Defining the optimal murine models to investigate immune checkpoint blockers and their combination with other immunotherapies

Annals of Oncology

Volumn 27, Issue 7, 2016, Pages 1190-1198

  Sanmamed, M F ^a   Chester, C ^b   Melero, I ^c   Kohrt, H ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NAVARRA   (Spain)

Author keywords

Checkpoint blocker; Humanized mice; Immunotherapy; Murine model; Tumor microenvironment

Indexed keywords

CANCER IMMUNOTHERAPY; CANCER RESEARCH; DISEASE MODEL; DRUG RESEARCH; GENETIC ENGINEERING; IMMUNOAVATAR MODEL; KNOCKOUT MOUSE; MOUSE MODEL; MURINE MODEL; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; HUMAN; IMMUNOLOGY; IMMUNOTHERAPY; MOUSE; NEOPLASM; TUMOR MICROENVIRONMENT;

CELL CYCLE PROTEIN; MONOCLONAL ANTIBODY;

ANIMALS; ANTIBODIES, MONOCLONAL; CELL CYCLE PROTEINS; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOTHERAPY; MICE; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84977110484     PISSN: 09237534     EISSN: 15698041     Source Type: Journal    
DOI: 10.1093/annonc/mdw041     Document Type: Review

References (71)

1. Arrowsmith J, Miller P. Trial watch: phase II and phase III attrition rates 2011-2012. Nat Rev Drug Discov 2013; 12(8): 569.
2. Arrowsmith J. Trial watch: phase II failures: 2008-2010. Nat Rev Drug Discov 2011; 10(5): 328-329.
3. Adams CP, Brantner VV. Estimating the cost of new drug development: is it really 802 million dollars? Health Aff 2006; 25(2): 420-428.
4. Gillet J-P, Calcagno AM, Varma S et al. Redefining the relevance of established cancer cell lines to the study of mechanisms of clinical anti-cancer drug resistance. Proc Natl Acad Sci USA 2011; 108(46): 18708-18713.
5. Kang Y. Analysis of cancer stem cell metastasis in xenograft animal models. Methods Mol Biol 2009; 568: 7-19.
6. Goldin A, Venditti JM, Kline I, Mantel N. Evaluation of antileukemic agents employing advanced leukemia L1210 in mice. Cancer Res 1959; 19: 429-466.
7. Suggitt M, Bibby MC. 50 years of preclinical anticancer drug screening: empirical to target-driven approaches. Clin Cancer Res 2005; 11(3): 971-981.
8. Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science 1996; 271(5256): 1734-1736.
9. Dong H, Strome SE, Salomao DR et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 2002; 8(8): 793-800.
10. Sanmamed MF, Chen L. Inducible expression of B7-H1 (PD-L1) and its selective role in tumor site immune modulation. Cancer J 2014; 20(4): 256-261.
11. Rangarajan A, Weinberg RA. Opinion: comparative biology of mouse versus human cells: modelling human cancer in mice. Nat Rev Cancer 2003; 3(12): 952-959.
12. Sharpless NE, DePinho RA. The mighty mouse: genetically engineered mouse models in cancer drug development. Nat Rev Drug Discov 2006; 5(9): 741-754.
13. Van Dyke T, Jacks T. Cancer modeling in the modern era: progress and challenges. Cell 2002; 108(2): 135-144.
14. Schönig K, Bujard H, Gossen M. The power of reversibility regulating gene activities via tetracycline-controlled transcription. Methods Enzymol 2010; 477: 429-453.
15. DuPage M, Dooley AL, Jacks T. Conditional mouse lung cancer models using adenoviral or lentiviral delivery of Cre recombinase. Nat Protoc 2009; 4(7): 1064-1072.
16. Sauer B, Henderson N. Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1. Proc Natl Acad Sci USA 1988; 85(14): 5166-5170.
17. Dow LE, Fisher J, O'Rourke KP et al. Inducible in vivo genome editing with CRISPR-Cas9. Nat Biotechnol 2015; 33(4): 390-394.
18. Chen S, Sanjana NE, Zheng K et al. Genome-wide CRISPR screen in a mouse model of tumor growth and metastasis. Cell 2015; 160(6): 1246-1260.
19. DuPage M, Mazumdar C, Schmidt LM et al. Expression of tumour-specific antigens underlies cancer immunoediting. Nature 2012; 482(7385): 405-409.
20. Lin JH. Applications and limitations of genetically modified mouse models in drug discovery and development. Curr Drug Metab 2008; 9(5): 419-438.
21. Jinek M, Chylinski K, Fonfara I et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 2012; 337(6096): 816-821.
22. Bulliard Y, Jolicoeur R, Windman M et al. Activating Fc γ receptors contribute to the antitumor activities of immunoregulatory receptor-targeting antibodies. J Exp Med 2013; 210(9): 1685-1693.
