Structure-function analysis of Hmo1 unveils an ancestral organization of HMG-Box factors involved in ribosomal DNA transcription from yeast to human

@article{Albert2013StructurefunctionAO,
  title={Structure-function analysis of Hmo1 unveils an ancestral organization of HMG-Box factors involved in ribosomal DNA transcription from yeast to human},
  author={Benjamin Albert and Christine Colleran and Isabelle L{\'e}ger-Silvestre and Axel Bernhard Berger and Christophe Dez and Christophe Normand and Jorge Perez-Fernandez and Brian McStay and Olivier Gadal},
  journal={Nucleic Acids Research},
  year={2013},
  volume={41},
  pages={10135 - 10149}
}
Ribosome biogenesis is a major metabolic effort for growing cells. In Saccharomyces cerevisiae, Hmo1, an abundant high-mobility group box protein (HMGB) binds to the coding region of the RNA polymerase I transcribed ribosomal RNAs genes and the promoters of ∼70% of ribosomal protein genes. In this study, we have demonstrated the functional conservation of eukaryotic HMGB proteins involved in ribosomal DNA (rDNA) transcription. We have shown that when expressed in budding yeast, human UBF1 and a… 

Figures from this paper

Oligomerization of Hmo1 mediated by box A is essential for DNA binding in vitro and in vivo
TLDR
The findings suggest that the principal role of box A is to assemble multiple box B in the appropriate orientation, thereby stabilizing the binding of Hmo1 to DNA and nucleating specific chromosomal architecture on its target genes.
Both HMG boxes in Hmo1 are essential for DNA binding in vitro and in vivo
TLDR
Characterization of Hmo1 mutants showed that the box A domain plays a pivotal role in DNA binding and may be required for the recognition of structural properties of target promoters that occur in native chromatin.
Conditional Inactivation of Upstream Binding Factor Reveals Its Epigenetic Functions and the Existence of a Somatic Nucleolar Precursor Body
TLDR
It is shown that UBF is essential for embryo development beyond morula and that it defines the active chromatin conformation of both gene and enhancer sequences, and arrest of rRNA synthesis does not suppress transcription of the 5S, tRNA or snRNA genes, nor expression of the several hundred mRNA genes implicated in ribosome biogenesis.
The C-terminal region of Net1 is an activator of RNA polymerase I transcription with conserved features from yeast to human
TLDR
It is found that the Pol I-stimulating function can be attributed to the very C-terminal region (CTR) of Net1, which was required for normal cell growth and Pol I recruitment to rRNA genes in vivo and sufficient to promote Pol I transcription in vitro.
HMGB Proteins as DNA Chaperones That Modulate Chromatin Activity
TLDR
The role that the HMBG proteins play in key intranuclear processes, including assembly of the preinitiation complex during transcription of ribosomal genes; transcription by RNA polymerases I, II, and III; recruitment of the SWI/SNF complex during recruitment of nonribosome genes; DNA repair; etc is discussed.
The high mobility group protein HMO1 functions as a linker histone in yeast
TLDR
That S. cerevisiae HMO1 protects linker DNA from nuclease digestion, a property also characteristic of mammalian linker histone H1, has implications for investigations of chromatin structure and function as well as for evolution of proteins with roles in chromatin compaction.
Molecular and functional analyses of the plant specific 3xHMG-box proteins expressed during mitosis/meiosis
TLDR
3xHMG-box proteins were found to associate with silenced A. thaliana NORs but also with some of the A. arenosa NORs, and construction of truncated and chimeric proteins suggested a function of the N-terminal domain for the specificity of 3xH MG-box1 for certain rDNA regions.
Fpr1, a primary target of rapamycin, functions as a transcription factor for ribosomal protein genes cooperatively with Hmo1 in Saccharomyces cerevisiae
TLDR
Extensive chromatin immunoprecipitation and ChIP-sequencing analyses revealed that Fpr1 associates specifically with the upstream activating sequences of nearly all RPG (ribosomal protein gene) promoters, presumably in a manner dependent on Rap1 (repressor/activator site binding protein 1).
Yeast HMO1: Linker Histone Reinvented
TLDR
HMO1 appears to have evolved a unique linker histone-like function involving the ability to stabilize both conventional nucleosome arrays as well as DNA regions characterized by low nucleosom density or the presence of noncanonical nucleosomes.
Characterization of nucleolus-associated chromatin domains during cellular aging and upon genetic inactivation of the Upstream Binding Factor protein
TLDR
The initial analyses suggest that NADs are stable units and their genomic maps show only minor differences between the population of proliferating and senescent IMR90 cells, and the nucleolus association of chromo- somal domains was mapped using comparative genomic hybridization on high-resolution microarrays.
...
...

