An evolutionary perspective on anti-tumor immunity

Frontiers in Oncology

Volumn 2 JAN, Issue , 2013, Pages

  Klinke II, David J ^a,b  

^a West Virginia University   (United States)

^b WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

Bayesian inference; Next generation sequencing; Proteomics; Simulation

Indexed keywords

BREAST CANCER; CARCINOGENESIS; CELL HETEROGENEITY; DNA DAMAGE; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; HOMEOSTASIS; HUMAN; MATHEMATICAL MODEL; MOLECULARLY TARGETED THERAPY; NONHUMAN; PREDICTION; PROTEOMICS; REVIEW; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; TUMOR REGRESSION;

EID: 84887022513     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2012.00202     Document Type: Review

References (114)

1. Amado, R. G., Wolf, M., Peeters, M., Van Cutsem, E., Siena, S., Freeman, D. J., et al. (2008). Wild-type KRAS is required for panitumumab efficacy in patients with metastatic colorectal cancer. J. Clin. Oncol. 26, 1626-1634.
2. Apetoh, L., Ghiringhelli, F., Tesniere, A., Obeid, M., Ortiz, C., Criollo, A., et al. (2007). Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med. 13, 1050-1059.
3. Bachman, J. A., and Sorger, P. (2011). New approaches to modeling complex biochemistry. Nat. Methods 8, 130-131.
4. Banerji, S., Cibulskis, K., Rangel-Escareno, C., Brown, K. K., Carter, S. L., Frederick, A. M., et al. (2012). Sequence analysis of mutations and translocations across breast cancer subtypes. Nature 486, 405-409.
5. Barr, S., Thomson, S., Buck, E., Russo, S., Petti, F., Sujka-Kwok, I., et al. (2008). Bypassing cellular egf receptor dependence through epithelial-to-mesenchymal-like transitions. Clin. Exp. Metastasis 25, 685-693.
6. Bergman, R. N., Ider, Y. Z., Bowden, C. R., and Cobelli, C. (1979). Quantitative estimation of insulin sensitivity. Am. J. Physiol. 236, E667-E677.
7. Bissell, M. J., and Hines, W. C. (2011). Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat. Med. 17, 320-329.
8. Boggio, K., Nicoletti, G., Di Carlo, E., Cavallo, F., Landuzzi, L., Melani, C., et al. (1998). Interleukin 12-mediated prevention of spontaneous mammary adenocarcinomas in two lines of Her-2/neu transgenic mice. J. Exp. Med. 188, 589-596.
9. Brown, K. S., Hill, C. C., Calero, G. A., Myers, C. R., Lee, K. H., Sethna, J. P., et al. (2004). The statistical mechanics of complex signaling networks: nerve growth factor signaling. Phys. Biol. 1, 184-195.
10. Brown, K. S. and Sethna, J. P. (2003). Statistical mechanical approaches to models with many poorly known parameters. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 68, 021904.
11. Calderhead, B., and Girolami, M. A. (2011). Statistical analysis of nonlinear dynamical systems using differential geometric sampling methods. Interface Focus 1, 821-835.
12. Campbell, D. I., Ferreira, C. R., Eberlin, L. S., and Cooks, R. G. (2012). Improved spatial resolution in the imaging of biological tissue using desorption electrospray ionization. Anal. Bioanal. Chem. 404, 389-398.
13. Ciampricotti, M., Hau, C. S., Doornebal, C. W., Jonkers, J., de Visser, K. E., et al. (2012). Chemotherapy response of spontaneous mammary tumors is independent of the adaptive immune system. Nat. Med. 18, 344-346.
14. Ciampricotti, M., Vrijland, K., Hau, C. S., Pemovska, T., Doornebal, C. W., Speksnijder, E. N., et al. (2011). Development of metastatic HER2(+) breast cancer is independent of the adaptive immune system. J. Pathol. 224, 56-66.
15. Curtis, C., Shah, S. P., Chin, S. F., Turashvili, G., Rueda, O. M., Dunning, M. J., et al. (2012). The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 486, 346-352.
