Prenatal omega 3 fatty acid supplementation to a micronutrient imbalanced diet protects brain neurotrophins in both the cortex and hippocampus in the adult rat offspring

Metabolism: Clinical and Experimental

Volumn 62, Issue 11, 2013, Pages 1607-1622

  Sable, Pratiksha S ^a   Kale, Anvita A ^a   Joshi, Sadhana R ^a  

^a Bharati Vidyapeeth Deemed University   (India)

Author keywords

Brain Derived Neurotrophic Factor; Cognition; Developmental Origins of Health and Disease; Docosahexaenoic Acid; Nerve Growth Factor

Indexed keywords

CYANOCOBALAMIN; FOLIC ACID; NEUROTROPHIN; OMEGA 3 FATTY ACID; TRACE ELEMENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN FUNCTION; COGNITION; CONTROLLED STUDY; CYANOCOBALAMIN DEFICIENCY; DIET RESTRICTION; DIET SUPPLEMENTATION; HIPPOCAMPUS; MATERNAL NUTRITION; NONHUMAN; PREGNANCY; PRENATAL CARE; PRIORITY JOURNAL; PROGENY; RAT;

AA; ARACHIDONIC ACID; BDNF; BRAIN DERIVED NEUROTROPHIC FACTOR; COGNITION; DEVELOPMENTAL ORIGINS OF HEALTH AND DISEASE; DHA; DOCOSAHEXAENOIC ACID; DOHAD; NERVE GROWTH FACTOR; NGF;

ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CEREBRAL CORTEX; COGNITION; DIET; DIETARY SUPPLEMENTS; FATTY ACIDS, OMEGA-3; FEMALE; FOLIC ACID; FOLIC ACID DEFICIENCY; HIPPOCAMPUS; HOMOCYSTEINE; MAZE LEARNING; MICRONUTRIENTS; NERVE GROWTH FACTOR; ORGAN SIZE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RANDOM ALLOCATION; RATS; VITAMIN B 12; VITAMIN B 12 DEFICIENCY;

EID: 84886417802     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2013.06.002     Document Type: Article

References (71)

