Prenatal choline supplementation mitigates the adverse effects of prenatal alcohol exposure on development in rats

Neurotoxicology and Teratology

Volumn 31, Issue 5, 2009, Pages 303-311

  Thomas, Jennifer D ^a   Abou, Elizabeth J ^a   Dominguez, Hector D ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

Ethanol; Fetal alcohol spectrum disorders; Fetal alcohol syndrome; Physical development; Reflex development; Treatment

Indexed keywords

ALCOHOL; CHOLINE;

ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN DISEASE; BRAIN WEIGHT; CONTROLLED STUDY; DIET SUPPLEMENTATION; DISEASE SEVERITY; FEMALE; FETOTOXICITY; FETUS; GESTATION PERIOD; HINDLIMB; INCISOR; LOW BIRTH WEIGHT; MALE; MATERNAL BEHAVIOR; MENTAL DEVELOPMENT; MOTOR COORDINATION; NONHUMAN; PHYSICAL DEVELOPMENT; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT; TOOTH DEVELOPMENT;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BODY WEIGHT; BRAIN; CHOLINE; DIETARY SUPPLEMENTS; ETHANOL; FEMALE; FETAL ALCOHOL SYNDROME; MALE; MATERNAL-FETAL EXCHANGE; MOTOR SKILLS; PREGNANCY; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; REFLEX;

ANIMALIA; RATTUS;

EID: 69549121616     PISSN: 08920362     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ntt.2009.07.002     Document Type: Article

References (99)

