DOI QR코드

DOI QR Code

Effects of Docosahexaenoic Acid on Neurotransmission

  • Tanaka, Kazuhiro (Department of Pharmacology, National University of Singapore) ;
  • Farooqui, Akhlaq A. (Department of Molecular and Cellular Biochemistry, The Ohio State University) ;
  • Siddiqi, Nikhat J. (Department of Biochemistry, College of Science, King Saud University) ;
  • Alhomida, Abdullah S. (Department of Biochemistry, College of Science, King Saud University) ;
  • Ong, Wei-Yi (Department of Anatomy, National University of Singapore)
  • Received : 2011.09.27
  • Accepted : 2011.12.05
  • Published : 2012.03.31

Abstract

Docosahexaenoic acid (DHA) is the major polyunsaturated fatty acid (PUFA) in the brain and a structural component of neuronal membranes. Changes in DHA content of neuronal membranes lead to functional changes in the activity of receptors and other proteins which might be associated with synaptic function. Accumulating evidence suggests the beneficial effects of dietary DHA supplementation on neurotransmission. This article reviews the beneficial effects of DHA on the brain; uptake, incorporation and release of DHA at synapses, effects of DHA on synapses, effects of DHA on neurotransmitters, DHA metabolites, and changes in DHA with age. Further studies to better understand the metabolome of DHA could result in more effective use of this molecule for treatment of neurodegenerative or neuropsychiatric diseases.

Keywords

References

  1. Aid, S., Vancassel, S., Poumès-Ballihaut, C., Chalon, S., Guesnet, P. and Lavialle, M. (2003) Effect of a diet-induced n-3 PUFA depletion on cholinergic parameters in the rat hippocampus. J. Lipid. Res. 44, 1545-1551. https://doi.org/10.1194/jlr.M300079-JLR200
  2. Arsenault. D., Julien, C. and Calon, F. (2011) Chronic dietary intake of $\alpha$-linolenic acid does not replicate the effects of DHA on passive properties of entorhinal cortex neurons. Br. J. Nutr. 19, 1-13.
  3. Bailes, J. E. and Mills, J. D. (2010) Docosahexaenoic acid reduces traumatic axonal injury in a rodent head injury model. J. Neurotrauma. 27, 1617-1624. https://doi.org/10.1089/neu.2009.1239
  4. Bazan, N. G. (2005) Neuroprotectin D1 (NPD1): a DHA-derived mediator that protects brain and retina against cell injury-induced oxidative stress. Brain Pathol. 15, 159-166.
  5. Bazan, N. G., Molina, M. F. and Gordon, W. C. (2011) Docosahexaenoic acid signalolipidomics in nutrition: signifi cance in aging, neuroinfl ammation, macular degeneration, Alzheimer's, and other neurodegenerative diseases. Annu. Rev. Nutr. 31, 321-351. https://doi.org/10.1146/annurev.nutr.012809.104635
  6. Beck, G., Sugiura, Y., Shinzawa, K., Kato, S., Setou, M., Tsujimoto, Y., Sakoda, S. and Sumi-Akamaru, H. (2011) Neuroaxonal dystrophy in calcium-independent phospholipase $A2{\beta}$ defi ciency results from insuffi cient remodeling and degeneration of mitochondrial and presynaptic membranes. J. Neurosci. 31, 11411-11420. https://doi.org/10.1523/JNEUROSCI.0345-11.2011
