Exploiting synergy: Immune-based combinations in the treatment of prostate cancer

Frontiers in Oncology

Volumn 4, Issue NOV, 2014, Pages

  Burotto, Mauricio ^a   Singh, Nishith ^b   Heery, Christopher R ^a   Gulley, James L ^a   Madan, Ravi A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b IU Health Arnett Hospital   (United States)

Author keywords

Check point inhibitors; Chemotherapy; Hormonal treatment; Immunotherapy; Prostate cancer; Radiation; Vaccines

Indexed keywords

ANTIANDROGEN; CANCER VACCINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; ENZALUTAMIDE; IMMUNOLOGICAL ADJUVANT; IMMUNOMODULATING AGENT; IPILIMUMAB; PREDNISONE; PROGRAMMED DEATH 1 RECEPTOR; PROSTATE SPECIFIC ANTIGEN; RADIUM CHLORIDE RA 223; RILIMOGENE GALVACIREPVEC; SAMARIUM 153; SIPULEUCEL T; TUMOR ANTIGEN;

ANDROGEN DEPRIVATION THERAPY; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CELL DEATH; CLINICAL TRIAL (TOPIC); HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; MULTICENTER STUDY (TOPIC); NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROSTATE CANCER; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; T LYMPHOCYTE ACTIVATION;

EID: 84915790949     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2014.00351     Document Type: Review

References (94)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA: a cancer journal for clinicians (2014) 64(1):9-29. Epub 2014/01/09. doi: 10.3322/caac.21208. PubMed PMID: 24399786.
2. Madan RA, Arlen PM. Recent advances revolutionize treatment of metastatic prostate cancer. Future Oncol (2013) 9(8):1133-44. Epub 2013/08/02. doi: 10.2217/fon.13.65. PubMed PMID: 23902245.
3. Halabi S, Vogelzang NJ, Kornblith AB, Ou SS, KantoffPW, Dawson NA, et al. Pain predicts overall survival in men with metastatic castration-refractory prostate cancer. Journal of clinical oncology: official journal of the American Society of Clinical Oncology (2008) 26(15):2544-9. Epub 2008/05/20. doi: 10.1200/JCO.2007.15.0367. PubMed PMID: 18487572.
4. Girardi M, Glusac E, Filler RB, Roberts SJ, Propperova I, Lewis J, et al. The distinct contributions of murine T cell receptor (TCR)gammadelta+ and TCRalphabeta+ T cells to different stages of chemically induced skin cancer. The Journal of experimental medicine (2003) 198(5):747-55. Epub 2003/09/04. doi: 10.1084/jem.20021282. PubMed PMID: 12953094; PubMed Central PMCID: PMC2194182.
5. Smyth MJ, Thia KY, Street SE, Cretney E, Trapani JA, Taniguchi M, et al. Differential tumor surveillance by natural killer (NK) and NKT cells. The Journal of experimental medicine (2000) 191(4):661-8. Epub 2000/02/24. PubMed PMID: 10684858; PubMed Central PMCID: PMC2195840.
6. Mellman I, Coukos G, DranoffG. Cancer immunotherapy comes of age. Nature (2011) 480(7378):480-9. Epub 2011/12/24. doi: 10.1038/nature10673. PubMed PMID: 22193102.
7. Andersen MH, Schrama D, Thor Straten P, Becker JC. Cytotoxic T cells. The Journal of investigative dermatology (2006) 126(1):32-41. Epub 2006/01/19. doi: 10.1038/sj.jid.5700001. PubMed PMID: 16417215.
8. Greenwald RJ, Freeman GJ, Sharpe AH. The B7 family revisited. Annual review of immunology (2005) 23:515-48. Epub 2005/03/18. doi: 10.1146/annurev.immunol.23.021704.115611. PubMed PMID: 15771580.
9. Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer immunology, immunotherapy: CII (2009) 58(1):49-59. Epub 2008/05/01. doi: 10.1007/s00262-008-0523-4. PubMed PMID: 18446337; PubMed Central PMCID: PMC3401888.
10. Madan RA, Arlen PM, Mohebtash M, Hodge JW, Gulley JL. Prostvac-VF: a vectorbased vaccine targeting PSA in prostate cancer. Expert opinion on investigational drugs (2009) 18(7):1001-11. Epub 2009/06/25. doi: 10.1517/13543780902997928. PubMed PMID: 19548854; PubMed Central PMCID: PMC3449276.
