Abstract
The availability and diversity of mouse models of human cancer that develop organ-specific neoplasms has increased significantly in the past 10 years. These, coupled with mouse strains where components of the immune system have been manipulated or deleted, have provided novel insights into how immune cells and immune function significantly contributes to cancer development. Herein, we review relevant literature, where mouse models of human cancer development have provided novel insights into mechanisms of pro- versus antitumor immunity.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, Sakagami M, Nakanishi K, Akira S (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9:143–150
Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499–511
Albini A, Sporn MB (2007) The tumour microenvironment as a target for chemoprevention. Nat Rev Cancer 7:139–147
Alexopoulou L, Holt AC, Medzhitov R, Flavell RA (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413:732–738
Almand B, Clark JI, Nikitina E, van Beynen J, English NR, Knight SC, Carbone DP, Gabrilovich DI (2001) Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J Immunol 166:678–689
Arbeit JM, Munger K, Howley PM, Hanahan D (1994) Progressive squamous epithelial neoplasia in K14-human papillomavirus type 16 transgenic mice. J Virol 68:4358–4368
Arber N, Eagle CJ, Spicak J, Racz I, Dite P, Hajer J, Zavoral M, Lechuga MJ, Gerletti P, Tang J et al (2006) Celecoxib for the prevention of colorectal adenomatous polyps. N Engl J Med 355:885–895
Arnott CH, Scott KA, Moore RJ, Robinson SC, Thompson RG, Balkwill FR (2004) Expression of both TNF-alpha receptor subtypes is essential for optimal skin tumour development. Oncogene 23:1902–1910
Balkwill F, Charles KA, Mantovani A (2005) Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 7:211–217
Beck BN, Henney CS (1981) An analysis of the natural killer cell defect in beige mice. Cell Immunol 61:343–352
Belardelli F, Ferrantini M (2002) Cytokines as a link between innate and adaptive antitumor immunity. Trends Immunol 23:201–208
Bennett CL, Clausen BE (2007) DC ablation in mice: promises, pitfalls, and challenges. Trends Immunol 28:525–531
Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, Tanzawa K, Thorpe P, Itohara S, Werb Z et al (2000) Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2:737–744
Bertagnolli MM, Eagle CJ, Zauber AG, Redston M, Solomon SD, Kim K, Tang J, Rosenstein RB, Wittes J, Corle D et al (2006) Celecoxib for the prevention of sporadic colorectal adenomas. N Engl J Med 355:873–884
Bhowmick NA, Moses HL (2005) Tumor-stroma interactions. Curr Opin Genet Dev 15:97–101
Borriello F, Sethna MP, Boyd SD, Schweitzer AN, Tivol EA, Jacoby D, Strom TB, Simpson EM, Freeman GJ, Sharpe AH (1997) B7-1 and B7-2 have overlapping, critical roles in immunoglobulin class switching and germinal center formation. Immunity 6:303–313
Boshoff C, Weiss R (2002) AIDS-related malignancies. Nat Rev Cancer 2:373–382
Bosma GC, Custer RP, Bosma MJ (1983) A severe combined immunodeficiency mutation in the mouse. Nature 301:527–530
Botto M, Dell’Agnola C, Bygrave AE, Thompson EM, Cook HT, Petry F, Loos M, Pandolfi PP, Walport MJ (1998) Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 19:56–59
Buckanovich RJ, Facciabene A, Kim S, Benencia F, Sasaroli D, Balint K, Katsaros D, O’Brien-Jenkins A, Gimotty PA, Coukos G (2008) Endothelin B receptor mediates the endothelial barrier to T cell homing to tumors and disables immune therapy. Nat Med 14:28–36
Buell JF, Gross TG, Woodle ES (2005) Malignancy after transplantation. Transplantation 80:S254–S264
Carroll MC (2004) The complement system in regulation of adaptive immunity. Nat Immunol 5:981–986
Casanovas O, Hicklin DJ, Bergers G, Hanahan D (2005) Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 8:299–309
Cha YI, DuBois RN (2007) NSAIDs and cancer prevention: targets downstream of COX-2. Annu Rev Med 58:239–252
