Quantitative and functional interrogation of parent-of-origin allelic expression biases in the brain

eLife

Volumn 4, Issue JULY 2015, 2015, Pages 41-

  Perez, Julio D ^a   Rubinstein, Nimrod D ^a   Fernandez, Daniel E ^b   Santoro, Stephen W ^c   Needleman, Leigh A ^a   Ho Shing, Olivia ^a   Choi, John J ^a   Zirlinger, Mariela ^d   Chen, Shau Kwaun ^e   Liu, Jun S ^b   Dulac, Catherine ^a  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c UNIVERSITY OF WYOMING   (United States)

^d Cell Press   (United States)

^e NATIONAL CHENGCHI UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BCL X; TRANSCRIPTOME;

ANIMAL TISSUE; ARTICLE; BAYESIAN INFERENCE; BAYESIAN REGRESSION ALLELIC IMBALANCE MODEL; BRAIN; CEREBELLUM; CONTROLLED STUDY; EPIGENETICS; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE DOSAGE; GENE EXPRESSION; GENE LOCATION; GENETIC ANALYSIS; GENOME IMPRINTING; GENOTYPE; GIIBBS SAMPLING; IMAGE ANALYSIS; IMMUNOFLUORESCENCE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PYROSEQUENCING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICAL MODEL; ALLELE; ANIMAL; BIOSTATISTICS; C57BL MOUSE; DNA SEQUENCE; GENE EXPRESSION PROFILING; MOLECULAR GENETICS; PHYSIOLOGY;

MAMMALIA;

ALLELES; ANIMALS; BIOSTATISTICS; CEREBELLUM; GENE EXPRESSION PROFILING; GENOMIC IMPRINTING; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA;

EID: 84938327301     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.07860     Document Type: Article

References (110)

1. Albrecht U, Sutcliffe JS, Cattanach BM, Beechey CV, Armstrong D, Eichele G, Beaudet AL. 1997. Imprinted expression of the murine Angelman syndrome gene, Ube3a, in hippocampal and Purkinje neurons. Nature Genetics 17:75-78. doi: 10.1038/ng0997-75.
2. Amaral DG, Schumann CM, Nordahl CW. 2008. Neuroanatomy of autism. Trends in Neurosciences 31:137-145. doi: 10.1016/j.tins.2007.12.005.
3. Arnaud P, Monk D, Hitchins M, Gordon E, Dean W, Beechey CV, Peters J, Craigen W, Preece M, Stanier P, Moore GE, Kelsey G. 2003. Conserved methylation imprints in the human and mouse GRB10 genes with divergent allelic expression suggests differential reading of the same mark. Human Molecular Genetics 12:1005-1019. doi: 10.1093/hmg/ddg110.
4. Babak T, Deveale B, Armour C, Raymond C, Cleary MA, van der Kooy D, Johnson JM, Lim LP. 2008. Global survey of genomic imprinting by transcriptome sequencing. Current Biology 18:1735-1741. doi: 10.1016/j.cub.2008.09.044.
5. Barel O, Shalev SA, Ofir R, Cohen A, Zlotogora J, Shorer Z, Mazor G, Finer G, Khateeb S, Zilberberg N, Birk OS. 2008. Maternally inherited birk barel mental retardation dysmorphism syndrome caused by a mutation in the genomically imprinted potassium channel KCNK9. American Journal of Human Genetics 83:193-199. doi: 10.1016/j.ajhg.2008.07.010.
6. Bartolomei MS, Ferguson-Smith AC. 2011. Mammalian genomic imprinting. Cold Spring Harbor Perspectives in Biology 3:1-17. doi: 10.1101/cshperspect.a002592.
7. Boise LH, Gonzalez-Garcıa M, Postema CE, Ding L, Lindsten T, Turka LA, Mao X, Nunez G, Thompson CB. 1993. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74:597-608. doi: 10.1016/0092-8674(93)90508-N.
