Immunotherapy in ovarian, endometrial and cervical cancer: State of the art and future perspectives

Cancer Treatment Reviews

Volumn 59, Issue , 2017, Pages 109-116

  Ventriglia, Jole ^a,b   Paciolla, Immacolata ^b,c   Pisano, Carmela ^b   Cecere, Sabrina Chiara ^b   Di Napoli, Marilena ^b   Tambaro, Rosa ^b   Califano, Daniela ^b   Losito, Simona ^b   Scognamiglio, Giosuè ^b   Setola, Sergio Venanzio ^b   Arenare, Laura ^b   Pignata, Sandro ^b   Della Pepa, Chiara ^b  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b NATIONAL CANCER INSTITUTE   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Cervical cancer; Endometrial cancer; Immunotherapy; Ovarian cancer; PD1 PD L1

Indexed keywords

ADXS 11 001; ANTINEOPLASTIC AGENT; ATEZOLIZUMAB; AVELUMAB; CARBOPLATIN; DURVALUMAB; IPILIMUMAB; MOTOLIMOD; NIVOLUMAB; PACLITAXEL; PEMBROLIZUMAB; UNCLASSIFIED DRUG; MONOCLONAL ANTIBODY;

ACTIVE IMMUNOTHERAPY; CANCER IMMUNOTHERAPY; CANCER PROGNOSIS; CANCER RESISTANCE; CANCER SURVIVAL; DRUG EFFICACY; ENDOMETRIUM CANCER; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; MONOTHERAPY; OUTCOME ASSESSMENT; OVARY CANCER; OVARY CARCINOMA; PASSIVE IMMUNIZATION; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); REVIEW; TUMOR MICROENVIRONMENT; UTERINE CERVIX CANCER; ADULT; AGED; DISEASE FREE SURVIVAL; ENDOMETRIAL NEOPLASMS; FEMALE; IMMUNOLOGY; IMMUNOTHERAPY; MIDDLE AGED; MORTALITY; OVARIAN NEOPLASMS; PATHOLOGY; PROCEDURES; PROGNOSIS; RISK ASSESSMENT; SURVIVAL ANALYSIS; UTERINE CERVICAL NEOPLASMS;

ADULT; AGED; ANTIBODIES, MONOCLONAL, HUMANIZED; DISEASE-FREE SURVIVAL; ENDOMETRIAL NEOPLASMS; FEMALE; HUMANS; IMMUNOTHERAPY; MIDDLE AGED; OVARIAN NEOPLASMS; PROGNOSIS; RISK ASSESSMENT; SURVIVAL ANALYSIS; UTERINE CERVICAL NEOPLASMS;

EID: 85026855517     PISSN: 03057372     EISSN: 15321967     Source Type: Journal    
DOI: 10.1016/j.ctrv.2017.07.008     Document Type: Review

References (90)

1. Steliarova-Foucher, E., O'Callaghan, M., Ferlay, J., Masuyer, E., Rosso, S., Forman, D., et al. The European cancer observatory: a new data resource. Eur J Cancer 51:9 (2015), 1131–1143.
2. Zsiros, E.1., Tanyi, J., Balint, K., Kandalaft, L.E., Immunotherapy for ovarian cancer: recent advances and perspectives. Curr Opin Oncol 26:5 (2014), 492–500.
3. Terme, M., Ullrich, E., Aymeric, L., Meinhardt, K., Desbois, M., Delahaye, N., et al. IL-18 induces PD-1–dependent immunosuppression in cancer. Cancer Res 71:16 (2011), 5393–5399.
4. Shankaran, V., Ikeda, H., Bruce, A.T., White, J.M., Swanson, P.E., Old, L.J., et al. Ifngamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410:6832 (2001 Apr 26), 1107–1111.
5. Smyth, M.J.1., Crowe, N.Y., Godfrey, D.I., NK cells and NKT cells collaborate in host protection from methylcholanthrene-induced fibrosarcoma. Int Immunol 13:4 (2001), 459–463.
