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Development and function of human innate immune cells in a humanized mouse model
Open accessAbstract
Mice repopulated with human hematopoietic cells are a powerful tool for the study of human hematopoiesis and immune function in vivo. However, existing humanized mouse models cannot support development of human innate immune cells, including myeloid cells and natural killer (NK) cells. Here we describe two mouse strains called MITRG and MISTRG, in which human versions of four genes encoding cytokines important for innate immune cell development are knocked into their respective mouse loci. The human cytokines support the development and function of monocytes, macrophages and NK cells derived from human fetal liver or adult CD34(+) progenitor cells injected into the mice. Human macrophages infiltrated a human tumor xenograft in MITRG and MISTRG mice in a manner resembling that observed in tumors obtained from human patients. This humanized mouse model may be used to model the human immune system in scenarios of health and pathology, and may enable evaluation of therapeutic candidates in an in vivo setting relevant to human physiology.
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“Species-specific differences between animals and humans cause differences in drug efficacy and toxicity tests in physiology and cell biology31–37.”
From Tumor-on-a-chip: from bioinspired design to biomedical application (2021) · cites this paper as [34]
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“MITRG mice allow for xenotransplantation and is designed to support human myeloid engraftment.”
From iPSC-derived human microglia-like cells to study neurological diseases (2017) · cites this paper as Rongvaux et al., 2014
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“Similarly, mice reconstituted with a functional human immune system (humanized mice) can be used for studying the therapeutic effects of nanomedicines against autoimmune diseases such as diabetes, or to harbour patient-derived tumours for preclinical testing of cancer immune nanomedicines95.”
From How to design preclinical studies in nanomedicine and cell therapy to maximize the prospects of clinical translation (2018) · cites this paper as [95]
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“In our study, we transplanted UiPSM and iMYOD UiPSM derived skeletal myocytes into the tibial anterior (TA) muscle of the MITRG mouse, which is an immune-deficient strain like NSG commonly used as a recipient of human hematopoietic cells [41].”
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“5Gy), 8-16 week old, female MISTRG mice (Regeneron Pharmaceuticals) (Rongvaux et al., 2014), with groups of five mice per condition.”
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“…of human hematopoietic and lymphoid cells in immunodeficient mice by introducing human cytokines, such as transgenic expression of human macrophage-stimulating factor (M-CSF), granulocyte-macrophage colony-stimulating factor (GM-CSF)/interleukin-3 (IL-3), and thrombopoietin (TPO) genes [11, 12].”
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“This would be consistent with more functional innate and adaptive T-lymphocyte immunity in humanized MISTRG mice compared to NSG mice (Rongvaux et al., 2014), which could be suppressing HIV-1 replication.”
InfluentialGeneration of CD68+ macrophage-depleted NOG mice for in vivo engraftment of human red blood cells
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“In addition, MISTRG mice are prone to anemia, and the post‑ engraftment lifespan is approximately 10–12 weeks [36, 38].”
InfluentialSobu, R., Kobayashi, Y., Kashima, S., Inoue, T., Sumiyoshi, T., Hamana, H., Takeda, M., Hiroshima, Y., Seki, S., Fujiyama, N., et al. (2026) · iScience · doi:10.1016/j.isci.2026.116386 · Cited by 1
“…human cytokine genes have been knocked in, enabling the reconstitution of human immunity upon transplantation of human hematopoietic stem cells, 41,42 in this model, T cells derived from human hematopoietic stem cells undergo thymic selection in the murine thymus, resulting in a TCR repertoire…”
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“Multiple replacements of M-CSF [6], IL-3, GM-CSF [7], and thrombopoietin (TPO) [8] genes with the corresponding human ortholog genes (MITRG mouse) have been used for human myeloid cell development [9].”
MethodThe Plasticity of Stem-Like States in Patient-Derived Tumor Xenografts
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MethodVerhoeff, K. K., Marfil‐Garza, B. A., Cuesta‐Gomez, N., Jasra, I. T., Dadheech, N., & Shapiro, A. M. J. (2022) · Advances in experimental medicine and biology · doi:10.1007/5584_2022_711 · Cited by 1
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“Frontiers in Pediatrics 11 through knock-in of human GM-CSF and other human cytokines (6).”
BackgroundMethodInfluentialResearch advancements and evaluation of multifactor‐induced murine models for gastric cancer
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“…model [8], have provided significant insights into A. baumannii ’s virulence factors and pathogenesis in response to murine whole blood, there are fundamental differences in immune function between species, and insights gained from mouse studies often cannot be directly applied to humans [9].”
