1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Cancer Biology
  4. Volume 6, 2022
  5. Article

Annual Review of Cancer Biology

Volume 6, 2022

Novel Mouse Models for Cancer Immunology

Abstract

Mouse models of cancer immunology provide excellent systems in which to study and test biological mechanisms of the immune response against cancer. Historically, these models were designed to have different strengths based on the current major research questions at the time. As such, many mouse models of immunology used today were not originally developed to study current questions in the relatively new field of cancer immunology, but instead have been adapted for such purposes. In this review, we discuss various mouse models of cancer immunology in a historical context in order to provide a fuller perspective of each model's strengths. From this outlook, we discuss the current state of the art and strategies for tackling future modeling challenges.

Keyword(s): cancer, genetically engineered animal, immunology, laboratory mice
Loading

Article metrics loading...

/content/journals/10.1146/annurev-cancerbio-070620-105523
2022-04-11
2024-05-03
Loading full text...

Full text loading...

/deliver/fulltext/cancerbio/6/1/annurev-cancerbio-070620-105523.html?itemId=/content/journals/10.1146/annurev-cancerbio-070620-105523&mimeType=html&fmt=ahah

Literature Cited

  1. Alonso R, Flament H, Lemoine S, Sedlik C, Bottasso E et al. 2018. Induction of anergic or regulatory tumor-specific CD4+ T cells in the tumor-draining lymph node. Nat. Commun. 9:2113
     [Google Scholar]
  2. Ashworth A, Lord CJ, Reis-Filho JS. 2011. Genetic interactions in cancer progression and treatment. Cell 145:30–38
     [Google Scholar]
  3. Baumjohann D, Brossart P. 2021. T follicular helper cells: linking cancer immunotherapy and immune-related adverse events. J. Immunother. Cancer 9:e002588
     [Google Scholar]
  4. Ben-David U, Ha G, Tseng YY, Greenwald NF, Oh C et al. 2017. Patient-derived xenografts undergo mouse-specific tumor evolution. Nat. Genet. 49:1567–75
     [Google Scholar]
  5. Billingham RE, Brent L, Medawar PB 1953.. ‘ Actively acquired tolerance’ of foreign cells. Nature 172:603–6
     [Google Scholar]
  6. Binnewies M, Roberts EW, Kersten K, Chan V, Fearon DF et al. 2018. Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat. Med. 24:541–50
     [Google Scholar]
  7. Bittner JJ. 1936. The spontaneous incidence of lung tumors in relation to the incidence of mammary tumors in an inbred strain of albino mice (strain A). Cancer Res. 27:519–24
     [Google Scholar]
  8. Bittner JJ. 1937. Mammary tumors in mice in relation to nursing. Cancer Res. 30:530–38
     [Google Scholar]
  9. Bittner JJ. 1939. Relation of nursing to the extra-chromosomal theory of breast cancer in mice. Am. J. Cancer 35:90–97
     [Google Scholar]
  10. Bogden AE, Griffen W, Reich SD, Costanza ME, Cobb WR. 1984. Predictive testing with the subrenal capsule assay. Cancer Treat. Rev. 11:113–24
     [Google Scholar]
  11. Boutin AT, Liao WT, Wang M, Hwang SS, Karpinets TV et al. 2017. Oncogenic Kras drives invasion and maintains metastases in colorectal cancer. Genes Dev. 31:370–82
     [Google Scholar]
  12. Brahmer J, Tykodi SS, Chow LQM, Hwu W, Topalian SL et al. 2012. Safety and activity of anti–PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med. 366:262455–65
     [Google Scholar]
  13. Brahmer JR, Lacchetti C, Schneider BJ, Atkins MB, Brassil KJ et al. 2017. Management of immune-related adverse events in patients treated with immune checkpoint inhibitor therapy: American Society of Clinical Oncology clinical practice guideline. J. Clin. Oncol. 36:171714–68
     [Google Scholar]
  14. Brichard V, Pel AV, Wölfel T, Wölfel C, Plaen ED et al. 1993. The tyrosinase gene codes for an antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J. Exp. Med. 178:489–95
     [Google Scholar]
