Developmental dynamics and disease potential of random monoallelic gene expression

Developmental Cell

Volumn 28, Issue 4, 2014, Pages 366-380

  Gendrel, Anne Valerie ^a,b   Attia, Mikael ^a,b   Chen, Chong Jian ^a,b,c,d   Diabangouaya, Patricia ^a,b   Servant, Nicolas ^a,c,d   Barillot, Emmanuel ^a,c,d   Heard, Edith ^a,b  

^a INSTITUT CURIE   (France)

^b INSTITUT CURIE   (France)

^c INSERM U900   (France)

^d PSL RESEARCH UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELES; ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELL LINE; DNA METHYLATION; EMBRYONIC STEM CELLS; GENE EXPRESSION; GENOTYPE; HUMANS; X CHROMOSOME INACTIVATION;

EID: 84894370544     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.01.016     Document Type: Article

References (48)

1. Allen E., Horvath S., Tong F., Kraft P., Spiteri E., Riggs A.D., Marahrens Y. High concentrations of long interspersed nuclear element sequence distinguish monoallelically expressed genes. Proc. Natl. Acad. Sci. USA 2003, 100:9940-9945.
2. Barlow D.P. Genomic imprinting: a mammalian epigenetic discovery model. Annu. Rev. Genet. 2011, 45:379-403.
3. Bönnemann C.G., Cox G.F., Shapiro F., Wu J.J., Feener C.A., Thompson T.G., Anthony D.C., Eyre D.R., Darras B.T., Kunkel L.M. A mutation in the alpha 3 chain of type IX collagen causes autosomal dominant multiple epiphyseal dysplasia with mild myopathy. Proc. Natl. Acad. Sci. USA 2000, 97:1212-1217.
4. Cedar H., Bergman Y. Choreography of Ig allelic exclusion. Curr. Opin. Immunol. 2008, 20:308-317.
5. Chartier-Harlin M.C., Kachergus J., Roumier C., Mouroux V., Douay X., Lincoln S., Levecque C., Larvor L., Andrieux J., Hulihan M., et al. Alpha-synuclein locus duplication as a cause of familial Parkinson's disease. Lancet 2004, 364:1167-1169.
6. Chaumeil J., Augui S., Chow J.C., Heard E. Combined immunofluorescence, RNA fluorescent insitu hybridization, and DNA fluorescent insitu hybridization to study chromatin changes, transcriptional activity, nuclear organization, and X-chromosome inactivation. Methods Mol. Biol. 2008, 463:297-308.
7. Chess A. Mechanisms and consequences of widespread random monoallelic expression. Nat. Rev. Genet. 2012, 13:421-428.
8. Conti L., Pollard S.M., Gorba T., Reitano E., Toselli M., Biella G., Sun Y., Sanzone S., Ying Q.L., Cattaneo E., Smith A. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 2005, 3:e283.
9. Depreux F.F., Darrow K., Conner D.A., Eavey R.D., Liberman M.C., Seidman C.E., Seidman J.G. Eya4-deficient mice are a model for heritable otitis media. J.Clin. Invest. 2008, 118:651-658.
10. Dixon J.R., Selvaraj S., Yue F., Kim A., Li Y., Shen Y., Hu M., Liu J.S., Ren B. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012, 485:376-380.
11. Ferrón S.R., Charalambous M., Radford E., McEwen K., Wildner H., Hind E., Morante-Redolat J.M., Laborda J., Guillemot F., Bauer S.R., et al. Postnatal loss of Dlk1 imprinting in stem cells and niche astrocytes regulates neurogenesis. Nature 2011, 475:381-385.
12. Gimelbrant A., Hutchinson J.N., Thompson B.R., Chess A. Widespread monoallelic expression on human autosomes. Science 2007, 318:1136-1140.
13. Gritti A., Bonfanti L., Doetsch F., Caille I., Alvarez-Buylla A., Lim D.A., Galli R., Verdugo J.M., Herrera D.G., Vescovi A.L. Multipotent neural stem cells reside into the rostral extension and olfactory bulb of adult rodents. J.Neurosci. 2002, 22:437-445.
