Combined deficiency of iron and (n-3) fatty acids in male rats disrupts brain monoamine metabolism and produces greater memory deficits than iron deficiency or (n-3) fatty acid deficiency alone

Journal of Nutrition

Volumn 142, Issue 8, 2012, Pages 1463-1471

  Baumgartner, Jeannine ^a,b   Smuts, Cornelius M ^b   Malan, Linda ^b   Arnold, Myrtha ^a   Yee, Benjamin K ^a,c   Bianco, Laura E ^d   Boekschoten, Mark V ^e   Müller, Michael ^e   Langhans, Wolfgang ^a   Hurrell, Richard F ^a   Zimmermann, Michael B ^a,e  

^a ETH ZURICH   (Switzerland)

^b NORTH WEST UNIVERSITY   (South Africa)

^c LEGACY RESEARCH   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

^e WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN ENZYME; CARBOXYLYASE; DIHYDROXYPHENYLACETIC ACID; DOPAMINE; IRON; MONOAMINE; NORADRENALIN; OMEGA 3 FATTY ACID; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BRAIN METABOLISM; BRAIN WEIGHT; CATECHOLAMINE BRAIN LEVEL; CONTROLLED STUDY; CORPUS STRIATUM; DIETARY INTAKE; DOPAMINE BRAIN LEVEL; DOWN REGULATION; ESSENTIAL FATTY ACID DEFICIENCY; FEMALE; FOOD INTAKE; FRONTAL CORTEX; GENE EXPRESSION; HIPPOCAMPUS; IRON DEFICIENCY; LIPID BRAIN LEVEL; MALE; MAZE TEST; MONOAMINE METABOLISM; NONHUMAN; NORADRENALIN BRAIN LEVEL; OLFACTORY BULB; PERINATAL PERIOD; RAT; REFERENCE MEMORY; SEROTONIN BRAIN LEVEL; SEX DIFFERENCE; SPATIAL MEMORY; TASK PERFORMANCE; TISSUE MICROARRAY; WEANING; WEIGHT GAIN; WORKING MEMORY;

ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; BIOGENIC MONOAMINES; BRAIN; DIET; FATTY ACIDS, OMEGA-3; FEMALE; GENE EXPRESSION REGULATION; IRON; MALE; MAZE LEARNING; MEMORY DISORDERS; PHOSPHOLIPIDS; PROTEIN ARRAY ANALYSIS; RANDOM ALLOCATION; RATS;

RATTUS;

EID: 84866282824     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.111.156281     Document Type: Article

References (54)