11. Rini BI. Technology evaluation: APC-8015, Dendreon. Current opinion in molecular therapeutics (2002) 4(1):76-9. Epub 2002/03/09. PubMed PMID: 11883698.
12. Oh S, Terabe M, Pendleton CD, Bhattacharyya A, Bera TK, Epel M, et al. Human CTLs to wild-type and enhanced epitopes of a novel prostate and breast tumor-associated protein, TARP, lyse human breast cancer cells. Cancer research (2004) 64(7):2610-8. Epub 2004/04/03. PubMed PMID: 15059918.
13. KantoffPW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. The New England journal of medicine (2010) 363(5):411-22. Epub 2010/09/08. doi: 10.1056/NEJMoa1001294. PubMed PMID: 20818862.
14. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. The New England journal of medicine (2010) 363(8):711-23. Epub 2010/06/08. doi: 10.1056/NEJMoa1003466. PubMed PMID: 20525992; PubMed Central PMCID: PMC3549297.
15. Small EJ, Fratesi P, Reese DM, Strang G, Laus R, Peshwa MV, et al. Immunotherapy of hormone-refractory prostate cancer with antigen-loaded dendritic cells. Journal of clinical oncology: official journal of the American Society of Clinical Oncology (2000) 18(23):3894-903. Epub 2000/12/01. PubMed PMID: 11099318.
16. Longo DL. New therapies for castration-resistant prostate cancer. The New England journal of medicine (2010) 363(5):479-81. Epub 2010/09/08. doi: 10.1056/NEJMe1006300. PubMed PMID: 20818868.
17. Schlom J, Sabzevari H, Grosenbach DW, Hodge JW. A triad of costimulatory molecules synergize to amplify T-cell activation in both vector-based and vector-infected dendritic cell vaccines. Artificial cells, blood substitutes, and immobilization biotechnology (2003) 31(2):193-228. Epub 2003/05/20. PubMed PMID: 12751840.
18. Arlen PM, Skarupa L, Pazdur M, Seetharam M, Tsang KY, Grosenbach DW, et al. Clinical safety of a viral vector based prostate cancer vaccine strategy. The Journal of urology (2007) 178(4 Pt 1):1515-20. Epub 2007/08/21. doi: 10.1016/j.juro.2007.05.117. PubMed PMID: 17707059.
19. Gulley JL, Arlen PM, Madan RA, Tsang KY, Pazdur MP, Skarupa L, et al. Immunologic and prognostic factors associated with overall survival employing a poxviral-based PSA vaccine in metastatic castrate-resistant prostate cancer. Cancer immunology, immunotherapy: CII (2010) 59(5):663-74. Epub 2009/11/06. doi: 10.1007/s00262-009-0782-8. PubMed PMID: 19890632; PubMed Central PMCID: PMC2832083.
20. KantoffPW, Schuetz TJ, Blumenstein BA, Glode LM, Bilhartz DL, Wyand M, et al. Overall survival analysis of a phase II randomized controlled trial of a Poxviral-based PSAtargeted immunotherapy in metastatic castration-resistant prostate cancer. Journal of clinical oncology: official journal of the American Society of Clinical Oncology (2010) 28(7):1099-105. Epub 2010/01/27. doi: 10.1200/JCO.2009.25.0597. PubMed PMID: 20100959; PubMed Central PMCID: PMC2834462.
21. Egen JG, Kuhns MS, Allison JP. CTLA-4: new insights into its biological function and use in tumor immunotherapy. Nature immunology (2002) 3(7):611-8. Epub 2002/06/28. doi: 10.1038/ni0702-611. PubMed PMID: 12087419.
22. Chambers CA, Sullivan TJ, Allison JP. Lymphoproliferation in CTLA-4-deficient mice is mediated by costimulation-dependent activation of CD4+ T cells. Immunity (1997) 7(6):885-95. Epub 1998/01/16. PubMed PMID: 9430233.
23. Weber JS. Practical management of immune-related adverse events from immune checkpoint protein antibodies for the oncologist. American Society of Clinical Oncology educational book/ASCO American Society of Clinical Oncology Meeting (2012):174-7. Epub 2012/01/01. doi: 10.14694/EdBook_AM.2012.32.174. PubMed PMID: 24451730.
