Therapeutic cancer vaccines in prostate cancer: The quest for intermediate markers of response

Cancers

Volumn 4, Issue 4, 2012, Pages 1229-1246

  Kim, Joseph W ^a   Bilusic, Marijo ^a   Heery, Christopher J ^a   Madan, Ravi A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Immune assay; Surrogate marker; Tumor growth rate; Tumor infiltrating lymphocytes

Indexed keywords

BIOLOGICAL MARKER; CANCER VACCINE; CYTOKINE; DENDRITIC CELL VACCINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN; PLACEBO; PROSTATE SPECIFIC ANTIGEN; SIPULEUCEL T; TRANSCRIPTION FACTOR FOXP3;

ADVANCED CANCER; ANTIBODY TITER; ANTIGEN EXPRESSION; CANCER ADJUVANT THERAPY; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER MORTALITY; CANCER PREVENTION; CANCER SURVIVAL; CASTRATION RESISTANT PROSTATE CANCER; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL INFILTRATION; CLINICAL EFFECTIVENESS; CLINICAL PRACTICE; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DOSE RESPONSE; DRUG EFFECT; DRUG MEGADOSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GROWTH RATE; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOASSAY; IMMUNOCOMPETENT CELL; IMMUNOSUPPRESSIVE TREATMENT; LOW DRUG DOSE; LYMPHOCYTE PROLIFERATION; MELANOMA; METASTASIS; OVERALL SURVIVAL; PATIENT ASSESSMENT; PROSTATE CANCER; REVIEW; SOLID TUMOR; TUMOR GROWTH; TUMOR IMMUNITY;

EID: 84871566470     PISSN: None     EISSN: 20726694     Source Type: Journal    
DOI: 10.3390/cancers4041229     Document Type: Review

References (82)

1. 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. et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N. Engl. J. Med. 2010, 363, 411-422.
2. Hodi, F.S.; O'Day, S.J.; McDermott, D.F.; Weber, R.W.; Sosman, J.A.; Haanen, J.B.; Gonzalez, R.; Robert, C.; Schadendorf, D.; Hassel, J.C. et al. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 2010, 363, 711-723.
3. Kantoff, P.W.; Schuetz, T.J.; Blumenstein, B.A.; Glode, L.M.; Bilhartz, D.L.; Wyand, M.; Manson, K.; Panicali, D.L.; Laus, R.; Schlom, J. et al. Overall survival analysis of a phase II randomized controlled trial of a Poxviral-based PSA-targeted immunotherapy in metastatic castration-resistant prostate cancer. J. Clin. Oncol. 2010, 28, 1099-1105.
4. Madan, R.A.; Gulley, J.L.; Fojo, T.; Dahut, W.L. Therapeutic cancer vaccines in prostate cancer: the paradox of improved survival without changes in time to progression. Oncologist 2010, 15, 969-975.
5. Cher, D.J.; Mosmann, T.R. Two types of murine helper T cell clone. II. Delayed-type hypersensitivity is mediated by TH1 clones. J. Immunol. 1987, 138, 3688-3694.
6. Aarntzen, E.H.; Figdor, C.G.; Adema, G.J.; Punt, C.J.; de Vries, I.J. Dendritic cell vaccination and immune monitoring. Cancer Immunol. Immunother. 2008, 57, 1559-1568.
7. Disis, M.L.; Schiffman, K.; Gooley, T.A.; McNeel, D.G.; Rinn, K.; Knutson, K.L. Delayed-type hypersensitivity response is a predictor of peripheral blood T-cell immunity after HER-2/neu peptide immunization. Clin. Cancer Res. 2000, 6, 1347-1350.
8. Nestle, F.O.; Alijagic, S.; Gilliet, M.; Sun, Y.; Grabbe, S.; Dummer, R.; Burg, G.; Schadendorf, D. Vaccination of melanoma patients with peptideor tumor lysate-pulsed dendritic cells. Nat. Med. 1998, 4, 328-332.
