From Flies to Mice: The Emerging Role of Non-Canonical PRC1 Members in Mammalian Development
Abstract
:1. Introduction
1.1. Discovery of the Polycomb Repressor System
1.2. Evolutionarily Conserved Domains in PcG Proteins
1.3. Discovery of Polycomb Repressive Complexes
2. Mammalian PRC Complexes
2.1. Mammalian PcG Gene Functions: Parallels and Differences between Mammals and Fruit Fly
2.2. Classification of Mammalian PRC Complexes
3. Canonical PRC1 Complexes
4. Studying Mammalian PcG Functions with Embryonic Stem Cell and Mouse Models
4.1. Advantages of Mouse Models in Studying Gene Function during Development
- Mice are experimentally tractable mammalian model systems.
- Mice have short reproducing time, easy to breed and maintain.
- Mice have relatively short gestation (20 days) and big litter size (5 to 15 pups), brief time for sexual maturity and rapid generation time, which makes an ideal model for studying embryonic development.
- Mice have small size and are easy to handle.
- Mice have close similarities with human development and disease.
- The genome size, number of genes and genomic organization of mice are similar to humans.
- Mice are suitable for derivation of stem cells, such as ES cells, which can be re-introduced to the mouse germline.
4.2. Advantages of ES Cells in Studying Gene Function during Development
- If required, ES cells lines can be newly established from mice or other species (e.g., bovine, pig) by isolating morula or blastocyst stage embryos [198].
- There are reproducible experimental conditions and a more serum/animal free environment (small molecules, inhibitors and proteins).
- Well scalable thus high throughput experiments can be executed.
- There is no limitation of starting material due to unlimited self-renewal.
- ES cells can be differentiated to all cell types of the body.
- Differentiation conditions can be tightly controlled, which is highly desired for industrial applications.
- Culture conditions for maintaining ES cells and for differentiating them could be internationally standardized conferring high reproducibility to the experimental systems.
- Finally, studying human development by the utilization of existing and approved human ES cell lines [199] circumvents the ethical barriers, as it does not require destruction of preimplantation human embryos.
5. General Description of Mammalian ncPRC1s
6. Core Subunits of ncPRCs
6.1. Core Members of ncPRCs
6.2. The Function of Yy1
6.3. Detailed Description of the Composition and Function of Different ncPRC1 Type Complexes
6.3.1. ncPRC1.1
6.3.2. ncPRC1.2 and ncPRC1.4
6.3.3. ncPRC1.3 and ncPRC1.5
6.3.4. ncPRC1.6
7. Targeting of Different ncPRC1 Complexes
8. Conclusions and Future Questions
8.1. There Are Profound Differences in PRC Function between Fly and Mice
8.2. The Function of ncPRC1 Subunits Are often Essential for Mammalian Development
8.3. The Dosage and Interactions of ncPRC1 Subunits Is Critical for Mammalian Development
8.4. The Assembly of ncPRC1 Subunits Is still under Debate
8.5. The Activator Function of ncPRC1s Opens New Perspectives in Gene Regulation
8.6. More Emphasis Is Placed on Integrative Approaches to Analyze ncPRC1 Functions in Differentiation
8.7. NcPRCs Have a Profound Role in Extraembryonic Lineage Commitment
8.8. The Role of ccPRCs in Initiating and Maintaining Naïve vs. Primed Pluripotent States Are Not Established
9. Concluding Remarks
Acknowledgments
Author Contributions
Conflicts of Interest
References
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Short Name of Mouse Homolog | Synonyms | ID Numbers (MGI, UNIPROT) | Chromosomal Localization | Drosophila Orthologs | Protein Domains and Conserved Regions | Complex |
