Birth weight, working memory and epigenetic signatures in IGF2 and related genes: A MZ twin study

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Córdova Palomera, Aldo ^a,b   Alemany, Silvia ^a,b   Fatjó Vilas, Mar ^a,b   Goldberg, Ximena ^a,b   Leza, Juan Carlos ^b,c,d   González Pinto, Ana ^b,e   Nenadic, Igor ^f   Fañanás, Lourdes ^a,b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^d HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

^e UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^f JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SOMATOMEDIN B; IGF2 PROTEIN, HUMAN;

ADULT; ARTICLE; BIRTH WEIGHT; COGNITION; CPG ISLAND; DNA METHYLATION; ENVIRONMENTAL FACTOR; EPIGENETICS; FEMALE; FETUS; GENE LOCUS; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; IGF2 GENE; IGF2BP1 GENE; IGF2BP2 GENE; IGF2BP3 GENE; INTELLIGENCE QUOTIENT; INTER INDIVIDUAL VARIABILITY; INTRAPAIR VARIABILITY; INTRON; MALE; MONOZYGOTIC TWINS; NAMED INVENTORIES, QUESTIONNAIRES AND RATING SCALES; PHENOTYPE; PREGNANCY COMPLICATION; PRENATAL STRESS; WECHSLER INTELLIGENCE SCALE; WORKING MEMORY; GENETIC EPIGENESIS; GENETICS; MOSAICISM; PHYSIOLOGY; PREGNANCY; SHORT TERM MEMORY; STATISTICS;

BIRTH WEIGHT; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; HUMANS; INSULIN-LIKE GROWTH FACTOR II; MEMORY, SHORT-TERM; MOSAICISM; PREGNANCY; STOCHASTIC PROCESSES; TWINS, MONOZYGOTIC;

EID: 84921355345     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103639     Document Type: Article

References (77)

