Characteristics of HMGB proteins in
Abstract
HMGB proteins are characterized for containing one or more HMG-box domains and are well conserved from yeasts to higher eukaryotes. The HMG-box domain is formed by three α-helices with an L-shaped fold. Although HMGB proteins also have cytoplasmic and extracellular functions, they bind to nuclear or mitochondrial DNA in a highly dynamic process that affects chromatin organization. In this review, we mainly focus on HMGB proteins from yeast and their human homologs as functionally involved in DNA repair and transcriptional regulation. Recent research reveals that these proteins participate in epigenetic control of gene expression, aging, disease, or stem-cell biology.
Keywords
- nonhistone proteins
- epigenetics
- transcriptional regulation
1. Introduction
Nucleosomes are fairly stable basic units of DNA packaging. Nevertheless, nucleosomal chromatin is surrounded by a highly dynamic protein pool that allows chromatin remodeling and favors replication, DNA repair, and gene transcription. Among proteins that transiently associate with chromatin are variants of the linker histone H1 family [1–3] and members of the high mobility group (HMG) protein superfamily [4–6]. Although HMG motifs are present in many nuclear proteins, the classification and nomenclature of the considered “canonical” HMG proteins is organized in three families named HMGA, HMGB, and HMGN, each one having a specific functional domain: the “AT hook” in HMGA, the “HMG-box” in HMGB, and the “nucleosomal binding domain” in HMGN proteins [7].
Some HMGB proteins have been related to nuclear, extranuclear, and extracellular functions during inflammation, cell differentiation, cell migration, and tumor metastasis [8, 9]. Their HMG-box domain contains 65–85 amino acids and has a characteristic L-shaped fold formed by three α-helices with an angle of ≈80° between the two arms. The long arm, or minor wing, is composed by the extended N-terminal strand and third α-helix, while first and second α-helices form the short arm, or major wing (Figure 1(a)). Because of protein interaction in the minor groove, DNA-bending and widening of the double helix is produced (Figure 1(b)).
There are two broad subfamilies of HMGB-containing proteins, based on structural and phylogenetic studies. One class includes those that bind to distorted DNA with low or without sequence specificity (nonsequence specificity (NSS), HMG-box domains) and have, in general, two or more
In this review, we focus on HMGB proteins from yeast, as functionally involved in DNA repair and transcriptional regulation, but also in their homologs from multicellular eukaryotes, with special reference to human proteins. Their functions may be modulated by nucleosome positioning and stability [12]. Interestingly, recent findings support that HMGB proteins may also play diverse roles in epigenetic control, since their interaction with chromatin affects the level of histone modifications [13]. In the light of recently opened research areas, in which HMGB proteins are involved, available knowledge is also discussed.
2. HMGB proteins from Saccharomyces cerevisiae
In
Protein | Amino acids | Molecular weight (Da) | pI | Aliphatic index | Instability index | Domain position |
---|---|---|---|---|---|---|
Abf2 | 183 | 21,575 | 10.24 | 67.27 | 42.94 | HMG: 42-112 HMG: 115-183 Coil 89-110 |
Hmo1 | 246 | 27,546 | 9.11 | 67.35 | 45.80 | HMG: 105-180 PHHR13711: 22-185 |
Nhp6A | 93 | 10,810 | 10.40 | 43.13 | 39.16 | HMG: 20-90 PHHR13711: 7-93 |
Nhp6B | 99 | 11,485 | 10.54 | 37.99 | 58.30 | HMG: 26-96 PTHR13711: 6-99 |
Nhp10 | 203 | 23,858 | 8.15 | 68.12 | 51.57 | Coil: 3-24 HMG: 93-159 PTHR13711: 74-182 |
Rox1 | 368 | 41,857 | 10.46 | 70.38 | 62.14 | Coil: 90-118 HMG: 9-84 |
Ixr1 | 597 | 67,858 | 8.36 | 51.20 | 70.67 | HMG: 360-430 HMG: 433-503 Poly-Q: 3 regions Coil: 292-313 PTHR13711: 1-594 |
With the exception of Rox1 that behaves as a specific transcriptional regulator of the hypoxic yeast regulon [14] and Ixr1 that has a dual function as specific transcription factor and DNA-binding protein without sequence specificity, also participating in DNA repair [15], the other HMGB proteins from
Although Abf2 and Ixr1 are considered paralogs, resulting from the whole genome duplication in an ancestor of
Hmo1 is not considered a specific transcriptional factor either, although it regulates rDNA transcription from RNA polymerase I promoters and also regulates start site selection of ribosomal protein genes by RNA polymerase II [23–25].
