Dietary docosahexaenoic acid alleviates autistic-like behaviors resulting from maternal immune activation in mice

Prostaglandins Leukotrienes and Essential Fatty Acids

Volumn 106, Issue , 2016, Pages 27-37

  Weiser, Michael J ^c   Mucha, Brittany ^a   Denheyer, Heather ^a   Atkinson, Devon ^a   Schanz, Norman ^a   Vassiliou, Evros ^b   Benno, Robert H ^a  

^a WILLIAM PATERSON UNIVERSITY   (United States)

^b KEAN UNIVERSITY   (United States)

^c DSM NUTRITIONAL PRODUCTS   (United States)

Author keywords

Development; Maternal immune activation; Nutrition; Omega 3 fatty acids; Pregnancy; Social behavior

Indexed keywords

ARACHIDONIC ACID; DOCOSAHEXAENOIC ACID; OMEGA 3 FATTY ACID; POLYNUCLEOTIDE; POLYRIBOINOSINIC-POLYRIBOCYTIDYLIC ACID;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTISM; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG EFFICACY; FATTY ACID ANALYSIS; FEMALE; FOOD COMPOSITION; IMMUNE RESPONSE; LIPID COMPOSITION; LOW FAT DIET; MOUSE; NONHUMAN; OPEN FIELD TEST; POST HOC ANALYSIS; PRIORITY JOURNAL; SOCIAL BEHAVIOR; VOCALIZATION; ADVERSE EFFECTS; ANIMAL; AUTISTIC DISORDER; DIETARY SUPPLEMENT; DISEASE MODEL; DRUG EFFECTS; EMBRYO DEVELOPMENT; FETOMATERNAL TRANSFUSION; IMMUNE SYSTEM; MALE; MATERNAL EXPOSURE; PREGNANCY;

ANIMALS; AUTISTIC DISORDER; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; EMBRYONIC DEVELOPMENT; FEMALE; IMMUNE SYSTEM; MALE; MATERNAL EXPOSURE; MATERNAL-FETAL EXCHANGE; MICE; POLYNUCLEOTIDES; PREGNANCY;

EID: 84959463204     PISSN: 09523278     EISSN: 15322823     Source Type: Journal    
DOI: 10.1016/j.plefa.2015.10.005     Document Type: Article

References (78)