8. Bradley RK, Merkin J, Lambert NJ, Burge CB. 2012. Alternative splicing of RNA triplets is often regulated and accelerates proteome evolution. PLOS Biology 10:e1001229. doi: 10.1371/journal.pbio.1001229.
9. Buss RR, Sun W, Oppenheim RW. 2006. Adaptive roles of programmed cell death during nervous system development. Annual Review of Neuroscience 29:1-35. doi: 10.1146/annurev.neuro.29.051605.112800.
10. Calaway J, Domınguez J. 2012. Intronic parent-of-origin dependent differential methylation at the Actn1 gene is conserved in rodents but is not associated with imprinted expression. PLOS ONE 7:e48936. doi: 10.1371/journal.pone.0048936.
11. Charalambous M, Cowley M, Geoghegan F, Smith FM, Radford EJ, Marlow BP, Graham CF, Hurst LD, Ward A. 2010. Maternally-inherited Grb10 reduces placental size and efficiency. Developmental Biology 337:1-8. doi: 10.1016/j.ydbio.2009.10.011.
12. Charalambous M, Smith FM, Bennett WR, Crew TE, Mackenzie F, Ward A. 2003. Disruption of the imprinted Grb10 gene leads to disproportionate overgrowth by an Igf2-independent mechanism. Proceedings of the National Academy of Sciences of USA 100:8292-8297. doi: 10.1073/pnas.1532175100.
13. Cheloufi S, Dos Santos CO, Chong MM, Hannon GJ. 2010. A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 465:584-589. doi: 10.1038/nature09092.
14. Chen WV, Maniatis T. 2013. Clustered protocadherins. Development 140:3297-3302. doi: 10.1242/dev.090621.
15. Chipman H, Hamada M, Wu C. 1997. A Bayesian variable-selection approach for analyzing designed experiments with complex aliasing. Technometrics 39:372-381. doi: 10.1080/00401706.1997.10485156.
16. Choi JD, Underkoffler LA, Wood AJ, Collins JN, Williams PT, Golden JA, Schuster EF, Loomes KM, Oakey RJ. 2005. A novel variant of Inpp5f is imprinted in brain, and its expression is correlated with differential methylation of an internal CpG island. Molecular and Cellular Biology 25:5514-5522. doi: 10.1128/MCB.25.13.5514-5522.2005.
17. Cleaton MA, Edwards CA, Ferguson-Smith AC. 2014. Phenotypic outcomes of imprinted gene models in mice: elucidation of pre- and postnatal functions of imprinted genes. Annual Review of Genomics and Human Genetics 15:93-126. doi: 10.1146/annurev-genom-091212-153441.
18. Cohen O, Rubinstein ND, Stern A, Gophna U, Pupko T. 2008. A likelihood framework to analyse phyletic patterns. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363:3903-3911. doi: 10.1098/rstb.2008.0177.
19. Cowley M, Wood AJ, Böhm S, Schulz R, Oakey RJ. 2012. Epigenetic control of alternative mRNA processing at the imprinted Herc3/Nap1l5 locus. Nucleic Acids Research 40:8917-8926. doi: 10.1093/nar/gks654.
20. Dao D, Frank D, Qian N, O’Keefe D, Vosatka RJ, Walsh CP, Tycko B. 1998. IMPT1, an imprinted gene similar to polyspecific transporter and multi-drug resistance genes. Human Molecular Genetics 7:597-608. doi: 10.1093/hmg/7.4.597.
21. Davies W, Isles A, Smith R, Karunadasa D, Burrmann D, Humby T, Ojarikre O, Biggin C, Skuse D, Burgoyne P, Wilkinson L. 2005. Xlr3b is a new imprinted candidate for X-linked parent-of-origin effects on cognitive function in mice. Nature Genetics 37:625-629. doi: 10.1038/ng1577.
