Tracing the origin of the compensasome: evolutionary history of DEAH helicase and MYST acetyltransferase gene families.

Dosage compensation in Drosophila is mediated by a complex of proteins and RNAs called the "compensasome." Two of the genes that encode proteins of the complex, maleless (mle) and males-absent-on-the-first (mof), respectively, belong to the DEAH helicase and MYST acetyltransferase gene families. We performed comprehensive phylogenetic and structural analyses to determine the evolutionary histories of these two gene families and thus to better understand the origin of the compensasome. All of the members of the DEAH and MYST families of the completely sequenced Saccharomyces cerevisiae and Caenorhabditis elegans genomes, as well as those so far (June 2000) found in Drosophila melanogaster (for which the euchromatic part of the genome has also been fully sequenced) and Homo sapiens, were analyzed. We describe a total of 39 DEAH helicases in these four species. Almost all of them can be grouped in just three main branches. The first branch includes the yeast PRP2, PRP16, PRP22, and PRP43 splicing factors and their orthologs in animal species. Each PRP gene has a single ortholog in metazoans. The second branch includes just four genes, found in yeast (Ecm16) and Drosophila (kurz) and their orthologs in humans and Caenorhabditis. The third branch includes (1) a single yeast gene (YLR419w); (2) six Drosophila genes, including maleless and spindle-E/homeless; (3) four human genes, among them the ortholog of maleless, which encodes RNA helicase A; and (4) three C. elegans genes, including orthologs of maleless and spindle-E. Thus, this branch has largely expanded in metazoans. We also show that, for the whole DEAH family, only MLE and its metazoan orthologs have acquired new protein domains since the fungi/animals split. We found a total of 17 MYST family proteins in the four analyzed species. We determined putative orthologs of mof in both C. elegans and H. sapiens, and we show that the most likely ortholog in yeast is the Sas2 gene. Moreover, a paralog of mof exists in Drosophila. All of these results, together with those found for a third member of the compensasome, msl-3, suggest that this complex emerged after the fungi/animals split and that it may be present in mammalian species. Both gene duplication and the acquisition of new protein modules may have played important roles in the origin of the compensasome.

[1]  A. Eisen,et al.  A novel DEAD-box RNA helicase exhibits high sequence conservation from yeast to humans. , 1998, Biochimica et biophysica acta.

[2]  Y. Shimura,et al.  Identification of a putative RNA helicase (HRH1), a human homolog of yeast Prp22 , 1994, Molecular and cellular biology.

[3]  N. Bertos,et al.  Identification of a Human Histone Acetyltransferase Related to Monocytic Leukemia Zinc Finger Protein* , 1999, The Journal of Biological Chemistry.

[4]  K. Manova,et al.  RNA helicase A is essential for normal gastrulation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[5]  B. S. Baker,et al.  Dosage compensation in Drosophila. , 1994, Annual review of genetics.

[6]  F. Grosse,et al.  Molecular Cloning of the Gene Encoding Nuclear DNA Helicase II. A BOVINE HOMOLOGUE OF HUMAN RNA HELICASE A AND DROSOPHILA Mle PROTEIN (*) , 1995, The Journal of Biological Chemistry.

[7]  R. Kelley,et al.  The role of chromosomal RNAs in marking the X for dosage compensation. , 2000, Current opinion in genetics & development.

[8]  D. St Johnston,et al.  Oocyte determination and the origin of polarity in Drosophila: the role of the spindle genes. , 1997, Development.

[9]  Ronald L. Davis,et al.  Epigenetic Spreading of the Drosophila Dosage Compensation Complex from roX RNA Genes into Flanking Chromatin , 1999, Cell.

[10]  C. Cole,et al.  Dbp5p/Rat8p is a yeast nuclear pore‐associated DEAD‐box protein essential for RNA export , 1998, The EMBO journal.

[11]  E. Koonin,et al.  Male‐specific lethal 2, a dosage compensation gene of Drosophila, undergoes sex‐specific regulation and encodes a protein with a RING finger and a metallothionein‐like cysteine cluster. , 1995, The EMBO journal.

[12]  A. Wagner,et al.  Evolution of gene networks by gene duplications: a mathematical model and its implications on genome organization. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[13]  B. S. Baker,et al.  The msl-2 dosage compensation gene of Drosophila encodes a putative DNA-binding protein whose expression is sex specifically regulated by Sex-lethal. , 1995, Development.

[14]  J. Kimble,et al.  The mog-1 gene is required for the switch from spermatogenesis to oogenesis in Caenorhabditis elegans. , 1993, Genetics.

[15]  J. Ahringer,et al.  Repression by the 3′ UTR of fem‐3, asex‐determining gene, relies on a ubiquitous mog‐dependent control in Caenorhabditis elegans , 1998, The EMBO journal.

[16]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[17]  B. Meyer,et al.  Sex in the wormcounting and compensating X-chromosome dose. , 2000, Trends in genetics : TIG.