6. Alberts BJA, Lewis J. Helper T cells and lymphocyte activation. 4th ed. Mol Biol New York: Cell Garland Science; 2002. 1464p.
7. Vivier, E.1., Tomasello, E., Baratin, M., Walzer, T., Ugolini, S., Functions of natural killer cells. Nat Immunol 9:5 (2008), 503–510 10.1038/Ni158 May.
8. Aguirre-Ghiso, J.A., Models, mechanisms and clinical evidence for cancer dormancy. Nat Rev Cancer 7:11 (2007), 834–846.
9. Gabrilovich, D., Ishida, T., Oyama, T., Ran, S., Kravtsov, V., Nadaf, S., et al. Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically effects the differentiation of multiple hematopoietic lineages in vivo. Blood 92:11 (1998), 4150–4166.
10. Yoshimura, Akihiko., Muto, Go., TGF-Β function in immune suppression. Curr Top Microbiol Immunol 350 (2011), 17–37.
11. Lob, S., Konigsrainer, A., Rammensee, H.G., Opelz, G., Terness, P., Inhibitors of indoleamine-2.3-dioxygenase for cancer therapy: can we see the wood for the tree?. Nat Rev Cancer 9:6 (2009), 445–452.
12. Garrido, F., Ruiz-Cabello, F., Cabrera, T., Pérez-Villar, J.J., López-Botet, M., Duggan-Keen, M., et al. Implications for immunosurveillance of altered HLA class I phenotypes in human tumours. Immunol Today 18:2 (1997), 89–95.
13. Jin, H.T., Ahmed, R., Okazaki, T., Role of PD-1 in regulating T-cell immunity. Curr Top Microbial Immunol 350 (2011), 17–37.
14. Borghaei, H., Paz-Ares, L., Horn, L., Spigel, David R., Steins, M., Ready, Neal E., et al. Nivolumab versus docetaxel in advanced non squamous non small cell lung cancer. N Engl J Med 373 (2015), 1627–1639.
15. Brahmer, J., Reckamp, K.L., Baas, P., Crinò, L., Eberhardt Wilfried, E.E., Poddubskaya, E., et al. Nivolumab versus docetaxel in advanced squamous-cell non small cell lung cancer. N Engl J Med 373 (2015), 123–135.
16. Cella, D., Grünwald, V., Nathan, P., Doan, J., Dastani, H., Taylor, F., et al. Quality of life in patients with advanced renal cell carcinoma given nivolumab versus everolimus incheckmate 025: a randomised, open-label, phase 3. Lancet Oncol 17:7 (2016 Jul), 994–1003.
17. Dr Jeffrey, S., Weber, Sandra P., D'Angelo, David Minor, Stephen Hodi, F., Gutzmer, Ralf, Neyns, Bart, et al. Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate 037): a randomised, controlled, open-label, phase 3 trial. Lancet Oncol 16:4 (2015), 375–384.
18. US Food and Drug Administration. Drugs: Pembrolizumab. < https://www.accessdata.fda.gov/drugsatfda_docs/nda/2014/125514Orig1s000SumR.pdf> < https://www.accessdata.fda.gov/drugsatfda_docs/label/2015/125514s004s006lbl.pdf>.
19. Longoria, S.C., Eskander, R.N., Immunotherapy in endometrial cancer – an evolving therapeutic paradigm. Gynecol Oncol Res Practice, 2, 2015, 11.
20. Lin Zhang, Jose R. Conejo-Garcia, Dionyssios Katsaros, Phyllis A. Gimotty, Marco Massobrio, Giorgia Regnani, et al. Intratumoral T Cells, Recurrence, And Survival In Epithelial Ovarian Cancer. -N Engl J Med Jan. 2003; 348:203–213.
