Allele-Specific Chromosome Removal after Cas9 Cleavage in Human Embryos

CRISPR/Cas9 was supposed to be used in this study to change a mutation in human embryos that cause a genetic disease. This disease is mediated by a mutation in the EYS gene and causes blindness (retinitis pigmentosa, retinal degeneration). The scientists envisaged that CRISPR/Cas9 causes a double-strand break (DSB) within the mutated EYS gene of the paternal chromosome in the fertilized human embryo. The maternal chromosome (without the disease-causing mutation) should now serve as a repair template to repair the DSB in the EYS gene. The guide RNA (gRNA) for the gene scissors was designed in such a way that the CRISPR/Cas9 system recognizes the mutant EYS allele (i.e. the disease-causing variant of the EYS gene) of the father, but not the normal one of the mother.

A male patient with the disease served as a donor for the trials. Donor egg cells were fertilized with the sperm (at different developmental stages of the embryo) and CRISPR/Cas9 plus the gRNA were introduced as well. In none of the experiments, as initially assumed, was the maternal, healthy gene used during the genome editing process in the cell to repair the double-strand break in the paternal chromosome. Half of the genome-edited embryos contained cells in which the target region of the EYS gene of the father was changed (small insertions, deletions or point mutations). Surprisingly, however, the scientists found that in many cases parts of the paternal chromosome 6, on which the EYS gene is located, up to the entire chromosome 6 have been lost. Unrepaired double strand breaks within the target sequence of the EYS gene apparently lead to the fact that the chromosomes cannot be completely divided between the two daughter cells during cell division, as is normal. This causes the loss of large parts of the chromosome or the entire chromosome during cell division. Normally, specific control mechanisms detect damage to the DNA prior to cell division and prevent damaged cells from dividing. As the authors state, it remains unclear why these control mechanisms do not work in the case of a double-strand break caused by CRISPR/Cas9. It is also questionable why the double-strand breaks in the experiments remained unrepaired for so long and were not recognized by the cell’s own repair mechanisms. The fate of the lost chromosomes or parts of them also remains unexplained. It is possible that parts of it could be incorporated again at a different part in the genome. Another study has already indicated in human cell lines that parts of chromosomes can become enclosed in micronuclei after the application of CRISPR/Cas9.

The loss of chromosomal parts can have various effects on the development of the embryo: cancer cells can develop, birth defects can occur or the embryo can die.

The scientists also found loss of chromosonal parts might be caused by DSBs at off-target areas, i.e. areas that are very similar to the actual target sequence and can be cut by the gene scissors: The unintended activity of the CRISPR/Cas9 on an off-target site on chromosome 16 caused the loss of parts of both the paternal and maternal chromosomes.

The authors of the study argue that the further development of Cas variants (e.g. Base Editing and Prime Editing) must be promoted, which do not cut both DNA double strands making this effect less likely.

Zuccaro MV, Xu J, Mitchell C, Marin D, Zimmerman R, Rana B, Weinstein E, King RT, Palmerola KL, Smith ME, Tsang SH, Goland R, Jasin M, Lobo R, Treff N, Egli D (2020) Allele-Specific Chromosome Removal after Cas9 Cleavage in Human Embryos. Cell. doi:https://doi.org/10.1016/j.cell.2020.10.025