Vol. 70 No. 1 (2024), REVIEWS

Vol. 70 No. 1 (2024)

The Significance of Xenogenic Models of Malignant Neoplasms In Vivo for Preclinical Studies in Experimental Oncology

REVIEWS

https://doi.org/10.37469/0507-3758-2024-70-1-16-26

Published 07.03.2024

Ahmed Hamid Al-Humairi⁺⁻
Olga Yur’evna Rybalkina⁺⁻
Cherdyntseva Nadezhda Viktorovna ⁺⁻
Vladimir Vasilyevich Udut⁺⁻

Ahmed Hamid Al-Humairi

Volgograd State Medical University

https://orcid.org/0000-0001-7545-8567

Olga Yur’evna Rybalkina

Goldberg Research Institute of Pharmacology and Regenerative Medicine; Tomsk National Research Medical Center, Russian Academy of Sciences

https://orcid.org/0000-0001-8577-4520

Cherdyntseva Nadezhda Viktorovna

Research Institute of Oncology, Tomsk National Research Medical Center, Russian Academy of Sciences; Corresponding Member of the Russian Academy of Sciences

https://orcid.org/0000-0003-1526-9013

Vladimir Vasilyevich Udut

Research Institute of Oncology, Tomsk National Research Medical Center, Russian Academy of Sciences

https://orcid.org/0000-0002-3829-7132

pdf (Русский)

Keywords

experimental oncology
tumor models
xenografts
patient-like models

How to Cite

Al-Humairi, A. H., Rybalkina, O. Y., Viktorovna , C. N., & Udut, V. V. (2024). The Significance of Xenogenic Models of Malignant Neoplasms In Vivo for Preclinical Studies in Experimental Oncology. Voprosy Onkologii, 70(1), 16–26. https://doi.org/10.37469/0507-3758-2024-70-1-16-26

Abstract

Models of xenogenic tumors in vivo play an important role in experimental studies of antitumor compounds. Despite the advances made in this field, chances for a new antitumor drug to be approved for use in an oncology clinic remain low. Such poor reproducibility of experimental results in the clinic is because the existing standard models of malignant neoplasms in vivo have low prognostic significance. Nevertheless, experiments on laboratory models of xenogeneic tumors have been and continue to be crucial in the testing and promotion of potential antiblastoma drugs in clinics. This review analyzes domestic and foreign literature on the creation and application of xenogeneic in vivo models in the experimental oncology.

https://doi.org/10.37469/0507-3758-2024-70-1-16-26

pdf (Русский)

References

Каприн А.Д., Старинский В.В., Шахзадова А.О. Злокачественные новообразования в России в 2021 году (заболеваемость и смертность). М.: МНИОИ им. П.А. Герцена − филиал ФГБУ «НМИЦ радиологии» Минздрава России. 2022: 252. [Kaprin A.D., Starinsky V.V., Shakhzadova A.O. Malignant neoplasms in Russia in 2021 (morbidity and mortality). Moscow: P. Hertsen MORI – branch of the FSBI NMRRC of the Ministry of Health of Russia. 2022: 252. (In Rus)].

Холоденко Р.М., Холоденко И.В., Доронин И.И. Опухолевые модели в изучении онкологических заболеваний. Иммунология. 2013; 5: 282-286. [Kholodenko R.M., Kholodenko I.V., Doronin I.I. Tumor models in the study of oncological diseases. Immunology. 2013; 5: 282-286. (In Rus)].

Кит О.И., Колесников Е.Н., Максимов А.Ю., и др. Методы создания ортотопических моделей рака пищевода и их применение в доклинических исследованиях. Вопросы онкологии. 2019; 2: 303-7. [Kit O.I., Kolesnikov E.N., Maksimov A.Yu., et al. Methods of creating orthotopic models of esophageal cancer and their application in preclinical studies. Voprosy Onkologii = Problems in Oncology. 2019; 2: 303-7. (In Rus)].