Nhp10 (alias Hmo2) is a nonessential subunit of the INO80 chromatin remodeling complex, and it affects telomere maintenance via recombination [26, 27].
Nhp6a and Nhp6b are also paralogs and functionally redundant [28], they bind to and remodel nucleosomes [29, 30], and both are required for transcriptional initiation fidelity of some tRNA genes [31]. Their protein levels increase in response to DNA replication stress [32]. Besides, Nhp6a and Nhp6b acting on chromatin tightly repress histone expression; paradoxically, histone gene overexpression in the double
Although few data are available about Ssp41 functions, it has been associated with chromatin remodeling [34], transcription, and RNA processing [35, 36]. Besides, overexpression causes chromosomal instability [36] and under hypoxia, it is rapidly exported to the cytosol [34].
An intriguing question is whether the
Pathway ID | Biological function; pathway description | Observed gene count | False discovery rate |
---|---|---|---|
GO.0006325 | Chromatin organization | 50 | 4.50E-27 |
GO.0010468 | Regulation of gene expression | 81 | 5.85E-25 |
GO.0051171 | Regulation of nitrogen compound metabolic process | 84 | 5.85E-25 |
GO.0051276 | Chromosome organization | 63 | 5.85E-25 |
GO.0006355 | Regulation of transcription, DNA-templated | 71 | 3.30E-24 |
GO.0051252 | Regulation of RNA metabolic process | 72 | 3.30E-24 |
GO.0071824 | Protein-DNA complex subunit organization | 39 | 1.27E-22 |
GO.0043933 | Macromolecular complex subunit organization | 78 | 1.24E-21 |
GO.0090304 | Nucleic acid metabolic process | 95 | 1.53E-21 |
GO.0034728 | Nucleosome organization | 27 | 3.55E-21 |
GO.0006338 | Chromatin remodeling | 26 | 3.00E-20 |
GO.0006351 | Transcription, DNA-templated | 61 | 3.69E-19 |
GO.0006974 | Cellular response to DNA damage stimulus | 43 | 5.34E-19 |
GO.0006333 | Chromatin assembly or disassembly | 24 | 7.13E-19 |
GO.0006281 | DNA repair | 39 | 2.21E-18 |
GO.0016568 | Chromatin modification | 36 | 3.02E-18 |
GO.0006259 | DNA metabolic process | 47 | 1.11E-17 |
GO.0010467 | Gene expression | 82 | 1.39E-15 |
GO.0016070 | RNA metabolic process | 78 | 1.73E-15 |
GO.0006357 | Regulation of transcription from RNA polymerase II promoter | 45 | 8.94E-14 |
GO.0006323 | DNA packaging | 16 | 1.73E-11 |
GO.0006366 | Transcription from RNA polymerase II promoter | 29 | 1.99E-11 |
GO.0043044 | ATP-dependent chromatin remodeling | 14 | 5.72E-11 |
GO.0006950 | Response to stress | 54 | 6.10E-10 |
GO.0016458 | Gene silencing | 22 | 1.12E-09 |
GO.0006354 | DNA-templated transcription, elongation | 16 | 1.21E-09 |
GO.0040029 | Regulation of gene expression, epigenetic | 23 | 1.75E-09 |
GO.0050896 | Response to stimulus | 67 | 3.76E-09 |
GO.0006342 | Chromatin silencing | 21 | 4.01E-09 |
GO.0071103 | DNA conformation change | 16 | 9.65E-08 |
GO.0016584 | Nucleosome positioning | 7 | 1.67E-07 |
GO.0007049 | Cell cycle | 49 | 2.67E-07 |
GO.0018193 | Peptidyl-amino acid modification | 18 | 5.44E-07 |
GO.0022607 | Cellular component assembly | 47 | 7.03E-07 |
GO.0065004 | Protein-DNA complex assembly | 17 | 9.19E-07 |
GO.1902589 | Single-organism organelle organization | 58 | 9.77E-07 |
GO.0042766 | Nucleosome mobilization | 7 | 9.81E-07 |
GO.0018205 | Peptidyl-lysine modification | 15 | 1.06E-06 |
GO.0022402 | Cell cycle process | 43 | 2.30E-06 |
GO.0006337 | Nucleosome disassembly | 8 | 2.35E-06 |
GO.0031498 | Chromatin disassembly | 8 | 2.35E-06 |
GO.0006368 | Transcription elongation from RNA polymerase II promoter | 12 | 2.40E-06 |
GO.0006302 | Double-strand break repair | 16 | 2.65E-06 |
GO.0098781 | ncRNA transcription | 12 | 4.52E-06 |
GO.0000122 | Negative regulation of transcription from RNA polymerase II | 19 | 7.75E-06 |
GO.0006383 | Transcription from RNA polymerase III promoter | 9 | 9.65E-06 |
GO.0000723 | Telomere maintenance | 12 | 4.18E-05 |
GO.0006360 | Transcription from RNA polymerase I promoter | 9 | 6.50E-05 |
GO.0009303 | rRNA transcription | 8 | 0.000151 |
GO.0016570 | Histone modification | 13 | 0.000222 |
References to the existence of interplay between the response to hypoxia, oxidative stress, and mitochondrial function have been reported, i.e., it is known that when cells experience hypoxia, up- or downregulation of an important number of oxygen-regulated genes in yeast depends on an active mitochondrial respiratory chain [38]. Treatment with antimycin A (respiration inhibitor) or oxygen deprivation cause downregulation of networks involved in the G1/S transition of the cell cycle as well as of those involved in energetically costly programs of ribosomal biogenesis and protein synthesis [37]. Similar regulation occurs in the response to DNA stress [39–41], and therefore, a wide gene-regulatory response might engage the functions of the HMGB proteins coordinately. Figure 3 summarizes the participation of HMGB proteins from