[18]  G. Crabtree,et al.  Diversity and specialization of mammalian SWI/SNF complexes. , 1996, Genes & development.

[19]  C. Disteche,et al.  The translocation t(8;16)(p11;p13) of acute myeloid leukaemia fuses a putative acetyltransferase to the CREB–binding protein , 1996, Nature Genetics.

[20]  J. Lucchesi.  Dosage compensation: roX marks the spot , 1999, Current Biology.

[21]  C. Lloréns,et al.  Ty3/Gypsy retrotransposons: description of new Arabidopsis thaliana elements and evolutionary perspectives derived from comparative genomic data. , 2000, Molecular biology and evolution.

[22]  J. Lucchesi,et al.  mof, a putative acetyl transferase gene related to the Tip60 and MOZ human genes and to the SAS genes of yeast, is required for dosage compensation in Drosophila , 1997, The EMBO journal.

[23]  Julie Dawn Thompson,et al.  Detection of dsRNA-binding domains in RNA helicase A and Drosophila maleless: implications for monomeric RNA helicases , 1994, Nucleic Acids Res..

[24]  M. Kuroda,et al.  Complex formation by the Drosophila MSL proteins: role of the MSL2 RING finger in protein complex assembly , 1998, The EMBO journal.

[25]  M. Kuroda,et al.  The male-specific lethal-one (msl-1) gene of Drosophila melanogaster encodes a novel protein that associates with the X chromosome in males. , 1993, Genetics.

[26]  Hugh B. Nicholas,et al.  GeneDoc: a tool for editing and annotating multiple sequence alignments , 1997 .

[27]  P. Becker,et al.  Chromatin-remodeling factors: machines that regulate? , 1998, Current opinion in cell biology.

[28]  C. Allis,et al.  The Drosophila MSL Complex Acetylates Histone H4 at Lysine 16, a Chromatin Modification Linked to Dosage Compensation , 2000, Molecular and Cellular Biology.

[29]  B. Stillman,et al.  Histone Acetyltransferase HBO1 Interacts with the ORC1 Subunit of the Human Initiator Protein* , 1999, The Journal of Biological Chemistry.

[30]  J. de la Cruz,et al.  Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. , 1999, Trends in biochemical sciences.

[31]  M. Kuroda,et al.  Acetylated histone H4 on the male X chromosome is associated with dosage compensation in Drosophila. , 1994, Genes & development.

[32]  B. S. Baker,et al.  The evolution of dosage‐compensation mechanisms , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[33]  E. Koonin,et al.  The chromo superfamily: new members, duplication of the chromo domain and possible role in delivering transcription regulators to chromatin. , 1995, Nucleic acids research.

[34]  C. Berg,et al.  Homeless is required for RNA localization in Drosophila oogenesis and encodes a new member of the DE-H family of RNA-dependent ATPases. , 1995, Genes & development.

[35]  B. S. Baker,et al.  The dosage compensation system of Drosophila is co-opted by newly evolved X chromosomes , 1996, Nature.

[36]  R. Reed,et al.  Human homologs of yeast Prp16 and Prp17 reveal conservation of the mechanism for catalytic step II of pre‐mRNA splicing , 1998, The EMBO journal.

[37]  M. Kuroda,et al.  The NTPase/helicase activities of Drosophila maleless, an essential factor in dosage compensation , 1997, The EMBO journal.

[38]  B. S. Baker,et al.  Origin and evolution of the regulatory gene male-specific lethal-3. , 2000, Molecular biology and evolution.

[39]  S. Morris,et al.  Metazoan phylogenies: falling into place or falling to pieces? A palaeontological perspective. , 1998, Current opinion in genetics & development.

[40]  Jun Qin,et al.  Involvement of the TIP60 Histone Acetylase Complex in DNA Repair and Apoptosis , 2000, Cell.

[41]  D. Stillman,et al.  Multiple links between the NuA4 histone acetyltransferase complex and epigenetic control of transcription. , 2000, Molecular cell.

[42]  M Gribskov,et al.  Translational initiation factors IF-1 and eIF-2 alpha share an RNA-binding motif with prokaryotic ribosomal protein S1 and polynucleotide phosphorylase. , 1992, Gene.

[43]  L. Pillus,et al.  Yeast SAS silencing genes and human genes associated with AML and HIV–1 Tat interactions are homologous with acetyltransferases , 1996, Nature Genetics.

[44]  B. Turner,et al.  Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei , 1992, Cell.

[45]  B. S. Baker,et al.  The maleless protein associates with the X chromosome to regulate dosage compensation in drosophila , 1991, Cell.

[46]  Yan Liu,et al.  Dbp5p, a cytosolic RNA helicase, is required for poly(A)+ RNA export , 1998, The EMBO journal.

[47]  K. Kuma,et al.  Evolution of gene families and relationship with organismal evolution: rapid divergence of tissue-specific genes in the early evolution of chordates. , 1996, Molecular biology and evolution.

