Summary and comparison of mouse models in the basic research in colorectal cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

ZHANG Yukun , HU Hanqing , SHENG Xiangzong , WU Hongyu , ZHANG Qian ,  WANG Guiyu

Department of Colorectal Cancer Surgery, The Second Affiliated Hospital of Harbin Medical University, Harbin 150086, P. R. China;

Corresponding author：

WANG Guiyu, Email: guiywang@163.com

Keywords：

colorectal cancer; mouse model; model evaluation; model comparison

DOI：

10.7507/1007-9424.202009011

Video：

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Objective To summarize the common mouse models and the latest research progress in the basic research of colorectal cancer, introducing advantages, disadvantages and applications of these various models, provide references for the researchers in the selection of mouse models for their experiments.Method Retrieved the related literatures from databases including PubMed, Web of Science, CNKI and WanFang, and after reading the literatures, different methods were sorted out, analyzed and summarized.Results The mouse models commonly used in colorectal cancer research include the cell-derived xenograft (CDX), patient-derived xenograft (PDX), chemical reagent-induced tumor in situ, transgenic mice (Apc^Min/+ mice), tumor cells derived from mice themselves were inoculated to the normal mice, and models of colorectal metastatic tumors (including liver, lung, abdomen and bone metastases, etc.). The CDX model cost shorter time to establish, and the PDX model restored the authentic phenotype of the tumor in patients, but the tumor were both colonized under the skin of nude mice, which lacked authenticity tumor microenvironment. The colorectal cancer in mice induced by chemical reagents and genetically engineered mice imitated the development of colorectal tumor in the situ intestine of mouse, but both of them were time-consuming. The model established by the tumor of mouse own was convenient for basic immune research of colorectal cancer, but the disadvantage was the unreal tumor microenvironment. The colorectal cancer metastasis model was an essential model for the study of the mechanism and treatment in metastasis colorectal tumor, but its establishment required higher operating skills and required the image examination to determine the whether the metastasis tumor was successfully generated or not.Conclusions Different mouse models of colorectal cancer have different emphases, advantages and disadvantages. Researchers need to make accurate selection according to the research purpose and design needs.

Citation： ZHANG Yukun, HU Hanqing, SHENG Xiangzong, WU Hongyu, ZHANG Qian, WANG Guiyu. Summary and comparison of mouse models in the basic research in colorectal cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2021, 28(6): 816-820. doi: 10.7507/1007-9424.202009011 Copy

