Random X inactivation and extensive mosaicism in human placenta revealed by analysis of allele-specific gene expression along the X chromosome

PLoS ONE

Volumn 5, Issue 6, 2010, Pages

  Moreira de Mello, Joana Carvalho ^a   de Araújo, Érica Sara Souza ^a   Stabellini, Raquel ^a   Fraga, Ana Maria ^a   de Souza, Jorge Estefano Santana ^b   Sumita, Denilce R ^c   Camargo, Anamaria A ^b   Pereira, Lygia V ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (Brazil)

^c Genomic Engenharia Molecular   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME PROTEIN; PROTEIN ATRX; PROTEIN CLIC2; PROTEIN DYNLT3; PROTEIN EBP; PROTEIN G6PD; PROTEIN GPC4; PROTEIN IL13RA1; PROTEIN MPP1; PROTEIN OPHN1; PROTEIN PIGA; PROTEIN SH3BGRL; PROTEIN SUV39H1; PROTEIN SYTL4; PROTEIN TBL1X; PROTEIN TCEAL4; PROTEIN TIMP1; PROTEIN TSPAN7; PROTEIN VBP1; PROTEIN XIST; PROTEIN ZFX; PROTEIN ZNF75D; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CHROMOSOME INACTIVATION; CONTROLLED STUDY; FEMALE; FETUS; GENE DOSAGE; GENE EXPRESSION; GENE SILENCING; GENETIC CONSERVATION; GENETIC HETEROGENEITY; HUMAN; HUMAN CELL; HUMAN TISSUE; PLACENTA; PROMOTER REGION; SEX CHROMOSOME MOSAICISM; SINGLE NUCLEOTIDE POLYMORPHISM; X CHROMOSOME;

ALLELES; CHROMOSOMES, HUMAN, X; FEMALE; GENE EXPRESSION; GENOMIC IMPRINTING; HUMANS; MALE; MOSAICISM; PLACENTA; POLYMORPHISM, SINGLE NUCLEOTIDE; PREGNANCY; X CHROMOSOME INACTIVATION;

BOVINAE; EUTHERIA; METATHERIA; MUS; THERIA;

EID: 77955188336     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010947     Document Type: Article

References (44)

