Placental methylome analysis from a prospective autism study

Molecular Autism

Volumn 7, Issue 1, 2016, Pages

  Schroeder, Diane I ^a   Schmidt, Rebecca J ^b,c   Crary Dooley, Florence K ^a   Walker, Cheryl K ^b,c   Ozonoff, Sally ^b,c   Tancredi, Daniel J ^b   Hertz Picciotto, Irva ^b,c   LaSalle, Janine M ^a,c  

^a Genome Center   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biomarkers; DNA methylation; Epigenetics; Genomics; Methylome; Placenta

Indexed keywords

ARTICLE; AUTISM; CHILD; CHILD DEVELOPMENT; CLINICAL ARTICLE; DLL1 GENE; DNA METHYLATION; DNA STRUCTURE; FEMALE; GENE; HIGHLY METHYLATED DOMAIN; HUMAN; HUMAN TISSUE; PARTIALLY METHYLATED DOMAIN; PLACENTA; PRIORITY JOURNAL; PROSPECTIVE STUDY; PYROSEQUENCING; AUTISM SPECTRUM DISORDER; EARLY DIAGNOSIS; ENHANCER REGION; GENETIC EPIGENESIS; GENETICS; GENOME-WIDE ASSOCIATION STUDY; HIGH THROUGHPUT SEQUENCING; HUMAN GENOME; MALE; METABOLISM; NEWBORN; PREGNANCY; PRESCHOOL CHILD;

BIOLOGICAL MARKER; DLK1 PROTEIN, HUMAN; MEMBRANE PROTEIN; SIGNAL PEPTIDE;

AUTISM SPECTRUM DISORDER; BIOMARKERS; CHILD, PRESCHOOL; DNA METHYLATION; EARLY DIAGNOSIS; ENHANCER ELEMENTS, GENETIC; EPIGENESIS, GENETIC; FEMALE; GENOME, HUMAN; GENOME-WIDE ASSOCIATION STUDY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INFANT, NEWBORN; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; PLACENTA; PREGNANCY;

EID: 85006255880     PISSN: None     EISSN: 20402392     Source Type: Journal    
DOI: 10.1186/s13229-016-0114-8     Document Type: Article

References (56)