16. Diaz, L. A., Williams, R. T., Wu, J., Kinde, I., Hecht, J. R., Berlin, J., et al. (2012). The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 486, 537-540.
17. Ding, L., Getz, G., Wheeler, D. A., Mardis, E. R., McLellan, M. D., Cibulskis, K., et al. (2008). Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455, 1069-1075.
18. Dunn, G. P., Bruce, A. T., Ikeda, H., Old, L. J., and Schreiber, R. D. (2002). Cancer immunoediting: from immunosurveillance to tumor escape. Nat. Immunol. 3, 991-998.
19. DuPage, M., Mazumdar, C., Schmidt, L. M., Cheung, A. F., and Jacks, T. (2012). Expression of tumour-specific antigens underlies cancer immunoediting. Nature 482, 405-409.
20. Ebos, J. M., Lee, C. R., Cruz-Munoz, W., Bjarnason, G. A.,.Christensen, J. G., and Kerbel, R. S. (2009). Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 15, 232-239.
21. Ellis, M. J., Ding, L., Shen, D., Luo, J., Suman, V. J., Wallis, J. W., et al. (2012). Whole-genome analysis informs breast cancer response to aromatase inhibition. Nature 486, 353-360.
22. Engelhardt, J., Boldajipour, J. B., Beemiller, P., Pandurangi, P., Sorensen, C., Werb, Z., et al. (2012). Marginating dendritic cells of the tumor microenvironment cross-present tumor antigens and stably engage tumor-specific T cells. Cancer Cell 21, 402-417.
23. Erguler, K., and Stumpf, M. P. (2011). Practical limits for reverse engineering of dynamical systems: a statistical analysis of sensitivity and parameter inferability in systems biology models. Mol. Biosyst. 7, 1593-1602.
24. Faeder, J. R., Blinov, M. L., and Hlavacek, W. S. (2009). Rule-based modeling of biochemical systems with bionetgen. Methods Mol. Biol. 500, 113-167.
25. Feret, J., Danos, V., Krivine, J., Harmer, R., and Fontana, W. (2009). Internal coarse-graining of molecular systems. Proc. Natl. Acad. Sci. U.S.A. 106, 6453-6458.
26. Fidler, I. J., and Kripke, M. L. (1977). Metastasis results from preexisting variant cells within a malignant tumor. Science 197, 893-895.
27. Fisher, R. (1935). The logic of inductive inference. J. Roy. Stat. Soc. 98, 39-82.
28. Friend, S., Bernards, H., R., Rogelj, S., Weinberg, R. A., Rapaport, J. M., Albert, D. M., et al. (1986). A human DNA segment with properties of the gene that predisposes to retinoblastoma and osteosarcoma. Nature 323, 643-646.
29. Gerlinger, M., Rowan, A. J., Horswell, S., Larkin, J., Endesfelder, D., Gronroos, E., et al. (2012). Intratumor heterogeneity and branchedevolution revealed by multiregion sequencing. N. Engl. J. Med. 366, 883-892.
30. Ghiringhelli, F., Apetoh, L., Tesniere, A., Aymeric, L., Ma, Y., Ortiz, C., et al. (2009). Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat. Med. 15, 1170-1178.
31. Gishizky, M. L., Johnson-White, J., and Witte, O. N., (1993). Efficient transplantation of BCR-ABL-induced chronic myelogenous leukemia-like syndrome in mice. Proc. Natl. Acad. Sci. U.S.A. 90, 3755-3759.
32. Greaves, M., and Maley, C. C. (2012). Clonal evolution in cancer. Nature 481, 306-313.
33. Green, W. H. (2007). Predictive kinetics: a new approach for the 21st century. Adv. Chem. Eng. 32, 1-50.
34. Greenman, C., Stephens, P., Smith, R., Dalgliesh, G. L., Hunter, C., Bignell, G., et al. (2007). Patterns of somatic mutation in human cancer genomes. Nature 446, 153-158.
35. Greenman, C. D., Pleasance, E. D., Newman, S., Yang, F., Fu, B., Nik-Zainal, S., et al. (2012). Estimation of rearrangement phylogeny for cancer genomes. Genome Res. 22, 346-361.
