Conservation and divergence in Toll-like receptor 4-regulated gene expression in primary human versus mouse macrophages
Evolutionary change in gene expression is generally considered to be a major driver of phenotypic differences between species. We investigated innate immune diversification by analyzing interspecies differences in the transcriptional responses of primary human and mouse macrophages to the Toll-like...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 109; no. 16; pp. 5925 - 5926 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
17.04.2012
National Acad Sciences |
| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0027-8424 1091-6490 1091-6490 |
| DOI | 10.1073/pnas.1110156109 |
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| Abstract | Evolutionary change in gene expression is generally considered to be a major driver of phenotypic differences between species. We investigated innate immune diversification by analyzing interspecies differences in the transcriptional responses of primary human and mouse macrophages to the Toll-like receptor (TLR)–4 agonist lipopolysaccharide (LPS). By using a custom platform permitting cross-species interrogation coupled with deep sequencing of mRNA 5′ ends, we identified extensive divergence in LPS-regulated orthologous gene expression between humans and mice (24% of orthologues were identified as “divergently regulated”). We further demonstrate concordant regulation of human-specific LPS target genes in primary pig macrophages. Divergently regulated orthologues were enriched for genes encoding cellular “inputs” such as cell surface receptors (e.g., TLR6, IL-7Rα) and functional “outputs” such as inflammatory cytokines/chemokines (e.g., CCL20, CXCL13). Conversely, intracellular signaling components linking inputs to outputs were typically concordantly regulated. Functional consequences of divergent gene regulation were confirmed by showing LPS pretreatment boosts subsequent TLR6 responses in mouse but not human macrophages, in keeping with mouse-specific TLR6 induction. Divergently regulated genes were associated with a large dynamic range of gene expression, and specific promoter architectural features (TATA box enrichment, CpG island depletion). Surprisingly, regulatory divergence was also associated with enhanced interspecies promoter conservation. Thus, the genes controlled by complex, highly conserved promoters that facilitate dynamic regulation are also the most susceptible to evolutionary change. |
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| AbstractList | Evolutionary change in gene expression is generally considered to be a major driver of phenotypic differences between species. We investigated innate immune diversification by analyzing interspecies differences in the transcriptional responses of primary human and mouse macrophages to the Toll-like receptor (TLR)-4 agonist lipopolysaccharide (LPS). By using a custom platform permitting cross-species interrogation coupled with deep sequencing of mRNA 5' ends, we identified extensive divergence in LPS-regulated orthologous gene expression between humans and mice (24% of orthologues were identified as "divergently regulated"). We further demonstrate concordant regulation of human-specific LPS target genes in primary pig macrophages. Divergently regulated orthologues were enriched for genes encoding cellular "inputs" such as cell surface receptors (e.g., TLR6, IL-7Rα) and functional "outputs" such as inflammatory cytokines/chemokines (e.g., CCL20, CXCL13). Conversely, intracellular signaling components linking inputs to outputs were typically concordantly regulated. Functional consequences of divergent gene regulation were confirmed by showing LPS pretreatment boosts subsequent TLR6 responses in mouse but not human macrophages, in keeping with mouse-specific TLR6 induction. Divergently regulated genes were associated with a large dynamic range of gene expression, and specific promoter architectural features (TATA box enrichment, CpG island depletion). Surprisingly, regulatory divergence was also associated with enhanced interspecies promoter conservation. Thus, the genes controlled by complex, highly conserved promoters that facilitate dynamic regulation are also the most susceptible to evolutionary change. [PUBLICATION ABSTRACT] Evolutionary change in gene expression is generally considered to be a major driver of phenotypic differences between species. We investigated innate immune diversification by analyzing interspecies differences in the transcriptional responses of primary human and mouse macrophages to the Toll-like receptor (TLR)–4 agonist lipopolysaccharide (LPS). By using a custom platform permitting cross-species interrogation coupled with deep sequencing of mRNA 5' ends, we identified extensive divergence in LPS-regulated orthologous gene expression between humans and mice (24% of orthologues were identified as "divergently regulated"). We further demonstrate concordant regulation of human-specific