1. Albright C.D., Tsai A.Y., Mar M.H., and Zeisel S.H. Choline availability modulates the expression of TGFbeta1 and cytoskeletal proteins in the hippocampus of developing rat brain. Neurochem. Res. 23 (1998) 751-758
2. Albright C.D., Friedrich C.B., Brown E.C., Mar M.H., and Zeisel S.H. Maternal dietary choline availability alters mitosis, apoptosis and the localization of TOAD-64 protein in the developing fetal rat septum. Brain Res. Dev. Brain Res. 115 (1999) 123-129
3. Albright C.D., Tsai A.Y., Friedrich C.B., Mar M.H., and Zeisel S.H. Choline availability alters embryonic development of the hippocampus and septum in the rat. Brain Res. Dev. Brain Res. 113 (1999) 13-20
4. Albright C.D., Mar M.H., Craciunescu C.N., Song J., and Zeisel S.H. Maternal dietary choline availability alters the balance of netrin-1 and DCC neuronal migration proteins in fetal mouse brain hippocampus. Brain Res. Dev. Brain Res. 159 (2005) 149-154
5. Albuquerque E.X., Alkondon M., Pereira E.F., Castro N.G., Schrattenholz A., Barbosa C.T., Bonfante-Cabarcas R., Aracava Y., Eisenberg H.M., and Maelicke A. Properties of neuronal nicotinic acetylcholine receptors: pharmacological characterization and modulation of synaptic function. J. Pharmacol. Exp. Ther. 280 (1997) 1117-1136
6. Alkondon M., Pereira E.F., Cortes W.S., Maelicke A., and Albuquerque E.X. Choline is a selective agonist of alpha7 nicotinic acetylcholine receptors in the rat brain neurons. Eur. J. NeuroSci. 9 (1997) 2734-2742
7. Berman R.F., and Hannigan J.H. Effects of prenatal alcohol exposure on the hippocampus: spatial behavior, electrophysiology, and neuroanatomy. Hippocampus 10 (2000) 94-110
8. Bonthius D.J., Karacay B., Dai D., and Pantazis N.J. FGF-2, NGF and IGF-1, but not BDNF, utilize a nitric oxide pathway to signal neurotrophic and neuroprotective effects against alcohol toxicity in cerebellar granule cell cultures. Brain Res. Dev. Brain Res. 140 (2003) 15-28
9. Chen S.Y., Dehart D.B., and Sulik K.K. Protection from ethanol-induced limb malformations by the superoxide dismutase/catalase mimetic, EUK-134. Faseb J. 18 (2004) 1234-1236
10. Chen S.Y., Charness M.E., Wilkemeyer M.F., and Sulik K.K. Peptide-mediated protection from ethanol-induced neural tube defects. Dev. Neurosci. 27 (2005) 13-19
11. Cheng R.K., Meck W.H., and Williams C.L. alpha7 Nicotinic acetylcholine receptors and temporal memory: synergistic effects of combining prenatal choline and nicotine on reinforcement-induced resetting of an interval clock. Learn Mem. 13 (2006) 127-134
12. Clarren S.K., Randels S.P., Sanderson M., and Fineman R.M. Screening for fetal alcohol syndrome in primary schools: a feasibility study. Teratology 63 (2001) 3-10
13. Cohen-Kerem R., and Koren G. Antioxidants and fetal protection against ethanol teratogenicity. I. Review of the experimental data and implications to humans. Neurotoxicol. Teratol. 25 (2003) 1-9
14. Costa L.G., and Guizzetti M. Muscarinic cholinergic receptor signal transduction as a potential target for the developmental neurotoxicity of ethanol. Biochem. Pharmacol. 57 (1999) 721-726
15. Craciunescu C.N., Albright C.D., Mar M.H., Song J., and Zeisel S.H. Choline availability during embryonic development alters progenitor cell mitosis in developing mouse hippocampus. J. Nutr. 133 (2003) 3614-3618
16. Dobbing J., and Sands J. Comparative aspects of the brain growth spurt. Early Hum. Dev. 3 (1979) 79-83
17. Endres M., Toso L., Roberson R., Park J., Abebe D., Poggi S., and Spong C.Y. Prevention of alcohol-induced developmental delays and learning abnormalities in a model of fetal alcohol syndrome. Am. J. Obstet. Gynecol. 193 (2005) 1028-1034
18. Fisher M.C., Zeisel S.H., Mar M.H., and Sadler T.W. Inhibitors of choline uptake and metabolism cause developmental abnormalities in neurulating mouse embryos. Teratology 64 (2001) 114-122
19. Fisher M.C., Zeisel S.H., Mar M.H., and Sadler T.W. Perturbations in choline metabolism cause neural tube defects in mouse embryos in vitro. Faseb J. 16 (2002) 619-621
