Increasing maternal or post-weaning folic acid alters gene expression and moderately changes behavior in the offspring

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Barua, Subit ^a   Chadman, Kathryn K ^a   Kuizon, Salomon ^a   Buenaventura, Diego ^a   Stapley, Nathan W ^a   Ruocco, Felicia ^a   Begum, Umme ^a   Guariglia, Sara R ^b   Brown, W Ted ^a   Junaid, Mohammed A ^a,c  

^a NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOLIC ACID; PROTEIN VGLL2P; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1; TRANSCRIPTOME;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR; CPN2 GENE; DOWN REGULATION; FEMALE; GENE; GENE EXPRESSION; HEMISPHERE; HTR4 GENE; HYPERACTIVITY; LEPREL1 GENE; MALE; MATERNAL NUTRITION; MICROARRAY ANALYSIS; MOUSE; NEWBORN; NFIX GENE; NKX6-3 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREGNANCY; PROGENY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SLC17A7 GENE; UPREGULATION; VGLL2 GENE; VITAMIN SUPPLEMENTATION; VOCALIZATION; WEANING; XIST GENE; ZFP353 GENE; ANIMAL; ANIMAL BEHAVIOR; BRAIN CORTEX; C57BL MOUSE; DIET SUPPLEMENTATION; DNA MICROARRAY; DRUG EFFECTS; FEEDING BEHAVIOR; FETOMATERNAL TRANSFUSION; GROOMING; MAZE TEST; METABOLISM; ORAL DRUG ADMINISTRATION; SOCIAL BEHAVIOR;

ADMINISTRATION, ORAL; ANIMALS; BEHAVIOR, ANIMAL; CEREBRAL CORTEX; DIETARY SUPPLEMENTS; FEEDING BEHAVIOR; FEMALE; FOLIC ACID; GROOMING; MALE; MATERNAL-FETAL EXCHANGE; MAZE LEARNING; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREGNANCY; SOCIAL BEHAVIOR; TRANSCRIPTOME;

EID: 84903976099     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101674     Document Type: Article

References (57)