Гуляев В.А., Хубутия М.Ш., Новрузбеков М.С., и др. Ксенотрансплантация: история, проблемы и перспективы развития. Трансплантология. 2019; 11(1): 37-54.-DOI: http://dx.doi.org/10.23873/2074-0506-2019-11-1-37-54. [Gulyaev V.A., Khubutia M.Sh., Novruzbekov M.S., et al. Xenotransplantation: history, problems and development prospects. Transplantologiya = The Russian Journal of Transplantation. 2019; 11(1): 37-54.-DOI: http://dx.doi.org/10.23873/2074-0506-2019-11-1-37-54. (In Rus)].

Cekanova M., Rathore K. Animal models and therapeutic molecular targets of cancer: utility and limitations. Drug Des Devel Ther. 2014; 8: 1911-1921.-DOI: https://doi.org/10.2147/DDDT.S49584.

Khaled W.T., Liu P. Cancer mouse models: past, present and future. Semin Cell Dev Biol. 2014; 27: 54-60.-DOI: https://doi.org/10.1016/j.semcdb.2014.04.003.

Kelland L.R. Of mice and men: values and liabilities of the athymic nude mouse model in anticancer drug development. Eur J Cancer. 2004; 40(6): 827-836.-DOI: https://doi.org/10.1016/j.ejca.2003.11.028.

Lee N.P., Chan C.M., Tung L.N., et al. Tumor xenograft animal models for esophageal squamous cell carcinoma. J Biomed Sci. 2018; 25(1): 66.-DOI: https://doi.org/10.1186/s12929-018-0468-7.

Cho S.Y., Kang W., Han J.Y., et al. An integrative approach to precision Cancer medicine using patient-derived xenografts. Mol Cells. 2016; 39(2): 77-86.-DOI: https://doi.org/10.14348/molcells.2016.2350.

Миндарь М.В., Лукбанова Е.А., Кит С.О., и др. Значение иммунодефицитных мышей для экспериментальных и доклинических исследований в онкологии. Сибирский научный медицинский журнал. 2020; 40(3): 10-20.-DOI: https://doi.org/10.15372/SSMJ20200302. [Mindar M.V., Lukyanova E.A., Kit S.O., et al. The importance of immunodeficient mice for experimental and preclinical studies in oncology. Siberian Scientific Medical Journal. 2020; 40(3): 10-20.-DOI: https://doi.org/10.15372/SSMJ20200302. (In Rus)].

Olson B., Li Y., Lin Y., et al. Mouse models for cancer immunotherapy research. Cancer Discov. 2018; 8(11): 1358-1365.-DOI: https://doi.org/10.1158/2159-8290.

Shackleton M., Fearon ER. Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell. 2009; 138: 822-829.-DOI: https://doi.org/10.1016/j.cell.2009.08.017.

Zhao X., Li L., Starr T.K., et al. Tumor location impacts immune response in mouse models of colon cancer. Oncotarget. 2017; 8(33): 54775-54787.-DOI: https://doi.org/10.18632/oncotarget.18423.

Ruggeri B.A., Camp F., Miknyoczki S. Animal models of disease: pre-clinical animal models of cancer and their applications and utility in drug discovery. Biochem Pharmacol. 2014; 87(1): 150-161.-DOI: https://doi.org/10.1016/j.bcp.2013.06.020.

Nair D.V., Reddy A.G. Laboratory animal models for esophageal cancer. Vet World. 2016; 9(11): 1229-1232.-DOI: https://doi.org/10.14202/vetworld.2016.1229-1232.

Гончарова А.С., Протасова Т.П., Лукбанова Е.А., и др. Разработка метода получения ксеногенной опухолевой модели с использованием пористого металлического скаффолда. Вопросы онкологии. 2021; 67(1): 127-13.-DOI: https://doi.org/10.37469/0507-3758-2021-67-1-127-133. [Goncharova A.S., Protasova T.P., Lukyanova E.A., et al. Development of a method for obtaining a xenogenic tumor model using a porous metal scaffold. Voprosy Onkologii = Problems in Oncology. 2021; 67(1): 127-133.-DOI: https://doi.org/10.37469/0507-3758-2021-67-1-127-133. (In Rus)].

Yan S., Jiang H., Fang S., et al. Microrna-340 inhibits esophageal Cancer cell growth and invasion by targeting phosphoserine aminotransferase 1. Cell Physiol Biochem. 2015; 37(1): 375-386.-DOI: https://doi.org/https://doi.org/10.1159/000430361.