20. Food and Nutrition Board, Institute of Medicine. Dietary reference intakes for thiamin, riboflavin, niacin, vitamin B6, folate, vitamin B12, pantothenic acid, Biotin, and choline (1998), National Academy Press, Washington, D.C.
21. Gabriel K.I., Johnston S., and Weinberg J. Prenatal ethanol exposure and spatial navigation: effects of postnatal handling and aging. Dev. Psychobiol. 40 (2002) 345-357
22. Gallo P.V., and Weinberg J. Neuromotor development and response inhibition following prenatal ethanol exposure. Neurobehav. Toxicol. Teratol. 4 (1982) 505-513
23. Garro A.J., McBeth D.L., Lima V., and Lieber C.S. Ethanol consumption inhibits fetal DNA methylation in mice: implications for the fetal alcohol syndrome. Alcohol. Clin. Exp. Res. 15 (1991) 395-398
24. Gottesfeld Z., and Silverman P.B. Developmental delays associated with prenatal alcohol exposure are reversed by thyroid hormone treatment. Neurosci. Lett. 109 (1990) 42-47
25. Guo-Ross S.X., Clark S., Montoya D.A., Jones K.H., Obernier J., Shetty A.K., White A.M., Blusztajn J.K., Wilson W.A., and Swartzwelder H.S. Prenatal choline supplementation protects against postnatal neurotoxicity. J. Neurosci. 22 (2002) RC195
26. Guo-Ross S.X., Jones K.H., Shetty A.K., Wilson W.A., and Swartzwelder H.S. Prenatal dietary choline availability alters postnatal neurotoxic vulnerability in the adult rat. Neurosci. Lett. 341 (2003) 161-163
27. Hannigan J.H. Effects of prenatal exposure to alcohol plus caffeine in rats: pregnancy outcome and early offspring development. Alcohol. Clin. Exp. Res. 19 (1995) 238-246
28. Hannigan J.H., O'Leary-Moore S.K., and Berman R.F. Postnatal environmental or experiential amelioration of neurobehavioral effects of perinatal alcohol exposure in rats. Neurosci. Biobehav. Rev. 31 (2007) 202-211
29. Heaton M.B., Paiva M., Swanson D.J., and Walker D.W. Modulation of ethanol neurotoxicity by nerve growth factor. Brain Res. 620 (1993) 78-85
30. Heaton M.B., Mitchell J.J., and Paiva M. Amelioration of ethanol-induced neurotoxicity in the neonatal rat central nervous system by antioxidant therapy. Alcohol. Clin. Exp. Res. 24 (2000) 512-518
31. Heaton M.B., Mitchell J.J., and Paiva M. Overexpression of NGF ameliorates ethanol neurotoxicity in the developing cerebellum. J. Neurobiol. 45 (2000) 95-104
32. Hobbs C.A., Cleves M.A., Melnyk S., Zhao W., and James S.J. Congenital heart defects and abnormal maternal biomarkers of methionine and homocysteine metabolism. Am. J. Clin. Nutr. 81 (2005) 147-153
33. Holmes G.L., Yang Y., Liu Z., Cermak J.M., Sarkisian M.R., Stafstrom C.E., Neill J.C., and Blusztajn J.K. Seizure-induced memory impairment is reduced by choline supplementation before or after status epilepticus. Epilepsy Res. 48 (2002) 3-13
34. Holson R.R., and Pearce B. Principles and pitfalls in the analysis of prenatal treatment effects in multiparous species. Neurotoxicol. Teratol. 14 (1992) 221-228
35. Hoyme H.E., May P.A., Kalberg W.O., Kodituwakku P., Gossage J.P., Trujillo P.M., Buckley D.G., Miller J.H., Aragon A.S., Khaole N., et al. A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 Institute of Medicine Criteria. Pediatrics 115 2005 (1996) 39-47
36. Janicke B., and Coper H. The effects of prenatal alcohol exposure on the behavior of rats during their life span. J. Gerontol. 48 (1993) 156-167
37. Jones J.P., Meck W.H., Williams C.L., Wilson W.A., and Swartzwelder H.S. Choline availability to the developing rat fetus alters adult hippocampal long-term potentiation. Brain Res. Dev. Brain Res. 118 (1999) 159-167
38. Kable J.A., Coles C.D., and Taddeo E. Socio-cognitive habilitation using the math interactive learning experience program for alcohol-affected children. Alcohol. Clin. Exp. Res. 31 (2007) 1425-2434
39. Kelly S.J., Hulsether S.A., and West J.R. Alterations in sensorimotor development: relationship to postnatal alcohol exposure. Neurotoxicol. Teratol. 9 (1987) 243-251
