Application of Animal Models in Cancer Research: Recent Progress and Future Prospects

Figures & data

Figure 1 Two commonly used classification methods of cancer animal models. Dashed red box represents the classification according to different modeling methods. Another classification is carried out according to different species. Blue arrows indicate the species of animals included in this classification.

Abbreviations: PDX, patient-derived tumor xenograft; CDX, cell line-derived xenograft.

Figure 2 Construction method of humanized mice of human immune system. The construction of humanized mice needs to use immunodeficient mice as a tool. By transplanting different human immune organs or cells into immunodeficient mice, three different humanized mice can be constructed. Among them, the Hu-HSC model also needs to destroy the hematopoietic function of bone marrow in mice.

Abbreviations: Hu-HSC, human hematopoietic stem cell; Hu-PBL, human peripheral blood lymphocyte; Hu-BLT, human bone marrow, liver and thymus.

Table 1 Zebrafish Model

Cancer Model	Modeling Mode	Finding	Reference
Acute lymphocytic leukemia	Transgenic model	They describe the first robust zebrafish pre-B ALL model. This model can reveal differences between MYC-driven pre-B vs T-ALL and be exploited to discover novel pre-B ALL therapies	[^Citation110]
Acute myeloid leukemia	Xenograft model	Bone marrow (BM) SOX4 expression could serve as an informative new biomarker for the clinical prognosis of AML patients. And the myeloid-specific expression of SOX4 can induce leukemic phenotype in zebrafish.	[^Citation111]
Breast cancer	Xenograft model	Administration of VEGFR inhibitors blocked tumor vascularization and a localized tumor growth but enhanced migration of neutrophils, which in turn promoted tumor invasion and formation of micrometastasis.	[^Citation112]
Breast cancer	Xenograft model	Grem1 is a pivotal factor in the reciprocal interplay between breast cancer cells and CAFs, which promotes cancer cell invasion. Targeting Grem1 could be beneficial in the treatment of breast cancer patients with high Grem1 expression.	[^Citation67]
Breast cancer	Xenograft model	When the tumor metastases, organ selectivity is driven by both vessel topography and cell-type-dependent extravasation.	[^Citation113]
Breast cancer	Xenograft model	SMYD3 is a pivotal SMAD3 cofactor that promotes TGFβ-dependent mesenchymal gene expression and cell migration in breast cancer.	[^Citation114]
Breast cancer	Xenograft model	PtPP-loaded and citrate-functionalized HA nanoparticles effectively decrease breast cancer cells survival both in vitro and in vivo in a similar manner to free PtPP.	[^Citation115]
Breast cancer and Liver cancer	Xenograft model	Furanodiene showed a markedly synergistic anti-cancer effect when used in combination with 5-FU (5-Fluorouracil) for both human breast cancer MDA-MB-231 cells and human liver cancer BEL-7402 cells xenotransplanted into zebrafish.	[^Citation68]
Colon Cancer	Xenograft model	After NR1D1 gene is knocked out, the cell viability is impaired and the formation of micrometastasis is reduced.	[^Citation116]
Colorectal cancer	Xenograft model	Endoglin-expressing fibroblasts enhanced colorectal tumor cell infiltration into the liver and decreased survival. And endoglin-expressing CAFs contribute to colorectal cancer progression and metastasis.	[^Citation117]
Colorectal cancer	Xenograft model	They found significantly less distant metastasis of ERB-041-treated cells compared to vehicle-treated cells. These results further support ERβ’s anti-tumor role in CRC and the possible use of its agonist in CRC patients.	[^Citation60]
Colorectal cancer	Transgenic model	They established a new transgenic zebrafish model with inducible expression of oncogenic kras^V12 specifically in the intestine and observed high rates of intestinal tumors.	[^Citation61]
Colorectal cancer	Xenograft model	cGAMP inhibited migration through angiogenesis by up-regulating IL-2, TNF-α, and IFN-γ, whereas STAT3 down-regulation inhibited CXCL8, BCL-2, and VEGFA expression.	[^Citation118]