22. DeVeale B, van der Kooy D, Babak T. 2012. Critical evaluation of imprinted gene expression by RNA-seq: a new perspective. PLOS Genetics 8:e1002600. doi: 10.1371/journal.pgen.1002600.
23. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 29:15-21. doi: 10.1093/bioinformatics/bts635.
24. Dolen G, Osterweil E, Rao BS, Smith GB, Auerbach BD, Chattarji S, Bear MF. 2007. Correction of fragile X syndrome in mice. Neuron 56:955-962. doi: 10.1016/j.neuron.2007.12.001.
25. Dulac C. 2010. Brain function and chromatin plasticity. Nature 465:728-735. doi: 10.1038/nature09231.
26. Engstrom PG, Steijger T, Sipos B, Grant GR, Kahles A, Ratsch G, Goldman N, Hubbard TJ, Harrow J, Guigo R, Bertone P, RGASP Consortium. 2013. Systematic evaluation of spliced alignment programs for RNA-seq data. Nature Methods 10:1185-1191. doi: 10.1038/nmeth.2722.
27. Ferron SR, Charalambous M, Radford E, McEwen K, Wildner H, Hind E, Morante-Redolat JM, Laborda J, Guillemot F, Bauer SR, Farinas I, Ferguson-Smith AC. 2012. Postnatal loss of Dlk1 imprinting in stem cells and niche astrocytes regulates neurogenesis. Nature 475:381-385. doi: 10.1038/nature10229.
28. Filson AJ, Louvi A, Efstratiadis A, Robertson EJ. 1993. Rescue of the T-associated maternal effect in mice carrying null mutations in Igf-2 and Igf2r, two reciprocally imprinted genes. Development 118:731-736.
29. Fishell G, Heintz N. 2013. The neuron identity problem: form meets function. Neuron 80:602-612. doi: 10.1016/j.neuron.2013.10.035.
30. Flicek P, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, Gil L, Giron CG, Gordon L, Hourlier T, Hunt S, Johnson N, Juettemann T, Kahari AK, Keenan S, Kulesha E, Martin FJ, Maurel T, McLaren WM, Murphy DN, Nag R, Overduin B, Pignatelli M, Pritchard B, Pritchard E, Riat HS, Ruffier M, Sheppard D, Taylor K, Thormann A, Trevanion SJ, Vullo A, Wilder SP, Wilson M, Zadissa A, Aken BL, Birney E, Cunningham F, Harrow J, Herrero J, Hubbard TJ, Kinsella R, Muffato M, Parker A, Spudich G, Yates A, Zerbino DR, Searle SM. 2014. Ensembl 2014. Nucleic Acids Research 42:D749-D755. doi: 10.1093/nar/gkt1196.
31. Garfield AS, Cowley M, Smith FM, Moorwood K, Stewart-Cox JE, Gilroy K, Baker S, Xia J, Dalley JW, Hurst LD, Wilkinson LS, Isles AR, Ward A. 2011. Distinct physiological and behavioural functions for parental alleles of imprinted Grb10. Nature 469:534-538. doi: 10.1038/nature09651.
32. Gelman A. 2008. Scaling regression inputs by dividing by two standard deviations. Statistics in Medicine 27: 2865-2873. doi: 10.1002/sim.3107.
33. Gelman A, Carlin J, Stern H, Dunson D. 2013. Bayesian data analysis. Boca Raton, FL: Chapman and Hall/CRC.
34. Gregg C. 2014. Known unknowns for allele-specific expression and genomic imprinting effects. F1000Prime Reports 6:75. doi: 10.12703/P6-75.
35. Gregg C, Zhang J, Weissbourd B, Luo S, Schroth GP, Haig D, Dulac C. 2010. High-resolution analysis of parent-oforigin allelic expression in the mouse brain. Science 329:643-648. doi: 10.1126/science.1190830.
36. Guo JU, Su Y, Zhong C, Ming GL, Song H. 2011. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145:423-434. doi: 10.1016/j.cell.2011.03.022.