  15. Bruggen PVD, Traversari C, Chomez P, Lurquin C, Plaen ED et al. 1991. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 254:50381643–47
     [Google Scholar]
  16. Cassidy JW, Caldas C, Bruna A 2015. Maintaining tumor heterogeneity in patient-derived tumor xenografts. Cancer Res. 75:2963–68
     [Google Scholar]
  17. Chen DS, Mellman I. 2013. Oncology meets immunology: the cancer-immunity cycle. Immunity 39:1–10
     [Google Scholar]
  18. Chen S, Sanjana NE, Zheng K, Shalem O, Lee K et al. 2015. Genome-wide CRISPR screen in a mouse model of tumor growth and metastasis. Cell 160:1246–60
     [Google Scholar]
  19. Cheng J, DeCaprio JA, Fluck MM, Schaffhausen BS. 2009. Cellular transformation by simian virus 40 and murine polyoma virus T antigens. Semin. Cancer Biol. 19:218–28
     [Google Scholar]
  20. Cherry SR, Biniszkiewicz D, Vanparus L, Baltimore D, Jaenisch R. 2000. Retroviral expression in embryonic stem cells and hematopoietic stem cells. Mol. Cell. Biol.207419–26
     [Google Scholar]
  21. Cheung AF, DuPage MJ, Dong HK, Chen J, Jacks T 2008. Regulated expression of a tumor-associated antigen reveals multiple levels of T-cell tolerance in a mouse model of lung cancer. Cancer Res. 68:9459–68
     [Google Scholar]
  22. Chung WJ, Daemen A, Cheng JH, Long JE, Cooper JE et al. 2017. Kras mutant genetically engineered mouse models of human cancers are genomically heterogeneous. PNAS 114:E10947–55
     [Google Scholar]
  23. Connolly KA, Kuchroo M, Venkat A, Khatun A, Wang J et al. 2021. A reservoir of stem-like CD8 T cells in the tumor-draining lymph node maintains the ongoing anti-tumor immune response. Sci. Immunol. 6:64eabg7836
     [Google Scholar]
  24. Cortez JT, Montauti E, Shifrut E, Gatchalian J, Zhang Y et al. 2020. CRISPR screen in regulatory T cells reveals modulators of Foxp3. Nature 582:416–20
     [Google Scholar]
  25. Cui C, Wang J, Fagerberg E, Chen P-M, Connolly KA et al. 2021. Neoantigen driven B cell and CD4 T follicular helper cell collaboration promotes robust anti-tumor CD8 T cell responses. Cell 184:6101–18.e13
     [Google Scholar]
  26. Curran MA, Montalvo W, Yagita H, Allison JP. 2010. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. PNAS 107:4275–80
     [Google Scholar]
  27. Damo M, Cui C, William I, Hornick NI, Kwok D et al. 2021. The PD-1 checkpoint receptor maintains tolerance of self-reactive CD8 T cell in skin. bioRxiv 2021.07.09.451765. https://doi.org/10.1101/2021.07.09.451765
    [Crossref]
  28. Damo M, Fitzgerald B, Lu Y, Nader M, William I et al. 2020. Inducible de novo expression of neoantigens in tumor cells and mice. Nat. Biotechnol. 39:64–73
     [Google Scholar]
  29. Dankort D, Curley DP, Cartlidge RA, Nelson B, Karnezis AN et al. 2009. BrafV600E cooperates with Pten loss to induce metastatic melanoma. Nat. Genet. 41:544–52
     [Google Scholar]
  30. Davis BW, Ostrander EA. 2014. Domestic dogs and cancer research: a breed-based genomics approach. ILAR J. 55:59–68
     [Google Scholar]
  31. DeVita VT Jr., Chu E. 2008. A history of cancer chemotherapy. Cancer Res. 68:8643–53
     [Google Scholar]
  32. Dewi FN, Cline JM. 2021. Nonhuman primate model in mammary gland biology and neoplasia research. Lab. Anim. Res. 37:3
     [Google Scholar]
  33. Dong H, Strome SE, Salomao DR, Tamura H, Hirano F et al. 2002. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 8:793–800
     [Google Scholar]
  34. Dong MB, Wang G, Chow RD, Ye L, Zhu L et al. 2019. Systematic immunotherapy target discovery using genome-scale in vivo CRISPR screens in CD8 T cells. Cell 178:1189–204.e23
     [Google Scholar]
  35. Dubrot J, Lane-Reticker SK, Kessler EA, Ayer A, Mishra G et al. 2021. In vivo screens using a selective CRISPR antigen removal lentiviral vector system reveal immune dependencies in renal cell carcinoma. Immunity 54:571–85.e6
     [Google Scholar]
  36. Dunn GP, Bruce AT, Sheehan KC, Shankaran V, Uppaluri R et al. 2005. A critical function for type I interferons in cancer immunoediting. Nat. Immunol. 6:722–29
     [Google Scholar]
