Table 1.
Proteins of human chromatin remodeling complexes
| Hugo name | Alternative names | Complex family | Bound complexes | Function | References | Implicated lncRNAs |
|---|---|---|---|---|---|---|
| SWI/SNF subunits (Histone dimer/nucleosome removal, nucleosome sliding) | ||||||
| 1. Catalytic subunit (SMARC subfamily A) | ||||||
| SMARCA4 | BRG1 | SWI/SNF | BAF, PBAF | ATP-dependent helicase | [6] |
Evf2, UCA1, TUG1, Myheart, CPS1‐IT1, NEAT1, MALAT1, LincRNA Cox2 IL-7–AS, LncFZD6, lncTCF7 |
| SMARCA2 | BRM | SWI/SNF | BAF | NEAT1, lncBRM | ||
| 2. SMARC subfamily B subunit | ||||||
| SMARCB1 | SNF5, BAF47 | SWI/SNF | BAF, PBAF | Constitutive Core Subunit, chromatin reader binding to H3K56Ac, Enhances DNA integration | [5] | SWINGN, HOTAIR |
| 3–4. SMARC subfamily C dimer (BAF155-155 or 155-170) | ||||||
| SMARCC1 | BAF155 | SWI/SNF | BAF, PBAF | Constitutive Core Subunit | [6] | |
| SMARCC2 | BAF170 | SWI/SNF | BAF | Core Subunit; mono-ADP-ribosylated by SIRT6 | [113] | |
| 5. AT-rich interaction domain subunit | ||||||
| ARID2 | BAF200 | SWI/SNF | PBAF | DNA and transcription factor binding | [6] | |
| ARID1A | BAF250A | SWI/SNF | BAF | HOTAIR, MVIH, DGCR5, LINC00163, CASC15 | ||
| ARID1B | BAF250B | SWI/SNF | BAF | |||
| 6. SMARC subfamily E subunit | ||||||
| SMARCE1 | BAF57 | SWI/SNF | cBAF, PBAF | Binding to '4-way' branched DNA (Holliday junction) | [6] | |
| 7–8. Actin-related Subunits | ||||||
| ACTL6A | BAF53A, Arp4, INO80K | General | BAF,PBAF, INO80, p400/TRRAP | SMARCA/TRRAP binding | [6] | uc.291 |
| ACTL6B | BAF53B | SWI/SNF | ncBAF | |||
| ACTB | (β-Actin) | General | BAF,PBAF, p400/TRRAP | |||
| 9. Poly-bromo subunit | ||||||
| PBRM1 | BAF180 | SWI/SNF | PBAF | chromatin reader binding to H3K14ac, phosphorylated by ATM | [11, 114] | |
| 10. B-cell lymphoma 11 subunit | ||||||
| BCL11A | General | BAF/PBAF, NuRD, SIN3A, PRC2 [115] | Enhances DNA integration | [6] | CDKN2B-AS1, uc.57 | |
| BCL11B | SWI/SNF | BAF/PBAF | ||||
| 11. Bromodomain subunit | ||||||
| BRD7 | SWI/SNF | PBAF | Bromo-domain interaction with acetylated lysine. | [116] | ||
| BRD9 | LAVS3040 | SWI/SNF | ncBAF | [117] | ||
| 12. B-cell lymphoma 7 subunit | ||||||
| BCL7A | SWI/SNF | BAF | (B-cell CLL/Lymphoma 7) | [6] | ||
| BCL7B | SWI/SNF | npBAF | ||||
| BCL7C | SWI/SNF | npBAF | ||||
| 13. SMARC subfamily D subunit | ||||||
| SMARCD1 | BAF60A | SWI/SNF | BAF/PBAF | Transcription factor binding [118] | DLEU1 | |
| SMARCD2 | BAF60B | SWI/SNF | PBAF | [118] | ||
| SMARCD3 | BAF60C | General | BAF, MyoD | [119] | ||
| 14. PHD-zinc finger subunit | ||||||
| PHF10 | BAF45A | SWI/SNF | PBAF | Phosphorylated protein, complex stability | [6] | |
| DPF1 | BAF45B, NEUD4 | SWI/SNF | BAF | (Double Plant homeodomain Finger) | [6] | |
