Antitumor effects of L-BLP25 Antigen-Specific tumor immunotherapy in a novel human MUC1 transgenic lung cancer mouse model

Journal of Translational Medicine

Volumn 11, Issue 1, 2013, Pages

  Wurz, Gregory T ^a   Gutierrez, Audrey M ^a   Greenberg, Brittany E ^a   Vang, Daniel P ^a   Griffey, Stephen M ^b   Kao, Chiao Jung ^a   Wolf, Michael ^c   DeGregorio, Michael W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MERCK KGAA   (Germany)

Author keywords

Cytokines; Immunotherapy; L BLP25; Lung cancer; MUC1

Indexed keywords

ANTINEOPLASTIC AGENT; CYCLOPHOSPHAMIDE; DIETHYLSTILBESTROL; EMEPEPIMUT S; GAMMA INTERFERON; IMMUNOMODULATING AGENT; INTERLEUKIN 12; INTERLEUKIN 2; MUCIN 1; URETHAN; AUTACOID; CANCER VACCINE; CYTOKINE; L-BLP25; MEMBRANE PROTEIN; TUMOR ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG MEGADOSE; DRUG SCREENING; FEMALE; LOW DRUG DOSE; LUNG CANCER; LUNG NON SMALL CELL CANCER; MALE; MONOTHERAPY; MOUSE; MULTIPLE CYCLE TREATMENT; NONHUMAN; POLARIZATION; PROTEIN BLOOD LEVEL; SINGLE DRUG DOSE; TH1 CELL; TH2 CELL; TRANSGENIC MOUSE; TREATMENT DURATION; TREATMENT RESPONSE; TUMOR XENOGRAFT; ADENOMA; ANIMAL; C57BL MOUSE; CARCINOGENESIS; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; HUMAN; IMMUNITY; IMMUNOLOGY; IMMUNOTHERAPY; LUNG NEOPLASMS; METABOLISM; PATHOLOGY; TIME;

ADENOMA; ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; CARCINOGENESIS; CYCLOPHOSPHAMIDE; CYTOKINES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; IMMUNITY; IMMUNOTHERAPY; INFLAMMATION MEDIATORS; LUNG NEOPLASMS; MEMBRANE GLYCOPROTEINS; MICE, INBRED C57BL; MICE, TRANSGENIC; MUCIN-1; TH1 CELLS; TIME FACTORS; URETHANE;

EID: 84874797583     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-11-64     Document Type: Article

References (41)