21. Hamanishi, J., Mandai, M., Iwasaki, M., Okazaki, T., Tanaka, Y., Yamaguchi, K., et al. Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+T lymphocytesare prognostic factors of human ovarian cancer. Proc Natl Acad Sci USA, 104, 2007.
22. Wouters, M.C., Komdeur, F.L., Workel, H.H., Klip, H.G., Plat, A., NM, K., et al. Surgical Outcome And T-Cell Differentiation Influence Prognostic Benefit Of Tumor-Infiltrating Lymphocytes In High-Grade Serous Ovarian Cancer. Clin Cancer Res, 2015.
23. Cancer Genome Atlas Research N. Integrated Genomic Analyses Of Ovarian Cance. Nature 474 (7353), 609–615; 2011.
24. Landskron, J.1., Helland, Ø., Torgersen, K.M., Aandahl, E.M., Gjertsen, B.T., Bjørge, L., et al. Activated regulatory and memory T-cells accumulate in malignant ascites from ovarian carcinoma patients. Cancer Immunol Immunother 64:3 (2015), 337–347.
25. Kumar, V., Chaudhary, N., Garg, M., Floudas, C.S., Soni, P., Chandra, A.B., Current diagnosis and management of immune related adverse events (irAEs) induced by immune checkpoint inhibitor therapy. Front Pharmacol, 8(8), 2017, 49.
26. Hamanishi, J., Mandai, M., Ikeda, T., Minami, M., Kawaguchi, A., Murayama, T., et al. Safety and antitumor activity of Anti-PD-1 antibody, nivolumab, in patients with platinum-resistant ovarian cancer. J Clin Oncol 33:34 (2015), 4015–4022.
27. Varga, A., Piha-Paul, S.A., Ott, P.A., Mehnert, J.M., Berton-Rigaud, D., Johnson, E.A., et al. Antitumor activity and safety of pembrolizumab in patients (pts) with PD-L1 positive advanced ovarian cancer: interim results from a phase Ib study. J Clin Oncol, 33, 2015 (suppl. abstract 5510). Available at: < http://meetinglibrary.asco.org/content/147724-156>.
28. Disis, M.L., Patel, M.R., Pant, S., Hamilton, E.P., Lockhart, A.C., Kelly, K., et al. Avelumab (MSB0010718C; anti-PD-L1) in patients with recurrent/refractory ovarian cancer from the JAVELIN Solid Tumor phase Ib trial: Safety and clinical activity. J Clin Oncol, 34, 2016 (suppl; abstr 5533). Available at: < http://meetinglibrary.asco.org/content/163764-176>.
29. Hodi, F.S., Lawrence, D., Lezcano, C., Wu, X., Zhou, J., Sasada, T., et al. Bevacizumab plus ipilimumab in patients with metastatic melanoma. Cancer Immunol Res 2:7 (2014), 632–642.
30. Wallin, J.J., Bendell, J.C., Funke, R., Sznol, M., Korski, K., Jones, S., et al. Atezolizumab in combination with bevacizumab enhances antigen-specific T-cell migration in metastatic renal cell carcinoma. Nat Commun, 7, 2016 12624.
31. Frumento, G., Rotondo, R., Tonetti, M., Damonte, G., Benatti, U., Ferrara, G.B., Tryptophan-derived catabolites are responsible for inhibition Of T And natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J Exp Med 196 (2002), 459–468.
32. Liu, X., Shin, N., Koblish, H.K., Yang, G., Wang, Q., Wang, K., et al. Selective inhibition of IDO1 effectively regulates mediators of antitumor immunity. Blood 115 (2010), 3520–3530.
33. Inaba, T., Ino, K., Kajiyama, H., Yamamoto, E., Shibata, K., Nawa, A., et al. Role of the immunosuppressive enzyme indoleamine 2,3-dioxygenase in the progression of ovarian carcinoma. Gynecol Oncol 115 (2009), 185–192.