1. Baxter A.J., Brugha T.S., Erskine H.E., Scheurer R.W., Vos T., Scott J.G. The epidemiology and global burden of autism spectrum disorders. Psychol. Med. 2015, 45:601-613. S003329171400172X [pii]. 10.1017/S003329171400172X.
2. Newschaffer C.J., Croen L.A., Daniels J., Giarelli E., Grether J.K., Levy S.E., Mandell D.S., Miller L.A., Pinto-Martin J., Reaven J., Reynolds A.M., Rice C.E., Schendel D., Windham G.C. The epidemiology of autism spectrum disorders. Annu. Rev. Public Health 2007, 28:235-258. 10.1146/annurev.publhealth.28.021406.144007.
3. Brown A.S., Sourander A., Hinkka-Yli-Salomaki S., McKeague I.W., Sundvall J., Surcel H.M. Elevated maternal C-reactive protein and autism in a national birth cohort. Mol. Psychiatry 2014, 19:259-264. mp2012197 [pii]. 10.1038/mp.2012.197.
4. Patterson P.H. Maternal infection and immune involvement in autism. Trends Mol. Med. 2011, 17:389-394. S1471-4914(11)00049-9 [pii]. 10.1016/j.molmed.2011.03.001.
5. Boksa P. Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav. Immun. 2010, 24:881-897. S0889-1591(10)00058-9 [pii]. 10.1016/j.bbi.2010.03.005.
6. Meyer U., Feldon J. Epidemiology-driven neurodevelopmental animal models of schizophrenia. Prog. Neurobiol. 2010, 90:285-326. S0301-0082(09)00169-5 [pii]. 10.1016/j.pneurobio.2009.10.018.
7. Schwartzer J.J., Careaga M., Onore C.E., Rushakoff J.A., Berman R.F., Ashwood P. Maternal immune activation and strain specific interactions in the development of autism-like behaviors in mice. Transl. Psychiatry 2013, 3:e240. tp201316 [pii]. 10.1038/tp.2013.16.
8. Malkova N.V., Yu C.Z., Hsiao E.Y., Moore M.J., Patterson P.H. Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism. Brain Behav. Immun. 2012, 26:607-616. S0889-1591(12)00013-X [pii]. 10.1016/j.bbi.2012.01.011.
9. Meyer U., Feldon J., Fatemi S.H. In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci. Biobehav. Rev. 2009, 33:1061-1079. S0149-7634(09)00071-2 [pii]. 10.1016/j.neubiorev.2009.05.001.
10. Pacheco-Lopez G., Giovanoli S., Langhans W., Meyer U. Priming of metabolic dysfunctions by prenatal immune activation in mice: relevance to schizophrenia. Schizophr. Bull. 2013, 39:319-329. sbr178 [pii]. 10.1093/schbul/sbr178.
11. Howland J.G., Cazakoff B.N., Zhang Y. Altered object-in-place recognition memory, prepulse inhibition, and locomotor activity in the offspring of rats exposed to a viral mimetic during pregnancy. Neuroscience 2012, 201:184-198. S0306-4522(11)01278-4 [pii]. 10.1016/j.neuroscience.2011.11.011.
12. Makrides M., Neumann M.A., Byard R.W., Simmer K., Gibson R.A. Fatty acid composition of brain, retina, and erythrocytes in breast- and formula-fed infants. Am. J. Clin. Nutr. 1994, 60:189-194.
13. Innis S.M. Essential fatty acid transfer and fetal development. Placenta 2005, 26(Suppl. A):S70-S75. doi:S0143-4004(05)00036-6 [pii]10.1016/j.placenta.2005.01.005.
14. Innis S.M. Human milk: maternal dietary lipids and infant development. Proc. Nutr. Soc. 2007, 66:397-404. doi:S0029665107005666 [pii]10.1017/S0029665107005666.
15. Trumbo P., Schlicker S., Yates A.A., Poos M. Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein and amino acids. J. Am. Diet. Assoc. 2002, 102:1621-1630.
16. Brenna J.T., Salem N., Sinclair A.J., Cunnane S.C. A. International Society for the Study of Fatty, I. Lipids, alpha-Linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prostaglandins, Leukot. Essent. Fatty Acids 2009, 80:85-91. 10.1016/j.plefa.2009.01.004.
17. Bradbury J. Docosahexaenoic acid (DHA): an ancient nutrient for the modern human brain. Nutrients 2011, 3:529-554. nutrients-03-00529 [pii]. 10.3390/nu3050529.
18. Guesnet P., Alessandri J.M. Docosahexaenoic acid (DHA) and the developing central nervous system (CNS)-Implications for dietary recommendations. Biochimie 2011, 93:7-12. S0300-9084(10)00182-3 [pii]. 10.1016/j.biochi.2010.05.005.