1. Esposito L, Conti D, Ailavajhala R, Khalil N, Giordano A. Lung Cancer: Are we up to the Challenge?. Curr Genomics 2010, 11:513-518. 10.2174/138920210793175903, 3048313, 21532835.
2. Hirschowitz EA, Hiestand DM, Yannelli JR. Vaccines for lung cancer. J Thorac Oncol 2006, 1:93-104. 10.1097/01243894-200601000-00019, 17409835.
3. Nemunaitis J, Murray N. Immune-modulating vaccines in non-small cell lung cancer. J Thorac Oncol 2006, 1:756-761. 10.1097/01243894-200609000-00033, 17409955.
4. Barnd DL, Lan MS, Metzgar RS, Finn OJ. Specific, major histocompatibility complex-unrestricted recognition of tumor-associated mucins by human cytotoxic T cells. Proc Natl Acad Sci U S A 1989, 86:7159-7163. 10.1073/pnas.86.18.7159, 298015, 2674949.
5. Choi C, Witzens M, Bucur M, Feuerer M, Sommerfeldt N, Trojan A, Ho A, Schirrmacher V, Goldschmidt H, Beckhove P. Enrichment of functional CD8 memory T cells specific for MUC1 in bone marrow of patients with multiple myeloma. Blood 2005, 105:2132-2134. 10.1182/blood-2004-01-0366, 15561890.
6. Szabo E. MUC1 expression in lung cancer. Methods Mol Med 2003, 74:251-258.
7. Dong Y, Walsh MD, Cummings MC, Wright RG, Khoo SK, Parsons PG, McGuckin MA. Expression of MUC1 and MUC2 mucins in epithelial ovarian tumours. J Pathol 1997, 183:311-317. 10.1002/(SICI)1096-9896(199711)183:3<311::AID-PATH917>3.0.CO;2-2, 9422987.
8. Gao J, McConnell MJ, Yu B, Li J, Balko JM, Black EP, Johnson JO, Lloyd MC, Altiok S, Haura EB. MUC1 is a downstream target of STAT3 and regulates lung cancer cell survival and invasion. Int J Oncol 2009, 35:337-345.
9. Giatromanolaki A, Koukourakis MI, Sivridis E, O'Byrne K, Cox G, Thorpe PE, Gatter KC, Harris AL. Coexpression of MUC1 glycoprotein with multiple angiogenic factors in non-small cell lung cancer suggests coactivation of angiogenic and migration pathways. Clin Cancer Res 2000, 6:1917-1921.
10. Guddo F, Giatromanolaki A, Koukourakis MI, Reina C, Vignola AM, Chlouverakis G, Hilkens J, Gatter KC, Harris AL, Bonsignore G. MUC1 (episialin) expression in non-small cell lung cancer is independent of EGFR and c-erbB-2 expression and correlates with poor survival in node positive patients. J Clin Pathol 1998, 51:667-671. 10.1136/jcp.51.9.667, 500903, 9930070.
11. Khodarev NN, Pitroda SP, Beckett MA, MacDermed DM, Huang L, Kufe DW, Weichselbaum RR. MUC1-induced transcriptional programs associated with tumorigenesis predict outcome in breast and lung cancer. Cancer Res 2009, 69:2833-2837. 10.1158/0008-5472.CAN-08-4513, 3034477, 19318547.
12. Raina D, Kosugi M, Ahmad R, Panchamoorthy G, Rajabi H, Alam M, Shimamura T, Shapiro GI, Supko J, Kharbanda S, Kufe D. Dependence on the MUC1-C oncoprotein in non-small cell lung cancer cells. Mol Cancer Ther 2011, 10:806-816. 10.1158/1535-7163.MCT-10-1050, 3092019, 21421804.
13. Mehta NR, Wurz GT, Burich RA, Greenberg BE, Griffey S, Gutierrez A, Bell KE, McCall JL, Wolf M, DeGregorio M. L-BLP25 vaccine plus letrozole induces a TH1 immune response and has additive antitumor activity in MUC1-expressing mammary tumors in mice. Clin Cancer Res 2012, 18:2861-2871. 10.1158/1078-0432.CCR-12-0168, 22434666.
14. Sangha R, Butts C. L-BLP25: a peptide vaccine strategy in non small cell lung cancer. Clin Cancer Res 2007, 13:s4652-s4654. 10.1158/1078-0432.CCR-07-0213, 17671159.
15. Salgaller ML. The development of immunotherapies for non-small cell lung cancer. Expert Opin Biol Ther 2002, 2:265-278. 10.1517/14712598.2.3.265, 11890866.
16. Butts C, Maksymiuk A, Goss G, Soulieres D, Marshall E, Cormier Y, Ellis PM, Price A, Sawhney R, Beier F. Updated survival analysis in patients with stage IIIB or IV non-small-cell lung cancer receiving BLP25 liposome vaccine (L-BLP25): phase IIB randomized, multicenter, open-label trial. J Cancer Res Clin Oncol 2011, 137:1337-1342. 10.1007/s00432-011-1003-3, 21744082.
17. Ohyanagi F, Horai T, Sekine I, Yamamoto N, Nakagawa K, Nishio M, Senger S, Morsli N, Tamura T. Safety of BLP25 liposome vaccine (L-BLP25) in Japanese patients with unresectable stage III NSCLC after primary chemoradiotherapy: preliminary results from a Phase I/II study. Jpn J Clin Oncol 2011, 41:718-722. 10.1093/jjco/hyr021, 21393255.
18. Alberti W, Anderson G, Bartolucci A, Bell D, Villalba JB, Brodin O, Cardiello C, Cartei F, Cartei G, Cellerino R. Chemotherapy in Non-Small-Cell Lung-Cancer - a Metaanalysis Using Updated Data on Individual Patients from 52 Randomized Clinical-Trials. Br Med J 1995, 311:899-909.
19. Stearman RS, Dwyer-Nield L, Zerbe L, Blaine SA, Chan Z, Bunn PA, Johnson GL, Hirsch FR, Merrick DT, Franklin WA. Analysis of orthologous gene expression between human pulmonary adenocarcinoma and a carcinogen-induced murine model. Am J Pathol 2005, 167:1763-1775. 10.1016/S0002-9440(10)61257-6, 1613183, 16314486.
20. Sweet-Cordero A, Mukherjee S, Subramanian A, You H, Roix JJ, Ladd-Acosta C, Mesirov J, Golub TR, Jacks T. An oncogenic KRAS2 expression signature identified by cross-species gene-expression analysis. Nat Genet 2005, 37:48-55.