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2.	American Type Culture Collection Standards Development Organization Workgroup ASN-0002. Cell line misidentification: the beginning of the end. Nat Rev Cancer, 2010, 10(6): 441-448.
3.	Greshock J, Bachman KE, Degenhardt YY, et al. Molecular target class is predictive of in vitro response profile. Cancer Res, 2010, 70(9): 3677-3686.
4.	Lee MS, Helms TL, Feng N, et al. Efficacy of the combination of MEK and CDK4/6 inhibitors in vitro and in vivo in KRAS mutant colorectal cancer models. Oncotarget, 2016, 7(26): 39595-39608.
5.	Kang XJ, Wang HY, Peng HG, et al. Codelivery of dihydro-artemisinin and doxorubicin in mannosylated liposomes for drug-resistant colon cancer therapy. Acta Pharmacol Sin, 2017, 38(6): 885-896.
6.	Bian Z, Zhang J, Li M, et al. LncRNA-FEZF1-AS1 promotes tumor proliferation and metastasis in colorectal cancer by regulating PKM2 signaling. Clin Cancer Res, 2018, 24(19): 4808-4819.
7.	Ye F, Chen C, Qin J, et al. Genetic profiling reveals an alarming rate of cross-contamination among human cell lines used in China. FASEB J, 2015, 29(10): 4268-4272.
8.	Kopetz S, Lemos R, Powis G. The promise of patient-derived xenografts: the best laid plans of mice and men. Clin Cancer Res, 2012, 18(19): 5160-5162.
9.	Inoue A, Deem AK, Kopetz S, et al. Current and future horizons of patient-derived xenograft models in colorectal cancer translational research. Cancers (Basel), 2019, 11(9): 1321.
10.	Kuwata T, Yanagihara K, Iino Y, et al. Establishment of novel gastric cancer patient-derived xenografts and cell lines: pathological comparison between primary tumor, patient-derived, and cell-line derived xenografts. Cells, 2019, 8(6): 585.
11.	王振强, 朱正纲. PDX 模型在肿瘤转化医学中的应用与发展. 中华胃肠外科杂志, 2017, 20(5): 596-600.
12.	Zhu Q, Jin Z, Wu W, et al. Analysis of the intestinal lumen microbiota in an animal model of colorectal cancer. PLoS One, 2014, 9(6): e90849.
13.	Angelou A, Andreatos N, Antoniou E, et al. A novel modification of the AOM/DSS model for inducing intestinal adenomas in mice. Anticancer Res, 2018, 38(6): 3467-3470.
14.	Wirtz S, Neufert C, Weigmann B, et al. Chemically induced mouse models of intestinal inflammation. Nat Protoc, 2007, 2(3): 541-546.
15.	Snider AJ, Bialkowska AB, Ghaleb AM, et al. Murine model for colitis-associated cancer of the colon. Methods Mol Biol, 2016, 1438: 245-254.
16.	Ke Z, Wang C, Wu T, et al. PAR2 deficiency enhances myeloid cell-mediated immunosuppression and promotes colitis-associated tumorigenesis. Cancer Lett, 2020, 469: 437-446.
17.	Wang CZ, Huang WH, Zhang CF, et al. Role of intestinal microbiome in American ginseng-mediated colon cancer prevention in high fat diet-fed AOM/DSS mice [corrected]. Clin Transl Oncol, 2018, 20(3): 302-312.
18.	Yassin M, Sadowska Z, Djurhuus D, et al. Upregulation of PD-1 follows tumour development in the AOM/DSS model of inflammation-induced colorectal cancer in mice. Immunology, 2019, 158(1): 35-46.
19.	Betzler AM, Kochall S, Blickensdörfer L, et al. A genetically engineered mouse model of sporadic colorectal cancer. J Vis Exp, 2017, 125: 55952.
20.	Lin YC, Lin YC, Chen CJ. Cancers complicating inflammatory bowel disease. N Engl J Med, 2015, 373(2): 194-195.
21.	Näthke IS. The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium. Annu Rev Cell Dev Biol, 2004, 20: 337-366.
22.	Su LK, Kinzler KW, Vogelstein B, et al. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science, 1992, 256(5057): 668-670.
23.	Yamada Y, Mori H. Multistep carcinogenesis of the colon in Apc^(Min/+) mouse. Cancer Sci, 2007, 98(1): 6-10.
24.	Taketo MM, Edelmann W. Mouse models of colon cancer. Gastroenterology, 2009, 136(3): 780-798.
25.	Fodde R. The APC gene in colorectal cancer. Eur J Cancer, 2002, 38(7): 867-871.
26.	Liu T, Guo Z, Song X, et al. High-fat diet-induced dysbiosis mediates MCP-1/CCR2 axis-dependent M2 macrophage polarization and promotes intestinal adenoma-adenocarcinoma sequence. J Cell Mol Med, 2020, 24(4): 2648-2662.
27.	Adachi S, Hamoya T, Fujii G, et al. Theracurmin inhibits intestinal polyp development in Apc-mutant mice by inhibiting inflammation-related factors. Cancer Sci, 2020, 111(4): 1367-1374.
28.	Zhang Q, Bi J, Zheng X, et al. Blockade of the checkpoint receptor TIGIT prevents NK cell exhaustion and elicits potent anti-tumor immunity. Nat Immunol, 2018, 19(7): 723-732.
29.	Park SM, Jeon SK, Kim OH, et al. Anti-tumor effects of the ethanolic extract of Trichosanthes kirilowii seeds in colorectal cancer. Chin Med, 2019, 14: 43.
30.	Schroeder A, Heller DA, Winslow MM, et al. Treating metastatic cancer with nanotechnology. Nat Rev Cancer, 2011, 12(1): 39-50.
31.	Nguyen DX, Bos PD, Massagué J. Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer, 2009, 9(4): 274-284.
32.	Mittal VK, Bhullar JS, Jayant K. Animal models of human colorectal cancer: Current status, uses and limitations. World J Gastroenterol, 2015, 21(41): 11854-11861.
33.	Okamoto K, Ishiguro T, Midorikawa Y, et al. MiR-493 induction during carcinogenesis blocks metastatic settlement of colon cancer cells in liver. EMBO J, 2012, 31(7): 1752-1763.
34.	Brouquet A, Vauthey JN, Contreras CM, et al. Improved survival after resection of liver and lung colorectal metastases compared with liver-only metastases: a study of 112 patients with limited lung metastatic disease. J Am Coll Surg, 2011, 213(1): 62-69.
35.	Wu X, Li R, Song Q, et al. JMJD2C promotes colorectal cancer metastasis via regulating histone methylation of MALAT1 promoter and enhancing β-catenin signaling pathway. J Exp Clin Cancer Res, 2019, 38(1): 435.
36.	Razavi R, Harrison LE. Thermal sensitization using induced oxidative stress decreases tumor growth in an in vivo model of hyperthermic intraperitoneal perfusion. Ann Surg Oncol, 2010, 17(1): 304-311.
37.	刘福英. 肿瘤骨转移动物模型研究进展. 中国比较医学杂志, 2010, 20(7): 1-4.
38.	刘希, 杨文生, 康政宇, 等. 可视化人结直肠癌细胞裸鼠直肠原位移植淋巴转移模型的建立. 中国普外基础与临床杂志, 2020, 27(6): 679-684.
39.	Peuker K, Muff S, Wang J, et al. Epithelial calcineurin controls microbiota-dependent intestinal tumor development. Nat Med, 2016, 22(5): 506-515.
40.	黄晓东, 郑勇斌, 杨玉杰, 等. Apc^loxP/loxP+Kras^LSL-G12D/-转基因小鼠模拟人散发性结直肠癌. 中华实验外科杂志, 2019, 36(10): 1791-1794.

