Maternal arachidonic acid supplementation improves neurodevelopment in young adult offspring from rat dams with and without diabetes

Prostaglandins Leukotrienes and Essential Fatty Acids

Volumn 84, Issue 1-2, 2011, Pages 63-70

  Zhao, Jinping ^a   Del Bigio, Marc R ^b   Weiler, Hope A ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Infants of diabetic mothers; Long term neurodevelopment; Maternal arachidonic acid supplementation; Rat

Indexed keywords

ARACHIDONIC ACID; DOCOSAHEXAENOIC ACID; INSULIN GLARGINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BRAIN DEVELOPMENT; CONTROLLED STUDY; DIABETES MELLITUS; DIET SUPPLEMENTATION; EXPLORATORY BEHAVIOR; FEMALE; FOOD COMPOSITION; GLYCEMIC CONTROL; GROOMING; HYPERGLYCEMIA; LATENT PERIOD; LEARNING; LOCOMOTION; MALE; MATERNAL NUTRITION; MAZE TEST; NONHUMAN; PRIORITY JOURNAL; PROGENY; PSYCHOMOTOR ACTIVITY; RAT; ROTAROD TEST; STREPTOZOCIN DIABETES; TASK PERFORMANCE;

ANIMALS; ARACHIDONIC ACID; BRAIN; DIABETES MELLITUS, EXPERIMENTAL; DIET; EXPLORATORY BEHAVIOR; FEMALE; MALE; MATERNAL-FETAL EXCHANGE; MAZE LEARNING; PREGNANCY; PREGNANCY IN DIABETICS; PRENATAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PSYCHOMOTOR PERFORMANCE; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 78650975096     PISSN: 09523278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plefa.2010.08.009     Document Type: Article

References (55)