9. Thomas-Kaskel, A.K.; Zeiser, R.; Jochim, R.; Robbel, C.; Schultze-Seemann, W.; Waller, C.F.; Veelken, H. Vaccination of advanced prostate cancer patients with PSCA and PSA peptide-loaded dendritic cells induces DTH responses that correlate with superior overall survival. Int. J. Cancer 2006, 119, 2428-2434.
10. Thurner, B.; Haendle, I.; Roder, C.; Dieckmann, D.; Keikavoussi, P.; Jonuleit, H.; Bender, A.; Maczek, C.; Schreiner, D.; von den Driesch, P. et al. Vaccination with mage-3A1 peptide-pulsed mature, monocyte-derived dendritic cells expands specific cytotoxic T cells and induces regression of some metastases in advanced stage IV melanoma. J. Exp. Med. 1999, 190, 1669-1678.
11. Morse, M.A.; Deng, Y.; Coleman, D.; Hull, S.; Kitrell-Fisher, E.; Nair, S.; Schlom, J.; Ryback, M.E.; Lyerly, H.K. A Phase I study of active immunotherapy with carcinoembryonic antigen peptide (CAP-1)-pulsed, autologous human cultured dendritic cells in patients with metastatic malignancies expressing carcinoembryonic antigen. Clin. Cancer Res. 1999, 5, 1331-1338.
12. Perambakam, S.; Hallmeyer, S.; Reddy, S.; Mahmud, N.; Bressler, L.; DeChristopher, P.; Mahmud, D.; Nunez, R.; Sosman, J.A.; Peace, D.J. Induction of specific T cell immunity in patients with prostate cancer by vaccination with PSA146-154 peptide. Cancer Immunol. Immunother. 2006, 55, 1033-1042.
13. Lopez, M.N.; Pereda, C.; Segal, G.; Munoz, L.; Aguilera, R.; Gonzalez, F.E.; Escobar, A.; Ginesta, A.; Reyes, D.; Gonzalez, R. et al. Prolonged survival of dendritic cell-vaccinated melanoma patients correlates with tumor-specific delayed type IV hypersensitivity response and reduction of tumor growth factor beta-expressing T cells. J. Clin. Oncol. 2009, 27, 945-952.
14. Altman, J.D.; Moss, P.A.; Goulder, P.J.; Barouch, D.H.; McHeyzer-Williams, M.G.; Bell, J.I.; McMichael, A.J.; Davis, M.M. Phenotypic analysis of antigen-specific T lymphocytes. Science 1996, 274, 94-96.
15. Hampl, J.; Chien, Y.H.; Davis, M.M. CD4 augments the response of a T cell to agonist but not to antagonist ligands. Immunity 1997, 7, 379-385.
16. Krogsgaard, M.; Li, Q.J.; Sumen, C.; Huppa, J.B.; Huse, M.; Davis, M.M. Agonist/endogenous peptide-MHC heterodimers drive T cell activation and sensitivity. Nature 2005, 434, 238-243.
17. Cochran, J.R.; Cameron, T.O.; Stern, L.J. The relationship of MHC-peptide binding and T cell activation probed using chemically defined MHC class II oligomers. Immunity 2000, 12, 241-250.
18. Konig, R.; Shen, X.; Germain, R.N. Involvement of both major histocompatibility complex class II alpha and beta chains in CD4 function indicates a role for ordered oligomerization in T cell activation. J. Exp. Med. 1995, 182, 779-787.
19. Barnes, E.; Ward, S.M.; Kasprowicz, V.O.; Dusheiko, G.; Klenerman, P.; Lucas, M. Ultra-sensitive class I tetramer analysis reveals previously undetectable populations of antiviral CD8+ T cells. Eur. J. Immunol. 2004, 34, 1570-1577.