Liu M., Hu Y., Zhang M.F., et al. MMP1 promotes tumor growth and metastasis in esophageal squamous cell carcinoma. Cancer Lett. 2016; 377(1): 97-104.-DOI: https://doi.org/10.1016/j.canlet.2016.04.034.

Yang Q., Wang R., Xiao W., et al. Cellular retinoic acid binding protein 2 is strikingly downregulated in human esophageal squamous cell carcinoma and functions as a tumor suppressor. Plos One. 2016; 11(2): e0148381.-DOI: https://doi.org/10.1371/journal.pone.0148381.

Ip J.C., Ko J.M., Yu V.Z., et al. A versatile orthotopic nude mouse model for study of esophageal squamous cell carcinoma. Biomed Res Int. 2015; 910715.-DOI: https://doi.org/10.1155/2015/910715.

Ng H.Y., Ko J.M., Yu V.Z., et al. DESC1, a novel tumor suppressor, sensitizes cells to apoptosis by downregulating the EGFR/AKT pathway in esophageal squamous cell carcinoma. Int J Cancer. 2016; 138(12): 2940-2951.-DOI: https://doi.org/10.1002/ijc.30034.

Чиж Г.А. Современные возможности прогнозирования метастазирования злокачественных новообразований. Маркеры метастазирования. Forcipe. 2019; 1: 31-41. [Chizh G.A. Modern possibilities of predicting metastasis of malignant neoplasms. Markers of metastasis. Forcipe. 2019; 1: 31-41. (In Rus)].

Даниленко Е.Д., Белкина А.О., Сысоева Г.М. Модели костных метастазов в экспериментальных исследованиях (обзор). Биофармацевтический журнал. 2015; 7(4): 3-13. [Danilenko E.D., Belkina A.O., Sysoeva G.M. Models of bone metastases in experimental studies (review). Biopharmaceutical Journal. 2015; 7(4): 3-13. (In Rus)].

Maciejko L., Smalley M., Goldman A. Cancer immunotherapy and personalized medicine: emerging technologies and biomarker-based approaches. J Mol Biomark Diagn. 2017; 8(5): 350.-DOI: https://doi.org/10.4172/2155-9929.1000350.

Beca F., Polyak K. Intratumor Heterogeneity in Breast Cancer. Adv Exp Med Biol. 2016; 882: 169-189.-DOI: https://doi.org/10.1007/978-3-319-22909-6_7.

Hait W.N. Anticancer drug development: the grand challenges. Nat Rev Drug Discov. 2010;9 (4): 253-254.-DOI: https://doi.org/10.1038/nrd3144.

Thibaudeau L., Taubenberger A.V., Holzapfel B.M., et al. Lissueengineered humanized xenograft model of human breast cancer metastasis to bone. Dis Model Mech. 2015; 7: 299-309.

Abate-Daga D., Lagisetty K.H., Tran E., et al. A novel chimeric antigen receptor against prostate stem cell antigen mediates tumor destruction in a humanized mouse model of pancreatic cancer. Hum Gene Ther. 2014; 25(12): 1003-1012.-DOI: https://doi.org/10.1089/hum.2013.209.

Rongvaux A., Willinger T., Martinek J., et al. Development and function of human innate immune cells in a humanized mouse model. Nat Biotechnol. 2014; 32(4): 364-72.-DOI: https://doi.org/10.1038/nbt.2858.

Zhao Y., Shuen T.W.H., Toh T.B., et al. Development of a new patient-derived xenograft humanised mouse model to study human-specific tumour microenvironment and immunotherapy. Gut. 2018; 67(10): 1845-54.-DOI: https://doi.org/10.1136/gutjnl-2017-315201.

Chu Y., Hochberg J., Yahr A., et al. Targeting CD20+ aggressive B-cell non-hodgkin lymphoma by Anti-CD20 CAR mrna-modified expanded natural killer cells in vitro and in NSG Mice. Cancer Immunol Res. 2015; 3(4): 333-44.-DOI: https://doi.org/10.1158/2326-6066.CIR-14-0114.