1. Zimmermann MB, Hurrell RF. Nutritional iron deficiency. Lancet. 2007;370:511-20.
2. Briend A, Dewey KG, Reinhart GA. Fatty acid status in early life in lowincome countries: overview of the situation, policy and research priorities. Matern Child Nutr. 2011;7 Suppl 2:141-8.
3. Bryan J, Osendarp S, Hughes D, Calvaresi E, Baghurst K, van Klinken JW. Nutrients for cognitive development in school-aged children. Nutr Rev. 2004;62:295-306.
4. Connor JR, Menzies SL. Relationship of iron to oligodendrocytes and myelination. Glia. 1996;17:83-93.
5. Beard JL, Connor JR. Iron status and neural functioning. Annu Rev Nutr. 2003;23:41-58.
6. Lozoff B, Georgieff MK. Iron deficiency and brain development. Semin Pediatr Neurol. 2006;13:158-65.
7. LeBlanc CP, Fiset S, Surette ME, O'Brien HT, Rioux FM. Maternal iron deficiency alters essential fatty acid and eicosanoid metabolism and increases locomotion in adult guinea pig offspring. J Nutr. 2009;139:1653-9.
8. Todorich B, Pasquini JM, Garcia CI, Paez PM, Connor JR. Oligodendrocytes and myelination: the role of iron. Glia. 2009;57:467-78.
9. Beard JL. Why iron deficiency is important in infant development. J Nutr. 2008;138:2534-6.
10. Thatcher RW. Maturation of the human frontal lobes: physiological evidence for staging. Dev Neuropsychol. 1991;7:397-419.
11. Uauy R, Dangour AD. Nutrition in brain development and aging: role of essential fatty acids. Nutr Rev. 2006;64:S24-33; discussion S72-91.
12. Salvati S, Natali F, Attorri L, Di Benedetto R, Leonardi F, Di Biase A, Ferri F, Fortuna S, Lorenzini P, Sanchez M, et al. Eicosapentaenoic acid stimulates the expression of myelin proteins in rat brain. J Neurosci Res. 2008;86:776-84.
13. Calder PC, Grimble RF. Polyunsaturated fatty acids, inflammation and immunity. Eur J Clin Nutr. 2002;56 Suppl 3:S14-9.
14. Chalon S. Omega-3 fatty acids and monoamine neurotransmission. Prostaglandins Leukot Essent Fatty Acids. 2006;75:259-69.
15. Su KP. Biological mechanism of antidepressant effect of omega-3 fatty acids: how does fish oil act as a mind-body interface? Neurosignals. 2009;17:144-52.
16. Uauy R, Mena P, Rojas C. Essential fatty acids in early life: structural and functional role. Proc Nutr Soc. 2000;59:3-15.
17. Nakamura MT, Nara TY. Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases. Annu Rev Nutr. 2004;24:345-76.
18. Smith WL, Marnett LJ. Prostaglandin endoperoxide synthase: structure and catalysis. Biochim Biophys Acta. 1991;1083:1-17.
19. Reeves PG, Nielsen FH, Fahey GC Jr. 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;123:1939-51.
20. Erikson KM, Pinero DJ, Connor JR, Beard JL. Regional brain iron, ferritin and transferrin concentrations during iron deficiency and iron repletion in developing rats. J Nutr. 1997;127:2030-8.
21. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226:497-509.
22. Nelson C, Erikson K, Pinero DJ, Beard JL. In vivo dopamine metabolism is altered in iron-deficient anemic rats. J Nutr. 1997;127: 2282-8.
23. Bianco LE, Wiesinger J, Earley CJ, Jones BC, Beard JL. Iron deficiency alters dopamine uptake and response to L-DOPA injection in Sprague-Dawley rats. J Neurochem. 2008;106:205-15.
24. de Wilde J, Mohren R, van den Berg S, Boekschoten M, Dijk KWV, de Groot P, Muller M, Mariman E, Smit E. Short-term high fat-feeding results in morphological and metabolic adaptations in the skeletal muscle of C57BL/6J mice. Physiol Genomics. 2008;32:360-9.
25. Honig WK. Studies of working memory in the pigeon. In: Hulse SH, Fowler H, Honig WK, editors. Cognitive processes in animal behaviour. Hillsdale (NJ): Erlbaum; 1978. p. 211-48.
26. Sartor MA, Tomlinson CR, Wesselkamper SC, Sivaganesan S, Leikauf GD, Medvedovic M. Intensity-based hierarchical Bayes method improves testing for differentially expressed genes in microarray experiments. BMC Bioinformatics. 2006;7:538.
27. Fretham SJB, Carlson ES, Georgieff MK. The role of iron in learning and memory. Adv Nutr. 2011;2:112-21.
28. Lapiz MD, Fulford A, Muchimapura S, Mason R, Parker T, Marsden CA. Influence of postweaning social isolation in the rat on brain development, conditioned behavior, and neurotransmission. Neurosci Behav Physiol. 2003;33:13-29.
29. Schuchardt JP, Huss M, Stauss-Grabo M, Hahn A. Significance of longchain polyunsaturated fatty acids (PUFAs) for the development and behaviour of children. Eur J Pediatr. 2010;169:149-64.
30. Wainwright PE, Huang YS, Coscina DV, Lévesque S, McCutcheon D. Brain and behavioral effects of dietary n-3 deficiency in mice: a three generational study. Dev Psychobiol. 1994;27:467-87.
