The need for improvement of the treatment of advanced and metastatic cervical cancer, the rationale for combined chemo-immunotherapy

Anti-Cancer Agents in Medicinal Chemistry

Volumn 14, Issue 2, 2014, Pages 190-203

  van Meir, Hélène ^a,b   Kenter, Gemma G ^c   Burggraaf, Jacobus ^b   Kroep, Judith R ^a   Welters, Marij J P ^a   Melief, Cornelis J M ^a,d   van der Burg, Sjoerd H ^a   van Poelgeest, Mariëtte I E ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b CENTRE FOR HUMAN DRUG RESEARCH   (Netherlands)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

^d ISA Pharmaceuticals   (Netherlands)

Author keywords

Anti cancer immunotherapy; Cervical cancer; Chemotherapy; Combined chemo immunotherapy; Immune modulation

Indexed keywords

ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; APOPTOSIS; BIOLOGICAL MARKERS; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; CLINICAL TRIALS AS TOPIC; COMBINED MODALITY THERAPY; FEMALE; HUMANS; IMMUNOTHERAPY; NEOPLASM METASTASIS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS E7 PROTEINS; REPRESSOR PROTEINS; T-LYMPHOCYTES, REGULATORY; UTERINE CERVICAL NEOPLASMS;

EID: 84893434727     PISSN: 18715206     EISSN: 18755992     Source Type: Journal    
DOI: 10.2174/18715206113136660372     Document Type: Review

References (131)

1. Benedet, J. L.; Odicino, F.; Maisonneuve, P.; Beller, U.; Creasman, W. T.; Heintz, A. P.; Ngan, H. Y.; Pecorelli, S. Carcinoma of the cervix uteri. Int. J. Gynaecol. Obstet., 2003, 83(Suppl 1), 41-78.
2. Cadron, I.; Van, G. T.; Amant, F.; Leunen, K.; Neven, P.; Vergote, I. Chemotherapy for recurrent cervical cancer. Gynecol. Oncol., 2007, 107(1 Suppl 1), S113-S118.
3. Monk, B. J.; Tewari, K. S.; Koh, W. J. Multimodality therapy for locally advanced cervical carcinoma: state of the art and future directions. J. Clin. Oncol., 2007, 25(20), 2952-2965.
4. Moore, D. H. Chemotherapy for advanced, recurrent, and metastatic cervical cancer. J. Natl. Compr. Canc. Netw., 2008, 6(1), 53-57.
5. Long, H. J., III; Bundy, B. N.; Grendys, E. C., Jr.; Benda, J. A.; McMeekin, D. S.; Sorosky, J.; Miller, D. S.; Eaton, L. A.; Fiorica, J. V. Randomized phase III trial of cisplatin with or without topotecan in carcinoma of the uterine cervix: a Gynecologic Oncology Group Study. J. Clin. Oncol., 2005, 23(21), 4626-4633.
6. Monk, B. J.; Sill, M. W.; McMeekin, D. S.; Cohn, D. E.; Ramondetta, L. M.; Boardman, C. H.; Benda, J.; Cella, D. Phase III trial of four cisplatin-containing doublet combinations in stage IVB, recurrent, or persistent cervical carcinoma: a Gynecologic Oncology Group study. J. Clin. Oncol., 2009, 27(28), 4649-4655.
7. Moore, D. H.; Blessing, J. A.; McQuellon, R. P.; Thaler, H. T.; Cella, D.; Benda, J.; Miller, D. S.; Olt, G.; King, S.; Boggess, J. F.; Rocereto, T. F. Phase III study of cisplatin with or without paclitaxel in stage IVB, recurrent, or persistent squamous cell carcinoma of the cervix: a gynecologic oncology group study. J. Clin. Oncol., 2004, 22(15), 3113-3119.
8. Monk, B. J.; Willmott, L. J.; Sumner, D. A. Anti-angiogenesis agents in metastatic or recurrent cervical cancer. Gynecol. Oncol., 2010, 116(2), 181-186.
9. Monk, B. J.; Mas, L. L.; Zarba, J. J.; Oaknin, A.; Tarpin, C.; Termrungruanglert, W.; Alber, J. A.; Ding, J.; Stutts, M. W.; Pandite, L. N. Phase II, open-label study of pazopanib or lapatinib monotherapy compared with pazopanib plus lapatinib combination therapy in patients with advanced and recurrent cervical cancer. J. Clin. Oncol., 2010, 28(22), 3562-3569.
10. Bosch, F. X.; Manos, M. M.; Munoz, N.; Sherman, M.; Jansen, A. M.; Peto, J.; Schiffman, M. H.; Moreno, V.; Kurman, R.; Shah, K. V. Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. International biological study on cervical cancer (IBSCC) Study Group. J. Natl. Cancer Inst., 1995, 87(11), 796-802.
11. Van der Burg, S. H.; Melief, C. J. Therapeutic vaccination against human papilloma virus induced malignancies. Curr. Opin. Immunol., 2011, 23(2), 252-257.
12. De, J. A.; Van der Burg, S. H.; Kwappenberg, K. M.; Van Der Hulst, J. M.; Franken, K. L.; Geluk, A.; Van Meijgaarden, K. E.; Drijfhout, J. W.; Kenter, G.; Vermeij, P.; Melief, C. J.; Offringa, R. Frequent detection of human papillomavirus 16 E2-specific T-helper immunity in healthy subjects. Cancer Res., 2002, 62(2), 472-479.
13. Welters, M. J.; De, J. A.; Van den Eeden, S. J.; Van der Hulst, J. M.; Kwappenberg, K. M.; Hassane, S.; Franken, K. L.; Drijfhout, J. W.; Fleuren, G. J.; Kenter, G.; Melief, C. J.; Offringa, R.; Van der Burg, S. H. Frequent display of human papillomavirus type 16 E6-specific memory t-Helper cells in the healthy population as witness of previous viral encounter. Cancer Res., 2003, 63(3), 636-641.
14. Bavinck, J. N.; Berkhout, R. J. HPV infections and immunosuppression. Clin Dermatol., 1997, 15(3), 427-437.
15. Jordanova, E. S.; Gorter, A.; Ayachi, O.; Prins, F.; Durrant, L. G.; Kenter, G. G.; Van der Burg, S. H.; Fleuren, G. J. Human leukocyte antigen class I, MHC class I chain-related molecule A, and CD8+/regulatory T-cell ratio: which variable determines survival of cervical cancer patients? Clin. Cancer Res., 2008, 14(7), 2028-2035.
