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CRISPR Editing of Hemoglobin Gene Shows Utility of Ribonucleoproteins in Hematopoetic Stem Cells

NEW YORK (GenomeWeb) – CRISPR gene editing using a purified Cas9 protein complexed with purified single guide RNA (sgRNA) offers a way to edit hematopoietic stem and progenitor cells and a possible path to gene editing therapies, according to a new study.

Led by first author Mark DeWitt and co-senior author Jacob Corn of the University of California, Berkeley, co-senior author Dana Carroll of the University of Utah, and co-senior author David Martin of the Children's Hospital Oakland Research Institute (CHORI), a team of researchers used the genome editing method in human-derived HSPCs to introduce new versions of the hemoglobin gene, the gene mutated in sickle cell disease and other hemoglobinopathies. They also showed that such cells could maintain edits for 16 weeks after being transplanted into immune-compromised mice.

"We feel we're getting a lot closer to a therapeutically useful level of editing," Carroll told GenomeWeb. "We did better than people had done before, using other platforms."

In a statement, Corn added, "There is still a lot of work to be done before this approach might be used in the clinic, but we’re hopeful that it will pave the way for new kinds of treatment for patients with sickle cell disease."

The scientists published their results yesterday in Science Translational Medicine, showcasing several ideas Corn's lab has developed to improve CRISPR editing efficiencies, especially when trying to leverage the homology directed repair (HDR) pathway for researcher-directed genome editing and not just random indel formation.

"Both the approach and the outcome are a bit different that what people have done before," Carroll said. Researchers have deployed other genome editing platforms, such as transcription activator-like effector nucleases and zinc finger nucleases (ZFNs), to similar effect. Sangamo Biosciences is also using its ZFN technology in pre-clinical studies for hemoglobinopathies.

Several CRISPR-focused researchers have also come up with clever strategies to address those diseases. As reported by GenomeWeb in 2015, scientists led by Dana-Farber Cancer Institute's Stuart Orkin came up with a way to use CRISPR/Cas9 editing to restart production of fetal hemoglobin, which could help ameliorate sickle cell disease. And in August of this year, a team from St. Jude Children's Research Hospital reported another CRISPR/Cas9-based editing strategy for hemoglobin disorders.

The Berkeley-Utah-CHORI team took a different tack. "Our approach is to go in and correct the mutation directly using an oligonucleotide donor," Carroll said. And the new study featured a twist: to establish their method for replacing the hemoglobin gene, the researchers actually took cells with the functioning wild-type allele and gave those cells the sickle cell mutation.

"It's not so easy to get cells from sickle cell patients," Carroll explained, and those they did acquire were used later, to establish that edited cells could reduce the sickle cell phenotype. The only difference between correcting the mutation and introducing it is a single nucleotide on the donor DNA used as a repair template, he said. Moreover, efficiencies of wild-type-to-sickle-cell-allele editing, and vice versa, were about the same.

The researchers first used CRISPR/Cas9 editing in an erythroleukemia cell line to screen several ribonucleoprotein complexes to find the most efficient ones. Then, they used those RNPs to develop ex vivo editing methods, using them to introduce the sickle cell mutation in HSPCs. They said they achieved 33 percent sequence displacement.

Finally, they validated that they could make the sickle cell mutation to wild-type edit in HSPCs form sickle cell patients, resulting in hemoglobin RNA and protein production. The results suggest the Cas9 RNP editing method is worth looking into as the foundation for hemoglobinopathy gene therapy.

Previous studies from bone marrow transplants indicate that even if the sickle cell patient takes up only 5 percent of wild-type bone marrow cells from the donor, they're still provided some therapeutic benefit, Carroll said.

Sixteen weeks after being transplanted into the immunocompromised mice, the edited alleles were found in anywhere between 1 percent and 6 percent of cells, approaching clinical utility. Carroll said the team was working on ways to improve that number.

While the electroporation used to get the RNPs into the cells could be improved, "the real key is to improve the efficiency of HDR," he said.

The study used a repair template design principle developed by the Corn lab, which can improve HDR-based editing of short DNA sections no longer than 30 base pairs. Without specifying what they are, Carroll said the team is already working on ways to improve the ratio of HDR events to indel-forming non-homologous end-joining events.

"Sickle cell disease is just one of many blood disorders caused by a single mutation in the genome," Corn said. "It’s very possible that other researchers and clinicians could use this type of gene editing to explore ways to cure a large number of diseases."