1. Roy S, Kale A, Dangat K, Sable P, Kulkarni A, et al. (2012) Maternal micronutrients (folic acid and vitamin B 12) and omega 3 fatty acids: implications for neurodevelopmental risk in the rat offspring. Brain Dev 34: 64271.
2. Wu G, Bazer FW, Cudd TA, Meininger CJ, Spencer TE (2004) Maternal nutrition and fetal development. J Nutr 134: 216922172.
3. Stanger O (2002) Physiology of folic acid in health and disease. Curr Drug Metab 3: 2112223.
4. Sweeney MR, McPartlin J, Scott J (2007) Folic acid fortification and public health: report on threshold doses above which unmetabolised folic acid appear in serum. BMC Public Health 7: 41.
5. U.S. Preventive Services Task Force (2009) Folic acid for the prevention of neural tube defects: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med 150: 6262631.
6. Ly A, Lee H, Chen J, Sie KK, Renlund R, et al. (2011) Effect of maternal and postweaning folic acid supplementation on mammary tumor risk in the offspring. Cancer Res 71: 9882997.
7. Dietrich M, Brown CJ, Block G (2005) The effect of folate fortification of cereal-grain products on blood folate status, dietary folate intake, and dietary folate sources among adult non-supplement users in the United States. J Am Coll Nutr 24: 2662274.
8. Choumenkovitch SF, Selhub J, Wilson PW, Rader JI, Rosenberg IH, et al. (2002) Folic acid intake from fortification in United States exceeds predictions. J Nutr 132: 279222798.
9. Smith AD, Kim YI, Refsum H (2008) Is folic acid good for everyone? Am J Clin Nutr 87: 5172533.
10. Haberg SE, London SJ, Stigum H, Nafstad P, Nystad W (2009) Folic acid supplements in pregnancy and early childhood respiratory health. Arch Dis Child 94: 1802184.
11. Whitrow MJ, Moore VM, Rumbold AR, Davies MJ (2009) Effect of supplemental folic acid in pregnancy on childhood asthma: a prospective birth cohort study. Am J Epidemiol 170: 148621493.
12. Yajnik CS, Deshmukh US (2008) Maternal nutrition, intrauterine programming and consequential risks in the offspring. Rev Endocr Metab Disord 9: 2032211.
13. Sweeney MR, McPartlin J, Weir DG, Daly S, Pentieva K, et al. (2005) Evidence of unmetabolised folic acid in cord blood of newborn and serum of 4-day-old infants. Br J Nutr 94: 7272730.
14. Junaid MA, Kuizon S, Cardona J, Azher T, Murakami N, et al. (2011) Folic acid supplementation dysregulates gene expression in lymphoblastoid cells-implications in nutrition. Biochem Biophys Res Commun 412: 6882692.
15. Barua S, Kuizon S, Chadman KK, Flory MJ, Brown WT, et al. (2014) Single-base resolution of mouse offspring brain methylome reveals epigenome modifications caused by gestational folic acid. Epigenetics Chromatin 7: 3.
16. Achon M, Reyes L, Alonso-Aperte E, Ubeda N, Varela-Moreiras G (1999) High dietary folate supplementation affects gestational development and dietary protein utilization in rats. J Nutr 129: 120421208.
17. Rampersaud GC, Kauwell GP, Hutson AD, Cerda JJ, Bailey LB (2000) Genomic DNA methylation decreases in response to moderate folate depletion in elderly women. Am J Clin Nutr 72: 99821003.
18. Sie KK, Li J, Ly A, Sohn KJ, Croxford R, et al. (2013) Effect of maternal and postweaning folic acid supplementation on global and gene-specific DNA methylation in the liver of the rat offspring. Mol Nutr Food Res 57: 6772685.
19. Pickell L, Brown K, Li D, Wang XL, Deng L, et al. (2011) High intake of folic acid disrupts embryonic development in mice. Birth Defects Res A Clin Mol Teratol 91: 8219.
20. Mikael LG, Deng L, Paul L, Selhub J, Rozen R (2013) Moderately high intake of folic acid has a negative impact on mouse embryonic development. Birth Defects Res A Clin Mol Teratol 97: 47252.
21. Miller JW, Ulrich CM (2013) Folic acid and cancer-where are we today? Lancet 381: 9742976.
22. Sittig LJ, Herzing LB, Xie H, Batra KK, Shukla PK, et al. (2012) Excess folate during adolescence suppresses thyroid function with permanent deficits in motivation and spatial memory. Genes Brain Behav 11: 1932200.
23. Heid MK, Bills ND, Hinrichs SH, Clifford AJ (1992) Folate deficiency alone does not produce neural tube defects in mice. J Nutr 122: 8882894.
24. Peng X, Wood CL, Blalock EM, Chen KC, Landfield PW, et al. (2003) Statistical implications of pooling RNA samples for microarray experiments. BMC Bioinformatics 4: 26.
25. Simon R, Lam A, Li MC, Ngan M, Menenzes S, et al. (2007) Analysis of gene expression data using BRB-ArrayTools. Cancer Inform 3: 11217.
26. Pfaffl MW (2004) Quantification strategies in real-time PCR. In: S.A Bustin, editors. A-Z of quantitative PCR. International University Line. 87(112.
27. Chadman KK, Gong S, Scattoni ML, Boltuck SE, Gandhy SU, et al. (2008) Minimal aberrant behavioral phenotypes of neuroligin-3 R451C knockin mice. Autism Res 1: 1472158.
28. Chadman KK (2011) Fluoxetine but not risperidone increases sociability in the BTBR mouse model of autism. Pharmacol Biochem Behav 97: 5862594.
29. Stapley NW, Guariglia SR, Chadman KK (2013) Cued and contextual fear conditioning in BTBR mice is improved with training or atomoxetine. Neurosci Lett 549: 1202124.
30. Chu PJ, Rivera JF, Arnold DB (2006) A role for Kif17 in transport of Kv4.2. J Biol Chem 281: 3652373.