1. Barker DJ (2004) The developmental origins of adult disease. J Am Coll Nutr 23: 588S-595S.
2. Eack SM, Bahorik AL, McKnight SA, Hogarty SS, Greenwald DP, et al. (2013) Commonalities in social and non-social cognitive impairments in adults with autism spectrum disorder and schizophrenia. Schizophr Res 148: 24-28.
3. Losh M, Esserman D, Anckarsater H, Sullivan PF, Lichtenstein P (2012) Lower birth weight indicates higher risk of autistic traits in discordant twin pairs. Psychol Med 42: 1091-1102.
4. Matheson SL, Shepherd AM, Laurens KR, Carr VJ (2011) A systematic meta-review grading the evidence for non-genetic risk factors and putative antecedents of schizophrenia. Schizophr Res 133: 133-142.
5. Cordova-Palomera A, Goldberg X, Alemany S, Nenadic I, Gasto C, et al. (2013) Letter to the Editor: Low birth weight and adult depression: eliciting their association. Psychol Med: 1-3.
6. Wojcik W, Lee W, Colman I, Hardy R, Hotopf M (2013) Foetal origins of depression? A systematic review and meta-analysis of low birth weight and later depression. Psychol Med 43: 1-12.
7. Burdge GC, Lillycrop KA (2010) Nutrition, epigenetics, and developmental plasticity: implications for understanding human disease. Annu Rev Nutr 30: 315-339.
8. Feinberg AP, Irizarry RA (2010) Evolution in health and medicine Sackler colloquium: Stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease. Proc Natl Acad Sci U S A 107 Suppl 1: 1757-1764.
9. Feinberg AP, Irizarry RA, Fradin D, Aryee MJ, Murakami P, et al. (2010) Personalized epigenomic signatures that are stable over time and covary with body mass index. Sci Transl Med 2: 49ra67.
10. Reynolds RM, Jacobsen GH, Drake AJ (2013) What is the evidence in humans that DNA methylation changes link events in utero and later life disease? Clin Endocrinol (Oxf) 78: 814-822.
11. Vardatsikos G, Sahu A, Srivastava AK (2009) The insulin-like growth factor family: molecular mechanisms, redox regulation, and clinical implications. Antioxid Redox Signal 11: 1165-1190.
12. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, et al. (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A 105: 17046-17049.
13. Hoyo C, Fortner K, Murtha AP, Schildkraut JM, Soubry A, et al. (2012) Association of cord blood methylation fractions at imprinted insulin-like growth factor 2 (IGF2), plasma IGF2, and birth weight. Cancer Causes Control 23: 635-645.
14. Hoyo C, Murtha AP, Schildkraut JM, Jirtle RL, Demark-Wahnefried W, et al. (2011) Methylation variation at IGF2 differentially methylated regions and maternal folic acid use before and during pregnancy. Epigenetics 6: 928-936.
15. Steegers-Theunissen RP, Obermann-Borst SA, Kremer D, Lindemans J, Siebel C, et al. (2009) Periconceptional maternal folic acid use of 400 microg per day is related to increased methylation of the IGF2 gene in the very young child. PLoS One 4: e7845.
16. Wehkalampi K, Muurinen M, Wirta SB, Hannula-Jouppi K, Hovi P, et al. (2013) Altered Methylation of Locus 20 Years after Preterm Birth at Very Low Birth Weight. PLoS One 8: e67379.
17. Pidsley R, Dempster E, Troakes C, Al-Sarraj S, Mill J (2012) Epigenetic and genetic variation at the IGF2/H19 imprinting control region on 11p15.5 is associated with cerebellum weight. Epigenetics 7: 155-163.
18. Pidsley R, Dempster EL, Mill J (2010) Brain weight in males is correlated with DNA methylation at IGF2. Mol Psychiatry 15: 880-881.
19. Pidsley R, Fernandes C, Viana J, Paya-Cano JL, Liu L, et al. (2012) DNA methylation at the Igf2/H19 imprinting control region is associated with cerebellum mass in outbred mice. Mol Brain 5: 42.
20. Sigurdsson T, Stark KL, Karayiorgou M, Gogos JA, Gordon JA (2010) Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 464: 763-767.
21. Alfimova MV, Lezheiko TV, Gritsenko IK, Golimbet VE (2012) [Association of the insulin-like growth factor II (IGF2) gene with human cognitive functions]. Genetika 48: 993-998.
22. Bracko O, Singer T, Aigner S, Knobloch M, Winner B, et al. (2012) Gene expression profiling of neural stem cells and their neuronal progeny reveals IGF2 as a regulator of adult hippocampal neurogenesis. J Neurosci 32: 3376-3387.
23. Nyberg F, Hallberg M (2013) Growth hormone and cognitive function. Nat Rev Endocrinol 9: 357-365.
24. Ouchi Y, Banno Y, Shimizu Y, Ando S, Hasegawa H, et al. (2013) Reduced Adult Hippocampal Neurogenesis and Working Memory Deficits in the Dgcr8-Deficient Mouse Model of 22q11.2 Deletion-Associated Schizophrenia Can Be Rescued by IGF2. J Neurosci 33: 9408-9419.
