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Published in: World Journal of Surgery 8/2011

01-08-2011

Expression and Function of a Large Non-coding RNA Gene XIST in Human Cancer

Published in: World Journal of Surgery | Issue 8/2011

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Abstract

Background

X inactive-specific transcript (XIST) RNA is involved in X chromosome silencing in female cells and allows X chromosome equilibration with males. X inactive-specific transcript expression has been found to be dysregulated in a variety of human cancers when compared to normal cells; meanwhile, the inactivated X chromosome has been noted to be conspicuously absent in human cancer specimens, whereas X chromosome duplications are widely noted. The specific pathways whereby changes in X chromosome status and XIST expression occur in cancer remain incompletely described. Nevertheless, a role for XIST in BRCA1-mediated epigenetic activity has been proposed.

Methods

Here we review the data regarding XIST expression and X chromosome status in a variety of female, male, and non–sex-related human cancers.

Conclusions

It is not yet known whether X chromosome duplication, XIST dysregulation, and over-expression of X-linked genes represent important factors in tumorgenesis or are simply a consequence of overall epigenetic instability in these cancers.
Literature
1.
go back to reference Perez DS, Hoage TR, Pritchett JR et al (2008) Long, abundantly expressed non-coding transcripts are altered in cancer. Hum Mol Genet 17:642–655PubMedCrossRef Perez DS, Hoage TR, Pritchett JR et al (2008) Long, abundantly expressed non-coding transcripts are altered in cancer. Hum Mol Genet 17:642–655PubMedCrossRef
2.
go back to reference Brown CJ, Ballabio A, Rupert JL et al (1991) A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 349:38–44PubMedCrossRef Brown CJ, Ballabio A, Rupert JL et al (1991) A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 349:38–44PubMedCrossRef
3.
go back to reference Agrelo R, Souabni A, Novatchkova M et al (2009) SATB1 defines the developmental context for gene silencing by XIST in lymphoma and embryonic cells. Dev Cell 16:507–516PubMedCrossRef Agrelo R, Souabni A, Novatchkova M et al (2009) SATB1 defines the developmental context for gene silencing by XIST in lymphoma and embryonic cells. Dev Cell 16:507–516PubMedCrossRef
4.
go back to reference Hall LL, Byron M, Sakai K et al (2002) An ectopic human XIST gene can induce chromosome inactivation in postdifferentiation human HT-1080 cells. Proc Natl Acad Sci USA 99:8677–8682PubMedCrossRef Hall LL, Byron M, Sakai K et al (2002) An ectopic human XIST gene can induce chromosome inactivation in postdifferentiation human HT-1080 cells. Proc Natl Acad Sci USA 99:8677–8682PubMedCrossRef
5.
go back to reference Lyon MF (1962) Sex chromatin and gene action in the mammalian X-chromosome. Am J Hum Genet 14:135–148PubMed Lyon MF (1962) Sex chromatin and gene action in the mammalian X-chromosome. Am J Hum Genet 14:135–148PubMed
6.
go back to reference Lyon MF (1961) Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190:372–373PubMedCrossRef Lyon MF (1961) Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190:372–373PubMedCrossRef
7.
go back to reference Barr ML, Bertram EG (1949) A morphological distinction between neurones of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Nature 163:676PubMedCrossRef Barr ML, Bertram EG (1949) A morphological distinction between neurones of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Nature 163:676PubMedCrossRef
8.
9.
go back to reference Pageau GJ, Hall LL, Ganesan S et al (2007) The disappearing Barr body in breast and ovarian cancers. Nat Rev Cancer 7:628–633PubMedCrossRef Pageau GJ, Hall LL, Ganesan S et al (2007) The disappearing Barr body in breast and ovarian cancers. Nat Rev Cancer 7:628–633PubMedCrossRef
10.
go back to reference Spatz A, Borg C, Feunteun J (2004) X-chromosome genetics and human cancer. Nat Rev Cancer 4:617–629PubMedCrossRef Spatz A, Borg C, Feunteun J (2004) X-chromosome genetics and human cancer. Nat Rev Cancer 4:617–629PubMedCrossRef