Colorectal carcinoma	Xenograft model	Zebrafish xenografts provide remarkable resolution to measure Cetuximab sensitivity. Zebrafish larvae xenografts constitute a promising fast assay for precision medicine, bridging the gap between genotype and phenotype in an in vivo setting.	[^Citation119]
Colorectal carcinoma	Xenograft model	L.sulphureus lectin (LSL) almost completely reduced growth, neovascularization and metastasis of human colorectal carcinoma and mouse melanoma. It could be used as safe adjuvant in chemotherapy against colorectal carcinoma and melanoma.	[^Citation120]
Colorectal carcinoma	Xenograft model	Crambescidine-816, −830, and −800 disrupt tumor cell adhesion and cytoskeletal integrity promoting the activation of the intrinsic apoptotic signaling, resulting in loss of mitochondrial membrane potential and concomitant caspase-3 cleavage and activation.	[^Citation121]
Gastric carcinoma	Xenograft model	The zebrafish xenograft study revealed that administration of Triphala inhibited the xenograft growth and metastasis of transplanted carcinoma cells in vivo.	[^Citation56]
Glioblastoma	Xenograft model	Treatment of GBM cells with compound 5 (CMP5) mirrored the effects of PRMT5 knockdown wherein it led to apoptosis of differentiated GBM cells and drove undifferentiated primary patient derived GBM cells into a nonreplicative senescent state.	[^Citation122]
Hepatocellular carcinoma	Transgenic model	Mifepristone-inducible and reversible kras^V12 transgenic system offers a novel model for understanding hepatocarcinogenesis and a high-throughput screening platform for anti-cancer drugs.	[^Citation123]
Hepatocellular carcinoma	Transgenic model	A small Myc target gene set of 16 genes can be used to identify liver tumors due to Myc upregulation. And their zebrafish model demonstrated the conserved role of Myc in promoting hepatocarcinogenesis in all vertebrate species.	[^Citation124]
Hepatocellular carcinoma	Chemically-induced model	Triploid zebrafish demonstrated an overall increase in latency period in the development of both types of hepatic tumors (hepatocellular carcinomas and adenomas), a finding that can be interpreted as an increased resistance of triploid animals to the carcinogenic effect of N-nitrosodimethylamine.	[^Citation125]
Hepatocellular carcinoma	Transgenic model	Metformin can suppress NAFLD-associated HCC progression by decreasing the number of pro-inflammatory macrophages and increasing T cell infiltration.	[^Citation126]
Hepatocellular carcinoma	Transgenic model	For tumor-infiltrated neutrophils and macrophages, significantly higher densities in male liver tumors were observed in both xmrk and Myc models. And there was a higher rate of HSC activation accompanied with a higher level of serotonin in male liver tumors.	[^Citation127]
Hepatocellular carcinoma	Transgenic model	After kras^V12 induction, fibrinogen was up-regulated in oncogenic hepatocytes. They reasoned that fibrinogen may bind to integrin αvβ5 on HSCs to activate HSCs.	[^Citation58]
Hepatocellular carcinoma	Transgenic model	Using the Tet-on system for liver-specific expression of fish oncogene xmrk, a hyperactive version of epidermal growth factor receptor homolog, they generated transgenic zebrafish with inducible development of liver cancer.	[^Citation128]
Hepatocellular carcinoma	Transgenic model	The distribution of neutrophils and macrophages in HCC was relatively uniform, whereas both types of immune cells were regionally clustered during tumor regression, especially with dominant blood vessel association of macrophage in late regression.	[^Citation129]
Hepatocellular carcinoma	Transgenic model	They used zebrafish model to screen for drugs that suppress β-catenin-induced liver growth, and identified two classes of hits, c-Jun N-terminal kinase (JNK) inhibitors and antidepressants, that suppressed this phenotype.	[^Citation130]
Hepatocellular carcinoma	Transgenic model	Their study provides an in vivo evidence of the relationship between chronic inflammation and tumorigenesis and reinforces the pivotal role of IL6 in the inflammation-associated hepatocarcinogenesis.	[^Citation59]
Hepatocellular carcinoma	Transgenic model	An inflammatory cue from oncogenic hepatocytes upon induction of kras^V12 expression causes a rapid recruitment of neutrophils to oncogenic liver and the neutrophils play a promoting role in early hepatocarcinogenesis.	[^Citation131]
