Comparative analysis of the primate X-inactivation center region and reconstruction of the ancestral primate XIST locus.

Here we provide a detailed comparative analysis across the candidate X-Inactivation Center (XIC) region and the XIST locus in the genomes of six primates and three mammalian outgroup species. Since lemurs and other strepsirrhine primates represent the sister lineage to all other primates, this analysis focuses on lemurs to reconstruct the ancestral primate sequences and to gain insight into the evolution of this region and the genes within it. This comparative evolutionary genomics approach reveals significant expansion in genomic size across the XIC region in higher primates, with minimal size alterations across the XIST locus itself. Reconstructed primate ancestral XIC sequences show that the most dramatic changes during the past 80 million years occurred between the ancestral primate and the lineage leading to Old World monkeys. In contrast, the XIST locus compared between human and the primate ancestor does not indicate any dramatic changes to exons or XIST-specific repeats; rather, evolution of this locus reflects small incremental changes in overall sequence identity and short repeat insertions. While this comparative analysis reinforces that the region around XIST has been subject to significant genomic change, even among primates, our data suggest that evolution of the XIST sequences themselves represents only small lineage-specific changes across the past 80 million years.

[1]  S. O’Brien,et al.  A Molecular Phylogeny of Living Primates , 2011, PLoS genetics.

[2]  Jeannie T. Lee,et al.  The Long Noncoding RNA, Jpx, Is a Molecular Switch for X Chromosome Inactivation , 2010, Cell.

[3]  E. Barillot,et al.  LINE-1 Activity in Facultative Heterochromatin Formation during X Chromosome Inactivation , 2010, Cell.

[4]  Xiaoyu Chen,et al.  Comparative assessment of methods for aligning multiple genome sequences , 2010, Nature Biotechnology.

[5]  J. Shendure,et al.  Global survey of escape from X inactivation by RNA-sequencing in mouse. , 2010, Genome research.

[6]  D. Trujillano,et al.  Long Noncoding RNAs, Chromatin, and Development , 2010, TheScientificWorldJournal.

[7]  P. Avner,et al.  2-D Structure of the A Region of Xist RNA and Its Implication for PRC2 Association , 2010, PLoS biology.

[8]  Mathieu Blanchette,et al.  Ancestors 1.0: a web server for ancestral sequence reconstruction , 2010, Bioinform..

[9]  E. Heard,et al.  Lessons from comparative analysis of X-chromosome inactivation in mammals , 2009, Chromosome Research.

[10]  E. Eichler,et al.  Comparative analysis of Alu repeats in primate genomes. , 2009, Genome research.

[11]  E. Birney,et al.  Genome-wide nucleotide-level mammalian ancestor reconstruction. , 2008, Genome research.

[12]  Jeannie T. Lee,et al.  Polycomb Proteins Targeted by a Short Repeat RNA to the Mouse X Chromosome , 2008, Science.

[13]  N. Brockdorff,et al.  A Dual Origin of the Xist Gene from a Protein-Coding Gene and a Set of Transposable Elements , 2008, PloS one.

[14]  Jennifer A. Erwin,et al.  New twists in X-chromosome inactivation. , 2008, Current opinion in cell biology.

[15]  T. Graves,et al.  Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. , 2008, Genome research.

[16]  H. Willard,et al.  Development and application of a phylogenomic toolkit: resolving the evolutionary history of Madagascar's lemurs. , 2008, Genome research.

[17]  David Haussler,et al.  Computational reconstruction of ancestral DNA sequences. , 2008, Methods in molecular biology.

[18]  M. Ferguson-Smith,et al.  Mammalian karyotype evolution , 2007, Nature Reviews Genetics.

[19]  Irmtraud M. Meyer,et al.  A cross-species comparison of X-chromosome inactivation in Eutheria. , 2007, Genomics.

[20]  J. Graves,et al.  Construction and evolution of imprinted loci in mammals. , 2007, Trends in genetics : TIG.

[21]  Mathieu Blanchette,et al.  Exact and Heuristic Algorithms for the Indel Maximum Likelihood Problem , 2007, J. Comput. Biol..

[22]  Webb Miller,et al.  Using genomic data to unravel the root of the placental mammal phylogeny. , 2007, Genome research.