3. HMGB proteins from other yeasts
Although the complete sequences of a huge number of genomes from yeast and fungi are available, functional studies of HMGB proteins are not very frequent and only a few HMGB homologs have been characterized so far.
In
In
Regarding the Rox1 homolog in
Although a low number of functional data is available, we may speculate that in yeasts the functions of “architectural” HMGB proteins are probably more conserved than those with functions as specific transcriptional factors. This is also predictable considering that transcriptional factors are among the proteins more strongly diverged between yeasts [48].
4. HMGB proteins in multicellular organisms
In multicellular eukaryotes, a large number of proteins contain HMG boxes, most of which are transcription factors that contain a single HMG-box [49], although some may have up to 6 HMG-box domains, like Ubf1 [50]. According to the classification from Bustin [7], “canonical” chromatin HMGB proteins represent a subgroup that invariably contains two in tandem HMG boxes. A model for the phylogenesis of HMGB genes in metazoan suggests that these two HMG boxes have their origin in the duplication of an ancient single HMG-box; even those which are part of HMG-box transcription factors might evolve from this ancestral ProtoBox [51].
Transcription factors (including SOX factors) are the most divergent group of HMG-box proteins in humans, whereas in plants the chromosomal HMGB-type proteins are most variable [52]. In plants, HMG-box proteins classify into four groups: HMGB-type proteins, structure-specific recognition protein 1 (SSRP1), proteins containing 3 HMG-box domains (3xHMG-box), and proteins that contain both an AT-rich interaction domain (ARID) and an HMG-box domain (ARID/HMG). These latter two groups are apparently specific for plants [52]. Conversely, HMG-box containing transcription factors such as Sry, a sex-determining factor that is necessary for testes development [53], Lef-1, which regulates gene expression during cell differentiation [54], and the SOX family are presumably not present in plants [52].
Table 3 resumes the homologies found between
Yeast | Associated human diseases | |
---|---|---|
Rox1 | Sox1 | |
Sox10 | Peripheral demyelinating neuropathy, central dysmyelination, Waardenburg syndrome, and Hirschsprung disease | |
Sox11 | Mental retardation, autosomal dominant 27 | |
Sox12 | ||
Sox13 | ||
Sox14 | ||
Sox15 | ||
Sox17 | Vesicoureteral reflux | |
Sox18 | Hypotrichosis-lymphedema-telangiectasia-renal defect syndrome | |
Sox2 | Microphthalmia, syndromic 3 | |
Sox21 | ||
Sox3 | Mental retardation, X-linked | |
Sox30 | ||
Sox4 | ||
Sox5 | ||
Sox6 | ||
Sox7 | ||
Sox8 | ||
Sox9 | Campomelic dysplasia | |
Sry | 46,Xx sex reversal 1 | |
Ixr1 | Hmg20a | |
Hmg20b | ||
Smarce1 | Susceptibility to familial meningioma | |
Sp110 | Susceptibility to | |
Sp140 | ||
Tfam | ||
Ubtf | ||
Ubtfl1 | ||
Abf2 | Tfam | |
Hmo1 | Hmg20a | |
Hmg20b | ||
Smarce1 | Susceptibility to familial meningioma | |
Sp110 | Susceptibility to | |
Sp140 | ||
Tfam | ||
Ubtf | ||
Ubtfl1 | ||
Nhp6a/b | Hmg20a | |
Hmg20b | ||
Hmgb1 | ||
Hmgb3 | Microphthalmia, syndromic 13 | |
Smarce1 | Susceptibility to familial meningioma | |
Sp110 | Susceptibility to | |
Sp140 | ||
Tfam | ||
Ubtf | ||
Ubtfl1 |
5. Mechanisms of transcriptional regulation mediated by HMGB proteins
5.1. Direct binding to target promoters
In
The first report about the participation of Ixr1 in the yeast hypoxic response was the aerobic repression of the
A cross-regulation between Rox1 and Ixr1 in the yeast hypoxic response has been reported [66]. In aerobiosis, low levels of
Rox1 from
