Making a monkey out of MISTRG mice

From the Rongvaux Laboratory, Clinical Research Division

Autologous hematopoietic stem cell (HSC) gene therapy can be used to treat various blood cell diseases. Genes can be added or edited in stem cells before being transplanted back into the patient. Such treatments could potentially cure HIV/AIDS, sickle-cell disease, and severe-combined immunodeficiency, among others. In order to ensure that autologous HSC gene therapies work safely, they are tested extensively in nonhuman primates (NHPs) prior to use in humans. HSCs in NHPs engraft similarly to human HSCs, and NHPs are so genetically similar to humans that they are ideal for testing of such therapies. However, conducting these experiments requires special facilities and is extremely costly. While laboratory mice are more cost-effective and convenient to experiment on, their immune systems are too dissimilar to humans. As a result, therapies that are successful in mice are not always effective or safe in patients.

The laboratories of Drs. Anthony Rongvaux and Hans-Peter Kiem (Clinical Research Division) published a study in Experimental Hematology on NHP HSC engraftment without transplanting cells into NHPs. Instead, they transplanted NHP HSCs into mice modified to express human genes which promote engraftment, known as MISTRG mice. This “monkeynized” mouse model would allow high-throughput screening of treatments and would be available for testing in labs that do not use NHP models.

Schematic showing the development of treatment strategies of HSC gene therapy. Monkeynized MISTRG mice are a new model which could reduce the need for large-animal model testing.
Schematic showing the development of treatment strategies of HSC gene therapy. Monkeynized MISTRG mice are a new model which could reduce the need for large-animal model testing. Image by Dr. Stefan Radtke

This study, led by Research Associate Dr. Stefan Radtke, compared NHP HSC transplants into two immunodeficient mouse models, NSG and MISTRG. NSG mice are deficient in B, T, and NK cells, and have been previously used for their ability to engraft human HSCs. The researchers transplanted NHP HSCs into NSG mice, and noted that they do not engraft, despite various subsets of HSCs and doses used. They hypothesized that the difference between human and NHP HSC engraftment in these mice could be due to a genetic polymorphism in the NSG SIRPα protein. SIRPα provides a “don’t eat me” signal to macrophages, and while NSG SIRPα can cross-react with human cells, it might not bind effectively to NHP cells. In order to counter this lack of SIRPα binding to NHP cells, Dr. Rongvaux and colleagues tested MISTRG mice. These mice contain knocked-in human SIRPA, along with other human cytokines involved in hematopoiesis. After transplanting CD34+ NHP HSCs into MISTRG mice, the scientists tracked engraftment over time. They noticed that differentiated NHP cells appeared in the spleen, bone marrow, thymus, and peripheral blood. These differentiated cells included monocytes, granulocytes, NK cells, B cells, and CD4+ and CD8+ T cells up to the experimental endpoint of 20 weeks post-transplant, demonstrating robust engraftment.

When asked why he thought the MISTRG mice were able to engraft NHP HSCs where NSG mice failed, Dr. Radtke said, “MISTRG mice are genetically modified and specifically optimized to support the development of human blood cells. Since humans and macaques are evolutionary closely related, we believe that these modifications are also crucial for the engraftment of nonhuman primate cells.”

The researchers believe this model will be useful for many future studies. Dr. Radtke said, “Virtually all of our nonhuman primate studies focusing on the blood system can be tested in this new monkeynized mouse model. Availability of the monkeynized mouse model nicely complements the humanized mouse and enables us to close the gap in between basic and translational stem cell research. For the Kiem Lab, this model is of particular interest to develop and test novel stem cell gene therapy/editing approaches, HIV immunization strategies, and CAR-T cell-mediated immunotherapy applications. The ability to perform an unbiased high-throughput screening of strategies in this new mouse model will enable us to pre-evaluate alternative approaches and ultimately enhance the clinical translation of ongoing projects.”

 

Radtke S, Chan Y-Y, Sippel TR, Kiem H-P, Rongvaux A. 2019. MISTRG mice support engraftment and assessment of nonhuman primate hematopoietic stem and progenitor cells. Experimental Hematology.70:31-41.e1. DOI: https://doi.org/10.1016/j.exphem.2018.12.003

This publication was supported by grants from the National Institutes of Health and the Bezos family.

Fred Hutch/UW Cancer Consortium members Hans-Peter Kiem (FH/UW) and Anthony Rongvaux (FH) contributed to this work.