16. van der Burg, S. H.; Piersma, S. J.; de, J. A.; van der Hulst, J. M.; Kwappenberg, K. M.; Van den Hende, M.; Welters, M. J.; Van Rood, J. J.; Fleuren, G. J.; Melief, C. J.; Kenter, G. G.; Offringa, R. Association of cervical cancer with the presence of CD4+ regulatory T cells specific for human papillomavirus antigens. Proc. Natl. Acad. Sci. USA, 2007, 104(29), 12087-12092.
17. Van der Burg, S. H.; Melief, C. J. Therapeutic vaccination against human papilloma virus induced malignancies. Curr. Opin. Immunol., 2011, 23(2), 252-257.
18. Mellman, I.; Coukos, G.; Dranoff, G. Cancer immunotherapy comes of age. Nature, 2011, 480 (7378), 480-489.
19. Monk, B. J.; Sill, M. W.; Burger, R. A.; Gray, H. J.; Buekers, T. E.; Roman, L. D. Phase II trial of bevacizumab in the treatment of persistent or recurrent squamous cell carcinoma of the cervix: a gynecologic oncology group study. J. Clin. Oncol., 2009, 27(7), 1069-1074.
20. Wright, J. D.; Viviano, D.; Powell, M. A.; Gibb, R. K.; Mutch, D. G.; Grigsby, P. W.; Rader, J. S. Bevacizumab combination therapy in heavily pretreated, recurrent cervical cancer. Gynecol. Oncol., 2006, 103(2), 489-493.
21. Heiss, M. M.; Murawa, P.; Koralewski, P.; Kutarska, E.; Kolesnik, O. O.; Ivanchenko, V. V.; Dudnichenko, A. S.; Aleknaviciene, B.; Razbadauskas, A.; Gore, M.; Ganea-Motan, E.; Ciuleanu, T.; Wimberger, P.; Schmittel, A.; Schmalfeldt, B.; Burges, A.; Bokemeyer, C.; Lindhofer, H.; Lahr, A.; Parsons, S. L. The trifunctional antibody catumaxomab for the treatment of malignant ascites due to epithelial cancer: Results of a prospective randomized phase II/III trial. Int. J. Cancer, 2010, 127(9), 2209-2221.
22. Culver, M. E.; Gatesman, M. L.; Mancl, E. E.; Lowe, D. K. Ipilimumab: a novel treatment for metastatic melanoma. Ann. Pharmacother., 2011, 45(4), 510-519.
23. Verdegaal, E. M.; Visser, M.; Ramwadhdoebe, T. H.; Van der Minne, C. E.; Van Steijn, J. A.; Kapiteijn, E.; Haanen, J. B.; Van der Burg, S. H.; Nortier, J. W.; Osanto, S. Successful treatment of metastatic melanoma by adoptive transfer of blood-derived polyclonal tumor-specific CD4+ and CD8+ T cells in combination with low-dose interferon-alpha. Cancer Immunol. Immunother., 2011, 60(7), 953-963.
24. Kantoff, P. W.; Higano, C. S.; Shore, N. D.; Berger, E. R.; Small, E. J.; Penson, D. F.; Redfern, C. H.; Ferrari, A. C.; Dreicer, R.; Sims, R. B.; Xu, Y.; Frohlich, M. W.; Schellhammer, P. F. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N. Engl. J Med., 2010, 363(5), 411-422.
25. Melief, C. J. Cancer immunotherapy by dendritic cells. Immunity, 2008, 29(3), 372-383.
26. Ernstoff, M. S.; Crocenzi, T. S.; Seigne, J. D.; Crosby, N. A.; Cole, B. F.; Fisher, J. L.; Uhlenhake, J. C.; Mellinger, D.; Foster, C.; Farnham, C. J.; Mackay, K.; Szczepiorkowski, Z. M.; Webber, S. M.; Schned, A. R.; Harris, R. D.; Barth, R. J., Jr.; Heaney, J. A.; Noelle, R. J. Developing a rational tumor vaccine therapy for renal cell carcinoma: immune yin and yang. Clin Cancer Res., 2007, 13(2 Pt 2), 733s-740s.
27. Van der Burg, S. H.; Arens, R.; Melief, C. J. Immunotherapy for persistent viral infections and associated disease. Trends Immunol., 2011, 32(3), 97-103.
28. Welters, M. J.; De Jong, A.; Van den Eeden, S. J.; Van der Hulst, J. M.; Kwappenberg, K. M.; Hassane, S.; Franken, K. L.; Drijfhout, J. W.; Fleuren, G. J.; Kenter, G.; Melief, C. J.; Offringa, R.; Van der Burg, S. H. Frequent display of human papillomavirus type 16 E6-specific memory t-Helper cells in the healthy population as witness of previous viral encounter. Cancer Res., 2003, 63(3), 636-641.
29. De Jong, A.; van Poelgeest, M. I.; Van der Hulst, J. M.; Drijfhout, J. W.; Fleuren, G. J.; Melief, C. J.; Kenter, G.; Offringa, R.; Van der Burg, S. H. Human papillomavirus type 16-positive cervical cancer is associated with impaired CD4+ T-cell immunity against early antigens E2 and E6. Cancer Res., 2004, 64 (15), 5449-5455.
30. Melief, C. J.; Van der Burg, S. H. Immunotherapy of established (pre)malignant disease by synthetic long peptide vaccines. Nat. Rev. Cancer, 2008, 8(5), 351-360.
31. Zitvogel, L.; Apetoh, L.; Ghiringhelli, F.; Kroemer, G. Immunological aspects of cancer chemotherapy. Nat. Rev Immunol., 2008, 8(1), 59-73.
32. Lutsiak, M. E.; Semnani, R. T.; De Pascalis, P. R.; Kashmiri, S. V.; 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), 2862-2868.
33. Head, J. F.; Elliott, R. L.; McCoy, J. L. Evaluation of lymphocyte immunity in breast cancer patients. Breast. Cancer Res. Treat., 1993, 26(1), 77-88.
34. Menard, C.; Martin, F.; Apetoh, L.; Bouyer, F.; Ghiringhelli, F. Cancer chemotherapy: not only a direct cytotoxic effect, but also an adjuvant for antitumor immunity. Cancer Immunol. Immunother., 2008, 57(11), 1579-1587.
35. Head, J. F.; Elliott, R. L.; McCoy, J. L. Evaluation of lymphocyte immunity in breast cancer patients. Breast. Cancer Res Treat., 1993, 26(1), 77-88.
36. Andersen, M. H.; Sorensen, R. B.; Schrama, D.; Svane, I. M.; Becker, J. C.; Thor, S. P. Cancer treatment: the combination of vaccination with other therapies. Cancer Immunol. Immunother., 2008, 57(11), 1735-1743.
