Chromosomal high mobility group (HMG) proteins of the HMGB-type occurring in the moss Physcomitrella patens
Introduction
High mobility group (HMG) proteins represent a heterogeneous group of small and relatively abundant non-histone proteins associated with the chromatin of eukaryotic organisms (Bianchi and Agresti, 2005, Bustin and Reeves, 1996, Bustin, 1999). Proteins belonging to the subclass of HMGB proteins (Bustin, 2001) act as architectural factors, facilitating the assembly of nucleoprotein complexes, which are involved in the regulation of transcription and other DNA-dependent processes (Bianchi and Agresti, 2005, Bustin, 1999, Thomas and Travers, 2001, Agresti and Bianchi, 2003). HMGB proteins contain one or two copies of a distinctive ∼ 75-amino acid residue DNA-binding domain, termed the HMG-box domain. The three-dimensional fold of this domain, consisting essentially of three α-helices which are arranged in an L-shape, is well conserved (Thomas and Travers, 2001, Travers, 2000). In addition to chromosomal HMGB proteins, HMG-box domain(s) are found in other DNA-binding proteins including transcription factors (Stros et al., in press). The HMG-box domain of the HMGB proteins mediates non-sequence-specific binding to linear DNA, and high affinity interactions with certain distorted DNA structures (Bustin, 1999, Zlatanova and van Holde, 1998, Thomas and Travers, 2001, Travers, 2000, Agresti and Bianchi, 2003). In complexes with B-DNA, the concave surface of the HMG-box domain binds predominantly the minor groove of the DNA, and the partial intercalation of amino acid residues between base pairs contributes to the bending of the DNA by over 90° (Thomas and Travers, 2001, Travers, 2000).
Members of the HMGB family of proteins have been characterised from various higher plant species, revealing that they share many properties with their counterparts from other eukaryotic organisms, and that they are different in some respects (Pedersen et al., 1991, Ritt et al., 1998b, Spiker, 1984, Webster et al., 1997, Webster et al., 2000, Wu et al., 2003b, Yamamoto and Minamikawa, 1998, Zhang et al., 2003). Plant genomes encode a variety of HMGB proteins ranging from ∼ 13–27 kDa. Thus, five different HMGB proteins were characterised from the monocot plant maize (Ritt et al., 1998b, Stemmer et al., 1999) and seven HMGB proteins encoded in the genome of the dicot plant Arabidopsis thaliana have been analysed (Grasser et al., 2004, Grasser et al., 2006, Stemmer et al., 1997). Typically, plant HMGB proteins have a single HMG-box domain, which is flanked by a basic N-terminal domain and an acidic C-terminal domain. The HMG-box domains of the various plant HMGB proteins are relatively conserved, but the basic and acidic flanking regions vary considerably in length and sequence (Grasser et al., 2007a). Based on Northern/Western blotting and expression analysis of HMGB gene promoter-reporter gene fusions, HMGB proteins are widely expressed in the plant (Kwak et al., 2007, Launholt et al., 2007, O'Neill and Zheng, 1998, Stemmer et al., 1999, Wu et al., 2003a, Yamamoto and Minamikawa, 1998). Plant HMGB proteins bind linear DNA non-sequence-specifically with moderate affinity, but recognise specifically certain DNA structures such as minicircles and four-way junctions, and they severely bend linear DNA upon binding (Ritt et al., 1998b, Stemmer et al., 1997, Webster et al., 2001, Wu et al., 2003b). In the cell nucleus, HMGB proteins display a high dynamics, interacting with DNA/chromatin only transiently before moving on to the next binding site, thereby scanning the nuclear space for binding sites (Launholt et al., 2006).
To date, HMGB proteins have been identified and characterised from a variety of mono-and dicot plants, but not from lower plant species. Here, we have searched databases for HMGB proteins encoded by the moss model Physcomitrella patens. Our survey yielded three candidate HMGB proteins that share structural features with higher plant HMGB proteins. Analysis of two Physcomitrella proteins revealed structural and functional similarities as well as differences compared to HMGB proteins of higher plants.