37. Hagiwara Y, Hirai M, Nishiyama K, Kanazawa I, Ueda T, Sakaki Y, Ito T. 1997. Screening for imprinted genes by allelic message display: Identification of a paternally expressed gene Impact on mouse chromosome 18. Proceedings of the National Academy of Sciences of USA 94:9249-9254. doi: 10.1073/pnas.94.17.9249.
38. Hashimoto M, Hibi M. 2012. Development and evolution of cerebellar neural circuits. Development, Growth & Differentiation 54:373-389. doi: 10.1111/j.1440-169X.2012.01348.x.
39. Hatada I, Morita S, Obata Y, Sotomaru Y, Shimoda M, Kono T. 2001. Identification of a new imprinted gene, Rian, on mouse chromosome 12 by fluorescent differential display screening. Journal of Biochemistry 130:187-190. doi: 10.1093/oxfordjournals.jbchem.a002971.
40. Hu JF, Balaguru KA, Ivaturi RD, Oruganti H, Li T, Nguyen BT, Vu TH, Hoffman AR. 1999. Lack of reciprocal genomic imprinting of sense and antisense RNA of mouse insulin-like growth factor II receptor in the central nervous system. Biochemical and Biophysical Research Communications 257:604-608. doi: 10.1006/bbrc.1999.0380.
41. Huang HS, Yoon BJ, Brooks S, Bakal R, Berrios J, Larsen RS, Wallace ML, Han JE, Chung EH, Zylka MJ, Philpot BD. 2014. Snx14 regulates neuronal excitability, promotes synaptic transmission, and is imprinted in the brain of mice. PLOS ONE 9:e98383. doi: 10.1371/journal.pone.0098383.
42. Isles AR, Davies W, Wilkinson LS. 2006. Genomic imprinting and the social brain. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 361:2229-2237. doi: 10.1098/rstb.2006.1942.
43. Jacobs AT, Marnett LJ. 2009. HSF1-mediated BAG3 expression attenuates apoptosis in 4-hydroxynonenal-treated colon cancer cells via stabilization of anti-apoptotic Bcl-2 proteins. The Journal of Biological Chemistry 284: 9176-9183. doi: 10.1074/jbc.M808656200.
44. Jiang H, Wong WH. 2009. Statistical inferences for isoform expression in RNA-Seq. Bioinformatics 25:1026-1032. doi: 10.1093/bioinformatics/btp113.
45. Kabayama H, Tokushige N, Takeuchi M, Mikoshiba K. 2008. Syntaxin 6 regulates nerve growth factor-dependent neurite outgrowth. Neuroscience Letters 436:340-344. doi: 10.1016/j.neulet.2008.03.061.
46. Kaneko-Ishino T, Kuroiwa Y, Miyoshi N, Kohda T, Suzuki R, Yokoyama M, Viville S, Barton SC, Ishino F, Surani MA. 1995. Peg1/Mest imprinted gene on chromosome 6 identified by cDNA subtraction hybridization. Nature Genetics 11:52-59. doi: 10.1038/ng0995-52.
47. Karolchik D, Barber GP, Casper J, Clawson H, Cline MS, Diekhans M, Dreszer TR, Fujita PA, Guruvadoo L, Haeussler M, Harte RA, Heitner S, Hinrichs AS, Learned K, Lee BT, Li CH, Raney BJ, Rhead B, Rosenbloom KR, Sloan CA, Speir ML, Zweig AS, Haussler D, Kuhn RM, Kent WJ. 2014. The UCSC genome browser database: 2014 update. Nucleic Acids Research 42:D764-D770. doi: 10.1093/nar/gkt1168.
48. Kasai S, Chuma S, Motoyama N, Nakatsuji N. 2003. Haploinsufficiency of Bcl-x leads to male-specific defects in fetal germ cells: differential regulation of germ cell apoptosis between the sexes. Developmental Biology 264: 202-216. doi: 10.1016/S0012-1606(03)00400-7.
