HIF1A contributes to the survival of aneuploid and mosaic pre-implantation embryos
Posted on: 11 October 2024
Preprint posted on 19 July 2024
Categories: cell biology, developmental biology, genetics, molecular biology
Background:
Human embryo development is an inefficient process in which two out of three embryos will not develop. The degree of chromosomal mosaicism (presence of euploid and aneuploid cells in the embryo) correlates with developmental fitness, implantation and survival of the embryo 1–3. However, how the microenvironment affects mosaicism, and how the embryo manages it is currently unknown. Addressing these points becomes critical not only to understand the molecular processes underlying embryonic robustness, but also to improve human embryo culture and fitness for reproductive medicine purposes.
Given the ethical concerns of working with human preimplantation embryos, the authors of this preprint turned to the mouse embryo as a model in this study. Of note, chromosomal mosaicism drastically differs between human (70%) and mouse (25%) preimplantation embryos in normal conditions3,4. To overcome this species-specific issue, the authors used two different MSP1 checkpoint inhibitors (Reversine and AZ3146) which trigger aneuploidy and mosaicism in the cleaving mouse embryos. Under this approach, the authors aimed to elucidate: i) what the fate is of aneuploid cells in the embryo (lineage wise) and ii) how hypoxia conditions affect developmental fitness of aneuploid and euploid cells.
Methods in a nutshell:
The authors cultured in vitro mouse preimplantation embryos. Between the 4-cell to 8-cell stage,chromosomal mosaicism was induced using MSP1 inhibitors. Afterwards, the medium was washed and the authors left the embryos to develop until late blastocyst stage (E4.5). Most of the experimental approach revolved around immunofluorescence staining of the embryos; the authors assessed, among different things, i) the presence of micronuclei and chromosome number imbalances by arresting cells in metaphase; ii) the DNA damage and repair activity in the embryo (by means of PARP1 and gH2AX expression, respectively); iii) the localization of HIF1a protein; as well as iv) the contribution of early embryonic cells towards the Epiblast, Primitive endoderm and Trophectoderm (staining for NANOG, SOX17 and CDX2 markers, respectively). In addition, the authors generated chimeras of euploid vs. mosaic cells from fluorescent-tagged mouse embryos to understand cellular competition across preimplantation development.
Key findings:
AZ3146 and Reversine MSP1 inhibitors trigger aneuploidy but also differential stress responses in the embryo.
The authors could confirm that MSP1 inhibition leads to aneuploidy and mosaicism associated events such as micronuclei formation in the embryo, as previously reported5. However, they observed an intriguing difference between both MSP1 inhibitors tested; while aneuploidy caused by reversine is accompanied by p53-dependent apoptosis and a sustained DNA damage response through morula and blastocyst stages, AZ3146 did not trigger a p53 response. In turn, AZ3146 increased HIF1a expression across preimplantation development. Furthermore, by performing challenging embryo transfer experiments, the authors could prove that reversine-treated embryos cannot develop, while 20% of AZ3146-treated embryos were born after transfer to the mother’s decidua. This suggests that differential stress responses of MSP1 inhibitors, rather than mosaicism or aneuploidy itself, controls embryo competence.
Hypoxia balances chromosomal mosaicism by cell competition between aneuploid and euploid embryonic cells.
Previous data suggest apoptotic clearance of Epiblast aneuploid cells in embryos treated with reversine5. By comparing both MSP1 inhibitor treatments, the authors sought to understand if this is something driven by aneuploidy or secondary effects of the drugs. Given the specific upregulation of the hypoxic master regulator HIF1a in embryos treated with AZ3146, the authors hypothesized that hypoxia might control aneuploid cell fate leading to embryo competence. After performing chimeric embryo experiments, they concluded that hypoxia supports epiblast euploid cell fitness over aneuploid cells, but not in extraembryonic lineages (trophoblast and primitive endoderm). Later on, they demonstrate that this effect is HIF1a specific. These results suggest that hypoxia enhances developmental competence by supporting euploid cellular fitness in the epiblast.
Why I chose this preprint?
I am very interested in understanding how cellular lineages respond to microenvironmental changes and sources of cellular stress in the context of development. The causes of the elevated rate of spontaneous human miscarriages per pregnancy are poorly understood, in great part due to the lack of human embryo availability for research purposes. This translates to enormous economic loss in the health care sector, as well as psychological and sociological hurdles that the pregnant mother and family have to overcome.
I like the approach taken by the authors to mimic mosaicism in the mouse embryo, and how they link a critical environmental factor like hypoxia to mosaicism, lineage specification and embryo viability. In fact, hypoxic conditions surround the embryo both in vivo (in the uterus) as well as in vitro during human in vitro fertilization (IVF) cycles, and it is perhaps not surprising how this can support the fittest conditions for embryo growth. I believe the next steps of this story should uncover the molecular mechanisms linking hypoxia and mosaicism in the embryo, and how this translates to physiological human embryo mosaic conditions.
Questions to the authors:
1) What are the aneuploidy rates of AZ3146 vs. Reversine treatment, beyond micronuclei formation? How many of the mitosis events under these treatments show imbalances in the number of chromosomes? I think this is an important quantification to understand the downstream effects of both MSP1 inhibitors.
2) It is very interesting to see how AZ3146 treatment does not seem to affect p53 signaling as reversine treatment does; however, relying only on TP53 mRNA levels can be misleading. Have you checked p53 Ser-15 phosphorylation or downstream targets of the cascade? Did you compare apoptotic rates between treatments? In a recent article, Regin et al. 6 demonstrate that aneuploidy-driven by Reversine triggers proteotoxic stress and autophagy; do you think similar events occur in AZ3146 treatment?
3) Recent discoveries point to the elevated replicative stress in the first cleavages as a source of chromosomal mosaicism in human embryos (Palmerola et al. Cell (2022)7). Besides this, MSP1 inhibition leads to massive and unscheduled aneuploidy. Do you think that triggering mild replicative stress (ie. with low doses of the DNA polymerase inhibitor Aphidicolin) could be a better option to mimic mosaicism than MSP1 inhibition?
4) Why do you think the epiblast does not tolerate the presence of aneuploid cells as well as extraembryonic lineages?
5) Do you think your findings translate well to human embryos? How comparable is physiological human embryo mosaicism to MSP1-I driven mosaicism in mouse embryos?
References:
- Capalbo, A. & Rienzi, L. Mosaicism between trophectoderm and inner cell mass. Fertility and Sterility vol. 107 1098–1106 (2017).
- Mccoy, R. C. Mosaicism in Preimplantation Human Embryos: When Chromosomal Abnormalities Are the Norm. (2017) doi:10.1016/j.tig.2017.04.001.
- Vanneste, E. et al. Chromosome instability iscommon in human cleavage-stage embryos. Nat. Med. Vol. 15, (2009).
- Lightfoot, D. A., Kouznetsova, A., Mahdy, E., Wilbertz, J. & Höög, C. The fate of mosaic aneuploid embryos during mouse development. Dev. Biol. 289, 384–394 (2006).
- Bolton, H. et al. Mouse model of chromosome mosaicism reveals lineage-specific depletion of aneuploid cells and normal developmental potential. Nat. Commun. 2016 71 7, 1–12 (2016).
- Regin, M. et al. Complex aneuploidy triggers autophagy and p53-mediated apoptosis and impairs the second lineage segregation in human preimplantation embryos. Elife 12, (2023).
- Palmerola, K. L. et al. ll Replication stress impairs chromosome segregation and preimplantation development in human embryos. Cell 185, 2988–3007 (2022).
doi: https://doi.org/10.1242/prelights.38652
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