  37. DuPage M, Cheung AF, Mazumdar C, Winslow MM, Bronson R et al. 2011. Endogenous T cell responses to antigens expressed in lung adenocarcinomas delay malignant tumor progression. Cancer Cell 19:72–85
     [Google Scholar]
  38. DuPage M, Jacks T. 2013. Genetically engineered mouse models of cancer reveal new insights about the antitumor immune response. Curr. Opin. Immunol. 25:192–99
     [Google Scholar]
  39. DuPage M, Mazumdar C, Schmidt LM, Cheung AF, Jacks T. 2012. Expression of tumour-specific antigens underlies cancer immunoediting. Nature 482:405–9
     [Google Scholar]
  40. El Sissy C, Kirilovsky A, van den Eynde M, Musina AM, Anitei MG et al. 2020. A diagnostic biopsy-adapted immunoscore predicts response to neoadjuvant treatment and selects patients with rectal cancer eligible for a watch-and-wait strategy. Clin. Cancer Res. 26:5198–207
     [Google Scholar]
  41. Engel AM, Svane IM, Rygaard J, Werdelin O 1997. MCA sarcomas induced in scid mice are more immunogenic than MCA sarcomas induced in congenic, immunocompetent mice. Scand. J. Immunol. 45:4463–70
     [Google Scholar]
  42. Engelhard VH, Rodriguez AB, Mauldin IS, Woods AN, Peske JD, Slingluff CL. 2018. Immune cell infiltration and tertiary lymphoid structures as determinants of antitumor immunity. J. Immunol. 200:432–42
     [Google Scholar]
  43. Fitzgerald B, Connolly KA, Cui C, Fagerberg E, Mariuzza DL et al. 2021. A mouse model for the study of anti-tumor T cell responses in Kras-driven lung adenocarcinoma. Cell Rep. Methods 1:5100080
     [Google Scholar]
  44. Foley EJ. 1953. Antigenic properties of methylcholanthrene-induced tumors in mice of the strain of origin. Cancer Res. 13:12835–37
     [Google Scholar]
  45. Forero A, Giacobbi NS, McCormick KD, Gjoerup OV, Bakkenist CJ et al. 2014. Simian virus 40 large T antigen induces IFN-stimulated genes through ATR kinase. J. Immunol. 192:5933–42
     [Google Scholar]
  46. Frese KK, Tuveson DA. 2007. Maximizing mouse cancer models. Nat. Rev. Cancer 7:645–58
     [Google Scholar]
  47. Fu C, Jiang A. 2018. Dendritic cells and CD8 T cell immunity in tumor microenvironment. Front. Immunol. 9:3059
     [Google Scholar]
  48. Gallily R, Woolley GW. 1958. The human tumor in the mouse. Ann. N.Y. Acad. Sci. 76:791–96
     [Google Scholar]
  49. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B et al. 2006. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313:57951960–64
     [Google Scholar]
  50. Gardiner RE, Jahangeer S, Forde P, Ariffin AB, Bird B et al. 2015. Low immunogenicity in non-small cell lung cancer; do new developments and novel treatments have a role?. Cancer Metastasis Rev. 34:129–44
     [Google Scholar]
  51. Germano G, Lamba S, Rospo G, Barault L, Magri A et al. 2017. Inactivation of DNA repair triggers neoantigen generation and impairs tumour growth. Nature 552:116–20
     [Google Scholar]
  52. Goel S, DeChristo MJ, Watt AC, Brinjones H, Sceneay J et al. 2017. CDK4/6 inhibition triggers anti-tumour immunity. Nature 548:471–75
     [Google Scholar]
  53. Goff SP, Berg P. 1976. Construction of hybrid viruses containing SV40 and a phage DNA segments and their propagation in cultured monkey cells. Cell 9:4 Pt. 2695–705
     [Google Scholar]
  54. Goldé A. 1970. Radio-induced mutants of the Schmidt-Ruppin strain of rous sarcoma virus. Virology 40:1022–29
     [Google Scholar]
  55. Gorer PA. 1936. The detection of antigenic differences in mouse erythrocytes by the employment of immune sera. Br. J. Exp. Pathol. 17:42–50
     [Google Scholar]
  56. Gross L. 1943. Intradermal immunization of C3H mice against a sarcoma that originated in an animal of the same line. Cancer Res. 3:326
     [Google Scholar]
  57. Guerin MV, Finisguerra V, van den Eynde BJ, Bercovici N, Trautmann A 2020. Preclinical murine tumor models: a structural and functional perspective. eLife 9:e50740
     [Google Scholar]
  58. Guil-Luna S, Sedlik C, Piaggio E 2021. Humanized mouse models to evaluate cancer immunotherapeutics. Annu. Rev. Cancer Biol. 5:119–36
