Maternal docosahexaenoic acid feeding protects against impairment of learning and memory and oxidative stress in prenatally stressed rats: Possible role of neuronal mitochondria metabolism

Antioxidants and Redox Signaling

Volumn 16, Issue 3, 2012, Pages 275-289

  Liu, Jiankang ^a   Feng, Zhihui ^a,b   Zou, Xuan ^a,c   Jia, Haiqun ^b,d   Li, Xuesen ^b,e   Zhu, Zhongliang ^a   Liu, Xuebo ^f   Bucheli, Peter ^g   Ballevre, Olivier ^g   Hou, Yangfeng ^g   Zhang, Weiguo ^g   Wang, Junkaun ^g   Chen, Yan ^b  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^c ZHEJIANG UNIVERSITY   (China)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f NORTHWEST A F UNIVERSITY   (China)

^g NESTLÉ RESEARCH CENTER   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; DOCOSAHEXAENOIC ACID; MESSENGER RNA; MITOFUSIN 1; MITOFUSIN 2; NITRIC OXIDE SYNTHASE; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BRAIN DYSFUNCTION; CONTROLLED STUDY; FEEDING; FEMALE; HIPPOCAMPUS; HUMAN; LEARNING; LEARNING DISORDER; MALE; MEMORY; MEMORY DISORDER; MITOCHONDRIAL RESPIRATION; NERVE CELL; NONHUMAN; OXIDATIVE STRESS; PREGNANCY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; RAT;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BRAIN-DERIVED NEUROTROPHIC FACTOR; COGNITION DISORDERS; DOCOSAHEXAENOIC ACIDS; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; FEMALE; HIPPOCAMPUS; LEARNING DISORDERS; MALE; MATERNAL-FETAL EXCHANGE; MAZE LEARNING; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROTEIN CARBONYLATION; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL; TRANSCRIPTION, GENETIC;

EID: 83255193365     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2010.3750     Document Type: Article

References (63)

