Expression of imprinted genes in placenta is associated with infant neurobehavioral development

Epigenetics

Volumn 10, Issue 9, 2015, Pages 834-841

  Green, Benjamin B ^a   Kappil, Maya ^b   Lambertini, Luca ^b   Armstrong, David A ^a   Guerin, Dylan J ^a   Sharp, Andrew J ^b   Lester, Barry M ^c   Chen, Jia ^b   Marsit, Carmen J ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c BROWN UNIVERSITY   (United States)

Author keywords

Developmental origins of health and disease; Epigenetics; Imprinting; Neurodevelopment; Placenta

Indexed keywords

ADULT; ARTICLE; COGNITION ASSESSMENT; EPIGENETICS; FEMALE; GENE EXPRESSION; GENETIC ANALYSIS; GENOME IMPRINTING; HUMAN; MRNA EXPRESSION ASSAY; NERVOUS SYSTEM FUNCTION; NEUROBEHAVIORAL DEVELOPMENT; PLACENTA; SCORING SYSTEM; CHILD BEHAVIOR; CHILD DEVELOPMENT; GENE EXPRESSION REGULATION; GENETIC VARIATION; INFANT; METABOLISM; NEWBORN; PHYSIOLOGY; PREGNANCY;

CHILD DEVELOPMENT; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VARIATION; GENOMIC IMPRINTING; HUMANS; INFANT; INFANT BEHAVIOR; INFANT, NEWBORN; PLACENTA; PREGNANCY;

EID: 84954569883     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.1080/15592294.2015.1073880     Document Type: Article

References (46)

