Early onset and enhanced growth of autochthonous mammary carcinomas in C3-deficient Her2/neu transgenic mice

OncoImmunology

Volumn 2, Issue 9, 2013, Pages

  Bandini, Silvio ^a   Curcio, Claudia ^b   Macagno, Marco ^a   Quaglino, Elena ^a   Arigoni, Maddalena ^a   Lanzardo, Stefania ^a   Hysi, Albana ^b   Barutello, Giuseppina ^a   Consolino, Lorena ^a   Longo, Dario Livio ^a   Musiani, Piero ^b   Forni, Guido ^a   Iezzi, Manuela ^b   Cavallo, Federica ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF CHIETI   (Italy)

Author keywords

Complement; Genetically engineered mice; Her2 neu; Immunosurveillance; Mammary cancer

Indexed keywords

CANCER ANTIBODY; COMPLEMENT COMPONENT C3; EPIDERMAL GROWTH FACTOR RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; BLOOD VESSEL PERMEABILITY; BREAST CARCINOMA; CANCER GROWTH; COMPLEMENT DEPOSITION; CONTROLLED STUDY; IMMUNOCOMPETENCE; IMMUNOSURVEILLANCE; LUNG METASTASIS; MOUSE; MULTIPLE CANCER; NONHUMAN; ONCOGENE NEU; PENETRANCE; REGULATORY T LYMPHOCYTE; TRANSGENIC MOUSE; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION;

EID: 84890288922     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.4161/onci.26137     Document Type: Article

References (52)

1. Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 2009; 30:1073-81; PMID:19468060; http://dx.doi. org/10.1093/carcin/bgp127
2. Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet 2001; 357:539-45; PMID:11229684; http://dx.doi.org/10.1016/ S0140-6736(00)04046-0
3. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity 2004; 21:137-48; PMID:15308095; http://dx.doi.org/10.1016/j.immuni.2004.07.017
4. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011; 331:1565- 70; PMID:21436444; http://dx.doi.org/10.1126/science.1203486
5. Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol 2011; 29:235-71; PMID:21219185; http://dx.doi.org/10.1146/annurev-immunol-031210-101324
6. Fujita T, Taira S, Kodama N, Matsushita M, Fujita T. Mannose-binding protein recognizes glioma cells: in vitro analysis of complement activation on glioma cells via the lectin pathway. Jpn J Cancer Res 1995; 86:187-92; PMID:7730143; http://dx.doi. org/10.1111/j.1349-7006.1995.tb03038.x
7. Swierzko AS, Kilpatrick DC, Cedzynski M. Mannan-binding lectin in malignancy. Mol Immunol 2013; 55:16-21; PMID:23062612; http://dx.doi. org/10.1016/j.molimm.2012.09.005
8. Gao LJ, Gu PQ, Fan WM, Liu Z, Qiu F, Peng YZ, Guo XR. The role of gC1qR in regulating survival of human papillomavirus 16 oncogene-transfected cervical cancer cells. Int J Oncol 2011; 39:1265-72; PMID:21725590
9. Vollmers HP, Brändlein S. Natural antibodies and cancer. N Biotechnol 2009; 25:294-8; PMID:19442595; http://dx.doi.org/10.1016/j. nbt.2009.03.016
10. Hamaï A, Duperrier-Amouriaux K, Pignon P, Raimbaud I, Memeo L, Colarossi C, Canzonieri V, Perin T, Classe JM, Campone M, et al. Antibody responses to NY-ESO-1 in primary breast cancer identify a subtype target for immunotherapy. PLoS One 2011; 6:e21129; PMID:21747904; http://dx.doi.org/10.1371/journal.pone.0021129
11. Lu H, Ladd J, Feng Z, Wu M, Goodell V, Pitteri SJ, Li CI, Prentice R, Hanash SM, Disis ML. Evaluation of known oncoantibodies, HER2, p53, and cyclin B1, in prediagnostic breast cancer sera. Cancer Prev Res (Phila) 2012; 5:1036-43; PMID:22715141; http://dx.doi.org/10.1158/1940-6207.CAPR-11-0558
12. Stover C. Dual role of complement in tumour growth and metastasis (Review). [Review]. Int J Mol Med 2010; 25:307-13; PMID:20127033; http://dx.doi. org/10.3892/ijmm_00000346
13. Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol 2010; 11:785- 97; PMID:20720586; http://dx.doi.org/10.1038/ni.1923
14. Nunez-Cruz S, Gimotty PA, Guerra MW, Connolly DC, Wu YQ, DeAngelis RA, Lambris JD, Coukos G, Scholler N. Genetic and pharmacologic inhibition of complement impairs endothelial cell function and ablates ovarian cancer neovascularization. Neoplasia 2012; 14:994-1004; PMID:23226093
15. Green JE, Hudson T. The promise of genetically engineered mice for cancer prevention studies. Nat Rev Cancer 2005 5:184-98; PMID:15738982; http://dx.doi.org/10.1038/nrc1565
16. Lollini PL, Cavallo F, Nanni P, Forni G. Vaccines for tumour prevention. Nat Rev Cancer 2006; 6:204- 16; PMID:16498443; http://dx.doi.org/10.1038/nrc1815
17. Cavallo F, Offringa R, van der Burg SH, Forni G, Melief CJ. Vaccination for treatment and prevention of cancer in animal models. Adv Immunol 2006; 90:175-213; PMID:16730264; http://dx.doi. org/10.1016/S0065-2776(06)90005-4
18. Quaglino E, Mastini C, Forni G, Cavallo F. ErbB2 transgenic mice: a tool for investigation of the immune prevention and treatment of mammary carcinomas. Curr Protoc Immunol 2008; Chapter 20:Unit 20 9 1- 9-10.
19. Conti L, Lanzardo S, Iezzi M, Montone M, Bolli E, Brioschi C, Maiocchi A, Forni G, Cavallo F. Optical imaging detection of microscopic mammary cancer in ErbB-2 transgenic mice through the DA364 probe binding av β3 integrins. Contrast Media Mol Imaging 2013; 8:350-60; PMID:23613438; http://dx.doi.org/10.1002/cmmi.1529
20. Hüsemann Y, Geigl JB, Schubert F, Musiani P, Meyer M, Burghart E, Forni G, Eils R, Fehm T, Riethmüller G, et al. Systemic spread is an early step in breast cancer. Cancer Cell 2008; 13:58-68; PMID:18167340; http://dx.doi.org/10.1016/j.ccr.2007.12.003
21. Sangaletti S, Tripodo C, Ratti C, Piconese S, Porcasi R, Salcedo R, Trinchieri G, Colombo MP, Chiodoni C. Oncogene-driven intrinsic inflammation induces leukocyte production of tumor necrosis factor that critically contributes to mammary carcinogenesis. Cancer Res 2010; 70:7764-75; PMID:20924115; http://dx.doi.org/10.1158/0008-5472.CAN-10-0471