36. Gutenkunst, R. N., Waterfall, J. J., Casey, F. P., Brown, K. S., Myers, C. R., and Sethna, J. P. (2007). Universally sloppy parameter sensitivities in systems biology models. PLoS Comput. Biol. 3:e189. doi: 10.1371/journal.pcbi.0030189
37. Hanahan, D., and Weinberg, R. A. (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674.
38. Hemming, A. W., Davis, N. L., Kluftinger, A., Robinson, B., Quenville, N. F., Liseman, B., et al. (1992). Prognostic markers of colorectal cancer: an evaluation of DNA content, epidermal growth factor receptor, and Ki-67. J. Surg. Oncol. 51, 147-152.
39. Herrmann, F., Lehr, H. A., Drexler, I., Sutter, G., Hengstler, J.,Wollscheid, U., et al. (2004). HER-2/neu-mediated regulation of components of the MHC class I antigen-processing pathway. Cancer Res. 64, 215-220.
40. Herschkowitz, J. I., Simin, K., Weigman, V. J., Mikaelian, I., Usary, J., Hu, Z., et al. (2007). Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol. 8, R76.
41. Higgins, D. F., Kimura, K., Bernhardt, W. M., Shrimanker, N., Akai, Y., Hohenstein, B., et al. (2007). Hypoxia promotes fibrogenesis in vivo via hif-1 stimulation of epithelial-to-mesenchymal transition. J. Clin. Invest. 117, 3810-3820.
42. Hodi, F. S., O'Day, S. J., McDermott, D. F., Weber, R. W., Sosman, J. A., Haanen, J. B., et al. (2010). Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363, 711-723.
43. Hollstein, M., Sidransky, D., Vogelstein, B., and Harris, C. C. (1991). p53 mutations in human cancers. Science 253, 49-53.
44. Hou, Y., Song, L., Zhu, P., Zhang, B., Tao, Y., Xu, X., et al. (2012). Single-cell exome sequencing and monoclonal evolution of a JAK2-negative myeloproliferative neoplasm. Cell 148, 873-885.
45. Hsu, P. P., and Sabatini, D. M. (2008). Cancer cell metabolism: Warburg and beyond. Cell 134, 703-707.
46. Jaqaman, K., and Danuser, G. (2006). Linking data to models: data regression. Nat. Rev. Mol. Cell Biol. 7, 813-819.
47. Jungmann, J. H., and Heeren, R. M. (2012). Emerging technologies in mass spectrometry imaging. J. Proteomics 75, 5077-5092.
48. Karapetis, C. S., Khambata-Ford, S., Jonker, D. J., O'Callaghan, C. J., Tu, D., Tebbutt, N. C., et al. (2008). K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N. Engl. J. Med. 359, 1757-1765.
49. Kerkar, S. P., Goldszmid, R. S., Muranski, P., Chinnasamy, D., Yu, Z., Reger, R. N., et al. (2011). IL-12 triggers a programmatic change in dysfunctional myeloid-derived cells within mouse tumors. J. Clin. Invest. 121, 4746-4757.
50. Kerkar, S. P., Muranski, P., Boni, A., Kaiser, A., Boni, A., Sanchez-Perez, L., et al. (2010). Tumor-specific CD8+ T cells expressing interleukin-12 eradicate established cancers in lymphodepleted hosts. Cancer Res. 70, 6725-6734.
51. Kerkar, S. P., and Restifo, N. P. (2012). Cellular constituents of immune escape within the tumor microenvironment. Cancer Res. 72, 3125-3130.
52. Khoo, M. C. K. (2000). Physiological Systems: Analysis, Simulation, and Estimation. New York, NY: IEEE Press.
53. Klinke, D. J. (2009). An empirical bayesian approach for model-based inference of cellular signaling networks. BMC Bioinform. 10:371. doi: 10.1186/1471-2105-10-371
54. Klinke, D. J. (2010a). A multiscale systems perspective on cancer, immunotherapy, and interleukin-12. Mol. Cancer 9, 242.
55. Klinke, D. J. (2010b). Signal transduction networks in cancer: Quantitative parameters influence network topology. Cancer Res. 70, 1773-1782.
56. Klinke, D. J., Cheng, N., and Chambers, E. (2012). Quantifying crosstalk among interferon-, interleukin-12, and tumor necrosis factor signaling pathways within a TH1 cell model. Sci. Signal. 5, ra32.
