Cancer-testis antigen, BORIS based vaccine delivered by dendritic cells is extremely effective against a very aggressive and highly metastatic mouse mammary carcinoma

Cellular Immunology

Volumn 270, Issue 2, 2011, Pages 188-197

  Mkrtichyan, Mikayel ^a   Ghochikyan, Anahit ^a   Davtyan, Hayk ^a   Movsesyan, Nina ^b   Loukinov, Dmitry ^c   Lobanenkov, Victor ^c   Cribbs, David H ^b,d   Laust, Amanda K ^b   Nelson, Edward L ^b,d   Agadjanyan, Michael G ^a,b  

^a INSTITUTE FOR MOLECULAR MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

4T1 mammary carcinoma; Brother of regulator of imprinted sites (BORIS); Dendritic cell (DC) based vaccine; Immunotherapy of breast cancer; Myeloid derived suppressor cells (MDSC); Tumor promoting transcription factor

Indexed keywords

BROTHER OF REGULATOR OF IMPRINTED SITE DENDRITIC CELL VACCINE; CANCER TESTIS ANTIGEN; DENDRITIC CELL VACCINE; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CARCINOMA; CANCER IMMUNIZATION; CD4 LYMPHOCYTE COUNT; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CLONOGENESIS; CONTROLLED STUDY; DENDRITIC CELL; EPIGENETICS; IMMUNOGENICITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR LOCALIZATION;

ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; DENDRITIC CELLS; DNA-BINDING PROTEINS; FEMALE; LUNG NEOPLASMS; MALE; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; RECOMBINANT PROTEINS; TESTIS; VACCINATION;

ANIMALIA; MUS;

EID: 80051667961     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2011.05.007     Document Type: Article

References (63)