Chambers CA, Cado D, Truong T, Allison JP (1997) Thymocyte development is normal in CTLA-4-deficient mice. Proc Natl Acad Sci USA 94:9296–9301
Chen J, Trounstine M, Alt FW, Young F, Kurahara C, Loring JF, Huszar D (1993) Immunoglobulin gene rearrangement in B cell deficient mice generated by targeted deletion of the JH locus. Int Immunol 5:647–656
Choudhury A, Mosolits S, Kokhaei P, Hansson L, Palma M, Mellstedt H (2006) Clinical results of vaccine therapy for cancer: learning from history for improving the future. Adv Cancer Res 95:147–202
Chulada PC, Thompson MB, Mahler JF, Doyle CM, Gaul BW, Lee C, Tiano HF, Morham SG, Smithies O, Langenbach R (2000) Genetic disruption of Ptgs-1, as well as Ptgs-2, reduces intestinal tumorigenesis in Min mice. Cancer Res 60:4705–4708
Colombo MP, Piconese S (2007) Regulatory T-cell inhibition versus depletion: the right choice in cancer immunotherapy. Nat Rev Cancer 7:880–887
Coussens LM, Hanahan D, Arbeit JM (1996) Genetic predisposition and parameters of malignant progression in K14- HPV16 transgenic mice. Am J Pathol 149:1899–1917
Coussens LM, Raymond WW, Bergers G, Laig-Webster M, Behrendtsen O, Werb Z, Caughey GH, Hanahan D (1999) Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev 13:1382–1397
Coussens LM, Tinkle CL, Hanahan D, Werb Z (2000) MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 103:481–490
Croci DO, Zacarias Fluck MF, Rico MJ, Matar P, Rabinovich GA, Scharovsky OG (2007) Dynamic cross-talk between tumor and immune cells in orchestrating the immunosuppressive network at the tumor microenvironment. Cancer Immunol Immunother 56:1687–1700
Cui J, Shin T, Kawano T, Sato H, Kondo E, Toura I, Kaneko Y, Koseki H, Kanno M, Taniguchi M (1997) Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science 278:1623–1626
Daniel D, Meyer-Morse N, Bergsland EK, Dehne K, Coussens LM, Hanahan D (2003) Immune enhancement of skin carcinogenesis by CD4+ T cells. J Exp Med 197:1017–1028
Dannenberg A, Subbaramaiah K (2003) Targeting cyclooxygenase-2 in human neoplasia: rationale and promise. Cancer Cell 4:431–436
De Giorgi U, Pupi A, Turrisi G, Montenora I, Morini S, Fayyaz M, De Simone M, Fiorentini G (2007) Critical update and emerging trends in imatinib treatment for gastrointestinal stromal tumor. Rev Recent Clin Trials 2:43–48
De Palma M, Venneri MA, Galli R, Sergi Sergi L, Politi LS, Sampaolesi M, Naldini L (2005) Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 8:211–226
de Visser KE, Korets LV, Coussens LM (2004) Early neoplastic progression is complement independent. Neoplasia 6:768–776
de Visser KE, Korets LV, Coussens LM (2005) De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 7:411–423
de Visser KE, Eichten A, Coussens LM (2006) Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 6:24–37
Dinchuk JE, Car BD, Focht RJ, Johnston JJ, Jaffee BD, Covington MB, Contel NR, Eng VM, Collins RJ, Czerniak PM et al (1995) Renal abnormalities and an altered inflammatory response in mice lacking cyclooxygenase II. Nature 378:406–409
Druker BJ (2004) Imatinib as a paradigm of targeted therapies. Adv Cancer Res 91:1–30
Duffield JS, Forbes SJ, Constandinou CM, Clay S, Partolina M, Vuthoori S, Wu S, Lang R, Iredale JP (2005) Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J Clin Invest 115:56–65
Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD (2002) Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 3:991–998
Dunn GP, Old LJ, Schreiber RD (2004) The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21:137–148
Dunn GP, Koebel CM, Schreiber RD (2006) Interferons, immunity and cancer immunoediting. Nat Rev Immunol 6:836–848
Duttlinger R, Manova K, Chu TY, Gyssler C, Zelenetz AD, Bachvarova RF, Besmer P (1993) W-sash affects positive and negative elements controlling c-kit expression: ectopic c-kit expression at sites of kit-ligand expression affects melanogenesis. Development 118:705–717