SOX proteins are highly dynamic regulators of cell functions due to their nucleocytoplasmic shuttling properties [75]. However, because of their low affinity for DNA binding, and despite SOX proteins usually have their own C-terminal activation/repression domain, they are committed to recruit partner proteins to fulfill their transcriptional regulatory task [76]. Homo- and heterodimerization of SOX proteins is also a mechanism used for the formation of these regulatory complexes [77]. SOX proteins also interact with signaling effectors, Wnt/β-catenin being one of the most studied signaling pathways [78]. Different molecular complexes of SOX factors and their partner proteins are formed along developmental processes. Besides, these specific interactions are usually dependent on posttranslational modifications of SOX proteins like phosphorylation, acetylation, SUMOylation, and ubiquitination [72].
5.2. Other mechanisms for transcriptional regulation
The HMGB proteins that are not classified as transcriptional factors also influence transcription by different mechanisms, which affect chromatin. Since these HMGB proteins are very dynamic in their interactions and have no DNA sequence specificity, they usually help transcription factors or cofactors to bind to their cognate sites by bending the DNA molecule, but are rarely retained within the formed complexes [79].
In plants, HMGB proteins contribute to transcriptional regulation by functional interaction with certain transcription factors like Dof2 [80]. In mammals, Hmgb1 alters the structure and stability of the canonical nucleosome in a nonenzymatic, ATP-independent way to facilitate strong binding of estrogen receptor to their regulatory elements [81].
HMGB proteins also interact with nucleosomes to promote their sliding or other chromatin remodeling processes [79]. Yeast Nhp6a, Nhp6b, and Hmo1 proteins stimulate the sliding activity of the yeast remodeler complex SWI/SNF, while octamer transfer and transient exposure of nucleosomal DNA catalyzed by this complex are only stimulated by Hmo1. Hmo1 also favors the sliding activity of the ISW1a complex [82].
Hmo1 in yeasts and the upstream binding factor (Ubf) in mammals function as cofactors in RNA polymerase I transcription and therefore are essential for transcription of the rRNA genes
Finally, HMGB proteins have been involved in the selection of modified histone variants. Studies carried out in mouse showed that conditional inactivation of Ubf is also accompanied by recruitment of H3K9me3, which reveals its function in the epigenetic control of gene expression [86].
6. Mechanisms of DNA repair mediated by HMGB proteins
The three HMG families (A, B, N) are involved in the four major DNA repair pathways. HMGB proteins contribute to nucleotide excision repair (NER), base excision repair (BER), double-strand break repair (DSBR), and mismatch repair (MMR), but with specific particularities (reviewed in Ref. [87]). The first report about participation of HMGB proteins in DNA repair was the identification of Hmgb1 binding to the major DNA lesions formed in cells treated with cisplatin, which are repaired by the NER pathway [88]. In general, the effects of HMGB proteins on DNA repair are achieved by different mechanisms. First, they contribute to modulate chromatin compaction and nucleosome occupancy; through interactions with chromatin-modifying enzymes and energy-dependent remodeling complexes, HMGB proteins favor or avoid the access of the repair machinery to altered DNA. Second, HMGB proteins can also regulate repair by direct modulation of the enzymatic activities and/or mechanistic steps implied in the diverse repair pathways. Third, acting as transcriptional regulators, HMGB proteins may change the expression levels of genes involved in DNA repair processes.
Hmgb1 and many other HMGB proteins (e.g., Ubf, Lef-1, Sry, and human mtTFA) inhibit NER [87]. If Hmgb1 binds first to a cisplatin adduct, the replication protein A (hRPA), necessary for NER repair, cannot displace it, thus potentially inhibiting repair [89]. On the contrary, Hmgb1 stimulates
Hmgb1 coimmunoprecipitates with proteins from the BER pathway, including Ape1, Fen-1, and Pol-beta, and
Also
Hmgb1 and Hmgb2 form part of a pentameric “damage-sensing” complex (also including heat shock protein 70, protein disulfide-isomerase Erp60, and glyceraldehyde3-phosphate dehydrogenase) specifically recruited to nonnatural nucleosides
Other important connection between Hmgb1 and DNA repair comes from the observation that this protein interacts with p53
7. HMGB proteins at the forefront of cutting-edge research
Recent publications on HMGB proteins reveal that these proteins are becoming a focus of interest due to their participation in cellular processes of great importance for humankind like epigenetic control of gene expression, aging, disease, or regenerative cellular therapies.