31. Setou M, Nakagawa T, Seog DH, Hirokawa N (2000) Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 288: 179621802.
32. Silberberg G, Ben Shachar D, Navon R (2010) Genetic analysis of nitric oxide synthase 1 variants in schizophrenia and bipolar disorder. Am J Med Genet B Neuropsychiatr Genet 153B: 131821328.
33. Hamilton SM, Spencer CM, Harrison WR, Yuva-Paylor LA, Graham DF, et al. (2011) Multiple autism-like behaviors in a novel transgenic mouse model. Behav Brain Res 218: 29241.
34. Nakatani J, Tamada K, Hatanaka F, Ise S, Ohta H, et al. (2009) Abnormal behavior in a chromosome-engineered mouse model for human 15q11-13 duplication seen in autism. Cell 137: 123521246.
35. Muris P, Steerneman P, Merckelbach H, Holdrinet I, Meesters C (1998) Comorbid anxiety symptoms in children with pervasive developmental disorders. J Anxiety Disord 12: 3872393.
36. Hu VW, Addington A, Hyman A (2011) Novel autism subtype-dependent genetic variants are revealed by quantitative trait and subphenotype association analyses of published GWAS data. PLoS One 6: e19067.
37. Vincent JB, Noor A, Windpassinger C, Gianakopoulos PJ, Schwarzbraun T, et al. (2009) Characterization of a de novo translocation t(5; 18) (q33.1; q12.1) in an autistic boy identifies a breakpoint close to SH3TC2, ADRB2, and HTR4 on 5q, and within the desmocollin gene cluster on 18q. Am J Med Genet B Neuropsychiatr Genet 150B: 8172826.
38. Ohtsuki T, Ishiguro H, Detera-Wadleigh SD, Toyota T, Shimizu H, et al. (2002) Association between serotonin 4 receptor gene polymorphisms and bipolar disorder in Japanese case-control samples and the NIMH Genetics Initiative Bipolar Pedigrees. Mol Psychiatry 7: 9542961.
39. Balschun D, Moechars D, Callaerts-Vegh Z, Vermaercke B, Van Acker N, et al. (2010) Vesicular glutamate transporter VGLUT1 has a role in hippocampal long-term potentiation and spatial reversal learning. Cereb Cortex 20: 6842693.
40. Fremeau RT Jr, Kam K, Qureshi T, Johnson J, Copenhagen DR, et al. (2004) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304: 181521819.
41. Fremeau RT Jr, Voglmaier S, Seal RP, Edwards RH (2004) VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci 27: 982103.
42. Wilson NR, Kang J, Hueske EV, Leung T, Varoqui H, et al. (2005) Presynaptic regulation of quantal size by the vesicular glutamate transporter VGLUT1. J Neurosci 25: 622126234.
43. Wojcik SM, Rhee JS, Herzog E, Sigler A, Jahn R, et al. (2004) An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc Natl Acad Sci U S A 101: 715827163.
44. Gilabert-Juan J, Varea E, Guirado R, Blasco-Ibanez JM, Crespo C, et al. (2012) Alterations in the expression of PSA-NCAM and synaptic proteins in the dorsolateral prefrontal cortex of psychiatric disorder patients. Neurosci Lett 530: 972102.
45. Callaerts-Vegh Z, Moechars D, Van Acker N, Daneels G, Goris I, et al. (2013) Haploinsufficiency of VGluT1 but not VGluT2 impairs extinction of spatial preference and response suppression. Behav Brain Res 245: 13221.
46. Heng YH, McLeay RC, Harvey TJ, Smith AG, Barry G, et al. (2012) NFIX Regulates Neural Progenitor Cell Differentiation During Hippocampal Morphogenesis. Cereb Cortex 24: 2612279.
47. Johnson CW, Hernandez-Lagunas L, Feng W, Melvin VS, Williams T, et al. (2011) Vgll2a is required for neural crest cell survival during zebrafish craniofacial development. Dev Biol 357: 2692281.
48. Chen Z, Schwahn BC, Wu Q, He X, Rozen R (2005) Postnatal cerebellar defects in mice deficient in methylenetetrahydrofolate reductase. Int J Dev Neurosci 23: 4652474.
49. Friso S, Choi SW, Girelli D, Mason JB, Dolnikowski GG, et al. (2002) A common mutation in the 5, 10-methylenetetrahydrofolate reductase gene affects genomic DNA methylation through an interaction with folate status. Proc Natl Acad Sci U S A 99: 560625611.
50. Dewing P, Shi T, Horvath S, Vilain E (2003) Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Brain Res Mol Brain Res 118: 82290.
51. Payer B, Lee JT (2008) X chromosome dosage compensation: how mammals keep the balance. Annu Rev Genet 42: 7332772.
52. Vawter MP, Harvey PD, DeLisi LE (2007) Dysregulation of X-linked gene expression in Klinefelter's syndrome and association with verbal cognition. Am J Med Genet B Neuropsychiatr Genet 144B: 7282734.
53. Ladd-Acosta C, Hansen KD, Briem E, Fallin MD, Kaufmann WE, et al. (2013) Common DNA methylation alterations in multiple brain regions in autism. Mol Psychiatry doi:10.1038/mp.2013.114 [Epub ahead of print].
54. Robertson KD, Wolffe AP (2000) DNA methylation in health and disease. Nat Rev Genet 1: 11219.
55. Zhao X, Ueba T, Christie BR, Barkho B, McConnell MJ, et al. (2003) Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function. Proc Natl Acad Sci U S A 100: 677726782.
56. Suren P, Roth C, Bresnahan M, Haugen M, Hornig M, et al. (2013) Association between maternal use of folic acid supplements and risk of autism spectrum disorders in children. JAMA 309: 5702577.
57. Iskandar BJ, Rizk E, Meier B, Hariharan N, Bottiglieri T, et al. (2010) Folate regulation of axonal regeneration in the rodent central nervous system through DNA methylation. J Clin Invest 120: 160321616.