  7. Berry, C. B., Hayes, D., Murphy, A., Wiessner, M., Rauen, T. and Mc- Bean, G. J. (2005) Differential modulation of the glutamate transporters GLT1, GLAST and EAAC1 by docosahexaenoic acid. Brain Res. 1037, 123-133. https://doi.org/10.1016/j.brainres.2005.01.008
  8. Calderon, F. and Kim, H. Y. (2004) Docosahexaenoic acid promotes neurite growth in hippocampal neurons. J. Neurochem. 90, 979- 988. https://doi.org/10.1111/j.1471-4159.2004.02520.x
  9. Calon, F., Lim, G. P., Yang, F., Morihara, T., Teter, B., Ubeda, O., Rostaing, P., Triller, A., Salem, N. Jr., Ashe, K. H., Frautschy, S. A. and Cole, G. M. (2004) Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron. 43, 633-645. https://doi.org/10.1016/j.neuron.2004.08.013
  10. Cao, D., Kevala, K., Kim, J., Moon, H. S., Jun, S. B., Lovinger, D. and Kim, H. Y. (2009) Docosahexaenoic acid promotes hippocampal neuronal development and synaptic function. J. Neurochem. 111, 510-521. https://doi.org/10.1111/j.1471-4159.2009.06335.x
  11. Chalon, S. (2006) Omega-3 fatty acids and monoamine neurotransmission. Prostaglandins. Leukot. Essent. Fatty Acids. 75, 259-269. https://doi.org/10.1016/j.plefa.2006.07.005
  12. Chytrova, G., Ying, Z. and Gomez-Pinilla, F. (2010) Exercise contributes to the effects of DHA dietary supplementation by acting on membrane-related synaptic systems. Brain Res. 1341, 32-40. https://doi.org/10.1016/j.brainres.2009.05.018
  13. Cole, G. M., Lim, G. P., Yang, F., Teter, B., Begum, A., Ma, Q., Harris- White, M. E. and Frautschy, S. A. (2005) Prevention of Alzheimer's disease: Omega-3 fatty acid and phenolic anti-oxidant interventions. Neurobiol. Aging. 26(Suppl 1), 133-136. https://doi.org/10.1016/j.neurobiolaging.2005.09.005
  14. Dagai, L., Peri-Naor, R. and Birk, R. Z. (2009) Docosahexaenoic acid signifi cantly stimulates immediate early response genes and neurite outgrowth. Neurochem. Res. 34, 867-875. https://doi.org/10.1007/s11064-008-9845-z
  15. de Urquiza, A. M., Liu, S., Sjöberg, M., Zetterström, R. H., Griffi ths, W., Sjövall, J. and Perlmann, T. (2000) Docosahexaenoic acid, a ligand for the retinoid X receptor in mouse brain. Science. 290, 2140-2144. https://doi.org/10.1126/science.290.5499.2140
  16. Dyall, S. C., Michael, G. J., Whelpton, R., Scott, A. G. and Michael-Titus, A. T. (2007) Dietary enrichment with omega-3 polyunsaturated fatty acids reverses age-related decreases in the GluR2 and NR2B glutamate receptor subunits in rat forebrain. Neurobiol. Aging. 28, 424-439. https://doi.org/10.1016/j.neurobiolaging.2006.01.002
  17. Farooqui, A. A. (2009) Bebefi cial Effects of Fish Oil on Human Brain. Springer, New York.
  18. Farooqui, A. A. (2010a) Purifi cation, properties and role of plasmalogen- selective PLA2 from pig brain. Mol. Neurobiol. 41, 267-273. https://doi.org/10.1007/s12035-009-8091-y
  19. Farooqui, A. A. (2010b) Modulation of neurotransmission signaling by neural membrane polyunsaturated fatty acids in Biogenic Amines: Pharmacological, Neurochemical, and Molecular Aspects in CNS, pp. 219-246, Nova Science Publishers Inc, Hauppauge, New York.
  20. Farooqui, A. A., Horrocks, L. A. and Farooqui, T. (2007) Modulation of infl ammation in brain: a matter of fat. J. Neurochem. 101, 577-599.
