Yin H, Liu W, Goleniewska K, Porter NA, Morrow JD, Peebles RS (2009) Dietary supplementation of omega-3 fatty acid-containing fish oil suppresses F2-isoprostanes but enhances inflammatory cytokine response in a mouse model of ovalbumin-induced allergic lung inflammation. Free Radic Biol Med 47:622-628
85. Zhang W, Li P, Hu X, Zhang F, Chen J, Gao Y (2011) Omega-3 polyunsaturated fatty acids in the brain: metabolism and neuroprotection. Front Biosci 17:2653-2670
86. Zoghbi HY (2009) Rett syndrome: what do we know for sure? Nat Neurosci 12:239-240