11.
go back to reference Kawakami T, Zhang C, Taniguchi T et al (2004) Characterization of loss-of-inactive X in Klinefelter syndrome and female-derived cancer cells. Oncogene 23:6163–6169PubMedCrossRef Kawakami T, Zhang C, Taniguchi T et al (2004) Characterization of loss-of-inactive X in Klinefelter syndrome and female-derived cancer cells. Oncogene 23:6163–6169PubMedCrossRef
12.
go back to reference Benoit MH, Hudson TJ, Maire G et al (2007) Global analysis of chromosome X gene expression in primary cultures of normal ovarian surface epithelial cells and epithelial ovarian cancer cell lines. Int J Oncol 30:5–17PubMed Benoit MH, Hudson TJ, Maire G et al (2007) Global analysis of chromosome X gene expression in primary cultures of normal ovarian surface epithelial cells and epithelial ovarian cancer cell lines. Int J Oncol 30:5–17PubMed
13.
go back to reference Huang KC, Rao PH, Lau CC et al (2002) Relationship of XIST expression and responses of ovarian cancer to chemotherapy. Mol Cancer Ther 1:769–776PubMed Huang KC, Rao PH, Lau CC et al (2002) Relationship of XIST expression and responses of ovarian cancer to chemotherapy. Mol Cancer Ther 1:769–776PubMed
14.
go back to reference Ganesan S, Silver DP, Greenberg RA et al (2002) BRCA1 supports XIST RNA concentration on the inactive X chromosome. Cell 111:393–405PubMedCrossRef Ganesan S, Silver DP, Greenberg RA et al (2002) BRCA1 supports XIST RNA concentration on the inactive X chromosome. Cell 111:393–405PubMedCrossRef
15.
go back to reference Ganesan S, Silver DP, Drapkin R et al (2004) Association of BRCA1 with the inactive X chromosome and XIST RNA. Philos Trans R Soc Lond B Biol Sci 359:123–128PubMedCrossRef Ganesan S, Silver DP, Drapkin R et al (2004) Association of BRCA1 with the inactive X chromosome and XIST RNA. Philos Trans R Soc Lond B Biol Sci 359:123–128PubMedCrossRef
16.
go back to reference Richardson AL, Wang ZC, De Nicolo A et al (2006) X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 9:121–132PubMedCrossRef Richardson AL, Wang ZC, De Nicolo A et al (2006) X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 9:121–132PubMedCrossRef
17.
go back to reference Pageau GJ, Lawrence JB (2006) BRCA1 foci in normal S-phase nuclei are linked to interphase centromeres and replication of pericentric heterochromatin. J Cell Biol 175:693–701PubMedCrossRef Pageau GJ, Lawrence JB (2006) BRCA1 foci in normal S-phase nuclei are linked to interphase centromeres and replication of pericentric heterochromatin. J Cell Biol 175:693–701PubMedCrossRef
18.
go back to reference Pageau GJ, Hall LL, Lawrence JB (2007) BRCA1 does not paint the inactive X to localize XIST RNA but may contribute to broad changes in cancer that impact XIST and Xi heterochromatin. J Cell Biochem 100:835–850PubMedCrossRef Pageau GJ, Hall LL, Lawrence JB (2007) BRCA1 does not paint the inactive X to localize XIST RNA but may contribute to broad changes in cancer that impact XIST and Xi heterochromatin. J Cell Biochem 100:835–850PubMedCrossRef
19.
go back to reference Xiao C, Sharp JA, Kawahara M et al (2007) The XIST noncoding RNA functions independently of BRCA1 in X inactivation. Cell 128:977–989PubMedCrossRef Xiao C, Sharp JA, Kawahara M et al (2007) The XIST noncoding RNA functions independently of BRCA1 in X inactivation. Cell 128:977–989PubMedCrossRef
20.
go back to reference Silver DP, Dimitrov SD, Feunteun J et al (2007) Further evidence for BRCA1 communication with the inactive X chromosome. Cell 128:991–1002PubMedCrossRef Silver DP, Dimitrov SD, Feunteun J et al (2007) Further evidence for BRCA1 communication with the inactive X chromosome. Cell 128:991–1002PubMedCrossRef
21.
go back to reference Sirchia SM, Ramoscelli L, Grati FR et al (2005) Loss of the inactive X chromosome and replication of the active X in BRCA1-defective and wild-type breast cancer cells. Cancer Res 65:2139–2146PubMedCrossRef Sirchia SM, Ramoscelli L, Grati FR et al (2005) Loss of the inactive X chromosome and replication of the active X in BRCA1-defective and wild-type breast cancer cells. Cancer Res 65:2139–2146PubMedCrossRef