1. R. Painter, C. Osmond, and P. Gluckman Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life BJOG 115 10 2008 1243 1249
2. C. Remacle, F. Bieswal, and V. Bol Developmental programming of adult obesity and cardiovascular disease in rodents by maternal nutrition imbalance Am J Clin Nutr 94 6 Suppl 2011 1846S 1852S
3. A. Van Abeelen, S. Elias, and P. Bossuyt Famine exposure in the young and the risk of type 2 diabetes in adulthood Diabetes 61 9 2012 2255 2260
4. D. Peleg-Raibstein, E. Luca, and C. Wolfrum Maternal high-fat diet in mice programs emotional behavior in adulthood Behav Brain Res 233 2 2012 398 404
5. 12 is not recovered by methionine supplementation J Nutrigenet Nutrigenomics 2 1 2009 29 36
6. A. Charles, T. Johnson, and J. Belshaw Supra-physiological folic acid concentrations induce aberrant DNA methylation in normal human cells in vitro Epigenetics 7 7 2012 689 694
7. C. Yajnik, and U. Deshmukh Fetal programming: maternal nutrition and role of one-carbon metabolism Rev Endocr Metab Disord 13 2 2012 121 127
8. 12 status of pregnant Indian women and cognitive function in their 9-year-old children Food Nutr Bull 29 4 2008 249 254
9. S. Roy, A. Kale, and K. Dangat Maternal micronutrients (folic acid and vitamin B(12)) and omega 3 fatty acids: implications for neurodevelopmental risk in the rat offspring Brain Dev 34 1 2012 64 71
10. B. Helland, L. Smith, and K. Saarem Maternal supplementation with very-long-chain n-3 fatty acids during pregnancy and lactation augments children's IQ at 4 years of age Pediatrics 111 1 2003 e39 e44
11. L. Chung, J. Chen, and M. Su Fish oil supplementation of control and (n-3) fatty acid-deficient male rats enhances reference and working memory performance and increases brain regional docosahexaenoic acid levels J Nutr 138 6 2008 1165 1171 (Pubitemid 351769146)
12. C. Cunha, R. Brambilla, and K. Thomas A simple role for BDNF in learning and memory? Front Mol Neurosci 9 3 2010 1
13. J. Conner, K. Franks, and A. Titterness NGF is essential for hippocampal plasticity and learning J Neurosci 29 35 2009 10883 10889
14. M. Li, R. Dai, and X. Du Infusion of BDNF into the nucleus accumbens of aged rats improves cognition and structural synaptic plasticity through PI3K-ILK-Akt signaling Behav Brain Res 231 1 2012 146 153
15. O. Islam, X. Loo, and K. Heese Brain-derived neurotrophic factor (BDNF) has proliferative effects on neural stem cells through the truncated TRK-B receptor MAP kinase AKT and STAT-3 signaling pathways Curr Neurovasc Res 6 1 2009 42 53
16. N. Nguyen, S. Lee, and Y. Lee Neuroprotection by NGF and BDNF against neurotoxin-exerted apoptotic death in neural stem cells are mediated through Trk receptors activating PI3-kinase and MAPK pathways Neurochem Res 34 5 2009 942 951
17. I. Branchi, I. D'Andrea, and M. Fiore Early social enrichment shapes social behavior and nerve growth factor and brain-derived neurotrophic factor levels in the adult mouse brain Biol Psychiatry 60 7 2006 690 696 (Pubitemid 44427759)
18. T. Roth, and J. Sweatt Epigenetic marking of the BDNF gene by early-life adverse experiences Horm Behav 59 3 2011 315 320
19. J. Howie, M. Sloboda, and H. Vickers Maternal undernutrition during critical windows of development results in differential and sex-specific effects on postnatal adiposity and related metabolic profiles in adult rat offspring Br J Nutr 108 2 2012 298 307
20. M. Vickers Developmental programming of the metabolic syndrome - critical windows for intervention World J Diabetes 2 9 2011 137 148
21. P. Sable, K. Dangat, and A. Kale Altered brain neurotrophins at birth: consequence of imbalance in maternal folic acid and vitamin B12 metabolism Neuroscience 190 2011 127 134
22. P. Sable, K. Dangat, and A. Joshi Maternal omega 3 fatty acid supplementation during pregnancy to a micronutrient-imbalanced diet protects postnatal reduction of brain neurotrophins in the rat offspring Neuroscience 217 2012 46 55
23. K. Dangat, A. Kale, and S. Joshi Maternal supplementation of omega 3 fatty acids to micronutrient-imbalanced diet improves lactation in rat Metabolism 60 9 2011 1318 1324
24. S. Joshi, S. Rao, and S. Girigosavi Differential effects of fish oil and folic acid supplementation during pregnancy in rats on cognitive performance and serum glucose in their offspring Nutrition 20 5 2004 465 472 (Pubitemid 38501801)