1. Peters J. The role of genomic imprinting in biology and disease: an expanding view. Nat Rev Genet 2014; 15:517-30; PMID:24958438; http://dx.doi.org/10.1038/nrg3766
2. Buiting K. Prader-Willi syndrome and Angelman syn- drome. Am J Med Genet 2010; 154C:365-76; http:// dx.doi.org/10.1002/ajmg.c.30273
3. Kent L, Bowdin S, Kirby GA, Cooper WN, Maher ER. Beckwith Weidemann syndrome: A behavioral pheno-type-genotype study. Am J Med Genet B: 840 Neuropsychiatric Genet 2008; 147B:1295-7; http://dx. doi.org/10.1002/ajmg.b.30729
4. Cassidy SB, Dykens E, Williams CA. Prader-Willi and Angelman syndromes: Sister imprinted disorders. Am J Med Genet 2000; 97:136-46; PMID:11180221; http://dx.doi.org/10.1002/1096-8628(200022)97:2%3c136::AID-AJMG5%3e3.0.CO;2-V
5. Pun FW, Zhao C, Lo WS, Ng SK, Tsang SY, Nim-gaonkar V, Chung WS, Ungvari GS, Xue H. Imprint- ing in the schizophrenia candidate gene GABRB2 encoding GABAA receptor b-2 subunit. Mol Psychiatry 2011; 16:557-68; PMID:20404824; http://dx.doi.org/10.1038/mp.2010.47
6. Davies W, Isles A, Smith R, Karunadasa D, Burrmann D, Humby T, Ojarikre O, Biggin C, Skuse D, Bur-goyne P, et al. Xlr3b is a new imprinted candidate for X-linked parent-of-origin effects on cognitive function in mice. Nat Genet 2005; 37:625-9; PMID:15908950; http://dx.doi.org/10.1038/ng1577
7. Mikaelsson MA, Constancia M, Dent CL, Wilkinson LS, Humby T. Placental programming of anxiety in adulthood revealed by Igf2-null models. Nat Commun 2013; 4:2311; PMID:23921428; http://dx.doi.org/10.1038/ncomms3311
8. Champagne FA, Curley JP, Swaney WT, Hasen NS, Keverne EB. Paternal influence on female behavior: The role of Peg3 in exploration, olfaction, and neuroendocrine regulation of maternal behavior of female mice. Behav Neurosci 2009; 123:469-80; PMID:19485553; http://dx.doi.org/10.1037/ a0015060
9. Maccani MA, Marsit CJ. Epigenetics in the Placenta. Am J Reprod Immunol 2009; 62:78-89; PMID:19614624; http://dx.doi.org/10.1111/j.1600- 0897.2009.00716.x
10. Novakovic B, Saffery R. The ever growing complexity of placental epigenetics - Role in adverse pregnancy outcomes and fetal programming. Placenta 2012; 33:959-70; PMID:23102655; http://dx.doi.org/10.1016/j.placenta.2012.10.003
11. Gutierrez-Marcos JF, Constancia M, Burton GJ. Maternal to offspring resource allocation in plants and mammals. Placenta 2012; 33, Supplement 2:e3-e10; PMID:22995735; http://dx.doi.org/10.1016/j. placenta.2012.08.006
12. Frost J, Moore G. The importance of imprinting in the human placenta. PLoS Genet 2010; 6:e1001015; PMID:20617174; http://dx.doi.org/10.1371/journal. pgen.1001015
13. Keverne EB. Genomic imprinting, action, and interaction of maternal and fetal genomes. Proc Natl Acad Sci USA2014;112(22):6834-40; PMID:25404322.
14. Diplas AI, Lambertini L, Lee M-J, Sperling R, Lee YL, Wetmur JG, Chen J. Differential expression of imprinted genes in normal and IUGR human pla- centas. Epigenetics 2009; 4:235-40; PMID:19483473; http://dx.doi.org/10.4161/epi.9019
15. Marsit CJ, Lambertini L, Maccani MA, Koestler DC, Houseman EA, Padbury JF, Lester BM, Chen J. Placenta-imprinted gene expression association of infant neurobehavior. J Pediatr 2012; 160:854-60.e2;PMID:22153677; http://dx.doi.org/10.1016/j. jpeds.2011.10.028
16. Lester BM, Tronick EZ. History and description of the neonatal intensive care unit network neurobehavioral scale. Pediatrics 2004; 113:634-40; PMID:14993523
17. Lester BM, Tronick EZ, in collaboration with T. Berry Brazelton M. The neonatal intensive care unit network neurobehavioral scale procedures. Pediatrics 2004; 113:641-67; PMID:14993524
18. Liu J, Bann C, Lester B, Tronick E, Das A, Lagasse L, Bauer C, Shankaran S, Bada H. Neonatal neurobehavior predicts medical and behavioral outcome. Pediatrics 2010; 125:e90-e8; PMID:19969621; http://dx.doi. org/10.1542/peds.2009-0204
19. Sucharew H, Khoury JC, Xu Y, Succop P, Yolton K. NICU network neurobehavioral scale profiles predict developmental outcomes in a low-risk sample. Paediatr Perinatal Epidemiol 2012; 26:344-52; PMID:22686386; http://dx.doi.org/10.1111/j.1365- 3016.2012.01288.x
20. Stephens BE, Liu J, Lester B, Lagasse L, Shankaran S, Bada H, Bauer C, Das A, Higgins R. Neurobehavioral assessment predicts motor outcome in preterm infants. J Pediatr 2010; 156:366-71; PMID:19880137; http:// dx.doi.org/10.1016/j.jpeds.2009.09.042
21. El-Dib M, Massaro AN, Glass P, Aly H. Neurodevelopmental assessment of the newborn: An opportunity for prediction of outcome. Brain Dev 2011; 33:95-105; PMID:20494536; http://dx.doi.org/10.1016/j. braindev.2010.04.004
22. Lesseur C, Armstrong DA, Murphy MA, Appleton AA, Koestler DC, Paquette AG, Lester BM, Marsit CJ. Sex-specific associations between placental leptin promoter DNA methylation and infant neurobehavior. Psycho- neuroendocrinology 2014; 40:1-9; PMID:24485470; http://dx.doi.org/10.1016/j.psyneuen.2013.10.012
23. Tycko B, Morison IM. Physiological functions of imprinted genes. J Cell Physiol 2002; 192:245-58; PMID:12124770; http://dx.doi.org/10.1002/ jcp.10129
24. Morison IM, Ramsay JP, Spencer HG. A census of mammalian imprinting. Trends Genet 2005; 21:457-65; PMID:15990197; http://dx.doi.org/10.1016/j. tig.2005.06.008
25. Kelsey G. Epigenetics and the brain: transcriptome sequencing reveals new depths to genomic imprinting. Bioessays 2011; 33:362-7; PMID:21425303; http://dx. doi.org/10.1002/bies.201100004