Leukemia	Transgenic model	Akt pathway activation is sufficient for tumor maintenance, even after loss of survival signals driven by the MYC oncogene.	[^Citation50]
Leukemia	Xenograft model	Xenotransplantation models of zebrafish can be used to screen non-teratogenic drugs for leukemia.	[^Citation132]
Leukemia	Transgenic model	After screening 26,400 molecules, they identified Lenaldekar (LDK), a compound that eliminates immature T cells in developing zebrafish without affecting the cell cycle in other cell types.	[^Citation54]
Leukemia	Xenograft model	Imaging-based LSC xenotransplant screening in zebrafish offers distinct advantages over other animal models and can greatly accelerate the phenotype-driven discovery of anti-LSC agents.	[^Citation133]
Liver cancer	Xenograft model	Most toxicants, namely chromium, bisphenol A, lindane, N-nitrosodiethylamine, and PCB126, resulted in increased inflammation and liver tumorigenesis, while arsenic and TCDD had opposite effects.	[^Citation134]
Liver cancer	Transgenic model	Halting RhoA signaling could augment Kras-mediated liver overgrowth and tumorigenesis. And activating Rho could be beneficial to suppress Kras-induced liver malignancies.	[^Citation135]
Lung cancer	Xenograft model	In the zebrafish xenograft model, knockdown of LINC00152 reduced the proliferation and migration of lung cancer cells and enhanced the inhibition effect of afatinib for lung cancer progression in cultured cells and the zebrafish xenograft model.	[^Citation69]
Lung cancer	Xenograft model	BPIQ-induced anti-lung cancer is involved in mitochondrial apoptosis. BPIQ could be a promising anti-lung cancer drug for further applications.	[^Citation136]
Lung cancer	Xenograft model	DFIQ exerts anticancer potential in vivo and in vitro and can induce apoptosis. DFIQ-induced apoptosis is associated with lysosome accumulation and the induction of the expression of apoptosis factors, such as Bax, Bad, and tBid.	[^Citation70]
Lung cancer	Xenograft model and Transgenic model	Bevacizumab, endostar and apatinib demonstrated remarkable angiogenesis and tumor inhibition effect in the zebrafish model, within the nonlethal dose range. Endostar and bevacizumab showed competitive anti-tumor efficacy.	[^Citation137]
Melanoma	Xenograft model	Nodal signaling has a key role in melanoma cell plasticity and tumorigenicity, thereby providing a previously unknown molecular target for regulating tumor progression.	[^Citation138]
Melanoma	Transgenic model	Although oncogenic NRAS expression alone was found to be insufficient to promote tumor formation, loss of functional p53 was found to collaborate with NRAS expression in the genesis of melanoma.	[^Citation44]
Melanoma	Transgenic model	BRAF activation is sufficient for f-nevus formation, that BRAF activation is among the primary events in melanoma development, and that the p53 and BRAF pathways interact genetically to produce melanoma.	[^Citation139]
Melanoma	Xenograft model	The zebrafish model reveals that Spint1a deficiency facilitates oncogenic transformation, regulates the tumor immune microenvironment crosstalk, accelerates the onset of SKCM and promotes metastatic invasion.	[^Citation46]
Melanoma	Transgenic model	In an adult model of chronic wounding in zebrafish, they show that repeated wounding with subsequent inflammation leads to a greater incidence of local melanoma formation.	[^Citation140]
Melanoma	Transgenic model	Transgenic THOR knockout produced fertilization defects in zebrafish and also conferred a resistance to melanoma onset. Likewise, ectopic expression of human THOR in zebrafish accelerated the onset of melanoma.	[^Citation141]
Melanoma	Xenograft model	Overexpression of bcl‐xL protein is able to enhance melanoma cell angiogenesis through increasing chemokine CXCL8 secretion. They demonstrate that this feature is associated with the increased ability of bcl‐xL overexpressing cells to enhance invasion in vivo.	[^Citation47]
Melanoma	Xenograft model	Employing in vivo imaging coupled with 3D reconstruction, they monitored the interactions between cancer cells and the external surface of zebrafish vessels. And they found that melanoma cells spread along the abluminal vascular surfaces.	[^Citation45]