14. Guy J., Gan J., Selfridge J., Cobb S., Bird A. Reversal of neurological defects in a mouse model of Rett syndrome. Science 2007, 315:1143-1147.
15. Hitchins M.P., Rapkins R.W., Kwok C.T., Srivastava S., Wong J.J., Khachigian L.M., Polly P., Goldblatt J., Ward R.L. Dominantly inherited constitutional epigenetic silencing of MLH1 in a cancer-affected family is linked to a single nucleotide variant within the 5'UTR. Cancer Cell 2011, 20:200-213.
16. Jeffries A.R., Perfect L.W., Ledderose J., Schalkwyk L.C., Bray N.J., Mill J., Price J. Stochastic choice of allelic expression in human neural stem cells. Stem Cells 2012, 30:1938-1947.
17. Kaghad M., Bonnet H., Yang A., Creancier L., Biscan J.C., Valent A., Minty A., Chalon P., Lelias J.M., Dumont X., et al. Monoallelically expressed gene related to p53 at 1p36, a region frequently deleted in neuroblastoma and other human cancers. Cell 1997, 90:809-819.
18. Kalatzis V., Sahly I., El-Amraoui A., Petit C. Eya1 expression in the developing ear and kidney: towards the understanding of the pathogenesis of Branchio-Oto-Renal (BOR) syndrome. Dev. Dyn. 1998, 213:486-499.
19. Keane T.M., Goodstadt L., Danecek P., White M.A., Wong K., Yalcin B., Heger A., Agam A., Slater G., Goodson M., et al. Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 2011, 477:289-294.
20. Kitsberg D., Selig S., Brandeis M., Simon I., Keshet I., Driscoll D.J., Nicholls R.D., Cedar H. Allele-specific replication timing of imprinted gene regions. Nature 1993, 364:459-463.
21. Li S.M., Valo Z., Wang J., Gao H., Bowers C.W., Singer-Sam J. Transcriptome-wide survey of mouse CNS-derived cells reveals monoallelic expression within novel gene families. PLoS One 2012, 7:e31751.
22. Mikkelsen T.S., Ku M., Jaffe D.B., Issac B., Lieberman E., Giannoukos G., Alvarez P., Brockman W., Kim T.K., Koche R.P., et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560.
23. Ming G.L., Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 2011, 70:687-702.
24. Miyanari Y., Torres-Padilla M.E. Control of ground-state pluripotency by allelic regulation of Nanog. Nature 2012, 483:470-473.
25. Nora E.P., Lajoie B.R., Schulz E.G., Giorgetti L., Okamoto I., Servant N., Piolot T., Van Berkum N.L., Meisig J., Sedat J., et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 2012, 485:381-385.
26. Nutt S.L., Busslinger M. Monoallelic expression of Pax5: a paradigm for the haploinsufficiency of mammalian Pax genes?. Biol. Chem. 1999, 380:601-611.
27. Nutt S.L., Vambrie S., Steinlein P., Kozmik Z., Rolink A., Weith A., Busslinger M. Independent regulation of the two Pax5 alleles during B-cell development. Nat. Genet. 1999, 21:390-395.
28. Ohlsson R. Genetics. Widespread monoallelic expression. Science 2007, 318:1077-1078.
29. Pessia E., Makino T., Bailly-Bechet M., McLysaght A., Marais G.A. Mammalian X chromosome inactivation evolved as a dosage-compensation mechanism for dosage-sensitive genes on the X chromosome. Proc. Natl. Acad. Sci. USA 2012, 109:5346-5351.
30. Rhoades K.L., Singh N., Simon I., Glidden B., Cedar H., Chess A. Allele-specific expression patterns of interleukin-2 and Pax-5 revealed by a sensitive single-cell RT-PCR analysis. Curr. Biol. 2000, 10:789-792.