25. 12 in pregnancy is associated with gestational 'diabesity' and later diabetes Diabetologia 52 11 2009 2350 2358
26. N. Van Wijk, C.J. Watkins, and R.J. Hageman Combined dietary folate vitamin B-12 and vitamin B-6 intake influences plasma docosahexaenoic acid concentration in rats Nutr Metab (Lond) 9 1 2012 49
27. 12 Clin Chem Lab Med 41 11 2003 1435 1437 (Pubitemid 37493557)
28. G. Burdge, K. Lillycrop, and E. Phillips Folic acid supplementation during the juvenile-pubertal period in rats modifies the phenotype and epigenotype induced by prenatal nutrition J Nutr 139 6 2009 1054 1060
29. M. Vickers, P. Gluckman, and A. Coveny Neonatal leptin treatment reverses developmental programming Endocrinology 146 10 2005 4211 4216 (Pubitemid 41324016)
30. I. Weaver, F. Champagne, and S. Brown Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life J Neurosci 25 47 2005 11045 11054 (Pubitemid 41692634)
31. L. Andersen Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci Biobehav Rev 27 1-2 2003 3 18
32. N. Berardi, T. Pizzorusso, and L. Maffei Critical periods during sensory development Curr Opin Neurobiol 10 1 2000 138 145 (Pubitemid 30102867)
33. Y. Xiao, Y. Huang, and Z. Chen Distribution depletion and recovery of docosahexaenoic acid are region-specific in rat brain Br J Nutr 94 4 2005 544 550 (Pubitemid 41555495)
34. J. Umhau, K. Dauphinais, and S. Patel The relationship between folate and docosahexaenoic acid in men Eur J Clin Nutr 60 3 2006 352 357 (Pubitemid 43354928)
35. N. Wadhwani, R. Manglekar, and K. Dangat Effect of maternal micronutrients (folic acid, vitamin B12) and omega 3 fatty acids on liver fatty acid desaturases and transport proteins in Wistar rats Prostaglandins Leukot Essent Fatty Acids 86 1-2 2012 21 27
36. N. Wadhwani, K. Dangat, and A. Joshi Maternal micronutrients and omega 3 fatty acids affect placental fatty acid desaturases and transport proteins in Wistar rats Prostaglandins Leukot Essent Fatty Acids 88 3 2013 235 242
37. H. Guillou, D. Zadravec, and P.G. Martin The key roles of elongases and desaturases in mammalian fatty acid metabolism: insights from transgenic mice Prog Lipid Res 49 2 2010 186 199
38. M. Igarashi, H. Kim, and L. Chang Dietary n-6 polyunsaturated fatty acid deprivation increases docosahexaenoic acid metabolism in rat brain J Neurochem 120 6 2012 985 997
39. J.S. Rao, R.N. Ertley, and J.C. DeMar Jr. Dietary n-3 PUFA deprivation alters expression of enzymes of the arachidonic and docosahexaenoic acid cascades in rat frontal cortex Mol Psychiatry 12 2 2007 151 157 (Pubitemid 46160980)
40. 12) and omega 3 fatty acids on indices of brain oxidative stress in the offspring. Brain Dev 2013 [Epub ahead of print].
41. E. Scherer, A. da Cunha, and J. Kolling Development of an animal model for chronic mild hyperhomocysteinemia and its response to oxidative damage Int J Dev Neurosci 29 7 2011 693 699
42. A. Kulkarni, K. Dangat, and A. Kale Effects of altered maternal folic acid, vitamin B12 and docosahexaenoic acid on placental global DNA methylation patterns in Wistar rats PLoS One 6 3 2011 e17706 10
43. S. Mehendale, A. Kilari, and K. Dangat Fatty acids, antioxidants, and oxidative stress in pre-eclampsia Int J Gynaecol Obstet 100 3 2008 234 238 (Pubitemid 351258086)
44. A. Kilari, S. Mehendale, and K. Dangat Long chain polyunsaturated fatty acids in mothers of preterm babies J Perinat Med 38 6 2010 659 664
45. M. Dhobale, N. Wadhwani, and S. Mehendale Reduced levels of placental long chain polyunsaturated fatty acids in preterm deliveries Prostaglandins Leukot Essent Fatty Acids 85 3-4 2011 149 153
46. S. Bhatia, R. Agrawal, and S. Sharma Omega-3 fatty acid deficiency during brain maturation reduces neuronal and behavioral plasticity in adulthood PLoS One 6 12 2011 e28451
47. N. Blondeau, C. Nguemeni, and D.N. Debruyne Subchronic alpha-linolenic acid treatment enhances brain plasticity and exerts an antidepressant effect: a versatile potential therapy for stroke Neuropsychopharmacology 34 12 2009 2548 2559
48. R. Cysneiros, D. Ferrari, and R. Arida Qualitative analysis of hippocampal plastic changes in rats with epilepsy supplemented with oral omega-3 fatty acids Epilepsy Behav 17 1 2010 33 38