     [Google Scholar]
  59. Hanahan D. 1985. Heritable formation of pancreatic β-cell tumours in transgenic mice expressing recombinant insulin/simian virus 40 oncogenes. Nature 315:115–22
     [Google Scholar]
  60. Hanahan D, Wagner EF, Palmiter RD. 2007. The origins of oncomice: a history of the first transgenic mice genetically engineered to develop cancer. Genes Dev. 21:2258–70
     [Google Scholar]
  61. Hasui M, Saikawa Y, Miura M, Takano N, Ueno Y et al. 1989. Effector and precursor phenotypes of lymphokine-activated killer cells in mice with severe combined immunodeficiency (Scid) and athymic (nude) mice. Cell. Immunol. 120:1230–39
     [Google Scholar]
  62. Hegde S, Krisnawan VE, Herzog BH, Zuo C, Breden MA et al. 2020. Dendritic cell paucity leads to dysfunctional immune surveillance in pancreatic cancer. Cancer Cell 37:289–307.e9
     [Google Scholar]
  63. Heyer J, Kwong LN, Lowe SW, Chin L. 2010. Non-germline genetically engineered mouse models for translational cancer research. Nat. Rev. Cancer 10:470–80
     [Google Scholar]
  64. Hui R, Garon EB, Goldman JW, Leighl NB, Hellmann MD et al. 2017. Pembrolizumab as first-line therapy for patients with PD-L1-positive advanced non-small cell lung cancer: a phase 1 trial. Ann. Oncol. 28:874–81
     [Google Scholar]
  65. Huijbers IJ, Del Bravo J, Bin Ali R, Pritchard C, Braumuller TM et al. 2015. Using the GEMM-ESC strategy to study gene function in mouse models. Nat. Protoc. 10:1755–85
     [Google Scholar]
  66. Huijbers IJ, Krimpenfort P, Berns A, Jonkers J. 2011. Rapid validation of cancer genes in chimeras derived from established genetically engineered mouse models. Bioessays 33:701–10
     [Google Scholar]
  67. Huijbers IJ, Soudja SM, Uyttenhove C, Buferne M, Inderberg-Suso EM et al. 2012. Minimal tolerance to a tumor antigen encoded by a cancer-germline gene. J. Immunol. 188:111–21
     [Google Scholar]
  68. Jaenisch R, Mintz B. 1974. Simian Virus 40 DNA sequences in DNA of healthy adult mice derived from preimplantation blastocysts injected with viral DNA. PNAS 71:1250–54
     [Google Scholar]
  69. Javier RT, Butel JS 2008. The history of tumor virology. Cancer Res. 68:7693–706
     [Google Scholar]
  70. Jonkers J, Berns A. 2002. Conditional mouse models of sporadic cancer. Nat. Rev. Cancer 2:251–65
     [Google Scholar]
  71. Joshi NS, Akama-Garren EH, Lu Y, Lee DY, Chang GP et al. 2015. Regulatory T cells in tumor-associated tertiary lymphoid structures suppress anti-tumor T cell responses. Immunity 43:579–90
     [Google Scholar]
  72. Kennaway EL, Hieger I. 1930. Carcinogenic substances and their fluorescence spectra. Br. Med. J. 1:36221044
     [Google Scholar]
  73. Kersten K, de Visser KE, van Miltenburg MH, Jonkers J. 2017. Genetically engineered mouse models in oncology research and cancer medicine. EMBO Mol. Med. 9:137–53
     [Google Scholar]
  74. Koebel CM, Vermi W, Swann JB, Zerafa N, Rodig SJ et al. 2007. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450:903–7
     [Google Scholar]
  75. Lathrop AEC, Loeb L. 1915a. Further investigations on the origin of tumors in mice: I. Tumor incidence and tumor age in various strains of mice. J. Exp. Med. 22:646–73
     [Google Scholar]
  76. Lathrop AEC, Loeb L. 1915b. Further investigations on the origin of tumors in mice: II. Tumor incidence and tumor age in hybrids. J. Exp. Med. 22:713–31
     [Google Scholar]
  77. Lathrop AEC, Loeb L. 1918. Further investigations on the origin of tumors in mice: V. The tumor rate in hybrid strains. J. Exp. Med. 28:475–500
     [Google Scholar]
  78. Lau J, Cheung J, Navarro A, Lianoglou S, Haley B et al. 2017. Tumour and host cell PD-L1 is required to mediate suppression of anti-tumour immunity in mice. Nat. Commun. 8:14572
     [Google Scholar]
  79. Leach DR, Krummel MF, Allison JP. 1996. Enhancement of antitumor immunity by CTLA-4 blockade. Science 271:1734–36
     [Google Scholar]
