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Humanized mouse

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A humanized mouse is a <a href="Genetically_modified_mouse" title="Genetically modified mouse">genetically modified mouse</a> that has functioning human genes, cells, tissues and/or organs.<a href="#cite_note-1">[1]</a> Humanized mice are commonly used as small <a href="Animal_models" class="mw-redirect" title="Animal models">animal models</a> in biological and medical research for human therapeutics.<a href="#cite_note-2">[2]</a>

A humanized mouse or a humanized mouse model is one that has been <a href="Xenotransplantation" title="Xenotransplantation">xenotransplanted</a> with human cells and/or engineered to express human gene products, so as to be utilized for gaining relevant insights in the <a href="In_vivo" title="In vivo">in vivo</a> context for understanding of human-specific physiology and pathologies.<a href="#cite_note-3">[3]</a> Several human biological processes have been explored using animal models like <a href="Rodent" title="Rodent">rodents</a> and <a href="Animal_testing_on_non-human_primates" title="Animal testing on non-human primates">non-human primates</a>. In particular, small animals such as mice are advantageous in such studies owing to their small size, brief reproductive cycle, easy handling and due to the genomic and physiological similarities with humans; moreover, these animals can also be genetically modified easily. Nevertheless, there are several incongruencies of these animal systems with those of humans, especially with regard to the components of the <a href="Immune_system" title="Immune system">immune system</a>. To overcome these limitations and to realize the full potential of animal models to enable researchers to get a clear picture of the nature and pathogenesis of immune responses mounted against human-specific pathogens, humanized mouse models have been developed. Such mouse models have also become an integral aspect of <a href="Preclinical" class="mw-redirect" title="Preclinical">preclinical</a> biomedical research.<a href="#cite_note-4">[4]</a>

<div class="mw-heading mw-heading2"><h2 id="History">History</h2></div>

The discovery of the athymic mouse, commonly known as the <a href="Nude_mouse" title="Nude mouse">nude mouse</a>, and that of the <a href="SCID_mouse" class="mw-redirect" title="SCID mouse">SCID mouse</a> were major events that paved the way for humanized mice models. The first such mouse model was derived by <a href="Backcrossing" title="Backcrossing">backcrossing</a> C57BL/Ka and <a href="BALB/c" title="BALB/c">BALB/c</a> mice, featuring a loss of function <a href="Mutation" title="Mutation">mutation</a> in the <a href="PRKDC_(gene)" class="mw-redirect" title="PRKDC (gene)">PRKDC gene</a>. The PRKDC gene product is necessary for resolving breaks in DNA strands during the development of <a href="T_cell" title="T cell">T cells</a> and <a href="B_cell" title="B cell">B cells</a>. A mutation in the Foxn1 gene on chromosome 11 resulted in impaired thymus development, leading to a deficiency in mature T lymphocytes. Dysfunctional PRKDC gene leads to impaired development of T and B lymphocytes which gives rise to severe combined immunodeficiency (SCID). In spite of the efforts in developing this mouse model, poor engraftment of human <a href="Hematopoietic_stem_cell" title="Hematopoietic stem cell">hematopoietic stem cells</a> (HSCs) was a major limitation that called for further advancement in the development humanized mouse models.<a href="#cite_note-5">[5]</a> Nude mice were the earliest immunodeficient mouse model. These mice primarily produced IgM and had minimal or no IgA. As a result, they did not exhibit a rejection response to allogeneic tissue. Commonly utilized strains included BALB/c-nu, Swiss-nu, NC-nu, and NIH-nu, which were extensively employed in the research of immune diseases and tumors. However, due to the retention of B cells and NK cells, they were unable to fully support engraftment of human immune cells, thus making them unsuitable as an ideal humanized mouse model.