| DPF2 | BAF45C | SWI/SNF | BAF | Chromatin reader binding to H3K4me1 | [14] | |
| DPF3 | BAF45D | SWI/SNF | BAF | [5] | ||
| 15. BRD-interacting subunit | ||||||
| BICRA | GLTSCR1 | SWI/SNF | ncBAF | (Glioma tumor suppressor candidate region 1), BRD interacting protein | [6] | |
| BICRAL | GLTSCR1L | SWI/SNF | ncBAF | [6] | ||
| 16. Synovial Sarcoma translocation protein Chr18 subunit | ||||||
| SS18 | SSXT/SYT | SWI/SNF | ncBAF | Interaction with BAF47 | [120] | |
| SS18L1 | CREST | SWI/SNF | ncBAF | Calcium-responsive transactivator | [120] | |
| INO80/SWR1 subunits (nucleosome replacement) | ||||||
| 1. Catalytic subunit (ATPase) | ||||||
| INO80 | INO80A, INOC1, | INO80/SWR1 | INO80 | ATPase | [121] | LCTS5, HAND2‐AS1 |
| SRCAP | EAF1, FLHS, SWR1, DOMO1 | INO80/SWR1 | SRCAP | [121] | LncKdm2b | |
| EP400 | p400 | INO80/SWR1 | p400/TRRAP | [121] | ||
| 2–3. Catalytic subunit dimer (helicase) | ||||||
| RUVBL1 | INO80H, RVB1, TIP49 | INO80/SWR1 | INO80, SRCAP, p400/TRRAP | ATP-dependent helicase | [121] | |
| RUVBL2 | INO80J, RVB2, TIP48 | INO80/SWR1 | INO80, SRCAP, p400/TRRAP | |||
| 4–6. Effector subunit | ||||||
| YY1 | INO80S | General | INO80 , p400/TRRAP, PRC2 | Transcription factor (GLI-Krüppel zinc finger), Polycomb proteins recruitment | [122] | ANRIL, Linc-YY1, TUG1, SPAG5-AS1, HOTAIR, LINC00899, LINC00668, Linc01134, |
| KAT5 | TIP60 | INO80/SWR1 | p400/TRRAP | Lysine (K) acetyltransferase 5 | [121] | |
| TRRAP | Tra1 | INO80/SWR1 | p400/TRRAP | Histone acyltransferase (H4) | [121] | |
| 7–9. Actin-related subunits | ||||||
| ACTR5 | ARP5, INO80M | INO80/SWR1 | INO80 | INO80 binding | [121] | |
| ACTR8 | ARP8, INO80N | INO80/SWR1 | INO80 | |||
| ACTL6A | Arp4, INO80K, BAF53A | General | INO80, SRCAP, p400/TRRAP, BAF, PBAF, | TRRAP/SMARCA binding | ||
| ACTB | (β-Actin) | General | p400/TRRAP, BAF, PBAF | |||
| ACTR6 | ARP6, CDA12; hARPX, HSPC281, MSTP136 | INO80/SWR1 | SRCAP | SRCAP binding | ||
| 10–17. INO80 subunits | ||||||
| INO80B | IES2, PAPA-1 | INO80/SWR1 | INO80 | INO80 binding | [121] | |
| INO80C | IES6 | INO80/SWR1 | INO80 | |||
| TFPT | INO80F, FB1, amida | INO80/SWR1 | INO80 | Modulated by SUMOylation (increases interaction with INO80E), transcription factor? | [123] | |
| INO80E | CCDC95 | INO80/SWR1 | INO80 | Binding to TFPT | [121] | |
| INO80D | INO80/SWR1 | INO80 | Has two putative DNA-binding domains | CR933609 | ||
| MCRS1 | INO80Q, MSP58, P78 | INO80/SWR1 | INO80 | Has a nuclear and nucleolar localization signal | ||
| NFRKB | INO80G | INO80/SWR1 | INO80 | NF (nuclear factor) binding to kappa B regulatory elements/winged-helix domains involved in protein-protein interactions, recruitment of EXO1 enhances resection, stimulating homologous recombinase DNA repair (non-essential for the in vitro nucleosome sliding) | [30] | |