1. WHO Cancer. Fact sheet No. 297 (2006).
2. Bertucci F., Birnbaum D. Distant metastasis: not out of reach any more. J. Biol. 2009, 8:28.
3. Anderson K.S. Tumor vaccines for breast cancer. Cancer Invest. 2009, 27:361-368.
4. Schadendorf D., Algarra S.M., Bastholt L., Cinat G., Dreno B., et al. Immunotherapy of distant metastatic disease. Ann Oncol 2009, 20(Suppl. 6):vi41-50.
5. Overwijk W.W. Breaking tolerance in cancer immunotherapy: time to ACT. Curr. Opin. Immunol. 2005, 17:187-194.
6. Waldmann T.A. Effective cancer therapy through immunomodulation. Annu. Rev. Med. 2006, 57:65-81.
7. Cunto-Amesty G., Monzavi-Karbassi B., Luo P., Jousheghany F., Kieber-Emmons T. Strategies in cancer vaccines development. Int. J. Parasitol. 2003, 33:597-613.
8. Cheever M.A., Allison J.P., Ferris A.S., Finn O.J., Hastings B.M., et al. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin. Cancer Res. 2009, 15:5323-5337.
9. Cheng F., Gabrilovich D., Sotomayor E.M. Immune tolerance in breast cancer. Breast Dis. 2004, 20:93-103.
10. Smyth M.J., Godfrey D.I., Trapani J.A. A fresh look at tumor immunosurveillance and immunotherapy. Nat. Immunol. 2001, 2:293-299.
11. Makki A., Weidt G., Blachere N.E., Lefrancois L., Srivastava P.K. Immunization against a dominant tumor antigen abrogates immunogenicity of the tumor. Cancer Immun. 2002, 2:4.
12. Scanlan M.J., Simpson A.J., Old L.J. The cancer/testis genes: review, standardization, and commentary. Cancer Immun. 2004, 4:1.
13. Simpson A.J., Caballero O.L., Jungbluth A., Chen Y.T., Old L.J. Cancer/testis antigens, gametogenesis and cancer. Nat. Rev. Cancer 2005, 5:615-625.
14. Davis I.D., Chen W., Jackson H., Parente P., Shackleton M., et al. Recombinant NY-ESO-1 protein with ISCOMATRIX adjuvant induces broad integrated antibody and CD4(+) and CD8(+) T cell responses in humans. Proc. Natl. Acad. Sci. USA 2004, 101:10697-10702.
15. Marchand M., van Baren N., Weynants P., Brichard V., Dreno B., et al. Tumor regressions observed in patients with metastatic melanoma treated with an antigenic peptide encoded by gene MAGE-3 and presented by HLA-A1. Int. J. Cancer 1999, 80:219-230.
16. Klenova E.M., Morse H.C., Ohlsson R., Lobanenkov V.V. The novel BORIS + CTCF gene family is uniquely involved in the epigenetics of normal biology and cancer. Semin. Cancer Biol. 2002, 12:399-414.
17. Loukinov D.I., Pugacheva E., Vatolin S., Pack S.D., Moon H., et al. BORIS, a novel male germ-line-specific protein associated with epigenetic reprogramming events, shares the same 11-zinc-finger domain with CTCF, the insulator protein involved in reading imprinting marks in the soma. Proc. Natl. Acad. Sci. USA 2002, 99:6806-6811.
18. D'Arcy V., Pore N., Docquier F., Abdullaev Z.K., Chernukhin I., et al. BORIS, a paralogue of the transcription factor, CTCF, is aberrantly expressed in breast tumours. Br. J. Cancer 2008, 98:571-579.
19. Hong J.A., Kang Y., Abdullaev Z., Flanagan P.T., Pack S.D., et al. Reciprocal binding of CTCF and BORIS to the NY-ESO-1 promoter coincides with derepression of this cancer-testis gene in lung cancer cells. Cancer Res. 2005, 65:7763-7774.
20. Kouprina N., Noskov V.N., Pavlicek A., Collins N.K., Schoppee Bortz P.D., et al. Evolutionary diversification of SPANX-N sperm protein gene structure and expression. PLoS ONE 2007, 2:e359.
21. Vatolin S., Abdullaev Z., Pack S.D., Flanagan P.T., Custer M., et al. Conditional expression of the CTCF-paralogous transcriptional factor BORIS in normal cells results in demethylation and derepression of MAGE-A1 and reactivation of other cancer-testis genes. Cancer Res. 2005, 65:7751-7762.
22. Woloszynska-Read A., James S.R., Link P.A., Yu J., Odunsi K., et al. DNA methylation-dependent regulation of BORIS/CTCFL expression in ovarian cancer. Cancer Immun. 2007, 7:21.