40. Klintsova A.Y., Scamra C., Hoffman M., Napper R.M., Goodlett C.R., and Greenough W.T. Therapeutic effects of complex motor training on motor performance deficits induced by neonatal binge-like alcohol exposure in rats: II. A quantitative stereological study of synaptic plasticity in female rat cerebellum. Brain Res. 937 (2002) 83-93
41. Kovacheva V.P., Mellott T.J., Davison J.M., Wagner N., Lopez-Coviella I., Schnitzler A.C., and Blusztajn J.K. Gestational choline deficiency causes global and Igf2 gene DNA hypermethylation by up-regulation of Dnmt1 expression. J. Biol. Chem. 282 (2007) 31777-31788
42. Li Q., Guo-Ross S., Lewis D.V., Turner D., White A.M., Wilson W.A., and Swartzwelder H.S. Dietary prenatal choline supplementation alters postnatal hippocampal structure and function. J. Neurophysiol. 91 (2004) 1545-1555
43. Lopez-Tejero D., Ferrer I., L.L. M, and Herrera E. Effects of prenatal ethanol exposure on physical growth, sensory reflex maturation and brain development in the rat. Neuropathol. Appl. Neurobiol. 12 (1986) 251-260
44. Marino M.D., Aksenov M.Y., and Kelly S.J. Vitamin E protects against alcohol-induced cell loss and oxidative stress in the neonatal rat hippocampus. Int. J. Dev. Neurosci. 22 (2004) 363-377
45. May P.A., and Gossage J.P. Estimating the prevalence of fetal alcohol syndrome. A summary. Alcohol Res. Health 25 (2001) 159-167
46. McAlhany Jr. R.E., West J.R., and Miranda R.C. Glial-derived neurotrophic factor (GDNF) prevents ethanol-induced apoptosis and JUN kinase phosphorylation. Brain Res. Dev. Brain Res. 119 (2000) 209-216
47. McCann J.C., Hudes M., and Ames B.N. An overview of evidence for a causal relationship between dietary availability of choline during development and cognitive function in offspring. Neurosci. Biobehav. Rev. 30 (2006) 696-712
48. McKeon-O'Malley C., Siwek D., Lamoureux J.A., Williams C.L., and Kowall N.W. Prenatal choline deficiency decreases the cross-sectional area of cholinergic neurons in the medial septal nucleus. Brain Res. 977 (2003) 278-283
49. Meck W.H., and Williams C.L. Simultaneous temporal processing is sensitive to prenatal choline availability in mature and aged rats. NeuroReport 8 (1997) 3045-3051
50. Meck W.H., and Williams C.L. Metabolic imprinting of choline by its availability during gestation: implications for memory and attentional processing across the lifespan. Neurosci. Biobehav. Rev. 27 (2003) 385-399
51. Meck W.H., Smith R.A., and Williams C.L. Pre- and postnatal choline supplementation produces long-term facilitation of spatial memory. Dev. Psychobiol. 21 (1988) 339-353
52. Mellott T.J., Follettie M.T., Diesl V., Hill A.A., Lopez-Coviella I., and Blusztajn J.K. Prenatal choline availability modulates hippocampal and cerebral cortical gene expression. Faseb J. 21 (2007) 1311-1323
53. Mike A., Castro N.G., and Albuquerque E.X. Choline and acetylcholine have similar kinetic properties of activation and desensitization on the alpha7 nicotinic receptors in rat hippocampal neurons. Brain Res. 882 (2000) 155-168
54. Miller M.W. Effects of prenatal exposure to ethanol on neocortical development: II. Cell proliferation in the ventricular and subventricular zones of the rat. J. Comp. Neurol. 287 (1989) 326-338
55. Mitchell J.J., Paiva M., and Heaton M.B. The antioxidants vitamin E and beta-carotene protect against ethanol-induced neurotoxicity in embryonic rat hippocampal cultures. Alcohol 17 (1999) 163-168
56. Molina J.C., Hoffman H., Spear L.P., and Spear N.E. Sensorimotor maturation and alcohol responsiveness in rats prenatally exposed to alcohol during gestational day 8. Neurotox. Teratol. 9 (1987) 121-128
57. Montoya D., and Swartzwelder H.S. Prenatal choline supplementation alters hippocampal N-methyl-d-aspartate receptor-mediated neurotransmission in adult rats. Neurosci. Lett. 296 (2000) 85-88
58. Mulholland P.J., Self R.L., Harris B.R., Littleton J.M., and Prendergast M.A. Choline exposure reduces potentiation of N-methyl-d-aspartate toxicity by corticosterone in the developing hippocampus. Brain Res. Dev. Brain Res. 153 (2004) 203-211