  80. Lee JW, Komar CA, Bengsch F, Graham K, Beatty GL 2016. Genetically engineered mouse models of pancreatic cancer: the KPC Model (LSL-KrasG12D/+;LSL-Trp53R172H/+;Pdx-1-Cre), its variants, and their application in immuno-oncology drug discovery. Curr. Protoc. Pharmacol. 73:14.39.1–14.39.20
     [Google Scholar]
  81. Lee PP, Yee C, Savage PA, Fong L, Brockstedt DG et al. 1999. Characterization of circulating T cells specific for tumor- associated antigens in melanoma patients. Nat. Med. 5:6677–85
     [Google Scholar]
  82. Levine AJ, Oren M. 2009. The first 30 years of p53: growing ever more complex. Nat. Rev. Cancer 9:749–58
     [Google Scholar]
  83. Li J, Lee Y, Li Y, Jiang Y, Lu H et al. 2018. Co-inhibitory molecule B7 superfamily member 1 expressed by tumor-infiltrating myeloid cells induces dysfunction of anti-tumor CD8+ T cells. Immunity 48:773–86.e5
     [Google Scholar]
  84. Little CC. 1911. The “dilute” forms of yellow mice. Science 33:896–97
     [Google Scholar]
  85. Little CC. 1913.. “ Yellow” and “agouti” factors in mice. Science 38:205
     [Google Scholar]
  86. Little CC. 1914. A possible mendelian explanation for a type of inheritance apparently non-mendelian in nature. Science 40:904–6
     [Google Scholar]
  87. Little CC. 1927. Notes on a species cross in mice and on an hypothesis concerning the quantitative potentiality of genes. Science 66:542–43
     [Google Scholar]
  88. Little CC, Tyzzer EE. 1916. Further experimental studies on the inheritance of susceptibility to a transplantable tumor, carcinoma (J. w. A.) of the Japanese waltzing mouse. J. Med. Res. 33:393–453
     [Google Scholar]
  89. Liu J, Blake SJ, Smyth MJ, Teng MW. 2014. Improved mouse models to assess tumour immunity and irAEs after combination cancer immunotherapies. Clin. Transl. Immunol. 3:e22
     [Google Scholar]
  90. Livshits G, Lowe SW. 2013. Accelerating cancer modeling with RNAi and nongermline genetically engineered mouse models. Cold Spring Harb. Protoc. 2013: https://doi.org/10.1101/pdb.top069856
    [Crossref] [Google Scholar]
  91. Loeb L. 1901. On transplantation of tumors. J. Med. Res. 6:28–38
     [Google Scholar]
  92. Ma L, Dichwalkar T, Chang JYH, Cossette B, Garafola D et al. 2019. Enhanced CAR–T cell activity against solid tumors by vaccine boosting through the chimeric receptor. Science 365:162–68
     [Google Scholar]
  93. Manguso RT, Pope HW, Zimmer MD, Brown FD, Yates KB et al. 2017. In vivo CRISPR screening identifies Ptpn2 as a cancer immunotherapy target. Nature 547:413–18
     [Google Scholar]
  94. McCreery MQ, Balmain A. 2017. Chemical carcinogenesis models of cancer: back to the future. Annu. Rev. Cancer Biol. 1:295–310
     [Google Scholar]
  95. McFadden DG, Politi K, Bhutkar A, Chen FK, Song X et al. 2016. Mutational landscape of EGFR-, MYC-, and Kras-driven genetically engineered mouse models of lung adenocarcinoma. PNAS 113:E6409–17
     [Google Scholar]
  96. Meraz IM, Majidi M, Meng F, Shao R, Ha MJ et al. 2019. An improved patient-derived xenograft humanized mouse model for evaluation of lung cancer immune responses. Cancer Immunol. Res. 7:1267–79
     [Google Scholar]
  97. Mian SA, Anjos-Afonso F, Bonnet D. 2020. Advances in human immune system mouse models for studying human hematopoiesis and cancer immunotherapy. Front. Immunol. 11:619236
     [Google Scholar]
  98. Moser AR, Luongo C, Gould KA, McNeley MK, Shoemaker AR, Dove WF. 1995. ApcMin: a mouse model for intestinal and mammary tumorigenesis. Eur. J. Cancer 31:1061–64
     [Google Scholar]
  99. Mulligan RC, Berg P. 1980. Expression of a bacterial gene in mammalian cells. Science 209:44631422–27
     [Google Scholar]
  100. Mulligan RC, Howard BH, Berg P. 1979. Synthesis of rabbit β-globin in cultured monkey kidney cells following infection with a SV40 13-globin recombinant genome. Nature 277:108–14
     [Google Scholar]
  101. Munoz-Erazo L, Rhodes JL, Marion VC, Kemp RA 2020. Tertiary lymphoid structures in cancer-considerations for patient prognosis. Cell Mol. Immunol. 17:570–75