57. Klinke, D. J., and Finley, S. D. (2012). Timescale analysis of rule-based biochemical reaction networks. Biotechnol. Prog. 28, 33-44.
58. Knutson, K. L., Lu, H., Stone, B., Reiman, J. M., Behrens, M. D., Prosperi, C. M., et al. (2006). Immunoediting of cancers may lead to epithelial to mesenchymal transition. J. Immunol. 177, 1526-1533.
59. Kulkarni, Y. M., Chambers, E., McGray, A. J., Ware, J. S., Bramson, J. L., and Klinke, D. J. (2012). A quantitative systems approach to identify paracrine mechanisms that locally suppress immune response to Interleukin-12 in the B16 melanoma model. Integr. Biol. (Camb) 4, 925-936.
60. Kuukasjarvi, T., Karhu, R., Tanner, M., Kahkonen, M., Schaffer, A., Nupponen, N., et al. (1997). Genetic heterogeneity and clonal evolution underlying development of asynchronous metastasis in human breast cancer. Cancer Res. 57, 1597-1604.
61. Liu, W., Laitinen, S., Khan, S., Vihinen, M., Kowalski, J., Yu, G., et al. (2009). Copy number analysis indicates monoclonal origin of lethal metastatic prostate cancer. Nat. Med. 15, 559-565.
62. Lollini, P. L., Nicoletti, G., Landuzzi, L., De Giovanni, C., Rossi, I., Di Carlo, E., et al. (1998). Down regulation of major histocompatibility complex class I expression in mammary carcinoma of HER-2/neu transgenic mice. Int. J. Cancer 77, 937-941.
63. Maccubbin, D. L., Mace, K. F., Ehrke, M. J., and Mihich, E. (1989). Modification of host antitumor defense mechanisms in mice by progressively growing tumor. Cancer Res. 49, 4216-4224.
64. Mani, S. A., Guo, W., Liao, M. J., Eaton, E. N., Ayyanan, A., Zhou, A. Y., et al. (2008). The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715.
65. Maruyama, T., Mimura, K., Sato, E., Watanabe, M., Mizukami, Y., Kawaguchi, Y., et al. (2010). Inverse correlation of HER2 with MHC class I expression on oesophageal squamous cell carcinoma. Br. J. Cancer 103, 552-559.
66. Matsushita, H., Vesely, M. D., Koboldt, D. C., Rickert, C. G., Uppaluri, R., Magrini, V. J., et al. (2012). Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 482, 400-404.
67. Mattarollo, S. R.,Loi, S., Duret, H., Ma, Y., Zitvogel, L., and Smyth, M. J. (2011). Pivotal role of innate and adaptive immunity in anthracycline chemotherapy of established tumors. Cancer Res. 71, 4809-4820.
68. Mayer, A., Takimoto, M., Fritz, E., Schellander, G., Kofler, K., and Ludwig, H. (1993). The prognostic significance of proliferating cell nuclear antigen, epidermal growth factor receptor, and mdr gene expression in colorectal cancer. Cancer 71, 2454-2460.
69. McLendon, R., Friedman, A., Bigner, D., Van Meir, E. G., Brat, D. J., Mastrogianakis, G. M., et al. (2008). Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455, 1061-1068.
70. Merlo, L. M., Pepper, J. W., Reid, B. J., and Maley, C. C. (2006). Cancer as an evolutionary and ecological process. Nat. Rev. Cancer 6, 924-935.
71. Movahedi, K., Laoui, D., Gysemans, C., Baeten, M., Stange, G., Van den Bossche, J., et al. (2010). Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res. 70, 5728-5739.
72. Muller, W. J., Sinn, E., Pattengale, P. K., Wallace, R., and Leder, P. (1988). Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell 54, 105-115.
73. Murphy, K., Travers, P., and Walport, M., (2007). Janeway's Immunobiology, 7th Edn, New York: Garland Science.
74. Muzny, D. M., Bainbridge, M. N.,Chang, K., Dinh, H. H., Drummond, J. A., Fowler, G., et al. (2012). Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330-337.
75. Nemes, P., A., Woods, S., and Vertes, A. (2010). Simultaneous imaging of small metabolites and lipids in rat brain tissues at atmospheric pressure by laser ablation electrospray ionization mass spectrometry. Anal. Chem. 82, 982-988.