59. Nag N., and Berger-Sweeney J.E. Postnatal dietary choline supplementation alters behavior in a mouse model of Rett syndrome. Neurobiol. Dis. 26 (2007) 473-480
60. Nagahara A.H., and Handa R.J. Fetal alcohol-exposed rats exhibit differential response to cholinergic drugs on a delay-dependent memory task. Neurobiol. Learn. Mem. 72 (1999) 230-243
61. Ness J.W., and Franchina J.J. Effects of prenatal alcohol exposure on rat pups' ability to elicit retrieval behavior from dams. Dev. Psychobiol. 23 (1990) 85-99
62. NIAAA. 10th Special Report to US Congress on alcohol and health (2000), National Institute of Health, Washington, DC
63. Niculescu M.D., Craciunescu C.N., and Zeisel S.H. Dietary choline deficiency alters global and gene-specific DNA methylation in the developing hippocampus of mouse fetal brains. Faseb J. 20 (2006) 43-49
64. Polache A., Martin-Algarra R.V., and Guerri C. Effects of chronic alcohol consumption on enzyme activities and active methionine absorption in the small intestine of pregnant rats. Alcohol. Clin. Exp. Res. 20 (1996) 1237-1242
65. Potter B.M., and Berntson G.G. Prenatal alcohol exposure: effects on acoustic startle and prepulse inhibition. Neurotox. Teratol. 9 (1987) 17-21
66. Pyapali G.K., Turner D.A., Williams C.L., Meck W.H., and Swartzwelder H.S. Prenatal dietary choline supplementation decreases the threshold for induction of long-term potentiation in young adult rats. J. Neurophysiol. 79 (1998) 1790-1796
67. Riley E.P., and McGee C.L. Fetal alcohol spectrum disorders: an overview with emphasis on changes in brain and behavior. Exp. Biol. Med. (Maywood) 230 (2005) 357-365
68. Sampson P.D., Streissguth A.P., Bookstein F.L., Little R.E., Clarren S.K., Dehaene P., Hanson J.W., and Graham Jr. J.M. Incidence of fetal alcohol syndrome and prevalence of alcohol-related neurodevelopmental disorder. Teratology 56 (1997) 317-326
69. Sandstrom N.J., Loy R., and Williams C.L. Prenatal choline supplementation increases NGF levels in the hippocampus and frontal cortex of young and adult rats. Brain Res. 947 (2002) 9-16
70. Shankar K., Hidestrand M., Liu X., Xiao R., Skinner C.M., Simmen F.A., Badger T.M., and Ronis M.J. Physiologic and genomic analyses of nutrition-ethanol interactions during gestation: implications for fetal ethanol toxicity. Exp. Biol. Med. (Maywood) 231 (2006) 1379-1397
71. Shaw G.M., Carmichael S.L., Yang W., Selvin S., and Schaffer D.M. Periconceptional dietary intake of choline and betaine and neural tube defects in offspring. Am. J. Epidemiol. 160 (2004) 102-109
72. Streissguth A.P., Bookstein F.L., Barr H.M., Sampson P.D., O'Malley K., and Young J.K. Risk factors for adverse life outcomes in fetal alcohol syndrome and fetal alcohol effects. J. Dev. Behav. Pediatr. 25 (2004) 228-238
73. Swanson D.J., King M.A., Walker D.W., and Heaton M.B. Chronic prenatal ethanol exposure alters the normal ontogeny of choline acetyltransferase activity in the rat septohippocampal system. Alcohol. Clin. Exp. Res. 19 (1995) 1252-1260
74. Thomas J.D., Fleming S.L., and Riley E.P. MK-801 can exacerbate or attenuate behavioral alterations associated with neonatal alcohol exposure in the rat, depending on the timing of administration. Alcohol Clin Exp Res 25 (2001) 764-773
75. Thomas J.D., La Fiette M.H., Quinn V.R., and Riley E.P. Neonatal choline supplementation ameliorates the effects of prenatal alcohol exposure on a discrimination learning task in rats. Neurotoxicol. Teratol. 22 (2000) 703-711
76. Thomas J.D., Garcia G.G., Dominguez H.D., and Riley E.P. Administration of eliprodil during ethanol withdrawal in the neonatal rat attenuates ethanol-induced learning deficits. Psychopharmacology 175 (2004) 189-195
77. Thomas J.D., Garrison M., and O'Neill T.M. Perinatal choline supplementation attenuates behavioral alterations associated with neonatal alcohol exposure in rats. Neurotoxicol. Teratol. 26 (2004) 35-45