37. Liu, J. Y.; Wu, Y.; Zhang, X. S.; Yang, J. L.; Li, H. L.; Mao, Y. Q.; Wang, Y.; Cheng, X.; Li, Y. Q.; Xia, J. C.; Masucci, M.; Zeng, Y. X. Single administration of low dose cyclophosphamide augments the antitumor effect of dendritic cell vaccine. Cancer Immunol. Immunother., 2007, 56(10), 1597-1604.
38. Lutsiak, M. E.; Semnani, R. T.; De Pascalis, R.; Kashmiri, S. V.; 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), 2862-2868.
39. Panaretakis, T.; Kepp, O.; Brockmeier, U.; Tesniere, A.; Bjorklund, A. C.; Chapman, D. C.; Durchschlag, M.; Joza, N.; Pierron, G.; Van, E. P.; Yuan, J.; Zitvogel, L.; Madeo, F.; Williams, D. B.; Kroemer, G. Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO. J., 2009, 28(5), 578-590.
40. Apetoh, L.; Ghiringhelli, F.; Tesniere, A.; Obeid, M.; Ortiz, C.; Criollo, A.; Mignot, G.; Maiuri, M. C.; Ullrich, E.; Saulnier, P.; Yang, H.; Amigorena, S.; Ryffel, B.; Barrat, F. J.; Saftig, P.; Levi, F.; Lidereau, R.; Nogues, C.; Mira, J. P.; Chompret, A.; Joulin, V.; Clavel-Chapelon, F.; Bourhis, J.; Andre, F.; Delaloge, S.; Tursz, T.; Kroemer, G.; Zitvogel, L. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med., 2007, 13(9), 1050-1059.
41. Casares, N.; Pequignot, M. O.; Tesniere, A.; Ghiringhelli, F.; Roux, S.; Chaput, N.; Schmitt, E.; Hamai, A.; Hervas-Stubbs, S.; Obeid, M.; Coutant, F.; Metivier, D.; Pichard, E.; Aucouturier, P.; Pierron, G.; Garrido, C.; Zitvogel, L.; Kroemer, G. Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J. Exp. Med., 2005, 202(12), 1691-1701.
42. Apetoh, L.; Ghiringhelli, F.; Tesniere, A.; Criollo, A.; Ortiz, C.; Lidereau, R.; Mariette, C.; Chaput, N.; Mira, J. P.; Delaloge, S.; Andre, F.; Tursz, T.; Kroemer, G.; Zitvogel, L. The interaction between HMGB1 and TLR4 dictates the outcome of anticancer chemotherapy and radiotherapy. Immunol. Rev., 2007, 220, 47-59.
43. Kelland, L. R. Of mice and men: values and liabilities of the athymic nude mouse model in anticancer drug development. Eur. J Cancer, 2004, 40(6), 827-836.
44. Van der Most, R. G.; Currie, A. J.; Cleaver, A. L.; Salmons, J.; Nowak, A. K.; Mahendran, S.; Larma, I.; Prosser, A.; Robinson, B. W.; Smyth, M. J.; Scalzo, A. A.; Degli-Esposti, M. A.; Lake, R. A. Cyclophosphamide chemotherapy sensitizes tumor cells to TRAILdependent CD8 T cell-mediated immune attack resulting in suppression of tumor growth. PLoS One, 2009, 4(9), e6982.
45. Raulet, D. H.; Guerra, N. Oncogenic stress sensed by the immune system: role of natural killer cell receptors. Nat. Rev. Immunol., 2009, 9(8), 568-580.
46. Scheffer, S. R.; Nave, H.; Korangy, F.; Schlote, K.; Pabst, R.; Jaffee, E. M.; Manns, M. P.; Greten, T. F. Apoptotic, but not necrotic, tumor cell vaccines induce a potent immune response in vivo. Int. J. Cancer, 2003, 103(2), 205-211.
47. Zhang, T.; Herlyn, D. Combination of active specific immunotherapy or adoptive antibody or lymphocyte immunotherapy with chemotherapy in the treatment of cancer. Cancer Immunol. Immunother., 2009, 58(4), 475-492.
48. Gardai, S. J.; McPhillips, K. A.; Frasch, S. C.; Janssen, W. J.; Starefeldt, A.; Murphy-Ullrich, J. E.; Bratton, D. L.; Oldenborg, P. A.; Michalak, M.; Henson, P. M. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell, 2005, 123(2), 321-334.
49. Aymeric, L.; Apetoh, L.; Ghiringhelli, F.; Tesniere, A.; Martins, I.; Kroemer, G.; Smyth, M. J.; Zitvogel, L. Tumor cell death and ATP release prime dendritic cells and efficient anticancer immunity. Cancer Res., 2010, 70 (3), 855-858.
50. Martins, I.; Tesniere, A.; Kepp, O.; Michaud, M.; Schlemmer, F.; Senovilla, L.; Seror, C.; Metivier, D.; Perfettini, J. L.; Zitvogel, L.; Kroemer, G. Chemotherapy induces ATP release from tumor cells. Cell Cycle, 2009, 8 (22), 3723-3728.
51. Zitvogel, L.; Kepp, O.; Kroemer, G. Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat Rev Clin Oncol., 2011, 8(3), 151-160.
52. Van der Most, R. G.; Currie, A. J.; Robinson, B. W.; Lake, R. A. Decoding dangerous death: how cytotoxic chemotherapy invokes inflammation, immunity or nothing at all. Cell Death Differ., 2008, 15(1), 13-20.
53. Gasser, S.; Orsulic, S.; Brown, E. J.; Raulet, D. H. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature, 2005, 436(7054), 1186-1190.
54. Lesterhuis, W. J.; Punt, C. J.; Hato, S. V.; Eleveld-Trancikova, D.; Jansen, B. J.; Nierkens, S.; Schreibelt, G.; De Boer, A.; Van Herpen, C. M.; Kaanders, J. H.; Van Krieken, J. H.; Adema, G. J.; Figdor, C. G.; de Vries, I. J. Platinum-based drugs disrupt STAT6-mediated suppression of immune responses against cancer in humans and mice. J. Clin. Invest., 2011, 121(8), 3100-3108.
55. Keir, M. E.; Butte, M. J.; Freeman, G. J.; Sharpe, A. H. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol., 2008, 26, 677-704.
56. Iwai, Y.; Ishida, M.; Tanaka, Y.; Okazaki, T.; Honjo, T.; Minato, N. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc Natl. Acad. Sci USA, 2002, 99(19), 12293-12297.