| UCHL5 | UCH37 | INO80/SWR1 | INO80, RPN13 | Deubiquitinating enzyme, but inhibited by NFRKB, recruitment of EXO1 (non-essential for the in vitro nucleosome sliding) | [124], | DRAIC |
| 9–12. SRCAP/TRAPP subunits | ||||||
| VPS72 | YL1; CFL1; Swc2; YL-1; TCFL1 | INO80/SWR1 | SRCAP, p400/TRRAP | Histone chaperone | [125] | |
| DMAP1 | SWC4, MEAF2, EAF2, DNMTAP1 | General | SRCAP, p400/TRRAP, DNMT1/HDAC complexes | Regulation of transcription by binding to DNMT1, HDAC2 and HAT complexes | [121] | |
| BRD8 | p120 | INO80/SWR1 | SRCAP, p400/TRRAP | Bromodomain interaction with acetylated lysine (histone H4) and nuclear receptors (TR, RXR) | [121] | RNCR3 |
| YEATS4 | GAS41; NUBI-1 | INO80/SWR1 | SRCAP, p400/TRRAP | Chromatin reader, binding to H3K23acK27ac binding, H3K122suc, homology to transcription factors MLLT 1, 3 | [126, 127] | lncAKHE |
| 13–14. SRCAP specific subunits | ||||||
| CFDP1 | Swc5, p97, BCNT | INO80/SWR1 | SRCAP | Interacting with H2A | [121] | |
| ZNHIT1 | ZNFN4A1 | INO80/SWR1 | SRCAP | Interacting with H2AZ | [128] | |
| 13–16. P400/TRAPP specific subunits | ||||||
| MORF4L1 | MRG15 | General | p400/TRRAP (MRG15-MRGBP), HDAC Rpd3S/ Sin3S (MRG15-Pf1) | Chromatin reader that binds to H3K36me3, H3K4me1 and H3K4me3 | [121] | |
| MRGBP | Eaf7, MRG15BP, URCC4 | INO80/SWR1 | p400/TRRAP | Interaction with BDR8, MORF4L1 | [121] | |
| ING3 | ING2, EAF4 | General | p400/TRRAP, | Chromatin reader, binding to H3K4me3, interaction with TP53 | [121] | CASC7 |
| MEAF6 | EAF6 | General | p400/TRRAP, HAT complexes (eg., MOZ/MORF, NuA3) | Interaction with EAF4 | [121] | |
| ISWI (nucleosome spacing, DNA repair) | ||||||
| 1. Catalytic subunit (ATP-dependent helicase) | ||||||
| SMARCA5 | SNF2H | ISWI | WICH, NoRC, RSF, ACF/CHRAC | ATP-dependent helicase | [46] | |
| SMARCA1 | SNF2L | ISWI | NURF, CERF | [46] | DLEU1 | |
| SMARCAD1 | ADERM, BASNS, ETL1, HEL1, HRZ | ? | “CUE” |
ATP-dependent helicase, binds to H2A-ubiquitin, CUE-domain binds KAP1; maintaining H3K9me3 marks. |
[129] | |
| HELLS | SMARCA6 | ? | CHIRRC | ATP-dependent helicase, binds to CDCA7 | [48] | BlackMamba |
| 2. Signature subunit | ||||||
| BAZ1B | WSTF | ISWI | WICH | Histone phosphorylation (H2A.X-pY142), interacts with RNA polymerase II, stimulates transcription-coupled homologous recombination | [52] | |
| BAZ2A | Tip5, NoRC | ISWI | NoRC | Chromatin reader that binds to H3K4, H4K16ac, H3K14ac. Binds also to TCF7L2 and ncRNAs. Responsible for heterochromatin formation at major clusters of repetitive elements | [130, 131] | Lnc pRNA |
| RSF | HBXAP | ISWI | RSF | Remodeling and spacing factor 1; histone chaperone, involved in homologous recombination DNA repair | [132] | |