The next big step in the development of humanized mice models came with transfer of the scid mutation to a non-obese diabetic mouse. This resulted in the creation of the NOD-scid mice which lacked <a href="T_cell" title="T cell">T cells</a>, <a href="B_cell" title="B cell">B cells</a>, and <a href="NK_cell" class="mw-redirect" title="NK cell">NK cells</a>. This mouse model permitted for a slightly higher level of human cell reconstitution. Nevertheless, a major breakthrough in this field came with the introduction of the mutant <a href="IL-2_receptor" title="IL-2 receptor">IL-2 receptor</a> (IL2rg) gene in the NOD-scid model. This accounted for the creation of the NOD-scid-γcnull mice (NCG, NSG or NOG) models which were found to have defective signaling of <a href="Interleukin" title="Interleukin">interleukins</a> IL-2, IL-4, IL-7, IL-9, IL-15 and IL-21. Researchers evolved this NSG model by <a href="Gene_knockout" title="Gene knockout">knocking out</a> the <a href="RAG1" title="RAG1">RAG1</a> and <a href="RAG2" title="RAG2">RAG2</a> genes (<a href="Recombination-activating_gene" title="Recombination-activating gene">recombination activation</a> genes), resulting into the RAGnull version of the NSG model that was devoid of major cells of the immune system including the <a href="Natural_killer_cell" title="Natural killer cell">natural killer cells</a>, <a href="B_cell" title="B cell">B lymphocytes</a> and <a href="T_cell" title="T cell">T lymphocytes</a>, <a href="Macrophage" title="Macrophage">macrophages</a> and <a href="Dendritic_cell" title="Dendritic cell">dendritic cells</a>, causing the greatest <a href="Immunodeficiency" title="Immunodeficiency">immunodeficiency</a> in mice models so far. The limitation with this model was that it lacked the <a href="Human_leukocyte_antigen" title="Human leukocyte antigen">human leukocyte antigen</a>. In accordance to this limitation, the human T cells when engrafted in the mice, failed to recognize human <a href="Antigen-presenting_cell" title="Antigen-presenting cell">antigen-presenting cells</a>, which consequated in defective <a href="Immunoglobulin_class_switching" title="Immunoglobulin class switching">immunoglobulin class switching</a> and improper organization of the <a href="Secondary_Lymphoid_Organ" class="mw-redirect" title="Secondary Lymphoid Organ">secondary lymphoid</a> tissue.<a href="#cite_note-6">[6]</a>

To circumvent this limitation, the next development came with the introduction of transgenes encoding for HLA I and HLA II in the NSG RAGnull model that enabled buildout of human T-lymphocyte repertoires as well as the respective immune responses.<a href="#cite_note-:0-7">[7]</a> Mice with such human genes are technically <a href="Human-animal_hybrid" class="mw-redirect" title="Human-animal hybrid">human-animal hybrids</a>.

<div class="mw-heading mw-heading2"><h2 id="Types">Types</h2></div>

Engrafting an immunodeficient mouse with functional human cells can be achieved by <a href="Intravenous" class="mw-redirect" title="Intravenous">intravenous</a> injections of human cells and tissue into the mouse, and/or creating a <a href="Genetically_modified_mouse" title="Genetically modified mouse">genetically modified mouse</a> from human genes. These models have been instrumental in studying human diseases, immune responses, and therapeutic interventions. This section highlights the various humanized mice models developed using the different methods.

<div class="mw-heading mw-heading3"><h3 id="Hu-PBL-scid_model">Hu-PBL-scid model</h3></div>

The human peripheral blood lymphocyte-severe combined immunodeficiency mouse model has been employed in a diverse array of research, encompassing investigations into Epstein-Barr virus (EBV)-associated lymphoproliferative disease, toxoplasmosis, human immunodeficiency virus (HIV) infection, and autoimmune diseases.<a href="#cite_note-8">[8]</a> These studies have highlighted the effectiveness of the hu-PBL-SCID mouse model in examining various facets of human diseases, including pathogenesis, immune responses, and therapeutic interventions. Furthermore, the model has been utilized to explore genetic and molecular factors linked to neuropsychiatric disorders such as schizophrenia, offering valuable insights into the pathophysiology and potential therapeutic targets for these conditions.<a href="#cite_note-9">[9]</a> This model is developed by intravenously injecting human <a href="PBMC" class="mw-redirect" title="PBMC">PBMCs</a> into immunodeficient mice. The <a href="Peripheral_blood_mononuclear_cell" title="Peripheral blood mononuclear cell">peripheral blood mononuclear cells</a> to be engrafted into the model are obtained from consented adult donors. The advantages associated with this method are that it is comparatively an easy technique, the model takes relatively less time to get established and that the model exhibits functional <a href="Memory_T_cell" title="Memory T cell">memory T cells</a>.<a href="#cite_note-10">[10]</a> It is particularly very effective for modelling <a href="Graft-versus-host_disease" title="Graft-versus-host disease">graft vs. host disease</a>.<a href="#cite_note-:0-7">[7]</a> The model lacks engraftment of B lymphocytes and <a href="Myeloid_cell" class="mw-redirect" title="Myeloid cell">myeloid cells</a>. Other limitations with this model are that it is suitable for use only in short-term experiments (<3 months) and the possibility that the model itself might develop graft vs. host disease.<a href="#cite_note-:0-7">[7]</a>