1. Cooper DW, VandeBerg JL, Sharman GB, Poole WE (1971) Phosphoglycerate kinase polymorphism in kangaroos provides further evidence for paternal X inactivation. Nat New Biol 230: 155-157.
2. Sharman GB (1971) Late DNA replication in the paternally derived X chromosome of female kangaroos. Nature 230: 231-232.
3. Takagi N, Sasaki M (1975) Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse. Nature 256: 640-642.
4. West JD, Frels WI, Chapman VM, Papaioannou VE (1977) Preferential expression of the maternally derived X chromosome in the mouse yolk sac. Cell 12: 873-882.
5. Wake N, Takagi N, Sasaki M (1976) Non-random inactivation of X chromosome in the rat yolk sac. Nature 262: 580-581.
6. Xue F, Tian XC, Du F, Kubota C, Taneja M, et al. (2002) Aberrant patterns of X chromosome inactivation in bovine clones. Nat Genet 31: 216-220.
7. Payer B, Lee JT (2008) X Chromosome Dosage Compensation: How Mammals Keep the Balance. Annu Rev Genet 42: 733-772.
8. Huynh KD, Lee JT (2003) Inheritance of a pre-inactivated paternal X chromosome in early mouse embryos. Nature 426: 857-862.
9. Okamoto I, Otte AP, Allis CD, Reinberg D, Heard E (2004) Epigenetic dynamics of imprinted X inactivation during early mouse development. Science 303: 644-649.
10. Patrat C, Okamoto I, Diabangouaya P, Vialon V, Le BP, et al. (2009) Dynamic changes in paternal X-chromosome activity during imprinted X-chromosome inactivation in mice. Proc Natl Acad Sci U S A 106: 5198-5203. 0810683106 [pii];10.1073/pnas.0810683106 [doi].
11. Mak W, Nesterova TB, de Napoles M, Appanah R, Yamanaka S, et al. (2004) Reactivation of the paternal X chromosome in early mouse embryos. Science 303: 666-669. 10.1126/science.1092674 [doi];303/5658/666 [pii].
12. Migeon BR, Do TT (1978) In search of nonrandom X inactivation: studies of the placenta from newborns heterozygous for glucose-6-phosphate dehydrogenase. Basic Life Sci 12: 379-391.
13. Ropers HH, Wolff G, Hitzeroth HW (1978) Preferential X inactivation in human placenta membranes: is the paternal X inactive in early embryonic development of female mammals? Hum Genet 43: 265-273.
14. Harrison KB, Warburton D (1986) Preferential X-chromosome activity in human female placental tissues. Cytogenet Cell Genet 41: 163-168.
15. Harrison KB (1989) X-chromosome inactivation in the human cytotrophoblast. Cytogenet Cell Genet 52: 37-41.
16. Migeon BR, Do TT (1979) In search of non-random X inactivation: studies of fetal membranes heterozygous for glucose-6-phosphate dehydrogenase. Am J Hum Genet 31: 581-585.
17. Mohandas TK, Passage MB, Williams JW 3rd, Sparkes RS, Yen PH, et al. (1989) X-chromosome inactivation in cultured cells from human chorionic villi. Somat Cell Mol Genet 15: 131-136.
18. Goto T, Wright E, Monk M (1997) Paternal X-chromosome inactivation in human trophoblastic cells. Mol Hum Reprod 3: 77-80.
19. Uehara S, Tamura M, Nata M, Ji G, Yaegashi N, et al. (2000) X-chromosome inactivation in the human trophoblast of early pregnancy. J Hum Genet 45: 119-126.
20. Zeng SM, Yankowitz J (2003) X-inactivation patterns in human embryonic and extra-embryonic tissues. Placenta 24: 270-275.
21. Anderson CL, Brown CJ (1999) Polymorphic X-chromosome inactivation of the human TIMP1 gene. Am J Hum Genet 65: 699-708. S0002-9297(07)62321-0 [pii];10.1086/302556 [doi].
22. Carrel L, Willard HF (2005) X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434: 400-404.
23. Ross MT, Grafham DV, Coffey AJ, Scherer S, McLay K, et al. (2005) The DNA sequence of the human X chromosome. Nature 434: 325-337. nature03440 [pii];10.1038/nature03440 [doi].
24. Vasques LR, Pereira LV (2001) Allele-specific X-linked gene activity in normal human cells assayed by expressed single nucleotide polymorphisms (cSNPs). DNA Res 8: 173-177.
25. Stabellini R, de Mello JC, Hernandes LM, Pereira LV (2009) MAOA and GYG2 are submitted to X chromosome inactivation in human fibroblasts. Epigenetics 4: 388-393. 9492 [pii].
26. Ge B, Gurd S, Gaudin T, Dore C, et al. (2005) Survey of allelic expression using EST mining. Genome Res 15: 1584-1591.
27. Looijenga LH, Gillis AJ, Verkerk AJ, van Putten WL, Oosterhuis JW (1999) Heterogeneous X inactivation in trophoblastic cells of human full-term female placentas. Am J Hum Genet 64: 1445-1452.
28. Bininda-Emonds OR, Cardillo M, Jones KE, MacPhee RD, Beck RM, et al. (2007) The delayed rise of present-day mammals. Nature 446: 507-512. nature05634 [pii];10.1038/nature05634 [doi].
29. van den Berg IM, Laven JS, Stevens M, Jonkers I, Galjaard RJ, et al. (2009) X chromosome inactivation is initiated in human preimplantation embryos. Am J Hum Genet 84: 771-779. S0002-9297(09)00200-6 [pii];10.1016/ j.ajhg.2009.05.003 [doi].
30. Dhara SK, Benvenisty N (2004) Gene trap as a tool for genome annotation and analysis of X chromosome inactivation in human embryonic stem cells. Nucleic Acids Res 32: 3995-4002. 10.1093/nar/gkh746 [doi];32/13/3995 [pii].
31. Migeon BR, Schmidt M, Axelman J, Cullen CR (1986) Complete reactivation of X chromosomes from human chorionic villi with a switch to early DNA replication. Proc Natl Acad Sci U S A 83: 2182-2186.
32. Migeon BR, Axelman J, Jeppesen P, (2005) Differential X reactivation in human placental cells: implications for reversal of X inactivation. Am J Hum Genet 77: 355-364. S0002-9297(07)63017-1 [pii];10.1086/432815 [doi].
33. Willemsen R, Bontekoe CJ, Severijnen LA, Oostra BA (2002) Timing of the absence of FMR1 expression in full mutation chorionic villi. Hum Genet 110: 601-605.
34. Shen Y, Matsuno Y, Fouse SD, Rao N, Root S, et al. (2008) X-inactivation in female human embryonic stem cells is in a nonrandom pattern and prone to epigenetic alterations. Proc Natl Acad Sci U S A 105: 4709-4714.
35. Silva SS, Rowntree RK, Mekhoubad S, Lee JT (2008) X-chromosome inactivation and epigenetic fluidity in human embryonic stem cells. Proc Natl Acad Sci U S A 105: 4820-4825. 0712136105 [pii];10.1073/pnas.0712136105 [doi].
36. Vasques LR, Klockner MN, Pereira LV (2002) X chromosome inactivation: how human are mice? Cytogenet Genome Res 99: 30-35. 10.1159/000071570 [doi];CGR20020991_4030 [pii].
37. Monk D, Arnaud P, Apostolidou S, Hills FA, et al. (2006) Limited evolutionary conservation of imprinting in the human placenta. Proc Natl Acad Sci U S A 103: 6623-6628. 0511031103 [pii];10.1073/pnas.0511031103 [doi].
38. Reik W, Lewis A (2005) Co-evolution of X-chromosome inactivation and imprinting in mammals. Nat Rev Genet 6: 403-410. nrg1602 [pii];10.1038/ nrg1602 [doi].
39. Wagschal A, Feil R (2006) Genomic imprinting in the placenta. Cytogenet Genome Res 113: 90-98. CGR20061131_4090 [pii];10.1159/000090819 [doi]
40. Richards B, Skoletsky J, Shuber AP, Balfour R, Stern RC, et al. (1993) Multiplex PCR amplification from the CFTR gene using DNA prepared from buccal brushes/swabs. Hum Mol Genet 2: 159-163.
41. Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8: 175-185.
42. Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8: 186-194.
43. Amos-Landgraf JM, Cottle A, Plenge RM, Friez M, Schwartz CE, et al. (2006) X chromosome-inactivation patterns of 1,005 phenotypically unaffected females. Am J Hum Genet 79: 493-499. S0002-9297(07)62748-7 [pii];10.1086/507565 [doi].
44. Brown CJ, Carrel L, Willard HF (1997) Expression of genes from the human active and inactive X chromosomes. Am J Hum Genet 60: 1333-1343.