  21. Farooqui, A. A., Ong, W. Y. and Horrocks, L. A. (2003) Plasmalogens, docosahexaenoic acid and neurological disorders. Adv. Exp. Med. Biol. 544, 335-354. https://doi.org/10.1007/978-1-4419-9072-3_45
  22. Grintal, B., Champeil-Potokar, G., Lavialle, M., Vancassel, S., Breton, S. and Denis, I. (2009) Inhibition of astroglial glutamate transport by polyunsaturated fatty acids: evidence for a signalling role of docosahexaenoic acid. Neurochem. Int. 54, 535-543. https://doi.org/10.1016/j.neuint.2009.02.018
  23. He, C., Qu, X., Cui, L., Wang, J. and Kang, J. X. (2009) Improved spatial learning performance of fat-1 mice is associated with enhanced neurogenesis and neuritogenesis by docosahexaenoic acid. Proc. Natl. Acad. Sci. USA. 106,11370-11375. https://doi.org/10.1073/pnas.0904835106
  24. Jones, C. R., Arai, T. and Rapoportm S, I. (1997) Evidence for the involvement of docosahexaenoic acid in cholinergic stimulated signal transduction at the synapse. Neurochem. Res. 22, 663-670. https://doi.org/10.1023/A:1027341707837
  25. Kim, H. Y., Moon, H. S., Cao, D., Lee, J., Kevala, K., Jun, S. B., Lovinger, D. M., Akbar, M. and Huang, B. X. (2011a) N-Docosahexaenoylethanolamide promotes development of hippocampal neurons. Biochem. J. 435, 327-336. https://doi.org/10.1042/BJ20102118
  26. Kim, H. Y., Spector, A. A. and Xiong, Z. M. (2011b) A synaptogenic amide N-docosahexaenoylethanolamide promotes hippocampal development. Prostaglandins. Other. Lipid. Mediat. 96, 114-120. https://doi.org/10.1016/j.prostaglandins.2011.07.002
  27. Kim, Y. J. and Chung, H. Y. (2007) Antioxidative and anti-infl ammatory actions of docosahexaenoic acid and eicosapentaenoic acid in renal epithelial cells and macrophages. J. Med. Food. 10, 225-231. https://doi.org/10.1089/jmf.2006.092
  28. Kitajka, K. , Puskás, L. G., Zvara, A., Hackler, L. Jr., Barceló-Coblijn, G., Yeo, Y. K. and Farkas, T. (2002) The role of n-3 polyunsaturated fatty acids in brain: modulation of rat brain gene expression by dietary n-3 fatty acids. Proc. Natl. Acad. Sci. USA. 99, 2619-2624. https://doi.org/10.1073/pnas.042698699
  29. Kodas, E., Galineau, L., Bodard, S., Vancassel, S., Guilloteau, D., Besnard, J. C. and Chalon, S. (2004) Serotoninergic neurotransmission is affected by n-3 polyunsaturated fatty acids in the rat. J. Neurochem. 89, 695-702. https://doi.org/10.1111/j.1471-4159.2004.02401.x
  30. Lafourcade, M., Larrieu, T., Mato, S., Duffaud, A., Sepers, M., Matias, I., De Smedt-Peyrusse, V., Labrousse, V. F., Bretillon, L., Matute, C., Rodriguez-Puertas, R., Layé, S. and Manzoni, O. J. (2011) Nutritional omega-3 defi ciency abolishes endocannabinoid-mediated neuronal functions. Nat. Neurosci. 14, 345-350. https://doi.org/10.1038/nn.2736
  31. Lengqvist, J., Mata De Urquiza, A., Bergman, A. C., Willson, T. M., Sjövall, J., Perlmann, T. and Griffi ths, W. J. (2004) Polyunsaturated fatty acids including docosahexaenoic and arachidonic acid bind to the retinoid X receptor alpha ligand-binding domain. Mol. Cell. Proteomics. 3, 692-703. https://doi.org/10.1074/mcp.M400003-MCP200
  32. Little, S. J., Lynch, M. A., Manku, M. and Nicolaou, A. (2007) Docosahexaenoic acid-induced changes in phospholipids in cortex of young and aged rats: a lipidomic analysis. Prostaglandins. Leukot. Essent. Fatty. Acids. 77, 155-162. https://doi.org/10.1016/j.plefa.2007.08.009
  33. Liu, J. W., Almaguel, F. G., Bu, L., De Leon, D. D. and De Leon, M. (2008) Expression of E-FABP in PC12 cells increases neurite extension during differentiation: involvement of n-3 and n-6 fatty acids. J. Neurochem. 106, 2015-2029.