49. V. Venna, D. Deplanque, and C. Allet PUFA induce antidepressant-like effects in parallel to structural and molecular changes in the hippocampus Psychoneuroendocrinology 34 2 2009 199 211
50. H. Shoji, C. Franke, and H. Demmelmair Effect of docosahexaenoic acid on oxidative stress in placental trophoblast cells Early Hum Dev 85 7 2009 433 437
51. A. Wu, Z. Ying, and F. Gomez-Pinilla The interplay between oxidative stress and brain-derived neurotrophic factor modulates the outcome of a saturated fat diet on synaptic plasticity and cognition Eur J Neurosci 19 7 2004 1699 1707 (Pubitemid 38482558)
52. F. Kapczinski, N. Frey, and C. Andreazza Increased oxidative stress as a mechanism for decreased BDNF levels in acute manic episodes Rev Bras Psiquiatr 30 3 2008 243 245
53. J. Kyle, E. Schaefer, and G. Patton Low serum docosahexaenoic acid is a significant risk factor for Alzheimer's dementia Lipids 34 Suppl 1999 S245
54. M. Muldoon, C. Ryan, and L. Sheu Serum phospholipid docosahexaenonic acid is associated with cognitive functioning during middle adulthood J Nutr 140 4 2010 848 853
55. S. Morris, F. Jacques, and H. Rosenberg Folate and vitamin B-12 status in relation to anemia macrocytosis and cognitive impairment in older Americans in the age of folic acid fortification Am J Clin Nutr 85 1 2007 193 200
56. K. Lövblad, G. Ramelli, and L. Remonda Retardation of myelination due to dietary vitamin B12 deficiency: cranial MRI findings Pediatr Radiol 27 2 1997 155 158 (Pubitemid 27101782)
57. B. Casella, M. Valente, and M. de Navarro Vitamin B12 deficiency in infancy as a cause of developmental regression Brain Dev 27 8 2005 592 594 (Pubitemid 41681759)
58. J. Faraji, H. Lehmann, and A. Metz Rats with hippocampal lesion show impaired learning and memory in the ziggurat task: a new task to evaluate spatial behavior Behav Brain Res 189 1 2008 17 31
59. X. Yin, H. Turner, and J. Lin Deficits in spatial learning and memory is associated with hippocampal volume loss in aged apolipoprotein E4 mice J Alzheimers Dis 27 1 2011 89 98
60. J. Broadbent, R. Squire, and E. Clark Spatial memory, recognition memory, and the hippocampus Proc Natl Acad Sci USA 101 40 2004 14515 14520
61. C. Rendeiro, D. Vauzour, and R. Kean Blueberry supplementation induces spatial memory improvements and region-specific regulation of hippocampal BDNF mRNA expression in young rats Psychopharmacology 223 3 2012 319 330
62. A. Joardar, A. Sen, and S. Das Docosahexaenoic acid facilitates cell maturation and beta-adrenergic transmission in astrocytes J Lipid Res 47 3 2006 571 581 (Pubitemid 43345598)
63. D. Soellner, T. Grandys, and J. Nuñez Chronic prenatal caffeine exposure impairs novel object recognition and radial arm maze behaviors in adult rats Behav Brain Res 205 1 2009 191 199
64. C. Davis, L. Franklin, and G. Johnson Prenatal oxycodone exposure impairs spatial learning and/or memory in rats Behav Brain Res 212 1 2010 27 34
65. L. Pyter, S. Cochrane, and R. Ouwenga Mammary tumors induce select cognitive impairments Brain Behav Immun 24 6 2010 903 907
66. M. Niculescu, C. Craciunescu, and S. Zeisel Dietary choline deficiency alters global and gene-specific DNA methylation in the developing hippocampus of mouse fetalbrains FASEB J 20 1 2006 43 49 (Pubitemid 43100474)
67. X. Zhang, G. Huang, and H. Liu Folic acid enhances Notch signaling, hippocampal neurogenesis, and cognitive function in a rat model of cerebral ischemia Nutr Neurosci 15 2 2012 55 61
68. Y. Chen, Z. Wang, and Y. Xie Folic acid deficiency inhibits neural rosette formation and neuronal differentiation from rhesus monkey embryonic stem cells J Neurosci Res 90 7 2012 1382 1391
69. V. Boshnjaku, S. Ichi, and Y. Shen Epigenetic regulation of sensory neurogenesis in the dorsal root ganglion cell line ND7 by folic acid Epigenetics 6 10 2011 1207 1216
70. K. Okada, H. Tanaka, and K. Temporin Methylcobalamin increases Erk1/2 and Akt activities through the methylation cycle and promotes nerve regeneration in a rat sciatic nerve injury model Exp Neurol 222 2 2010 191 203
71. S. Battaglia-Hsu, N. Akchiche, and N. Noel Vitamin B12 deficiency reduces proliferation and promotes differentiation of neuroblastoma cells and up-regulates PP2A, proNGF, and TACE Proc Natl Acad Sci USA 106 51 2009 21930 21935