Complexities of X chromosome inactivation status in female human induced pluripotent stem cells - A brief review and scientific update for autism research

Journal of Neurodevelopmental Disorders

Volumn 8, Issue 1, 2016, Pages

  Dandulakis, Mary G ^a   Meganathan, Kesavan ^a   Kroll, Kristen L ^a   Bonni, Azad ^b   Constantino, John N ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

ASD; Autism; Developmental disorders; Female protective effect; iPSC; X chromosome; X inactivation; X linked ASD; X reactivation

Indexed keywords

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; AUTISM; CELL DIFFERENTIATION; CELL FUNCTION; CELL POPULATION; DNA METHYLATION; GENE MUTATION; GENETIC BACKGROUND; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; INDUCED PLURIPOTENT STEM CELL; MOUSE; NONHUMAN; PENETRANCE; PHENOTYPE; PRIORITY JOURNAL; REVIEW; X CHROMOSOME; X CHROMOSOME INACTIVATION;

EID: 84974712458     PISSN: 18661947     EISSN: 18661955     Source Type: Journal    
DOI: 10.1186/s11689-016-9155-8     Document Type: Review

References (39)

1. Baker E, Jeste SS. Diagnosis and management of autism spectrum disorder in the era of genomics: rare disorders can pave the way for targeted treatments. Pediatr Clin North Am. 2015. doi: 10.1016/j.pcl.2015.03.003.
2. Kim DS, Ross PJ, Zaslavsky K, Ellis J. Optimizing neuronal differentiation from induced pluripotent stem cells to model ASD. Front Cell Neurosci. 2014. doi: 10.3389/fncel.2014.00109.
3. Prilutsky D, Palmer NP, Smedemark-Margulies N, Schlaeger TM, Margulies DM, Kohane IS. iPSC-derived neurons as a higher-throughput readout for autism: promises and pitfalls. Trends Mol Med. 2014. doi: 10.1016/j.molmed.2013.11.004.
4. Griesi-Oliveira K, Acab A, Gupta AR, Sunaga DY, Chailangkarn T, Nicol X, et al. Modeling non-syndromic autism and the impact of TRPC6 disruption in human neurons. Mol Psychiatry. 2014. doi: 10.1038/mp.2014.141.
5. Acab A, Muotri AR. The use of induced pluripotent stem cell technology to advance autism research and treatment. Neurotherapeutics. 2015. doi: 10.1007/s13311-015-0354-x.
6. Tian Y, Voineagu I, Pasca SP, Won HJ, Chandran V, Horvath S, et al. Alteration in basal and depolarization induced transcriptional network in iPSC derived neurons from Timothy syndrome. Genome Med. 2014;6(10):75. doi: 10.1186/s13073-014-0075-5.
7. Gockley J, Willsey AJ, Dong S, Dougherty JD, Constantino JN, Sanders SJ. The female protective effect in autism spectrum disorder is not mediated by a single genetic locus. Mol Autism. 2015. doi: 10.1186/s13229-015-0014-3.
8. Gaugler T, Klei L, Sanders SJ, Bodea CA, Goldberg AP, Lee AB, et al. Most genetic risk for autism resides with common variation. Nat Genet. 2014. doi: 10.1038/ng.3039.
9. Christensen DL, et al. 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; doi: 10.15585/mmwr.ss6503a1
10. Boumil RM, Lee JT. Forty years of decoding the silence in X-chromosome inactivation. Hum Mol Genet. 2001;10(20):2225-32.
11. Pontier DB, Gribnau J. Xist regulation and function explored. Hum Genet. 2011. doi: 10.1007/s00439-011-1008-7.
12. Wutz A. Gene silencing in X-chromosome inactivation: advances in understanding facultative heterochromatin formation. Nat Rev Genet. 2011. doi: 10.1038/nrg3035.
13. Briggs SF, Reijo Pera RA. X chromosome inactivation: recent advances and a look forward. Curr Opin Genet Dev. 2014. doi: 10.1016/j.gde.2014.09.010.
14. Newall AE, Duthie S, Formstone E, Nesterova T, Alexiou M, Johnston C, et al. Primary non-random X inactivation associated with disruption of Xist promoter regulation. Hum Mol Genet. 2001;10(6):581-9.
15. Gong X, Bacchelli E, Blasi F, Toma C, Betancur C, Chaste P et al. Analysis of X chromosome inactivation in autism spectrum disorders. Am J Med Genet B Neuropsychiatr Genet. 2008;147B(6): doi: 10.1002/ajmg.b.30688.
16. Maria CN et al. Pluripotent stem cells in neurodegenerative and neurodevelopmental diseases. Hum Mol Genet. 2010. doi: 10.1093/hmg/ddq159.
17. Srikanth P et al. Stem cells on the brain: modeling neurodevelopmental an neurodegenerative diseases using human iPSCs. J Neurogenet. 2014. doi: 10.3109/01677063.2014.881358.