Ebnet K, Hausmann M, Lehmann-Grube F, Mullbacher A, Kopf M, Lamers M, Simon MM (1995) Granzyme A-deficient mice retain potent cell-mediated cytotoxicity. EMBO J 14:4230–4239
Enzler T, Gillessen S, Manis JP, Ferguson D, Fleming J, Alt FW, Mihm M, Dranoff G (2003) Deficiencies of GM-CSF and interferon gamma link inflammation and cancer. J Exp Med 197:1213–1219
Feuillet V, Medjane S, Mondor I, Demaria O, Pagni PP, Galan JE, Flavell RA, Alexopoulou L (2006) Involvement of Toll-like receptor 5 in the recognition of flagellated bacteria. Proc Natl Acad Sci USA 103:12487–12492
Finke J, Ferrone S, Frey A, Mufson A, Ochoa A (1999) Where have all the T cells gone? Mechanisms of immune evasion by tumors. Immunol Today 20:158–160
Fischer C, Jonckx B, Mazzone M, Zacchigna S, Loges S, Pattarini L, Chorianopoulos E, Liesenborghs L, Koch M, De Mol M et al (2007) Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels. Cell 131:463–475
Freeman GJ, Borriello F, Hodes RJ, Reiser H, Hathcock KS, Laszlo G, McKnight AJ, Kim J, Du L, Lombard DB et al (1993) Uncovering of functional alternative CTLA-4 counter-receptor in B7-deficient mice. Science 262:907–909
Frese KK, Tuveson DA (2007) Maximizing mouse cancer models. Nat Rev Cancer 7:645–658
Fukata M, Chen A, Vamadevan AS, Cohen J, Breglio K, Krishnareddy S, Hsu D, Xu R, Harpaz N, Dannenberg AJ et al (2007) Toll-like receptor-4 promotes the development of colitis-associated colorectal tumors. Gastroenterology 133:1869–1881
Fung-Leung WP, Schilham MW, Rahemtulla A, Kundig TM, Vollenweider M, Potter J, van Ewijk W, Mak TW (1991) CD8 is needed for development of cytotoxic T cells but not helper T cells. Cell 65:443–449
Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, Camus M, Berger A, Wind P et al (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313:1960–1964
Garbe AI, Vermeer B, Gamrekelashvili J, von Wasielewski R, Greten FR, Westendorf AM, Buer J, Schmid RM, Manns MP, Korangy F et al (2006) Genetically induced pancreatic adenocarcinoma is highly immunogenic and causes spontaneous tumor-specific immune responses. Cancer Res 66:508–516
Girardi M, Oppenheim DE, Steele CR, Lewis JM, Glusac E, Filler R, Hobby P, Sutton B, Tigelaar RE, Hayday AC (2001) Regulation of cutaneous malignancy by gammadelta T cells. Science 294:605–609
Girardi M, Glusac E, Filler RB, Roberts SJ, Propperova I, Lewis J, Tigelaar RE, Hayday AC (2003) The distinct contributions of murine T cell receptor (TCR)gammadelta+ and TCRalphabeta+ T cells to different stages of chemically induced skin cancer. J Exp Med 198:747–755
Giraudo E, Inoue M, Hanahan D (2004) An amino-bisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis. J Clin Invest 114:623–633
Goldrath AW, Bevan MJ (1999) Selecting and maintaining a diverse T-cell repertoire. Nature 402:255–262
Gounaris E, Erdman SE, Restaino C, Gurish MF, Friend DS, Gounari F, Lee DM, Zhang G, Glickman JN, Shin K et al (2007) Mast cells are an essential hematopoietic component for polyp development. Proc Natl Acad Sci USA 104:19977–19982
Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, Egan LJ, Kagnoff MF, Karin M (2004) IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118:285–296
Grimbaldeston MA, Chen CC, Piliponsky AM, Tsai M, Tam SY, Galli SJ (2005) Mast cell-deficient W-sash c-kit mutant Kit W-sh/W-sh mice as a model for investigating mast cell biology in vivo. Am J Pathol 167:835–848
Grulich AE, van Leeuwen MT, Falster MO, Vajdic CM (2007) Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet 370:59–67
Guerra C, Schuhmacher AJ, Canamero M, Grippo PJ, Verdaguer L, Perez-Gallego L, Dubus P, Sandgren EP, Barbacid M (2007) Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice. Cancer Cell 11:291–302
Gupta RA, Dubois RN (2001) Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2. Nat Rev Cancer 1:11–21
Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70
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 21:2258–2270