57. Ramakrishnan, R.; Assudani, D.; Nagaraj, S.; Hunter, T.; Cho, H. I.; Antonia, S.; Altiok, S.; Celis, E.; Gabrilovich, D. I. Chemotherapy enhances tumor cell susceptibility to CTL-mediated killing during cancer immunotherapy in mice. J. Clin. Invest., 2010, 120(4), 1111-1124.
58. Sutton, V. R.; Davis, J. E.; Cancilla, M.; Johnstone, R. W.; Ruefli, A. A.; Sedelies, K.; Browne, K. A.; Trapani, J. A. Initiation of apoptosis by granzyme B requires direct cleavage of bid, but not direct granzyme B-mediated caspase activation. J. Exp. Med., 2000, 192(10), 1403-1414.
59. Ramakrishnan, R.; Assudani, D.; Nagaraj, S.; Hunter, T.; Cho, H. I.; Antonia, S.; Altiok, S.; Celis, E.; Gabrilovich, D. I. Chemotherapy enhances tumor cell susceptibility to CTL-mediated killing during cancer immunotherapy in mice. J. Clin. Invest., 2010, 120(4), 1111-1124.
60. Eralp, Y.; Wang, X.; Wang, J. P.; Maughan, M. F.; Polo, J. M.; Lachman, L. B. Doxorubicin and paclitaxel enhance the antitumor efficacy of vaccines directed against HER 2/neu in a murine mammary carcinoma model. Breast Cancer Res., 2004, 6(4), R275-R283.
61. Song, C. K.; Han, H. D.; Noh, K. H.; Kang, T. H.; Park, Y. S.; Kim, J. H.; Park, E. S.; Shin, B. C.; Kim, TW. Chemotherapy enhances CD8(+) T cell-mediated antitumor immunity induced by vaccination with vaccinia virus. Mol. Ther., 2007, 15(8), 1558-1563.
62. Tan, G. H.; Tian, L.; Wei, Y. Q.; Zhao, X.; Li, J.; Wu, Y.; Wen, Y. J.; Yi, T.; Ding, Z. Y.; Kan, B.; Mao, Y. Q.; Deng, H. X.; Li, H. L.; Zou, C. H.; Fu, C. H. Combination of low-dose cisplatin and recombinant xenogeneic endoglin as a vaccine induces synergistic antitumor activities. Int. J. Cancer, 2004, 112(4), 701-706.
63. Bae, S. H.; Park, Y. J.; Park, J. B.; Choi, Y. S.; Kim, M. S.; Sin, J. I. Therapeutic synergy of human papillomavirus E7 subunit vaccines plus cisplatin in an animal tumor model: causal involvement of increased sensitivity of cisplatin-treated tumors to CTL-mediated killing in therapeutic synergy. Clin. Cancer Res., 2007, 13(1), 341-349.
64. Tseng, C. W.; Hung, C. F.; Alvarez, R. D.; Trimble, C.; Huh, W. K.; Kim, D.; Chuang, C. M.; Lin, C. T.; Tsai, Y. C.; He, L.; Monie, A.; Wu, T. C. Pretreatment with cisplatin enhances E7-specific CD8+ T-Cell-mediated antitumor immunity induced by DNA vaccination. Clin. Cancer Res., 2008, 14 (10), 3185-3192.
65. Machiels, J. P.; Reilly, R. T.; Emens, L. A.; Ercolini, A. M.; Lei, R. Y.; Weintraub, D.; Okoye, F. I.; Jaffee, E. M. Cyclophosphamide, doxorubicin, and paclitaxel enhance the antitumor immune response of granulocyte/macrophage-colony stimulating factorsecreting whole-cell vaccines in HER-2/neu tolerized mice. Cancer Res., 2001, 61(9), 3689-3697.
66. De Souza, A. P.; Bonorino, C. Tumor immunosuppressive environment: Effects on tumor-specific and nontumor antigen immune responses. Exp. Rev. Anticancer Ther., 2009, 9(9), 1317-1332.
67. Ghiringhelli, F.; Menard, C.; Puig, P. E.; Ladoire, S.; Roux, S.; Martin, F.; Solary, E.; Le, C. A.; Zitvogel, L.; Chauffert, B. Metronomic cyclophosphamide regimen selectively depletes CD4+CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol. Immunother., 2007, 56(5), 641-648.
68. Suzuki, E.; Kapoor, V.; Jassar, A. S.; Kaiser, L. R.; Albelda, S. M. Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin. Cancer Res., 2005, 11(18), 6713-6721.
69. Vincent, J.; Mignot, G.; Chalmin, F.; Ladoire, S.; Bruchard, M.; Chevriaux, A.; Martin, F.; Apetoh, L.; Rebe, C.; Ghiringhelli, F. 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res., 2010, 70(8), 3052-3061.
70. Lutsiak, M. E.; Semnani, R. T.; De, P. R.; Kashmiri, S. V.; 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), 2862-2868.
71. Colombo, M. P.; Piconese, S. Regulatory-T-cell inhibition versus depletion: the right choice in cancer immunotherapy. Nat. Rev. Cancer, 2007, 7(11), 880-887.
72. Battaglia, A.; Buzzonetti, A.; Monego, G.; Peri, L.; Ferrandina, G.; Fanfani, F.; Scambia, G.; Fattorossi, A. Neuropilin-1 expression identifies a subset of regulatory T cells in human lymph nodes that is modulated by preoperative chemoradiation therapy in cervical cancer. Immunology, 2008, 123(1), 129-138.
73. Fattorossi, A.; Battaglia, A.; Ferrandina, G.; Coronetta, F.; Legge, F.; Salutari, V.; Scambia, G. Neoadjuvant therapy changes the lymphocyte composition of tumor-draining lymph nodes in cervical carcinoma. Cancer, 2004, 100(7), 1418-1428.
74. Zhu, Y.; Liu, N.; Xiong, S. D.; Zheng, Y. J.; Chu, Y. W. CD4+Foxp3+ regulatory T-cell impairment by paclitaxel is independent of toll-like receptor 4. Scand. J. Immunol., 2011, 73(4), 301-308.
75. Carson, W. E., III; Shapiro, C. L.; Crespin, T. R.; Thornton, L. M.; Andersen, B. L. Cellular immunity in breast cancer patients completing taxane treatment. Clin. Cancer Res., 2004, 10(10), 3401-3409.
76. Vierboom, M. P.; Bos, G. M.; Ooms, M.; Offringa, R.; Melief, C. J. Cyclophosphamide enhances anti-tumor effect of wild-type p53-specific CTL. Int. J. Cancer, 2000, 87(2), 253-260.