Smith D.J., Lin L.J., Moon H., et al. Propagating humanized BLT mice for the study of human immunology and immunotherapy. Stem Cells and Development. 2016; 25(24): 1863-1873.

Wege A.K., Ernst W., Eckl S., et al. Humanized tumor mice – a new model to study and manipulate the immune response in advanced cancer therapy. Fnt J Cancer. 2011; 129: 2194-2206.

Nguyen R., Patel A.G., Griffiths L.M., et al. Next-generation humanized patient-derived xenograft mouse model for pre-clinical antibody studies in neuroblastoma. Cancer Immunol Immunother. 2021; 70(3): 721-732.-DOI: https://doi.org/10.1007/s00262-020-02713-6.

Scherer S.D., Riggio A.I., Haroun F., et al. An immune-humanized patient-derived xenograft model of estrogen-independent, hormone receptor positive metastatic breast cancer. Breast Cancer Res. 2021; 30; 23(1):100.-DOI: https://doi.org/10.1186/s13058-021-01476-x.

Beaber E., Buist D., Barlow W., et al. Recent oral contraceptive use by formulationand breast cancer riskamong women 20 to 49 years of age. Cancer Rese arch. 2014; 74(15): 4078-4089.

Гончарова А.С., Шевченко А.Н., Дашкова И.Р., и др. Методологические аспекты создания ксенотрансплантатов опухолей, полученных от пациентов. Казанский медицинский журнал. 2021; 102 (5): 694-702.-DOI: https://doi.org/10.17816/KMJ2021-694. [Goncharova A.S., Shevchenko A.N., Dashkova I.R., et al. Methodological aspects of creating xenografts of tumors obtained from patients. Kazan Medical Journal. 2021; 102 (5): 694-702.-DOI: https://doi.org/10.17816/KMJ2021-694. (In Rus)].

Wang Y., Wang J.X., Xue H., et al. Subrenal capsule grafting technology in human cancer modeling and translational cancer research. Differentiation. 2016; 91(4-5): 15-19.-DOI: https://doi.org/10.1016/j.diff.2015.10.012.

Serna V.A., Kurita T. Patient-derived xenograft model for uterine leiomyoma by sub-renal capsule graf¬ting. J Biol Methods. 2018; 5(2): e91.-DOI: https://doi.org/10.14440/jbm.2018.243.

Larmour L.I., Cousins F.L., Teague J.A., et al. A patient derived xenograft model of cervical cancer and cervical dysplasia. Plos One. 2018; 13(10): e0206539.-DOI: https://doi.org/10.1371/journal.pone.0206539.

Priolo C., Agostini M., Vena N., et al. Establishment and genomic characterization of mouse xenografts of human primary prostate tumors. Am J Pathol. 2010; 176(4): 1901-1913.-DOI: https://doi.org/10.2353/ajpath.2010.090873.

Zhao H., Nolley R., Chen Z., et al. Tissue slice grafts: an in vivo model of human prostate androgen signaling. Am J Pathol. 2010; 177(1): 229-239.-DOI: https://doi.org/10.2353/ajpath.2010.090821.

Qu S., Ci X., Xue H., et al. Treatment with docetaxel in combination with Aneustat leads to potent inhibition of metastasis in a patient-derived xenograft model of advanced prostate cancer. Brit J Cancer. 2018; 118(6): 802-812.-DOI: https://doi.org/10.1038/bjc.2017.474.

Tang S., Yang R., Zhou X., et al. Expression of GOLPH3 in patients with non-small cell lung cancer and xenografts models. Oncology Letters. 2018; 15(5): 7555-7562.-DOI: https://doi.org/10.3892/ol.2018.8340.

Heo E.J., Cho Y.J., Cho W.C., et al. Patient-derived xenograft models of epithelial ovarian cancer for preclinical studies. Cancer Res. Treat. 2017; 49(4): 915-926.-DOI: https://doi.org/10.4143/crt.2016.322.

Yu D.S., Lee C.F., Chang S.Y. Immunotherapy for orthotopic murine bladder cancer using bacillus Calmette-Guerin recombinant protein Mpt64. J Urol. 2007; 177(2): 738-42.-DOI: https://doi.org/10.1016/j.juro.2006.09.074.