1. Siddappa A.M., Georgieff M.K., Wewerka S., Worwa C., Nelson C.A., Deregnier R.A. Iron deficiency alters auditory recognition memory in newborn infants of diabetic mothers. Pediatr. Res. 2004, 55:1034-1041.
2. DeBoer T., Wewerka S., Bauer P.J., Georgieff M.K., Nelson C.A. Explicit memory performance in infants of diabetic mothers at 1 year of age. Dev. Med. Child Neurol. 2005, 47:525-531.
3. Rizzo T., Metzger B.E., Burns W.J., Burns K. Correlations between antepartum maternal metabolism and child intelligence. N. Engl. J. Med. 1991, 325:911-916.
4. Ornoy A. Growth and neurodevelopmental outcome of children born to mothers with pregestational and gestational diabetes. Pediatr. Endocrinol. Rev. 2005, 3:104-113.
5. Nelson C.A., Wewerka S., Thomas K.M., Tribby-Walbridge S., deRegnier R., Georgieff M. Neurocognitive sequelae of infants of diabetic mothers. Behav. Neurosci. 2000, 114:950-956.
6. Lauritzen L., Hansen H.S., Jorgensen M.H., Michaelsen K.F. The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina. Prog. Lipid Res. 2001, 40:1-94.
7. Ghebremeskel K., Thomas B., Lowy C., Min Y., Crawford M.A. Type 1 diabetes compromises plasma arachidonic and docosahexaenoic acids in newborn babies. Lipids 2004, 39:335-342.
8. Min Y., Lowy C., Ghebremeskel K., Thomas B., Offley-Shore B., Crawford M. Unfavorable effect of type 1 and type 2 diabetes on maternal and fetal essential fatty acid status: a potential marker of fetal insulin resistance. Am. J. Clin. Nutr. 2005, 82:1162-1168.
9. Wijendran V., Bendel R.B., Couch S.C., Philipson E.H., Cheruku S., Lammi-Keefe C.J. Fetal erythrocyte phospholipid polyunsaturated fatty acids are altered in pregnancy complicated with gestational diabetes mellitus. Lipids 2000, 35:927-931.
10. Dijck-Brouwer D.A., Hadders-Algra M., Bouwstra H., Decsi T., Boehm G., Martini I.A., Boersma E.R., Muskiet F.A. Lower fetal status of docosahexaenoic acid, arachidonic acid and essential fatty acids is associated with less favorable neonatal neurological condition. Prostaglandins Leukot. Essent. Fatty Acids 2005, 72:21-28.
11. Holman R.T., Johnson S.B., Gerrard J.M., Mauer S.M., Kupcho-Sandberg S., Brown D.M. Arachidonic acid deficiency in streptozotocin-induced diabetes. Proc. Natl. Acad. Sci. USA 1983, 80:2375-2379.
12. Hu Q., Ishii E., Nakagawa Y. Differential changes in relative levels of arachidonic acid in major phospholipids from rat tissues during the progression of diabetes. J. Biochem. 1994, 115:405-408.
13. Hadders-Algra M. Prenatal long-chain polyunsaturated fatty acid status: the importance of a balanced intake of docosahexaenoic acid and arachidonic acid. J. Perinat. Med. 2008, 36:101-109.
14. Uchida K., Kumihashi K., Kurosawa S., Kobayashi T., Itoi K., Machida T. Stimulatory effects of prostaglandin E2 on neurogenesis in the dentate gyrus of the adult rat. Zoolog. Sci. 2002, 19:1211-1216.
15. Maekawa M., Takashima N., Matsumata M., Ikegami S., Kontani M., Hara Y., Kawashima H., Owada Y., Kiso Y., Yoshikawa T., Inokuchi K., Osumi N. Arachidonic acid drives postnatal neurogenesis and elicits a beneficial effect on prepulse inhibition, a biological trait of psychiatric illnesses. PLoS One 2009, 4:) e5085.
16. Kinney B.A., Rabe M.B., Jensen R.A., Steger R.W. Maternal hyperglycemia leads to gender-dependent deficits in learning and memory in offspring. Exp. Biol. Med. (Maywood) 2003, 228:152-159.
17. Zhao J., Del Bigio M.R., Weiler H.A. Maternal arachidonic acid supplementation improves neurodevelopment of offspring from healthy and diabetic rats. Prostaglandins Leukot. Essent. Fatty Acids 2009, 81:349-356.
18. Enslen M., Milon H., Malnoe A. Effect of low intake of n-3 fatty acids during development on brain phospholipid fatty acid composition and exploratory behavior in rats. Lipids 1991, 26:203-208.
19. Muskiet F.A., van Goor S.A., Kuipers R.S., Velzing-Aarts F.V., Smit E.N., Bouwstra H., Dijck-Brouwer D.A., Boersma E.R., Hadders-Algra M. Long-chain polyunsaturated fatty acids in maternal and infant nutrition. Prostaglandins Leukot. Essent. Fatty Acids 2006, 75:135-144.
20. Riggins T., Miller N.C., Bauer P.J., Georgieff M.K., Nelson C.A. Consequences of low neonatal iron status due to maternal diabetes mellitus on explicit memory performance in childhood. Dev. Neuropsychol. 2009, 34:762-779.
21. Reeves P.G. Components of the AIN-93 diets as improvements in the AIN-76A diet. J. Nutr. 1997, 127:838S-841S.
22. Altman J., Sudarshan K. Postnatal development of locomotion in the laboratory rat. Anim. Behav. 1975, 23:896-920.
23. Mills D.E., Ward R.P., Young C. Effects of prenatal and early postnatal fatty acid supplementation on behavior. Nutr. Res. 1988, 8:273-286.
24. Pierce R.C., Kalivas P.W. Locomotor behavior. Curr. Protoc. Neurosci. 2007, (Chapter 8) Unit 8 1.
25. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
26. Del Bigio M.R., Wang X., Wilson M.J. Sodium channel-blocking agents are not of benefit to rats with kaolin-induced hydrocephalus. Neurosurgery 2002, 51:460-466. discussion 466-467.
27. Folch J., Lees M., Stanley G.H. Sloane A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957, 226:497-509.