     [Google Scholar]
  102. Murray WS, Little CC. 1935. Further data on the existence of extra-chromosomal influence on the incidence of mammary tumors in mice. Science 82:2123228–30
     [Google Scholar]
  103. Old LJ. 1981. Cancer immunology: the search for specificity—G. H. A. Clowes Memorial Lecture. Cancer Res. 41:2361–75
     [Google Scholar]
  104. Olson B, Li Y, Lin Y, Liu ET, Patnaik A. 2018. Mouse models for cancer immunotherapy research. Cancer Discov. 8:111358–65
     [Google Scholar]
  105. Ono M, Yasunaga T, Miyata T, Ushikubo H 1986. Nucleotide sequence of human endogenous retrovirus genome related to the mouse mammary tumor virus genome. J. Virol. 60:2589–98
     [Google Scholar]
  106. Outzen HC. 1975. Spontaneous and induced tumor incidence in germfree “nude” mice. J. Reticuloendothel. Soc. 17:11–9
     [Google Scholar]
  107. Palm JE, Teller MN, Merker PC, Woolley GW. 1958. HOST conditioning in experimental chemotherapy. Ann. N.Y. Acad. Sci. 76:812–20
     [Google Scholar]
  108. Pan D, Kobayashi A, Jiang P, de Andrade LF, Tay RE et al. 2018. A major chromatin regulator determines resistance of tumor cells to T cell–mediated killing. Science 359:6377770–75
     [Google Scholar]
  109. Parish CR. 2003. Cancer immunotherapy: the past, the present and the future. Immunol. Cell Biol. 81:106–13
     [Google Scholar]
  110. Perez-Ruiz E, Minute L, Otano I, Alvarez M, Ochoa MC et al. 2019. Prophylactic TNF blockade uncouples efficacy and toxicity in dual CTLA-4 and PD-1 immunotherapy. Nature 569:428–32
     [Google Scholar]
  111. Politi K, Pao W. 2011. How genetically engineered mouse tumor models provide insights into human cancers. J. Clin. Oncol. 29:2273–81
     [Google Scholar]
  112. Postow MA, Sidlow R, Hellmann MD. 2018. Immune-related adverse events associated with immune checkpoint blockade. N. Engl. J. Med. 378:158–68
     [Google Scholar]
  113. Prehn RT, Main JM. 1957. Immunity to methylcholanthrene-induced sarcomas. J. Natl. Cancer Inst. 18:6769–78
     [Google Scholar]
  114. Radkevich-Brown O, Piechocki MP, Back JB, Weise AM, Pilon-Thomas S, Wei WZ. 2010. Intratumoral DNA electroporation induces anti-tumor immunity and tumor regression. Cancer Immunol. Immunother. 59:409–17
     [Google Scholar]
  115. Raez LE, Fein S, Podack ER. 2005. Lung cancer immunotherapy. Clin. Med. Res. 3:221–28
     [Google Scholar]
  116. Ribatti D. 2016. The concept of immune surveillance against tumors: the first theories. Oncotarget 8:47175–80
     [Google Scholar]
  117. Rosenberg SA, Spiess P, Lafreniere R. 1986. A new approach to the adoptive immunotherapy of cancer with tumor-infiltrating lymphocytes. Science 233:47701318–21
     [Google Scholar]
  118. Roth TL, Li PJ, Blaeschke F, Nies JF, Apathy R et al. 2020. Pooled knockin targeting for genome engineering of cellular immunotherapies. Cell 181:728–44.e21
     [Google Scholar]
  119. Runge A, Hu J, Wieland M, Bergeest JP, Mogler C et al. 2014. An inducible hepatocellular carcinoma model for preclinical evaluation of antiangiogenic therapy in adult mice. Cancer Res. 74:4157–69
     [Google Scholar]
  120. Schachtschneider KM, Schwind RM, Newson J, Kinachtchouk N, Rizko M et al. 2017. The oncopig cancer model: an innovative large animal translational oncology platform. Front. Oncol. 7:190
     [Google Scholar]
  121. Schietinger A, Philip M, Krisnawan VE, Chiu EY, Delrow JJ et al. 2016. Tumor-specific T cell dysfunction is a dynamic antigen-driven differentiation program initiated early during tumorigenesis. Immunity 45:389–401
     [Google Scholar]
  122. Schonhuber N, Seidler B, Schuck K, Veltkamp C, Schachtler C et al. 2014. A next-generation dual-recombinase system for time- and host-specific targeting of pancreatic cancer. Nat. Med. 20:1340–47
     [Google Scholar]
  123. Schreiber TH, Podack ER. 2009. A critical analysis of the tumour immunosurveillance controversy for 3-MCA-induced sarcomas. Br. J. Cancer 101:381–86
