A new method to remove hybridization bias for interspecies comparison of global gene expression profiles uncovers an association between mRNA sequence divergence and differential gene expression in Xenopus

The recent sequencing of a large number of Xenopus tropicalis expressed sequences has allowed development of a high-throughput approach to study Xenopus global RNA gene expression. We examined the global gene expression similarities and differences between the historically significant Xenopus laevis model system and the increasingly used X.tropicalis model system and assessed whether an X.tropicalis microarray platform can be used for X.laevis. These closely related species were also used to investigate a more general question: is there an association between mRNA sequence divergence and differences in gene expression levels? We carried out a comprehensive comparison of global gene expression profiles using microarrays of different tissues and developmental stages of X.laevis and X.tropicalis. We (i) show that the X.tropicalis probes provide an efficacious microarray platform for X.laevis, (ii) describe methods to compare interspecies mRNA profiles that correct differences in hybridization efficiency and (iii) show independently of hybridization bias that as mRNA sequence divergence increases between X.laevis and X.tropicalis differences in mRNA expression levels also increase.

[1]  Lewis Wolpert,et al.  Principles of Development , 1997 .

[2]  Nancy Papalopulu,et al.  Defining a large set of full-length clones from a Xenopus tropicalis EST project. , 2004, Developmental biology.

[3]  R. Irizarry,et al.  In vitro identification and in silico utilization of interspecies sequence similarities using GeneChip® technology , 2005, BMC Genomics.

[4]  Mark Gerstein,et al.  Multi-species microarrays reveal the effect of sequence divergence on gene expression profiles. , 2005, Genome research.

[5]  J. Gurdon.  Perspective on the Xenopus field , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[6]  D. Botstein,et al.  Cluster analysis and display of genome-wide expression patterns. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Principles of Development. Lewis Wolpert , Rosa Beddington , Jeremy Brockes , Thomas Jessell , Peter Lawrence , Elliot Meyerowitz , 1999 .

[8]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[9]  Ka Yee Yeung,et al.  Bayesian mixture model based clustering of replicated microarray data , 2004, Bioinform..

[10]  S. Karlin,et al.  Methods for assessing the statistical significance of molecular sequence features by using general scoring schemes. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[11]  A. Wilson,et al.  Albumin phylogeny for clawed frogs (Xenopus). , 1977, Science.

[12]  J. Slack.  Essential Developmental Biology , 2001 .

[13]  A Xenopus tropicalis oligonucleotide microarray works across species using RNA from Xenopus laevis , 2005, Mechanisms of Development.

[14]  J. Faber,et al.  Normal table of Xenopus laevis (Daudin). A systematical and chronological survey of the development from the fertilized egg till the end of metamorphosis. , 1956 .

[15]  Nancy Papalopulu,et al.  Techniques and probes for the study of Xenopus tropicalis development , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[16]  Ken W. Y. Cho,et al.  Microarray-based identification of VegT targets in Xenopus , 2005, Mechanisms of Development.

[17]  Yoav Benjamini,et al.  Identifying differentially expressed genes using false discovery rate controlling procedures , 2003, Bioinform..

[18]  Ken W. Y. Cho,et al.  Global gene expression profiling and cluster analysis in Xenopus laevis , 2005, Mechanisms of Development.

[19]  Mario Medvedovic,et al.  Expression of genes in the TGF-beta signaling pathway is significantly deregulated in smooth muscle cells from aorta of aryl hydrocarbon receptor knockout mice. , 2004, Toxicology and applied pharmacology.

[20]  Zhining Wang,et al.  Identification and utilization of inter-species conserved (ISC) probesets on Affymetrix human GeneChip® platforms for the optimization of the assessment of expression patterns in non human primate (NHP) samples , 2004, BMC Bioinformatics.

[21]  F. B. Pickett,et al.  Splitting pairs: the diverging fates of duplicated genes , 2002, Nature Reviews Genetics.

[22]  A. Brivanlou,et al.  Gene profiling during neural induction in Xenopus laevis: regulation of BMP signaling by post-transcriptional mechanisms and TAB3, a novel TAK1-binding protein , 2002, Development.

[23]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[24]  H. Lehrach,et al.  Cross-species hybridisation of human and bovine orthologous genes on high density cDNA microarrays , 2004, BMC Genomics.

[25]  Colin D. Meiklejohn,et al.  Sex-Dependent Gene Expression and Evolution of the Drosophila Transcriptome , 2003, Science.

[26]  A. Hughes,et al.  Evolution of duplicate genes in a tetraploid animal, Xenopus laevis. , 1993, Molecular biology and evolution.

[27]  Mario Medvedovic,et al.  Different global gene expression profiles in benzo[a]pyrene-and dioxin-treated vascular smooth muscle cells of AHR-knockout and wild-type mice , 2007, Cardiovascular Toxicology.

[28]  L. Zimmerman,et al.  Xenopus, the next generation: X. Tropicalis genetics and genomics , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[29]  E. Amaya,et al.  Frog genetics: Xenopus tropicalis jumps into the future. , 1998, Trends in genetics : TIG.

[30]  Pierre R. Bushel,et al.  Assessing Gene Significance from cDNA Microarray Expression Data via Mixed Models , 2001, J. Comput. Biol..

[31]  A. Brivanlou,et al.  Microarray-based analysis of early development in Xenopus laevis. , 2001, Developmental biology.

[32]  Mario Medvedovic,et al.  Microarray results improve significantly as hybridization approaches equilibrium. , 2004, BioTechniques.

[33]  Mario Medvedovic,et al.  Bayesian infinite mixture model based clustering of gene expression profiles , 2002, Bioinform..

[34]  S. Pääbo,et al.  A Neutral Model of Transcriptome Evolution , 2004, PLoS biology.

[35]  T. Jukes,et al.  The neutral theory of molecular evolution. , 2000, Genetics.

[36]  Douglas A. Hosack,et al.  Identifying biological themes within lists of genes with EASE , 2003, Genome Biology.