49. Kelsey G, Bartolomei MS. 2012. Imprinted genes and the number is? PLoS Genetics 8:e1002601. doi: 10.1371/journal.pgen.1002601.
50. Keverne EB. 2012. Importance of the matriline for genomic imprinting, brain development and behaviour. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 368:20110327. doi: 10.1098/rstb.2011.0327.
51. Khatib H. 2007. Is it genomic imprinting or preferential expression? Bioessays 29:1022-1028. doi: 10.1002/bies.20637.
52. Krajewska M, Mai JK, Zapata JM, Ashwell KWS, Schendel SL, Reed JC, Krajewski S. 2002. Dynamics of expression of apoptosis-regulatory proteins Bid, Bcl-2, Bcl-X, Bax and Bak during development of murine nervous system. Cell Death & Disease 9:145-157. doi: 10.1038/sj.cdd.4400934.
53. Kuan CY, Roth KA, Flavell RA, Rakic P. 2000. Mechanisms of programmed cell death in the developing brain. Trends in Neurosciences 23:291-297. doi: 10.1016/S0166-2236(00)01581-2.
54. Kulinski TM, Barlow DP, Hudson QJ. 2013. Imprinted silencing is extended over broad chromosomal domains in mouse extra-embryonic lineages. Current Opinion in Cell Biology 25:297-304. doi: 10.1016/j.ceb.2013.02.012.
55. Lefebvre L, Viville S, Barton SC, Ishino F, Keverne EB, Surani MA. 1998. Abnormal maternal behaviour and growth retardation associated with loss of the imprinted gene Mest. Nature Genetics 20:163-169. doi: 10.1038/2464.
56. Levitt P, Barbe MF, Eagleson KL. 1997. Patterning and specification of the cerebral cortex. Annual Review of Neuroscience 20:1-24. doi: 10.1146/annurev.neuro.20.1.1.
57. Lewis A, Mitsuya K, Umlauf D, Smith P, Dean W, Walter J, Higgins M, Feil R, Reik W. 2004. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation. Nature Genetics 36:1291-1295. doi: 10.1038/ng1468.
58. Li L, Keverne EB, Aparicio SA, Ishino F, Barton SC, Surani MA. 1999. Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science 284:330-333. doi: 10.1126/science.284.5412.330.
59. Lindley D, Smith A. 1972. Bayes estimates for the linear model. Journal of the Royal Statistical Society 34:1-41.
60. Ludwig T, Eggenschwiler J, Fisher P, D’Ercole AJ, Davenport ML, Efstratiadis A. 1996. Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Developmental Biology 177:517-535. doi: 10.1006/dbio.1996.0182.
61. McCole RB, Oakey RJ. 2008. Unwitting hosts fall victimto imprinting. Epigenetics 3:258-260. doi: 10.4161/epi.3.5.7052.
62. Menheniott TR, Woodfine K, Schulz R, Wood AJ, Monk D, Giraud AS, Baldwin HS, Moore GE, Oakey RJ. 2008. Genomic imprinting of Dopa decarboxylase in heart and reciprocal allelic expression with neighboring Grb10. Molecular and Cellular Biology 28:386-396. doi: 10.1128/MCB.00862-07.
63. Mituyama T, Yamada K, Hattori E, Okida H, Ono Y, Terai G, Yoshizawa A, Komori T, Asai K. 2009. The functional RNA database 3.0: databases to support mining and annotation of functional RNAs. Nucleic Acids Research 37: D89-D92. doi: 10.1093/nar/gkn805.
64. Morison IM, Ramsay JP, Spencer HG. 2005. A census of mammalian imprinting. Trends in Genetics 21:457-465. doi: 10.1016/j.tig.2005.06.008.