  34. Logan, A. C. (2004) Omega-3 fatty acids and major depression: a primer for the mental health professional. Lipids. Health Dis. 3, 25. https://doi.org/10.1186/1476-511X-3-25
  35. Ma, D., Zhang, M., Larsen, C. P., Xu, F., Hua, W., Yamashima, T., Mao, Y. and Zhou, L. (2010) DHA promotes the neuronal differentiation of rat neural stem cells transfected with GPR40 gene. Brain Res. 1330, 1-8. https://doi.org/10.1016/j.brainres.2010.03.002
  36. Mathieu, G., Denis, S., Langelier, B., Denis, I., Lavialle, M. and Vancassel, S. (2010) DHA enhances the noradrenaline release by SHSY5Y cells. Neurochem. Int. 56, 94-100. https://doi.org/10.1016/j.neuint.2009.09.006
  37. Matta, J. A., Miyares, R. L. and Ahern, G. P. (2007) TRPV1 is a novel target for omega-3 polyunsaturated fatty acids. J. Physiol. 578, 397-411. https://doi.org/10.1113/jphysiol.2006.121988
  38. Mayurasakorn. K., Williams, J. J., Ten, V. S. and Deckelbaum, R. J. (2011) Docosahexaenoic acid: brain accretion and roles in neuroprotection after brain hypoxia and ischemia. Curr. Opin. Clin. Nutr. Metab. Care. 14, 158-167. https://doi.org/10.1097/MCO.0b013e328342cba5
  39. Mazelova, J., Ransom, N., Astuto-Gribble, L., Wilson, M. C. and Deretic, D. (2003) Syntaxin 3 and SNAP-25 pairing, regulated by omega-3 docosahexaenoic acid, controls the delivery of rhodopsin for the biogenesis of cilia-derived sensory organelles, the rod outer segments. J. Cell Sci. 122, 2003-2013.
  40. McNamara, R. K., Sullivan, J., Richtand, N. M., Jandacek, R., Rider, T., Tso, P., Campbell, N. and Lipton, J. (2008) Omega-3 fatty acid defi ciency augments amphetamine-induced behavioral sensitization in adult DBA/2J mice: relationship with ventral striatum dopamine concentrations. Synapse. 62, 725-735. https://doi.org/10.1002/syn.20542
  41. Mukherjee, P. K., Marcheselli, V. L., Serhan, C. N. and Bazan, N. G. (2004) Neuroprotectin D1: a docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress. Proc. Natl. Acad. Sci. USA. 101, 8491-8496. https://doi.org/10.1073/pnas.0402531101
  42. Nabekura, J., Noguchi, K., Witt, M. R., Nielsen, M. and Akaike, N. (1998) Functional modulation of human recombinant gamma-aminobutyric acid type A receptor by docosahexaenoic acid. J. Biol. Chem. 273, 11056-11061. https://doi.org/10.1074/jbc.273.18.11056
  43. Nakamoto, K., Nishinaka, T., Mankura, M., Fujita-Hamabe, W. and Tokuyama, S. (2010) Antinociceptive effects of docosahexaenoic acid against various pain stimuli in mice. Biol. Pharm. Bull. 33, 1070-1072. https://doi.org/10.1248/bpb.33.1070
  44. Oster, T. and Pillot, T. (2010) Docosahexaenoic acid and synaptic protection in Alzheimer's disease mice. Biochim. Biophys. Acta. 1801, 791-798. https://doi.org/10.1016/j.bbalip.2010.02.011
  45. Perez, S. E., Berg, B. M., Moore, K. A., He, B., Counts, S. E., Fritz, J. J., Hu, Y. S., Lazarov, O., Lah, J. J. and Mufson, E. J. (2010) DHA diet reduces AD pathology in young APPswe/PS1 Delta E9 transgenic mice: possible gender effects. J. Neurosci. Res. 88, 1026-1040.