20. Perambakam, S.; Xie, H.; Edassery, S.; Peace, D.J. Long-term follow-up of HLA-A2+ patients with high-risk, hormone-sensitive prostate cancer vaccinated with the prostate specific antigen peptide homologue (PSA146-154). Clin. Dev. Immunol. 2010, 2010, 473453.
21. Scher, H.I.; Eisenberger, M.; D'Amico, A.V.; Halabi, S.; Small, E.J.; Morris, M.; Kattan, M.W.; Roach, M.; Kantoff, P.; Pienta, K.J. et al. Eligibility and outcomes reporting guidelines for clinical trials for patients in the state of a rising prostate-specific antigen: Recommendations from the Prostate-Specific Antigen Working Group. J. Clin. Oncol. 2004, 22, 537-556.
22. Weber, J.S.; Vogelzang, N.J.; Ernstoff, M.S.; Goodman, O.B.; Cranmer, L.D.; Marshall, J.L.; Miles, S.; Rosario, D.; Diamond, D.C.; Qiu, Z. et al. A phase 1 study of a vaccine targeting preferentially expressed antigen in melanoma and prostate-specific membrane antigen in patients with advanced solid tumors. J. Immunother. 2011, 34, 556-567.
23. Dangoor, A.; Lorigan, P.; Keilholz, U.; Schadendorf, D.; Harris, A.; Ottensmeier, C.; Smyth, J.; Hoffmann, K.; Anderson, R.; Cripps, M. et al. Clinical and immunological responses in metastatic melanoma patients vaccinated with a high-dose poly-epitope vaccine. Cancer Immunol. Immunother. 2010, 59, 863-873.
24. Froebel, K.S.; Pakker, N.G.; Aiuti, F.; Bofill, M.; Choremi-Papadopoulou, H.; Economidou, J.; Rabian, C.; Roos, M.T.; Ryder, L.P.; Miedema, F. et al. Standardisation and quality assurance of lymphocyte proliferation assays for use in the assessment of immune function. European Concerted Action on Immunological and Virological Markers of HIV Disease Progression. J. Immunol. Methods 1999, 227, 85-97.
25. Beer, T.M.; Bernstein, G.T.; Corman, J.M.; Glode, L.M.; Hall, S.J.; Poll, W.L.; Schellhammer, P.F.; Jones, L.A.; Xu, Y.; Kylstra, J.W. et al. Randomized trial of autologous cellular immunotherapy with sipuleucel-T in androgen-dependent prostate cancer. Clin. Cancer Res. 2011, 17, 4558-4567.
26. Johnson, L.E.; Frye, T.P.; Arnot, A.R.; Marquette, C.; Couture, L.A.; Gendron-Fitzpatrick, A.; McNeel, D.G. Safety and immunological efficacy of a prostate cancer plasmid DNA vaccine encoding prostatic acid phosphatase (PAP). Vaccine 2006, 24, 293-303.
27. McNeel, D.G.; Dunphy, E.J.; Davies, J.G.; Frye, T.P.; Johnson, L.E.; Staab, M.J.; Horvath, D.L.; Straus, J.; Alberti, D.; Marnocha, R. et al. Safety and immunological efficacy of a DNA vaccine encoding prostatic acid phosphatase in patients with stage D0 prostate cancer. J. Clin. Oncol. 2009, 27, 4047-4054.
28. Sheikh, N.A.; Petrylak, D.; Kantoff, P.W.; Dela Rosa, C.; Stewart, F.P.; Kuan, L.Y.; Whitmore, J.B.; Trager, J.B.; Poehlein, C.H.; Frohlich, M.W. et al. Sipuleucel-T immune parameters correlate with survival: An analysis of the randomized phase 3 clinical trials in men with castration-resistant prostate cancer. Cancer Immunol. Immunother. 2012, doi:10.1007/s00262-012-1317-2.
29. Burleson, G.R.; Burleson, F.G.; Dietert, R.R. The cytotoxic T lymphocyte assay for evaluating cell-mediated immune function. Methods Mol. Biol. 2010, 598, 195-205.