26. Diplas AI, Lambertini L, Lee MJ, Sperling R, Lee YL, Wetmur J, Chen J. Differential expression of imprinted genes in normal and IUGR human placentas. Epigenetics 2009; 4:235-40; PMID:19483473; http://dx. doi.org/10.4161/epi.9019
27. Lambertini L, Marsit CJ, Sharma P, Maccani M, Ma Y, Hu J, Chen J. Imprinted gene expression in fetal growth and development. Placenta 2012; 33:480-6; PMID:22465419; http://dx.doi.org/10.1016/j. placenta.2012.03.001
28. Bagner DM, Sheinkopf SJ, Miller-Loncar C, LaGasse LL, Lester BM, Liu J, Bauer CR, Shankaran S, Bada H, Das A. The effect of parenting stress on child behavior problems in high-risk children with prenatal drug expo- sure. Child Psychiatry Human Dev 2009; 40:73-84; PMID:18626768; http://dx.doi.org/10.1007/s10578- 008-0109-6
29. Liu J, Bann C, Lester B, Tronick E, Das A, Lagasse L, Bauer C, Shankaran S, Bada H. Neonatal neurobehavior predicts medical and behavioral outcome. Pediatrics 2010; 125:e90-8; PMID:19969621; http://dx.doi.org/10.1542/peds.2009-0204
30. Liaw A, Wiener M. Classification and Regression by randomForest. R News 2002; 2:18-22
31. Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, Dunaway DL, Fell HP, Ferree S, George RD, Grogan T, et al. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 2008; 26:317-25; PMID:18278033; http://dx.doi. org/10.1038/nbt1385
32. Yamasaki K, Hayashida S, Miura K, Masuzaki H, Ishimaru T, Niikawa N, Kishino T. The Novel Gene, g2-COP (COPG2), in the 7q32 Imprinted Domain Escapes Genomic Imprinting. Genomics 2000; 68:330-5; PMID:10995575; http://dx.doi.org/10.1006/geno.2000.6265
33. Bentley L, Nakabayashi K, Monk D, Beechey C, Peters J, Birjandi Z, Khayat FE, Patel M, Preece MA, Stanier P, et al. The imprinted region on human chromosome 7q32 extends to the carboxypeptidase A gene cluster: an imprinted candidate for Silver-Russell syndrome. J Med Genet 2003; 40:249-56; PMID:12676894; http://dx.doi.org/10.1136/jmg.40.4.249
34. Kotzot D, Balmer D, Baumer A, Chrzanowska K, Hamel BC, Ilyina H, Krajewska-Walasek M, Lurie IW, Otten BJ, Schoenle E, et al. Maternal uniparental dis- omy 7-review and further delineation of the phenotype. Eur J Pediatr 2000; 159:247-56; PMID:10789928; http://dx.doi.org/10.1007/s004310050064
35. Neumann LC, Markaki Y, Mladenov E, Hoffmann D, Buiting K, Horsthemke B. The imprinted NPAP1/C15orf2 gene in the Prader-Willi syndrome region enc- odes a nuclear pore complex associated protein. Hum Mol Genet 2012; 21:4038-48; PMID:22694955; http://dx.doi.org/10.1093/hmg/dds228
36. Wawrzik M, Unmehopa U, Swaab D, van de Nes J, Buiting K, Horsthemke B. The C15orf2 gene in the Prader-Willi syndrome region is subject to genomic imprinting and positive selection. Neurogenetics 2010; 11:153-61; PMID:20020165; http://dx.doi.org/10.1007/s10048-009-0231-z
37. D’Angelo Maximiliano A, Gomez-Cavazos JS, Mei A, Lackner Daniel H, Hetzer Martin W. A change in nuclear pore complex composition regulates cell differ- entiation. Dev Cell 2012; 22:446-58; PMID:22264802; http://dx.doi.org/10.1016/j. devcel.2011.11.021
38. Lupu F, Alves A, Anderson K, Doye V, Lacy E. Nuclear pore composition regulates neural stem/progenitor cell differentiation in the mouse embryo. Dev Cell 2008; 14:831-42; PMID:18539113; http://dx.doi.org/10.1016/j.devcel.2008.03.011
39. Grabrucker AM, Schmeisser MJ, Schoen M, Boeckers TM. Postsynaptic ProSAP/Shank scaffolds in the cross-hair of synaptopathies. Trends Cell Biol 2011; 21:594-603; PMID:21840719; http://dx.doi.org/10.1016/j. tcb.2011.07.003
40. Du Y, Weed SA, Xiong W-C, Marshall TD, Parsons JT. Identification of a novel cortactin sh3 domain-binding protein and its localization to growth cones of cultured neurons. Mol Cell Biol 1998; 18:5838-51; PMID:9742101
41. Schmeisser MJ, Ey E, Wegener S, Bockmann J, Stem- pel AV, Kuebler A, Janssen A-L, Udvardi PT, Shiban E, Spilker C, et al. Autistic-like behaviours and hyper- activity in mice lacking ProSAP1/Shank2. Nature 2012; 486:256-60; PMID:22699619
42. Berkel S, Marshall CR, Weiss B, Howe J, Roeth R, Moog U, Endris V, Roberts W, Szatmari P, Pinto D, et al. Mutations in the SHANK2 synaptic scaffolding gene in autism spectrum disorder and mental retarda- tion. Nat Genet 2010; 42:489-91; PMID:20473310; http://dx.doi.org/10.1038/ng.589
43. Boeckers TM, Bockmann J, Kreutz MR, Gundelfinger ED. ProSAP/Shank proteins - a family of higher order organizing molecules of the postsynaptic density with an emerging role in human neurological disease. J Neu- rochem 2002; 81:903-10; PMID:12065602; http://dx. doi.org/10.1046/j.1471-4159.2002.00931.x
44. Fenton T, Nasser R, Eliasziw M, Kim J, Bilan D, Sauve R. Validating the weight gain of preterm infants between the reference growth curve of the fetus and the term infant. BMC Pediatr 2013; 13:92; PMID:23758808; http://dx.doi.org/10.1186/1471- 2431-13-92
45. Tronick EZ, Olson K, Rosenberg R, Bohne L, Lu J, Lester BM. Normative neurobehavioral performance of healthy infants on the neonatal intensive care unit net- work neurobehavioral scale. Pediatrics 2004; 113:676-8; PMID:14993526
46. Charrad M, Ghazzali N, Boiteau V, Niknafs A. NbClust: an r package for determining the relevant number of clusters in a data set. J Statistical Software 2014; 61