1. Acheson A, Conover JC, Fandl JP, DeChiara TM, Russell M, Thadani A, Squinto SP, Yancopoulos GD, and Lindsay RM. A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature 374: 450-453, 1995.
2. Aksenov V, Long J, Lokuge S, Foster JA, Liu J, and Rollo CD. Dietary amelioration of locomotor, neurotransmitter and mitochondrial aging. Exp Biol Med (Maywood) 235: 66-76, 2010.
3. Aliev G, Liu J, Shenk JC, Fischbach K, Pacheco GJ, Chen SG, Obrenovich ME, Ward WF, Richardson AG, Smith MA, Gasimov E, Perry G, and Ames BN. Neuronal mitochondrial amelioration by feeding acetyl-L-carnitine and lipoic acid to aged rats. J Cell Mol Med 13: 320-333, 2009.
4. Au AK, Bayir H, Kochanek PM, and Clark RS. Evaluation of autophagy using mouse models of brain injury. Biochim Biophys Acta 1802: 918-923, 2010.
5. Bechoua S, Dubois M, Dominguez Z, Goncalves A, Nemoz G, Lagarde M, and Prigent AF. Protective effect of docosahexaenoic acid against hydrogen peroxide-induced oxidative stress in human lymphocytes. Biochem Pharmacol 57: 1021-1030, 1999. (Pubitemid 29168550)
6. Bishop NA, Lu T, and Yankner BA. Neural mechanisms of ageing and cognitive decline. Nature 464: 529-535, 2010.
7. Bohme GA, Bon C, Lemaire M, Reibaud M, Piot O, Stutzmann JM, Doble A, and Blanchard JC. Altered synaptic plasticity and memory formation in nitric oxide synthase inhibitor-treated rats. Proc Natl Acad Sci USA 90: 9191-9194, 1993. (Pubitemid 23306478)
8. Bon CL and Garthwaite J. On the role of nitric oxide in hippocampal long-term potentiation. J Neurosci 23: 1941-1948, 2003. (Pubitemid 36314749)
9. Brune B. Nitric oxide: NO apoptosis or turning it ON? Cell Death Differ 10: 864-869, 2003. (Pubitemid 36939696)
10. Burton CL, Chatterjee D, Chatterjee-Chakraborty M, Lovic V, Grella SL, Steiner M, and Fleming AS. Prenatal restraint stress and motherless rearing disrupts expression of plasticity markers and stress-induced corticosterone release in adult female Sprague-Dawley rats. Brain Res 1158: 28-38, 2007. (Pubitemid 47068410)
11. Calderon F and Kim HY. Docosahexaenoic acid promotes neurite growth in hippocampal neurons. J Neurochem 90: 979-988, 2004. (Pubitemid 39099980)
12. Carboni E, Barros VG, Ibba M, Silvagni A, Mura C, and Antonelli MC. Prenatal restraint stress: An in vivo microdialysis study on catecholamine release in the rat prefrontal cortex. Neuroscience 168: 156-166.
13. Carloni S, Girelli S, Scopa C, Buonocore G, Longini M, and Balduini W. Activation of autophagy and Akt/CREB signaling play an equivalent role in the neuroprotective effect of rapamycin in neonatal hypoxia-ischemia. Autophagy 6: 366-377, 2010.
14. Chen MJ and Russo-Neustadt AA. Nitric oxide signaling participates in norepinephrine-induced activity of neuronal intracellular survival pathways. Life Sci 81: 1280-1290, 2007. (Pubitemid 47554569)
15. Cherian SB, Bairy KL, and Rao MS. Chronic prenatal restraint stress induced memory impairment in passive avoidance task in post weaned male and female Wistar rats. Indian J Exp Biol 47: 893-899, 2009.
16. Clay HB, Sillivan S, and Konradi C. Mitochondrial dysfunction and pathology in bipolar disorder and schizophrenia. Int J Dev Neurosci 29: 311-323, 2011.
17. Darnaudery M and Maccari S. Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev 57: 571-585, 2008.
18. Dumont M and Beal MF. Neuroprotective strategies involving ROS in Alzheimer's disease. Free Radic Biol Med 51: 1014-1026, 2011.
19. Fliesler SJ and Anderson RE. Chemistry and metabolism of lipids in the vertebrate retina. Prog Lipid Res 22: 79-131, 1983.
20. Gibson GE, Starkov A, Blass JP, Ratan RR, and Beal MF. Cause and consequence: mitochondrial dysfunction initiates and propagates neuronal dysfunction, neuronal death and behavioral abnormalities in age-associated neurodegenerative diseases. Biochim Biophys Acta 1802: 122-134, 2010.
21. Glade MJ. Oxidative stress and cognitive longevity. Nutrition 26: 595-603, 2010.
22. Green P, Glozman S, Kamensky B, and Yavin E. Developmental changes in rat brain membrane lipids and fatty acids. The preferential prenatal accumulation of docosahexaenoic acid. J Lipid Res 40: 960-966, 1999. (Pubitemid 29220538)
23. Haley JE, Wilcox GL, and Chapman PF. The role of nitric oxide in hippocampal long-term potentiation. Neuron 8: 211-216, 1992.