77. Ember, I.; Kiss, I.; Vermes, E. Early effect of cyclophosphamide on oncogene expression in vivo. In Vivo, 1998, 12 (2), 201-207.
78. Zhang, B.; Bowerman, N. A.; Salama, J. K.; Schmidt, H.; Spiotto, M. T.; Schietinger, A.; Yu, P.; Fu, Y. X.; Weichselbaum, R. R.; Rowley, D. A.; Kranz, D. M.; Schreiber, H. Induced sensitization of tumor stroma leads to eradication of established cancer by T cells. J. Exp. Med., 2007, 204(1), 49-55.
79. Bracci, L.; Moschella, F.; Sestili, P.; La, S., V; Valentini, M.; Canini, I.; Baccarini, S.; Maccari, S.; Ramoni, C.; Belardelli, F.; Proietti, E. Cyclophosphamide enhances the antitumor efficacy of adoptively transferred immune cells through the induction of cytokine expression, B-cell and T-cell homeostatic proliferation, and specific tumor infiltration. Clin. Cancer Res., 2007, 13(2 Pt 1), 644-653.
80. Masters, G. R.; Berger, M. A.; Albone, E. F. Synergistic effects of combined therapy using paclitaxel and [90Y-DOTA]776. 1 on growth of OVCAR-3 ovarian carcinoma xenografts. Gynecol. Oncol., 2006, 102 (3), 462-467.
81. Kievit, E.; Pinedo, H. M.; Schluper, H. M.; Boven, E. Addition of cisplatin improves efficacy of 131I-labeled monoclonal antibody 323/A3 in experimental human ovarian cancer. Int. J. Radiat. Oncol. Biol Phys., 1997, 38 (2), 419-428.
82. DeNardo, S. J.; Kukis, D. L.; Kroger, L. A.; O'Donnell, R. T.; Lamborn, K. R.; Miers, L. A.; DeNardo, D. G.; Meares, C. F.; DeNardo, G. L. Synergy of Taxol and radioimmunotherapy with yttrium-90-labeled chimeric L6 antibody: efficacy and toxicity in breast cancer xenografts. Proc Natl. Acad. Sci. USA, 1997, 94(8), 4000-4004.
83. Baselga, J.; Norton, L.; Albanell, J.; Kim, Y. M.; Mendelsohn, J. Recombinant humanized anti-HER2 antibody (Herceptin) enhances the antitumor activity of paclitaxel and doxorubicin against HER2/neu overexpressing human breast cancer xenografts. Cancer Res., 1998, 58(13), 2825-2831.
84. Weiner, L. M.; Surana, R.; Wang, S. Monoclonal antibodies: versatile platforms for cancer immunotherapy. Nat. Rev. Immunol., 2010, 10(5), 317-327.
85. Adams, G. P.; Weiner, L. M. Monoclonal antibody therapy of cancer. Nat. Biotechnol., 2005, 23(9), 1147-1157.
86. Miller, K.; Wang, M.; Gralow, J.; Dickler, M.; Cobleigh, M.; Perez, E. A.; Shenkier, T.; Cella, D.; Davidson, N. E. Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer. N. Engl. J. Med., 2007, 357(26), 2666-2676.
87. Burger, R. A.; Brady, M. F.; Bookman, M. A.; Fleming, G. F.; Monk, B. J.; Huang, H.; Mannel, R. S.; Homesley, H. D.; Fowler, J.; Greer, B. E.; Boente, M.; Birrer, M. J.; Liang, S. X. Incorporation of bevacizumab in the primary treatment of ovarian cancer. N. Engl. J. Med., 2011, 365(26), 2473-2483.
88. Perren, T. J.; Swart, A. M.; Pfisterer, J.; Ledermann, J. A.; Pujade-Lauraine, E.; Kristensen, G.; Carey, M. S.; Beale, P.; Cervantes, A.; Kurzeder, C.; Du, B. A.; Sehouli, J.; Kimmig, R.; Stahle, A.; Collinson, F.; Essapen, S.; Gourley, C.; Lortholary, A.; Selle, F.; Mirza, M. R.; Leminen, A.; Plante, M.; Stark, D.; Qian, W.; Parmar, M. K.; Oza, A. M. A phase 3 trial of bevacizumab in ovarian cancer. N. Engl. J. Med., 2011, 365(26), 2484-2496.
89. Hurwitz, H.; Fehrenbacher, L.; Novotny, W.; Cartwright, T.; Hainsworth, J.; Heim, W.; Berlin, J.; Baron, A.; Griffing, S.; Holmgren, E.; Ferrara, N.; Fyfe, G.; Rogers, B.; Ross, R.; Kabbinavar, F. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N. Engl. J. Med., 2004, 350(23), 2335-2342.
90. Slamon, D. J.; Leyland-Jones, B.; Shak, S.; Fuchs, H.; Paton, V.; Bajamonde, A.; Fleming, T.; Eiermann, W.; Wolter, J.; Pegram, M.; Baselga, J.; Norton, L. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N. Engl. J. Med., 2001, 344 (11), 783-792.
91. Romond, E. H.; Perez, E. A.; Bryant, J.; Suman, V. J.; Geyer, C. E., Jr.; Davidson, N. E.; Tan-Chiu, E.; Martino, S.; Paik, S.; Kaufman, P. A.; Swain, S. M.; Pisansky, T. M.; Fehrenbacher, L.; Kutteh, L. A.; Vogel, V. G.; Visscher, D. W.; Yothers, G.; Jenkins, R. B.; Brown, A. M.; Dakhil, S. R.; Mamounas, E. P.; Lingle, W. L.; Klein, P. M.; Ingle, J. N.; Wolmark, N. Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N. Engl. J. Med., 2005, 353(16), 1673-1684.
92. Sato, Y.; Fujiwara, T.; Mine, T.; Shomura, H.; Homma, S.; Maeda, Y.; Tokunaga, N.; Ikeda, Y.; Ishihara, Y.; Yamada, A.; Tanaka, N.; Itoh, K.; Harada, M.; Todo, S. Immunological evaluation of personalized peptide vaccination in combination with a 5-fluorouracil derivative (TS-1) for advanced gastric or colorectal carcinoma patients. Cancer Sci., 2007, 98 (7), 1113-1119.
93. Quoix, E.; Ramlau, R.; Westeel, V.; Papai, Z.; Madroszyk, A.; Riviere, A.; Koralewski, P.; Breton, J. L.; Stoelben, E.; Braun, D.; Debieuvre, D.; Lena, H.; Buyse, M.; Chenard, M. P.; Acres, B.; Lacoste, G.; Bastien, B.; Tavernaro, A.; Bizouarne, N.; Bonnefoy, J. Y.; Limacher, J. M. Therapeutic vaccination with TG4010 and first-line chemotherapy in advanced non-small-cell lung cancer: a controlled phase 2B trial. Lancet Oncol., 2011, 12(12), 1125-1133.