Филоненко Д.В., Андронова Н.В., Трещалина Е.М., и др. Оценка чувствительности к герцептину продкожных ксенографтов рака молочной железы человека SKBR3 при трансплантации иммунодефицитным мышам Balb/c nude разведения ГУ РОНЦ им. Н. Н. Блохина РАМН. Российский биотерапевтический журнал. 2008; 3: 42-48. [Filonenko D.V., Andronova N.V., Treshchalina E.M., et al. Evaluation of sensitivity to herceptin of subcutaneous xenografts of human breast cancer SKBR3 during transplantation to immunodeficient mice Balb/c nude breeding of the N. N. Blokhin State Research Center of the Russian Academy of Medical Sciences. Russian Biotherapeutic Journal. 2008; 3: 42-48. (In Rus)].

Abdolahi S., Ghazvinian Z., Muhammadnejad S., et al. Patient-derived xenograft (PDX) models, applications and challenges in cancer research. J Transl Med. 2022; 20(1): 206.-DOI: https://doi.org/10.1186/s12967-022-03405-8.

Kopetz S., Desai J., Chan E., et al. Phase II pilot study of vemurafenib in patients with metastatic BRAF-mutated colorectal cancer. J Clin Oncol. 2015; 33(34): 4032.-DOI: https://doi.org/10.1200/JCO.2015.63.2497.

Hidalgo M., Amant F., Biankin A.V., et al. Patient-derived xenograft models: an emerging platform for translational cancer research. Cancer Discov. 2014; 4(9): 998-1013.-DOI: https://doi.org/10.1158/2159-8290.CD-14-0001.

Byrne A.T., Alférez D.G., Amant F., et al. Interrogating open issues in cancer precision medicine with patient-derived xenografts. Nat Rev Cancer. 2017; 17(4): 254.-DOI: https://doi.org/10.1038/nrc.2016.140.

Marangoni E., Vincent-Salomon A., Auger N., et al. A new model of patient tumor-derived breast cancer xenografts for preclinical assays. Clin Cancer Res. 2007; 13(13): 3989-3998.-DOI: https://doi.org/10.1158/1078-0432.CCR-07-0078.

Zhang X., Claerhout S., Prat A., et al. A renewable tissue resource of phenotypically stable, biologically and ethnically diverse, patient-derived human breast cancer xenograft models. Can Res. 2013; 73(15): 4885-4897.-DOI: https://doi.org/10.1158/0008-5472.CAN-12-4081.

Bertotti A., Migliardi G., Galimi F., et al. A molecularly annotated platform of patient-derived xenografts (“xenopatients”) identifies HER2 as an effective therapeutic target in cetuximab-resistant colorectal cancer. Cancer Discov. 2011; 1(6): 508-523.-DOI: https://doi.org/10.1158/2159-8290.CD-11-0109.

Nunes M., Vrignaud P., Vacher S., et al. Evaluating patient-derived colorectal cancer xenografts as preclinical models by comparison with patient clinical data. Can Res. 2015; 75(8): 1560-1566.-DOI: https://doi.org/10.1158/0008-5472.CAN-14-1590.

Kim M.K., Osada T., Barry W.T., et al. Characterization of an oxaliplatin sensitivity predictor in a preclinical murine model of colorectal cancer. Mol Cancer Ther. 2012; 11(7): 1500-1509.-DOI: https://doi.org/10.1158/1535-7163.MCT-11-0937.

Liu Y., Wu W., Cai C., et al. Patient-derived xenograft models in cancer therapy: technologies and applications. Sig Transduct Target Ther. 2023; 8: 160.-DOI: https://doi.org/10.1038/s41392-023-01419-2.

Maru Y., Hippo Y. Current status of patient-derived ovarian cancer models. Cells. 2019; 8(5): 505.-DOI: https://doi.org/10.3390/cells8050505.

Buolamwini J.K. Novel anticancer drug discovery. Curr Opin Chem Biol. 1999; 3(4): 500-9.-DOI: https://doi.org/10.1016/S1367-5931(99)80073-8.

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