Hazenbos WL, Gessner JE, Hofhuis FM, Kuipers H, Meyer D, Heijnen IA, Schmidt RE, Sandor M, Capel PJ, Daeron M et al (1996) Impaired IgG-dependent anaphylaxis and Arthus reaction in Fc gamma RIII (CD16) deficient mice. Immunity 5:181–188
Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, Matsumoto M, Hoshino K, Wagner H, Takeda K et al (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408:740–745
Hemmi H, Kaisho T, Takeuchi O, Sato S, Sanjo H, Hoshino K, Horiuchi T, Tomizawa H, Takeda K, Akira S (2002) Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol 3:196–200
Hennings H, Glick AB, Greenhalgh DA, Morgan DL, Strickland JE, Tennenbaum T, Yuspa SH (1993) Critical aspects of initiation, promotion, and progression in multistage epidermal carcinogenesis. Proc Soc Exp Biol Med 202:1–8
Heusel JW, Wesselschmidt RL, Shresta S, Russell JH, Ley TJ (1994) Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell 76:977–987
Hopken UE, Lu B, Gerard NP, Gerard C (1996) The C5a chemoattractant receptor mediates mucosal defence to infection. Nature 383:86–89
Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S (1999) Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 162:3749–3752
Howe LR, Chang SH, Tolle KC, Dillon R, Young LJ, Cardiff RD, Newman RA, Yang P, Thaler HT, Muller WJ et al (2005) HER2/neu-induced mammary tumorigenesis and angiogenesis are reduced in cyclooxygenase-2 knockout mice. Cancer Res 65:10113–10119
Ikehara S, Pahwa RN, Fernandes G, Hansen CT, Good RA (1984) Functional T cells in athymic nude mice. Proc Natl Acad Sci USA 81:886–888
Imada A, Shijubo N, Kojima H, Abe S (2000) Mast cells correlate with angiogenesis and poor outcome in stage I lung adenocarcinoma. Eur Respir J 15:1087–1093
Itohara S, Mombaerts P, Lafaille J, Iacomini J, Nelson A, Clarke AR, Hooper ML, Farr A, Tonegawa S (1993) T cell receptor delta gene mutant mice: independent generation of alpha beta T cells and programmed rearrangements of gamma delta TCR genes. Cell 72:337–348
Jain RK (2005) Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307:58–62
Jain RK (2008) Lessons from multidisciplinary translational trials on anti-angiogenic therapy of cancer. Nat Rev Cancer 8:309–316
Janeway CA Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216
Janeway CA, Travers P, Walport M, Shlomchik M (2001) Immunobiology, 5th edn. Garland Publishing, New York
Johansson M, Denardo DG, Coussens LM (2008) Polarized immune responses differentially regulate cancer development. Immunol Rev 222:145–154
Jonkers J, Derksen PW (2007) Modeling metastatic breast cancer in mice. J Mammary Gland Biol Neoplasia 12:191–203
Joyce JA (2005) Therapeutic targeting of the tumor microenvironment. Cancer Cell 7:513–520
Jung S, Unutmaz D, Wong P, Sano G, De los Santos K, Sparwasser T, Wu S, Vuthoori S, Ko K, Zavala F et al (2002) In vivo depletion of CD11c(+) dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens. Immunity 17:211–220
Kagi D, Ledermann B, Burki K, Seiler P, Odermatt B, Olsen KJ, Podack ER, Zinkernagel RM, Hengartner H (1994) Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369:31–37
Kaplan DH, Shankaran V, Dighe AS, Stockert E, Aguet M, Old LJ, Schreiber RD (1998) Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci USA 95:7556–7561
Karin M (2006) NF-kappaB and cancer: mechanisms and targets. Mol Carcinog 45:355–361
Kim CF, Jackson EL, Kirsch DG, Grimm J, Shaw AT, Lane K, Kissil J, Olive KP, Sweet-Cordero A, Weissleder R et al (2005) Mouse models of human non-small-cell lung cancer: raising the bar. Cold Spring Harb Symp Quant Biol 70:241–250
Kitamura Y, Go S, Hatanaka K (1978) Decrease of mast cells in W/Wv mice and their increase by bone marrow transplantation. Blood 52:447–452
Kitamura D, Roes J, Kuhn R, Rajewsky K (1991) A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 350:423–426
Klein S, McCormick F, Levitzki A (2005) Killing time for cancer cells. Nat Rev Cancer 5:573–580