  46. Pifferi, F., Roux, F., Langelier, B., Alessandri, J. M., Vancassel, S., Jouin, M., Lavialle, M. and Guesnet, P. (2005) (n-3) polyunsaturated fatty acid defi ciency reduces the expression of both isoforms of the brain glucose transporter GLUT1 in rats. J. Nutr. 135, 2241- 2246.
  47. Rapoport, S. I. and Igarashi, M. (2009) Can the rat liver maintain normal brain DHA metabolism in the absence of dietary DHA? Prostaglandins. Leukot. Essent. Fatty. Acids. 81, 119-123. https://doi.org/10.1016/j.plefa.2009.05.021
  48. Rosa, A. O. and Rapoport, S. I. (2009) Intracellular- and extracellular-derived $Ca^{2+}$ infl uence phospholipase A(2)-mediated fatty acid release from brain phospholipids. Biochim. Biophys. Acta. 1791, 697-705. https://doi.org/10.1016/j.bbalip.2009.03.009
  49. Sakamoto, T., Cansev, M. and Wurtman, R, J. (2007) Oral supplementation with docosahexaenoic acid and uridine-5'-monophosphate increases dendritic spine density in adult gerbil hippocampus. Brain Res. 1182, 50-59. https://doi.org/10.1016/j.brainres.2007.08.089
  50. Scott, B. L. and Bazan, N. G. (1989) Membrane docosahexaenoate is supplied to the developing brain and retina by the liver. Proc. Natl. Acad. Sci. USA. 86, 2903-2907. https://doi.org/10.1073/pnas.86.8.2903
  51. Shahdat, H., Hashimoto, M., Shimada, T. and Shido, O. (2004) Synaptic plasma membrane-bound acetylcholinesterase activity is not affected by docosahexaenoic acid-induced decrease in membrane order. Life Sci. 74, 3009-3024. https://doi.org/10.1016/j.lfs.2003.10.028
  52. Sharma, S., Ying, Z. and Gomez-Pinilla, F. (2010) A pyrazole curcumin derivative restores membrane homeostasis disrupted after brain trauma. Exp. Neurol. 226, 191-199. https://doi.org/10.1016/j.expneurol.2010.08.027
  53. Shrivastava, R., Vincent, B., Gobron, S., Cucuat, N. and John, G. W. (2005) Evidence for growth-promoting effects of omega n - 3 fatty acids alone and in combination with a specifi c vitamin and mineral complex in rat neuroblastoma cells. Nutr. Neurosci. 8, 317-321. https://doi.org/10.1080/10284150500510242
  54. Strokin, M., Sergeeva, M. and Reiser, G. (2003) Docosahexaenoic acid and arachidonic acid release in rat brain astrocytes is mediated by two separate isoforms of phospholipase A2 and is differently regulated by cyclic AMP and $Ca^{2+}$. Br. J. Pharmacol. 139, 1014-1022. https://doi.org/10.1038/sj.bjp.0705326
  55. Su, H. M. (2010) Mechanisms of n-3 fatty acid-mediated development and maintenance of learning memory performance. J. Nutr. Biochem. 21, 364-373. https://doi.org/10.1016/j.jnutbio.2009.11.003
  56. Utsunomiya, A., Owada, Y., Yoshimoto, T. and Kondo, H. (1997) Localization of mRNA for fatty acid transport protein in developing and mature brain of rats. Brain Res. Mol. Brain Res. 46, 217-222. https://doi.org/10.1016/S0169-328X(96)00303-8
  57. Walczewska, A., Stepien, T., Bewicz-Binkowska, D. and Zgorzynska, E. (2011) The role of docosahexaenoic acid in neuronal function. Postepy. Hig. Med. Dosw (Online). 65, 314-327. https://doi.org/10.5604/17322693.945763
  58. Wang, X., Zhao, X., Mao, Z. Y., Wang, X. M. and Liu, Z. L. (2003) Neuroprotective effect of docosahexaenoic acid on glutamateinduced cytotoxicity in rat hippocampal cultures. Neuroreport. 14, 2457-2461. https://doi.org/10.1097/00001756-200312190-00033
  59. Wu, A., Ying, Z. and Gomez-Pinilla, F. (2011) The salutary effects of DHA dietary supplementation on cognition, neuroplasticity, and membrane homeostasis after brain trauma. J. Neurotrauma. 28, 2113-2122. https://doi.org/10.1089/neu.2011.1872
  60. Wu, H., Ichikawa, S., Tani, C., Zhu, B., Tada, M., Shimoishi, Y., Murata, Y. and Nakamura, Y. (2009) Docosahexaenoic acid induces ERK1/2 activation and neuritogenesis via intracellular reactive oxygen species production in human neuroblastoma SH-SY5Y cells. Biochim. Biophys. Acta. 1791, 8-16. https://doi.org/10.1016/j.bbalip.2008.10.004
  61. Wurtman, R. J., Cansev, M., Sakamoto, T. and Ulus, I. H. (2009a) Use of phosphatide precursors to promote synaptogenesis. Annu. Rev. Nutr. 29, 59-87.