76. Neyman, J., and Pearson, E. S. (1933). On the problem of the most efficient tests of statistical hypotheses. Phil. Trans. Royal Soc. 231, 289-337.
77. Nik-Zainal, S., Van Loo, P., Wedge, D. C., Alexandrov, L. B., Greenman, C. D., Lau, K. W., et al. (2012). The life history of 21 breast cancers. Cell 149, 994-1007.
78. Nowak, M. (2006). "Evolutionary dynamics of cancer," in Evolutionary Dynamics (Cambridge, MA: Harvard University Press), 209-248.
79. Obeid, M., Tesniere, A,. Ghiringhelli, F., Fimia, G. M., Apetoh, L., Perfettini, J. L., et al. (2007). Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 13, 54-61.
80. O'Sullivan, T., Saddawi-Konefka, R., Vermi, W., Koebel, C. M., Arthur, C., White, J. M., et al. (2012). Cancer immunoediting by the innate immune system in the absence of adaptive immunity. J. Exp. Med. 209, 1869-1882.
81. Pàez-Ribes, M., Allen, E., Hudock, J., Takeda, T., Okuyama, H., Vinals, F., et al. (2009). Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15, 220-231.
82. Pawson, T., and Warner, N. (2007). Oncogenic re-wiring of cellular signaling pathways. Oncogene 26, 1268-1275.
83. Pegram, H. J., Lee, J. C., Hayman, E. G., Imperato, G. H., Tedder, T. F., Sadelain, M., et al. (2012). Tumor-targeted T cells modified to secrete IL-12 eradicate systemic tumors without need for prior conditioning. Blood 119, 4133-4141.
84. Platt, J. R. (1964). Strong Inference: Certain systematic methods of scientific thinking may produce much more rapid progress than others. Science 146, 347-353.
85. Pleasance, E. D., Cheetham, R. K., Stephens, P. J., McBride, D. J.,Humphray, S. J., Greenman, C. D., et al. (2010a). A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 463, 191-196.
86. Pleasance, E. D., Stephens, P. J., O'Meara, S., McBride, D. J., Meynert, A., Jones, D., et al. (2010b). A small-cell lung cancer genome with complex signatures of tobacco exposure. Nature 463, 184-190.
87. Prehn, R. T., and Main, J. M. (1957). Immunity to methylcholanthrene-induced sarcomas. J. Natl. Cancer Inst. 18, 769-778.
88. Pulaski, B. A., and Ostrand-Rosenberg, S. (1998). Reduction of established spontaneous mammary carcinoma metastases following immunotherapy with major histocompatibility complex class II and B7.1 cell-based tumor vaccines. Cancer Res. 58, 1486-1493.
89. Roth, J., Qureshi, S., Whitford, I., Vranic, M., Kahn, C. R., Fantus, I. G., et al. (2012). Insulin's discovery: new insights on its ninetieth birthday. Diabetes Metab. Res. Rev. 28, 293-304.
90. Shah, N. P., Nicoll, J. M., Nagar, B., Gorre, M. E., Paquette, R. L., Kuriyan, J., et al. (2002). Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (sti571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell 2, 117-125.
91. Shah, S. P.,Morin, R. D., Khattra, J., Prentice, L., Pugh, T., Burleigh, A., et al. (2009). Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 461, 809-813.
92. Shah, S. P., Roth, A., Goya, R., Oloumi, A., Ha, G., Zhao, Y., et al. (2012). The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 486, 395-399.
93. Shankaran, V., Ikeda, H., Bruce, A. T., White, J. M., Swanson, P. E., Old, L. J., et al. (2001). IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410, 1107-1111.
94. Sharma, S. V., Lee, D. Y., Li, B., Quinlan, M. P., Takahashi, F., Maheswaran, S., et al. (2010). A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141, 69-80.