<div class="mw-heading mw-heading3"><h3 id="Hu-SRC-scid_model">Hu-SRC-scid model</h3></div>

The humanized severe combined immunodeficiency (SCID) mouse model, also known as the hu-SRC-scid model, has been extensively utilized in various research areas, including immunology, infectious diseases, cancer, and drug development. This model has been instrumental in studying the human immune response to xenogeneic and allogeneic decellularized biomaterials, providing valuable insights into the biocompatibility and gene expression regulation of these materials.<a href="#cite_note-11">[11]</a> Hu-SRC-scid mice are developed by engrafting <a href="CD34%2B" class="mw-redirect" title="CD34+">CD34+</a> human <a href="Hematopoietic_stem_cell" title="Hematopoietic stem cell">hematopoietic stem cells</a> into immunodeficient mice. The cells are obtained from human fetal <a href="Liver" title="Liver">liver</a>, <a href="Bone_marrow" title="Bone marrow">bone marrow</a> or from <a href="Umbilical_cord_blood" class="mw-redirect" title="Umbilical cord blood">blood derived from the umbilical cord</a>,<a href="#cite_note-12">[12]</a> and engrafted via intravenous injection. The advantages of this model are that it offers multilineage development of hematopoietic cells, generation of a naïve immune system, and if engraftment is carried out by intrahepatic injection of newborn mice within 72 hours of birth, it can lead to enhanced human cell reconstitution. Nevertheless, limitations associated with the model are that it takes a minimum of 10 weeks for <a href="Cell_differentiation" class="mw-redirect" title="Cell differentiation">cell differentiation</a> to occur, it harbors low levels of human <a href="RBCs" class="mw-redirect" title="RBCs">RBCs</a>, <a href="Polymorphonuclear_leukocytes" class="mw-redirect" title="Polymorphonuclear leukocytes">polymorphonuclear leukocytes</a>, and <a href="Megakaryocyte" title="Megakaryocyte">megakaryocytes</a>.<a href="#cite_note-:0-7">[7]</a>

<div class="mw-heading mw-heading3"><h3 id="BLT_(bone_marrow/liver/thymus)_model">BLT (bone marrow/liver/thymus) model</h3></div>

The BLT model is constituted with human <a href="Hematopoietic_stem_cell" title="Hematopoietic stem cell">HSCs</a>, bone marrow, liver, and <a href="Thymus" title="Thymus">thymus</a>. The engraftment is carried out by implantation of liver and thymus under the <a href="Kidney_capsule" class="mw-redirect" title="Kidney capsule">kidney capsule</a> and by transplantation of HSCs obtained from fetal liver. The BLT model has a complete and totally functional human immune system with <a href="MHC_restriction" title="MHC restriction">HLA-restricted</a> T lymphocytes. The model also comprises a mucosal system that is similar to that of humans. Moreover, among all models the BLT model has the highest level of human cell reconstitution.<a href="#cite_note-13">[13]</a>

However, since it requires surgical implantation, this model is the most difficult and time-consuming to develop. Other drawbacks associated with the model are that it portrays weak immune responses to <a href="Xenobiotic" title="Xenobiotic">xenobiotics</a>, sub-optimal <a href="Immunoglobulin_class_switching" title="Immunoglobulin class switching">class switching</a> and may develop <a href="GvHD" class="mw-redirect" title="GvHD">GvHD</a>.<a href="#cite_note-:0-7">[7]</a>

<div class="mw-heading mw-heading3"><h3 id="Transplanted_human_organoids">Transplanted human organoids</h3></div>

Bio- and electrical engineers have shown that human <a href="Cerebral_organoid" title="Cerebral organoid">cerebral organoids</a> transplanted into mice functionally integrate with their visual cortex.<a href="#cite_note-14">[14]</a><a href="#cite_note-15">[15]</a> Such models may raise similar ethical issues <a href="Cerebral_organoid#Humanized_animals" title="Cerebral organoid">as organoid-based humanization of other animals</a>.