[48]  M. J. Scott,et al.  MSL1 plays a central role in assembly of the MSL complex, essential for dosage compensation in Drosophila , 2000, The EMBO journal.

[49]  R. Rosli,et al.  Requiem: a novel zinc finger gene essential for apoptosis in myeloid cells. , 1994, The Journal of biological chemistry.

[50]  J. Parvin,et al.  BRCA1 protein is linked to the RNA polymerase II holoenzyme complex via RNA helicase A , 1998, Nature Genetics.

[51]  P. Grant,et al.  NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM‐related cofactor Tra1p , 1999, The EMBO journal.

[52]  J. Lucchesi,et al.  A new human member of the MYST family of histone acetyl transferases with high sequence similarity to Drosophila MOF. , 2000, Biochimica et biophysica acta.

[53]  D. Sankoff,et al.  Comparable rates of gene loss and functional divergence after genome duplications early in vertebrate evolution. , 1997, Genetics.

[54]  R. Kelley,et al.  Ordered assembly of roX RNAs into MSL complexes on the dosage-compensated X chromosome in Drosophila , 2000, Current Biology.

[55]  C. Allis,et al.  ESA1 is a histone acetyltransferase that is essential for growth in yeast. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Mark Proctor,et al.  The Solution Structure of the S1 RNA Binding Domain: A Member of an Ancient Nucleic Acid–Binding Fold , 1997, Cell.

[57]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[58]  Jeffrey D. Parvin,et al.  RNA Helicase A Mediates Association of CBP with RNA Polymerase II , 1997, Cell.

[59]  R. Reenan,et al.  The mlenapts RNA Helicase Mutation in Drosophila Results in a Splicing Catastrophe of the para Na+ Channel Transcript in a Region of RNA Editing , 2000, Neuron.

[60]  J. Conboy,et al.  Cloning of mDEAH9, a putative RNA helicase and mammalian homologue of Saccharomyces cerevisiae splicing factor Prp43. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[61]  B. S. Baker,et al.  napts , a Mutation affecting sodium channel activity in Drosophila, Is an allele of mle a regulator of X chromosome transcription , 1991, Cell.

[62]  A. Stewart,et al.  The chromo shadow domain, a second chromo domain in heterochromatin-binding protein 1, HP1. , 1995, Nucleic acids research.

[63]  V. Solovyev,et al.  Expression of Msl-2 causes assembly of dosage compensation regulators on the X chromosomes and female lethality in Drosophila , 1995, Cell.

[64]  P. Becker,et al.  Activation of transcription through histone H4 acetylation by MOF, an acetyltransferase essential for dosage compensation in Drosophila. , 2000, Molecular cell.

[65]  Eckhard Jankowsky,et al.  The DExH/D protein family database , 2000, Nucleic Acids Res..

[66]  T. Gibson,et al.  The PHD finger: implications for chromatin-mediated transcriptional regulation. , 1995, Trends in biochemical sciences.

[67]  J. Lucchesi,et al.  Dosage compensation in flies and worms: the ups and downs of X-chromosome regulation. , 1998, Current opinion in genetics & development.

[68]  B. S. Baker,et al.  The rox1 and rox2 RNAs are essential components of the compensasome, which mediates dosage compensation in Drosophila. , 1999, Molecular cell.

[69]  J. Hurwitz,et al.  Human RNA helicase A is homologous to the maleless protein of Drosophila. , 1993, The Journal of biological chemistry.

[70]  F. Wong-Staal,et al.  A Novel Shuttle Protein Binds to RNA Helicase A and Activates the Retroviral Constitutive Transport Element* , 2000, The Journal of Biological Chemistry.

[71]  D. McDonald,et al.  The Carboxyl Terminus of RNA Helicase A Contains a Bidirectional Nuclear Transport Domain , 1999, Molecular and Cellular Biology.

[72]  B. Meyer,et al.  Vive la différence: males vs females in flies vs worms. , 1996, Annual review of genetics.

[73]  J. Kimble,et al.  The Caenorhabditis elegans Sex Determination Gene mog-1 Encodes a Member of the DEAH-Box Protein Family , 1999, Molecular and Cellular Biology.

[74]  J. Kimble,et al.  The hermaphrodite sperm/oocyte switch requires the Caenorhabditis elegans homologs of PRP2 and PRP22. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[75]  W. Michael.  Nucleocytoplasmic shuttling signals: two for the price of one. , 2000, Trends in cell biology.

[76]  T. Schedl,et al.  More mog genes that influence the switch from spermatogenesis to oogenesis in the hermaphrodite germ line of Caenorhabditis elegans. , 1993, Developmental genetics.

[77]  V. Meller.  Dosage compensation: making 1X equal 2X. , 2000, Trends in cell biology.

[78]  Roderic D. M. Page,et al.  TreeView: an application to display phylogenetic trees on personal computers , 1996, Comput. Appl. Biosci..