34. Nonaka, H., Saga, Y., Fujiwara, H., Akimoto, H., Yamada, A., Kagawa, S., et al. Indoleamine 2,3- dioxygenase promotes peritoneal dissemination of ovarian cancer. Int J Oncol 38 (2011), 113–120.
35. Jackson R, Dees EC, Kauh JS, Harvey RD, Neuger A, Lush R, et al. A phase I study of indoximod in combination with docetaxel in metastatic solid tumors. In: ASCO Annual Meeting; 2013. Abstract #3026.
36. Newton RC, Scherle PA, Bowman K, Liu X, Beatty GL, O'Dwyer PJ, et al. Pharmacodynamic assessment of INCB024360, an inhibitor of indoleamine 2,3-dioxygenase 1 (IDO1) in advancer cancer patients, ASCO Annual Meeting. 2012. Abstract #2500. http://meetinglibrary.asco.org/content/96898-114.
37. Monk, B.J., Brady, M.F., Aghajanian, C., Lankes, H.A., Rizack, T., Leach, J., et al. A phase 2, randomized, double-blind, placebo- controlled study of chemo-immunotherapy combination using motolimod with pegylated liposomal doxorubicin in recurrent or persistent ovarian cancer: a Gynecologic Oncology Group partners study. Ann Oncol 28:5 (2017), 996–1004.
38. Topalian, S.L., Hodi, F.S., Brahmer, J.R., Gettinger, S.N., Smith, D.C., McDermott, D.F., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 366 (2012), 2443–2454.
39. Le, D.T., Uram, J.N., Wang, H., Bartlett, B.R., Kemberling, H., Eyring, A.D., et al. PD-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med 372 (2015), 2509–2520.
40. Llosa, N.J., Cruise, M., Tam, A., Wicks, E.C., Hechenbleikner, E.M., Taube, J.M., et al. The vigorous immune microenvironment of microsatellite instable colon cancer is balanced by multiple counter-inhibitory checkpoints. Cancer Discov 5 (2014), 43–51.
41. TCGA. Integrated genomic analyses of ovarian carcinoma. Nature; 2011; 474:609–615.
42. Ceccaldi, R., Liu, J.C., Amunugama, R., Hajdu, I., Primack, B., Petalcorin, M.I., et al. Homologous-recombination-deficient tumours are dependent on Poltheta-mediated repair. Nature 518 (2015), 258–262.
43. Mateos-Gomez, P.A., Gong, F., Nair, N., Miller, K.M., Lazzerini- Denchi, E., Sfeir, A., Mammalian polymerase theta promotes alternative NHEJ and suppresses recombination. Nature 518 (2015), 254–257.
44. Birkbak, N.J., Kochupurakkal, B., Izarzugaza, J.M., Eklund, A.C., Li, Y., Liu, J., et al. Tumor mutation burden forecasts outcome in ovarian cancer with BRCA1 or BRCA2 mutations. PLoS One, 8, 2013, e80023.
45. Strickland, K.C., Howitt, B.E., Shukla, S.A., Rodig, S., Ritterhouse, L.L., Liu, J.F., et al. Association and prognostic significance of BRCA1/2-mutation status with neoantigen load, number of tumor-infiltrating lymphocytes and expression of PD-1/PD-L1 in high grade serous ovarian cancer”. Oncotarget 7:12 (2016), 13587–13598.
46. Lee, J.M., Dos Santos Zimmer, A., Lipkowitz, S., Annunziata, C.M., Ho, T., Chiou, V.L., et al. Phase I study of the PD-L1 inhibitor, durvalumab (MEDI4736; D) in combination with a PARP inhibitor, olaparib (O) or a VEGFR inhibitor, cediranib (C) in women's cancers (NCT02484404). J Clin Oncol, 34, 2016 (suppl; abstr 3015). Available at: http://meetinglibrary.asco.org/print/2390591.
47. Strickland, K., Howitt, B.E., Rodig, S.J., Matulonis, U.A., Konstantinopoulos, P., Immunogenicity of clear cell ovarian cancer: association with ARID1A loss, microsatellite instability and endometriosis. J Clin Oncol, 34, 2016.