24. Huang EJ and Reichardt LF. Neurotrophins: Roles in neuronal development and function. Annu Rev Neurosci 24: 677-736, 2001. (Pubitemid 32695243)
25. Ikemoto A, Kobayashi T, Emoto K, Umeda M, Watanabe S, and Okuyama H. Effects of docosahexaenoic and arachidonic acids on the synthesis and distribution of aminophospholipids during neuronal differentiation of PC12 cells. Arch Biochem Biophys 364: 67-74, 1999. (Pubitemid 29394292)
26. Jezek P and Plecita-Hlavata L. Mitochondrial reticulum network dynamics in relation to oxidative stress, redox regulation, and hypoxia. Int J Biochem Cell Biol 41: 1790-1804, 2009.
27. Kelly GS. Nutritional and botanical interventions to assist with the adaptation to stress. Altern Med Rev 4: 249-265, 1999. (Pubitemid 29418312)
28. Khairallah RJ, Sparagna GC, Khanna N, O'Shea KM, Hecker PA, Kristian T, Fiskum G, Des Rosiers C, Polster BM, and Stanley WC. Dietary supplementation with docosahexaenoic acid, but not eicosapentaenoic acid, dramatically alters cardiac mitochondrial phospholipid fatty acid composition and prevents permeability transition. Biochim Biophys Acta 1797: 1555-1562, 2010.
29. Lamaziere A, Richard D, Barbe U, Kefi K, Bausero P, Wolf C, and Visioli F. Differential distribution of DHA-phospholipids in rat brain after feeding: A lipidomic approach. Prostaglandins Leukot Essent Fatty Acids 84: 7-11, 2011.
30. Li H, Li QH, Zhu ZL, Chen R, Cheng DX, Cai Q, Jia N, and Song L. [Prenatal restraint stress decreases neurogranin expression in rat offspring hippocampus]. Sheng Li Xue Bao 59: 299-304, 2007.
31. Liu J, Head E, Gharib AM, Yuan W, Ingersoll RT, Hagen TM, Cotman CW, and Ames BN. Memory loss in old rats is associated with brain mitochondrial decay and RNA/DNA oxidation: partial reversal by feeding acetyl-L-carnitine and/or R-alpha-lipoic acid. Proc Natl Acad SciUSA 99: 2356-2361, 2002. (Pubitemid 34169065)
32. Liu J and Mori A. Stress, aging, and brain oxidative damage. Neurochem Res 24: 1479-1497, 1999. (Pubitemid 29505958)
33. Liu J, Wang X, Shigenaga MK, Yeo HC, Mori A, and Ames BN. Immobilization stress causes oxidative damage to lipid, protein, and DNA in the brain of rats. FASEB J 10: 1532-1538, 1996. (Pubitemid 26384450)
34. Long J, Gao F, Tong L, Cotman CW, Ames BN, and Liu J. Mitochondrial decay in the brains of old rats: Ameliorating effect of alpha-lipoic acid and acetyl-L-carnitine. Neurochem Res 34: 755-763, 2009.
35. Long J, Wang X, Gao H, Liu Z, Liu C, Miao M, and Liu J. Malonaldehyde acts as a mitochondrial toxin: Inhibitory effects on respiratory function and enzyme activities in isolated rat liver mitochondria. Life Sci 79: 1466-1472, 2006.
36. Maccari S and Morley-Fletcher S. Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 32 Suppl 1: S10-15, 2007. (Pubitemid 47211641)
37. McMillin JB and Dowhan W. Cardiolipin and apoptosis. Biochim Biophys Acta 1585: 97-107, 2002. (Pubitemid 36092073)
38. McNamara RK and Carlson SE. Role of omega-3 fatty acids in brain development and function: Potential implications for the pathogenesis and prevention of psychopathology. Prostaglandins Leukot Essent Fatty Acids 75: 329-349, 2006. (Pubitemid 44442917)
39. Muller WE, Eckert A, Kurz C, Eckert GP, and Leuner K. Mitochondrial dysfunction: Common final pathway in brain aging and Alzheimer's disease-Therapeutic aspects. Mol Neurobiol 41: 159-171, 2010.
40. O'Shea KM, Khairallah RJ, Sparagna GC, Xu W, Hecker PA, Robillard-Frayne I, Des Rosiers C, Kristian T, Murphy RC, Fiskum G, and Stanley WC. Dietary omega-3 fatty acids alter cardiac mitochondrial phospholipid composition and delay Ca2 +-induced permeability transition. J Mol Cell Cardiol 47: 819-827, 2009.
41. Ostrander DB, Sparagna GC, Amoscato AA, McMillin JB,and Dowhan W. Decreased cardiolipin synthesis corresponds with cytochrome c release in palmitate-induced cardiomyocyte apoptosis. J Biol Chem 276: 38061-38067, 2001.
42. Paradies G, Petrosillo G, Pistolese M, Di Venosa N, Serena D, and Ruggiero FM. Lipid peroxidation and alterations to oxidative metabolism in mitochondria isolated from rat heart subjected to ischemia and reperfusion. Free Radic Biol Med 27: 42-50, 1999. (Pubitemid 29353082)
43. Petrosillo G, Ruggiero FM, Pistolese M, and Paradies G. Reactive oxygen species generated from the mitochondrial electron transport chain induce cytochrome c dissociation from beef-heart submitochondrial particles via cardiolipin peroxidation. Possible role in the apoptosis. FEBS Lett 509: 435-438, 2001. (Pubitemid 34031974)