LPS target genes in primary pig macrophages. Divergently regulated orthologues were enriched for genes encoding cellular "inputs" such as cell surface receptors (e.g., TLR6, IL-7Rα) and functional "outputs" such as inflammatory cytokines/chemokines (e.g., CCL20, CXCL13). Conversely, intracellular signaling components linking inputs to outputs were typically concordantly regulated. Functional consequences of divergent gene regulation were confirmed by showing LPS pretreatment boosts subsequent TLR6 responses in mouse but not human macrophages, in keeping with mouse-specific TLR6 induction. Divergently regulated genes were associated with a large dynamic range of gene expression, and specific promoter architectural features (TATA box enrichment, CpG island depletion). Surprisingly, regulatory divergence was also associated with enhanced interspecies promoter conservation. Thus, the genes controlled by complex, highly conserved promoters that facilitate dynamic regulation are also the most susceptible to evolutionary change. Evolutionary change in gene expression is generally considered to be a major driver of phenotypic differences between species. We investigated innate immune diversification by analyzing interspecies differences in the transcriptional responses of primary human and mouse macrophages to the Toll-like receptor (TLR)-4 agonist lipopolysaccharide (LPS). By using a custom platform permitting cross-species interrogation coupled with deep sequencing of mRNA 5' ends, we identified extensive divergence in LPS-regulated orthologous gene expression between humans and mice (24% of orthologues were identified as "divergently regulated"). We further demonstrate concordant regulation of human-specific LPS target genes in primary pig macrophages. Divergently regulated orthologues were enriched for genes encoding cellular "inputs" such as cell surface receptors (e.g., TLR6, IL-7R alpha ) and functional "outputs" such as inflammatory cytokines/chemokines (e.g., CCL20, CXCL13). Conversely, intracellular signaling components linking inputs to outputs were typically concordantly regulated. Functional consequences of divergent gene regulation were confirmed by showing LPS pretreatment boosts subsequent TLR6 responses in mouse but not human macrophages, in keeping with mouse-specific TLR6 induction. Divergently regulated genes were associated with a large dynamic range of gene expression, and specific promoter architectural features (TATA box enrichment, CpG island depletion). Surprisingly, regulatory divergence was also associated with enhanced interspecies promoter conservation. Thus, the genes controlled by complex, highly conserved promoters that facilitate dynamic regulation are also the most susceptible to evolutionary change. Evolutionary change in gene expression is generally considered to be a major driver of phenotypic differences between species. We investigated innate immune diversification by analyzing interspecies differences in the transcriptional responses of primary human and mouse macrophages to the Toll-like receptor (TLR)–4 agonist lipopolysaccharide (LPS). By using a custom platform permitting cross-species interrogation coupled with deep sequencing of mRNA 5′ ends, we identified extensive divergence in LPS-regulated orthologous gene expression between humans and mice (24% of orthologues were identified as “divergently regulated”). We further demonstrate concordant regulation of human-specific LPS target genes in primary pig macrophages. Divergently regulated orthologues were enriched for genes encoding cellular “inputs” such as cell surface receptors (e.g., TLR6, IL-7Rα) and functional “outputs” such as inflammatory cytokines/chemokines (e.g., CCL20, CXCL13). Conversely, intracellular signaling components linking inputs to outputs were typically concordantly regulated. Functional consequences of divergent gene regulation were confirmed by showing LPS pretreatment boosts subsequent TLR6 responses in mouse but not human macrophages, in keeping with mouse-specific TLR6 induction. Divergently regulated genes were associated with a large dynamic range of gene expression, and specific promoter architectural features (TATA box enrichment, CpG island depletion). Surprisingly, regulatory divergence was also associated with enhanced interspecies promoter conservation. Thus, the genes controlled by complex, highly conserved promoters that facilitate dynamic regulation are also the most susceptible to evolutionary change. We have performed the most stringent human–mouse comparison of innate immune gene regulation and promoter architecture reported to date, as far as we are aware. Importantly, our findings show that transcriptional plasticity in response to a stimulus within a species and variability between species are intrinsically linked. The capacity for expression variation in both cases is associated with specific promoter properties. Our analyses indicate that dynamically regulated genes, controlled by complex and highly