19. Brenna J.T., Carlson S.E. Docosahexaenoic acid and human brain development: evidence that a dietary supply is needed for optimal development. J. Hum. Evol. 2014, 77:99-106. S0047-2484(14)00083-9 [pii]. 10.1016/j.jhevol.2014.02.017.
20. Brenna J.T. Animal studies of the functional consequences of suboptimal polyunsaturated fatty acid status during pregnancy, lactation and early post-natal life. Matern. Child. Nutr. 2011, 7:59-79. Suppl 2. 10.1111/j.1740-8709.2011.00301.x.
21. Fedorova I., Alvheim A.R., Hussein N., Salem N. Deficit in prepulse inhibition in mice caused by dietary n-3 fatty acid deficiency. Behav. Neurosci. 2009, 123:1218-1225. 2009-23588-007 [pii]. 10.1037/a0017446.
22. Weiser M.J., Wynalda K., Salem N., Butt C.M. Dietary DHA during development affects depression-like behaviors and biomarkers that emerge after puberty in adolescent rats. J. Lipid Res. 2015, 56:151-166. jlr.M055558 [pii]. 10.1194/jlr.M055558.
23. Colombo J., Kannass K.N., Shaddy D.J., Kundurthi S., Maikranz J.M., Anderson C.J., Blaga O.M., Carlson S.E. Maternal DHA and the development of attention in infancy and toddlerhood. Child. Dev. 2004, 75:1254-1267. 10.1111/j.1467-8624.2004.00737.x.
24. Jensen C.L., Voigt R.G., Prager T.C., Zou Y.L., Fraley J.K., Rozelle J.C., Turcich M.R., Llorente A.M., Anderson R.E., Heird W.C. Effects of maternal docosahexaenoic acid intake on visual function and neurodevelopment in breastfed term infants. Am. J. Clin. Nutr. 2005, 82:125-132.
25. Richardson A.J., Burton J.R., Sewell R.P., Spreckelsen T.F., Montgomery P. Docosahexaenoic acid for reading, cognition and behavior in children aged 7-9 years: a randomized, controlled trial (the DOLAB Study). PLoS One 2012, 7:e43909. 10.1371/journal.pone.0043909.
26. van Elst K., Bruining H., Birtoli B., Terreaux C., Buitelaar J.K., Kas M.J. Food for thought: dietary changes in essential fatty acid ratios and the increase in autism spectrum disorders. Neurosci. Biobehav. Rev. 2014, 45:369-378. S0149-7634(14)00168-7 [pii]. 10.1016/j.neubiorev.2014.07.004.
27. Orr S.K., Palumbo S., Bosetti F., Mount H.T., Kang J.X., Greenwood C.E., Ma D.W., Serhan C.N., Bazinet R.P. Unesterified docosahexaenoic acid is protective in neuroinflammation. J. Neurochem. 2013, 127:378-393. 10.1111/jnc.12392.
28. Reeves P.G., Nielsen F.H., Fahey G.C. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 1993, 123:1939-1951.
29. Reeves P.G., Rossow K.L., Lindlauf J. Development and testing of the AIN-93 purified diets for rodents: results on growth, kidney calcification and bone mineralization in rats and mice. J. Nutr. 1993, 123:1923-1931.
30. Meyer U., Nyffeler M., Schwendener S., Knuesel I., Yee B.K., Feldon J. Relative prenatal and postnatal maternal contributions to schizophrenia-related neurochemical dysfunction after in utero immune challenge. Neuropsychopharmacology 2008, 33:441-456. doi:1301413 [pii]10.1038/sj.npp.1301413.
31. Defensor E.B., Pearson B.L., Pobbe R.L., Bolivar V.J., Blanchard D.C., Blanchard R.J. A novel social proximity test suggests patterns of social avoidance and gaze aversion-like behavior in BTBR T+ tf/J mice. Behav. Brain Res. 2011, 217:302-308. S0166-4328(10)00718-7 [pii]. 10.1016/j.bbr.2010.10.033.
32. McFarlane H.G., Kusek G.K., Yang M. J.L. Phoenix, V.J. Bolivar, J.N. Crawley, Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes Brain Behav. 2008, 7:152-163. doi:GBB330 [pii]10.1111/j.1601-183X.2007.00330.x.
33. Ta T.A., Koenig C.M., Golub M.S., Pessah I.N., Qi L., Aronov P.A., Berman R.F. Bioaccumulation and behavioral effects of 2,2',4,4'-tetrabromodiphenyl ether (BDE-47) in perinatally exposed mice. Neurotoxicol Teratol. 2011, 33:393-404. S0892-0362(11)00010-9 [pii]. 10.1016/j.ntt.2011.02.003.