23. Dahan R, Sega E, Selby M et al. FcgRs modulate the anti-tumor activity of antibodies targeting the PD-1/PD-L1 axis article FcgRs modulate the antitumor activity of antibodies targeting the PD-1/PD-L1 axis. Cell 2015; 28(3): 285-295.
24. Bournazos S, DiLillo DJ, Ravetch JV. Humanized mice to study FcγR function. Curr Top Microbiol Immunol 2014; 382: 237-248.
25. Lute KD, May KF, Lu P et al. Human CTLA4 knock-in mice unravel the quantitative link between tumor immunity and autoimmunity induced by anti-CTLA-4 antibodies. Blood 2005; 106(9): 3127-3133.
26. Kelland LR. 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.
27. Mak IW, Evaniew N, Ghert M. Lost in translation: animal models and clinical trials in cancer treatment. Am J Transl Res 2014; 6(2): 114-118.
28. Galluzzi L, Buqué A, Kepp O et al. Immunological effects of conventional chemotherapy and targeted anticancer agents. Cancer Cell 2015; 28(6): 690-714.
29. Hidalgo M, Amant F, Biankin AV et al. Patient-derived xenograft models: an emerging platform for translational cancer research. Cancer Discov 2014; 4(9): 998-1013.
30. Tentler JJ, Tan AC, Weekes CD et al. Patient-derived tumour xenografts as models for oncology drug development. Nat Rev Clin Oncol 2012; 9(6): 338-350.
31. 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. Cancer Res 2013; 73(15): 4885-4897.
32. Talmadge JE, Singh RK, Fidler IJ, Raz A. Murine models to evaluate novel and conventional therapeutic strategies for cancer. Am J Pathol 2007; 170(3): 793-804.
33. Williams SA, Anderson WC, Santaguida MT, Dylla SJ. Patient-derived xenografts, the cancer stem cell paradigm, and cancer pathobiology in the 21st century. Lab Investig 2013; 93(9): 970-982.
34. Gao H, Korn JM, Ferretti S et al. High-throughput screening using patient-derived tumor xenografts to predict clinical trial drug response. Nat Med 2015. doi:10.1038/nm.3954.
35. Rongvaux A, Takizawa H, Strowig T et al. Human hemato-lymphoid system mice: current use and future potential for medicine. Annu Rev Immunol 2013; 31: 635-674.
36. Bosma GC, Custer RP, Bosma MJ. A severe combined immunodeficiency mutation in the mouse. Nature 1983; 301(5900): 527-530.
37. Lapidot T, Pflumio F, Doedens M et al. Cytokine stimulation of multilineage hematopoiesis from immature human cells engrafted in SCID mice. Science 1992; 255(5048): 1137-1141.
38. Mosier DE, Gulizia RJ, Baird SM, Wilson DB. Transfer of a functional human immune system to mice with severe combined immunodeficiency. Nature 1988; 335(6187): 256-259.
39. McCune JM, Namikawa R, Kaneshima H et al. The SCID-hu mouse: murine model for the analysis of human hematolymphoid differentiation and function. Science 1988; 241(4873): 1632-1639.
40. Makino S, Kunimoto K, Muraoka Y et al. Breeding of a non-obese, diabetic strain of mice. Jikken Dobutsu 1980; 29: 1-13.
41. Shultz LD, Schweitzer PA, Christianson SW et al. Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J Immunol 1995; 154(1): 180-191.
42. Shinkai Y, Rathbun G, Lam KP et al. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 1992; 68(5): 855-867.
43. Mombaerts P, Iacomini J, Johnson RS et al. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 1992; 68(5): 869-877.
44. Goldman JP, Blundell MP, Lopes L et al. Enhanced human cell engraftment in mice deficient in RAG2 and the common cytokine receptor gamma chain. Br J Haematol 1998; 103(2): 335-342.
45. Ito M, Hiramatsu H, Kobayashi K et al. NOD/SCID/gamma(c)(null) mouse: an excellent recipient mouse model for engraftment of human cells. Blood 2002; 100 (9): 3175-3182.
46. Fisher TS, Kamperschroer C, Oliphant T et al. Targeting of 4-1BB by monoclonal antibody PF-05082566 enhances T-cell function and promotes anti-tumor activity. Cancer Immunol Immunother 2012; 61(10): 1721-1733.
47. Sanmamed MF, Rodriguez I, Schalper KA et al. Nivolumab and urelumab enhance antitumor activity of human T lymphocytes engrafted in Rag2-/-IL2R null immunodeficient mice. Cancer Res 2015; 75(17): 3466-3478.
48. McCormack E, Adams KJ, Hassan NJ et al. Bi-specific TCR-anti CD3 redirected Tcell targeting of NY-ESO-1-and LAGE-1-positive tumors. Cancer Immunol Immunother 2013; 62(4): 773-785.
49. May KFM, Jr, Roychowdhury S, Bhatt D et al. Anti-human CTLA-4 monoclonal antibody promotes T-cell expansion and immunity in a hu-PBL-SCID model: a new method for preclinical screening of costimulatory monoclonal antibodies. Blood 2005; 105(3): 1114-1121.