18. Corti S et al. Human pluripotent stem cells as tools for neurodegenerative and neurodevelopmental disease modeling and drug discovery. Expert Opin Drug Discov. 2015. doi: 10.1517/17460441.2015.1037737.
19. Lewitzky M, Yamanaka S. Reprogramming somatic cells towards pluripotency by defined factors. Curr Opin Biotechnol. 2007;18(5): doi: 10.1016/j.copbio.2007.09.007.
20. Papp B, Plath K. Reprogramming to pluripotency: stepwise resetting of the epigenetic landscape. Cell Res. 2011;21(3): doi: 10.1038/cr.2011.28.
21. Malik N, Rao MS. A review of the methods for human iPSC derivation. Methods Mol Biol. 2013. doi: 10.1007/978-1-62703-348-0-3.
22. Marchetto MC, Carromeu C, Acab A, Yu D, Yeo GW, Mu Y, et al. A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell. 2010. doi: 10.1016/j.cell.2010.10.016.
23. Ananiev G, Williams EC, Li H, Chang Q. Isogenic pairs of wild type and mutant induced pluripotent stem cell (iPSC) lines from Rett syndrome patients as in vitro disease model. PLoS One. 2011. doi: 10.1371/journal.pone.0025255.
24. Tchieu J, Kuoy E, Chin MH, Trinh H, Patterson M, Sherman SP, et al. Female human iPSCs retain an inactive X chromosome. Cell Stem Cell. 2010. doi: 10.1016/j.stem.2010.06.024.
25. Kim KY, Hysolli E, Park IH. Neuronal maturation defect in induced pluripotent stem cells from patients with Rett syndrome. Proc Natl Acad Sci U S A. 2011. doi: 10.1073/pnas.1018979108.
26. Barakat TS, Ghazvini M, de Hoon B, Li T, Eussen B, Douben H, et al. Stable X chromosome reactivation in female human induced pluripotent stem cells. Stem Cell Reports. 2015. doi: 10.1016/j.stemcr.2014.12.012.
27. Tomoda K, Takahashi K, Leung K, Okada A, Narita M, Yamada NA, et al. Derivation conditions impact X-inactivation status in female human induced pluripotent stem cells. Cell Stem Cell. 2012. doi: 10.1016/j.stem.2012.05.019.
28. Pomp et al. Unexpected X chromosome skewing during culture and reprogramming of human somatic cells can be alleviated by exogenous telomerase. Cell Stem Cell. 2011. doi: 10.1016/j.stem.2011.06.004.
29. Lessing D, Anguera M. X chromosome inactivation and epigenetic responses to cellular reprogramming. Annu Rev Gemonics Hum Genet. 2013. doi: 10.1146/annurev-genom-091212-153530.
30. Davidson KC, Mason EA, Pera MF. The pluripotent state in mouse and human. Development. 2015. doi: 10.1242/dev.116061.
31. Manor YS, Massarwa R, Hanna JH. Establishing the human naïve pluripotent state. Curr Opin Genet Der. 2015. doi: 10.1016/j.gde.2015.07.005.
32. Mekhoubad S, Bock C, de Boer AS, Kiskinis E, Meissner A, Eggan K. Erosion of dosage compensation impacts human iPSC disease modeling. Cell Stem Cell. 2012. doi: 10.1016/j.stem.2012.02.014.
33. Vallot C, Ouimette JF, Makhlouf M, Feraud O, Pontis J, Come J, et al. Erosion of X chromosome inactivation in human pluripotent cells initiates with XACT coating and depends on a specific heterochromatin landscape. Cell Stem Cell. 2015. doi: 10.1016/j.stem.2015.03.016.
34. Allen RC, Zoghbi HY, Moseley AB, Rosenblatt HM, Belmont JW. Methylation of HpaII and HhaI sites near the polymorphic CAG repeat in the human androgen-receptor gene correlates with X chromosome inactivation. Am J Hum Genet. 1992;51(6):1229-39.
35. Bruck T, Benvenisty N. Meta-analysis of the heterogeneity of X chromosome inactivation in human pluripotent stem cells. Stem Cell Res. 2011. doi: 10.1016/j.scr.2010.12.001.
36. DeRosa BA et al. Derivation of autism spectrum disorder-specific induced pluripotent stem cells from peripheral blood mononuclear cells. Neurosci Lett. 2012. doi: 10.1016/j.neulet.2012.02.086.
37. Richner M, Victor MB, Liu Y, Abernathy D, Yoo AS. MicroRNA-based conversion of human fibroblasts into striatal medium spiny neurons. Nat Protoc. 2015. doi: 10.1038/nprot.2015.102.
38. Gregg C et al. Sex-specific parent-of-origin allelic expression in the mouse brain. Science. 2010. doi: 10.1126/science.1190831.
39. Chadwick LH, Willard HF. Genetic and parent-of-origin influences on X chromosome choice in Xce heterozygous mice. Mamm Genome. 2005;16(9):691-9.