---|---|---|---|---|---|---|
Auts2 | - | MGI:1919847 UniProt Q8VDM3 | Ch: 5 | TAY limited similarity | None predicted | ncPRC 1.3/1.5 |
Bcor | - | MGI:1918708 UniProt: Q8CGN4 | Ch: X | CG14073 limited similarity | PFUD:PCGF1 binding domain, Ankyrin repeat: protein interaction Blc6 non ankyrin domain | ncPRC1.1 and BCOR |
Cbx3 | Hp1γ | MGI:109372 UniProt Q61686 | Ch: 15 | HP1 | Chromo domain: H3K27 binding Chromo shadow: dimerization, protein binding | ncPRC 1.6 |
Csnk2a2 | Ck2 | MGI:88547 UniProt O54833 | Ch: 8 | CKIIalfa | Protein kinase domain: catalytic, phosphorylation | ncPRC 1.3/1.5 |
E2f6 | - | MGI:1354159 UniProt O54917 | Ch: 12 | No homolog identified | Winged helix-like: DNA binding CC-MB domain: E2F-DP1 dimerization | ncPRC1.6 |
Fbrs | Fbs, Fbs1 | MGI:104648 UniProt Q8R089 | Ch: 7 | TAY has limited similarity | None predicted | ncPRC 1.3/1.5 |
Hdac1 | Rpd3, Hd1 | MGI:108086 UniProt O09106 | Ch: 4 | HDAC1/RPD3 | Histone deacetylase domain: removing acetyl group from histones | ncPRC 1.6 |
Hdac2 | Yaf1, Yy1bp | MGI:1097691 UniProt P70288 | Ch: 10 | HDAC1/RPD3 | Histone deacetylase domain: removing acetyl group from histones | ncPRC 1.6 |
Kdm2b | Fbxl10, Jhdm1b, Cxxc2, | MGI:1354737 UniProt Q6P1G2 | Ch: 5 | dKDM2 | Ring domain: protein interaction JMJC domain: histone demethylation FBOX: protein interaction with SKP1 Zn finger CXXC: CpG binding | ncPRC1.1 and BCOR |
L3mbtl2 | M4mbt | MGI:2443584 UniProt P59178 | Ch: 15 | L3MBT | FCS-type Zn finger: 4 MBT: mono-, dimethylated histone binding | ncPRC 1.6 |
Max | bHLHd4 | MGI:96921 UniProt P28574 | Ch: 12 | MAX | HLH: DNA binding | ncPRC 1.6 |
Mga | Cdrap, Mia1 | MGI:109615 UnidKDM2Prot Q61865 | Ch: 7 | BYN/TRG limited similarity | T-box: DNA binding CDD, HLH: DNA binding | ncPRC 1.6 |
Pcgf1 | Nspc1, Rnf68 | MGI:1917087 UniProt Q8R023 | Ch: 6 | PSC, SU(Z)2 | Ring domain: dimerization RAWUL: BCOR binding | ncPRC1.1 |
Pcgf2 | Mel18 | MGI:99161 UniProt P23798 | Ch: 11 | PSC, SU(Z)2 | Ring domain: dimerization RAWUL: protein interaction | ncPRC1.2/1.4 |
Pcgf3 | Dong1, Rnf3 | MGI:1916837 UniProt Q8BTQ0 | Ch: 5 | PSC, SU(Z)2 | Ring domain: dimerization RAWUL: protein interaction | ncPRC 1.3/1.5 |
Pcgf4 | Bmi1, Rnf51 | MGI:88174 UniProt P25916 | Ch: 2 | PSC, SU(Z)2 | Ring domain: dimerization RAWUL: protein interaction | ncPRC 1.2/1.4 |
Pcgf5 | Rnf159 | MGI:1923505 UniProt Q3UK78 | Ch: 19 | PSC, SU(Z)2 | Ring domain: dimerization RAWUL: protein interaction | ncPRC 1.3/1.5 |
Pcgf6 | Mblr, Rnf134 | MGI:1918291 UniProt Q99NA9 | Ch: 19 | PSC, SU(Z)2 | Ring domain: dimerization RAWUL: protein interaction | ncPRC 1.6 |
Ring1 | Ring1A | MGI:1101770 UniProt: O35730 | Ch: 17 | SCE/dRING | Ring domain: dimerization RAWUL: Cbx, Rybp binding | CORE |
Rnf2 | Ring2, Ring1B, dinG | MGI:1101759 UniProt Q9CQJ4 | Ch: 1 | SCE/dRING | Ring domain: dimerization RAWUL: Cbx, Rybp binding | CORE |
Rybp | Dedaf, Yeaf1 | MGI:1929059 UniProt Q8CCI5 | Ch: 6 | dRYBP | RanBP2-type Zn finger: YAF2/RYBP C-terminal binding: RING binding | CORE |
Skp1a | Skp1, p19 | MGI:103575 UniProt Q9WTX5 | Ch: 11 | dSKPA | POZ domain, dimerization domain | ncPRC1.1 |
Tfdp1 | Dp1, Drtf1 | MGI:101934 UniProt Q08639 | Ch: 8 | dDP | Winged helix-like: DNA binding Dimerization domain: E2F-DP1 dimerization | ncPRC1.6 |
Usp7 | Hausp | MGI:2182061 UniProt Q6A4J8 | Ch: 16 | USP7 | MATH/TRAF, ubiquitin protease | ncPRC1.1 |
Wdr5 | Big, Big3 | MGI:2155884 UniProt P61965 | Ch: 2 | WDS | WD repeats | ncPRC1.6 |
Yaf2 | - | MGI:1914307 UniProt Q99LW6 | Ch: 15 | Only RYBP present | RanBP2-type Zn finger: YAF2/RYBP C-terminal binding: RING binding | CORE |