30. Liu, L.; Chahroudi, A.; Silvestri, G.; Wernett, M.E.; Kaiser, W.J.; Safrit, J.T.; Komoriya, A.; Altman, J.D.; Packard, B.Z.; Feinberg, M.B. Visualization and quantification of T cell-mediated cytotoxicity using cell-permeable fluorogenic caspase substrates. Nat. Med. 2002, 8, 185-189.
31. Berke, G. The CTL's kiss of death. Cell 1995, 81, 9-12.
32. Henkart, P.A.; Williams, M.S.; Zacharchuk, C.M.; Sarin, A. Do CTL kill target cells by inducing apoptosis? Semin. Immunol. 1997, 9, 135-144.
33. Jerome, K.R.; Sloan, D.D.; Aubert, M. Measuring T-cell-mediated cytotoxicity using antibody to activated caspase 3. Nat. Med. 2003, 9, 4-5.
34. Koido, S.; Hara, E.; Homma, S.; Torii, A.; Toyama, Y.; Kawahara, H.; Watanabe, M.; Yanaga, K.; Fujise, K.; Tajiri, H. et al. Dendritic cells fused with allogeneic colorectal cancer cell line present multiple colorectal cancer-specific antigens and induce antitumor immunity against autologous tumor cells. Clin. Cancer Res. 2005, 11, 7891-7900.
35. Jerome, K.R.; Sloan, D.D.; Aubert, M. Measurement of CTL-induced cytotoxicity: The caspase 3 assay. Apoptosis 2003, 8, 563-571.
36. Zumkeller, W.; Schofield, P.N. Growth factors, cytokines and soluble forms of receptor molecules in cancer patients. Anticancer Res. 1995, 15, 343-348.
37. Tanguay, S.; Killion, J.J. Direct comparison of ELISPOT and ELISA-based assays for detection of individual cytokine-secreting cells. Lymphokine Cytokine Res. 1994, 13, 259-263.
38. Ronnelid, J.; Klareskog, L. A comparison between ELISPOT methods for the detection of cytokine producing cells: Greater sensitivity and specificity using ELISA plates as compared to nitrocellulose membranes. J. Immunol. Methods 1997, 200, 17-26.
39. Czerkinsky, C.; Andersson, G.; Ekre, H.P.; Nilsson, L.A.; Klareskog, L.; Ouchterlony, O. Reverse ELISPOT assay for clonal analysis of cytokine production. I. Enumeration of gamma-interferonsecreting cells. J. Immunol. Methods 1988, 110, 29-36.
40. Whiteside, T. ELISPOT assay assessment of cellular immune responses to anti-cancer vaccine. In Analysis of T Cell Response How to Analyze Cellular Immune Responses against Tumor Associated Antigens; Nagorsen, D., Marincola, F.M., Eds.; Springer: Dordrecht, The Netherlands, 2005; pp. 143-155.
41. Asai, T.; Storkus, W.J.; Whiteside, T.L. Evaluation of the modified ELISPOT assay for gamma interferon production in cancer patients receiving antitumor vaccines. Clin. Diagn. Lab. Immunol. 2000, 7, 145-154.
42. Ryan, J.E.; Ovsyannikova, I.G.; Dhiman, N.; Pinsky, N.A.; Vierkant, R.A.; Jacobson, R.M.; Poland, G.A. Inter-operator variation in ELISPOT analysis of measles virus-specific IFN-gamma- secreting T cells. Scand. J. Clin. Lab. Invest. 2005, 65, 681-689.
43. Cox, J.H.; Ferrari, G.; Kalams, S.A.; Lopaczynski, W.; Oden, N.; D'Souza M P. Results of an ELISPOT proficiency panel conducted in 11 laboratories participating in international human immunodeficiency virus type 1 vaccine trials. AIDS Res. Hum. Retroviruses. 2005, 21, 68-81.