25. Alberini CM, Chen DY (2012) Memory enhancement: consolidation, reconsolidation and insulin-like growth factor 2. Trends Neurosci 35: 274-283.
26. Chen DY, Stern SA, Garcia-Osta A, Saunier-Rebori B, Pollonini G, et al. (2011) A critical role for IGF-II in memory consolidation and enhancement. Nature 469: 491-497.
27. Baddeley A (2010) Working memory. Curr Biol 20: R136-140.
28. Baddeley A (2012) Working memory: theories, models, and controversies. Annu Rev Psychol 63: 1-29.
29. Gathercole SE, Pickering SJ, Ambridge B, Wearing H (2004) The structure of working memory from 4 to 15 years of age. Dev Psychol 40: 177-190. (Pubitemid 38284496)
30. Tamnes CK, Walhovd KB, Grydeland H, Holland D, Ostby Y, et al. (2013) Longitudinal working memory development is related to structural maturation of frontal and parietal cortices. J Cogn Neurosci 25: 1611-1623.
31. Shipstead Z, Redick TS, Engle RW (2012) Is working memory training effective? Psychol Bull 138: 628-654.
32. Bennett DS, Mohamed FB, Carmody DP, Malik M, Faro SH, et al. (2013) Prenatal tobacco exposure predicts differential brain function during working memory in early adolescence: a preliminary investigation. Brain Imaging Behav 7: 49-59.
33. Kodituwakku PW, Kalberg W, May PA (2001) The effects of prenatal alcohol exposure on executive functioning. Alcohol Res Health 25: 192-198. (Pubitemid 33708982)
34. Freedman D, Bao Y, Kremen WS, Vinogradov S, McKeague IW, et al. (2013) Birth weight and neurocognition in schizophrenia spectrum disorders. Schizophr Bull 39: 592-600.
35. Guilherme R, Drunat S, Delezoide AL, Oury JF, Luton D (2009) Zygosity and chorionicity in triplet pregnancies: new data. Hum Reprod 24: 100-105.
36. Bibikova M, Barnes B, Tsan C, Ho V, Klotzle B, et al. (2011) High density DNA methylation array with single CpG site resolution. Genomics 98: 288-295.
37. Sandoval J, Heyn H, Moran S, Serra-Musach J, Pujana MA, et al. (2011) Validation of a DNA methylation microarray for 450,000 CpG sites in the human genome. Epigenetics 6: 692-702.
38. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, et al. (2002) The human genome browser at UCSC. Genome Res 12: 996-1006. (Pubitemid 34662293)
39. Lewis S, Owen M, Murray R (1989) Obstetric complications and schizophrenia: methodology and mechanisms. New York: Oxford University Press.
40. Catov JM, Newman AB, Kelsey SF, Roberts JM, Sutton-Tyrrell KC, et al. (2006) Accuracy and reliability of maternal recall of infant birth weight among older women. Ann Epidemiol 16: 429-431. (Pubitemid 43744460)
41. Luecke RH, Wosilait WD, Young JF (1995) Mathematical representation of organ growth in the human embryo/fetus. Int J Biomed Comput 39: 337-347.
42. Glinianaia SV, Skjaerven R, Magnus P (2000) Birthweight percentiles by gestational age in multiple births. A population-based study of Norwegian twins and triplets. Acta Obstet Gynecol Scand 79: 450-458. (Pubitemid 30326125)
43. Sattler JM (2001) Assessment of children: cognitive applications. San Diego: J.M. Sattler.
44. Wechsler D, Cordero Pando A, Yela Granizo M, Zimmerman IL, Woo-Sam JM, et al. (1997) WAIS escala de inteligencia de Wechsler para adultos. Madrid; Barcelona: TEA Ediciones.
45. Goldberg X, Alemany S, Rosa A, Picchioni M, Nenadic I, et al. (2013) Substantial genetic link between iq and working memory: Implications for molecular genetic studies on schizophrenia. the european twin study of schizophrenia (EUTwinsS). Am J Med Genet B Neuropsychiatr Genet 162: 413-418.
46. Oberauer K, Schulze R, Wilhelm O, Suss HM (2005) Working memory and intelligence-their correlation and their relation: comment on Ackerman, Beier, and Boyle (2005). Psychol Bull 131: 61-65; author reply 72-65.
47. Begg MD, Parides MK (2003) Separation of individual-level and cluster-level covariate effects in regression analysis of correlated data. Stat Med 22: 2591-2602. (Pubitemid 36974582)
48. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
49. Bates D, Maechler M, Bolker B (2013) lme4: Linear mixed-effects models using S4 classes.
50. Baayen RH (2011) languageR: Data sets and functions with "Analyzing Linguistic Data: A practical introduction to statistics".
51. Parets SE, Conneely KN, Kilaru V, Fortunato SJ, Syed TA, et al. (2013) Fetal DNA Methylation Associates with Early Spontaneous Preterm Birth and Gestational Age. PLoS One 8: e67489.
52. Ursini G, Bollati V, Fazio L, Porcelli A, Iacovelli L, et al. (2011) Stress-related methylation of the catechol-O-methyltransferase Val 158 allele predicts human prefrontal cognition and activity. J Neurosci 31: 6692-6698.