22. Coscia M, Quaglino E, Iezzi M, Curcio C, Pantaleoni F, Riganti C, Holen I, Mönkkönen H, Boccadoro M, Forni G, et al. Zoledronic acid repolarizes tumourassociated macrophages and inhibits mammary carcinogenesis by targeting the mevalonate pathway. J Cell Mol Med 2010; 14:2803-15; PMID:19818098; http://dx.doi.org/10.1111/j.1582-4934.2009.00926.x
23. Street SE, Zerafa N, Iezzi M, Westwood JA, Stagg J, Musiani P, Smyth MJ. Host perforin reduces tumor number but does not increase survival in oncogenedriven mammary adenocarcinoma. Cancer Res 2007; 67:5454-60; PMID:17545627; http://dx.doi. org/10.1158/0008-5472.CAN-06-4084
24. Rolla S, Ria F, Occhipinti S, Di Sante G, Iezzi M, Spadaro M, Nicolò C, Ambrosino E, Merighi IF, Musiani P, et al. Erbb2 DNA vaccine combined with regulatory T cell deletion enhances antibody response and reveals latent low-avidity T cells: potential and limits of its therapeutic efficacy. J Immunol 2010; 184:6124-32; PMID:20435927; http://dx.doi. org/10.4049/jimmunol.0901215
25. Ambrosino E, Spadaro M, Iezzi M, Curcio C, Forni G, Musiani P, Wei WZ, Cavallo F. Immunosurveillance of Erbb2 carcinogenesis in transgenic mice is concealed by a dominant regulatory T-cell self-tolerance. Cancer Res 2006; 66:7734-40; PMID:16885376; http://dx.doi.org/10.1158/0008-5472.CAN-06-1432
26. Spadaro M, Ambrosino E, Iezzi M, Di Carlo E, Sacchetti P, Curcio C, Amici A, Wei WZ, Musiani P, Lollini PL, et al. Cure of mammary carcinomas in Her-2 transgenic mice through sequential stimulation of innate (neoadjuvant interleukin-12) and adaptive (DNA vaccine electroporation) immunity. Clin Cancer Res 2005; 11:1941-52; PMID:15756020; http://dx.doi.org/10.1158/1078-0432.CCR-04-1873
27. Calogero RA, Cordero F, Forni G, Cavallo F. Inflammation and breast cancer. Inflammatory component of mammary carcinogenesis in ErbB2 transgenic mice. Breast Cancer Res 2007; 9:211; PMID:17705881; http://dx.doi.org/10.1186/bcr1745
28. Strainic MG, Shevach EM, An F, Lin F, Medof ME. Absence of signaling into CD4+ cells via C3aR and C5aR enables autoinductive TGF-β1 signaling and induction of Foxp3+ regulatory T cells. Nat Immunol 2013; 14:162-71; PMID:23263555; http://dx.doi. org/10.1038/ni.2499
29. Kwan WH, van der Touw W, Paz-Artal E, Li MO, Heeger PS. Signaling through C5a receptor and C3a receptor diminishes function of murine natural regulatory T cells. J Exp Med 2013; 210:257- 68; PMID:23382542; http://dx.doi.org/10.1084/jem.20121525
30. Langer HF, Chung KJ, Orlova VV, Choi EY, Kaul S, Kruhlak MJ, Alatsatianos M, DeAngelis RA, Roche PA, Magotti P, et al. Complement-mediated inhibition of neovascularization reveals a point of convergence between innate immunity and angiogenesis. Blood 2010; 116:4395-403; PMID:20625009; http://dx.doi.org/10.1182/blood-2010-01-261503
31. Melani C, Chiodoni C, Forni G, Colombo MP. Myeloid cell expansion elicited by the progression of spontaneous mammary carcinomas in c-erbB-2 transgenic BALB/c mice suppresses immune reactivity. Blood 2003; 102:2138-45; PMID:12750171; http://dx.doi.org/10.1182/blood-2003-01-0190
32. Brunn GJ, Saadi S, Platt JL. Constitutive repression of interleukin-1alpha in endothelial cells. Circ Res 2008; 102:823-30; PMID:18292602; http://dx.doi. org/10.1161/CIRCRESAHA.107.165332
33. Muto S, Sakuma K, Taniguchi A, Matsumoto K. Human mannose-binding lectin preferentially binds to human colon adenocarcinoma cell lines expressing high amount of Lewis A and Lewis B antigens. Biol Pharm Bull 1999; 22:347-52; PMID:10328552; http://dx.doi.org/10.1248/bpb.22.347
34. Halperin JA, Taratuska A, Nicholson-Weller A. Terminal complement complex C5b-9 stimulates mitogenesis in 3T3 cells. J Clin Invest 1993; 91:1974- 8; PMID:8486768; http://dx.doi.org/10.1172/JCI116418
35. Reiter Y, Ciobotariu A, Fishelson Z. Sublytic complement attack protects tumor cells from lytic doses of antibody and complement. Eur J Immunol 1992; 22:1207-13; PMID:1577063; http://dx.doi. org/10.1002/eji.1830220515
36. Markiewski MM, DeAngelis RA, Benencia F, Ricklin-Lichtsteiner SK, Koutoulaki A, Gerard C, Coukos G, Lambris JD. Modulation of the antitumor immune response by complement. Nat Immunol 2008; 9:1225-35; PMID:18820683; http://dx.doi. org/10.1038/ni.1655
37. Gunn L, Ding C, Liu M, Ma Y, Qi C, Cai Y, Hu X, Aggarwal D, Zhang HG, Yan J. Opposing roles for complement component C5a in tumor progression and the tumor microenvironment. J Immunol 2012; 189:2985-94; PMID:22914051; http://dx.doi. org/10.4049/jimmunol.1200846