34. Kuratko C.N., Salem N. Biomarkers of DHA status. Prostaglandins Leukot. Essent. Fatty Acids 2009, 81:111-118. S0952-3278(09)00098-2 [pii]. 10.1016/j.plefa.2009.05.007.
35. Murray C., Griffin E.W., O'Loughlin E., Lyons A., Sherwin E., Ahmed S., Stevenson N.J., Harkin A., Cunningham C. Interdependent and independent roles of type I interferons and IL-6 in innate immune, neuroinflammatory and sickness behaviour responses to systemic poly I:C. Brain Behav. Immun. 2015, 48:274-286. S0889-1591(15)00114-2 [pii]. 10.1016/j.bbi.2015.04.009.
36. Orr S.K., Bazinet R.P. The emerging role of docosahexaenoic acid in neuroinflammation. Curr. Opin. Investig. Drugs 2008, 9:735-743.
37. Simopoulos A.P. The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed. Pharmacother. 2002, 56:365-379.
38. Jones K.L., Will M.J., Hecht P.M., Parker C.L., Beversdorf D.Q. Maternal diet rich in omega-6 polyunsaturated fatty acids during gestation and lactation produces autistic-like sociability deficits in adult offspring. Behav. Brain Res. 2013, 238:193-199. S0166-4328(12)00678-X [pii]. 10.1016/j.bbr.2012.10.028.
39. Brigandi S.A., Shao H., Qian S.Y., Shen Y., Wu B.L., Kang J.X. Autistic children exhibit decreased levels of essential Fatty acids in red blood cells. Int. J. Mol. Sci. 2015, 16:10061-10076. ijms160510061 [pii]. 10.3390/ijms160510061.
40. Faa G., Marcialis M.A., Ravarino A., Piras M., Pintus M.C., Fanos V. Fetal programming of the human brain: is there a link with insurgence of neurodegenerative disorders in adulthood?. Curr. Med. Chem. 2014, 21:3854-3876. doi:CMC-EPUB-60776 [pii].
41. Velten M., Britt R.D., Heyob K.M., Tipple T.E., Rogers L.K. Maternal dietary docosahexaenoic acid supplementation attenuates fetal growth restriction and enhances pulmonary function in a newborn mouse model of perinatal inflammation. J. Nutr. 2014, 144:258-266. jn.113.179259 [pii]. 10.3945/jn.113.179259.
42. Clandinin M.T., Van Aerde J.E., Merkel K.L., Harris C.L., Springer M.A., Hansen J.W., Diersen-Schade D.A. Growth and development of preterm infants fed infant formulas containing docosahexaenoic acid and arachidonic acid. J. Pediatr. 2005, 146:461-468. doi:S0022347604011175 [pii]10.1016/j.jpeds.2004.11.030.
43. Innis S.M., Adamkin D.H., Hall R.T., Kalhan S.C., Lair C., Lim M., Stevens D.C., Twist P.F., Diersen-Schade D.A., Harris C.L., Merkel K.L., Hansen J.W. Docosahexaenoic acid and arachidonic acid enhance growth with no adverse effects in preterm infants fed formula. J. Pediatr. 2002, 140:547-554. doi:S0022-3476(02)58526-7 [pii]10.1067/mpd.2002.123282.
44. Burghardt P.R., Kemmerer E.S., Buck B.J., Osetek A.J., Yan C., Koch L.G., Britton S.L., Evans S.J. Dietary n-3:n-6 fatty acid ratios differentially influence hormonal signature in a rodent model of metabolic syndrome relative to healthy controls. Nutr. Metab. (Lond.) 2010, 7:53. 1743-7075-7-53 [pii]. 10.1186/1743-7075-7-53.
45. Crawley J.N. Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol. 2007, 17:448-459. doi:BPA096 [pii] 10.1111/j.1750-3639.2007.00096.x.
46. Silverman J.L., Yang M., Lord C., Crawley J.N. Behavioural phenotyping assays for mouse models of autism. Nat. Rev. Neurosci. 2010, 11:490-502. [pii]. 10.1038/nrn2851nrn2851.
47. Scattoni M.L., Gandhy S.U., Ricceri L., Crawley J.N. Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism. PLoS One 2008, 3:e3067. 10.1371/journal.pone.0003067.
48. Hahn M.E., Karkowski L., Weinreb L., Henry A., Schanz N., Hahn E.M. Genetic and developmental influences on infant mouse ultrasonic calling. II. Developmental patterns in the calls of mice 2-12 days of age. Behav. Genet. 1998, 28:315-325.
49. Pietropaolo S., Guilleminot A., Martin B., D'Amato F.R., Crusio W.E. Genetic-background modulation of core and variable autistic-like symptoms in Fmr1 knock-out mice. PLoS One 2011, 6:e17073. 10.1371/journal.pone.0017073.