conserved promoters, are exquisitely sensitive to evolutionary changes. Functional analyses of TLR4 target genes uniquely regulated in human macrophages are likely to provide important insights into human immunology that are not able to be observed in mouse models of infectious and inflammatory disease. We next hypothesized that interspecies evolution in gene regulation would be associated with specific promoter architectural features. Indeed, we found that, compared with non-DR genes, DR gene promoters were significantly enriched for the presence of one regulatory feature, the TATA box motif, and significantly depleted for another, CpG islands. Work from others has associated such TATA-containing, CpG-island-less promoter architectures with complex promoters that integrate a high degree of regulatory input. Such associations are consistent with our own data. TATA enrichment and CpG island depletion were also associated with the magnitude of change in gene expression over the course of a response to LPS stimulation (i.e., a large dynamic range). In keeping with this, a gene's dynamic range of expression was also clearly associated with regulatory divergence, such that the most highly regulated genes were among the most evolvable, and vice versa. In total, these results indicate that complex, sensitive promoters confer an inherent plasticity in gene transcription, in the magnitude of mRNA response to LPS and in expression divergence between species ( Fig. P1 ). We precisely defined macrophage transcription start sites (TSSs) by using genome-wide Cap Analysis of Gene Expression ( 3 , 4 ), a method that identifies mRNA 5′ ends by deep sequencing of transcript fragments (i.e., tags) trapped by the 5′ cap modification. This was performed in parallel with expression profiling of LPS-regulated genes by using our focused, custom microarray ( Fig. P1 ). Cap Analysis of Gene Expression analysis yielded 5.3 million human macrophage and 2.6 million mouse macrophage tags that define TSSs, and therefore proximal promoter regions. Hypothesizing that evolution in these gene-regulatory sequences drives regulatory divergence, we analyzed human–mouse sequence conservation in promoters of DR vs. non-DR genes. Several approaches confirmed the very surprising finding that promoters driving DR genes are demonstrably more conserved than non-DR promoters: ( i ) the region surrounding DR gene TSSs exhibited a greater fraction of nucleotides that align between human and mouse, compared with non-DR genes; ( ii ) DR genes were significantly associated with conserved, noncoding regions compared with non-DR genes; and ( iii ) core promoter sequences of DR genes have undergone fewer nucleotide substitutions than non-DR genes over the approximately 70 million years since humans and mice diverged. Together, these data indicate that DR promoter sequences are under greater evolutionary constraint than those of non-DR genes. This in turn supports the conclusion the promoters controlling DR gene expression are highly complex, that is, they contain more functional sequences that have been conserved throughout evolution ( Fig. P1 ). Specific classes of molecules appeared to be under differential evolutionary pressure. Intracellular factors that participate in the TLR signaling pathway were generally conserved in their regulation, whereas secreted molecules and membrane proteins, such as the TLRs themselves, showed widespread regulatory divergence. Functional consequences of divergent gene regulation were confirmed by demonstrating that LPS pretreatment boosts subsequent TLR6 responses in mouse but not in human macrophages, in keeping with mouse-specific TLR6 induction by LPS. We also validated human-specific induction of the IL-7 receptor, and secretion of the cytokines CCL20 and CXCL13, which are likely to further modulate immune defense in vivo. Of particular interest, given the evolutionary arms race between host and pathogen, our analyses identified regulatory divergence in orthologues with antimicrobial functions (e.g., LCN2 and P2X7R ). To determine the extent of interspecies regulatory divergence in this setting, we designed custom microarray platforms that enable interspecies comparisons (human vs. mouse) of LPS-regulated gene (mRNA) expression. We adopted a stringent approach to identifying regulatory divergence, requiring any gene classified as “divergently regulated” (DR) to exhibit significantly divergent regulation between human macrophages and two different mouse macrophage populations. We directly compared regulation of “orthologous” human and mouse genes, that is, pairs of genes in the two species that evolved from the same ancestral gene. We found that 23.9% (598 of 2,505) of LPS-regulated orthologous gene pairs exhibited significant regulatory divergence between species, whereas significant regulatory conservation was apparent for 30.3% (759 of 2,505) of orthologues. Interestingly, we demonstrate that human-specific LPS-target genes are concordantly regulated in