23. Dougherty C.J., Ichim T.E., Liu L., Reznik G., Min W.P., et al. Selective apoptosis of breast cancer cells by siRNA targeting of BORIS. Biochem. Biophys. Res. Commun. 2008, 370:109-112.
24. Loukinov D., Ghochikyan A., Mkrtichyan M., Ichim T.E., Lobanenkov V.V., et al. Antitumor efficacy of DNA vaccination to the epigenetically acting tumor promoting transcription factor BORIS and CD80 molecular adjuvant. J. Cell Biochem. 2006, 98:1037-1043.
25. Ghochikyan A., Mkrtichyan M., Loukinov D., Mamikonyan G., Pack S.D., et al. Epigenetically acting tumor promoting transcription factor BORIS is widely expressed TAA inducing anti-tumor specific T cell responses. J. Immunol. 2007, 178:556-573.
26. Mkrtichyan M., Ghochikyan A., Loukinov D., Davtyan H., Ichim T.E., et al. DNA, but not protein vaccine based on mutated BORIS antigen significantly inhibits tumor growth and prolongs the survival of mice. Gene Ther. 2008, 15:61-64.
27. Steinman R.M., Banchereau J. Taking dendritic cells into medicine. Nature 2007, 449:419-426.
28. Kaplan J.M., Yu Q., Piraino S.T., Pennington S.E., Shankara S., et al. Induction of antitumor immunity with dendritic cells transduced with adenovirus vector-encoding endogenous tumor-associated antigens. J. Immunol. 1999, 163:699-707.
29. Pulaski B.A., Ostrand-Rosenberg S. Reduction of established spontaneous mammary carcinoma metastases following immunotherapy with major histocompatibility complex class II and B7.1 cell-based tumor vaccines. Cancer Res. 1998, 58:1486-1493.
30. J.E. Coligan, A.M. Kruisbeek, D.H. Margulies, E.M. Shevach, W. Strober, Mouse 4T1 Breast Tumor Model, Current Protocols in Immunology, John Willey and Sons, New York, 2004, pp. 20-22.
31. Pulaski B.A., Terman D.S., Khan S., Muller E., Ostrand-Rosenberg S. Cooperativity of Staphylococcal aureus enterotoxin B superantigen, major histocompatibility complex class II, and CD80 for immunotherapy of advanced spontaneous metastases in a clinically relevant postoperative mouse breast cancer model. Cancer Res. 2000, 60:2710-2715.
32. Schreurs M.W., Eggert A.A., de Boer A.J., Vissers J.L., van Hall T., et al. Dendritic cells break tolerance and induce protective immunity against a melanocyte differentiation antigen in an autologous melanoma model. Cancer Res. 2000, 60:6995-7001.
33. Wang H.Y., Fu T., Wang G., Zeng G., Perry-Lalley D.M., et al. Induction of CD4(+) T cell-dependent antitumor immunity by TAT-mediated tumor antigen delivery into dendritic cells. J. Clin. Invest. 2002, 109:1463-1470.
34. Sun H.X., Xie Y., Ye Y.P. Advances in saponin-based adjuvants. Vaccine 2009, 27:1787-1796.
35. Gabrilovich D.I., Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009, 9:162-174.
36. Hortobagyi G.N. Treatment of breast cancer. N. Engl. J. Med. 1998, 339:974-984.
37. Waeckerle-Men Y., Uetz-von Allmen E., Fopp M., von Moos R., Bohme C., et al. Dendritic cell-based multi-epitope immunotherapy of hormone-refractory prostate carcinoma. Cancer Immunol. Immunother. 2006, 55:1524-1533.
38. Rosenberg S.A., Yang J.C., Restifo N.P. Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 2004, 10:909-915.
39. Palucka K., Ueno H., Fay J., Banchereau J. Harnessing dendritic cells to generate cancer vaccines. Ann. N. Y. Acad. Sci. 2009, 1174:88-98.
40. Melief C.J. Cancer immunotherapy by dendritic cells. Immunity 2008, 29:372-383.
41. Miller B.E., Roi L.D., Howard L.M., Miller F.R. Quantitative selectivity of contact-mediated intercellular communication in a metastatic mouse mammary tumor line. Cancer Res. 1983, 43:4102-4107.
42. Tomin R., Donegan W.L. Screening for recurrent breast cancer-its effectiveness and prognostic value. J. Clin. Oncol. 1987, 5:62-67.
43. Rutgers E.J., van Slooten E.A., Kluck H.M. Follow-up after treatment of primary breast cancer. Br. J. Surg. 1989, 76:187-190.