50. Weylandt K.H., Chiu C.Y., Gomolka B., Waechter S.F., Wiedenmann B. Omega-3 fatty acids and their lipid mediators: towards an understanding of resolvin and protectin formation. Prostaglandins Other Lipid Mediat. 2012, 97:73-82. S1098-8823(12)00020-2 [pii]. 10.1016/j.prostaglandins.2012.01.005.
51. Ariel A., Serhan C.N. Resolvins and protectins in the termination program of acute inflammation. Trends Immunol. 2007, 28:176-183. doi:S1471-4906(07)00049-X [pii] 10.1016/j.it.2007.02.007.
52. Bazan N.G. Cell survival matters: docosahexaenoic acid signaling, neuroprotection and photoreceptors. Trends Neurosci. 2006, 29:263-271. doi:S0166-2236(06)00068-3 [pii]10.1016/j.tins.2006.03.005.
53. Carrie I., Clement M., de Javel D., Frances H., Bourre J.M. Phospholipid supplementation reverses behavioral and biochemical alterations induced by n-3 polyunsaturated fatty acid deficiency in mice. J. Lipid Res. 2000, 41:473-480.
54. Takeuchi T., Iwanaga M., Harada E. Possible regulatory mechanism of DHA-induced anti-stress reaction in rats. Brain Res. 2003, 964:136-143. doi:S0006899302041136 [pii].
55. Belzung C., Leguisquet A.M., Barreau S., Delion-Vancassel S., Chalon S., Durand G. Alpha-linolenic acid deficiency modifies distractibility but not anxiety and locomotion in rats during aging. J. Nutr. 1998, 128:1537-1542.
56. Moriguchi T., Greiner R.S., Salem N. Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. J. Neurochem. 2000, 75:2563-2573.
57. Fedorova I., Salem N. Omega-3 fatty acids and rodent behavior. Prostaglandins Leukot. Essent. Fatty Acids 2006, 75:271-289. doi:S0952-3278(06)00120-7 [pii] 10.1016/j.plefa.2006.07.006.
58. Meyer U., Engler A., Weber L., Schedlowski M., Feldon J. Preliminary evidence for a modulation of fetal dopaminergic development by maternal immune activation during pregnancy. Neuroscience 2008, 154:701-709. S0306-4522(08)00597-6 [pii]. 10.1016/j.neuroscience.2008.04.031.
59. Ozawa K., Hashimoto K., Kishimoto T., Shimizu E., Ishikura H., Iyo M. Immune activation during pregnancy in mice leads to dopaminergic hyperfunction and cognitive impairment in the offspring: a neurodevelopmental animal model of schizophrenia. Biol. Psychiatry 2006, 59:546-554. doi:S0006-3223(05)00920-0 [pii]10.1016/j.biopsych.2005.07.031.
60. Zuckerman L., Rehavi M., Nachman R., Weiner I. Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: a novel neurodevelopmental model of schizophrenia. Neuropsychopharmacology 2003, 28:1778-1789. 1300248 [pii]. 10.1038/sj.npp.1300248.
61. Fu Y., Yuan Y., Halliday G., Rusznak Z., Watson C., Paxinos G. A cytoarchitectonic and chemoarchitectonic analysis of the dopamine cell groups in the substantia nigra, ventral tegmental area, and retrorubral field in the mouse. Brain Struct. Funct. 2012, 217:591-612. 10.1007/s00429-011-0349-2.
62. McNamara R.K., Sullivan J., Richtand N.M., Jandacek R., Rider T., Tso P., Campbell N., Lipton J. Omega-3 fatty acid deficiency augments amphetamine-induced behavioral sensitization in adult DBA/2J mice: relationship with ventral striatum dopamine concentrations. Synapse 2008, 62:725-735. 10.1002/syn.20542.
63. Deleidi M., Hallett P.J., Koprich J.B., Chung C.Y., Isacson O. The Toll-like receptor-3 agonist polyinosinic:polycytidylic acid triggers nigrostriatal dopaminergic degeneration. J. Neurosci. 2010, 30:16091-16101. 30/48/16091 [pii]. 10.1523/JNEUROSCI.2400-10.2010.
64. Smith S.E., Li J., Garbett K., Mirnics K., Patterson P.H. Maternal immune activation alters fetal brain development through interleukin-6. J. Neurosci. 2007, 27:10695-10702. doi:27/40/10695 [pii]10.1523/JNEUROSCI.2178-07.2007.
65. Garay P.A., Hsiao E.Y., Patterson P.H., McAllister A.K. Maternal immune activation causes age- and region-specific changes in brain cytokines in offspring throughout development. Brain Behav. Immun. 2013, 31:54-68. S0889-1591(12)00191-2 [pii]. 10.1016/j.bbi.2012.07.008.