28. Zhao J., Weiler H.A. Long-term effects of gestational diabetes on offspring health are more pronounced in skeletal growth than body composition and glucose tolerance. Br. J. Nutr. 2010, 1-9.
29. Heyser C.J., Spear N.E., Spear L.P. Effects of prenatal exposure to cocaine on Morris water maze performance in adult rats. Behav. Neurosci. 1995, 109:734-743.
30. de Haan M., Mishkin M., Baldeweg T., Vargha-Khadem F. Human memory development and its dysfunction after early hippocampal injury. Trends Neurosci. 2006, 29:374-381.
31. Georgieff M.K. The role of iron in neurodevelopment: fetal iron deficiency and the developing hippocampus. Biochem. Soc. Trans. 2008, 36:1267-1271.
32. Levant B., Radel J.D., Carlson S.E. Decreased brain docosahexaenoic acid during development alters dopamine-related behaviors in adult rats that are differentially affected by dietary remediation. Behav. Brain Res. 2004, 152:49-57.
33. 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.
34. Johansson B., Meyerson B., Eriksson U.J. Behavioral effects of an intrauterine or neonatal diabetic environment in the rat. Biol. Neonate 1991, 59:226-235.
35. McGahon B., Clements M.P., Lynch M.A. The ability of aged rats to sustain long-term potentiation is restored when the age-related decrease in membrane arachidonic acid concentration is reversed. Neuroscience 1997, 81:9-16.
36. Kotani S., Nakazawa H., Tokimasa T., Akimoto K., Kawashima H., Toyoda-Ono Y., Kiso Y., Okaichi H., Sakakibara M. Synaptic plasticity preserved with arachidonic acid diet in aged rats. Neurosci. Res. 2003, 46:453-461.
37. Wainwright P.E., Xing H.C., Mutsaers L., McCutcheon D., Kyle D. Arachidonic acid offsets the effects on mouse brain and behavior of a diet with a low (n-6):(n-3) ratio and very high levels of docosahexaenoic acid. J. Nutr. 1997, 127:184-193.
38. Brenner R.R. Hormonal modulation of delta6 and delta5 desaturases: case of diabetes. Prostaglandins Leukot. Essent. Fatty Acids 2003, 68:151-162.
39. Faas F.H., Carter W.J. Altered microsomal phospholipid composition in the streptozotocin diabetic rat. Lipids 1983, 18:339-342.
40. Ramsammy L.S., Haynes B., Josepovitz C., Kaloyanides G.J. Mechanism of decreased arachidonic acid in the renal cortex of rats with diabetes mellitus. Lipids 1993, 28:433-439.
41. Percy P., Percy A., Vilbergsson G., Mansson J.E. Polyunsaturated fatty acid accretion in first- and second-trimester human fetal brain: lack of correlation with levels in paired placental samples. Biochem. Mol. Med. 1996, 59:38-43.
42. Clandinin M.T., Chappell J.E., Leong S., Heim T., Swyer P.R., Chance G.W. Intrauterine fatty acid accretion rates in human brain: implications for fatty acid requirements. Early Hum. Dev. 1980, 4:121-129.
43. Dobbing J., Sands J. Quantitative growth and development of human brain. Arch. Dis. Child 1973, 48:757-767.
44. Hadders-Algra M., Bouwstra H., van Goor S.A., Dijck-Brouwer D.A., Muskiet F.A. Prenatal and early postnatal fatty acid status and neurodevelopmental outcome. J. Perinat. Med. 2007, 35(Suppl. 1):S28-34.
45. Lefkowith J.B., Flippo V., Sprecher H., Needleman P. Paradoxical conservation of cardiac and renal arachidonate content in essential fatty acid deficiency. J. Biol. Chem. 1985, 260:15736-15744.
46. 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.
47. Groen S.E., de Blecourt A.C., Postema K., Hadders-Algra M. General movements in early infancy predict neuromotor development at 9 to 12 years of age. Dev. Med. Child Neurol. 2005, 47:731-738.
48. Bouwstra H., Dijck-Brouwer D.J., Decsi T., Boehm G., Boersma E.R., Muskiet F.A., Hadders-Algra M. Relationship between umbilical cord essential fatty acid content and the quality of general movements of healthy term infants at 3 months. Pediatr. Res. 2006, 59:717-722.
49. van Goor S.A., Schaafsma A., Erwich J.J., Dijck-Brouwer D.A., Muskiet F.A. Mildly abnormal general movement quality in infants is associated with higher Mead acid and lower arachidonic acid and shows a U-shaped relation with the DHA/AA ratio. Prostaglandins Leukot. Essent. Fatty Acids 2010, 82:15-20.
50. van Goor S.A., Dijck-Brouwer D.A., Doornbos B., Erwich J.J., Schaafsma A., Muskiet F.A., Hadders-Algra M. Supplementation of DHA but not DHA with arachidonic acid during pregnancy and lactation influences general movement quality in 12-week-old term infants. Br. J. Nutr. 2010, 103:235-242.
51. Svennerholm L., Bostrom K., Fredman P., Mansson J.E., Rosengren B., Rynmark B.M. Human brain gangliosides: developmental changes from early fetal stage to advanced age. Biochim. Biophys. Acta 1989, 1005:109-117.
52. Clandinin M.T., Chappell J.E., Leong S., Heim T., Swyer P.R., Chance G.W. Extrauterine fatty acid accretion in infant brain: implications for fatty acid requirements. Early Hum. Dev. 1980, 4:131-138.
53. Godfrey K.M., Barker D.J. Fetal nutrition and adult disease. Am. J. Clin. Nutr. 2000, 71:1344S-1352S.
54. Jonasson Z. Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data. Neurosci. Biobehav. Rev. 2005, 28:811-825.
55. Fedorova I., Hussein N., Baumann M.H., Di Martino C., Salem N. An n-3 fatty acid deficiency impairs rat spatial learning in the Barnes maze. Behav. Neurosci. 2009, 123:196-205.