     [Google Scholar]
  124. Schreiber TH, Raez L, Rosenblatt JD, Podack ER. 2010. Tumor immunogenicity and responsiveness to cancer vaccine therapy: the state of the art. Semin. Immunol. 22:105–12
     [Google Scholar]
  125. Scott OCA. 1991. Tumor transplantation and tumor immunity: a personal view. Cancer Res. 51:757–63
     [Google Scholar]
  126. Sen T, Rodriguez BL, Chen L, Corte CMD, Morikawa N et al. 2019. Targeting DNA damage response promotes antitumor immunity through STING-mediated T-cell activation in small cell lung cancer. Cancer Discov. 9:646–61
     [Google Scholar]
  127. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE et al. 2001. IFNγ and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410:68321107–11
     [Google Scholar]
  128. Shibata H, Toyama K, Shioya H, Ito M, Hirota M et al. 1997. Rapid colorectal adenoma formation initiated by conditional targeting of the Apc gene. Science 278:5335120–23
     [Google Scholar]
  129. Shinkai Y, Rathbun G, Lam K, Oltz EM, Stewart V et al. 1992. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68:5855–67
     [Google Scholar]
  130. Shu S, Wu H-J, Ge JY, Zeid R, Harris IS et al. 2020. Synthetic lethal and resistance interactions with BET bromodomain inhibitors in triple-negative breast cancer. Mol. Cell 78:1096–113.e8
     [Google Scholar]
  131. Shultz LD, Brehm MA, Garcia-Martinez JV, Greiner DL. 2012. Humanized mice for immune system investigation: progress, promise and challenges. Nat. Rev. Immunol. 12:786–98
     [Google Scholar]
  132. Smyth MJ, Godfrey DI, Trapani JA 2001. A fresh look at tumor immunosurveillance and immunotherapy. Nat. Immunol. 2:293–99
     [Google Scholar]
  133. Snell GD. 1948. Methods for the study of histocompatibility genes. J. Genet. 49:287–108
     [Google Scholar]
  134. Steensma DP, Kyle RA, Shampo MA 2010. Abbie Lathrop, the “mouse woman of Granby”: rodent fancier and accidental genetics pioneer. Mayo Clin. Proc. 85:e83
     [Google Scholar]
  135. Strong LC. 1935. The establishment of the C3H inbred strain of mice for the study of spontaneous carcinoma of the mammary gland. Genetics 20:6586–91
     [Google Scholar]
  136. Stutman O. 1974. Tumor development after 3-methylcholanthrene in immunologically deficient athymic-nude mice. Science 183:4124534–36
     [Google Scholar]
  137. Stutman O. 1979. Spontaneous tumors in nude mice: effect of the viable yellow gene. Exp. Cell Biol. 47:129–35
     [Google Scholar]
  138. Swann JB, Smyth MJ. 2007. Immune surveillance of tumors. J. Clin. Investig. 117:1137–46
     [Google Scholar]
  139. Tivol EA, Borriello F, Schweitzer AN, Lynch WP, Bluestone JA, Sharpe AH. 1995. Loss of CTLA-4 leads to massive lymphproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 3:541–47
     [Google Scholar]
  140. Toolan HW. 1951. Successful subcutaneous growth and transplantation of human tumors in X-irradiated laboratory animals. Proc. Soc. Exp. Biol. Med. 77:572–78
     [Google Scholar]
  141. Toolan HW. 1958. The transplantable human tumor. Ann. N.Y. Acad. Sci. 76:733–41
     [Google Scholar]
  142. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC et al. 2012. Safety, activity, and immune correlates of anti–PD-1 antibody in cancer. N. Engl. J. Med. 366:2443–54
     [Google Scholar]
  143. Torfadottir H, Freysdottir J, Skaftadottir I, Haraldsson A, Sigfusson G, Ogmundsdottir HM. 2006. Evidence for extrathymic T cell maturation after thymectomy in infancy. Clin. Exp. Immunol. 145:407–12
     [Google Scholar]
  144. Townsend SE, Allison JP. 1993. Tumor rejection after direct costimulation of CD8+ T cells by B7-transfected melanoma cells. Science 259:5093368–70
     [Google Scholar]
  145. Toyoshima K, Friis RR, Vogt PK. 1970. The reproductive and cell-transforming capacities of avian sarcoma virus B77: inactivation with UV light. Virology 42:163–70
     [Google Scholar]