65. Ono R, Shiura H, Aburatani H, Kohda T, Kaneko-Ishino T, Ishino F. 2003. Identification of a large novel imprinted gene cluster on mouse proximal chromosome 6. Genome Research 13:1696-1705. doi: 10.1101/gr.906803.
66. Owuor K, Harel NY, Englot DJ, Hisama F, Blumenfeld H, Strittmatter SM. 2009. LGI1-associated epilepsy through altered ADAM23-dependent neuronal morphology. Molecular and Cellular Neurosciences 42:448-457. doi: 10.1016/j.mcn.2009.09.008.
67. Paxinos G, Franklin K. 2007. The mouse brain in stereotaxic coordinates, third edition: Elsevier, New York. 9780123694607.
68. Peters J. 2014. The role of genomic imprinting in biology and disease: an expanding view. Nature Reviews. Genetics 15:517-530. doi: 10.1038/nrg3766.
69. Peters J, Williamson CM. 2007. Control of imprinting at the Gnas cluster. Epigenetics 2:207-213. doi: 10.4161/epi.2.4.5380.
70. Prickett AR, Oakey RJ. 2012. A survey of tissue-specific genomic imprinting in mammals. Molecular Genetics and Genomics 287:621-630. doi: 10.1007/s00438-012-0708-6.
71. Proudhon C, Duffie R, Ajjan S, Cowley M, Iranzo J, Carbajosa G, Saadeh H, Holland ML, Oakey RJ, Rakyan VK, Schulz R, Bourc’his D. 2012. Protection against de novo methylation is Instrumental in maintaining parent-oforigin methylation inherited from the gametes. Molecular Cell 47:909-920. doi: 10.1016/j.molcel.2012.07.010.
72. Quenneville S, Verde G, Corsinotti A, Kapopoulou A, Jakobsson J, Offner S, Baglivo I, Pedone PV, Grimaldi G, Riccio A, Trono D. 2011. In Embryonic stem cells, ZFP57/KAP1 Recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions. Molecular Cell 44:361-372. doi: 10.1016/j.molcel.2011.08.032.
73. Ramocki MB, Zoghbi HY. 2008. Failure of neuronal homeostasis results in common neuropsychiatric phenotypes. Nature 455:912-918. doi: 10.1038/nature07457.
74. Reik W, Walter J. 2001. Genomic imprinting: Parental influence on the genome. Nature Reviews. Genetics 2:21-32. doi: 10.1038/35047554.
75. Roberts A, Pachter L. 2013. Streaming fragment assignment for real-time analysis of sequencing experiments. Nature Methods 10:71-73. doi: 10.1038/nmeth.2251.
76. Roma-Mateo C, Sanz P, Gentry M. 2012. Deciphering the role of malin in the lafora progressive myoclonus epilepsy. IUBMB Life 64:801-808. doi: 10.1002/iub.1072.
77. Rosati A, Graziano V, De Laurenzi V, Pascale M, Turco MC. 2011. BAG3: a multifaceted protein that regulates major cell pathways. Cell Death & Disease 2:e141-e146. doi: 10.1038/cddis.2011.24.
78. Roth K, D’Sa C. 2001. Apoptosis and brain development. Mental Retardation and Developmental Disabilities 7: 261-266. doi: 10.1002/mrdd.1036.
79. Rougeulle C, Glatt H, Lalande M. 1997. The Angelman syndrome candidate gene, UBE3AIE6-AP, is imprinted in brain. Nature Genetics 17:14-15.
80. Royo JL, Hidalgo M, Ruiz A. 2007. Pyrosequencing protocol using a universal biotinylated primer for mutation detection and SNP genotyping. Nature Protocols 2:1734-1739. doi: 10.1038/nprot.2007.244.
81. Rozowsky J, Abyzov A, Wang J, Alves P, Raha D, Harmanci A, Leng J, Bjornson R, Kong Y, Kitabayashi N, Bhardwaj N, Rubin M, Snyder M, Gerstein M. 2011. AlleleSeq: analysis of allele-specific expression and binding in a network framework. Molecular Systems Biology 7:522. doi: 10.1038/msb.2011.54.