48. Howitt BE, Strickland KC, Sholl LM, Rodig S, Ritterhouse LL, Chowdhury D, et al. Clear cell ovarian cancers with microsatellite instability: a unique subset of ovarian cancers with increased tumor-infiltrating lymphocytes and PD-1/PD-L1 expression.
49. Wira, C.R., Fahey, J.V., Ghosh, M., Patel, M.V., Hickey, D.K., Ochiel, D.O., Sex hormone regulation of innate immunity in the female reproductive tract: the role of epithelial cells in balancing reproductive potential with protection against sexually transmitted pathogens. Am J Reprod Immunol (New York, NY: 1989) 63:6 (2010), 544–565.
50. Vanderstraeten, A., Tuyaerts, S., Amant, F., The immune system in the normal endometrium and implications for endometrial cancer development. J Reprod Immunol 109 (2015), 7–16.
51. Deligdisch, L., Morphologic correlates of host response in endometrial carcinoma. Am J Reproduc Immunol (New York, NY: 1989) 2:1 (1982), 54–57.
52. Silverberg, S.G., Sasano, N., Yajima, A., Endometrial carcinoma in Miyagi Prefecture, Japan: histopathologic analysis of a cancer registry-based series and comparison with cases in American women. Cancer 49:7 (1982), 1504–1510.
53. de Jong, R.A., Leffers, N., Boezen, H.M., ten Hoor, K.A., van der Zee, A.G., Hollema, H., et al. Presence of tumor-infiltrating lymphocytes is an independent prognostic factor in type I and II endometrial cancer. Gynecol Oncol 114:1 (2009), 105–110.
54. Hashimoto, I., Kodama, J., Seki, N., Hongo, A., Miyagi, Y., Yoshinouchi, M., et al. Macrophage infiltration and angiogenesis in endometrial cancer. Anticancer Res 20:6c (2000), 4853–4856.
55. Soeda, S., Nakamura, N., Ozeki, T., Nishiyama, H., Hojo, H., Yamada, H., et al. Tumor-associated macrophages correlate with vascular space invasion and myometrial invasion in endometrial carcinoma. Gynecol Oncol 109:1 (2008), 122–128.
56. Espinosa, I., Jose Carnicer, M., Catasus, L., Canet, B., D'Angelo, E., Zannoni, G.F., et al. Myometrial invasion and lymph node metastasis in endometrioid carcinomas: tumor-associated macrophages, microvessel density, and HIF1A have a crucial role. Am J Surg Pathol 34:11 (2010), 1708–1714.
57. Kubler, K., Ayub, T.H., Weber, S.K., Zivanovic, O., Abramian, A., Keyver-Paik, M.D., et al. Prognostic significance of tumor-associated macrophages in endometrial adenocarcinoma. Gynecol Oncol 135:2 (2014), 176–183.
58. Vanderstraeten, A., Luyten, C., Verbist, G., Tuyaerts, S., Amant, F., Mapping the immunosuppressive environment in uterine tumors: implications for immunotherapy. Cancer Immunol Immunother 63:6 (2014), 545–557.
59. Herzog, T., Arguello, D., Reddy, S., Gatalica, Z., PD-1 and PD-L1 expression in 1599 gynecological malignancies - implications for immunotherapy. Gynecol Oncol 137:Suppl 1 (2015), 204–205.
60. Gargiulo, P., Della Pepa, C., Berardi, S., Califano, D., Scala, S., Buonaguro, L., et al. Tumor genotype and immune microenvironment in POLE-ultramutated and MSI-hypermutated Endometrial Cancers: new candidates for checkpoint blockade immunotherapy?. Cancer Treat Rev 48 (2016), 61–68.