24. Slovin SF, Higano CS, Hamid O, Tejwani S, Harzstark A, Alumkal JJ, et al. Ipilimumab alone or in combination with radiotherapy in metastatic castration-resistant prostate cancer: results from an open-label, multicenter phase I/II study. Annals of oncology: official journal of the European Society for Medical Oncology/ESMO (2013) 24(7):1813-21. Epub 2013/03/29. doi: 10.1093/annonc/mdt107. PubMed PMID: 23535954; PubMed Central PMCID: PMC3707423.
25. Madan RA, Mohebtash M, Arlen PM, Vergati M, Rauckhorst M, Steinberg SM, et al. Ipilimumab and a poxviral vaccine targeting prostate-specific antigen in metastatic castrationresistant prostate cancer: a phase 1 dose-escalation trial. The lancet oncology (2012) 13(5):501-8. Epub 2012/02/14. doi: 10.1016/S1470-2045(12)70006-2. PubMed PMID: 22326924.
26. Small EJ, Tchekmedyian NS, Rini BI, Fong L, Lowy I, Allison JP. A pilot trial of CTLA-4 blockade with human anti-CTLA-4 in patients with hormone-refractory prostate cancer. Clinical cancer research: an official journal of the American Association for Cancer Research (2007) 13(6):1810-5. Epub 2007/03/17. doi: 10.1158/1078-0432.CCR-06-2318. PubMed PMID: 17363537.
27. van den Eertwegh AJ, Versluis J, van den Berg HP, Santegoets SJ, van Moorselaar RJ, van der Sluis TM, et al. Combined immunotherapy with granulocyte-macrophage colonystimulating factor-transduced allogeneic prostate cancer cells and ipilimumab in patients with metastatic castration-resistant prostate cancer: a phase 1 dose-escalation trial. The Lancet Oncology (2012) 13(5):509-17. Epub 2012/02/14. doi: 10.1016/S1470-2045(12)70007-4. PubMed PMID: 22326922.
28. Kwon ED, Drake CG, Scher HI, Fizazi K, Bossi A, van den Eertwegh AJ, et al. Ipilimumab versus placebo after radiotherapy in patients with metastatic castration-resistant prostate cancer that had progressed after docetaxel chemotherapy (CA184-043): a multicentre, randomised, double-blind, phase 3 trial. The lancet oncology (2014) 15(7):700-12. Epub 2014/05/17. doi: 10.1016/S1470-2045(14)70189-5. PubMed PMID: 24831977.
29. Westin JR, Chu F, Zhang M, Fayad LE, Kwak LW, Fowler N, et al. Safety and activity of PD1 blockade by pidilizumab in combination with rituximab in patients with relapsed follicular lymphoma: a single group, open-label, phase 2 trial. The lancet oncology (2014) 15(1):69-77. Epub 2013/12/18. doi: 10.1016/S1470-2045(13)70551-5. PubMed PMID: 24332512; PubMed Central PMCID: PMC3922714.
30. Topalian SL, Sznol M, McDermott DF, Kluger HM, Carvajal RD, Sharfman WH, et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. Journal of clinical oncology: official journal of the American Society of Clinical Oncology (2014) 32(10):1020-30. Epub 2014/03/05. doi: 10.1200/JCO.2013.53.0105. PubMed PMID: 24590637.
31. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nature reviews Cancer (2012) 12(4):252-64. Epub 2012/03/23. doi: 10.1038/nrc3239. PubMed PMID: 22437870.
32. Woo SR, Turnis ME, Goldberg MV, Bankoti J, Selby M, Nirschl CJ, et al. Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T-cell function to promote tumoral immune escape. Cancer research (2012) 72(4):917-27. Epub 2011/12/22. doi: 10.1158/0008-5472.CAN-11-1620. PubMed PMID: 22186141; PubMed Central PMCID: PMC3288154.
33. Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G. Immunological aspects of cancer chemotherapy. Nature reviews Immunology (2008) 8(1):59-73. Epub 2007/12/22. doi: 10.1038/nri2216. PubMed PMID: 18097448.
34. Gallucci S, Matzinger P. Danger signals: SOS to the immune system. Current opinion in immunology (2001) 13(1):114-9. Epub 2001/01/13. PubMed PMID: 11154927.
35. Tesniere A, Panaretakis T, Kepp O, Apetoh L, Ghiringhelli F, Zitvogel L, et al. Molecular characteristics of immunogenic cancer cell death. Cell death and differentiation (2008) 15(1):3-12. Epub 2007/11/17. doi: 10.1038/sj.cdd.4402269. PubMed PMID: 18007663.