66. Endres S., Ghorbani R., Kelley V.E., Georgilis K., Lonnemann G., van der Meer J.W., Cannon J.G., Rogers T.S., Klempner M.S., Weber P.C., et al. The effect of dietary supplementation with n-3 polyunsaturated fatty acids on the synthesis of interleukin-1 and tumor necrosis factor by mononuclear cells. N Engl. J. Med. 1989, 320:265-271. 10.1056/NEJM198902023200501.
67. Weldon S.M., Mullen A.C., Loscher C.E., Hurley L.A., Roche H.M. Docosahexaenoic acid induces an anti-inflammatory profile in lipopolysaccharide-stimulated human THP-1 macrophages more effectively than eicosapentaenoic acid. J. Nutr. Biochem. 2007, 18:250-258. doi:S0955-2863(06)00103-3 [pii]10.1016/j.jnutbio.2006.04.003.
68. Bale T.L., Baram T.Z., Brown A.S., Goldstein J.M., Insel T.R., McCarthy M.M., Nemeroff C.B., Reyes T.M., Simerly R.B., Susser E.S., Nestler E.J. Early life programming and neurodevelopmental disorders. Biol. Psychiatry 2010, 68:314-319. S0006-3223(10)00527-5 [pii]. 10.1016/j.biopsych.2010.05.028.
69. Dietert R.R., Dietert J.M. Potential for early-life immune insult including developmental immunotoxicity in autism and autism spectrum disorders: focus on critical windows of immune vulnerability. J. Toxicol. Environ. Health B Critic. Rev. 2008, 11:660-680. 903024619 [pii]. 10.1080/10937400802370923.
70. Khashan A.S., Abel K.M., McNamee R., Pedersen M.G., Webb R.T., Baker P.N., Kenny L.C., Mortensen P.B. Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch. Gen. Psychiatry 2008, 65:146-152. 65/2/146 [pii]. 10.1001/archgenpsychiatry.2007.20.
71. Luo Z.C., Xiao L., Nuyt A.M. Mechanisms of developmental programming of the metabolic syndrome and related disorders. World J. Diabetes 2010, 1:89-98. 10.4239/wjd.v1.i3.89.
72. Mathieu G., Oualian C., Denis I., Lavialle M., Gisquet-Verrier P., Vancassel S. Dietary n-3 polyunsaturated fatty acid deprivation together with early maternal separation increases anxiety and vulnerability to stress in adult rats. Prostaglandins Leukot. Essent. Fatty Acids 2011, 85:129-136. S0952-3278(11)00096-2 [pii]. 10.1016/j.plefa.2011.07.001.
73. 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., Laye S., Manzoni O.J. Nutritional omega-3 deficiency abolishes endocannabinoid-mediated neuronal functions. Nat. Neurosci. 2011, 14:345-350. nn.2736 [pii]. 10.1038/nn.2736.
74. Larrieu T., Hilal M.L., Fourrier C., De Smedt-Peyrusse V., Sans N., Capuron L., Laye S. Nutritional omega-3 modulates neuronal morphology in the prefrontal cortex along with depression-related behaviour through corticosterone secretion. Transl. Psychiatry 2014, 4:e437. tp201477 [pii]. 10.1038/tp.2014.77.
75. Larrieu T., Madore C., Joffre C., Laye S. Nutritional n-3 polyunsaturated fatty acids deficiency alters cannabinoid receptor signaling pathway in the brain and associated anxiety-like behavior in mice. J. Physiol. Biochem. 2012, 68:671-681. 10.1007/s13105-012-0179-6.
76. Dunstan J.A., Mori T.A., Barden A., Beilin L.J., Taylor A.L., Holt P.G., Prescott S.L. Fish oil supplementation in pregnancy modifies neonatal allergen-specific immune responses and clinical outcomes in infants at high risk of atopy: a randomized, controlled trial. J. Allergy Clin. Immunol. 2003, 112:1178-1184. S0091674903022711 [pii]. 10.1016/j.jaci.2003.09.009.
77. Dunstan J.A., Mori T.A., Barden A., Beilin L.J., Taylor A.L., Holt P.G., Prescott S.L. Maternal fish oil supplementation in pregnancy reduces interleukin-13 levels in cord blood of infants at high risk of atopy. Clin. Exp. Allergy 2003, 33:442-448. doi:1590 [pii].
78. Bourre J.M., Francois M., Youyou A., Dumont O., Piciotti M., Pascal G., Durand G. The effects of dietary alpha-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. J. Nutr. 1989, 119:1880-1892.