[23]  H. Willard,et al.  Primate comparative genomics: lemur biology and evolution. , 2007, Trends in genetics : TIG.

[24]  M. Wakefield,et al.  The region homologous to the X-chromosome inactivation centre has been disrupted in marsupial and monotreme mammals , 2007, Chromosome Research.

[25]  Saurabh Sinha,et al.  Indelign: a probabilistic framework for annotation of insertions and deletions in a multiple alignment , 2007, Bioinform..

[26]  Jennifer A. Erwin,et al.  The DXPas34 repeat regulates random and imprinted X inactivation. , 2007, Developmental cell.

[27]  Laurent Duret,et al.  The Xist RNA Gene Evolved in Eutherians by Pseudogenization of a Protein-Coding Gene , 2006, Science.

[28]  J. Mattick,et al.  Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function. , 2006, Trends in genetics : TIG.

[29]  E. Eichler,et al.  A genome-wide comparison of recent chimpanzee and human segmental duplications , 2005, Nature.

[30]  P. Pevzner,et al.  Dynamics of Mammalian Chromosome Evolution Inferred from Multispecies Comparative Maps , 2005, Science.

[31]  H. Willard,et al.  X-inactivation profile reveals extensive variability in X-linked gene expression in females , 2005, Nature.

[32]  D. Haussler,et al.  Reconstructing large regions of an ancestral mammalian genome in silico. , 2004, Genome research.

[33]  Bradley I. Coleman,et al.  An intermediate grade of finished genomic sequence suitable for comparative analyses. , 2004, Genome research.

[34]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[35]  Lior Pachter,et al.  VISTA: computational tools for comparative genomics , 2004, Nucleic Acids Res..

[36]  G. Sarto,et al.  Center for Barr body condensation on the proximal part of the human Xq: a hypothesis , 1974, Chromosoma.

[37]  H. Willard,et al.  Barring gene expression after XIST: maintaining facultative heterochromatin on the inactive X. , 2003, Seminars in cell & developmental biology.

[38]  B. Roe,et al.  Using a pericentromeric interspersed repeat to recapitulate the phylogeny and expansion of human centromeric segmental duplications. , 2003, Molecular biology and evolution.

[39]  M. Springer,et al.  The evolution of tribospheny and the antiquity of mammalian clades. , 2003, Molecular phylogenetics and evolution.

[40]  Chuong B. Do,et al.  Access the most recent version at doi: 10.1101/gr.926603 References , 2003 .

[41]  E. Eichler,et al.  Analysis of primate genomic variation reveals a repeat-driven expansion of the human genome. , 2003, Genome research.

[42]  Jon D. McAuliffe,et al.  Phylogenetic Shadowing of Primate Sequences to Find Functional Regions of the Human Genome , 2003, Science.

[43]  B. Migeon,et al.  Species differences in TSIX/Tsix reveal the roles of these genes in X-chromosome inactivation. , 2002, American journal of human genetics.

[44]  N. Brockdorff X-chromosome inactivation: closing in on proteins that bind Xist RNA. , 2002, Trends in genetics : TIG.

[45]  H. Willard,et al.  Cell cycle–dependent localization of macroH2A in chromatin of the inactive X chromosome , 2002, The Journal of cell biology.

[46]  Tom H. Pringle,et al.  The human genome browser at UCSC. , 2002, Genome research.

[47]  Rudolf Jaenisch,et al.  Chromosomal silencing and localization are mediated by different domains of Xist RNA , 2002, Nature Genetics.

[48]  Laurent Duret,et al.  Comparative sequence analysis of the X-inactivation center region in mouse, human, and bovine. , 2000, Genome research.

[49]  D. Swofford PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[50]  A. C. Chinault,et al.  Differentially methylated forms of histone H3 show unique association patterns with inactive human X chromosomes , 2002, Nature Genetics.

[51]  C. Allis,et al.  Methylation of Histone H3 at Lys-9 Is an Early Mark on the X Chromosome during X Inactivation , 2001, Cell.

[52]  Jeannie T. Lee,et al.  CTCF, a Candidate Trans-Acting Factor for X-Inactivation Choice , 2001, Science.

[53]  T B Nesterova,et al.  Characterization of the genomic Xist locus in rodents reveals conservation of overall gene structure and tandem repeats but rapid evolution of unique sequence. , 2001, Genome research.