Melanoma	Xenograft model	Combined MEK/autophagy inhibition reduced the invasive and metastatic potential of MEKi-resistant cells in an in vivo zebrafish xenograft.	[^Citation142]
Pancreatic cancer	Xenograft model	Xenografts of primary human tumors showed invasiveness and micrometastasis formation within 24 hours after transplantation, which was absent when non-tumor tissue was implanted.	[^Citation143]
Rhabdomyosarcoma	Transgenic model	Their novel zebrafish rhabdomyosarcoma model identifies a new PAX3-FOXO1 target, her3/HES3, that contributes to impaired myogenic differentiation and has prognostic significance in human disease.	[^Citation144]
T-cell acute lymphoblastic leukemia	Xenograft model	Using a focused chemical genomic approach, they demonstrate that xenografted cell lines harboring mutations in the NOTCH1 and PI3K/AKT pathways respond concordantly to their targeted therapies.	[^Citation145]
Thyroid carcinoma	Transgenic model	The expression of TWIST2 plays a role in an early step of BRAF^V600E-mediated transformation.	[^Citation146]

Table 2 PDX Model

Cancer Model	Animal Species	Finding	Reference
Adenoid cystic carcinoma	Zebrafish	The CR/zebrafish model mirrors the PDX mouse model and identifies regorafenib as a potential therapeutic drug to treat this cancer type that mimic the drug sensitivity profile in PDX model.	[^Citation147]
Breast cancer	Mouse	Through various experimental and computational approaches using human tumors within immunocompromised mice, the lung was found to be the most common site of relapse; lymph nodes and liver were the other most common metastatic sites.	[^Citation148]
Breast cancer	Zebrafish	They propose an original approach to study the metastatic process and cancer cell aggressiveness comprising the use of patient-derived primary cultures in the in vivo ZF model.	[^Citation149]
Breast cancer	Mouse	Growth of breast cancer PDX tumors was significantly enhanced by co-transplantation with ADSCs in vivo, and it was weakened when co-transplanted with the adipsin knocked-down ADSCs.	[^Citation150]
Breast cancer	Mouse	PARP inhibition can have activity beyond germline BRCA1/2 altered tumors, causing regression in a variety of molecular subtypes.	[^Citation151]
Breast cancer	Mouse	Concurrent inhibition of sfRon and PI3K in breast PDX tumors with wild-type PIK3CA provided durable tumor stasis after therapy cessation, whereas discontinuation of either monotherapy facilitated tumor recurrence.	[^Citation152]
Cervical cancer	Mouse	In vivo studies with PDXs revealed that TAO significantly decreased tumor weight for both primary squamous cell carcinoma and adenocarcinoma of the cervix. However, this anti-cancer effect was not seen in PDXs with recurrent cancers.	[^Citation153]
Colon Carcinoma	Mouse	HER2-specific CAR-T cells showed long-term persistence in vivo and effectively eliminated the freshly transplanted tumor tissues.	[^Citation154]
Colorectal cancer	Mouse	The gluconeogenic enzyme PCK1 enhanced liver metastatic growth by driving pyrimidine nucleotide biosynthesis under hypoxia. Therapeutic inhibition of the pyrimidine biosynthetic enzyme DHODH with leflunomide substantially impaired CRC liver metastatic colonization and hypoxic growth.	[^Citation155]
Colorectal cancer	Mouse	MAPK and EGFR pathway activations are two major molecular hallmarks of colorectal cancer. Concurrent EGFR and RAF inhibition demonstrated synergistic antitumor activity for colorectal cancer PDX models with a KRAS or BRAF mutation.	[^Citation156]
Colorectal cancer	Mouse	The combination of mefloquine with chemotherapeutic agents in the PDX model potentially disrupts the hierarchy of colorectal cancer cells and identify endolysosomal RAB5/7 and LAMP1/2 as promising therapeutic targets in CSCs.	[^Citation157]
Colorectal cancer	Mouse	HER2 activating mutations cause EGFR antibody resistance in colorectal cell lines, and PDXs with HER2 mutations show durable tumor regression when treated with dual HER2-targeted therapy.	[^Citation158]
Colorectal cancer	Mouse	Ex vivo culture of organoids generated from PDX demonstrates that metformin inhibits growth by executing metabolic changes to decrease oxygen consumption and activating AMPK-mediated pathways.	[^Citation159]