primary pig macrophages. Macrophages are cells of the immune system that use pattern-recognition receptors such as Toll-like receptors (TLRs) to recognize distinct microbial products. For example, TLR4 detects LPS, a cell-wall component of Gram-negative bacteria, triggering a signaling cascade that leads to changes in gene expression, activating immune defenses ( 1 ). Although the TLR4 signaling pathway is broadly conserved between humans and mice, several examples of divergent gene regulation downstream of TLR stimulation have been described ( 2 ). Moreover, humans are more sensitive to LPS-mediated toxicity than mice ( 2 ), suggesting fundamental differences in the species’ responses to this bacterial stimulus. However, the extent of regulatory divergence and the underlying evolutionary mechanisms have not been investigated. Mice are widely used as experimental models for human immunology, but these species are distant relatives. Moreover, as rapidly evolving pathogens exert intense pressure on the immune system to coevolve, substantial differences between these species’ immune systems are likely. To help address these differences, we compared regulated gene expression in human and mouse immune cells in response to the archetypal inflammatory stimulus lipopolysaccharide (LPS). We identified marked divergence in gene regulation between species ( http://www.macgate.qfab.org/index.htm ), and found that dynamically regulated genes are exquisitely sensitive to evolutionary changes. Our study maps the strengths and weaknesses of the mouse model and identifies human-specific responses as therapeutic targets for infectious and inflammatory diseases. Evolutionary change in gene expression is generally considered to be a major driver of phenotypic differences between species. We investigated innate immune diversification by analyzing interspecies differences in the transcriptional responses of primary human and mouse macrophages to the Toll-like receptor (TLR)-4 agonist lipopolysaccharide (LPS). By using a custom platform permitting cross-species interrogation coupled with deep sequencing of mRNA 5' ends, we identified extensive divergence in LPS-regulated orthologous gene expression between humans and mice (24% of orthologues were identified as "divergently regulated"). We further demonstrate concordant regulation of human-specific LPS target genes in primary pig macrophages. Divergently regulated orthologues were enriched for genes encoding cellular "inputs" such as cell surface receptors (e.g., TLR6, IL-7Rα) and functional "outputs" such as inflammatory cytokines/chemokines (e.g., CCL20, CXCL13). Conversely, intracellular signaling components linking inputs to outputs were typically concordantly regulated. Functional consequences of divergent gene regulation were confirmed by showing LPS pretreatment boosts subsequent TLR6 responses in mouse but not human macrophages, in keeping with mouse-specific TLR6 induction. Divergently regulated genes were associated with a large dynamic range of gene expression, and specific promoter architectural features (TATA box enrichment, CpG island depletion). Surprisingly, regulatory divergence was also associated with enhanced interspecies promoter conservation. Thus, the genes controlled by complex, highly conserved promoters that facilitate dynamic regulation are also the most susceptible to evolutionary change.Evolutionary change in gene expression is generally considered to be a major driver of phenotypic differences between species. We investigated innate immune diversification by analyzing interspecies differences in the transcriptional responses of primary human and mouse macrophages to the Toll-like receptor (TLR)-4 agonist lipopolysaccharide (LPS). By using a custom platform permitting cross-species interrogation coupled with deep sequencing of mRNA 5' ends, we identified extensive divergence in LPS-regulated orthologous gene expression between humans and mice (24% of orthologues were identified as "divergently regulated"). We further demonstrate concordant regulation of human-specific LPS target genes in primary pig macrophages. Divergently regulated orthologues were enriched for genes encoding cellular "inputs" such as cell surface receptors (e.g., TLR6, IL-7Rα) and functional "outputs" such as inflammatory cytokines/chemokines (e.g., CCL20, CXCL13). Conversely, intracellular signaling components linking inputs to outputs were typically concordantly regulated. Functional consequences of divergent gene regulation were confirmed by showing LPS pretreatment boosts subsequent TLR6 responses in mouse but not human macrophages, in keeping with mouse-specific TLR6 induction. Divergently regulated genes were associated with a large dynamic range of gene expression, and specific promoter architectural features (TATA box enrichment, CpG island depletion). Surprisingly, regulatory divergence was also associated with enhanced interspecies promoter conservation. Thus, the genes controlled by complex, highly conserved promoters that facilitate dynamic regulation are also the most susceptible to evolutionary change. |