Koller BH, Marrack P, Kappler JW, Smithies O (1990) Normal development of mice deficient in beta 2M, MHC class I proteins, and CD8+ T cells. Science 248:1227–1230
Kontgen F, Suss G, Stewart C, Steinmetz M, Bluethmann H (1993) Targeted disruption of the MHC class II Aa gene in C57BL/6 mice. Int Immunol 5:957–964
Kusmartsev S, Gabrilovich DI (2006) Effect of tumor-derived cytokines and growth factors on differentiation and immune suppressive features of myeloid cells in cancer. Cancer Metastasis Rev 25:323–331
Kwon BS, Hurtado JC, Lee ZH, Kwack KB, Seo SK, Choi BK, Koller BH, Wolisi G, Broxmeyer HE, Vinay DS (2002) Immune responses in 4-1BB (CD137)-deficient mice. J Immunol 168:5483–5490
Langenbach R, Morham SG, Tiano HF, Loftin CD, Ghanayem BI, Chulada PC, Mahler JF, Lee CA, Goulding EH, Kluckman KD et al (1995) Prostaglandin synthase 1 gene disruption in mice reduces arachidonic acid-induced inflammation and indomethacin-induced gastric ulceration. Cell 83:483–492
Langowski JL, Zhang X, Wu L, Mattson JD, Chen T, Smith K, Basham B, McClanahan T, Kastelein RA, Oft M (2006) IL-23 promotes tumour incidence and growth. Nature 442:461–465
Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL (1996) Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res 56:4625–4629
Lin EY, Nguyen AV, Russell RG, Pollard JW (2001) Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med 193:727–740
Luo JL, Tan W, Ricono JM, Korchynskyi O, Zhang M, Gonias SL, Cheresh DA, Karin M (2007) Nuclear cytokine-activated IKKalpha controls prostate cancer metastasis by repressing Maspin. Nature 446:690–694
Luster AD (2002) The role of chemokines in linking innate and adaptive immunity. Curr Opin Immunol 14:129–135
Marks SC Jr, Lane PW (1976) Osteopetrosis, a new recessive skeletal mutation on chromosome 12 of the mouse. J Hered 67:11–18
McHeyzer-Williams MG (2003) B cells as effectors. Curr Opin Immunol 15:354–361
Molina H, Holers VM, Li B, Fung Y, Mariathasan S, Goellner J, Strauss-Schoenberger J, Karr RW, Chaplin DD (1996) Markedly impaired humoral immune response in mice deficient in complement receptors 1 and 2. Proc Natl Acad Sci USA 93:3357–3361
Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE (1992) RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68:869–877
Mombaerts P, Arnoldi J, Russ F, Tonegawa S, Kaufmann SH (1993) Different roles of alpha beta and gamma delta T cells in immunity against an intracellular bacterial pathogen. Nature 365:53–56
Moore RJ, Owens DM, Stamp G, Arnott C, Burke F, East N, Holdsworth H, Turner L, Rollins B, Pasparakis M et al (1999) Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat Med 5:828–831
Morham SG, Langenbach R, Loftin CD, Tiano HF, Vouloumanos N, Jennette JC, Mahler JF, Kluckman KD, Ledford A, Lee CA et al (1995) Prostaglandin synthase 2 gene disruption causes severe renal pathology in the mouse. Cell 83:473–482
Murphy JE, Robert C, Kupper TS (2000) Interleukin-1 and cutaneous inflammation: a crucial link between innate and acquired immunity. J Invest Dermatol 114:602–608
Nelson CM, Bissell MJ (2006) Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu Rev Cell Dev Biol 22:287–309
Nozawa H, Chiu C, Hanahan D (2006) Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci USA 103:12493–12498
Oshima M, Dinchuk JE, Kargman SL, Oshima H, Hancock B, Kwong E, Trzaskos JM, Evans JF, Taketo MM (1996) Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 87:803–809
Ostrand-Rosenberg S (2008) Immune surveillance: a balance between protumor and antitumor immunity. Curr Opin Genet Dev 18:11–18
Persano L, Crescenzi M, Indraccolo S (2007) Anti-angiogenic gene therapy of cancer: current status and future prospects. Mol Aspects Med 28:87–114
Peto J (2001) Cancer epidemiology in the last century and the next decade. Nature 411:390–395