Colorectal cancer	Mouse	Anti-tumor activity of cabozantinib would be superior to regorafenib in CRC PDX models due to dual inhibition of MET and VEGFR2, as well as potentially other metabolic and autophagy mechanisms.	[^Citation160]
Esophageal cancer	Mouse	APIO-EE-9 significantly decreased the size of esophageal patient-derived xenograft (PDX) tumors implanted in SCID mice. It is a specific Aurora kinase inhibitor that could be developed as a therapeutic agent against esophageal cancer.	[^Citation161]
Gastric cancer	Zebrafish	They describe a new in vivo zPDX model of GC. This model can be used to study tumor angiogenesis, cell invasiveness and drug responses in a time-saving and cost-saving manner.	[^Citation162]
Gastric cancer	Mouse	They demonstrated that microRNA-133a-3p overexpression could block the activation of autophagy to ruin the abnormal glutaminolysis and further inhibit the growth and metastasis of gastric cancer cells	[^Citation163]
Gastric cancer	Mouse	Knockdown of circNRIP1 successfully blocked proliferation, migration, invasion and the expression level of AKT1 in GC cells.	[^Citation164]
Gastric cancer	Mouse	CAFs-derived LOX at liver metastatic niche of GC promotes niche formation and outgrowth thus predicts poor prognosis. Meanwhile tumor cells in niche secrete TGF-β1 to nourish CAFs and stimulate them to produce more LOX in turn.	[^Citation165]
Gastric cancer	Mouse	They explored the therapeutic potential of NNT inhibition in PDX models via in vivo siRNA treatment. Silencing NNT significantly suppressed tumor growth and induced cell apoptosis.	[^Citation166]
Gastric cancer	Mouse	ROS-activated ABL1 mediates inflammation through regulating NF-κB1 and STAT3, which subsequently leads to the development of GC and GC-related depression.	[^Citation167]
Gastric cancer	Mouse	Gastrin inhibited GC growth and enhanced the suppression of GC by cisplatin in mice or PGC cell culture models through activating the ERK-P65-miR23a/27a/24 axis or its components.	[^Citation168]
Gastric cancer	Mouse	LH inhibited tumorigenicity in gastric cancer through down-regulating the expression of MCL1. And LH combined with HA14–1 (inhibitor of BCL2) exhibited a more significant inhibitory effect than LH alone in vivo.	[^Citation169]
Gastric cancer	Mouse	In the PDX models with EGFR amplification, mRNA or protein overexpression, cetuximab treatment was associated with a better survival compared with that noted in the untreated group in the PDX models (P<0.05), while the survival was not statistically different in the other cases (P>0.05).	[^Citation170]
Gastric cancer	Mouse	The anti-tumor effect of trastuzumab was enhanced by its combination with anti-HER3 antibodies (1A5–3D4) in NCI-N87 xenograft and patient derived xenografts (PDX). Particularly in an HER2-negative whereas neuregulin1 (a ligand of HER3) positive PDX, the combination was also superior to monotherapy.	[^Citation171]
Gastric cancer	Mouse	124I-trastuzumab was feasible to detect HER2-positive lesions in primary and metastatic gastric cancer patients and to differentiate HER2-positive and HER2-negative lesions quantitatively.	[^Citation172]
Hepatocellular carcinoma	Mouse	A CDK1 inhibitor (RO3306) in combination with sorafenib acts on hepatocellular carcinoma with a synergistic antitumor growth effect on PDX tumor models, which may be due to its effects on decreasing the liver cancer stem cell stemness via the CDK1/PDK1/β-Catenin signaling pathway.	[^Citation173]
High-grade serous ovarian cancer	Mouse	CUB-domain containing protein 1 (CDCP1) is over-expressed by the majority of HGSCs. CDCP1 has a role in HGSC and that it can be targeted to inhibit progression of this cancer.	[^Citation174]
Leukemia	Mouse	Zapadcine-1 drastically eliminates the xenografts in both CDX and PDX models of human acute leukemia. And it does not have notable toxic side effects on heart, liver, lung and kidney.	[^Citation175]
Lung cancer	Mouse	PG545 was highly effective in PDX that did not respond to conventional chemotherapy (cisplatin), while other PDX tumors responded well to cisplatin and to a lower extent to PG545.	[^Citation176]