Section snippets
Analysis of sequences encoding HMGB-type proteins
EST sequences encoding putative Physcomitrella HMGB proteins were identified by searching the translated NCBI nucleotide database (http://www.ncbi.nlm.nih.gov/) using TBLASTN and the amino acid sequence of the HMG-box DNA-binding domain of the maize HMGB1 protein as a query. The obtained sequences were assembled into contigs using the software SeqMan (DNASTAR). Sequences were aligned pairwise (http://www.ebi.ac.uk/emboss/align/index.html) and by multiple sequence alignments (//www.ebi.ac.uk/Tools/clustalw/index.html
Discovery of sequences encoding Physcomitrella HMGB-type proteins
A BLAST search of the NCBI database (http://www.ncbi.nlm.nih.gov/) using the amino acid sequence of the HMG-box DNA binding domain of the maize HMGB1 protein (which is a typical representative of the plant HMGB family) identified EST sequences encoding putative Physcomitrella patens HMGB proteins. The EST sequences were assembled into three contigs representing complete coding sequences. The contigs code for three candidate HMGB proteins that were termed HMGB1 (215 aa, 22.7 kDa), HMGB2 (165 aa,
Discussion
Higher plants express several HMGB proteins that are structurally variable, in particular outside the HMG-box DNA-binding domain (Grasser et al., 2007a). In line with their structural variability, the various HMGB proteins differ in their DNA and chromatin interactions, as well as in their functional interaction with other proteins (Krohn et al., 2002, Lichota and Grasser, 2001, Ritt et al., 1998b, Schultz et al., 1996, Stemmer et al., 1997, Zhang et al., 2003). By searching databases we have
Acknowledgements
We would like to thank Hanne Krone Nielsen and Carla Hehn for excellent technical assistance. AM-Pharma B.V., The Netherlands, is gratefully acknowledged for providing the gene for secretable human intestinal alkaline phosphatase and the assay to detect AP activity. This research was supported in part by grants from the Danish Research Council to KDG.
References (66)
- et al.
HMGB proteins and gene expression
Curr. Opin. Genet. Dev.
(2003) - et al.
HMG proteins: dynamic players in gene regulation and differentiation
Curr. Opin. Genet. Dev.
(2005) Revised nomenclature for high mobility group (HMG) chromosomal proteins
Trends Biochem. Sci.
(2001)- et al.
Maize chromosomal HMGc: two closely related structure-specific DNA-binding proteins specify a second type of plant HMG-box protein
J. Biol. Chem.
(1996) - et al.
Stimulatory effect of the maize HMGa protein on reporter gene expression in maize protoplasts
FEBS Lett.
(1993) - et al.
High mobility group proteins of the plant HMGB family: dynamic chromatin modulators
Biochim. Biophys. Acta
(2007) - et al.
The Arabidopsis genome encodes structurally and functionally diverse HMGB-type proteins
J. Mol. Biol.
(2006) - et al.
Optimisation of a bioreactor culture of the moss Physcomitrella patens for mass production of protoplasts
Plant Sci.
(2002) - et al.
Specificity of the stimulatory interaction between chromosomal HMGB proteins and the transcription factor Dof2 and its negative regulation by protein kinase CK2-mediated phosphorylation
J. Biol. Chem.
(2002) - et al.
Overlapping expression patterns among the genes encoding Arabidopsis chromosomal high mobility group (HMG) proteins
FEBS Lett.
(2007)
Multifocal two-photon laser scanning microscopy combined with photo-activatable GFP for in vivo monitoring intracellular protein dynamics in real time
J. Struct. Biol.
The S. cerevisiae architectural HMGB protein NHP6A complexed with DNA: DNA and protein conformational changes upon binding
J. Mol. Biol.
Histone H1 enhances the DNA binding activity of the transcription factor EmBP-1
J. Biol. Chem.
High mobility group chromosomal proteins of wheat
J. Biol. Chem.
Protein kinase CK2 differentially phosphorylates maize chromosomal high mobility group B (HMGB) proteins modulating their stability and DNA interactions
J. Biol. Chem.
A role of basic residues and the putative intercalating phenylalanine of the HMG-1 box B in DNA supercoiling and binding to four-way junctions
J. Biol. Chem.
HMGB1 and HMGB2 cell-specifically down-regulate the p53- and p73-dependent sequence-specific transactivation from the human Bax gene promoter
J. Biol. Chem.
HMG1 and 2, and related architectural DNA-binding proteins
Trends Biochem. Sci.
Recognition of distorted DNA structures by HMG domains
Curr. Opin. Struct. Biol.
High mobility group proteins 1 and 2 stimulate transcription in vitro by RNA polymerases II and III
J. Biol. Chem.
Cloning and characterization of rice HMGB1 gene
Gene
Rice HMGB1 protein recognizes DNA structures and bends DNA efficiently
Arch. Biochem. Biophys.
The isolation and characterisation of a cDNA encoding a high mobility group protein HMG-1 from Canavalia gladiata D.C.