<div class="mw-heading mw-heading3"><h3 id="Mouse-human_hybrid">Mouse-human hybrid</h3></div>

A mouse-human hybrid is a <a href="Genetically_modified_mouse" title="Genetically modified mouse">genetically modified mouse</a> whose genome has both mouse and human genes, thus being a <a href="Murinae" title="Murinae">murine</a> form of a <a href="Human-animal_hybrid" class="mw-redirect" title="Human-animal hybrid">human-animal hybrid</a>. For example, genetically modified mice may be born with <a href="Human_leukocyte_antigen" title="Human leukocyte antigen">human leukocyte antigen</a> genes in order to provide a more realistic environment when introducing human <a href="White_blood_cells" class="mw-redirect" title="White blood cells">white blood cells</a> into them in order to study <a href="Immune_system" title="Immune system">immune system</a> responses.<a href="#cite_note-:0-7">[7]</a> One such application is the identification of <a href="Hepatitis_C_virus" title="Hepatitis C virus">hepatitis C virus</a> (HCV) peptides that bind to HLA, and that can be recognized by the human immune system, thereby potentially being targets for future vaccines against HCV.<a href="#cite_note-16">[16]</a>

<div class="mw-heading mw-heading2"><h2 id="Established_models_for_human_diseases">Established models for human diseases</h2></div>

Several mechanisms underlying human maladies are not fully understood. Utilization of humanized mice models in this context allows researchers to determine and unravel important factors that bring about the development of several human diseases and disorders falling under the categories of infectious disease, cancer, autoimmunity, and GvHD.

<div class="mw-heading mw-heading3"><h3 id="Infectious_diseases">Infectious diseases</h3></div>

Among the human-specific infectious pathogens studied on humanized mice models, the <a href="Human_immunodeficiency_virus" class="mw-redirect" title="Human immunodeficiency virus">human immunodeficiency virus</a> has been successfully studied.<a href="#cite_note-:0-7">[7]</a> Besides this, humanized models for studying <a href="Zaire_ebolavirus" title="Zaire ebolavirus">Ebola virus</a>,<a href="#cite_note-17">[17]</a> <a href="Hepatitis_B" title="Hepatitis B">Hepatitis B</a>,<a href="#cite_note-18">[18]</a> <a href="Hepatitis_C" title="Hepatitis C">Hepatitis C</a>,<a href="#cite_note-19">[19]</a> <a href="Kaposi's_sarcoma-associated_herpesvirus" title="Kaposi's sarcoma-associated herpesvirus">Kaposi's sarcoma-associated herpesvirus</a>,<a href="#cite_note-20">[20]</a> <a href="Leishmania_major" title="Leishmania major">Leishmania major</a>,<a href="#cite_note-21">[21]</a> <a href="Malaria" title="Malaria">malaria</a>,<a href="#cite_note-22">[22]</a> and <a href="Tuberculosis" title="Tuberculosis">tuberculosis</a><a href="#cite_note-23">[23]</a> have been reported by various studies.

NOD/scid mice models for <a href="Dengue_virus" title="Dengue virus">dengue virus</a><a href="#cite_note-24">[24]</a> and <a href="Varicella_zoster_virus" title="Varicella zoster virus">varicella-zoster virus</a>,<a href="#cite_note-25">[25]</a> and a Rag2null𝛾cnull model for studying <a href="Influenza_virus" class="mw-redirect" title="Influenza virus">influenza virus</a><a href="#cite_note-26">[26]</a> have also been developed.

<div class="mw-heading mw-heading3"><h3 id="Cancers">Cancers</h3></div>

On the basis of the type of human cells/tissues that have been used for engraftment, humanized mouse models for <a href="Cancer" title="Cancer">cancer</a> can be classified as <a href="Patient-derived_xenograft" class="mw-redirect" title="Patient-derived xenograft">patient-derived xenografts</a> or cell line-derived xenografts.<a href="#cite_note-:1-27">[27]</a> PDX models are considered to retain the parental malignancy characteristics at a greater extent and hence these are regarded as the more powerful tool for evaluating the effect of <a href="Anticancer" class="mw-redirect" title="Anticancer">anticancer</a> drugs in <a href="Pre-clinical_studies" class="mw-redirect" title="Pre-clinical studies">pre-clinical studies</a>.<a href="#cite_note-:1-27">[27]</a><a href="#cite_note-28">[28]</a> Humanized mouse models for studying cancers of various organs have been designed. A mouse model for the study of <a href="Breast_cancer" title="Breast cancer">breast cancer</a> has been generated by the intrahepatic engraftment of <a href="SK-BR-3" class="mw-redirect" title="SK-BR-3">SK-BR-3</a> cells in NSG mice.<a href="#cite_note-29">[29]</a> Similarly, NSG mice intravenously engrafted with patient-derived <a href="Acute_myeloid_leukemia" title="Acute myeloid leukemia">AML</a> cells,<a href="#cite_note-30">[30]</a> and those engrafted (via <a href="Subcutaneous_injection" class="mw-redirect" title="Subcutaneous injection">subcutaneous</a>, <a href="Intravenous_therapy" title="Intravenous therapy">intravenous</a> or intra-pancreatic injections) with patient-derived pancreatic cancer tumors<a href="#cite_note-31">[31]</a> have also been developed for the study of leukemia and pancreatic cancer respectively. Several other humanized rodent models for the study of cancer and <a href="Cancer_immunotherapy" title="Cancer immunotherapy">cancer immunotherapy</a> have also been reported.<a href="#cite_note-32">[32]</a>