Lung cancer	Rat	The severely immunodeficient SD‐RG rats support fast growth of PDX compared with mice, thus holding great potential to serve as a new model for oncology research.	[^Citation177]
Lung squamous cell carcinoma	Mouse	Combination therapy with a FGFR tyrosine kinase inhibitor and cisplatin reduced tumor growth by decreasing cell proliferation and increasing cell death.	[^Citation178]
Melanoma	Mouse	Genetic aberration of CDK4 pathway is a frequent event in acral melanoma. Acral melanoma cell lines and PDX containing CDK4 pathway aberrations are sensitive to CDK4/6 inhibitors.	[^Citation179]
Oesophageal adenocarcinoma	Mouse	APR-246 demonstrated potent antitumour activity in CLX and PDX models, and restored chemosensitivity to a cisplatin/5-fluorouracil-resistant xenograft model.	[^Citation180]
Ovarian cancer	Mouse	Treatment with an anti-CD20 monoclonal antibody, rituximab, not only inhibited the proliferation of established B-cell lymphoma in SCID mice but also prevented the occurrence of lymphomatous outgrowth in early-passage xenografts.	[^Citation181]
Ovarian cancer	Mouse	Both the activity of bevacizumab in combination with chemotherapy for the treatment of ovarian tumors and that this antitumor activity can be further improved by the addition of another targeted agents (MEK inhibitor).	[^Citation182]
Pancreatic cancer	Mouse	The VEGF pathway–mediated angiogenesis might influence tumor implantation as well as the growth in PDXs, thus affecting prognosis in patients or tumor‐bearing mice.	[^Citation183]
Pancreatic cancer	Mouse	miR-193a stimulated pancreatic cancer cell repopulation and metastasis through modulating TGF-β2/TGF-βRIII signalings, and miR-193a might be a potential therapeutic target for pancreatic cancer repopulation and metastasis.	[^Citation184]
Pancreatic cancer	Mouse	Adenosine induces apoptosis in pancreatic cancers, and GSK690693 can exert sensitizing effects when applied in combination with adenosine.	[^Citation185]
Pancreatic cancer	Mouse	They developed apratoxin S10 (Apra S10) as an anti-pancreatic cancer agent which potently inhibited the growth of both established and patient-derived primary pancreatic cancer cells.	[^Citation186]
Papillary renal cell carcinoma	Mouse	AZD6094 treatment resulted in tumor regressions, whereas sunitinib or crizotinib resulted in unsustained growth inhibition.	[^Citation187]
Prostate cancer	Mouse	MET in tumor cells is not a persistent therapeutic target for metastatic CRPC, but inhibition of VEGF-R2 and MET in endothelial cells and direct effects on osteoblasts are responsible for cabozantinib-induced tumor inhibition.	[^Citation188]
Prostatic carcinoma	Mouse	Cyclin D1 loss identifies prostate tumors with small cell differentiation and may identify a small subset of adenocarcinomas with poor prognosis.	[^Citation189]
Receptor-negative breast cancer	Mouse	Vandetanib treatment could be useful for patients with ER negative breast cancers overexpressing Vandetanib’s main targets. In a PDX model with no expression of RET nor EGFR, Vandetanib slowed tumor growth without inducing tumor regression.	[^Citation190]
Small cell lung cancer	Mouse	PARP trapping may play an important role in radiosensitization of SCLC cells, as talazoparib was a more effective radiosensitizer compared to veliparib at concentrations chosen to result in equivalent enzymatic inhibition.	[^Citation191]
Triple-negative breast cancer	Mouse	ATF4 expression inhibition reduced migration, invasiveness, mammosphere-forming efficiency, proliferation, epithelial-mesenchymal transition, and antiapoptotic and stemness marker levels. In PDX models, ATF4 silencing decreased metastases, tumor growth, and relapse after chemotherapy.	[^Citation192]
Triple-negative breast cancer	Mouse	Capecitabine was effective against 60% of TNBC PDX derived from tumors previously treated with anthracyclines and taxanes, and we identified TYMP and RB1 expression as putative biomarkers predictive of the response to capecitabine.	[^Citation193]
Triple-negative breast cancer	Mouse	Selinexor is a promising agent in the treatment of TNBC, with enhanced antitumor activity in combination with chemotherapy.	[^Citation194]

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