  146. Tyzzer EE. 1909. A study of inheritance in mice with reference to their susceptibility to transplantable tumors. J. Med. Res. 21:519–73
     [Google Scholar]
  147. van der Leun AM, Thommen DS, Schumacher TN. 2020. CD8+ T cell states in human cancer: insights from single-cell analysis. Nat. Rev. Cancer 20:218–32
     [Google Scholar]
  148. van Dyke T, Jacks T. 2002. Cancer modeling in the modern era: progress and challenges. Cell 108:2135–44
     [Google Scholar]
  149. Vareki SM. 2018. High and low mutational burden tumors versus immunologically hot and cold tumors and response to immune checkpoint inhibitors. J. Immunother. Cancer 6:157
     [Google Scholar]
  150. Verma B, Wesa A. 2020. Establishment of humanized mice from peripheral blood mononuclear cells or cord blood CD34+ hematopoietic stem cells for immune-oncology studies evaluating new therapeutic agents. Curr. Protoc. Pharmacol. 89:1e77
     [Google Scholar]
  151. Visscher MB, Green RG, Bittner JJ. 1942. Characterization of milk influence in spontaneous mammary carcinoma. Proc. Soc. Exp. Biol. Med. 49:194–96
     [Google Scholar]
  152. Vooijis M, Jonkers J, Berns A. 2001. A highly efficient ligand-regulated Cre recombinase mouse line shows that LoxP recombination is position dependent. EMBO Rep. 2:4292–97
     [Google Scholar]
  153. Walrath JC, Hawes JJ, van Dyke T, Reilly KM. 2010. Genetically engineered mouse models in cancer research. Adv. Cancer Res. 106:113–64
     [Google Scholar]
  154. Wang J, Perry CJ, Meeth K, Thakral D, Damsky W et al. 2017. UV-induced somatic mutations elicit a functional T cell response in the YUMMER1.7 mouse melanoma model. Pigment Cell Melanoma Res. 30:428–35
     [Google Scholar]
  155. Weiss RA. 2020. A perspective on the early days of RAS research. Cancer Metastasis Rev. 39:1023–28
     [Google Scholar]
  156. Weiss RA, Vogt PK. 2011. 100 years of Rous sarcoma virus. J. Exp. Med. 208:2351–55
     [Google Scholar]
  157. White SB, Chen J, Gordon AC, Harris KR, Nicolai JR et al. 2015. Percutaneous ultrasound guided implantation of VX2 for creation of a rabbit hepatic tumor model. PLOS ONE 10:e0123888
     [Google Scholar]
  158. Wölfel T, Hauer M, Schneider J, Serrano M, Wölfel C et al. 1995. A p16INK4a-insensitive CDK4 mutant targeted by cytolytic T lymphocytes in a human melanoma. Science 269:52281281–84
     [Google Scholar]
  159. Wynder EL, Graham EA, Croninger AB 1953. Experimental production of carcinoma with cigarette tar. Cancer Res. 13:12855–64
     [Google Scholar]
  160. Xia X, Zhang Y, Zieth CR, Zhang S. 2007. Transgenes delivered by lentiviral vector are suppressed in human embryonic stem cells in a promoter-dependent manner. Stem Cells Dev. 16:1167–76
     [Google Scholar]
  161. Yamagiwa K, Ichikawa K. 1918. Experimental study of the pathogenesis of carcinoma. J. Cancer Res. 27:3174–81
     [Google Scholar]
  162. Yang H, Wang H, Shivalila CS, Cheng AW, Shi L, Jaenisch R. 2013. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154:1370–79
     [Google Scholar]
  163. Yao LC, Aryee KE, Cheng M, Kaur P, Keck JG, Brehm MA. 2019. Creation of PDX-bearing humanized mice to study immuno-oncology. Methods Mol. Biol. 1953:241–52
     [Google Scholar]
  164. Zhang Y, Zhang Z. 2020. The history and advances in cancer immunotherapy: understanding the characteristics of tumor-infiltrating immune cells and their therapeutic implications. Cell Mol. Immunol. 17:807–21
     [Google Scholar]
  165. Zhong W, Myers JS, Wang F, Wang K, Lucas J et al. 2020. Comparison of the molecular and cellular phenotypes of common mouse syngeneic models with human tumors. BMC Genom. 21:2
     [Google Scholar]
/content/journals/10.1146/annurev-cancerbio-070620-105523
Loading
Novel Mouse Models for Cancer Immunology
Annual Review of Cancer Biology 6, 269 (2022); https://doi.org/10.1146/annurev-cancerbio-070620-105523
/content/journals/10.1146/annurev-cancerbio-070620-105523
/content/journals/10.1146/annurev-cancerbio-070620-105523
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error