50. King MA, Covassin L, Brehm MA et al. Human peripheral blood leucocyte non-obese diabetic-severe combined immunodeficiency interleukin-2 receptor gamma chain gene mouse model of xenogeneic graft-versus-host-like disease and the role of host major histocompatibility complex. Clin Exp Immunol 2009; 157(1): 104-118.
51. Nervi B, Rettig MP, Ritchey JK et al. Factors affecting human T cell engraftment, trafficking, and associated xenogeneic graft-vs-host disease in NOD/SCID beta2mnull mice. Exp Hematol 2007; 35(12): 1823-1838.
52. Matsumura T, Kametani Y, Ando K et al. Functional CD5+ B cells develop predominantly in the spleen of NOD/SCID/gammac(null) (NOG) mice transplanted either with human umbilical cord blood, bone marrow, or mobilized peripheral blood CD34+ cells. Exp Hematol 2003; 31(9): 789-797.
53. Chen Q, Khoury M, Chen J. Expression of human cytokines dramatically improves reconstitution of specific human-blood lineage cells in humanized mice. Proc Natl Acad Sci USA 2009; 106(51): 21783-21788.
54. Huntington ND, Legrand N, Alves NL et al. IL-15 trans-presentation promotes human NK cell development and differentiation in vivo. J Exp Med 2009; 206(1): 25-34.
55. Nicolini FE, Cashman JD, Hogge DE et al. NOD/SCID mice engineered to express human IL-3, GM-CSF and Steel factor constitutively mobilize engrafted human progenitors and compromise human stem cell regeneration. Leukemia 2003; 18 (2): 341-347.
56. 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): 364-372.
57. Tonomura N, Habiro K, Shimizu A et al. Antigen-specific human T-cell responses and T cell-dependent production of human antibodies in a humanized mouse model. Blood 2008; 111(8): 4293-4296.
58. Williams SS, Chen FA, Kida H et al. Engraftment of human tumor-infiltrating lymphocytes and the production of anti-tumor antibodies in SCID mice. J Immunol 1996; 156(5): 1908-1915.
59. Hess SD, Egilmez NK, Bailey N et al. Human CD4+ T cells present within the microenvironment of human lung tumors are mobilized by the local and sustained release of IL-12 to kill tumors in situ by indirect effects of IFN-gamma. J Immunol 2003; 170(1): 400-412.
60. Broderick L, Yokota SJ, Reineke J et al. Human CD4+ effector memory T cells persisting in the microenvironment of lung cancer xenografts are activated by local delivery of IL-12 to proliferate, produce IFN-gamma, and eradicate tumor cells. J Immunol 2005; 174(2): 898-906.
61. Simpson-Abelson MR, Sonnenberg GF, Takita H et al. Long-term engraftment and expansion of tumor-derived memory T cells following the implantation of nondisrupted pieces of human lung tumor into NOD-scid IL2Rgamma(null) mice. J Immunol 2008; 180(10): 7009-7018.
62. Yokota SJ, Facciponte JG, Kelleher RJ et al. Changes in ovarian tumor cell number, tumor vasculature, and T cell function monitored in vivo using a novel xenograft model. Cancer Immunol 2013; 13: 11.
63. Sznol M, Chen L. Antagonist antibodies to PD-1 and B7-H1 (PD-L1) in the treatment of advanced human cancer-response. Clin Cancer Res 2013; 19(19): 5542.
64. Wolchok JD, Kluger H, Callahan MK et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369(2): 122-133.
65. Melero I, Berman DM, Aznar MA et al. Evolving synergistic combinations of targeted immunotherapies to combat cancer. Nat Rev Cancer 2015; 15(8): 457-472.
66. Boggio K, Di Carlo E, Rovero S et al. Ability of systemic interleukin-12 to hamper progressive stages of mammary carcinogenesis in HER2/neu transgenic mice. Cancer Res 2000; 60(2): 359-364.
67. Morales-Kastresana A, Sanmamed MF, Rodriguez I et al. Combined immunostimulatory monoclonal antibodies extend survival in an aggressive transgenic hepatocellular carcinoma mouse model. Clin Cancer Res 2013; 19(22): 6151-6162.
68. Uno T, Takeda K, Kojima Y et al. Eradication of established tumors in mice by a combination antibody-based therapy. Nat Med 2006; 12(6): 693-698.
69. Lancaster MA, Knoblich JA. Organogenesis in a dish: modeling development and disease using organoid technologies. doi:10.1126/science.1247125.
70. Freeman aE, Hoffman RM. In vivo-like growth of human tumors in vitro. Proc Natl Acad Sci USA 1986; 83(8): 2694-2698.
71. Burel JG, Apte SH, Doolan DL. Systems approaches towards molecular profiling of human immunity. Trends Immunol 2016; 37(1): 53-67.