31. Rovelet-Lecrux A., Hannequin D., Raux G., Le Meur N., Laquerrière A., Vital A., Dumanchin C., Feuillette S., Brice A., Vercelletto M., et al. APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat. Genet. 2006, 38:24-26.
32. Selcen D., Muntoni F., Burton B.K., Pegoraro E., Sewry C., Bite A.V., Engel A.G. Mutation in BAG3 causes severe dominant childhood muscular dystrophy. Ann. Neurol. 2009, 65:83-89.
33. Shykind B.M. Regulation of odorant receptors: one allele at a time. Hum. Mol. Genet. 2005, 14(Spec No 1):R33-R39.
34. Simon I., Tenzen T., Reubinoff B.E., Hillman D., McCarrey J.R., Cedar H. Asynchronous replication of imprinted genes is established in the gametes and maintained during development. Nature 1999, 401:929-932.
35. Singh N., Ebrahimi F.A., Gimelbrant A.A., Ensminger A.W., Tackett M.R., Qi P., Gribnau J., Chess A. Coordination of the random asynchronous replication of autosomal loci. Nat. Genet. 2003, 33:339-341.
36. Singleton A.B., Farrer M., Johnson J., Singleton A., Hague S., Kachergus J., Hulihan M., Peuralinna T., Dutra A., Nussbaum R., et al. alpha-Synuclein locus triplication causes Parkinson's disease. Science 2003, 302:841.
37. Slansky J.E., Farnham P.J. Transcriptional regulation of the dihydrofolate reductase gene. Bioessays 1996, 18:55-62.
38. Söker T., Dalke C., Puk O., Floss T., Becker L., Bolle I., Favor J., Hans W., Hölter S.M., Horsch M., et al. Pleiotropic effects in Eya3 knockout mice. BMC Dev. Biol. 2008, 8:118.
39. Stadler M.B., Murr R., Burger L., Ivanek R., Lienert F., Schöler A., Van Nimwegen E., Wirbelauer C., Oakeley E.J., Gaidatzis D., et al. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 2011, 480:490-495.
40. Takagi N., Sugawara O., Sasaki M. Regional and temporal changes in the pattern of X-chromosome replication during the early post-implantation development of the female mouse. Chromosoma 1982, 85:275-286.
41. Takizawa T., Gudla P.R., Guo L., Lockett S., Misteli T. Allele-specific nuclear positioning of the monoallelically expressed astrocyte marker GFAP. Genes Dev. 2008, 22:489-498.
42. Wang J., Valo Z., Bowers C.W., Smith D.D., Liu Z., Singer-Sam J. Dual DNA methylation patterns in the CNS reveal developmentally poised chromatin and monoallelic expression of critical genes. PLoS One 2010, 5:e13843.
43. Wutz A. Gene silencing in X-chromosome inactivation: advances inunderstanding facultative heterochromatin formation. Nat. Rev. Genet. 2011, 12:542-553.
44. Xu P.X. The EYA-SO/SIX complex in development and disease. Pediatr. Nephrol. 2013, 28:843-854.
45. Xu P.X., Adams J., Peters H., Brown M.C., Heaney S., Maas R. Eya1-deficient mice lack ears and kidneys and show abnormal apoptosis of organ primordia. Nat. Genet. 1999, 23:113-117.
46. Xu P.X., Zheng W., Huang L., Maire P., Laclef C., Silvius D. Six1 is required for the early organogenesis of mammalian kidney. Development 2003, 130:3085-3094.
47. Zou D., Erickson C., Kim E.H., Jin D., Fritzsch B., Xu P.X. Eya1 gene dosage critically affects the development of sensory epithelia in the mammalian inner ear. Hum. Mol. Genet. 2008, 17:3340-3356.
48. Zwemer L.M., Zak A., Thompson B.R., Kirby A., Daly M.J., Chess A., Gimelbrant A.A. Autosomal monoallelic expression in the mouse. Genome Biol. 2012, 13:R10.