| Author | Taylor, Martin S. Carninci, Piero Labzin, Larisa I. Masterman, Kelly-Anne Schroder, Kate Baillie, John Kenneth Le Cao, Kim-Anh Suzuki, Harukazu McLachlan, Geoffrey J. Gongora, Milena Hayashizaki, Yoshihide Daub, Carsten O. Sweet, Matthew J. Grimmond, Sean M. Irvine, Katharine M. Semple, Colin A. Lenhard, Boris Bokil, Nilesh J. Kapetanovic, Ronan Faulkner, Geoffrey J. Goldman, Nick Akalin, Altuna Kawaji, Hideya Hume, David A. Fairbairn, Lynsey |
| Author_xml | – sequence: 1 givenname: Kate surname: Schroder fullname: Schroder, Kate – sequence: 2 givenname: Katharine M. surname: Irvine fullname: Irvine, Katharine M. – sequence: 3 givenname: Martin S. surname: Taylor fullname: Taylor, Martin S. – sequence: 4 givenname: Nilesh J. surname: Bokil fullname: Bokil, Nilesh J. – sequence: 5 givenname: Kim-Anh surname: Le Cao fullname: Le Cao, Kim-Anh – sequence: 6 givenname: Kelly-Anne surname: Masterman fullname: Masterman, Kelly-Anne – sequence: 7 givenname: Larisa I. surname: Labzin fullname: Labzin, Larisa I. – sequence: 8 givenname: Colin A. surname: Semple fullname: Semple, Colin A. – sequence: 9 givenname: Ronan surname: Kapetanovic fullname: Kapetanovic, Ronan – sequence: 10 givenname: Lynsey surname: Fairbairn fullname: Fairbairn, Lynsey – sequence: 11 givenname: Altuna surname: Akalin fullname: Akalin, Altuna – sequence: 12 givenname: Geoffrey J. surname: Faulkner fullname: Faulkner, Geoffrey J. – sequence: 13 givenname: John Kenneth surname: Baillie fullname: Baillie, John Kenneth – sequence: 14 givenname: Milena surname: Gongora fullname: Gongora, Milena – sequence: 15 givenname: Carsten O. surname: Daub fullname: Daub, Carsten O. – sequence: 16 givenname: Hideya surname: Kawaji fullname: Kawaji, Hideya – sequence: 17 givenname: Geoffrey J. surname: McLachlan fullname: McLachlan, Geoffrey J. – sequence: 18 givenname: Nick surname: Goldman fullname: Goldman, Nick – sequence: 19 givenname: Sean M. surname: Grimmond fullname: Grimmond, Sean M. – sequence: 20 givenname: Piero surname: Carninci fullname: Carninci, Piero – sequence: 21 givenname: Harukazu surname: Suzuki fullname: Suzuki, Harukazu – sequence: 22 givenname: Yoshihide surname: Hayashizaki fullname: Hayashizaki, Yoshihide – sequence: 23 givenname: Boris surname: Lenhard fullname: Lenhard, Boris – sequence: 24 givenname: David A. surname: Hume fullname: Hume, David A. – sequence: 25 givenname: Matthew J. surname: Sweet fullname: Sweet, Matthew J. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22451944$$D View this record in MEDLINE/PubMed https://hal.inrae.fr/hal-04387254$$DView record in HAL |
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| Keywords | Innate immunity Inflammation evolution Transcriptional regulation Pattern-recognition receptor |
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| Notes | SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 Author contributions: K.S., K.M.I., M.S.T., D.A.H., and M.J.S. designed research; K.S., K.M.I., N.J.B., K.-A.M., L.I.L., R.K., and L.F. performed research; K.S., K.M.I., M.S.T., G.J.F., M.G., C.O.D., H.K., G.J.M., N.G., S.M.G., P.C., H.S., and Y.H. contributed new reagents/analytic tools; K.S., K.M.I., M.S.T., K.-A.L.C., C.A.S., A.A., J.K.B., B.L., D.A.H., and M.J.S. analyzed data; and K.S., K.M.I., M.S.T., D.A.H., and M.J.S. wrote the paper. Edited by Shizuo Akira, Osaka University, Osaka, Japan, and approved February 24, 2012 (received for review June 23, 2011) 1K.S., K.M.I., and M.S.T. contributed equally to this work. |
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| SubjectTerms | agonists Animals Biological Sciences Cell Line Cells, Cultured Chemokine CCL20 Chemokine CCL20 - genetics Chemokine CXCL13 Chemokine CXCL13 - genetics chemokines drug effects Evolution Evolution, Molecular Female Gene expression Gene Expression Profiling gene expression regulation Gene Expression Regulation - drug effects genes Genetic Variation genetics genomic islands high-throughput nucleotide sequencing Host-Pathogen Interactions Human subjects Humans Immunology Leukocytes Life Sciences lipopolysaccharides Lipopolysaccharides - pharmacology macrophages Macrophages - drug effects Macrophages - metabolism Macrophages - microbiology Male messenger RNA metabolism Mice Mice, Inbred BALB C Mice, Inbred C57BL Mice, Knockout microbiology Microbiology and Parasitology Oligonucleotide Array Sequence Analysis pharmacology physiology PNAS Plus PNAS PLUS (AUTHOR SUMMARIES) receptors Reverse Transcriptase Polymerase Chain Reaction Rodents Salmonella typhimurium Salmonella typhimurium - physiology Signal transduction Species Specificity Swine TATA box Toll-Like Receptor 4 Toll-Like Receptor 4 - agonists Toll-Like Receptor 4 - genetics |
| Title | Conservation and divergence in Toll-like receptor 4-regulated gene expression in primary human versus mouse macrophages |
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