94. Yanagimoto, H.; Mine, T.; Yamamoto, K.; Satoi, S.; Terakawa, N.; Takahashi, K.; Nakahara, K.; Honma, S.; Tanaka, M.; Mizoguchi, J.; Yamada, A.; Oka, M.; Kamiyama, Y.; Itoh, K.; Takai, S. Immunological evaluation of personalized peptide vaccination with gemcitabine for pancreatic cancer. Cancer Sci., 2007, 98(4), 605-611.
95. Wheeler, C. J.; Das, A.; Liu, G.; Yu, J. S.; Black, K. L. Clinical responsiveness of glioblastoma multiforme to chemotherapy after vaccination. Clin. Cancer Res., 2004, 10(16), 5316-5326.
96. Antonia, S. J.; Mirza, N.; Fricke, I.; Chiappori, A.; Thompson, P.; Williams, N.; Bepler, G.; Simon, G.; Janssen, W.; Lee, J. H.; Menander, K.; Chada, S.; Gabrilovich, D. I. Combination of p53 cancer vaccine with chemotherapy in patients with extensive stage small cell lung cancer. Clin. Cancer Res., 2006, 12(3 Pt 1), 878-887.
97. Arlen, P. M.; Gulley, J. L.; Parker, C.; Skarupa, L.; Pazdur, M.; Panicali, D.; Beetham, P.; Tsang, K. Y.; Grosenbach, D. W.; Feldman, J.; Steinberg, S. M.; Jones, E.; Chen, C.; Marte, J.; Schlom, J.; Dahut, W. A randomized phase II study of concurrent docetaxel plus vaccine versus vaccine alone in metastatic androgen-independent prostate cancer. Clin. Cancer Res., 2006, 12(4), 1260-1269.
98. Gribben, J. G.; Ryan, D. P.; Boyajian, R.; Urban, R. G.; Hedley, M. L.; Beach, K.; Nealon, P.; Matulonis, U.; Campos, S.; Gilligan, T. D.; Richardson, P. G.; Marshall, B.; Neuberg, D.; Nadler, L. M. Unexpected association between induction of immunity to the universal tumor antigen CYP1B1 and response to next therapy. Clin. Cancer Res., 2005, 11(12), 4430-4436.
99. Noguchi, M.; Kakuma, T.; Uemura, H.; Nasu, Y.; Kumon, H.; Hirao, Y.; Moriya, F.; Suekane, S.; Matsuoka, K.; Komatsu, N.; Shichijo, S.; Yamada, A.; Itoh, K. A randomized phase II trial of personalized peptide vaccine plus low dose estramustine phosphate (EMP) versus standard dose EMP in patients with castration resistant prostate cancer. Cancer Immunol. Immunother., 2010, 59(7), 1001-1009.
100. Hoos, A.; Eggermont, A. M.; Janetzki, S.; Hodi, F. S.; Ibrahim, R.; Anderson, A.; Humphrey, R.; Blumenstein, B.; Old, L.; Wolchok, J. Improved endpoints for cancer immunotherapy trials. J. Natl. Cancer Inst., 2010, 102(18), 1388-1397.
101. Zitvogel, L.; Kepp, O.; Kroemer, G. Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat. Rev. Clin. Oncol., 2011, 8(3), 151-160.
102. Taylor, C.; Hershman, D.; Shah, N.; Suciu-Foca, N.; Petrylak, D. P.; Taub, R.; Vahdat, L.; Cheng, B.; Pegram, M.; Knutson, K. L.; Clynes, R. Augmented HER-2 specific immunity during treatment with trastuzumab and chemotherapy. Clin. Cancer Res., 2007, 13(17), 5133-5143.
103. Nistico, P.; Capone, I.; Palermo, B.; Del, B. D.; Ferraresi, V.; Moschella, F.; Arico, E.; Valentini, M.; Bracci, L.; Cognetti, F.; Ciccarese, M.; Vercillo, G.; Roselli, M.; Fossile, E.; Tosti, M. E.; Wang, E.; Marincola, F.; Imberti, L.; Catricala, C.; Natali, P. G.; Belardelli, F.; Proietti, E. Chemotherapy enhances vaccine-induced antitumor immunity in melanoma patients. Int. J. Cancer, 2009, 124(1), 130-139.
104. Lesterhuis, W. J.; De Vries, I. J.; Aarntzen, E. A.; De Boer, A.; Scharenborg, N. M.; Van de Rakt, M.; Van Spronsen, D. J.; Preijers, F. W.; Figdor, C. G.; Adema, G. J.; Punt, C. J. A pilot study on the immunogenicity of dendritic cell vaccination during adjuvant oxaliplatin/capecitabine chemotherapy in colon cancer patients. Br. J. Cancer, 2010, 103(9), 1415-1421.
105. Apetoh, L.; Ghiringhelli, F.; Tesniere, A.; Obeid, M.; Ortiz, C.; Criollo, A.; Mignot, G.; Maiuri, M. C.; Ullrich, E.; Saulnier, P.; Yang, H.; Amigorena, S.; Ryffel, B.; Barrat, F. J.; Saftig, P.; Levi, F.; Lidereau, R.; Nogues, C.; Mira, J. P.; Chompret, A.; Joulin, V.; Clavel-Chapelon, F.; Bourhis, J.; Andre, F.; Delaloge, S.; Tursz, T.; Kroemer, G.; Zitvogel, L. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med., 2007, 13(9), 1050-1059.
106. Ghiringhelli, F.; Apetoh, L.; Tesniere, A.; Aymeric, L.; Ma, Y.; Ortiz, C.; Vermaelen, K.; Panaretakis, T.; Mignot, G.; Ullrich, E.; Perfettini, J. L.; Schlemmer, F.; Tasdemir, E.; Uhl, M.; Genin, P.; Civas, A.; Ryffel, B.; Kanellopoulos, J.; Tschopp, J.; Andre, F.; Lidereau, R.; McLaughlin, N. M.; Haynes, N. M.; Smyth, M. J.; Kroemer, G.; Zitvogel, L. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat. Med., 2009, 15(10), 1170-1178.
