Imprinting as Basis for Complex Evolutionary Novelties in Eutherians
Abstract
:Simple Summary
Abstract
1. Introduction
2. Theories of Evolution of Genomic Imprinting
3. Imprinting from the Vantage Point of Diploidy and Haploidy
4. The Importance of Dosage Compensation
5. Monoallelic Expression in Development and Disease
6. The Broader Picture of Allele-Specific Expression
7. Evolution of Imprinting in Organs
- (1)
- Placenta
- (2)
- Brain
8. Conclusions
- (1)
- The comparison of theories regarding the origin of imprinting demonstrates that all current hypotheses explain certain, but not all, aspects of why such a complex and vulnerable regulatory process evolved with the origin of mammals.
- (2)
- Imprinting might represent a functional haploidy of some genes. Regarding an allele-specific expression, imprinting is not a unique feature in mammals. This aspect is also known in immune and neuronal adhesion molecules. Therefore, comparing effects of imprinting in several regions of the body could provide insights into the evolution of this mechanism.
- (3)
- Imprinting is important in gene dosage regulation, while the origin of expression (maternal or paternal) might be irrelevant in these instances. A monoallelic expression possibly allows a better fine-tuning of gene regulation. Over- and under-expression of distinct genes can cause a phenotypic effect, which are often contrary in their phenotypic aspects. Several imprinted genes are dysregulated in cancer and other severe pathological processes. Notably, XCI and imprinting share many common features, including gene dosage compensation. Research into the similarities and differences of XCI and imprinting (silencing) of single genes potentially enables not only the understanding of dosage effects, but also of threshold effects and roles in gene regulatory networks that depend on precise dosages.
- (4)
- Disturbed monoallelic expression is not only known for imprinting disorders. For example, an escape of XCI is regularly suggested as a reason for higher prevalence of auto-immune diseases women. LOI (loss of prominent imprinting) is associated with many congenital disorders and might be also involved in tumorigenesis, neurological disorders, and complications of pregnancy such as pre-eclampsia. For that reason, and following up on point 2 and 3 above, is it important to further investigate the mechanisms of gene regulations (dosage, imprinting), as this might lead to new treatments using, for example, CRISPR to regulate gene dosages, and therefore reduce the impact of XCI escape or LOI.
- (5)
- Beside the classical canonical imprinting based on parent-specific DNA methylation, an additional mechanism of imprinting exists. The non-canonical imprinting is based primarily on histone modifications and was described in embryonic stages and extraembryonic tissues. However, this layer of epigenetic regulation is poorly conserved among species and the detailed role(s) of non-canonical imprinting remains to be elucidated. The description of developmental stage specific imprinted genes in mice suggests that imprinting is more complex than previously thought.
- (6)
- The biased allele-specific expression (ASE), erroneously also designated as non-canonical imprinting, stresses the concept of a uniform biallelic expression and the current hypothesis of the occurrence of imprinting. With the implementation of single-cell expression analysis and the investigation of epigenetic modifications, future research will not only focus on the spatiotemporal expression patterns but also ASE.
- (7)
- The placenta as an evolutionary novelty and the massive brain enlargement are the hallmarks of mammals. Both organs represent hotspots of imprinting, and several imprinting disorders are associated with neurological and placental anomalies. The placenta–brain axis signifies how the placenta modulates fetal brain development. Genomic imprinting allows a high plasticity on cells and organs, and both organs are characterized by high plasticity and their capability of fast adaptations to environmental changes. Genomic imprinting might not only contribute substantially to the plasticity of the placenta–brain axis but might be the key evolutionary driver of these organs.
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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DNMTs | Function | References |
---|---|---|
DNMT1 | mainly maintains methylation and therefore imprints | [32,118] |
DNMT2 | transfer RNA methylation | |
DNMT3 | de novo methylation of unmethylated DNA | |
DNMT3A | imprinting and methylation at major satellite repeats; maternal-specific germline DMR methylation occurs postnatally in growing oocytes but prenatally in prospermatogonia before onset of meiosis in male germline | [119,120] |
DNMT3B | minor satellite repeat methylation | [121] |
Dnmt3c (rodents) | methylates young retrotransposons in male germ line | [122] |
DNMT3L | contains no catalytic domain for methylation, instead, it co-orchestrates de novo methylation; establishes genomic imprints in oocyte | [123,124] |
Canonical Imprinting | Non-Canonical Imprinting | ASE | |
---|---|---|---|
Establishment of imprinting | DNA methylation in oocyte or sperm at imprinting control region | H3K27me3 H2AK119ub | Allele-specific histone modifications (H3K9ac; H3K9me3) |
Established by | Oocyte: Dnmt3a, Dnmt3L, Kdm1b, Zfp57; Sperm: Dnmt3a, Dnmt3b, Dnmt3L, piRNA, CTCFL/Prm7 | PRC2, Pcg1/6-PRC1 | Unclear |
Maintenance of imprinting | ZFP57 and/or ZNF445 required to maintain DNA-methylation of imprinting control regions | H3K27me3 replaced by monoallelic DNA methylation | Unclear |
Regulated by | Dnmt1, Dppa3, Zfp57 | PRC2, Smchd1 | Unclear |
Set of imprinting | During oogenesis and spermatogenesis | During oogenesis | Unclear |
Location | Widely distributed over the body, predominantly in neural and placental tissues | Extraembryonic and embryonic cell lineages | Widely distributed over the body, highly tissue-specific |
Conservation between species | High | Low | Unclear |
Clinical picture of imprinting abnormalities | Infertility, moles, miscarriage, classical clinical pictures of imprinting disorders such as Angelman, Beckwith–Wiedemann or Prader–Willi syndrome | Placental defects in murine loss of function/loss of prominent imprinting mutants with (sub)-lethality | Unclear |
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Schuff, M.; Strong, A.D.; Welborn, L.K.; Ziermann-Canabarro, J.M. Imprinting as Basis for Complex Evolutionary Novelties in Eutherians. Biology 2024, 13, 682. https://doi.org/10.3390/biology13090682
Schuff M, Strong AD, Welborn LK, Ziermann-Canabarro JM. Imprinting as Basis for Complex Evolutionary Novelties in Eutherians. Biology. 2024; 13(9):682. https://doi.org/10.3390/biology13090682
Chicago/Turabian StyleSchuff, Maximillian, Amanda D. Strong, Lyvia K. Welborn, and Janine M. Ziermann-Canabarro. 2024. "Imprinting as Basis for Complex Evolutionary Novelties in Eutherians" Biology 13, no. 9: 682. https://doi.org/10.3390/biology13090682