61. Howitt, B.E., Shukla, S.A., Sholl, L.M., Ritterhouse, L.L., Watkins, J.C., Rodig, S., et al. Association of polymerase e-mutated and microsatellite-instable endometrial cancers With neoantigen load, number of tumor-infiltrating lymphocytes, and expression of PD-1 and PD-L1. JAMA Oncol 1:9 (2015), 1319–1323.
62. Ott PA, Bang YJ, Berton-Rigaud D, Elez E, Pishvaian MJ, Rugo HS, et al. Pembrolizumab in advanced endometrial cancer: preliminary results from the phase 1b KEYNOTE-028. J Clin Oncol 2016;34: abstr5581. Available at: http://meetinglibrary.asco.org/content/164683-176.
63. Ferlay Jacques, Soerjomataram Isabelle, Dikshit Rajesh, Eser Sultan, Mathers Colin, Rebelo Marise, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012.
64. Torre, L.A., Bray, F., Siegel, R.L., Ferlay, J., Lortet-Tieulent, J., Jemal, A., Global cancer statistics, 2012. CA Cancer J Clin 65 (2015), 87–108.
65. Siegel, R.L., Miller, K.D., Jemal, A., Cancer statisctics, 2016. CA Cancer J Clin 66 (2016), 7–30.
66. Wakeham, K., Kavanagh, The burden of HPV-associated anogenital cancers. Curr Oncol Rep, 16, 2014, 402.
67. Ma, B., Maraj, B., Tran, N.P., Knoff, J., Chen, A., Alvarez, R.D., et al. Emerging human papillomavirus vaccines. Expert Opin Emerg Drugs 17 (2012), 469–492.
68. Herrero, R., Gonzalez, P., Markowitz, L.E., Present status of human papillomavirus vaccine development and implementation. Lancet Oncol 16:5 (2015), e206–e216.
69. Lin, K., Roosinovich, E., Ma, B., Hung, C.F., Wu, T.C., Therapeutic HPV DNA vaccines. Immunol Res 47 (2010), 86–112.
70. Liao, J.B., Immunotherapy for gynecologic cancers. Gynecol Oncol 142:1 (2016), 3–5.
71. Lee, S.J., Yang, A., Wu, T.C., Hung, C.F., Immunotherapy for human papillomavirus-associated disease and cervical cancer: review of clinical and translational research. J Gynecol Oncol, 27(5), 2016, e51.
72. Muñoz, N., Bosch, F.X., de Sanjosé, S., Herrero, R., Castellsagué, X., Shah, K.V., et al. International agency for research on cancer multicenter cervical cancer study group epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 348 (2003), 518–527.
73. Walboomers, J.M., Jacobs, M.V., Manos, M.M., Bosch, F.X., Kummer, J.A., Shah, K.V., et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189 (1999), 12–19.
74. Kawana, K., Adachi, K., Kojima, S., Taguchi, A., Tomio, K., Yamashita, A., et al. Oral vaccination against HPV E7 for treatment of cervical intraepithelial neoplasia grade 3 (CIN3) elicits E7-specific mucosal immunity in the cervix of CIN3 patients. Vaccine 32 (2014), 6233–6239.
75. Cory, L., Chu, C., ADXS-HPV: a therapeutic Listeria vaccination targeting cervical cancers expressing the HPV E7 antigen. Hum Vaccin Immunother 10 (2014), 3190–3195.
76. Alvarez, R.D., Huh, W.K., Bae, S., Lamb, L.S. Jr, Conner, M.G., Boyer, J., et al. A pilot study of pNGVL4a-CRT/E7(detox) for the treatment of patients with HPV16+ cervical intraepithelial neoplasia 2/3 (CIN2/3). Gynecol Oncol 140 (2016), 245–252.
77. Trimble, C.I., Morrow, M.P., Kraynyak, J.A., Shen, X., Dallas, M., Yan, J., et al. Safety, efficacy, and immunogenicity of VGX-3100, a therapeutic synthetic DNA vaccine targeting human papillomavirus 16 and 18 E6 and E7 proteins for cervical intraephitelial neoplasia 2/3: a randomised, double-blind, placebo-controlled phase 2b trial. Lancet 386 (2015), 2078–2088 (10008)n.