1. Callaway E. Contamination hits cell work. Nature, 2014, 511(7511): 518.
2. American Type Culture Collection Standards Development Organization Workgroup ASN-0002. Cell line misidentification: the beginning of the end. Nat Rev Cancer, 2010, 10(6): 441-448.
3. Greshock J, Bachman KE, Degenhardt YY, et al. Molecular target class is predictive of in vitro response profile. Cancer Res, 2010, 70(9): 3677-3686.
4. Lee MS, Helms TL, Feng N, et al. Efficacy of the combination of MEK and CDK4/6 inhibitors in vitro and in vivo in KRAS mutant colorectal cancer models. Oncotarget, 2016, 7(26): 39595-39608.
5. Kang XJ, Wang HY, Peng HG, et al. Codelivery of dihydro-artemisinin and doxorubicin in mannosylated liposomes for drug-resistant colon cancer therapy. Acta Pharmacol Sin, 2017, 38(6): 885-896.
6. Bian Z, Zhang J, Li M, et al. LncRNA-FEZF1-AS1 promotes tumor proliferation and metastasis in colorectal cancer by regulating PKM2 signaling. Clin Cancer Res, 2018, 24(19): 4808-4819.
7. Ye F, Chen C, Qin J, et al. Genetic profiling reveals an alarming rate of cross-contamination among human cell lines used in China. FASEB J, 2015, 29(10): 4268-4272.
8. Kopetz S, Lemos R, Powis G. The promise of patient-derived xenografts: the best laid plans of mice and men. Clin Cancer Res, 2012, 18(19): 5160-5162.
9. Inoue A, Deem AK, Kopetz S, et al. Current and future horizons of patient-derived xenograft models in colorectal cancer translational research. Cancers (Basel), 2019, 11(9): 1321.
10. Kuwata T, Yanagihara K, Iino Y, et al. Establishment of novel gastric cancer patient-derived xenografts and cell lines: pathological comparison between primary tumor, patient-derived, and cell-line derived xenografts. Cells, 2019, 8(6): 585.
11. 王振强, 朱正纲. PDX 模型在肿瘤转化医学中的应用与发展. 中华胃肠外科杂志, 2017, 20(5): 596-600.
12. Zhu Q, Jin Z, Wu W, et al. Analysis of the intestinal lumen microbiota in an animal model of colorectal cancer. PLoS One, 2014, 9(6): e90849.
13. Angelou A, Andreatos N, Antoniou E, et al. A novel modification of the AOM/DSS model for inducing intestinal adenomas in mice. Anticancer Res, 2018, 38(6): 3467-3470.
14. Wirtz S, Neufert C, Weigmann B, et al. Chemically induced mouse models of intestinal inflammation. Nat Protoc, 2007, 2(3): 541-546.
15. Snider AJ, Bialkowska AB, Ghaleb AM, et al. Murine model for colitis-associated cancer of the colon. Methods Mol Biol, 2016, 1438: 245-254.
16. Ke Z, Wang C, Wu T, et al. PAR2 deficiency enhances myeloid cell-mediated immunosuppression and promotes colitis-associated tumorigenesis. Cancer Lett, 2020, 469: 437-446.
17. Wang CZ, Huang WH, Zhang CF, et al. Role of intestinal microbiome in American ginseng-mediated colon cancer prevention in high fat diet-fed AOM/DSS mice [corrected]. Clin Transl Oncol, 2018, 20(3): 302-312.
18. Yassin M, Sadowska Z, Djurhuus D, et al. Upregulation of PD-1 follows tumour development in the AOM/DSS model of inflammation-induced colorectal cancer in mice. Immunology, 2019, 158(1): 35-46.
19. Betzler AM, Kochall S, Blickensdörfer L, et al. A genetically engineered mouse model of sporadic colorectal cancer. J Vis Exp, 2017, 125: 55952.
20. Lin YC, Lin YC, Chen CJ. Cancers complicating inflammatory bowel disease. N Engl J Med, 2015, 373(2): 194-195.