  62. Wurtman, R. J., Cansev, M. and Ulus, I. H. (2009b) Synapse formation is enhanced by oral administration of uridine and DHA, the circulating precursors of brain phosphatides. J. Nutr. Health Aging. 13, 189-197. https://doi.org/10.1007/s12603-009-0056-3
  63. Wurtman, R. J., Cansev, M., Sakamoto, T. and Ulus, I. (2010) Nutritional modifi ers of aging brain function: use of uridine and other phosphatide precursors to increase formation of brain synapses. Nutr. Rev. 68(Suppl 2), S88-101. https://doi.org/10.1111/j.1753-4887.2010.00344.x
  64. Zimmer, L., Hembert, S., Durand, G., Breton, P., Guilloteau, D., Besnard, J. C. and Chalon, S. (1998) Chronic n-3 polyunsaturated fatty acid diet-defi ciency acts on dopamine metabolism in the rat frontal cortex: a microdialysis study. Neurosci. Lett. 240, 177-181. https://doi.org/10.1016/S0304-3940(97)00938-5

Cited by

  1. Nutritional n-3 PUFAs deficiency during perinatal periods alters brain innate immune system and neuronal plasticity-associated genes vol.41, 2014, https://doi.org/10.1016/j.bbi.2014.03.021
  2. Membrane omega-3 fatty acids modulate the oligomerisation kinetics of adenosine A2A and dopamine D2 receptors vol.6, pp.1, 2016, https://doi.org/10.1038/srep19839
  3. Lack of Dietary Polyunsaturated Fatty Acids Causes Synapse Dysfunction in the Drosophila Visual System vol.10, pp.8, 2015, https://doi.org/10.1371/journal.pone.0135353
  4. Omega-3 fatty acids moderate effects of physical activity on cognitive function vol.59, 2014, https://doi.org/10.1016/j.neuropsychologia.2014.04.018
  5. Quantitative Erythrocyte Omega-3 EPA Plus DHA Levels are Related to Higher Regional Cerebral Blood Flow on Brain SPECT vol.58, pp.4, 2017, https://doi.org/10.3233/JAD-170281
  6. Polyunsaturated fatty acids and endocannabinoids in health and disease 2017, https://doi.org/10.1080/1028415X.2017.1347373
  7. Serum phosphatidylinositol as a biomarker for bipolar disorder liability vol.19, pp.2, 2017, https://doi.org/10.1111/bdi.12468
  8. Phosphatidylserine and the human brain vol.31, pp.6, 2015, https://doi.org/10.1016/j.nut.2014.10.014
  9. Recent developments in lipid metabolism in ruminants – the role of fat in maintaining animal health and performance vol.54, pp.10, 2014, https://doi.org/10.1071/AN14555
  10. Phosphatidylserine enhancesIKBKAPtranscription by activating the MAPK/ERK signaling pathway vol.25, pp.7, 2016, https://doi.org/10.1093/hmg/ddw011
  11. Docosahexaenoic acid prevents resistance to antiepileptic drugs in two animal models of drug-resistant epilepsy pp.1476-8305, 2018, https://doi.org/10.1080/1028415X.2017.1422903
  12. Effects of emulsifier type on physical and oxidative stabilities of algae il-in-water emulsions pp.09505423, 2018, https://doi.org/10.1111/ijfs.13981
  13. Comparative study on the independent and combined effects of omega-3 and vitamin B12 on phospholipids and phospholipase A2 as phospholipid hydrolyzing enzymes in PPA-treated rats as a model for autistic traits vol.17, pp.1, 2018, https://doi.org/10.1186/s12944-018-0850-1