78. Rothman, J., Paterson, Y., Live-attenuated Listeria-based immunotherapy. Expert Rev Vaccines 12 (2013), 493–504.
79. Petit, R.G., Basu, Partha, ADXS11–001 immunotherapy targeting HPV-E7: updated survival and safety data from a phase 2 study in Indian women with recurrent/refractory cervical cancer. J Immunother Cancer, 1, 2013, P231.
80. Howitt, B.E., Sun, H.H., Roemer, M.G., Kelley, A., Chapuy, B., Aviki, E., et al. Genetic basis for PD-L1 expression in squamous cell carcinomas of the cervix and vulva. JAMA Oncol 2:4 (2016), 518–522.
81. Frenel Jean-Sebastien, Le Tourneau Christophe, O'Neil Bert H, Ott Patrick Alexander, Piha-Paul Sarina Anne, Gomez-Roca Carlos Alberto, et al., Pembrolizumab in patients with advanced cervical squamous cell cancer: preliminary results from the phase Ib KEYNOTE-028 study. J Clin Oncol 2016;34:(suppl; abstr 5515).
82. Rosenberg, S.A., Lotze, M.T., Muul, L.M., Leitman, S., Chang, A.E., Ettinghausen, S.E., et al. Observations on the systemic administration of autologous lymphokine-activated killer cells and recombinant interleukin-2 to patients with metastatic cancer. N Engl J Med 313 (1985), 1485–1492.
83. Rosenberg, S.A., Yang, J.C., Sherry, R.M., Kammula, U.S., Hughes, M.S., Phan, G.Q., et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 17 (2011), 4550–4557.
84. Rosenberg, S.A., Packard, B.S., Aebersold, P.M., Solomon, D., Topalian, S.L., Toy, S.T., et al. Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report. N Engl J Med 319 (1988), 1676–1680.
85. Joseph, R.W., Peddareddigari, V.R., Liu, P., Miller, P.W., Overwijk, W.W., Bekele, N.B., et al. Impact of clinical and pathologic features on tumor-infiltrating lymphocyte expansion from surgically excised melanoma metastases for adoptive T-cell therapy. Clin Cancer Res 17 (2011), 4882–4891.
86. Goff, S.L., Smith, F.O., Klapper, J.A., Sherry, R., Wunderlich, J.R., Steinberg, S.M., et al. Tumor infiltrating lymphocyte therapy for metastatic melanoma: analysis of tumors resected for TIL. J Immunother 33 (2010), 840–847.
87. Besser, M.J., Shapira-Frommer, R., Treves, A.J., Zippel, D., Itzhaki, O., Schallmach, E., et al. Minimally cultured or selected autologous tumor-infiltrating lymphocytes after a lympho-depleting chemotherapy regimen in metastatic melanoma patients. J Immunother 32 (2009), 415–423.
88. Stevanović, S., Draper, L.M., Langhan, M.M., Campbell, T.E., Kwong, M.L., Wunderlich, J.R., et al. Complete regression of metastatic cervical cancer after treatment with human papillomavirus-targeted tumor-infiltrating T cells. J Clin Oncol 33:14 (2015), 1543–1550.
89. Sucker, A., Zhao, F., Pieper, N., Heeke, C., Maltaner, R., Stadtler, N., et al. Acquired IFN resistance impairs anti-tumor immunity and gives rise to T-cell-resistant melanoma lesions. Nat Commun, 31(8), 2017, 15440.
90. Ren, Y., Zhang, Y., Liu, R.Z., Fenstermacher, D.A., Wright, K.L., Teer, J.K., et al. JAK1 truncating mutations in gynecologic cancer define new role of cancer-associated protein tyrosine kinase aberrations. Sci Rep, 3, 2013, 3042.