22.
go back to reference Vincent-Salomon A, Ganem-Elbaz C, Manie E et al (2007) X inactive-specific transcript RNA coating and genetic instability of the X chromosome in BRCA1 breast tumors. Cancer Res 67:5134–5140PubMedCrossRef Vincent-Salomon A, Ganem-Elbaz C, Manie E et al (2007) X inactive-specific transcript RNA coating and genetic instability of the X chromosome in BRCA1 breast tumors. Cancer Res 67:5134–5140PubMedCrossRef
23.
go back to reference Sirchia SM, Tabano S, Monti L et al (2009) Misbehaviour of XIST RNA in breast cancer cells. PLoS One 4:e5559PubMedCrossRef Sirchia SM, Tabano S, Monti L et al (2009) Misbehaviour of XIST RNA in breast cancer cells. PLoS One 4:e5559PubMedCrossRef
24.
go back to reference Ayoub N, Richler C, Wahrman J (1997) Xist RNA is associated with the transcriptionally inactive XY body in mammalian male meiosis. Chromosoma 106:1–10PubMedCrossRef Ayoub N, Richler C, Wahrman J (1997) Xist RNA is associated with the transcriptionally inactive XY body in mammalian male meiosis. Chromosoma 106:1–10PubMedCrossRef
25.
go back to reference Richler C, Soreq H, Wahrman J (1992) X inactivation in mammalian testis is correlated with inactive X-specific transcription. Nat Genet 2:192–195PubMedCrossRef Richler C, Soreq H, Wahrman J (1992) X inactivation in mammalian testis is correlated with inactive X-specific transcription. Nat Genet 2:192–195PubMedCrossRef
26.
go back to reference McCarrey JR, Watson C, Atencio J et al (2002) X-chromosome inactivation during spermatogenesis is regulated by an Xist/Tsix-independent mechanism in the mouse. Genesis 34:257–266PubMedCrossRef McCarrey JR, Watson C, Atencio J et al (2002) X-chromosome inactivation during spermatogenesis is regulated by an Xist/Tsix-independent mechanism in the mouse. Genesis 34:257–266PubMedCrossRef
27.
go back to reference Looijenga LH, Gillis AJ, van Gurp RJ et al (1997) X inactivation in human testicular tumors. XIST expression and androgen receptor methylation status. Am J Pathol 151:581–590PubMed Looijenga LH, Gillis AJ, van Gurp RJ et al (1997) X inactivation in human testicular tumors. XIST expression and androgen receptor methylation status. Am J Pathol 151:581–590PubMed
28.
go back to reference Kawakami T, Okamoto K, Sugihara H et al (2003) The roles of supernumerical X chromosomes and XIST expression in testicular germ cell tumors. J Urol 169:1546–1552PubMedCrossRef Kawakami T, Okamoto K, Sugihara H et al (2003) The roles of supernumerical X chromosomes and XIST expression in testicular germ cell tumors. J Urol 169:1546–1552PubMedCrossRef
29.
go back to reference Kawakami T, Okamoto K, Ogawa O et al (2004) XIST unmethylated DNA fragments in male-derived plasma as a tumour marker for testicular cancer. Lancet 363:40–42PubMedCrossRef Kawakami T, Okamoto K, Ogawa O et al (2004) XIST unmethylated DNA fragments in male-derived plasma as a tumour marker for testicular cancer. Lancet 363:40–42PubMedCrossRef
30.
go back to reference Zhang C, Kawakami T, Okada Y et al (2005) Distinctive epigenetic phenotype of cancer testis antigen genes among seminomatous and nonseminomatous testicular germ-cell tumors. Genes Chromosomes Cancer 43:104–112PubMedCrossRef Zhang C, Kawakami T, Okada Y et al (2005) Distinctive epigenetic phenotype of cancer testis antigen genes among seminomatous and nonseminomatous testicular germ-cell tumors. Genes Chromosomes Cancer 43:104–112PubMedCrossRef
31.
go back to reference Song MA, Park JH, Jeong KS et al (2007) Quantification of CpG methylation at the 5′-region of XIST by pyrosequencing from human serum. Electrophoresis 28:2379–2384PubMedCrossRef Song MA, Park JH, Jeong KS et al (2007) Quantification of CpG methylation at the 5′-region of XIST by pyrosequencing from human serum. Electrophoresis 28:2379–2384PubMedCrossRef
32.