  14. An update on intracerebral stem cell grafts vol.18, pp.7, 2018, https://doi.org/10.1080/14737175.2018.1491309
  15. Principal component analysis identifies differential gender-specific dietary patterns that may be linked to mental distress in human adults pp.1476-8305, 2018, https://doi.org/10.1080/1028415X.2018.1500198
  16. Antioxidative capacity of hydrolyzed rapeseed cake extract and oxidative stability of fish oil-in-water emulsion added with the extract vol.24, pp.4, 2012, https://doi.org/10.11002/kjfp.2017.24.4.529
  17. Inverse Phosphatidylcholine/Phosphatidylinositol Levels as Peripheral Biomarkers and Phosphatidylcholine/Lysophosphatidylethanolamine-Phosphatidylserine as Hippocampal Indicator of Postischemic Cognit vol.12, pp.None, 2012, https://doi.org/10.3389/fnins.2018.00989
  18. Relationship between diet, the gut microbiota, and brain function vol.76, pp.8, 2012, https://doi.org/10.1093/nutrit/nuy016
  19. Docosahexaenoic Acid: Outlining the Therapeutic Nutrient Potential to Combat the Prenatal Alcohol-Induced Insults on Brain Development vol.11, pp.3, 2012, https://doi.org/10.1093/advances/nmz135
  20. OMEGA-3 Interventions in Alcohol Dependence and Related Outcomes: A Systematic Review and Propositions vol.18, pp.5, 2020, https://doi.org/10.2174/1570159x18666200128120729
  21. Docosahexaenoic Acid (DHA, C22:6, ω-3) Composition of Milk and Mammary Gland Tissues of Lactating Mother Rats Is Severely Affected by Lead (Pb) Exposure vol.195, pp.2, 2012, https://doi.org/10.1007/s12011-019-01878-1
  22. Cross-talk between lipid homeostasis and endoplasmic reticulum stress in neurodegeneration: Insights for HIV-1 associated neurocognitive disorders (HAND) vol.141, pp.None, 2012, https://doi.org/10.1016/j.neuint.2020.104880
  23. Early Lipid Intake Improves Cerebellar Growth in Very Low‐Birth‐Weight Preterm Infants vol.45, pp.3, 2012, https://doi.org/10.1002/jpen.1868
  24. Lipid Intake and Neurodevelopment in Preterm Infants vol.22, pp.6, 2012, https://doi.org/10.1542/neo.22-6-e370
  25. The association between plasma metabolites and sleep quality in the Southall and Brent Revisited (SABRE) Study: A cross‐sectional analysis vol.30, pp.4, 2012, https://doi.org/10.1111/jsr.13245
  26. Smoflipid Is Better Than Lipofundin for Long-Term Neurodevelopmental Outcomes in Preterm Infants vol.13, pp.8, 2012, https://doi.org/10.3390/nu13082548
  27. An overview on the role of microalgal metabolites and pigments in apoptosis induction against copious diseases vol.60, pp.None, 2012, https://doi.org/10.1016/j.algal.2021.102556
  28. The effect of omega-3 long chain polyunsaturated fatty acids on aggressive behaviour in adult male prisoners: a structured study protocol for a multi-centre, double-blind, randomised placebo-controlle vol.22, pp.1, 2021, https://doi.org/10.1186/s13063-021-05252-2