36. Bernstein MB, Garnett CT, Zhang H, Velcich A, Wattenberg MM, Gameiro SR, et al. Radiation-induced modulation of costimulatory and coinhibitory T-cell signaling molecules on human prostate carcinoma cells promotes productive antitumor immune interactions. Cancer biotherapy & radiopharmaceuticals (2014) 29(4):153-61. Epub 2014/04/04. doi: 10.1089/cbr.2013.1578. PubMed PMID: 24693958; PubMed Central PMCID: PMC4024843.
37. SharifiN, Gulley JL, Dahut WL. An update on androgen deprivation therapy for prostate cancer. Endocrine-related cancer (2010) 17(4):R305-15. Epub 2010/09/24. doi: 10.1677/ERC-10-0187. PubMed PMID: 20861285; PubMed Central PMCID: PMC3461824.
38. Sutherland JS, Goldberg GL, Hammett MV, Uldrich AP, Berzins SP, Heng TS, et al. Activation of thymic regeneration in mice and humans following androgen blockade. J Immunol (2005) 175(4):2741-53. Epub 2005/08/06. PubMed PMID: 16081852.
39. Roden AC, Moser MT, Tri SD, Mercader M, Kuntz SM, Dong H, et al. Augmentation of T cell levels and responses induced by androgen deprivation. J Immunol (2004) 173(10):6098-108. Epub 2004/11/06. PubMed PMID: 15528346.
40. Drake CG, Doody AD, Mihalyo MA, Huang CT, Kelleher E, Ravi S, et al. Androgen ablation mitigates tolerance to a prostate/prostate cancer-restricted antigen. Cancer cell (2005) 7(3):239-49. Epub 2005/03/16. doi: 10.1016/j.ccr.2005.01.027. PubMed PMID: 15766662; PubMed Central PMCID: PMC2846360.
41. Tang S, Moore ML, Grayson JM, Dubey P. Increased CD8+ T-cell function following castration and immunization is countered by parallel expansion of regulatory T cells. Cancer research (2012) 72(8):1975-85. Epub 2012/03/01. doi: 10.1158/0008-5472.CAN-11-2499. PubMed PMID: 22374980.
42. Akins EJ, Moore ML, Tang S, Willingham MC, Tooze JA, Dubey P. In situ vaccination combined with androgen ablation and regulatory T-cell depletion reduces castration-resistant tumor burden in prostate-specific pten knockout mice. Cancer research (2010) 70(9):3473-82. Epub 2010/04/22. doi: 10.1158/0008-5472.CAN-09-2490. PubMed PMID: 20406970; PubMed Central PMCID: PMC2866496.
43. Beer TM, Armstrong AJ, Rathkopf DE, Loriot Y, Sternberg CN, Higano CS, et al. Enzalutamide in metastatic prostate cancer before chemotherapy. The New England journal of medicine (2014) 371(5):424-33. Epub 2014/06/03. doi: 10.1056/NEJMoa1405095. PubMed PMID: 24881730.
44. Scher HI, Fizazi K, Saad F, Taplin ME, Sternberg CN, Miller K, et al. Increased survival with enzalutamide in prostate cancer after chemotherapy. The New England journal of medicine (2012) 367(13):1187-97. Epub 2012/08/17. doi: 10.1056/NEJMoa1207506. PubMed PMID: 22894553.
45. Ardiani A, Farsaci B, Rogers CJ, Protter A, Guo Z, King TH, et al. Combination therapy with a second-generation androgen receptor antagonist and a metastasis vaccine improves survival in a spontaneous prostate cancer model. Clinical cancer research: an official journal of the American Association for Cancer Research (2013) 19(22):6205-18. Epub 2013/09/21. doi: 10.1158/1078-0432.CCR-13-1026. PubMed PMID: 24048332; PubMed Central PMCID: PMC3833876.
46. Gameiro SR, Jammeh ML, Wattenberg MM, Tsang KY, Ferrone S, Hodge JW. Radiation-induced immunogenic modulation of tumor enhances antigen processing and calreticulin exposure, resulting in enhanced T-cell killing. Oncotarget (2014) 5(2):403-16. Epub 2014/02/01. PubMed PMID: 24480782; PubMed Central PMCID: PMC3964216.