21. Malkinson AM. Primary lung tumors in mice as an aid for understanding, preventing, and treating human adenocarcinoma of the lung. Lung Cancer 2001, 32:265-279. 10.1016/S0169-5002(00)00232-4, 11390008.
22. Rowse GJ, Tempero RM, VanLith ML, Hollingsworth MA, Gendler SJ. Tolerance and immunity to MUC1 in a human MUC1 transgenic murine model. Cancer Res 1998, 58:315-321.
23. Tuveson DA, Jacks T. Modeling human lung cancer in mice: similarities and shortcomings. Oncogene 1999, 18:5318-5324. 10.1038/sj.onc.1203107, 10498884.
24. Miller YE, Dwyer-Nield LD, Keith RL, Le M, Franklin WA, Malkinson AM. Induction of a high incidence of lung tumors in C57BL/6 mice with multiple ethyl carbamate injections. Cancer Lett 2003, 198:139-144. 10.1016/S0304-3835(03)00309-4, 12957351.
25. Jiang YG, Chen JK, Wu ZL. Promotive effect of diethylstilbestrol on urethan-induced mouse lung tumorigenesis. Chemosphere 2000, 41:187-190. 10.1016/S0045-6535(99)00410-5, 10819200.
26. Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J 2008, 22:659-661.
27. Nikitin AY, Alcaraz A, Anver MR, Bronson RT, Cardiff RD, Dixon D, Fraire AE, Gabrielson EW, Gunning WT, Haines DC. Classification of proliferative pulmonary lesions of the mouse: recommendations of the mouse models of human cancers consortium. Cancer Res 2004, 64:2307-2316. 10.1158/0008-5472.CAN-03-3376, 15059877.
28. Dwinell MB, Lugering N, Eckmann L, Kagnoff MF. Regulated production of interferon-inducible T-cell chemoattractants by human intestinal epithelial cells. Gastroenterology 2001, 120:49-59. 10.1053/gast.2001.20914, 11208713.
29. Barbon CM, Yang M, Wands GD, Ramesh R, Slusher BS, Hedley ML, Luby TM. Consecutive low doses of cyclophosphamide preferentially target Tregs and potentiate T cell responses induced by DNA PLG microparticle immunization. Cell Immunol 2010, 262:150-161. 10.1016/j.cellimm.2010.02.007, 20206921.
30. Berd D, Mastrangelo MJ. Effect of low dose cyclophosphamide on the immune system of cancer patients: reduction of T-suppressor function without depletion of the CD8+ subset. Cancer Res 1987, 47:3317-3321.
31. Ercolini AM, Ladle BH, Manning EA, Pfannenstiel LW, Armstrong TD, Machiels JP, Bieler JG, Emens LA, Reilly RT, Jaffee EM. Recruitment of latent pools of high-avidity CD8(+) T cells to the antitumor immune response. J Exp Med 2005, 201:1591-1602. 10.1084/jem.20042167, 2212915, 15883172.
32. Lutsiak ME, Semnani RT, De Pascalis R, Kashmiri SV, Schlom J, Sabzevari H. Inhibition of CD4(+)25+ T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood 2005, 105:2862-2868. 10.1182/blood-2004-06-2410, 15591121.
33. Motoyoshi Y, Kaminoda K, Saitoh O, Hamasaki K, Nakao K, Ishii N, Nagayama Y, Eguchi K. Different mechanisms for anti-tumor effects of low- and high-dose cyclophosphamide. Oncol Rep 2006, 16:141-146.
34. Huyan XH, Lin YP, Gao T, Chen RY, Fan YM. Immunosuppressive effect of cyclophosphamide on white blood cells and lymphocyte subpopulations from peripheral blood of Balb/c mice. Int Immunopharmacol 2011, 11:1293-1297. 10.1016/j.intimp.2011.04.011, 21530682.
35. Malvicini M, Alaniz L, Bayo J, Garcia M, Piccioni F, Fiore E, Atorrasagasti C, Aquino JB, Matar P, Mazzolini G. Single low-dose cyclophosphamide combined with interleukin-12 gene therapy is superior to a metronomic schedule in inducing immunity against colorectal carcinoma in mice. OncoImmunology 2012, 1:1-10. 10.4161/onci.1.1.17645, 3376949, 22720206.
36. Rabinovich GA, Rubinstein N, Matar P, Rozados V, Gervasoni S, Scharovsky GO. The antimetastatic effect of a single low dose of cyclophosphamide involves modulation of galectin-1 and Bcl-2 expression. Cancer Immunol Immunother 2002, 50:597-603. 10.1007/s00262-001-0238-2, 11807623.
37. Mukherjee P, Ginardi AR, Madsen CS, Tinder TL, Jacobs F, Parker J, Agrawal B, Longenecker BM, Gendler SJ. MUC1-specific CTLs are non-functional within a pancreatic tumor microenvironment. Glycoconj J 2001, 18:931-942. 10.1023/A:1022260711583, 12820727.
38. Turner MS, Cohen PA, Finn OJ. Lack of effective MUC1 tumor antigen-specific immunity in MUC1-transgenic mice results from a Th/T regulatory cell imbalance that can be corrected by adoptive transfer of wild-type Th cells. J Immunol 2007, 178:2787-2793.
39. Machiels JP, Reilly RT, Emens LA, Ercolini AM, Lei RY, Weintraub D, Okoye FI, Jaffee EM. Cyclophosphamide, doxorubicin, and paclitaxel enhance the antitumor immune response of granulocyte/macrophage-colony stimulating factor-secreting whole-cell vaccines in HER-2/neu tolerized mice. Cancer Res 2001, 61:3689-3697.
40. Schlom J. Recent advances in therapeutic cancer vaccines. Cancer Biother Radiopharm 2012, 27:2-5. 10.1089/cbr.2012.1200, 3282014, 22251077.
41. DeGregorio M, Wurz GT, Gutierrez A, Wolf M. L-BLP25 vaccine plus letrozole for breast cancer: Is translation possible?. OncoImmunology 2012, 1:1422-1424. 10.4161/onci.21129, 3518524, 23243615.