78. Thomas J.D., O'Neill T.M., and Dominguez H.D. Perinatal choline supplementation does not mitigate motor coordination deficits associated with neonatal alcohol exposure in rats. Neurotoxicol. Teratol. 26 (2004) 223-229
79. Thomas J.D., Biane J.S., O'Bryan K.A., O'Neill T.M., and Dominguez H.D. Choline supplementation following third-trimester-equivalent alcohol exposure attenuates behavioral alterations in rats. Behav. Neurosci. 121 (2007) 120-130
80. Tonjes R., Hecht K., Brautzsch M., Lucius R., and Dorner G. Behavioural changes in adult rats produced by early postnatal maternal deprivation and treatment with choline chloride. Exp. Clin. Endocrinol. 88 (1986) 151-157
81. Tran T., and Thomas J.D. Perinatal choline supplementation mitigates trace eyeblink conditioning deficits associated with 3rd trimester alcohol exposure in rats (2007), Society for Neuroscience, San Diego, CA
82. Vink J., Auth J., Abebe D.T., Brenneman D.E., and Spong C.Y. Novel peptides prevent alcohol-induced spatial learning deficits and proinflammatory cytokine release in a mouse model of fetal alcohol syndrome. Am. J. Obstet. Gynecol. 193 (2005) 825-829
83. Vorhees C.V., and Fernandez K. Effects of short-term prenatal alcohol exposure on maze, activity, and olfactory orientation performance in rats. Neurobehav. Toxicol. Teratol. 8 (1986) 23-28
84. Wagner A.F., and Hunt P.S. Impaired trace fear conditioning following neonatal ethanol: reversal by choline. Behav. Neurosci. 120 (2006) 482-487
85. Wainwright P., and Fritz G. Effect of moderate prenatal ethanol exposure on postnatal brain and behavioral development in BALB/c mice. Exp. Neurol. 89 (1985) 237-249
86. Warren K.R., Calhoun F.J., May P.A., Viljoen D.L., Li T.K., Tanaka H., Marinicheva G.S., Robinson L.K., and Mundle G. Fetal alcohol syndrome: an international perspective. Alcohol. Clin. Exp. Res. 25 (2001) 202S-206S
87. Weinberg J. Effects of ethanol and maternal nutritional status on fetal development. Alcohol. Clin. Exp. Res. 9 (1985) 49-55
88. Weinberg J., D'Alquen G., and Bezio S. Interactive effects of ethanol intake and maternal nutritional status on skeletal development of fetal rats. Alcohol 7 (1990) 383-388
89. Wen Z., and Kim H.Y. Alterations in hippocampal phospholipid profile by prenatal exposure to ethanol. J. Neurochem. 89 (2004) 1368-1377
90. Wiener S.G., Shoemaker W.J., Koda L.Y., and Bloom F.E. Interaction of ethanol and nutrition during gestation: influence on maternal and offspring development in the rat. J. Pharmacol. Exp. Ther. 216 (1981) 572-579
91. Wilkemeyer M.F., Menkari C.E., Spong C.Y., and Charness M.E. Peptide antagonists of ethanol inhibition of l1-mediated cell-cell adhesion. J. Pharm. Exp. Ther. 303 (2002) 110-116
92. Wilkemeyer M.F., Chen S.Y., Menkari C.E., Brenneman D.E., Sulik K.K., and Charness M.E. Differential effects of ethanol antagonism and neuroprotection in peptide fragment NAPVSIPQ prevention of ethanol-induced developmental toxicity. Proc. Natl. Acad. Sci. U S A 100 (2003) 8543-8548
93. Williams C.L., Meck W.H., Heyer D.D., and Loy R. Hypertrophy of basal forebrain neurons and enhanced visuospatial memory in perinatally choline-supplemented rats. Brain Res. 794 (1998) 225-238
94. Yang Y., Liu Z., Cermak J.M., Tandon P., Sarkisian M.R., Stafstrom C.E., Neill J.C., Blusztajn J.K., and Holmes G.L. Protective effects of prenatal choline supplementation on seizure-induced memory impairment. J. Neurosci. 20 (2000) RC109
95. Zeisel S.H. Choline: critical role during fetal development and dietary requirements in adults. Annu. Rev. Nutr. 26 (2006) 229-250
96. Zeisel S.H. The fetal origins of memory: the role of dietary choline in optimal brain development. J. Pediatr. 149 (2006) S131-S136
97. Zeisel S.H., and Blusztajn J.K. Choline and human nutrition. Annu. Rev. Nutr. 14 (1994) 269-296
98. Zeisel S.H., and Niculescu M.D. Perinatal choline influences brain structure and function. Nutr. Rev. 64 (2006) 197-203
99. Zhou F.C., Sari Y., Powrozek T.A., and Spong C.Y. A neuroprotective peptide antagonizes fetal alcohol exposure-compromised brain growth. J. Mol. Neurosci. 24 (2004) 189-199