82. Rucker EB, Dierisseau P, Wagner KU, Garrett L, Wynshaw-Boris A, Flaws JA, Hennighausen L. 2000. Bcl-x and Bax regulate mouse primordial germ cell survival and apoptosis during embryogenesis. Molecular Endocrinology 14: 1038-1052. doi: 10.1210/mend.14.7.0465.
83. Ruf N, Dunzinger U, Brinckmann A, Haaf T, Nurnberg P, Zechner U. 2006. Expression profiling of uniparental mouse embryos is inefficient in identifying novel imprinted genes. Genomics 87:509-519. doi: 10.1016/j.ygeno.2005.12.007.
84. Sato M, Stryker MP. 2010. Genomic imprinting of experience-dependent cortical plasticity by the ubiquitin ligase gene Ube3a. Proceedings of the National Academy of Sciences of USA 107:5611-5616. doi: 10.1073/pnas.1001281107.
85. Schmidt-Edelkraut U, Daniel G, Hoffmann A, Spengler D. 2014. Zac1 regulates cell cycle arrest in neuronal progenitors via Tcf4. Molecular and Cellular Biology 34:1020-1030. doi: 10.1128/MCB.01195-13.
86. Shimogori T, Lee DA, Miranda-Angulo A, Yang Y, Wang H, Jiang L, Yoshida AC, Kataoka A, Mashiko H, Avetisyan M, Qi L, Qian J, Blackshaw S. 2010. A genomic atlas of mouse hypothalamic development. Nature Neuroscience 13: 767-775. doi: 10.1038/nn.2545.
87. Sillitoe RV, Joyner AL. 2007. Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Annual Review of Cell and Developmental Biology 23:549-577. doi: 10.1146/annurev.cellbio.23.090506.123237.
88. Steijger T, Abril JF, Engstrom PG, Kokocinski F, Akerman M, Alioto T, Ambrosini G, Antonarakis SE, Behr J, Bertone P. 2013. Assessment of transcript reconstruction methods for RNA-seq. Nature Methods 10:1177-1184. doi: 10.1038/nmeth.2714.
89. Tierling S, Gasparoni G, Youngson N, Paulsen M. 2009. The Begain gene marks the centromeric boundary of the imprinted region on mouse chromosome 12. Mammalian Genome 20:699-710. doi: 10.1007/s00335-009-9205-6.
90. Tiwari A, Jung JJ, Inamdar SM, Brown CO, Goel A, Choudhury A. 2011. Endothelial cell migration on fibronectin is regulated by syntaxin 6-mediated 5 1 integrin recycling. The Journal of Biological Chemistry 286:36749-36761. doi: 10.1074/jbc.M111.260828.
91. Townley-Tilson WH, Wu Y, Ferguson JE, Patterson C. 2014. The ubiquitin ligase ASB4 promotes trophoblast differentiation through the degradation of ID2. PLOS ONE 9:e89451. doi: 10.1371/journal.pone.0089451.
92. Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L. 2013. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nature Biotechnology 31:46-53. doi: 10.1038/nbt.2450.
93. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, Schu¨ tz G. 1999. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nature Genetics 23:99-103. doi: 10.1038/12703.
94. Tsai PT, Hull C, Chu Y, Greene-Colozzi E, Sadowski AR, Leech JM, Steinberg J, Crawley JN, Regehr WG, Sahin M. 2012. Autistic-like behaviour and cerebellar dysfunction in Purkinje cell Tsc1 mutant mice. Nature 488:647-651. doi: 10.1038/nature11310.
95. Tunster SJ, Jensen AB, John RM. 2013. Imprinted genes in mouse placental development and the regulation of fetal energy stores. Reproduction: The Official Journal of the Society for the Study of Fertility 145:R117-R137. doi: 10.1530/REP-12-0511.