47. Mercader M, Sengupta S, Bodner BK, Manecke RG, Cosar EF, Moser MT, et al. Early effects of pharmacological androgen deprivation in human prostate cancer. BJU international (2007) 99(1):60-7. Epub 2007/01/18. doi: 10.1111/j.1464-410X.2007.06538.x. PubMed PMID: 17227493.
48. Gannon PO, Poisson AO, Delvoye N, Lapointe R, Mes-Masson AM, Saad F. Characterization of the intra-prostatic immune cell infiltration in androgen-deprived prostate cancer patients. Journal of immunological methods (2009) 348(1-2):9-17. Epub 2009/06/26. doi: 10.1016/j.jim.2009.06.004. PubMed PMID: 19552894.
49. Beer TM, Bernstein GT, Corman JM, Glode LM, Hall SJ, Poll WL, et al. Randomized trial of autologous cellular immunotherapy with sipuleucel-T in androgen-dependent prostate cancer. Clinical cancer research: an official journal of the American Association for Cancer Research (2011) 17(13):4558-67. Epub 2011/05/12. doi: 10.1158/1078-0432.CCR-10-3223. PubMed PMID: 21558406.
50. Stein WD, Gulley JL, Schlom J, Madan RA, Dahut W, Figg WD, et al. Tumor regression and growth rates determined in five intramural NCI prostate cancer trials: the growth rate constant as an indicator of therapeutic efficacy. Clinical cancer research: an official journal of the American Association for Cancer Research (2011) 17(4):907-17. Epub 2010/11/26. doi: 10.1158/1078-0432.CCR-10-1762. PubMed PMID: 21106727.
51. Small EJ, Lance RS, Redfer CH, Millard FE, Gardner TA, Karsh LI, et al. A randomized phase II trial of sipuleucel-T with concurrent or sequential abiraterone acetate (AA) plus prednisone (P) in metastatic castrate-resistant prostate cancer (mCRPC). J Clin Oncol 31, 2013 (suppl; abstr 5047).
52. Arlen PM, Gulley JL, Todd N, Lieberman R, Steinberg SM, Morin S, et al. Antiandrogen, vaccine and combination therapy in patients with nonmetastatic hormone refractory prostate cancer. The Journal of urology (2005) 174(2):539-46. Epub 2005/07/12. doi: 10.1097/01.ju.0000165159.33772.5b. PubMed PMID: 16006888.
53. Madan RA, Gulley JL, Schlom J, Steinberg SM, Liewehr DJ, Dahut WL, et al. Analysis of overall survival in patients with nonmetastatic castration-resistant prostate cancer treated with vaccine, nilutamide, and combination therapy. Clinical cancer research: an official journal of the American Association for Cancer Research (2008) 14(14):4526-31. Epub 2008/07/17. doi: 10.1158/1078-0432.CCR-07-5048. PubMed PMID: 18628467; PubMed Central PMCID: PMC2682417.
54. Hodge JW, Ardiani A, Farsaci B, Kwilas AR, Gameiro SR. The tipping point for combination therapy: cancer vaccines with radiation, chemotherapy, or targeted small molecule inhibitors. Seminars in oncology (2012) 39(3):323-39. Epub 2012/05/19. doi: 10.1053/j.seminoncol.2012.02.006. PubMed PMID: 22595055; PubMed Central PMCID: PMC3356994.
55. Hodge JW, Sharp HJ, Gameiro SR. Abscopal regression of antigen disparate tumors by antigen cascade after systemic tumor vaccination in combination with local tumor radiation. Cancer biotherapy & radiopharmaceuticals (2012) 27(1):12-22. Epub 2012/01/31. doi: 10.1089/cbr.2012.1202. PubMed PMID: 22283603; PubMed Central PMCID: PMC3277931.
56. Finkelstein SE, Fishman M. Clinical opportunities in combining immunotherapy with radiation therapy. Frontiers in oncology (2012) 2:169. Epub 2012/12/13. doi: 10.3389/fonc.2012.00169. PubMed PMID: 23233905; PubMed Central PMCID: PMC3515996.
57. Kwilas AR, Donahue RN, Bernstein MB, Hodge JW. In the field: exploiting the untapped potential of immunogenic modulation by radiation in combination with immunotherapy for the treatment of cancer. Frontiers in oncology (2012) 2:104. Epub 2012/09/14. doi: 10.3389/fonc.2012.00104. PubMed PMID: 22973551; PubMed Central PMCID: PMC3434425.