Translational Animal Models for Regenerative Medicine Research
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Stem Cell Model of Hematologic Diseases
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“Immune reactions can be modelled in 7 xenografts with "humanized" mice, which develop human immune components (Rongvaux et al. 2014).”
BackgroundBoettcher, A. N., Li, Y., Ahrens, A. P., Kiupel, M., Byrne, K. A., Loving, C. L., Cino-Ozuna, A. G., Wiarda, J. E., Adur, M. K., Schultz, B., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/614404 · Cited by 1
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“174 175 To evaluate whether CAR T cells induce PD-L1 expression in tumor-associated macrophages in 176 vivo, we humanized mice by engrafting human CD34 hematopoietic stem cells in immune177 compromised MISTRG mice,[38].”
MethodSteinkamp, M. P., Lagutina, I. V., Brayer, K. J., Schultz, F. A., Burke, D., Pankratz, V. S., Adams, S. F., Hudson, L. G., Ness, S. A., & Wandinger‐Ness, A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.07.01.498335 · Cited by 1
Humanized Mouse Models for Cancer Immunotherapy: A Focus on Human PBMC and HSPC Reconstitution
Li, Z. Y., Yang, X. J., & Song, X. (2022) · Wiley eBooks · doi:10.1002/9781119535331.ch7 · Cited by 1
Cattin, A., Pham, T. N. Q., Dias, J., do Rosário, N. F., Marchand, L. R., Volodina, O., Guimond, J.-V., Patey, N., Li, Y., Béland, K., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.01.31.635552 · Cited by 1
The Role of AF9 and AF9-Mediated Protein Interactions in Hematopoiesis and Leukemogenesis
Lokken, A. A. (2014) · Loyola eCommons (Loyola University of Chicago)
Mice with a human innate compartment
Leavy, O. (2014) · Nature reviews. Immunology · doi:10.1038/nri3654
New Humanized Mouse Model of Bronchiolitis Obliterans Syndrome
Anegón, I. (2015) · Transplantation · doi:10.1097/tp.0000000000000631
“To increase and enrich hematopoietic engraftment, other genetic modifications have been introduced in immunodeficient mice, such as human signal-regulatory protein alpha (interacting with human CD47 on engrafted human hematopoietic cells providing “ do not eat me signals” to mouse macrophages); different cytokines (fo…”
BackgroundModeling Normal and Disordered Human
Beer, H. A., & Eaves, C. J. (2015)
Leukemias and bones: humanizing the niche in mice
Stripecke, R. (2016) · Blood · doi:10.1182/blood-2016-11-746867
“can potentially activate myeloid cells, including leukemia cells.(5) Eventually, the incremental combination of new engineered mouse strains with innovative ossicle implants will indeed allow a deeper understanding of the niche and spatiotemporal events steering the human polyclonal or oligoclonal leukemogenesis.”
BackgroundPatient-Derived Xenograft Models of Ovarian/Gynecologic Tumors
Liang, L., Mercado‐Uribe, I., Niu, N., Jiang, Y., Cheng, W., Zhang, J., Mills, G. B., Scott, C. L., Sood, A. K., & Liu, J. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804010-2.00019-9
Li, Y. (2016) · Open Access Victoria University of Wellington | Te Herenga Waka (Figshare) · doi:10.26686/wgtn.20388027
“For example, a study has used MI(S)TRG mouse strain in which the mice are knocked in four human genes encoding cytokines important for the development of innate immune cell (Rongvaux et al., 2014).”
MethodBaldwin, J. (2017) · Queensland University of Technology · doi:10.5204/thesis.eprints.110638
Modeling Unique Patients in Humanized Mice: Toward a Curative Strategy for HIV
Dorner, M., & de Jong, Y. P. (2018) · Molecular Therapy · doi:10.1016/j.ymthe.2018.01.003
“Further manipulations, such as supplementation of human growth factors or co-transplantation of human liver, might broaden the humanization of these models.(7,8) Yet, future modifications in these models will be required to study the role of various anti-HIV immune functions.”