References

SHOWING 1-10 OF 61 REFERENCES
Hmo1, an HMG‐box protein, belongs to the yeast ribosomal DNA transcription system
TLDR
Hmo1 overexpression suppresses rpa49‐Δ mutants lacking Rpa49, a non‐essential but conserved subunit of RNA polymerase I corresponding to the animal RNA polymerases I factor PAF53, and strongly increases de novo rRNA synthesis.
Assembly of Regulatory Factors on rRNA and Ribosomal Protein Genes in Saccharomyces cerevisiae
TLDR
The results show that HMO1 associates with the 35S rRNA gene in an RNA polymerase I-dependent manner and that RPG promoters can be classified into several distinct groups based on H MO1 abundance at the promoter and the HMO 1 dependence of FHL1 and/or RAP1 binding to the promoter.
Hmo1 Is Required for TOR-Dependent Regulation of Ribosomal Protein Gene Transcription
TLDR
It is shown here that Saccharomyces cerevisiae Hmo1 is directly involved in coordinating rDNA transcription by Pol I and RP gene expression by Pol II under the control of the TOR pathway.
Saccharomyces cerevisiae HMO1 interacts with TFIID and participates in start site selection by RNA polymerase II
Saccharomyces cerevisiae HMO1, a high mobility group B (HMGB) protein, associates with the rRNA locus and with the promoters of many ribosomal protein genes (RPGs). Here, the Sos recruitment system
An HMG Protein, Hmo1, Associates with Promoters of Many Ribosomal Protein Genes and throughout the rRNA Gene Locus in Saccharomyces cerevisiae
TLDR
Ch chromatin immunoprecipitation coupled with microarray analysis suggests that Hmo1 is required for the assembly of transcription factor complexes containing Fhl1 and Ifh1 at RP promoters and that proteins other than Fhl2 and ifh1 also play an important role in RP transcription.
RNA polymerase I associated factor 53 binds to the nucleolar transcription factor UBF and functions in specific rDNA transcription.
TLDR
It is suggested that PAF53 is involved in the formation of the initiation complex at the promoter by mediating the interaction between Pol I and UBF for the active rRNA synthesis.
Suppression of yeast RNA polymerase III mutations by FHL1, a gene coding for a fork head protein involved in rRNA processing.
TLDR
The isolation of FHL1 as a dosage-dependent suppressor suggests that rRNA processing depends on a still-unidentified RNA polymerase III transcript and plays a key role in the control of r RNA processing.
gar2 is a nucleolar protein from Schizosaccharomyces pombe required for 18S rRNA and 40S ribosomal subunit accumulation.
TLDR
It is proposed that gar2 helps the assembly of pre-ribosomal particles containing 18S rRNA and is able to rescue a S.cerevisiae mutant lacking NSR1, thus establishing gar2 as a functional homolog ofNSR1.
The fission yeast RPA51 is a functional homolog of the budding yeast A49 subunit of RNA polymerase I and required for maximizing transcription of ribosomal DNA.
Saccharomyces cerevisiae A49 and mouse PAF53 are subunits specific to RNA polymerase I (Pol I) in eukaryotes. It has been known that Pol I without A49 or PAF53 maintains non-specific transcription
Multiple domains of the RNA polymerase I activator hUBF interact with the TATA-binding protein complex hSL1 to mediate transcription.
TLDR
An important role of transcription activation domains of hUBF is suggested in mediating interactions with the TBP-TAF complex hSL1, suggestive of specific protein-protein interactions.
...
...