Biochim. Biophys. Acta
Interaction of wheat high-mobility-group proteins with four-way-junction DNA and characterization of the structure and expression of HMGA gene
Arch. Biochem. Biophys.
High-mobility group chromatin proteins 1 and 2 functionally interact with steroid hormone receptors to enhance their DNA binding in vitro and transcriptional activity in mammalian cells
Mol. Cell. Biol.
Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins
Mol. Cell. Biol.
High-mobility-group chromosomal proteins: architectural components that facilitate chromatin function
Prog. Nucleic Acids Res.
HMG boxes of DSP1 protein interact with the Rel homology domain of transcription factors
Nucleic Acids Res.
A close relative of the nuclear, chromosomal high-mobility-group protein HMG1 in yeast mitochondria
Proc. Natl. Acad. Sci. U. S. A.
Chromatin-associated HMGA and HMGB proteins: versatile co-regulators of DNA-dependent processes
Plant Mol. Biol.
HMGB6 from Arabidopsis thaliana specifies a novel type of plant chromosomal HMGB protein
Biochemistry
Chromatin-associated architectural HMGA and HMGB proteins assist transcription factor function
Basic and acidic regions flanking the HMG-box domain of maize HMGB1 and HMGB5 modulate the stimulatory effect on the DNA-binding of transcription factor Dof2
Biochemistry
Cited by (9)
The HMGB1-TLR4 axis contributes to myocardial ischemia/reperfusion injury via regulation of cardiomyocyte apoptosis
2013, GeneCitation Excerpt :Although the main mechanism responsible for myocardial I/R injury is poorly understood, it is widely accepted that the inflammatory response and apoptotic cell death participate in the development of ischemic heart damage (Frangogiannis et al., 2002; Hansen, 1995; Liao et al., 2012; Vakeva et al., 1998). High mobility group box 1 (HMGB1), a 30-kd nuclear protein involved in the structural organization of DNA, serves as a mediator of inflammation after being released by necrotic cells or upon cellular activation in various pathological conditions including diverse cardiovascular diseases and myocardial I/R injury (Andrassy et al., 2008; de Oliveira et al., 2006; Ding and Yang, 2010; Kiilerich et al., 2008; Scaffidi et al., 2002). Meanwhile, TLR4, an important receptor for HMGB1, is also involved in the induction of the inflammatory response and can attenuate the inflammation interruption of the ligands-TLR4 axis via multiple approaches (Akira et al., 2001; Yang et al., 2012; Yang et al., 2010).
High mobility box 1 mediates neutrophil recruitment in myocardial ischemia-reperfusion injury through toll like receptor 4-related pathway
2012, GeneCitation Excerpt :Toll-like receptor 4 (TLR4), one of the pattern recognition receptors, plays a crucial role in the induction of the inflammatory response, and its activation is linked to the activation of downstream signaling (such as nuclear factor kappa B (NF-κB) ) in several cell types (Akira et al., 2001; Baumgarten et al., 2001; Cha et al., 2008; Kajikawa et al., 2005). High mobility box 1 (HMGB1), a non-chromosomal nuclear protein, has been identified as a new pro-inflammatory cytokine after being released by necrotic or activated innate immune cells in inflammatory conditions, such as arthritis, as well as in cardiovascular diseases (de Oliveira et al., 2006; Ding and Yang, 2010; Kiilerich et al., 2008; Scaffidi et al., 2002; Sharman et al., 1997; Taniguchi et al., 2003). Recent studies have demonstrated that HMGB1 plays an important role in the pathogenesis of myocardial I/R and can mediate neutrophil recruitment (Andrassy et al., 2008; Degryse and de Virgilio, 2003; Hu et al., 2009; Orlova et al., 2007).
Transcript Elongation Factor TFIIS Is Involved in Arabidopsis Seed Dormancy
2009, Journal of Molecular BiologyPhyscomitrella HMGA-type proteins display structural differences compared to their higher plant counterparts
2008, Biochemical and Biophysical Research CommunicationsCitation Excerpt :Physcomitrella protoplast cotransformation assay. Protoplasts derived from Physcomitrella protonema suspension cultures were prepared and transformed (with reporter plasmids [18] and effector plasmid pPpUbq::HMGA2) by PEG-mediated transformation as previously described. Likewise reporter gene expression was quantified as previously described [18].
HBD1 protein with a tandem repeat of two HMG-box domains is a DNA clip to organize chloroplast nucleoids in Chlamydomonas reinhardtii
2021, Proceedings of the National Academy of Sciences of the United States of America