107. Tesniere, A.; Schlemmer, F.; Boige, V.; Kepp, O.; Martins, I.; Ghiringhelli, F.; Aymeric, L.; Michaud, M.; Apetoh, L.; Barault, L.; Mendiboure, J.; Pignon, J. P.; Jooste, V.; Van Endert, P.; Ducreux, M.; Zitvogel, L.; Piard, F.; Kroemer, G. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene, 2010, 29(4), 482-491.
108. Vermeij, R.; Leffers, N.; Hoogeboom, B. N.; Hamming, I. L.; Wolf, R.; Reyners, A. K.; Molmans, B. H.; Hollema, H.; Bart, J.; Drijfhout, J. W.; Oostendorp, J.; Van der Zee, A. G.; Melief, C. J.; Van der Burg, S. H.; Daemen, T.; Nijman, H. W. Potentiation of a p53-SLP vaccine by cyclophosphamide in ovarian cancer, a single arm phase II study. Int. J. Cancer, 2012, 131(5), E670-E680.
109. Leffers, N.; Lambeck, A. J.; Gooden, M. J.; Hoogeboom, B. N.; Wolf, R.; Hamming, I. E.; Hepkema, B. G.; Willemse, P. H.; Molmans, B. H.; Hollema, H.; Drijfhout, J. W.; Sluiter, W. J.; Valentijn, A. R.; Fathers, L. M.; Oostendorp, J.; Van der Zee, A. G.; Melief, C. J.; Van der Burg, S. H.; Daemen, T.; Nijman, H. W. Immunization with a P53 synthetic long peptide vaccine induces P53-specific immune responses in ovarian cancer patients, a phase II trial. Int. J. Cancer, 2009, 125(9), 2104-2113.
110. Audia, S.; Nicolas, A.; Cathelin, D.; Larmonier, N.; Ferrand, C.; Foucher, P.; Fanton, A.; Bergoin, E.; Maynadie, M.; Arnould, L.; Bateman, A.; Lorcerie, B.; Solary, E.; Chauffert, B.; Bonnotte, B. 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(3), 523-530.
111. Hoon, D. S.; Foshag, L. J.; Nizze, A. S.; Bohman, R.; Morton, D. L. Suppressor cell activity in a randomized trial of patients receiving active specific immunotherapy with melanoma cell vaccine and low dosages of cyclophosphamide. Cancer Res., 1990, 50(17), 5358-5364.
112. Schiavoni, G.; Mattei, F.; Di Pucchio, T.; Santini, S. M.; Bracci, L.; Belardelli, F.; Proietti, E. Cyclophosphamide induces type I interferon and augments the number of CD44(hi) T lymphocytes in mice: implications for strategies of chemoimmunotherapy of cancer. Blood, 2000, 95(6), 2024-2030.
113. Laheru, D.; Lutz, E.; Burke, J.; Biedrzycki, B.; Solt, S.; Onners, B.; Tartakovsky, I.; Nemunaitis, J.; Le, D.; Sugar, E.; Hege, K.; Jaffee, E. Allogeneic granulocyte macrophage colony-stimulating factorsecreting tumor immunotherapy alone or in sequence with cyclophosphamide for metastatic pancreatic cancer: a pilot study of safety, feasibility, and immune activation. Clin. Cancer Res., 2008, 14(5), 1455-1463.
114. Reck, M.; Bondarenko, I.; Luft, A.; Serwatowski, P.; Barlesi, F.; Chacko, R.; Sebastian, M.; Lu, H.; Cuillerot, J. M.; Lynch, T. J. Ipilimumab in combination with paclitaxel and carboplatin as firstline therapy in extensive-disease-small-cell lung cancer: results from a randomized, double-blind, multicenter phase 2 trial. Ann. Oncol., 2013, 24(1), 75-83.
115. Gabrilovich, D. I. Combination of chemotherapy and immunotherapy for cancer: a paradigm revisited. Lancet Oncol., 2007, 8(1), 2-3.
116. Yanagimoto, H.; Shiomi, H.; Satoi, S.; Mine, T.; Toyokawa, H.; Yamamoto, T.; Tani, T.; Yamada, A.; Kwon, A. H.; Komatsu, N.; Itoh, K.; Noguchi, M. A phase II study of personalized peptide vaccination combined with gemcitabine for non-resectable pancreatic cancer patients. Oncol. Rep., 2010, 24(3), 795-801.
117. Robert, C.; Thomas, L.; Bondarenko, I.; O'Day, S.; M D. J. W.; Garbe, C.; Lebbe, C.; Baurain, J. F.; Testori, A.; Grob, J. J.; Davidson, N.; Richards, J.; Maio, M.; Hauschild, A.; Miller, W. H., Jr.; Gascon, P.; Lotem, M.; Harmankaya, K.; Ibrahim, R.; Francis, S.; Chen, T. T.; Humphrey, R.; Hoos, A.; Wolchok, J. D. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N. Engl. J. Med., 2011, 364(26), 2517-2526.
118. Eckardt, J. R. Emerging role of weekly topotecan in recurrent small cell lung cancer. Oncologist, 2004, 9(Suppl 6), 25-32.
119. Maecker, B.; Sherr, D. H.; Vonderheide, R. H.; Von Bergwelt-Baildon, M. S.; Hirano, N.; Anderson, K. S.; Xia, Z.; Butler, M. O.; Wucherpfennig, K. W.; O'Hara, C.; Cole, G.; Kwak, S. S.; Ramstedt, U.; Tomlinson, A. J.; Chicz, R. M.; Nadler, L. M.; Schultze, J. L. The shared tumor-associated antigen cytochrome P450 1B1 is recognized by specific cytotoxic T cells. Blood, 2003, 102(9), 3287-3294.
120. Cella, D.; Huang, H. Q.; Monk, B. J.; Wenzel, L.; Benda, J.; McMeekin, D. S.; Cohn, D.; Ramondetta, L.; Boardman, C. H. Health-related quality of life outcomes associated with four cisplatin-based doublet chemotherapy regimens for stage IVB recurrent or persistent cervical cancer: a Gynecologic Oncology Group study. Gynecol. Oncol., 2010, 119(3), 531-537.
121. Moore, K. N.; Herzog, T. J.; Lewin, S.; Giuntoli, R. L.; Armstrong, D. K.; Rocconi, R. P.; Spannuth, W. A.; Gold, M. A. A comparison of cisplatin/paclitaxel and carboplatin/paclitaxel in stage IVB, recurrent or persistent cervical cancer. Gynecol. Oncol., 2007, 105(2), 299-303.
122. Saito, I.; Kitagawa, R.; Fukuda, H.; Shibata, T.; Katsumata, N.; Konishi, I.; Yoshikawa, H.; Kamura, T. A phase III trial of paclitaxel plus carboplatin versus paclitaxel plus cisplatin in stage IVB, persistent or recurrent cervical cancer: Gynecologic Cancer Study Group/Japan Clinical Oncology Group Study (JCOG0505). Jpn. J. Clin Oncol., 2010, 40 (1), 90-93.