21. Näthke IS. The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium. Annu Rev Cell Dev Biol, 2004, 20: 337-366.
22. Su LK, Kinzler KW, Vogelstein B, et al. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science, 1992, 256(5057): 668-670.
23. Yamada Y, Mori H. Multistep carcinogenesis of the colon in Apc^(Min/+) mouse. Cancer Sci, 2007, 98(1): 6-10.
24. Taketo MM, Edelmann W. Mouse models of colon cancer. Gastroenterology, 2009, 136(3): 780-798.
25. Fodde R. The APC gene in colorectal cancer. Eur J Cancer, 2002, 38(7): 867-871.
26. Liu T, Guo Z, Song X, et al. High-fat diet-induced dysbiosis mediates MCP-1/CCR2 axis-dependent M2 macrophage polarization and promotes intestinal adenoma-adenocarcinoma sequence. J Cell Mol Med, 2020, 24(4): 2648-2662.
27. Adachi S, Hamoya T, Fujii G, et al. Theracurmin inhibits intestinal polyp development in Apc-mutant mice by inhibiting inflammation-related factors. Cancer Sci, 2020, 111(4): 1367-1374.
28. Zhang Q, Bi J, Zheng X, et al. Blockade of the checkpoint receptor TIGIT prevents NK cell exhaustion and elicits potent anti-tumor immunity. Nat Immunol, 2018, 19(7): 723-732.
29. Park SM, Jeon SK, Kim OH, et al. Anti-tumor effects of the ethanolic extract of Trichosanthes kirilowii seeds in colorectal cancer. Chin Med, 2019, 14: 43.
30. Schroeder A, Heller DA, Winslow MM, et al. Treating metastatic cancer with nanotechnology. Nat Rev Cancer, 2011, 12(1): 39-50.
31. Nguyen DX, Bos PD, Massagué J. Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer, 2009, 9(4): 274-284.
32. Mittal VK, Bhullar JS, Jayant K. Animal models of human colorectal cancer: Current status, uses and limitations. World J Gastroenterol, 2015, 21(41): 11854-11861.
33. Okamoto K, Ishiguro T, Midorikawa Y, et al. MiR-493 induction during carcinogenesis blocks metastatic settlement of colon cancer cells in liver. EMBO J, 2012, 31(7): 1752-1763.
34. Brouquet A, Vauthey JN, Contreras CM, et al. Improved survival after resection of liver and lung colorectal metastases compared with liver-only metastases: a study of 112 patients with limited lung metastatic disease. J Am Coll Surg, 2011, 213(1): 62-69.
35. Wu X, Li R, Song Q, et al. JMJD2C promotes colorectal cancer metastasis via regulating histone methylation of MALAT1 promoter and enhancing β-catenin signaling pathway. J Exp Clin Cancer Res, 2019, 38(1): 435.
36. Razavi R, Harrison LE. Thermal sensitization using induced oxidative stress decreases tumor growth in an in vivo model of hyperthermic intraperitoneal perfusion. Ann Surg Oncol, 2010, 17(1): 304-311.
37. 刘福英. 肿瘤骨转移动物模型研究进展. 中国比较医学杂志, 2010, 20(7): 1-4.
38. 刘希, 杨文生, 康政宇, 等. 可视化人结直肠癌细胞裸鼠直肠原位移植淋巴转移模型的建立. 中国普外基础与临床杂志, 2020, 27(6): 679-684.
39. Peuker K, Muff S, Wang J, et al. Epithelial calcineurin controls microbiota-dependent intestinal tumor development. Nat Med, 2016, 22(5): 506-515.
40. 黄晓东, 郑勇斌, 杨玉杰, 等. Apc^loxP/loxP+Kras^LSL-G12D/-转基因小鼠模拟人散发性结直肠癌. 中华实验外科杂志, 2019, 36(10): 1791-1794.

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Summary and comparison of mouse models in the basic research in colorectal cancer

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