Pikarsky E, Porat RM, Stein I, Abramovitch R, Amit S, Kasem S, Gutkovich-Pyest E, Urieli-Shoval S, Galun E, Ben-Neriah Y (2004) NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 431:461–466
Qin Z, Blankenstein T (2004) A cancer immunosurveillance controversy. Nat Immunol 5:3–4
Rahemtulla A, Fung-Leung WP, Schilham MW, Kundig TM, Sambhara SR, Narendran A, Arabian A, Wakeham A, Paige CJ, Zinkernagel RM et al (1991) Normal development and function of CD8+ cells but markedly decreased helper cell activity in mice lacking CD4. Nature 353:180–184
Roberts SJ, Ng BY, Filler RB, Lewis J, Glusac EJ, Hayday AC, Tigelaar RE, Girardi M (2007) Characterizing tumor-promoting T cells in chemically induced cutaneous carcinogenesis. Proc Natl Acad Sci USA 104:6770–6775
Sawyers C (2004) Targeted cancer therapy. Nature 432:294–297
Serafini P, De Santo C, Marigo I, Cingarlini S, Dolcetti L, Gallina G, Zanovello P, Bronte V (2004) Derangement of immune responses by myeloid suppressor cells. Cancer Immunol Immunother 53:64–72
Shahinian A, Pfeffer K, Lee KP, Kundig TM, Kishihara K, Wakeham A, Kawai K, Ohashi PS, Thompson CB, Mak TW (1993) Differential T cell costimulatory requirements in CD28-deficient mice. Science 261:609–612
Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, Schreiber RD (2001) IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410:1107–1111
Shinkai Y, Rathbun G, Lam KP, Oltz EM, Stewart V, Mendelsohn M, Charron J, Datta M, Young F, Stall AM et al (1992) RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68:855–867
Sinnamon MJ, Carter KJ, Sims LP, Lafleur B, Fingleton B, Matrisian LM (2008) A protective role for mast cells in intestinal tumorigenesis. Carcinogenesis 29(4):880–886
Smyth MJ, Thia KY, Street SE, Cretney E, Trapani JA, Taniguchi M, Kawano T, Pelikan SB, Crowe NY, Godfrey DI (2000) Differential tumor surveillance by natural killer (NK) and NKT cells. J Exp Med 191:661–668
Smyth MJ, Crowe NY, Godfrey DI (2001) NK cells and NKT cells collaborate in host protection from methylcholanthrene-induced fibrosarcoma. Int Immunol 13:459–463
Soucek L, Lawlor ER, Soto D, Shchors K, Swigart LB, Evan GI (2007) Mast cells are required for angiogenesis and macroscopic expansion of Myc-induced pancreatic islet tumors. Nat Med 13:1211–1218
Sprent J, Surh CD (2002) T cell memory. Annu Rev Immunol 20:551–579
Street SE, Zerafa N, Iezzi M, Westwood JA, Stagg J, Musiani P, Smyth MJ (2007) Host perforin reduces tumor number but does not increase survival in oncogene-driven mammary adenocarcinoma. Cancer Res 67:5454–5460
Swann JB, Smyth MJ (2007) Immune surveillance of tumors. J Clin Invest 117:1137–1146
Swann JB, Vesely MD, Silva A, Sharkey J, Akira S, Schreiber RD, Smyth MJ (2008) Demonstration of inflammation-induced cancer and cancer immunoediting during primary tumorigenesis. Proc Natl Acad Sci USA 105:652–656
Tabi Z, Man S (2006) Challenges for cancer vaccine development. Adv Drug Deliv Rev 58:902–915
Takahashi T, Tanaka M, Brannan CI, Jenkins NA, Copeland NG, Suda T, Nagata S (1994) Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 76:969–976
Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV (1994) FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell 76:519–529
Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, Ogawa T, Takeda K, Akira S (1999) Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11:443–451
Takeuchi O, Kawai T, Muhlradt PF, Morr M, Radolf JD, Zychlinsky A, Takeda K, Akira S (2001) Discrimination of bacterial lipoproteins by Toll-like receptor 6. Int Immunol 13:933–940
Takeuchi O, Sato S, Horiuchi T, Hoshino K, Takeda K, Dong Z, Modlin RL, Akira S (2002) Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. J Immunol 169:10–14
Taylor PR, Nash JT, Theodoridis E, Bygrave AE, Walport MJ, Botto M (1998) A targeted disruption of the murine complement factor B gene resulting in loss of expression of three genes in close proximity, factor B, C2, and D17H6S45. J Biol Chem 273:1699–1704