1. Center for Disease Control and Prevention. Prevalence and characteristics of autism spectrum disorder among children aged 8 years - Autism and Developmental Disabilities Monitoring Network, 11 Sites, United States, 2012. MMWR Surveill Summ. 2016;65:1-23.
2. Messinger D, Young GS, Ozonoff S, Dobkins K, Carter A, Zwaigenbaum L, Landa RJ, Charman T, Stone WL, Constantino JN, et al. Beyond autism: a baby siblings research consortium study of high-risk children at three years of age. J Am Acad Child Adolesc Psychiatry. 2013;52(3):300-8. e301.
3. Chawarska K, Shic F, Macari S, Campbell DJ, Brian J, Landa R, Hutman T, Nelson CA, Ozonoff S, Tager-Flusberg H, et al. 18-month predictors of later outcomes in younger siblings of children with autism spectrum disorder: a baby siblings research consortium study. J Am Acad Child Adolesc Psychiatry. 2014;53(12):1317-27. e1311.
4. Ozonoff S, Young GS, Carter A, Messinger D, Yirmiya N, Zwaigenbaum L, Bryson S, Carver LJ, Constantino JN, Dobkins K, et al. Recurrence risk for autism spectrum disorders: a baby siblings research consortium study. Pediatrics. 2011;128(3):e488-95.
5. Bourgeron T. From the genetic architecture to synaptic plasticity in autism spectrum disorder. Nat Rev Neurosci. 2015;16(9):551-63.
6. Geschwind DH, State MW. Gene hunting in autism spectrum disorder: on the path to precision medicine. Lancet Neurol. 2015;14(11):1109-20.
7. LaSalle JM. Epigenomic strategies at the interface of genetic and environmental risk factors for autism. J Hum Genet. 2013;58(7):396-401.
8. Hellerstedt WL, McGovern PM, Fontaine P, Oberg CN, Cordes JE. Prenatal environmental exposures and child health: Minnesota's role in the National Children's Study. Minn Med. 2008;91(9):40-3.
9. Brown AS. Epidemiologic studies of exposure to prenatal infection and risk of schizophrenia and autism. Dev Neurobiol. 2012;72(10):1272-6.
10. Roberts AL, Lyall K, Hart JE, Laden F, Just AC, Bobb JF, Koenen KC, Ascherio A, Weisskopf MG. Perinatal air pollutant exposures and autism spectrum disorder in the children of nurses' health study II participants. Environ Health Perspect. 2013;121(8):978-84.
11. Schmidt RJ, Tancredi DJ, Ozonoff S, Hansen RL, Hartiala J, Allayee H, Schmidt LC, Tassone F, Hertz-Picciotto I. Maternal periconceptional folic acid intake and risk of autism spectrum disorders and developmental delay in the CHARGE (CHildhood Autism Risks from Genetics and Environment) case-control study. Am J Clin Nutr. 2012;96(1):80-9.
12. Schmidt RJ. Maternal folic acid supplements associated with reduced autism risk in the child. Evid Based Med. 2013;18(6):e53.
13. Estes A, Munson J, Rogers SJ, Greenson J, Winter J, Dawson G. Long-term outcomes of early intervention in 6-year-old children with autism spectrum disorder. J Am Acad Child Adolesc Psychiatry. 2015;54(7):580-7.
14. Loke YJ, Hannan AJ, Craig JM. The role of epigenetic change in autism spectrum disorders. Front Neurol. 2015;6:107.
15. Flanagan JM. Epigenome-wide association studies (EWAS): past, present, and future. Methods Mol Biol. 2015;1238:51-63.
16. Schroeder DI, Blair JD, Lott P, Yu HO, Hong D, Crary F, Ashwood P, Walker C, Korf I, Robinson WP, et al. The human placenta methylome. Proc Natl Acad Sci U S A. 2013;110(15):6037-42.
17. Schroeder DI, Lott P, Korf I, LaSalle JM. Large-scale methylation domains mark a functional subset of neuronally expressed genes. Genome Res. 2011;21(10):1583-91.
18. Schroeder DI, Jayashankar K, Douglas KC, Thirkill TL, York D, Dickinson PJ, Williams LE, Samollow PB, Ross PJ, Bannasch DL, et al. Early developmental and evolutionary origins of gene body DNA methylation patterns in mammalian placentas. PLoS Genet. 2015;11(8):e1005442.