58. Friedman EJ. Immune modulation by ionizing radiation and its implications for cancer immunotherapy. Current pharmaceutical design (2002) 8(19):1765-80. Epub 2002/08/13. PubMed PMID: 12171547.
59. Garnett CT, Palena C, Chakraborty M, Tsang KY, Schlom J, Hodge JW. Sublethal irradiation of human tumor cells modulates phenotype resulting in enhanced killing by cytotoxic T lymphocytes. Cancer research (2004) 64(21):7985-94. Epub 2004/11/03. doi: 10.1158/0008-5472.CAN-04-1525. PubMed PMID: 15520206.
60. Chakraborty M, Abrams SI, Camphausen K, Liu K, Scott T, Coleman CN, et al. Irradiation of tumor cells up-regulates Fas and enhances CTL lytic activity and CTL adoptive immunotherapy. J Immunol (2003) 170(12):6338-47. Epub 2003/06/10. PubMed PMID: 12794167.
61. Hannan R, Zhang H, Wallecha A, Singh R, Liu L, Cohen P, et al. Combined immunotherapy with Listeria monocytogenes-based PSA vaccine and radiation therapy leads to a therapeutic response in a murine model of prostate cancer. Cancer immunology, immunotherapy: CII (2012) 61(12):2227-38. Epub 2012/05/31. doi: 10.1007/s00262-012-1257-x. PubMed PMID: 22644735.
62. Gulley JL, Arlen PM, Bastian A, Morin S, Marte J, Beetham P, et al. Combining a recombinant cancer vaccine with standard definitive radiotherapy in patients with localized prostate cancer. Clinical cancer research: an official journal of the American Association for Cancer Research (2005) 11(9):3353-62. Epub 2005/05/04. doi: 10.1158/1078-0432.CCR-04-2062. PubMed PMID: 15867235.
63. Lechleider RJ, Arlen PM, Tsang KY, Steinberg SM, Yokokawa J, Cereda V, et al. Safety and immunologic response of a viral vaccine to prostate-specific antigen in combination with radiation therapy when metronomic-dose interleukin 2 is used as an adjuvant. Clinical cancer research: an official journal of the American Association for Cancer Research (2008) 14(16):5284-91. Epub 2008/08/14. doi: 10.1158/1078-0432.CCR-07-5162. PubMed PMID: 18698048; PubMed Central PMCID: PMC2639763.
64. Sartor O, Reid RH, Hoskin PJ, Quick DP, Ell PJ, Coleman RE, et al. Samarium-153-Lexidronam complex for treatment of painful bone metastases in hormone-refractory prostate cancer. Urology (2004) 63(5):940-5. Epub 2004/05/12. doi: 10.1016/j.urology.2004.01.034. PubMed PMID: 15134985.
65. Chakraborty M, Wansley EK, Carrasquillo JA, Yu S, Paik CH, Camphausen K, et al. The use of chelated radionuclide (samarium-153-ethylenediaminetetramethylenephosphonate) to modulate phenotype of tumor cells and enhance T cell-mediated killing. Clinical cancer research: an official journal of the American Association for Cancer Research (2008) 14(13):4241-9. Epub 2008/07/03. doi: 10.1158/1078-0432.CCR-08-0335. PubMed PMID: 18594006; PubMed Central PMCID: PMC3407883.
66. Heery CR, Madan RA, Bilusic M, Kim JW, Singh NK, Rauckhorst M, et al. A phase II randomized clinical trial of samarium-153 EDTMP (Sm-153) with or without PSA-tricom vaccine in metastatic castration-resistant prostate cancer (mCRPC) after docetaxel. J Clin Oncol 31, 2013 (suppl 6; abstr 102).
67. Parker C, Nilsson S, Heinrich D, Helle SI, O'Sullivan JM, Fossa SD, et al. Alpha emitter radium-223 and survival in metastatic prostate cancer. The New England journal of medicine (2013) 369(3):213-23. Epub 2013/07/19. doi: 10.1056/NEJMoa1213755. PubMed PMID: 23863050.
68. Gameiro SR, Ardiani A, Kwilas A, Hodge JW. Radiation-induced survival responses promote immunogenic modulation to enhance immunotherapy in combinatorial regimens. Oncoimmunology (2014) 3:e28643. Epub 2014/08/07. doi: 10.4161/onci.28643. PubMed PMID: 25097803; PubMed Central PMCID: PMC4091054.