44. Britten, C.M.; Meyer, R.G.; Kreer, T.; Drexler, I.; Wolfel, T.; Herr, W. The use of HLA-A*0201- transfected K562 as standard antigen-presenting cells for CD8(+) T lymphocytes in IFN-gamma ELISPOT assays. J. Immunol. Methods 2002, 259, 95-110.
45. Almeida, C.A.; Roberts, S.G.; Laird, R.; McKinnon, E.; Ahmed, I.; Pfafferott, K.; Turley, J.; Keane, N.M.; Lucas, A.; Rushton, B. et al. Automation of the ELISpot assay for high-throughput detection of antigen-specific T-cell responses. J. Immunol. Methods 2009, 344, 1-5.
46. Hernandez-Fuentes, M.P.; Warrens, A.N.; Lechler, R.I. Immunologic monitoring. Immunol. Rev. 2003, 196, 247-264.
47. Sander, B.; Andersson, J.; Andersson, U. Assessment of cytokines by immunofluorescence and the paraformaldehyde-saponin procedure. Immunol. Rev. 1991, 119, 65-93.
48. Leng, S.X.; McElhaney, J.E.; Walston, J.D.; Xie, D.; Fedarko, N.S.; Kuchel, G.A. ELISA and multiplex technologies for cytokine measurement in inflammation and aging research. J. Gerontol. A Biol. Sci. Med. Sci. 2008, 63, 879-884.
49. Aziz, N.; Nishanian, P.; Mitsuyasu, R.; Detels, R.; Fahey, J.L. Variables that affect assays for plasma cytokines and soluble activation markers. Clin. Diagn. Lab. Immunol. 1999, 6, 89-95.
50. Toellner, K.M.; Scheel-Toellner, D.; Seitzer, U.; Sprenger, R.; Trumper, L.; Schluter, C.; Flad, H.D.; Gerdes, J. The use of reverse transcription polymerase chain reaction to analyse large numbers of mRNA species from a single cell. J. Immunol. Methods 1996, 191, 71-75.
51. Smyth, M.J.; Dunn, G.P.; Schreiber, R.D. Cancer immunosurveillance and immunoediting: The roles of immunity in suppressing tumor development and shaping tumor immunogenicity. Adv. Immunol. 2006, 90, 1-50.
52. Miyara, M.; Sakaguchi, S. Natural regulatory T cells: Mechanisms of suppression. Trends Mol. Med. 2007, 13, 108-116.
53. Nagaraj, S.; Gabrilovich, D.I. Tumor escape mechanism governed by myeloid-derived suppressor cells. Cancer Res. 2008, 68, 2561-2563.
54. Mantovani, A.; Schioppa, T.; Porta, C.; Allavena, P.; Sica, A. Role of tumor-associated macrophages in tumor progression and invasion. Cancer Metastasis Rev. 2006, 25, 315-322.
55. Fassnacht, M.; Lee, J.; Milazzo, C.; Boczkowski, D.; Su, Z.; Nair, S.; Gilboa, E. Induction of CD4(+) and CD8(+) T-cell responses to the human stromal antigen, fibroblast activation protein: Implication for cancer immunotherapy. Clin. Cancer Res. 2005, 11, 5566-5571.
56. Shurin, M.R.; Yurkovetsky, Z.R.; Tourkova, I.L.; Balkir, L.; Shurin, G.V. Inhibition of CD40 expression and CD40-mediated dendritic cell function by tumor-derived IL-10. Int. J. Cancer 2002, 101, 61-68.
57. Elgert, K.D.; Alleva, D.G.; Mullins, D.W. Tumor-induced immune dysfunction: The macrophage connection. J. Leukoc. Biol. 1998, 64, 275-290.
58. Uyttenhove, C.; Pilotte, L.; Theate, I.; Stroobant, V.; Colau, D.; Parmentier, N.; Boon, T.; van den Eynde, B.J. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat. Med. 2003, 9, 1269-1274.