19. Walker CK, Anderson KW, Milano KM, Ye S, Tancredi DJ, Pessah IN, Hertz-Picciotto I, Kliman HJ. Trophoblast inclusions are significantly increased in the placentas of children in families at risk for autism. Biol Psychiatry. 2013;74(3):204-11.
20. Lord C, Risi S, Lambrecht L, Cook Jr EH, Leventhal BL, DiLavore PC, Pickles A, Rutter M. The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord. 2000;30(3):205-23.
21. Lord C, Rutter M, DiLavore PC, Risi S. The Autism Diagnostic Observation Schedule (ADOS). Los Angeles: Western Psychological Services; 2000.
22. Chen PY, Cokus SJ, Pellegrini M. BS Seeker: precise mapping for bisulfite sequencing. BMC Bioinformatics. 2010;11:203.
23. Lott PC, Korf I. StochHMM: a flexible hidden Markov model tool and C++ library. Bioinformatics. 2014;30(11):1625-6.
24. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol. 1995;57(1):289-300.
25. Bozdogan H. Model selection and Akaike's Information Criterion (AIC): the general theory and its analytical extensions. Psychometrika. 1987;52(3):345-70.
26. Akaike H. Information theory and an extension of the maximum likelihood principle. In: Csaki BNPBF, editor. Second international symposium on information theory. Budapest: Academiai Kiado; 1973.
27. Cotton AM, Avila L, Penaherrera MS, Affleck JG, Robinson WP, Brown CJ. Inactive X chromosome-specific reduction in placental DNA methylation. Hum Mol Genet. 2009;18(19):3544-52.
28. Kundaje A, Meuleman W, Ernst J, Bilenky M, Yen A, Heravi-Moussavi A, Kheradpour P, Zhang Z, Wang J, Ziller MJ, et al. Integrative analysis of 111 reference human epigenomes. Nature. 2015;518(7539):317-30.
29. Rao SS, Huntley MH, Durand NC, Stamenova EK, Bochkov ID, Robinson JT, Sanborn AL, Machol I, Omer AD, Lander ES, et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell. 2014;159(7):1665-80.
30. Shimojo H, Ohtsuka T, Kageyama R. Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron. 2008;58(1):52-64.
31. Shimojo H, Isomura A, Ohtsuka T, Kori H, Miyachi H, Kageyama R. Oscillatory control of Delta-like1 in cell interactions regulates dynamic gene expression and tissue morphogenesis. Genes Dev. 2016;30(1):102-16.
32. Amiri A, Cho W, Zhou J, Birnbaum SG, Sinton CM, McKay RM, Parada LF. Pten deletion in adult hippocampal neural stem/progenitor cells causes cellular abnormalities and alters neurogenesis. J Neurosci. 2012;32(17):5880-90.
33. Chen J, Alberts I, Li X. Dysregulation of the IGF-I/PI3K/AKT/mTOR signaling pathway in autism spectrum disorders. Int J Dev Neurosci. 2014;35:35-41.
34. Hormozdiari F, Penn O, Borenstein E, Eichler EE. The discovery of integrated gene networks for autism and related disorders. Genome Res. 2015;25(1):142-54.
35. Baron-Cohen S, Lombardo MV, Auyeung B, Ashwin E, Chakrabarti B, Knickmeyer R. Why are autism spectrum conditions more prevalent in males? PLoS Biol. 2011;9(6):e1001081.
36. Nugent BM, Wright CL, Shetty AC, Hodes GE, Lenz KM, Mahurkar A, Russo SJ, Devine SE, McCarthy MM. Brain feminization requires active repression of masculinization via DNA methylation. Nat Neurosci. 2015;18(5):690-7.
37. Dhiman VK, Attwood K, Campbell MJ, Smiraglia DJ. Hormone stimulation of androgen receptor mediates dynamic changes in DNA methylation patterns at regulatory elements. Oncotarget. 2015;6(40):42575-89.
38. Otti GR, Saleh L, Velicky P, Fiala C, Pollheimer J, Knofler M. Notch2 controls prolactin and insulin-like growth factor binding protein-1 expression in decidualizing human stromal cells of early pregnancy. PLoS ONE. 2014;9(11):e112723.
39. Murta D, Batista M, Trindade A, Silva E, Mateus L, Duarte A, Lopes-da-Costa L. Dynamics of Notch signalling in the mouse oviduct and uterus during the oestrous cycle. Reprod Fertil Dev. 2015;28(11):1663-78. doi:10.1071/RD15029.