Yy1 | - | MGI:99150 UniProt Q00899 | Ch: 12 | PHO | CH2 Zn-finger: DNA binding REPO: Recruitment of PC | INTERACTOR of Rybp/Yaf2 |
Gene Name | Embryonic Phenotype | Extra-Embryonic Phenotype | ES Cell Phenotype | Role in Lineage Commitment | Ref. | ||||
---|---|---|---|---|---|---|---|---|---|
NEU | CAR | HEM | GER | MISC | |||||
Ring1 | Ring1−/− viable | ND | No | No | No | No | No | Homeotic transformation of the axial skeleton | [151] |
Rnf2 | Rnf2−/− E6.5–E7.0 lethal Rnf2+/− mice are viable with homeotic transformations | Defects | No | Premature differentiation | Premature differentiation | ND | ND | ND | [226,227,228,229,230] |
Ring1-Rnf2 double knockout | ND | ND | Proliferation arrest | ND | ND | ND | ND | ND | [235] |
Rybp | Rybp−/− E5.0–E6.0 lethal; Rybp+/−semipenetrant lethal at birth due to NTDs | ND | No | Impairment in terminal phase of differentiation | Impairment in contractile cardiomyocyte formation | Increased number of B-1 progenitors and loss of B-2 progenitors | ND | ND | [166,240,243,244,245] |
Yaf2 | Yaf2−/− ND | ND | ND | ND | ND | ND | ND | ND | - |
Gene Name | Embryonic Phenotype | Extra-Embryonic Phenotype | ES Cell Phenotype | Role in Lineage Commitment | Ref. | ||||
---|---|---|---|---|---|---|---|---|---|
NEU | CAR | HEM | GERM | MISC | |||||
Pcgf1 | ND | ND | Impaired differentiation | Promotes ectodermal lineage specification | Promotes mesodermal lineage specification | Promotes mesodermal lineage specification | No | Promotes ectodermal lineage specification | [264] |
Kdm2b | Kdm2b−/− semipenetrant lethal at birth due to NTDs | ND | Premature differentiation | Altered cell-cycle processes in neural precursors | Induces early mesoderm differentiation | Impaired hematopoiesis | Reduced number of spermatozoa | Induces early endoderm differentiation | [162,280,282] |
Bcor | Bcor−/− E5–E6.5 male lethal | Defect in extraembryonic tissues | ND | Delayed activation of genes responsible for ectodermal lineage specification | Delayed activation of genes responsible for mesodermal lineage specification; failure of heart looping | Impaired mesodermal lineage specification; and primitive erythrocyte formation | ND | ND | [272,273] |
Skp1 | Skp1−/− ND | ND | ND | Increases susceptibility to cell death in neuronal cells in mice | ND | Reduced proliferation in the lymphoid organs | ND | Hypoplasia | [289,290] |
Usp7 | Usp7−/− E6.5–E7.5 lethal | Defect in extraembryonic tissues | ND | Promotes neuronal differentiation and disrupts self-renewal | ND | ND | ND | Compromised osteogenic differentiation | [294,296,298] |
Gene Name | Embryonic Phenotype | Extra-Embryonic Phenotype | ES Cell Phenotype | Role in Lineage Commitment | Ref. | ||||
---|---|---|---|---|---|---|---|---|---|
NEU | CAR | HEM | GERM | MISC | |||||
Pcgf2 | Pcgf2−/− viable, but growth retardation, posterior transformations of the axial skeleton | No | No | ND | Impairs proper cardiac differentiation | Compromised T and B lymphocyte development | ND | Hypertrophy of intestinal smooth muscle, obstruction of the lower intestine | [80,301,305] |
Pcgf4 | Pcgf4−/− viable | No | Defect in postnatal stem cell maintenance in hematopoietic and neural tissues | Postnatal stem cell maintenance in neural tissues; neurological abnormalities | Represses cardio-myocyte fate | Postnatal stem cell maintenance in hematopoietic tissues; defect in hematopoiesis | ND | ND | [148,306,307,310] |
Gene Name | Embryonic Phenotype | Extra-Embryonic | ES Cell Phenotype | Role in Lineage Commitment | Ref. | ||||
---|---|---|---|---|---|---|---|---|---|
NEU | CAR | HEM | GERM | MISC | |||||