<div class="mw-heading mw-heading3"><h3 id="Autoimmune_diseases">Autoimmune diseases</h3></div>

Problems posed by the differences in the human and rodent immune systems have been overcome using a few strategies, so as to enable researchers to study <a href="Autoimmune_disease" title="Autoimmune disease">autoimmune disorders</a> using humanized models. As a result, the use of humanized mouse models has extended to various areas of immunology and disease research. For instance, humanized mice have been utilized to study human-tropic pathogens, liver cancer models, and the comparison of mouse models to human diseases NSG mice engrafted with <a href="PBMC" class="mw-redirect" title="PBMC">PBMCs</a> and administered with myelin antigens in <a href="Freund's_adjuvant" title="Freund's adjuvant">Freund's adjuvant</a>, and antigen-pulsed autologous <a href="Dendritic_cell" title="Dendritic cell">dendritic cells</a> have been used to study <a href="Multiple_sclerosis" title="Multiple sclerosis">multiple sclerosis</a>.<a href="#cite_note-33">[33]</a> Similarly, NSG mice engrafted with hematopoietic stem cells and administered with <a href="Pristane" title="Pristane">pristane</a> have been used for studying <a href="Lupus_erythematosus" title="Lupus erythematosus">lupus erythematosus</a>.<a href="#cite_note-34">[34]</a> Furthermore, NOG mice engrafted with PBMCs has been used to study mechanisms of allografts rejection in vivo.<a href="#cite_note-35">[35]</a> The development of humanized mouse models has significantly advanced the study of autoimmune disorders and various areas of immunology and disease research. These models have provided a platform for investigating human diseases, immune responses, and therapeutic interventions, bridging the gap between human and rodent immune systems and offering valuable insights into disease pathogenesis and potential therapeutic strategies.

<ul><li><a href="Nude_mouse" title="Nude mouse">Nude mouse</a></li>

<li><a href="SCID_mouse" class="mw-redirect" title="SCID mouse">SCID mouse</a></li>

<li><a href="NOG_mouse" title="NOG mouse">NOG mouse</a></li>

<li><a href="NSG_mouse" title="NSG mouse">NSG mouse</a></li>

<li><a href="Mouse_model_of_colorectal_and_intestinal_cancer" title="Mouse model of colorectal and intestinal cancer">Mouse model of colorectal and intestinal cancer</a></li>

<li><a href="Mouse_models_of_breast_cancer_metastasis" title="Mouse models of breast cancer metastasis">Mouse models of breast cancer metastasis</a></li>

<li><a href="Knockout_mouse" title="Knockout mouse">Knockout mouse</a></li></ul>

<div class="mw-heading mw-heading2"><h2 id="References">References</h2></div>

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<div class="mw-heading mw-heading2"><h2 id="Further_reading">Further reading</h2></div>

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<li><cite id="CITEREFItoTakahashiKatanoIto2012" class="citation journal cs1">Ito R, Takahashi T, Katano I, Ito M (May 2012). <a rel="nofollow" class="external text" href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4012844">"Current advances in humanized mouse models"</a>. Cellular & Molecular Immunology. 9 (3): 208–14. <a href="Doi_(identifier)" class="mw-redirect" title="Doi (identifier)">doi</a>:<a rel="nofollow" class="external text" href="https://doi.org/10.1038%2Fcmi.2012.2">10.1038/cmi.2012.2</a>. <a href="PMC_(identifier)" class="mw-redirect" title="PMC (identifier)">PMC</a> <a rel="nofollow" class="external text" href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4012844">4012844</a>. <a href="PMID_(identifier)" class="mw-redirect" title="PMID (identifier)">PMID</a> <a rel="nofollow" class="external text" href="https://pubmed.ncbi.nlm.nih.gov/22327211">22327211</a>.</cite></li>

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