59. Fricke, I.; Mirza, N.; Dupont, J.; Lockhart, C.; Jackson, A.; Lee, J.H.; Sosman, J.A.; Gabrilovich, D.I. Vascular endothelial growth factor-trap overcomes defects in dendritic cell differentiation but does not improve antigen-specific immune responses. Clin. Cancer Res. 2007, 13, 4840-4848.
60. Takeda, K.; Kojima, Y.; Uno, T.; Hayakawa, Y.; Teng, M.W.; Yoshizawa, H.; Yagita, H.; Gejyo, F.; Okumura, K.; Smyth, M.J. Combination therapy of established tumors by antibodies targeting immune activating and suppressing molecules. J. Immunol. 2010, 184, 5493-5501.
61. Ohta, T.; Elnemr, A.; Kitagawa, H.; Kayahara, M.; Takamura, H.; Fujimura, T.; Nishimura, G.; Shimizu, K.; Yi, S.Q.; Miwa, K. Fas ligand expression in human pancreatic cancer. Oncol. Rep. 2004, 12, 749-754.
62. Hori, S.; Nomura, T.; Sakaguchi, S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003, 299, 1057-1061.
63. Yokokawa, J.; Cereda, V.; Remondo, C.; Gulley, J.L.; Arlen, P.M.; Schlom, J.; Tsang, K.Y. Enhanced functionality of CD4+CD25(high)FoxP3+ regulatory T cells in the peripheral blood of patients with prostate cancer. Clin. Cancer Res. 2008, 14, 1032-1040.
64. Gulley, J.L.; Arlen, P.M.; Madan, R.A.; Tsang, K.Y.; Pazdur, M.P.; Skarupa, L.; Jones, J.L.; Poole, D.J.; Higgins, J.P.; Hodge, J.W. et al. Immunologic and prognostic factors associated with overall survival employing a poxviral-based PSA vaccine in metastatic castrate-resistant prostate cancer. Cancer Immunol. Immunother. 2010, 59, 663-674.
65. Vergati, M.; Cereda, V.; Madan, R.A.; Gulley, J.L.; Huen, N.Y.; Rogers, C.J.; Hance, K.W.; Arlen, P.M.; Schlom, J.; Tsang, K.Y. Analysis of circulating regulatory T cells in patients with metastatic prostate cancer preversus post-vaccination. Cancer Immunol. Immunother. 2011, 60, 197-206.
66. Zhang, Y.; Campbell, C.; Li, Q.; Gildersleeve, J.C. Multidimensional glycan arrays for enhanced antibody profiling. Mol. Biosyst. 2010, 6, 1583-1591.
67. Fong, L.; Weinberg, V.K.; Chan, S.E.; Corman, J.M.; Amling, C.L.; Stephenson, R.A.; Formaker, C.; Simko, J.; Sims, R.B.; Carroll, P. et al. Neoadjuvant sipuleucel-T in localized prostate cancer: Effects on immune cells within the prostate tumor microenvironment. J. Clin. Oncol. 2012, 30, Abstract 2564.
68. Lu, C.; Williams, A.K.; Chalasani, V.; Martinez, C.H.; Chin, J. Immunotherapy for metastatic prostate cancer: Where are we at with sipuleucel-T? Expert Opin. Biol. Ther. 2011, 11, 99-108.
69. Zhang, L.; Conejo-Garcia, J.R.; Katsaros, D.; Gimotty, P.A.; Massobrio, M.; Regnani, G.; Makrigiannakis, A.; Gray, H.; Schlienger, K.; Liebman, M.N. et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N. Engl. J. Med. 2003, 348, 203-213.
70. Kondratiev, S.; Sabo, E.; Yakirevich, E.; Lavie, O.; Resnick, M.B. Intratumoral CD8 T lymphocytes as a prognostic factor of survival in endometrial carcinoma. Clin. Cancer Res. 2004, 10, 4450-4456.