31. Moriguchi T, Loewke J, Garrison M, Catalan JN, Salem N Jr. Reversal of docosahexaenoic acid deficiency in the rat brain, retina, liver, and serum. J Lipid Res. 2001;42:419-27.
32. Tinoco SM, Sichieri R, Setta CL, Moura AS, Carmo MG. n-3 polyunsaturated fatty acids in milk is associate to weight gain and growth in premature infants. Lipids Health Dis. 2009;8:23.
33. Cooke RW, Lucas A, Yudkin PL, Pryse-Davies J. Head circumference as an index of brain weight in the fetus and newborn. Early Hum Dev. 1977;1:145-9.
34. Felt BT, Beard JL, Schallert T, Shao J, Aldridge JW, Connor JR, Georgieff MK, Lozoff B. Persistent neurochemical and behavioral abnormalities in adulthood despite early iron supplementation for perinatal iron deficiency anemia in rats. Behav Brain Res. 2006;171:261-70.
35. Beard JL, Chen Q, Connor J, Jones BC. Altered monoamine metabolism in caudate-putamen of iron-deficicent rats. Pharmacol Biochem Behav. 1994;48:621-4.
36. Beard JL, Felt B, Schallert T, Burhans M, Connor JR, Georgieff MK. Moderate iron deficiency in infancy: biology and behavior in young rats. Behav Brain Res. 2006;170:224-32.
37. Erikson KM, Jones BC, Beard JL. Iron deficiency alters dopamine transporter functioning in rat striatum. J Nutr. 2000;130:2831-7.
38. Erikson KM, Jones BC, Hess EJ, Zhang Q, Beard JL. Iron deficiency decreases dopamine D-1 and D-2 receptors in rat brain. Pharmacol Biochem Behav. 2001;69:409-18.
39. Bianco LE, Unger EL, Beard J. Iron deficiency and neuropharmacology. In: Iron deficiency and overload: from basic biology to clinical medicine. New York: Humana Press; 2010. p. 141-58.
40. Zimmer L, Vancassel S, Cantagrel S, Breton P, Delamanche S, Guilloteau D, Durand G, Chalon S. The dopamine mesocorticolimbic pathway is affected by deficiency in n-3 polyunsaturated fatty acids. Am J Clin Nutr. 2002;75:662-7.
41. Delion S, Chalon S, Herault J, Guilloteau D, Besnard JC, Durand G. Chronic dietary alpha-linolenic acid deficiency alters dopaminergic and serotoninergic neurotransmission in rats. J Nutr. 1994;124:2466-76.
42. Kodas E, Vancassel S, Lejeune B, Guilloteau D, Chalon S. Reversibility of n-3 fatty acid deficiency-induced changes in dopaminergic neurotransmission in rats: critical role of developmental stage. J Lipid Res. 2002;43:1209-19.
43. Ellis KA, Nathan PJ. The pharmacology of human working memory. Int J Neuropsychopharmacol. 2001;4:299-313.
44. Meneses A. Physiological, pathophysiological and therapeutic roles of 5-HT systems in learning and memory. Rev Neurosci. 1998;9:275-89.
45. Youdim MBH. Brain iron deficiency and excess. Cognitive impairment and neurodegeneration with involvement of striatum and hippocampus. Neurotox Res. 2008;14:45-56.
46. Kodas E, Galineau L, Bodard S, Vancassel S, Guilloteau D, Besnard JC, Chalon S. Serotoninergic neurotransmission is affected by n-3 polyunsaturated fatty acids in the rat. J Neurochem. 2004;89:695-702.
47. Innis SM, de La Presa Owens S. Dietary fatty acid composition in pregnancy alters neurite membrane fatty acids and dopamine in newborn rat brain. J Nutr. 2001;131:118-22.
48. McNamara RK, Able J, Liu Y, Jandacek R, Rider T, Tso P, Lipton JW. Omega-3 fatty acid deficiency during perinatal development increases serotonin turnover in the prefrontal cortex and decreases midbrain tryptophan hydroxylase-2 expression in adult female rats: dissociation from estrogenic effects. J Psychiatr Res. 2009;43:656-63.
49. Delion S, Chalon S, Guilloteau D, Besnard JC, Durand G. a-Linolenic acid dietary deficiency alters age-related changes of dopaminergic and serotoninergic neurotransmission in the rat frontal cortex. J Neurochem. 1996 Apr;66:1582-91.
50. Qu Y, Chang L, Klaff J, Balbo A, Rapoport SI. Imaging Brain Phospholipase A2 Activation in Awake Rats in Response to the 5-HT2A/2C Agonist ([+/-])2,5-Dimethoxy-4-Iodophenyl-2-Aminopropane (DOI). Neuropsychopharmacology. 2003;28:244-52.
51. Rao JS, Rapoport SI. Mood-stabilizers target the brain arachidonic acid cascade. Curr Mol Pharmacol. 2009 Jun;2:207-14.
52. Otero GA, Pliego-Rivero FB, Porcayo-Mercado R, Mendieta-Alcantara G. Working memory impairment and recovery in iron deficient children. Clin Neurophysiol. 2008;119:1739-46.
53. Chung WL, Chen JJ, Su HM. 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. 2008;138:1165-71.
54. McNamara RK, Able J, Jandacek R, Rider T, Tso P. Gender differences in rat erythrocyte and brain docosahexaenoic acid composition: role of ovarian hormones and dietary omega-3 fatty acid composition. Psychoneuroendocrinology. 2009;34:532-9.