38. Schwartz-Albiez R, Laban S, Eichmüller S, Kirschfink M. Cytotoxic natural antibodies against human tumours: an option for anti-cancer immunotherapy? Autoimmun Rev 2008; 7:491-5; PMID:18558368; http://dx.doi.org/10.1016/j.autrev.2008.03.012
39. Quaglino E, Rolla S, Iezzi M, Spadaro M, Musiani P, De Giovanni C, Lollini PL, Lanzardo S, Forni G, Sanges R, et al. Concordant morphologic and gene expression data show that a vaccine halts HER-2/neu preneoplastic lesions. J Clin Invest 2004; 113:709-17; PMID:14991069
40. Porzia A, Lanzardo S, Citti A, Cavallo F, Forni G, Santoni A, Galandrini R, Paolini R. Attenuation of PI3K/Akt-mediated tumorigenic signals through PTEN activation by DNA vaccine-induced anti- ErbB2 antibodies. J Immunol 2010; 184:4170-7; PMID:20220087; http://dx.doi.org/10.4049/jimmunol.0903375
41. Spendlove I, Ramage JM, Bradley R, Harris C, Durrant LG. Complement decay accelerating factor (DAF)/CD55 in cancer. Cancer Immunol Immunother 2006; 55:987-95; PMID:16485129; http://dx.doi.org/10.1007/s00262-006-0136-8
42. Vêtvicka V, Hanikýrová M, Vêtvicková J, Ross GD. Regulation of CR3 (CD11b/CD18)-dependent natural killer (NK) cell cytotoxicity by tumour target cell MHC class I molecules. Clin Exp Immunol 1999; 115:229-35; PMID:9933447; http://dx.doi. org/10.1046/j.1365-2249.1999.00800.x
43. Inoue M, Mimura K, Izawa S, Shiraishi K, Inoue A, Shiba S, Watanabe M, Maruyama T, Kawaguchi Y, Inoue S, et al. Expression of MHC Class I on breast cancer cells correlates inversely with HER2 expression. Oncoimmunology 2012; 1:1104-10; PMID:23170258; http://dx.doi.org/10.4161/onci.21056
44. Okita R, Mougiakakos D, Ando T, Mao Y, Sarhan D, Wennerberg E, Seliger B, Lundqvist A, Mimura K, Kiessling R. HER2/HER3 signaling regulates NK cell-mediated cytotoxicity via MHC class I chain-related molecule A and B expression in human breast cancer cell lines. J Immunol 2012; 188:2136- 45; PMID:22301547; http://dx.doi.org/10.4049/jimmunol.1102237
45. Strainic MG, Liu J, Huang D, An F, Lalli PN, Muqim N, Shapiro VS, Dubyak GR, Heeger PS, Medof ME. Locally produced complement fragments C5a and C3a provide both costimulatory and survival signals to naive CD4+ T cells. Immunity 2008; 28:425- 35; PMID:18328742; http://dx.doi.org/10.1016/j. immuni.2008.02.001
46. Amara U, Flierl MA, Rittirsch D, Klos A, Chen H, Acker B, Brückner UB, Nilsson B, Gebhard F, Lambris JD, et al. Molecular intercommunication between the complement and coagulation systems. J Immunol 2010; 185:5628-36; PMID:20870944; http://dx.doi.org/10.4049/jimmunol.0903678
47. Huber-Lang M, Sarma JV, Zetoune FS, Rittirsch D, Neff TA, McGuire SR, Lambris JD, Warner RL, Flierl MA, Hoesel LM, et al. Generation of C5a in the absence of C3: a new complement activation pathway. Nat Med 2006; 12:682-7; PMID:16715088; http://dx.doi.org/10.1038/nm1419
48. O'Sullivan T, Saddawi-Konefka R, Vermi W, Koebel CM, Arthur C, White JM, Uppaluri R, Andrews DM, Ngiow SF, Teng MW, et al. Cancer immunoediting by the innate immune system in the absence of adaptive immunity. J Exp Med 2012; 209:1869- 82; PMID:22927549; http://dx.doi.org/10.1084/jem.20112738
49. Corrales L, Ajona D, Rafail S, Lasarte JJ, Riezu-Boj JI, Lambris JD, Rouzaut A, Pajares MJ, Montuenga LM, Pio R. Anaphylatoxin C5a creates a favorable microenvironment for lung cancer progression. J Immunol 2012; 189:4674-83; PMID:23028051; http://dx.doi.org/10.4049/jimmunol.1201654
50. Trendelenburg M, Fossati-Jimack L, Cortes- Hernandez J, Turnberg D, Lewis M, Izui S, Cook HT, Botto M. The role of complement in cryoglobulin- induced immune complex glomerulonephritis. J Immunol 2005; 175:6909-14; PMID:16272350
51. Rovero S, Amici A, Di Carlo E, Bei R, Nanni P, Quaglino E, Porcedda P, Boggio K, Smorlesi A, Lollini PL, et al. DNA vaccination against rat her-2/Neu p185 more effectively inhibits carcinogenesis than transplantable carcinomas in transgenic BALB/c mice. J Immunol 2000; 165:5133-42; PMID:11046045
52. Arigoni M, Barutello G, Lanzardo S, Longo D, Aime S, Curcio C, Iezzi M, Zheng Y, Barkefors I, Holmgren L, et al. A vaccine targeting angiomotin induces an antibody response which alters tumor vessel permeability and hampers the growth of established tumors. Angiogenesis 2012; 15:305-16; PMID:22426512; http://dx.doi.org/10.1007/s10456-012-9263-3