Pcgf3 | Pcgf3−/− viable | No | No | No | No | No | No | Impairs mesoderm differentiation, absent spleen | [180,311] |
Pcgf5 | Pcgf5−/− viable | No | No | No | No | No | No | Impairs mesoderm differentiation | [31,32] |
Pcgf3-Pcgf5 double knockout | Pcgf3−/−/Pcgf5−/− female-specific embryo lethality at mid-gestation | Placental defects; lack of throphoblast and labirynth cell layers | No | No | No | No | No | Impairs mesoderm differentiation | [311] |
Auts2 | Auts2−/− ND | ND | ND | Defects in CNS development in mice; Auts2+/− ES cells have premature neuronal differentiation during in vitro corticogenesis | Mesodermal genes are upregulated in Auts2+/− ES cells during in vitro corticogenesis | ND | ND | ND | [311,313] |
Fbrs | Fbrs−/− ND | ND | ND | ND | ND | ND | ND | ND | - |
Ck2 β * | Ck2 β−/− E3.5 lethal | ND | CK2β is required for stem cell maintenance | In NES conditional mutants defect in oligodendrogenesis in telencephalon; NTDs | ND | Improper hematopoietic differentiation | Male mice are infertile | Improper adipogenic and osteogenic differentiation | [317,318,319,320] |
CK2α * | CK2α−/− E9.5–10.5 lethal | ND | ND | ND | NTDs. improper branchial arch and heart development | ND | ND | ND | [318,319,320] |
CK2α’ * | CK2α’−/− viable but infertile | ND | ND | ND | ND | ND | Defect in germ cell development | ND | [318,319,320] |
Gene Name | Embryonic Phenotype | Extra-Embryonic Phenotype | ES Cell Phenotype | Role in Lineage Commitment | Ref. | ||||
---|---|---|---|---|---|---|---|---|---|
NEU | CAR | HEM | GERM | MISC | |||||
Pcgf6 | Pcgf6−/− ND | ND | Decreased proliferation; required for maintaining ES cell pluripotency | ND | ND | Suppresses dendritic cell activation | Suppress premature differentiation; Ectopic male germ cell specific gene expression | Ectopic mesodermal specific gene expression | [173,338,339,340,341] |
E2f6 | E2f6−/− viable with homeotic transformations | No | ND | No | No | No | Oligozospermia, ectopic male germ cell specific gene expression | ND | [345,346] |
Tfdp1 | Tfdp1−/− E10.5–E11.5 lethal | Defect in trophectoderm development, disorganized ectoplacental cone | ND | ND | ND | ND | ND | ND | [347] |
L3mbtl2 | L3mbtl2−/− E6.5 lethal | No distinct pro-amniotic cavity, chorion or amnion | Compromised proliferation of ES cells | ND | ND | ND | ND | No EB formation | [215] |
Max | Max−/− E5.0–E5.5 lethal | Growth arrest | Compromised proliferation of ES cells | ND | ND | ND | Early meiotic entry in vitro ectopic expression of germ cell related genes | ND | [181,182,343] |
Mga | Mga−/− E5.0–E5.5 lethal | Empty decidua capsularis | Not viable | ND | ND | ND | ND | ND | [344] |
Cbx3 | Cbx3−/− viable | No | ND | ND | ND | ND | Compromised spermatogenesis, male infertility, small testis | ND | [335] |
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Share and Cite
Bajusz, I.; Kovács, G.; Pirity, M.K. From Flies to Mice: The Emerging Role of Non-Canonical PRC1 Members in Mammalian Development. Epigenomes 2018, 2, 4. https://doi.org/10.3390/epigenomes2010004
Bajusz I, Kovács G, Pirity MK. From Flies to Mice: The Emerging Role of Non-Canonical PRC1 Members in Mammalian Development. Epigenomes. 2018; 2(1):4. https://doi.org/10.3390/epigenomes2010004
Chicago/Turabian StyleBajusz, Izabella, Gergő Kovács, and Melinda K. Pirity. 2018. "From Flies to Mice: The Emerging Role of Non-Canonical PRC1 Members in Mammalian Development" Epigenomes 2, no. 1: 4. https://doi.org/10.3390/epigenomes2010004
APA StyleBajusz, I., Kovács, G., & Pirity, M. K. (2018). From Flies to Mice: The Emerging Role of Non-Canonical PRC1 Members in Mammalian Development. Epigenomes, 2(1), 4. https://doi.org/10.3390/epigenomes2010004