53. Yisraeli JK (2005) VICKZ proteins: a multi-talented family of regulatory RNA-binding proteins. Biol Cell 97: 87-96.
54. Waterhouse EG, Xu B (2009) New insights into the role of brain-derived neurotrophic factor in synaptic plasticity. Mol Cell Neurosci 42: 81-89.
55. Sasaki Y, Welshhans K, Wen Z, Yao J, Xu M, et al. (2010) Phosphorylation of zipcode binding protein 1 is required for brain-derived neurotrophic factor signaling of local beta-actin synthesis and growth cone turning. J Neurosci 30: 9349-9358.
56. Welshhans K, Bassell GJ (2011) Netrin-1-induced local beta-actin synthesis and growth cone guidance requires zipcode binding protein 1. J Neurosci 31: 9800-9813.
57. Perycz M, Urbanska AS, Krawczyk PS, Parobczak K, Jaworski J (2011) Zipcode binding protein 1 regulates the development of dendritic arbors in hippocampal neurons. J Neurosci 31: 5271-5285.
58. Tiruchinapalli DM, Oleynikov Y, Kelic S, Shenoy SM, Hartley A, et al. (2003) Activity-dependent trafficking and dynamic localization of zipcode binding protein 1 and beta-actin mRNA in dendrites and spines of hippocampal neurons. J Neurosci 23: 3251-3261. (Pubitemid 36531966)
59. van Eijk KR, de Jong S, Boks MP, Langeveld T, Colas F, et al. (2012) Genetic analysis of DNA methylation and gene expression levels in whole blood of healthy human subjects. BMC Genomics 13: 636.
60. LaSalle JM, Powell WT, Yasui DH (2013) Epigenetic layers and players underlying neurodevelopment. Trends Neurosci 36: 460-470.
61. Rauch TA, Wu X, Zhong X, Riggs AD, Pfeifer GP (2009) A human B cell methylome at 100-base pair resolution. Proc Natl Acad Sci U S A 106: 671-678.
62. Maziade M, Paccalet T (2013) A protective-compensatory model may reconcile the genetic and the developmental findings in schizophrenia. Schizophr Res 144: 9-15.
63. Miller J, Chauhan SP, Abuhamad AZ (2012) Discordant twins: diagnosis, evaluation and management. Am J Obstet Gynecol 206: 10-20.
64. Ollikainen M, Smith KR, Joo EJ, Ng HK, Andronikos R, et al. (2010) DNA methylation analysis of multiple tissues from newborn twins reveals both genetic and intrauterine components to variation in the human neonatal epigenome. Hum Mol Genet 19: 4176-4188.
65. Gordon L, Joo JE, Powell JE, Ollikainen M, Novakovic B, et al. (2012) Neonatal DNA methylation profile in human twins is specified by a complex interplay between intrauterine environmental and genetic factors, subject to tissue-specific influence. Genome Res 22: 1395-1406.
66. Souren NY, Lutsik P, Gasparoni G, Tierling S, Gries J, et al. (2013) Adult monozygotic twins discordant for intra-uterine growth have indistinguishable genome-wide DNA methylation profiles. Genome Biol 14: R44.
67. Karlsgodt KH, Kochunov P, Winkler AM, Laird AR, Almasy L, et al. (2010) A multimodal assessment of the genetic control over working memory. J Neurosci 30: 8197-8202.
68. Malleret G, Alarcon JM, Martel G, Takizawa S, Vronskaya S, et al. (2010) Bidirectional regulation of hippocampal long-term synaptic plasticity and its influence on opposing forms of memory. J Neurosci 30: 3813-3825.
69. Mukhopadhyay P, Horn KH, Greene RM, Michele Pisano M (2010) Prenatal exposure to environmental tobacco smoke alters gene expression in the developing murine hippocampus. Reprod Toxicol 29: 164-175.
70. Sherry ST, Ward MH, Kholodov M, Baker J, Phan L, et al. (2001) dbSNP: the NCBI database of genetic variation. Nucleic Acids Res 29: 308-311. (Pubitemid 32054478)
71. Davies MN, Volta M, Pidsley R, Lunnon K, Dixit A, et al. (2012) Functional annotation of the human brain methylome identifies tissue-specific epigenetic variation across brain and blood. Genome Biol 13: R43.
72. Varley KE, Gertz J, Bowling KM, Parker SL, Reddy TE, et al. (2013) Dynamic DNA methylation across diverse human cell lines and tissues. Genome Res 23: 555-567.
73. Provencal N, Suderman MJ, Guillemin C, Massart R, Ruggiero A, et al. (2012) The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells. J Neurosci 32: 15626-15642.
74. Szyf M (2013) DNA methylation, behavior and early life adversity. J Genet Genomics 40: 331-338.
75. Szyf M, Bick J (2013) DNA methylation: a mechanism for embedding early life experiences in the genome. Child Dev 84: 49-57.
76. Hayashi-Takagi A, Vawter MP, Iwamoto K (2013) Peripheral Biomarkers Revisited: Integrative Profiling of Peripheral Samples for Psychiatric Research. Biol Psychiatry.
77. Tylee DS, Kawaguchi DM, Glatt SJ (2013) On the outside, looking in: a review and evaluation of the comparability of blood and brain "-omes". Am J Med Genet B Neuropsychiatr Genet 162B: 595-603.