95. Shipitsin, M., Campbell, L. L., Argani, P., Weremowicz, S., Bloushtain-Qimron, N., Yao, J., et al. (2007). Molecular definition of breast tumor heterogeneity. Cancer Cell 11, 259-273.
96. Sjoblom, T., Jones, S., Wood, L. D., Parsons, D. W., Lin, J., Barber, T. D., et al. (2006). The consensus coding sequences of human breast and colorectal cancers. Science 314, 268-274.
97. Stauber, J.,MacAleese, L.,Franck, J., Claude, E., Snel, M., Kaletas, B. K., et al. (2010). On-tissue protein identification and imaging by MALDI-ion mobility mass spectrometry. J. Am. Soc. Mass Spectrom. 21, 338-347.
98. Stephens, P. J., McBride, D. J., Lin, M. L., Varela, I., Pleasance, E. D., Simpson, J. T., et al. (2009). Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature 462, 1005-1010.
99. Stephens, P. J., Tarpey, P. S,.Davies, H., Van Loo, P., Greenman, C., Wedge, D. C., et al. (2012). The landscape of cancer genes and mutational processes in breast cancer. Nature 486, 400-404.
100. Straussman, R., Morikawa, T., Shee, K., Barzily-Rokni, M., Qian, Z. R., Du, J., et al. (2012). Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 487, 500-504.
101. Théry, C., Ostrowski, M., and Segura, E. (2009). Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9, 581-593.
102. Toni, T., and Stumpf, M. P., (2010). Simulation-based model selection for dynamical systems in systems and population biology. Bioinformatics 26, 104-110.
103. Toni, T., Welch, D., Strelkowa, N., Ipsen, A., and Stumpf, M. P. (2009). Approximate Bayesian computation scheme for parameter inference and model selection in dynamical systems. J. R. Soc. Interface 6, 187-202.
104. Torres, L., Ribeiro, F. R., Pandis, N., Andersen, J. A., Heim, S., and Teixeira, M. R. (2007). Intratumor genomic heterogeneity in breast cancer with clonal divergence between primary carcinomas and lymph node metastases. Breast Cancer Res. Treat. 102, 143- 155.
105. van Elsas, A., Hurwitz, A. A., and Allison, J. P., (1999). Combination immunotherapy of B16 melanoma using anti-cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) and granulocyte/macrophage colony-stimulating factor (GM-CSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation. J. Exp. Med. 190, 355-366.
106. van Leeuwen, F., and Nusse, R. (1995). Oncogene activation and oncogene cooperation in MMTV-induced mouse mammary cancer. Semin. Cancer Biol. 6, 127-133.
107. Venkatasubramanian, R., Henson, M., and Forbes, N. (2006). Incorporating energy metabolism into a growth model of multicellular tumor spheroids. J. Theor. Bio. 242, 440-453.
108. Voulgari, A., and Pintzas, A. (2009). Epithelial-mesenchymal transition in cancer metastasis: Mechanisms, markers and strategies to overcome drug resistance in the clinic. Biochim. Biophys. Acta 1796, 75-90.
109. Vyshemirsky, V., and Girolami, M. A. (2008). Bayesian ranking of biochemical system models. Bioinformatics 24, 833-839.
110. Wang, L. X., Shu, S., Disis, M. L., and Plautz, G. E. (2007). Adoptive transfer of tumor-primed, in vitro-activated, CD4+ T effector cells (TEs) combined with CD8+ TEs provides intratumoral TE proliferation and synergistic antitumor response. Blood 109, 4865-4876.
111. Warburg, O. (1956). On respiratory impairment in cancer cells. Science 124, 269-270.
112. Wei, G., Wei, L., Zhu, J., Zang, C., Hu-Li, J.,Yao, Z., et al. (2009). Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30, 155-167.
113. Weinstein, I. B., and Joe, A. (2008). Oncogene addiction. Cancer Res. 68, 3077-3080.
114. Xu, X., Hou, Y., Yin, X., Bao, L.,Tang, A.,Song, L., et al. (2012). Single-cell exome sequencing reveals single-nucleotide mutation characteristics of a kidney tumor. Cell 148, 886-895.