go back to reference Kleinheinz A, Schulze W (1994) Klinefelter’s syndrome: new and rapid diagnosis by PCR analysis of XIST gene expression. Andrologia 26:127–129PubMedCrossRef Kleinheinz A, Schulze W (1994) Klinefelter’s syndrome: new and rapid diagnosis by PCR analysis of XIST gene expression. Andrologia 26:127–129PubMedCrossRef
33.
go back to reference Swerdlow AJ, Schoemaker MJ, Higgins CD et al (2005) Cancer incidence and mortality in men with Klinefelter syndrome: a cohort study. J Natl Cancer Inst 97:1204–1210PubMedCrossRef Swerdlow AJ, Schoemaker MJ, Higgins CD et al (2005) Cancer incidence and mortality in men with Klinefelter syndrome: a cohort study. J Natl Cancer Inst 97:1204–1210PubMedCrossRef
34.
go back to reference Teixeira MR, Pandis N, Dietrich CU et al (1998) Chromosome banding analysis of gynecomastias and breast carcinomas in men. Genes Chromosomes Cancer 23:16–20PubMedCrossRef Teixeira MR, Pandis N, Dietrich CU et al (1998) Chromosome banding analysis of gynecomastias and breast carcinomas in men. Genes Chromosomes Cancer 23:16–20PubMedCrossRef
35.
go back to reference Rudas M, Schmidinger M, Wenzel C et al (2000) Karyotypic findings in two cases of male breast cancer. Cancer Genet Cytogenet 121:190–193PubMedCrossRef Rudas M, Schmidinger M, Wenzel C et al (2000) Karyotypic findings in two cases of male breast cancer. Cancer Genet Cytogenet 121:190–193PubMedCrossRef
36.
go back to reference Wu ZS, Lee JH, Kwon JA et al (2009) Genetic alterations and chemosensitivity profile in newly established human renal collecting duct carcinoma cell lines. BJU Int 103:1721–1728PubMedCrossRef Wu ZS, Lee JH, Kwon JA et al (2009) Genetic alterations and chemosensitivity profile in newly established human renal collecting duct carcinoma cell lines. BJU Int 103:1721–1728PubMedCrossRef
37.
go back to reference Lassmann S, Weis R, Makowiec F et al (2007) Array CGH identifies distinct DNA copy number profiles of oncogenes and tumor suppressor genes in chromosomal- and microsatellite-unstable sporadic colorectal carcinomas. J Mol Med 85:293–304PubMedCrossRef Lassmann S, Weis R, Makowiec F et al (2007) Array CGH identifies distinct DNA copy number profiles of oncogenes and tumor suppressor genes in chromosomal- and microsatellite-unstable sporadic colorectal carcinomas. J Mol Med 85:293–304PubMedCrossRef
38.
go back to reference Shi Z, Dragin N, Miller ML et al (2010) Oral benzo[a]pyrene-induced cancer: two distinct types in different target organs depend on the mouse Cyp1 genotype. Int J Cancer 127:2334–2350PubMedCrossRef Shi Z, Dragin N, Miller ML et al (2010) Oral benzo[a]pyrene-induced cancer: two distinct types in different target organs depend on the mouse Cyp1 genotype. Int J Cancer 127:2334–2350PubMedCrossRef
39.
go back to reference Nomura S, Baxter T, Yamaguchi H et al (2004) Spasmolytic polypeptide expressing metaplasia to preneoplasia in H. felis-infected mice. Gastroenterology 127:582–594PubMedCrossRef Nomura S, Baxter T, Yamaguchi H et al (2004) Spasmolytic polypeptide expressing metaplasia to preneoplasia in H. felis-infected mice. Gastroenterology 127:582–594PubMedCrossRef
40.
go back to reference McDonald HL, Gascoyne RD, Horsman D et al (2000) Involvement of the X chromosome in non-Hodgkin lymphoma. Genes Chromosomes Cancer 28:246–257PubMedCrossRef McDonald HL, Gascoyne RD, Horsman D et al (2000) Involvement of the X chromosome in non-Hodgkin lymphoma. Genes Chromosomes Cancer 28:246–257PubMedCrossRef
41.
go back to reference Rack KA, Chelly J, Gibbons RJ et al (1994) Absence of the XIST gene from late-replicating isodicentric X chromosomes in leukaemia. Hum Mol Genet 3:1053–1059PubMedCrossRef Rack KA, Chelly J, Gibbons RJ et al (1994) Absence of the XIST gene from late-replicating isodicentric X chromosomes in leukaemia. Hum Mol Genet 3:1053–1059PubMedCrossRef
Metadata
Title
Expression and Function of a Large Non-coding RNA Gene XIST in Human Cancer
Publication date
01-08-2011
Published in
World Journal of Surgery / Issue 8/2011
Print ISSN: 0364-2313
Electronic ISSN: 1432-2323
DOI
https://doi.org/10.1007/s00268-010-0951-0

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