BackgroundTherapeutic Uses of Broadly Neutralizing Anti-HIV-1 Antibodies in Humanized Mice
Halper-Stromberg, A. (2025) · Digital Commons - RU (Rockefeller University) · doi:10.48496/dpcp-1745
Targeted therapy to annihilate the immune-evading phenotype in cancer evolution
Fernández, A. (2018) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2018.1450867
Wagner, F. (2018) · Queensland University of Technology · doi:10.5204/thesis.eprints.116423
Unraveling clonal heterogeneity in acute myeloid leukemia
de Boer, B. (2020) · University of Groningen research database (University of Groningen / Centre for Information Technology) · doi:10.33612/diss.113125010
SIRPAssing other xenograft murine models?
Rau, R. E. (2020) · Blood · doi:10.1182/blood.2020005554
[Advances on mouse transplantation model of myelodysplastic syndrome].
Fang, Y., & Chang, C. (2020) · PubMed Central · doi:10.3760/cma.j.issn.0253-2727.2020.04.017
A humanized model to investigate targeted therapeutic strategies against cancer bone metastasis
Landgraf, M. (2020) · Queensland University of Technology · doi:10.5204/thesis.eprints.204176
Therapeutic targeting of the leukaemic fusion genes
Issa, H. (2019)
Patient-Derived Xenograft Models in Gynaecological Malignancies
Tanaka, T., & Ohmichi, M. (2021) · Current human cell research and applications · doi:10.1007/978-981-33-6013-6_2
Intrafemoral Delivery of Hematopoietic Progenitors
Evrard, M., Kwok, I., & Ng, L. G. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1425-9_13
Adoptive NK cell therapies in children with cancer: Clinical challenges and future possibilities
Nguyen, R., & Furman, W. L. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-824375-6.00018-7
Martínek, J., Lin, J., Kim, K. I., Wang, V. G., Wu, T.-C., Chiorazzi, M., Boruchov, H., Gulati, A., Seeniraj, S., Marches, F., et al. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3903548
A faithful in vivo model of human macrophages in metastatic melanomaPreprint
Voillet, V., Berger, T. R., McKenna, K. M., Paulson, K. G., Smythe, K. S., Hunter, D. S., Valente, W. J., Weaver, S., Campbell, J. S., Kim, T. S., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.09.459682
Myszy humanizowane - zastosowanie do modelowania chorób zakaźnych
Nowak, W. N., Noworyta, I., Sokołowski, G., & Józkowicz, A. (2021) · Kosmos · doi:10.36921/kos.2021_2815
Weinhäuser, I. (2021) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.17.2021.tde-07022022-174003
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Modeling Infectious Diseases in Mice with a “Humanized” Immune System
Li, Y., & Santo, J. P. D. (2020) · John Wiley & Sons, Inc. eBooks · doi:10.1128/9781683670261.ch21
Metadata
- Authors
- Rongvaux, A., Willinger, T., Martinek, J., Strowig, T., Gearty, S. V., Teichmann, L. L., Saito, Y., Marches, F., Halene, S., Palucka, A. K., Manz, M. G., & Flavell, R. A.
- Affiliations
- Yale University (US)
- University Hospital Bonn (DE)
- University Hospital Zurich (CH)
- Yale Cancer Center (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Manz, Markus G
- Flavell, Richard A
- ORCID
- Venue
- Nature Biotechnology
- Published
- 2014-03-16
- Volume
- 32
- Issue
- 4
- Pages
- 364-372
- ISSN
- 0733-222X (ISSN-L)
- 1087-0156
- 1546-1696
- PMC
- PMC4017589
- OpenAlex
- W2007987850
- Cited by
- 789
- References
- 50
- Citations by year
- 2026: 48 · 2025: 52 · 2024: 61 · 2023: 69 · 2022: 70 · 2021: 94 · 2020: 70 · 2019: 67 · 2018: 65 · 2017: 62 · 2016: 62 · 2015: 46 · 2014: 23
- FWCI
- 45.61
- Type
- journal article
- Language
- en
- Update notices
- erratum (2017-12-01)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Biotechnology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Cancer Institute (R01CA140602, CA84512, P01CA084512, R01CA129350, CA129350, R01CA156689, CA156689, CA140602)
- Topics
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Health Sciences › Medicine › Surgery › Xenotransplantation and immune response
- Keywords
- humanized mice, innate immune cells, myeloid cell development, natural killer cells, monocytes, macrophages, CD34+ cells, tumor xenografts
- MeSH terms
- Animals, Humans, Immunity, Innate, Killer Cells, Natural, Mice, Transgenic, Neoplasms, Experimental, Transplantation, Heterologous, Leukemic Infiltration, Myeloid Cells, Mice
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