96. Turro E, Astle WJ, Tavare S. 2014. Flexible analysis of RNA-seq data using mixed effects models. Bioinformatics 30: 180-188. doi: 10.1093/bioinformatics/btt624.
97. Turro E, Su SY, Goncalves A, Coin LJ, Richardson S, Lewin A. 2011. Haplotype and isoform specific expression estimation using multi-mapping RNA-seq reads. Genome Biology 12:R13. doi: 10.1186/gb-2011-12-2-r13.
98. Tury A, Mairet-Coello G, DiCicco-Bloom E. 2012. The multiple roles of the cyclin-dependent kinase inhibitory protein p57KIP2 in cerebral cortical neurogenesis. Developmental Neurobiology 72:821-842. doi: 10.1002/dneu.20999.
99. Vijaya Satya R, Zavaljevski N, Reifman J. 2012. A new strategy to reduce allelic bias in RNA-Seq readmapping. Nucleic Acids Research 40:e127. doi: 10.1093/nar/gks425.
100. Wagner GP, Kin K, Lynch VJ. 2012. Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples. Theory in Biosciences 131:281-285. doi: 10.1007/s12064-012-0162-3.
101. Wang H, Elbein SC. 2007. Detection of allelic imbalance in gene expression using pyrosequencing. Methods in Molecular Biology 373:157-176. doi: 10.1385/1-59745-377-3:157.
102. Wang L, Zhang J, Duan J, Gao X, Zhu W, Lu X, Yang L, Zhang J, Li G, Ci W, Li W, Zhou Q, Aluru N, Tang F, He C, Huang X, Liu J. 2014a. Programming and inheritance of parental DNA methylomes in mammals. Cell 157: 979-991. doi: 10.1016/j.cell.2014.04.017.
103. Wang SS, Kloth AD, Badura A. 2014b. The cerebellum, sensitive periods, and autism. Neuron 83:518-532. doi: 10.1016/j.neuron.2014.07.016.
104. Wang X, Sun Q, McGrath SD, Mardis ER, Soloway PD, Clark AG. 2008. Transcriptome-wide identification of novel imprinted genes in neonatal mouse brain. PLOS ONE 3:e3839. doi: 10.1371/journal.pone.0003839.
105. Weinstein LS, Yu S, Ecelbarger CA. 2000. Variable imprinting of the heterotrimeric G protein G(s) alpha-subunit within different segments of the nephron. American Journal of physiology. Renal Physiology 278:F507-F514.
106. Wilkinson LS, Davies W, Isles AR. 2007. Genomic imprinting effects on brain development and function. Nature Reviews. Neuroscience 8:832-843. doi: 10.1038/nrn2235.
107. Wood AJ, Schulz R, Woodfine K, Koltowska K, Beechey CV, Peters J, Bourc’his D, Oakey RJ. 2008. Regulation of alternative polyadenylation by genomic imprinting. Genes & Development 22:1141-1146. doi: 10.1101/gad.473408.
108. Xie W, Barr C, Kim A, Yue F, Lee A. 2012. Base-resolution analyses of sequence and parent-of-origin dependent DNA methylation in the mouse genome. Cell 148:816-831. doi: 10.1016/j.cell.2011.12.035.
109. Yamasaki K, Joh K, Ohta T, Masuzaki H, Ishimaru T, Mukai T, Niikawa N, Ogawa M, Wagstaff J, Kishino T. 2003. Neurons but not glial cells show reciprocal imprinting of sense and antisense transcripts of Ube3a. Human Molecular Genetics 12:837-847. doi: 10.1093/hmg/ddg106.
110. Zou F, Sun W, Crowley JJ, Zhabotynsky V, Sullivan PF, de Villena FP. 2014. A novel statistical approach for jointly analyzing RNA-seq data from F1 reciprocal crosses and inbred lines. Genetics 197:389-399. doi: 10.1534/genetics.113.160119.