| BAZ1A | ACF1 | ISWI | ACF/CHRAC | Dimer ACF complex, RNF20-mediated chromatin relaxation, and KU70 interaction, mediating DNA repair | [55] | NEXN-AS1 |
| BPTF | NURF301 | ISWI | NURF | Chromatin reader binding to H3K4me3 and H4K16ac, interacts with AT rich DNA sequences | [57] | NMR (LINC01672) |
| CECR2 | CERF | ISWI | CERF | Chromatin reader binding to acetyl-lysine residues of histone H2A and H3, stimulating γH2A.X formation | [53] | |
| TRIM28 | KAP1 | ? | “CUE” | Maintaining H3K9me3 marks. | [129] | Paupar |
| CDCA7 | ICF3, JPO1 | ? | CHIRRC | Nucleosome sliding | [48] | FGD5-AS1 |
| 3–4 CHRAC subunits | ||||||
| CHRAC1 | YCL1, CHRAC15 | ISWI | ACF/CHRAC | Chromatin accessibility complex subunit 1; histone‐fold protein that form a stable complex with POLE3 and binds naked DNA | [76] | |
| POLE3 | CHRAC17, p17, YBL1 | General | ACF/CHRAC, DNA POL ϵ complex, HAT GCN5/PCAF complex | DNA polymerase epsilon 3; accessory subunit; histone H3, H4 chaperone | [133] | |
| 3–4 RB binding subunits | ||||||
| RBBP4 | NURF55, RBAP48 | General | NURF, NuRD , PRC2 complex | RB binding protein 4; histone tetramer deposition; histone H3 and BCL11A binding | [76] | |
| RBBP7 | RbAp46 | General | NURF, NuRD, PRC2 complex | Binding to histone H4, histone acetyltransferase HAT1 | [76] | |
| CHD (chromodomain helicase DNA-binding, DNA repair; NuRD, histone deacetylation/demethylase complex) | ||||||
| 1. Catalytic subunit (Chromodomain Helicase DNA-binding) | ||||||
| CHD1 | PILBOS | CHD1/ PAF1, CHD1/ SSRP1, CHD1/ NCoR CHD1/HAT complexes ( SAGA/SLIK/GCN5) | Chromatin reader that binds to H3K4me2/3, stabilization of H2AX at DSBs, stabilization of H2B(tail)K123ub | [67–70, 134] | MATN1-AS1 | |
| CHD2 | EEOC | CHD2/PARP-1 | Deposition of histone variant H3.3 in NHEJ DNA-repair | [72] | CHASERR | |
| CHD6 | CHD5, RIGB | CHD6/Polycomb units | Chromatin reader that binds to H3K27me3 | [135] | ||
| CHD7 | CRG, KAL5 | CHD7/SOX2, CHD7/SOX9, CHD7/8, PBAF | SOX2, SOX9, SMARCC2 binding | [79] | LINC01410 | |
| CHD8 | AUTS18 | CHD8/β-catenin, CHD8/CHD7, CHD8/MT complexes (BRD4-NSD3, BACH1-MAFG-DNMT3, KMT2) | Binds to histone H1, H3K36 methyltransferase (MT) complex | [80, 81] | ||
| CHD9 | KISH2 | CHD2/PPARα, CHD2/PPARγ, BAF |
Chromatin reader that binds to H3 (K9me2/3,K27me3), also interaction with PPARα, γ, SMARCA2. Ribosomal gene regulation |
[76] | ||
| 1. Catalytic subunit NuRD | ||||||
| CHD3 | Mi-2a | NuRD | NuRD, PRC2 complex | Generation of compacted chromatin after DNA replication; isoforms CHD3.1 and CHD3.3: SUMOylated KAP-1 binding; transcription factor interaction | [55] | |
| CHD4 | Mi-2b | NuRD | NuRD, PRC2 complex | Transcription factor interaction, interaction with RNF8 | [76, 136] | |