44. Pitsikas N. Effects of scopolamine and L-NAME on rats' performance in the object location test. Behav Brain Res 179: 294-298, 2007. (Pubitemid 46497468)
45. Raught B, Gingras AC, and Sonenberg N. The target of rapamycin (TOR) proteins. Proc Natl Acad Sci USA 98: 7037-7044, 2001. (Pubitemid 32567899)
46. Rotstein NP, Politi LE, German OL, and Girotti R. Protective effect of docosahexaenoic acid on oxidative stress-induced apoptosis of retina photoreceptors. Invest Ophthalmol Vis Sci 44: 2252-2259, 2003. (Pubitemid 36520324)
47. Rubinsztein DC, DiFiglia M, Heintz N, Nixon RA, Qin ZH, Ravikumar B, Stefanis L, and Tolkovsky A. Autophagy and its possible roles in nervous system diseases, damage and repair. Autophagy 1: 11-22, 2005.
48. Shenk JC, Liu J, Fischbach K, Xu K, Puchowicz M, Obrenovich ME, Gasimov E, Alvarez LM, Ames BN, Lamanna JC, and Aliev G. The effect of acetyl-L-carnitine and R-alphalipoic acid treatment in ApoE4 mouse as a model of human Alzheimer's disease. J Neurol Sci 283: 199-206, 2009.
49. Shimazawa M, Nakajima Y, Mashima Y, and Hara H. Docosahexaenoic acid (DHA) has neuroprotective effects against oxidative stress in retinal ganglion cells. Brain Res 1251: 269-275, 2009.
50. Silvagni A, Barros VG, Mura C, Antonelli MC, and Carboni E. Prenatal restraint stress differentially modifies basal and stimulated dopamine and noradrenaline release in the nucleus accumbens shell: An 'in vivo' microdialysis study in adolescent and young adult rats. Eur J Neurosci 28: 744-758, 2008.
51. Sun L, Luo C, Long J, Wei D, and Liu J. Acrolein is a mitochondrial toxin: Effects on respiratory function and enzyme activities in isolated rat liver mitochondria. Mitochondrion 6: 136-142, 2006. (Pubitemid 43890605)
52. Suter B. Grob K., and Pacciarelli B. Determination of fat content and fatty acid composition through 1-min transesterification in the food sample. Z Lebensm Unters Forsch A 204: 252-258, 1997. (Pubitemid 127789610)
53. Van den Hove DL, Blanco CE, Aendekerk B, Desbonnet L, Bruschettini M, Steinbusch HP, Prickaerts J, and Steinbusch HW. Prenatal restraint stress and long-term affective consequences. Dev Neurosci 27: 313-320, 2005. (Pubitemid 41243219)
54. Wallace DC. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: A dawn for evolutionary medicine. Annu Rev Genet 39: 359-407, 2005. (Pubitemid 43011120)
55. Watkins SM, Carter LC, and German JB. Docosahexaenoic acid accumulates in cardiolipin and enhances HT-29 cell oxidant production. J Lipid Res 39: 1583-1588, 1998. (Pubitemid 28377921)
56. Wu J, Song TB, Li YJ, He KS, Ge L, and Wang LR. Prenatal restraint stress impairs learning and memory and hippocampal PKCbeta1 expression and translocation in offspring rats. Brain Res 1141: 205-213, 2007. (Pubitemid 46365651)
57. Yamada K and Nabeshima T. Brain-derived neurotrophic factor/TrkB signaling in memory processes. J Pharmacol Sci 91: 267-270, 2003. (Pubitemid 36581946)
58. Yamada Y, Suzuki NN, Hanada T, Ichimura Y, Kumeta H, Fujioka Y, Ohsumi Y, and Inagaki F. The crystal structure of Atg3, an autophagy-related ubiquitin carrier protein (E2) enzyme that mediates Atg8 lipidation. J Biol Chem282: 8036-8043, 2007. (Pubitemid 47093560)
59. Yavin E. Versatile roles of docosahexaenoic acid in the prenatal brain: From pro-and antioxidant features to regulation of gene expression. Prostaglandins Leukot Essent Fatty Acids 75: 203-211, 2006. (Pubitemid 44292525)
60. Zemke D, Azhar S, and Majid A. The mTOR pathway as a potential target for the development of therapies against neurological disease. Drug News Perspect 20: 495-499, 2007. (Pubitemid 351182792)
61. Zhu Z, Li X, Chen W, Zhao Y, Li H, Qing C, Jia N, Bai Z, and Liu J. Prenatal stress causes gender-dependent neuronal loss and oxidative stress in rat hippocampus. J Neurosci Res 78: 837-844, 2004. (Pubitemid 39657571)
62. Zou LB, Yamada K, Tanaka T, Kameyama T, and Nabeshima T. Nitric oxide synthase inhibitors impair reference memory formation in a radial arm maze task in rats. Neuropharmacology 37: 323-330, 1998. (Pubitemid 28282637)
63. Zuena AR, Mairesse J, Casolini P, Cinque C, Alema GS, Morley-Fletcher S, Chiodi V, Spagnoli LG, Gradini R, Catalani A, Nicoletti F, and Maccari S. Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS ONE 3: e2170, 2008.