[54]  H. Willard,et al.  A Novel Chromatin Protein, Distantly Related to Histone H2a, Is Largely Excluded from the Inactive X Chromosome , 2001, The Journal of cell biology.

[55]  Lior Pachter,et al.  VISTA : visualizing global DNA sequence alignments of arbitrary length , 2000, Bioinform..

[56]  J A Bailey,et al.  Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: the Lyon repeat hypothesis. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[57]  P. Avner,et al.  Functional Analysis of the DXPas34Locus, a 3′ Regulator of Xist Expression , 1999, Molecular and Cellular Biology.

[58]  P. Avner,et al.  Xist Yeast Artificial Chromosome Transgenes Function as X-Inactivation Centers Only in Multicopy Arrays and Not as Single Copies , 1999, Molecular and Cellular Biology.

[59]  Jeannie T. Lee,et al.  Tsix, a gene antisense to Xist at the X-inactivation centre , 1999, Nature Genetics.

[60]  J. Lee,et al.  Genetic analysis of the mouse X inactivation center defines an 80-kb multifunction domain. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[61]  G. Benson,et al.  Tandem repeats finder: a program to analyze DNA sequences. , 1999, Nucleic acids research.

[62]  M. Lyon,et al.  X-Chromosome inactivation: a repeat hypothesis , 1998, Cytogenetic and Genome Research.

[63]  C. Groves,et al.  Toward a phylogenetic classification of Primates based on DNA evidence complemented by fossil evidence. , 1998, Molecular phylogenetics and evolution.

[64]  Brian D. Hendrich,et al.  Identification and characterization of the human XIST gene promoter: implications for models of X chromosome inactivation , 1997, Nucleic Acids Res..

[65]  Alan Ashworth,et al.  Xist has properties of the X-chromosome inactivation centre , 1997, Nature.

[66]  Carolyn J. Brown,et al.  Evidence that heteronuclear proteins interact with the XIST RNA in vitro , 1996, Somatic cell and molecular genetics.

[67]  R. Jaenisch,et al.  A 450 kb Transgene Displays Properties of the Mammalian X-Inactivation Center , 1996, Cell.

[68]  R. Hamvas,et al.  Xist expression from an Xist YAC transgene carried on the mouse Y chromosome. , 1996, Human molecular genetics.

[69]  A. Ashworth,et al.  Transgenic mice carrying an Xist-containing YAC. , 1996, Human molecular genetics.

[70]  S. Rastan,et al.  Requirement for Xist in X chromosome inactivation , 1996, Nature.

[71]  A. Monaco,et al.  2.6 Mb YAC contig of the human X inactivation center region in Xq13: physical linkage of the RPS4X, PHKA1, XIST and DXS128E genes. , 1993, Human molecular genetics.

[72]  S. Bressler,et al.  Mapping of the distal boundary of the X-inactivation center in a rearranged X chromosome from a female expressing XIST. , 1993, Human molecular genetics.

[73]  Dominic P. Norris,et al.  The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus , 1992, Cell.

[74]  Carolyn J. Brown,et al.  The human XIST gene: Analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus , 1992, Cell.

[75]  A. Ashworth,et al.  Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome , 1991, Nature.

[76]  H. Willard,et al.  Characterization of a murine gene expressed from the inactive X chromosome , 1991, Nature.

[77]  Carolyn J. Brown,et al.  Localization of the X inactivation centre on the human X chromosome in Xq13 , 1991, Nature.

[78]  Carolyn J. Brown,et al.  A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome , 1991, Nature.

[79]  E. Dees,et al.  The product of the H19 gene may function as an RNA , 1990, Molecular and cellular biology.

[80]  V A Zakian,et al.  Structure and function of telomeres. , 1989, Annual review of genetics.

[81]  Daniel S. Weld Comparative Analysis , 1987, IJCAI.

[82]  S. Rastan Non-random X-chromosome inactivation in mouse X-autosome translocation embryos--location of the inactivation centre. , 1983, Journal of embryology and experimental morphology.

[83]  K. Ikemura Development and application , 1971 .

[84]  M. Lyon Gene Action in the X-chromosome of the Mouse (Mus musculus L.) , 1961, Nature.