An interesting research field concerning HMGB proteins is their function replacing histones under specific conditions. In eukaryotic chromatin, histone H1 associates with the linker DNA in the nucleosome core particle to stabilize the higher-order chromatin structure and to modulate the ability of specific regulatory factors to access their final targets. It has been demonstrated that in
Environmental changes, sensed through signaling cascades, regulate chromatin organization, thus contributing to gene expression and, ultimately, cell adaptation to external stimulus. These responses are related to cell fate and aging. In yeast, the nutrient-dependent target-of-rapamycin complex 1 (TORC1) pathway and histone H3 collaborate to retain HMGB proteins within the nucleus, and in this way, they increase longevity [103].
The role of HMGB proteins remodeling chromatin on a genome-wide scale relates to the onset of several human diseases. Two chromatin structural proteins, CCCTC-binding factor (Ctcf) and high mobility group protein B2 (Hmgb2), regulate pathologic transcription in myocytes during heart disease [104]. The response of macrophages to inflammation starts by nucleosome loss and cell lacking Hmgb1 contains 20% less nucleosomes and has a specific transcription pattern. In a mouse model, unstimulated Hmgb1-/- macrophages activate transcriptional pathways associated with cell migration and chemotaxis. Wild-type macrophages, under lipopolysaccharide (LPS)/interferon (IFN)-γ exposure, rapidly secrete Hmgb1 and reduce their histone content [105].
Hmgb1 is overexpressed in many types of cancer, including those of etiology based on oxidative damage [8], and frequently, Hmgb1 expression increases with tumor stage and metastasis. In the pediatric acute lymphoblastic leukemia, autophagy is regarded as a mechanism that underlies chemoresistance. Since autophagy depends on the Hmgb1 translocation from nucleus to cytoplasm, this protein is a good target of study in order to overcome the problem [106]. It has been found that Hmgb1 expression is inversely correlated with semaphorin 3A expression, a suppressor of angiogenesis and cell migration. The epigenetic mechanism causing semaphorin 3A repression by Hmgb1 implies that it promotes heterochromatin formation and decreased occupancy of acetylated histones at the semaphorin 3A locus [107].
Other remarkable function of HMGB proteins, yet not fully understood, is their participation in telomere maintenance, studied in yeast [108] plants [109] and notoriously in animals [110], because of their implications in cancer development. The telomerase that conserves telomere structures is formed by a catalytic protein subunit (telomerase reverse transcriptase (TERT)) and an RNA subunit (telomerase RNA, TR), and both physically interact with Hmgb1
Evidences linking HMGB proteins with stem cell biology and cellular reprograming are also found. Sox factors participate in embryonic pluripotent cell differentiation; Oct4 interacts with Sox2 to maintain pluripotency or with Sox17 to promote endoderm commitment [111]. Expression of Hmgb2 changes notably at different time points during embryogenesis [112] and controls the differentiation of neural stem cells into neurons, astrocytes, and oligodendrocytes. Besides, several Sox factors [113, 114] and also chromatin HMGB proteins [115] are involved in back-reprograming differentiated cells into stem cells. Hmgb1 was also proposed as an efficient stem cell recruiter with tissue-regenerating roles; it was able to induce stem cell transmigration through an endothelial barrier or to capture in muscle the stem cells injected into the general circulation [116]. In murine and human mammary cancer stem cells, Hmgb1 promotes self-renewal of these cells [117], which are responsible for tumor progression, metastases, resistance to therapy, and tumor recurrence. Therefore, HMGB proteins are clues in the search of more effective cancer therapies and cellular regenerative treatments.
Acknowledgments
Funding is acknowledged both from the Instituto de Salud Carlos III under Grant Agreement no. PI14/01031 cofinanced by FEDER and from Xunta de Galicia (Consolidación D.O.G. X-12-2016. Contract Number: 2016/012). Aida Barreiro-Alonso was funded by a predoctoral fellowship from Plan I2C Xunta de Galicia-2013 (Spain). Agustín Rico-Diaz was funded by a predoctoral fellowship from Plan I2C Xunta de Galicia-2012 (Spain). We thank STRING facilities and development.
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