69. Bertino JR. Chemical action and pharmacology of methotrexate, azathioprine and cyclophosphamide in man. Arthritis and rheumatism (1973) 16(1):79-83. Epub 1973/01/01. PubMed PMID: 4540289.
70. Van den Neste E, Cardoen S, Offner F, Bontemps F. Old and new insights into the mechanisms of action of two nucleoside analogs active in lymphoid malignancies: fludarabine and cladribine (review). International journal of oncology (2005) 27(4):1113-24. Epub 2005/09/06. PubMed PMID: 16142330.
71. 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(7):2862-8. Epub 2004/12/14. doi: 10.1182/blood-2004-06-2410. PubMed PMID: 15591121.
72. North RJ. Cyclophosphamide-facilitated adoptive immunotherapy of an established tumor depends on elimination of tumor-induced suppressor T cells. The Journal of experimental medicine (1982) 155(4):1063-74. Epub 1982/04/01. PubMed PMID: 6460831; PubMed Central PMCID: PMC2186638.
73. Antonarakis ES, Carducci MA. Combining low-dose cyclophosphamide with GM-CSFsecreting prostate cancer immunotherapy enhances antitumor immune effects. Expert opinion on investigational drugs (2010) 19(2):311-4. Epub 2010/01/06. doi: 10.1517/13543780903530678. PubMed PMID: 20047504.
74. Veltman JD, Lambers ME, van Nimwegen M, de Jong S, Hendriks RW, Hoogsteden HC, et al. Low-dose cyclophosphamide synergizes with dendritic cell-based immunotherapy in antitumor activity. Journal of biomedicine & biotechnology (2010) 2010:798467. Epub 2010/05/29. doi: 10.1155/2010/798467. PubMed PMID: 20508851; PubMed Central PMCID: PMC2874992.
75. Kepp O, Galluzzi L, Martins I, Schlemmer F, Adjemian S, Michaud M, et al. Molecular determinants of immunogenic cell death elicited by anticancer chemotherapy. Cancer metastasis reviews (2011) 30(1):61-9. Epub 2011/01/21. doi: 10.1007/s10555-011-9273-4. PubMed PMID: 21249425.
76. Galluzzi L, Senovilla L, Zitvogel L, Kroemer G. The secret ally: immunostimulation by anticancer drugs. Nature reviews Drug discovery (2012) 11(3):215-33. Epub 2012/02/04. doi: 10.1038/nrd3626. PubMed PMID: 22301798.
77. Garnett CT, Schlom J, Hodge JW. Combination of docetaxel and recombinant vaccine enhances T-cell responses and antitumor activity: effects of docetaxel on immune enhancement. Clinical cancer research: an official journal of the American Association for Cancer Research (2008) 14(11):3536-44. Epub 2008/06/04. doi: 10.1158/1078-0432.CCR-07-4025. PubMed PMID: 18519787; PubMed Central PMCID: PMC2682419.
78. Hodge JW, Garnett CT, Farsaci B, Palena C, Tsang KY, Ferrone S, et al. Chemotherapyinduced immunogenic modulation of tumor cells enhances killing by cytotoxic T lymphocytes and is distinct from immunogenic cell death. International journal of cancer Journal international du cancer (2013). Epub 2013/02/01. doi: 10.1002/ijc.28070. PubMed PMID: 23364915.
79. Arlen PM, Gulley JL, Parker C, Skarupa L, Pazdur M, Panicali D, et al. A randomized phase II study of concurrent docetaxel plus vaccine versus vaccine alone in metastatic androgenindependent prostate cancer. Clinical cancer research: an official journal of the American Association for Cancer Research (2006) 12(4):1260-9. Epub 2006/02/21. doi: 10.1158/1078-0432.CCR-05-2059. PubMed PMID: 16489082; PubMed Central PMCID: PMC1526707.
80. Madan RA, Arlen PM, Gulley JL. PANVAC-VF: poxviral-based vaccine therapy targeting CEA and MUC1 in carcinoma. Expert opinion on biological therapy (2007) 7(4):543-54. Epub 2007/03/22. doi: 10.1517/14712598.7.4.543. PubMed PMID: 17373905.