44. Chen L., Huang T.G., Meseck M., Mandeli J., Fallon J., et al. Rejection of metastatic 4T1 breast cancer by attenuation of Treg cells in combination with immune stimulation. Mol. Ther. 2007, 15:2194-2202.
45. Ostrand-Rosenberg S., Clements V.K., Terabe M., Park J.M., Berzofsky J.A., et al. Resistance to metastatic disease in STAT6-deficient mice requires hemopoietic and nonhemopoietic cells and is IFN-gamma dependent. J. Immunol. 2002, 169:5796-5804.
46. Kim S.H., Castro F., Gonzalez D., Maciag P.C., Paterson Y., et al. Mage-b vaccine delivered by recombinant Listeria monocytogenes is highly effective against breast cancer metastases. Br. J. Cancer 2008, 99:741-749.
47. Smith F.O., Downey S.G., Klapper J.A., Yang J.C., Sherry R.M., et al. Treatment of metastatic melanoma using interleukin-2 alone or in conjunction with vaccines. Clin. Cancer Res. 2008, 14:5610-5618.
48. Marigo I., Dolcetti L., Serafini P., Zanovello P., Bronte V. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol. Rev. 2008, 222:162-179.
49. Darrasse-Jeze G., Bergot A.S., Durgeau A., Billiard F., Salomon B.L., et al. Tumor emergence is sensed by self-specific CD44hi memory Tregs that create a dominant tolerogenic environment for tumors in mice. J. Clin. Invest. 2009, 119:2648-2662.
50. Bunt S.K., Sinha P., Clements V.K., Leips J., Ostrand-Rosenberg S. Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression. J. Immunol. 2006, 176:284-290.
51. Stewart T.J., Greeneltch K.M., Reid J.E., Liewehr D.J., Steinberg S.M., et al. Interferon Regulatory Factor-8 Modulates the Development of Tumor-Induced CD11bGr-1 Myeloid Cells. J. Cell Mol. Med. 2009, 13:3939-3950.
52. Xiang X., Poliakov A., Liu C., Liu Y., Deng Z.B., et al. Induction of myeloid-derived suppressor cells by tumor exosomes. Int. J. Cancer 2009, 124:2621-2633.
53. Ostrand-Rosenberg S., Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J. Immunol. 2009, 182:4499-4506.
54. Peranzoni E., Zilio S., Marigo I., Dolcetti L., Zanovello P., et al. Myeloid-derived suppressor cell heterogeneity and subset definition. Curr. Opin. Immunol. 2010, 22:238-244.
55. Hoechst B., Ormandy L.A., Ballmaier M., Lehner F., Kruger C., et al. A new population of myeloid-derived suppressor cells in hepatocellular carcinoma patients induces CD4(+)CD25(+)Foxp3(+) T cells. Gastroenterology 2008, 135:234-243.
56. Murdoch C., Muthana M., Coffelt S.B., Lewis C.E. The role of myeloid cells in the promotion of tumour angiogenesis. Nat. Rev. Cancer 2008, 8:618-631.
57. Dannull J., Su Z., Rizzieri D., Yang B.K., Coleman D., et al. Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J. Clin. Invest. 2005, 115:3623-3633.
58. Diaz-Montero C.M., Salem M.L., Nishimura M.I., Garrett-Mayer E., Cole D.J., et al. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol. Immunother. 2009, 58:49-59.
59. Ribas A. Anti-CTLA4 antibody clinical trials in melanoma. Update Cancer Ther. 2007, 2:133-139.
60. Audia S., Nicolas A., Cathelin D., Larmonier N., Ferrand C., et al. Increase of CD4+ CD25+ regulatory T cells in the peripheral blood of patients with metastatic carcinoma: a Phase I clinical trial using cyclophosphamide and immunotherapy to eliminate CD4+ CD25+ T lymphocytes. Clin. Exp. Immunol. 2007, 150:523-530.
61. Ozao-Choy J., Ma G., Kao J., Wang G.X., Meseck M., et al. The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune-based cancer therapies. Cancer Res. 2009, 69:2514-2522.
62. Ko J.S., Zea A.H., Rini B.I., Ireland J.L., Elson P., et al. Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin. Cancer Res. 2009, 15:2148-2157.
63. Ghosh I., Kumar L., Seth R., Thavraj V. Sustained remission achieved with ATRA and chemotherapy in second relapse of acute promyelocytic leukemia in Down syndrome. J. Pediatr. Hematol. Oncol. 2009, 31:539-540.