Tiano HF, Loftin CD, Akunda J, Lee CA, Spalding J, Sessoms A, Dunson DB, Rogan EG, Morham SG, Smart RC et al (2002) Deficiency of either cyclooxygenase (COX)-1 or COX-2 alters epidermal differentiation and reduces mouse skin tumorigenesis. Cancer Res 62:3395–3401
Tonegawa S (1983) Somatic generation of antibody diversity. Nature 302:575–581
Turini ME, DuBois RN (2002) Cyclooxygenase-2: a therapeutic target. Annu Rev Med 53:35–37
Tuveson DA, Jacks T (2002) Technologically advanced cancer modeling in mice. Curr Opin Genet Dev 12:105–110
van den Broek ME, Kagi D, Ossendorp F, Toes R, Vamvakas S, Lutz WK, Melief CJ, Zinkernagel RM, Hengartner H (1996) Decreased tumor surveillance in perforin-deficient mice. J Exp Med 184:1781–1790
Van Dyke T, Jacks T (2002) Cancer modeling in the modern era: progress and challenges. Cell 108:135–144
Van Kaer L, Ashton-Rickardt PG, Ploegh HL, Tonegawa S (1992) TAP1 mutant mice are deficient in antigen presentation, surface class I molecules, and CD4-8+ T cells. Cell 71:1205–1214
van Kempen LC, de Visser KE, Coussens LM (2006) Inflammation, proteases and cancer. Eur J Cancer 42:728–734
Van Rooijen N, Sanders A (1994) Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods 174:83–93
Walport MJ (2001a) Complement. First of two parts. N Engl J Med 344:1058–1066
Walport MJ (2001b) Complement. Second of two parts. N Engl J Med 344:1140–1144
Wedemeyer J, Galli SJ (2005) Decreased susceptibility of mast cell-deficient Kit(W)/Kit(W-v) mice to the development of 1, 2-dimethylhydrazine-induced intestinal tumors. Lab Invest 85:388–396
Wessels MR, Butko P, Ma M, Warren HB, Lage AL, Carroll MC (1995) Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. Proc Natl Acad Sci USA 92:11490–11494
Willimsky G, Blankenstein T (2005) Sporadic immunogenic tumours avoid destruction by inducing T-cell tolerance. Nature 437:141–146
Wyckoff J, Wang W, Lin EY, Wang Y, Pixley F, Stanley ER, Graf T, Pollard JW, Segall J, Condeelis J (2004) A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res 64:7022–7029
Yu P, Rowley DA, Fu YX, Schreiber H (2006) The role of stroma in immune recognition and destruction of well-established solid tumors. Curr Opin Immunol 18:226–231
Yuspa SH (2000) Overview of carcinogenesis: past, present and future. Carcinogenesis 21:341–344
Yusuf N, Nasti TH, Long JA, Naseemuddin M, Lucas AP, Xu H, Elmets CA (2008) Protective role of Toll-like receptor 4 during the initiation stage of cutaneous chemical carcinogenesis. Cancer Res 68:615–622
Zlotnik A, Yoshie O (2000) Chemokines: a new classification system and their role in immunity. Immunity 12:121–127
Zou W (2005) Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 5:263–274
Zou W (2006) Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 6:295–307
Acknowledgments
The authors thank all those that have contributed to work discussed here but are not referenced due to space constraints. The authors acknowledge support by grants from the National Institutes of Health (NIH)/NCI (R01CA130980, R01CA132566, R01CA140943, P50CA58207), and the Department of Defense (W81XWH-06-1-0416, PR080717 to L.M.C., and grants from the Dutch Cancer Society (2006-3715 and 2011-5004), the Netherlands Organization for Scientific Research (VIDI 917.96.307), and the Association for International Cancer Research (AICR 11-0677) to K.E.d.V.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer Science+Business Media, LLC
About this chapter
Cite this chapter
de Visser, K.E., Coussens, L.M. (2012). Utilizing Mouse Models of Human Cancer for Assessing Immune Modulation of Cancer Development. In: Green, J., Ried, T. (eds) Genetically Engineered Mice for Cancer Research. Springer, New York, NY. https://doi.org/10.1007/978-0-387-69805-2_21
Download citation
DOI: https://doi.org/10.1007/978-0-387-69805-2_21
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-0-387-69803-8
Online ISBN: 978-0-387-69805-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)