| CHD5 | NuRD | NuRD, PRC2 complex | H3K27me3 binding | [135] | ||
| 2. Interacting subunit | ||||||
| FAM124B | CHD7/8 | [86] | ||||
| 3. GATA-type Zn-finger subunit | ||||||
| GATAD2A | p66a | NuRD | NuRD/CHD5 | CHD and MBD2 binding | [75] | |
| GATAD2B | p68 | NuRD | NuRD/CHD5 | Protein-protein interaction, deacetylating, methylated nucleosomes | ||
| 4–5 Histone deacetylase Subunit | ||||||
| HDAC1 | general | NuRD, PRC2 complex | Histone deacetylase (Kac) | [76] | ANRIL | |
| HDAC2 | general | NuRD, PRC2 complex | SNHG15, ARAP1-AS1 | |||
| 6–7 RB binding subunits | ||||||
| RBBP4 | NURF55, RBAP48 | general | NURF, NuRD , PRC2 complex | RB binding protein 4; histone tetramer deposition, histone H3 and BCL11A binding | [76] | |
| RBBP7 | RbAp46 | general | NURF, NuRD, PRC2 complex | Binding to histone H4 and histone acetyltransferase HAT1 | ||
| 2. Interacting subunit | ||||||
| CTBP2 | NuRD | NuRD, PRC2 complex | C-terminal binding protein 2; NADH-dependent interaction with p300-Runx2 complex, decoy inhibiting transcriptional activation of this complex | [137] | ||
| 3. Methyl-CpG binding subunit | ||||||
| MBD3 | NuRD | NuRD, PRC2 complex | methyl-CpG binding domain protein 3; no binding to methylated DNA, mediates the association of MTA2 with HDAC, H3K4me3 binding | [136] | ||
| MBD2 | DMTase | NuRD | NuRD, PRC2 complex | methyl-CpG binding domain protein 2; reposition nucleosomes away from unmethylated CpG-rich regions of the genome | [136] | |
| 4. Metastasis-associated subunit | ||||||
| MTA1 | NuRD | NuRD, PRC2 complex | Metastasis-associated protein 1 | [76] | ||
| MTA2 | NuRD | NuRD, PRC2 complex | Metastasis-associated protein 2 | [76] | HOTAIR | |
| MTA3 | NuRD | NuRD, DMT complex LSD1/SIX3, PRC2 complex | Binds to pan-acetylated H3, histone demethylase, opposing action to MTA1, binding to BCL6 | [76] | ||
| 5. Associated subunit | ||||||
| CDK2AP1 | DOC1 | NuRD | NuRD/CHD3/4 | NuRD recruitment to displace SWI/SNF complex | [75] | |
ARID AT-rich interactive domain, ARP actin-related protein, BAF BRG1-associated factor, BAZ bromodomain adjacent to zinc finger domain, BRD bromodomain containing, BPTF bromodomain PHD finger transcription factor, CHD Chromodomain Helicase DNA-binding, CHIRRC CDCA7–HELLS ICF-related nucleosome remodeling complex, EAF Esa1- associated factor, HAT histone acetyltransferase, HDAC histone deacetylase, ISWI Imitation SWI, Kac acetyl-lysine, Ksuc succinyl-lysine, Kub ubiquitin-lysine, NURF nucleosome remodeling factor, NuRD Nucleosome remodeling and histone deacetylation, SMARC SWI/SNF related, matrix associated, actin-dependent regulator of chromatin, SNF Sucrose Non-Fermentable, SWI SWItch [128]