40. Baron-Cohen S, Auyeung B, Norgaard-Pedersen B, Hougaard DM, Abdallah MW, Melgaard L, Cohen AS, Chakrabarti B, Ruta L, Lombardo MV. Elevated fetal steroidogenic activity in autism. Mol Psychiatry. 2015;20(3):369-76.
41. Huuskonen P, Amezaga MR, Bellingham M, Jones LH, Storvik M, Hakkinen M, Keski-Nisula L, Heinonen S, O'Shaughnessy PJ, Fowler PA, et al. The human placental proteome is affected by maternal smoking. Reprod Toxicol. 2016;63:22-31.
42. Ladd-Acosta C, Hansen KD, Briem E, Fallin MD, Kaufmann WE, Feinberg AP. Common DNA methylation alterations in multiple brain regions in autism. Mol Psychiatry. 2014;19(8):862-71.
43. Nardone S, Sams DS, Reuveni E, Getselter D, Oron O, Karpuj M, Elliott E. DNA methylation analysis of the autistic brain reveals multiple dysregulated biological pathways. Transl Psychiatry. 2014;4:e433.
44. Feinberg JI, Bakulski KM, Jaffe AE, Tryggvadottir R, Brown SC, Goldman LR, Croen LA, Hertz-Picciotto I, Newschaffer CJ, Fallin MD, et al. Paternal sperm DNA methylation associated with early signs of autism risk in an autism-enriched cohort. Int J Epidemiol. 2015;44(4):1199-210.
45. Berko ER, Suzuki M, Beren F, Lemetre C, Alaimo CM, Calder RB, Ballaban-Gil K, Gounder B, Kampf K, Kirschen J, et al. Mosaic epigenetic dysregulation of ectodermal cells in autism spectrum disorder. PLoS Genet. 2014;10(5):e1004402.
46. CV B, CJ M, E F, K N, JM G, DC D, J H, N H, JM L, R S et al: Small magnitude effect sizes in epigenetic endpoints are important in children's environmental health studies. Environ Health Perspect. in press.
47. Gregory SG, Connelly JJ, Towers AJ, Johnson J, Biscocho D, Markunas CA, Lintas C, Abramson RK, Wright HH, Ellis P, et al. Genomic and epigenetic evidence for oxytocin receptor deficiency in autism. BMC Med. 2009;7:62.
48. Behnia F, Parets SE, Kechichian T, Yin H, Dutta EH, Saade GR, Smith AK, Menon R. Fetal DNA methylation of autism spectrum disorders (ASD) candidate genes: association with spontaneous preterm birth. Am J Obstet Gynecol. 2015;212(4):533.e1-9.
49. James SJ, Shpyleva S, Melnyk S, Pavliv O, Pogribny IP. Elevated 5-hydroxymethylcytosine in the Engrailed-2 (EN-2) promoter is associated with increased gene expression and decreased MeCP2 binding in autism cerebellum. Transl Psychiatry. 2014;4:e460.
50. James SJ, Shpyleva S, Melnyk S, Pavliv O, Pogribny IP. Complex epigenetic regulation of engrailed-2 (EN-2) homeobox gene in the autism cerebellum. Transl Psychiatry. 2013;3:e232.
51. Nagarajan RP, Patzel KA, Martin M, Yasui DH, Swanberg SE, Hertz-Picciotto I, Hansen RL, Van de Water J, Pessah IN, Jiang R, et al. MECP2 promoter methylation and X chromosome inactivation in autism. Autism Res. 2008;1(3):169-78.
52. Nagarajan RP, Hogart AR, Gwye Y, Martin MR, LaSalle JM. Reduced MeCP2 expression is frequent in autism frontal cortex and correlates with aberrant MECP2 promoter methylation. Epigenetics. 2006;1(4):e1-11.
53. Wang YS Z. Chapter 4, Cell Types of the Placenta. In: Vascular biology of the placenta. San Rafael (CA): Morgan & Claypool Life Sciences; 2010.
54. Van Handel B, Prashad SL, Hassanzadeh-Kiabi N, Huang A, Magnusson M, Atanassova B, Chen A, Hamalainen EI, Mikkola HK. The first trimester human placenta is a site for terminal maturation of primitive erythroid cells. Blood. 2010;116(17):3321-30.
55. de Goede OM, Razzaghian HR, Price EM, Jones MJ, Kobor MS, Robinson WP, Lavoie PM. Nucleated red blood cells impact DNA methylation and expression analyses of cord blood hematopoietic cells. Clin Epigenetics. 2015;7:95.
56. Bakulski KM, Feinberg JI, Andrews SV, Yang J, Brown S, Mckenney SL, Witter F, Walston J, Feinberg AP, Fallin MD. DNA methylation of cord blood cell types: applications for mixed cell birth studies. Epigenetics. 2016;11(5):354-62.