123. Bellati, F.; Napoletano, C.; Gasparri, M. L.; Visconti, V.; Zizzari, I. G.; Ruscito, I.; Caccetta, J.; Rughetti, A.; Benedetti-Panici, P.; Nuti, M. Monoclonal antibodies in gynecological cancer: a critical point of view. Clin. Dev. Immunol., 2011, 2011, 890758.
124. Kenter, G. G.; Welters, M. J.; Valentijn, A. R.; Lowik, M. J.; Berends-van der Meer, D. M.; Vloon, A. P.; Drijfhout, J. W.; Wafelman, A. R.; Oostendorp, J.; Fleuren, G. J.; Offringa, R.; Van der Burg, S. H.; Melief, C. J. Phase I immunotherapeutic trial with long peptides spanning the E6 and E7 sequences of high-risk human papillomavirus 16 in end-stage cervical cancer patients shows low toxicity and robust immunogenicity. Clin. Cancer Res., 2008, 14(1), 169-177.
125. Welters, M. J.; Filippov, D. V.; Van den Eeden, S. J.; Franken, K. L.; Nouta, J.; Valentijn, A. R.; Van der Marel, G. A.; Overkleeft, H. S.; Lipford, G.; Offringa, R.; Melief, C. J.; Van Boom, J. H.; Van der Burg, S. H.; Drijfhout, J. W. Chemically synthesized protein as tumour-specific vaccine: immunogenicity and efficacy of synthetic HPV16 E7 in the TC-1 mouse tumour model. Vaccine, 2004, 23(3), 305-311.
126. Kenter, G. G.; Welters, M. J.; Valentijn, A. R.; Lowik, M. J.; Berends-van der Meer, D. M.; Vloon, A. P.; Essahsah, F.; Fathers, L. M.; Offringa, R.; Drijfhout, J. W.; Wafelman, A. R.; Oostendorp, J.; Fleuren, G. J.; Van der Burg, S. H.; Melief, C. J. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N. Engl. J. Med., 2009, 361(19), 1838-1847.
127. Welters, M. J.; Kenter, G. G.; De Vos van Steenwijk PJ; Lowik, M. J.; Berends-van der Meer, D. M; Essahsah, F.; Stynenbosch, L. F.; Vloon, A. P.; Ramwadhdoebe, T. H.; Piersma, S. J.; Van der Hulst, J. M.; Valentijn, A. R.; Fathers, L. M.; Drijfhout, J. W.; Franken, K. L.; Oostendorp, J.; Fleuren, G. J.; Melief, C. J.; Van der Burg, S. H. Success or failure of vaccination for HPV16-positive vulvar lesions correlates with kinetics and phenotype of induced T-cell responses. Proc Natl. Acad. Sci USA, 2010, 107(26), 11895-11899.
128. Welters, M. J.; Kenter, G. G.; Piersma, S. J.; Vloon, A. P.; Lowik, M. J.; Der Meer DM; Drijfhout, J. W.; Valentijn, A. R.; Wafelman, A. R.; Oostendorp, J.; Fleuren, G. J.; Offringa, R.; Melief, C. J.; Van der Burg, S. H. Induction of tumor-specific CD4+ and CD8+ T-cell immunity in cervical cancer patients by a human papillomavirus type 16 E6 and E7 long peptides vaccine. Clin. Cancer Res., 2008, 14(1), 178-187.
129. Van der Burg, S. H.; Melief, C. J. Therapeutic vaccination against human papilloma virus induced malignancies. Curr. Opin. Immunol., 2011, 23(2), 252-257.
130. Fox, B. A.; Schendel, D. J.; Butterfield, L. H.; Aamdal, S.; Allison, J. P.; Ascierto, P. A.; Atkins, M. B.; Bartunkova, J.; Bergmann, L.; Berinstein, N.; Bonorino, C. C.; Borden, E.; Bramson, J. L.; Britten, C. M.; Cao, X.; Carson, W. E.; Chang, A. E.; Characiejus, D.; Choudhury, A. R.; Coukos, G.; De, Gruijl, T.; Dillman, R. O.; Dolstra, H.; Dranoff, G.; Durrant, L. G.; Finke, J. H.; Galon, J.; Gollob, J. A.; Gouttefangeas, C.; Grizzi, F.; Guida, M.; Hakansson, L.; Hege, K.; Herberman, R. B.; Hodi, F. S.; Hoos, A.; Huber, C.; Hwu, P.; Imai, K.; Jaffee, E. M.; Janetzki, S.; June, C. H.; Kalinski, P.; Kaufman, H. L.; Kawakami, K.; Kawakami, Y.; Keilholtz, U.; Khleif, S. N.; Kiessling, R.; Kotlan, B.; Kroemer, G.; Lapointe, R.; Levitsky, H. I.; Lotze, M. T.; Maccalli, C.; Maio, M.; Marschner, J. P.; Mastrangelo, M. J.; Masucci, G.; Melero, I.; Nelief, C.; Murphy, W. J.; Nelson, B.; Nicolini, A.; Nishimura, M. I.; Odunsi, K.; Ohashi, P. S.; O'Donnell-Tormey, J.; Old, L. J.; Ottensmeier, C.; Papamichail, M.; Parmiani, G.; Pawelec, G.; Proietti, E.; Qin, S.; Rees, R.; Ribas, A.; Ridolfi, R.; Ritter, G.; Rivoltini, L.; Romero, P. J.; Salem, M. L.; Scheper, R. J.; Seliger, B.; Sharma, P.; Shiku, H.; Singh-Jasuja, H.; Song, W.; Straten, P. T.; Tahara, H.; Tian, Z.; Van Der Burg, S. H.; von, H. P.; Wang, E.; Welters, M. J.; Winter, H.; Withington, T.; Wolchok, J. D.; Xiao, W.; Zitvogel, L.; Zwierzina, H.; Marincola, F. M.; Gajewski, T. F.; Wigginton, J. M.; Disis, M. L. Defining the critical hurdles in cancer immunotherapy. J. Transl. Med., 2011, 9(1), 214.
131. Hoos, A.; Parmiani, G.; Hege, K.; Sznol, M.; Loibner, H.; Eggermont, A.; Urba, W.; Blumenstein, B.; Sacks, N.; Keilholz, U.; Nichol, G. A clinical development paradigm for cancer vaccines and related biologics. J. Immunother., 2007, 30(1), 1-15.