71. Ladanyi, A.; Kiss, J.; Somlai, B.; Gilde, K.; Fejos, Z.; Mohos, A.; Gaudi, I.; Timar, J. Density of DC-LAMP(+) mature dendritic cells in combination with activated T lymphocytes infiltrating primary cutaneous melanoma is a strong independent prognostic factor. Cancer Immunol. Immunother. 2007, 56, 1459-1469.
72. Pages, F.; Kirilovsky, A.; Mlecnik, B.; Asslaber, M.; Tosolini, M.; Bindea, G.; Lagorce, C.; Wind, P.; Marliot, F.; Bruneval, P. et al. In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. J. Clin. Oncol. 2009, 27, 5944-5951.
73. Pages, F.; Berger, A.; Camus, M.; Sanchez-Cabo, F.; Costes, A.; Molidor, R.; Mlecnik, B.; Kirilovsky, A.; Nilsson, M.; Damotte, D. et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N. Engl. J. Med. 2005, 353, 2654-2666.
74. Yamada, N.; Oizumi, S.; Kikuchi, E.; Shinagawa, N.; Konishi-Sakakibara, J.; Ishimine, A.; Aoe, K.; Gemba, K.; Kishimoto, T.; Torigoe, T. et al. CD8+ tumor-infiltrating lymphocytes predict favorable prognosis in malignant pleural mesothelioma after resection. Cancer Immunol. Immunother. 2010, 59, 1543-1549.
75. Bates, G.J.; Fox, S.B.; Han, C.; Leek, R.D.; Garcia, J.F.; Harris, A.L.; Banham, A.H. Quantification of regulatory T cells enables the identification of high-risk breast cancer patients and those at risk of late relapse. J. Clin. Oncol. 2006, 24, 5373-5380.
76. Shimizu, K.; Nakata, M.; Hirami, Y.; Yukawa, T.; Maeda, A.; Tanemoto, K. Tumor-infiltrating Foxp3+ regulatory T cells are correlated with cyclooxygenase-2 expression and are associated with recurrence in resected non-small cell lung cancer. J. Thorac. Oncol. 2010, 5, 585-590.
77. Shen, Z.; Zhou, S.; Wang, Y.; Li, R.L.; Zhong, C.; Liang, C.; Sun, Y. Higher intratumoral infiltrated Foxp3+ Treg numbers and Foxp3+/CD8+ ratio are associated with adverse prognosis in resectable gastric cancer. J. Cancer Res. Clin. Oncol. 2010, 136, 1585-1595.
78. Liotta, F.; Gacci, M.; Frosali, F.; Querci, V.; Vittori, G.; Lapini, A.; Santarlasci, V.; Serni, S.; Cosmi, L.; Maggi, L. et al. Frequency of regulatory T cells in peripheral blood and in tumourinfiltrating lymphocytes correlates with poor prognosis in renal cell carcinoma. BJU Int. 2011, 107, 1500-1506.
79. Heery, C.; Pinto, P.; Schlom, J.; Tsang, K.; Madan, R.; Poole, D.; Vergati, M.; Walter Rodriguez, B.; Merino, M.; Gulley, J. Intraprostatic vaccine administration in patients with locally recurrent prostate cancer. J. Clin. Oncol. 2011, 29, Abstract 141.
80. Stein, W.D.; Gulley, J.L.; Schlom, J.; Madan, R.A.; Dahut, W.; Figg, W.D.; Ning, Y.M.; Arlen, P.M.; Price, D.; Bates, S.E. 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. Clin. Cancer Res. 2011, 17, 907-917.
81. Stein, W.D.; Figg, W.D.; Dahut, W.; Stein, A.D.; Hoshen, M.B.; Price, D.; Bates, S.E.; Fojo, T. Tumor growth rates derived from data for patients in a clinical trial correlate strongly with patient survival: A novel strategy for evaluation of clinical trial data. Oncologist 2008, 13, 1046-1054.
82. Gulley, J.L.; Madan, R.A.; Schlom, J. Impact of tumour volume on the potential efficacy of therapeutic vaccines. Curr. Oncol. 2011, 18, e150-e157.