81. Heery CR, Ibrahim NK, Mohebtash M, Madan RA, Arlen PM, Kim JW, et al. A phase 2 randomized trial of docetaxel (DOC) alone or in combination with therapeutic cancer vaccine, CEA-, MUC-1-TRICOM (PANVAC) Cancer research Volume 72, Issue 24, Supplement 3
82. Sweeney CJ. ECOG: CHAARTED--ChemoHormonal therapy versus androgen ablation randomized trial for extensive disease in prostate cancer. Clinical advances in hematology & oncology: H&O (2006) 4(8):588-90. Epub 2006/11/23. PubMed PMID: 17111557.
83. Madan RA, Bilusic M, Heery C, Schlom J, Gulley JL. Clinical evaluation of TRICOM vector therapeutic cancer vaccines. Seminars in oncology (2012) 39(3):296-304. Epub 2012/05/19. doi: 10.1053/j.seminoncol.2012.02.010. PubMed PMID: 22595052; PubMed Central PMCID: PMC3398615.
84. Wada S, Jackson CM, Yoshimura K, Yen HR, Getnet D, Harris TJ, et al. Sequencing CTLA-4 blockade with cell-based immunotherapy for prostate cancer. Journal of translational medicine (2013) 11:89. Epub 2013/04/06. doi: 10.1186/1479-5876-11-89. PubMed PMID: 23557194; PubMed Central PMCID: PMC3666941.
85. Bullock TN, Mullins DW, Colella TA, Engelhard VH. Manipulation of avidity to improve effectiveness of adoptively transferred CD8(+) T cells for melanoma immunotherapy in human MHC class I-transgenic mice. J Immunol (2001) 167(10):5824-31. Epub 2001/11/08. PubMed PMID: 11698456.
86. Hodge JW, Chakraborty M, Kudo-Saito C, Garnett CT, Schlom J. Multiple costimulatory modalities enhance CTL avidity. J Immunol (2005) 174(10):5994-6004. Epub 2005/05/10. PubMed PMID: 15879092; PubMed Central PMCID: PMC1924685.
87. Zeh HJ, 3rd, Perry-Lalley D, Dudley ME, Rosenberg SA, Yang JC. High avidity CTLs for two self-antigens demonstrate superior in vitro and in vivo antitumor efficacy. J Immunol (1999) 162(2):989-94. Epub 1999/01/23. PubMed PMID: 9916724.
88. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. The New England journal of medicine (2012) 366(26):2455-65. Epub 2012/06/05. doi: 10.1056/NEJMoa1200694. PubMed PMID: 22658128; PubMed Central PMCID: PMC3563263.
89. Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity (2013) 39(1):1-10. Epub 2013/07/31. doi: 10.1016/j.immuni.2013.07.012. PubMed PMID: 23890059.
90. Yachida S, Jones S, Bozic I, Antal T, Leary R, Fu B, et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature (2010) 467(7319):1114-7. Epub 2010/10/29. doi: 10.1038/nature09515. PubMed PMID: 20981102; PubMed Central PMCID: PMC3148940.
91. Campbell PJ, Yachida S, Mudie LJ, Stephens PJ, Pleasance ED, Stebbings LA, et al. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature (2010) 467(7319):1109-13. Epub 2010/10/29. doi: 10.1038/nature09460. PubMed PMID: 20981101; PubMed Central PMCID: PMC3137369.
92. Nesslinger NJ, Ng A, Tsang KY, Ferrara T, Schlom J, Gulley JL, et al. A viral vaccine encoding prostate-specific antigen induces antigen spreading to a common set of self-proteins in prostate cancer patients. Clinical cancer research: an official journal of the American Association for Cancer Research (2010) 16(15):4046-56. Epub 2010/06/22. doi: 10.1158/1078-0432.CCR-10-0948. PubMed PMID: 20562209; PubMed Central PMCID: PMC2912964.
93. Disis ML, Goodell V, Schiffman K, Knutson KL. Humoral epitope-spreading following immunization with a HER-2/neu peptide based vaccine in cancer patients. Journal of clinical immunology (2004) 24(5):571-8. Epub 2004/09/11. doi: 10.1023/B:JOCI.0000040928.67495.52. PubMed PMID: 15359116.
94. Gulley JL, Madan RA, Tsang KY, Jochems C, Marte JL, Farsaci B, et al. Immune impact induced by PROSTVAC (PSA-TRICOM), a therapeutic vaccine for prostate cancer. Cancer immunology research (2014) 2(2):133-41. Epub 2014/04/30. doi: 10.1158/2326-6066.CIR-13-0108. PubMed PMID: 24778277; PubMed Central PMCID: PMC4004961.