2,246
Views
0
CrossRef citations to date
0
Altmetric
Review

GEN-1 Immunotherapy for the Treatment of Ovarian Cancer

, , &
Pages 421-438 | Received 03 Jun 2018, Accepted 24 Sep 2018, Published online: 16 Oct 2018

References

  • Siegel RL , MillerKD, JemalA. Cancer statistics, 2018. CA Cancer J. Clin.68, 7–30 (2018).
  • Cress RD , ChenYS, MorrisCR, PetersenM, LeiserowitzGS. Characteristics of long-term survivors of epithelial ovarian cancer. Obstet. Gynecol.126(3), 491–497 (2015).
  • National Comprehensive Cancer Network (NCCN) . Clinical practice guidelines in oncology (NCCN Guidelines®): ovarian cancer version 2.2018. https://www.nccn.org/professionals/physician_gls/recently_updated.aspx.
  • Kehoe S , HookJ, NankivellMet al. Primary chemotherapy versus primary surgery for newly diagnosed advanced ovarian cancer (CHORUS): an open-label, randomised, controlled, non-inferiority trial. Lancet386(9990), 249–257 (2015).
  • Vergote I , TropeCG, AmantFet al. Neoadjuvant chemotherapy or primary surgery in stage IIIC or IV ovarian cancer. N. Engl. J. Med.363(10), 943–953 (2010).
  • McGuire WP 3rd , MarkmanM. Primary ovarian cancer chemotherapy: current standards of care. Br. J. Cancer.89(Suppl. 3), S3–S8 (2003).
  • Bhatt A , GlehenO. The role of cytoreductive surgery and hyperthermic intraperitoneal chemotherapy (HIPEC) in ovarian cancer: a review. Indian J. Surg. Oncol.7(2), 188–197 (2016).
  • Schlienger K , ChuCS, WooEYet al. TRANCE- and CD40 ligand-matured dendritic cells reveal MHC class I-restricted T cells specific for autologous tumor in late-stage ovarian cancer patients. Clin. Cancer Res.9(4), 1517–1527 (2003).
  • Zhang L , Conejo-GarciaJR, KatsarosDet al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N. Engl. J. Med.348(3), 203–213 (2003).
  • Hwang WT , AdamsSF, TahirovicE, HagemannIS, CoukosG. Prognostic significance of tumor-infiltrating T cells in ovarian cancer: a meta-analysis. Gynecol. Oncol.124(2), 192–198 (2012).
  • Curiel TJ , CoukosG, ZouLet al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med.10(9), 942–949 (2004).
  • Sato E , OlsonSH, AhnJet al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc. Natl Acad. Sci. USA102(51), 18538–18543 (2005).
  • Santoiemma PP , PowellDJJr. Tumor infiltrating lymphocytes in ovarian cancer. Cancer Biol. Ther.16(6), 807–820 (2015).
  • Schiavoni G , GabrieleL, MatteiF. The tumor microenvironment: a pitch for multiple players. Front. Oncol.3, 90 (2013).
  • Hansen JM , ColemanRL, SoodAK. Targeting the tumour microenvironment in ovarian cancer. Eur. J. Cancer56, 131–143 (2016).
  • Freedman RS , LenziR, KudelkaAP, LawrenceDD, RosenblumM, PlatsoucasCD. Intraperitoneal immunotherapy of peritoneal carcinomatosis. Cytokines Cell Mol. Ther.4(2), 121–140 (1998).
  • Robertson MJ , RitzJ. Interleukin 12: basic biology and potential applications in cancer treatment. Oncologist1(1 & 2), 88–97 (1996).
  • Tugues S , BurkhardSH, OhsIet al. New insights into IL-12-mediated tumor suppression. Cell Death Differ.22(2), 237–246 (2015).
  • Sgadari C , AngiolilloAL, TosatoG. Inhibition of angiogenesis by interleukin-12 is mediated by the interferon-inducible protein 10. Blood87(9), 3877–3882 (1996).
  • Albini A , BrigatiC, VenturaAet al. Angiostatin anti-angiogenesis requires IL-12: the innate immune system as a key target. J. Transl. Med.7, 5 (2009).
  • Berek JS , HackerNF, LichtensteinAet al. Intraperitoneal recombinant α-interferon for ‘salvage’ immunotherapy in stage III epithelial ovarian cancer: a Gynecologic Oncology Group Study. Cancer Res.45(9), 4447–4453 (1985).
  • Berek JS , MarkmanM, StonebrakerBet al. Intraperitoneal interferon-α in residual ovarian carcinoma: a Phase II gynecologic oncology group study. Gynecol. Oncol.75(1), 10–14 (1999).
  • Mantia-Smaldone GM , CorrB, ChuCS. Immunotherapy in ovarian cancer. Hum. Vaccin. Immunother.8(9), 1179–1191 (2012).
  • Pujade-Lauraine E , GuastallaJP, ColomboNet al. Intraperitoneal recombinant interferon gamma in ovarian cancer patients with residual disease at second-look laparotomy. J. Clin. Oncol.14(2), 343–350 (1996).
  • Thaker PH , BradyWE, LankesHAet al. A Phase I trial of intraperitoneal GEN-1, an IL-12 plasmid formulated with PEG-PEI-cholesterol lipopolymer, administered with pegylated liposomal doxorubicin in patients with recurrent or persistent epithelial ovarian, fallopian tube or primary peritoneal cancers: an NRG Oncology/Gynecologic Oncology Group study. Gynecol. Oncol.147(2), 283–290 (2017).
  • Vlad AM , BudiuRA, LenznerDEet al. A Phase II trial of intraperitoneal interleukin-2 in patients with platinum-resistant or platinum-refractory ovarian cancer. Cancer Immunol. Immunother.59(2), 293–301 (2010).
  • Atkins MB , RobertsonMJ, GordonMet al. Phase I evaluation of intravenous recombinant human interleukin 12 in patients with advanced malignancies. Clin. Cancer Res.3(3), 409–417 (1997).
  • Bajetta E , Del VecchioM, MortariniRet al. Pilot study of subcutaneous recombinant human interleukin 12 in metastatic melanoma. Clin. Cancer Res.4(1), 75–85 (1998).
  • Cebon J , JagerE, ShackletonMJet al. Two Phase I studies of low dose recombinant human IL-12 with Melan-A and influenza peptides in subjects with advanced malignant melanoma. Cancer Immun.3, 7 (2003).
  • Gollob JA , MierJW, VeenstraKet al. Phase I trial of twice-weekly intravenous interleukin 12 in patients with metastatic renal cell cancer or malignant melanoma: ability to maintain IFN-γ induction is associated with clinical response. Clin. Cancer Res.6(5), 1678–1692 (2000).
  • Rook AH , WoodGS, YooEKet al. Interleukin-12 therapy of cutaneous T-cell lymphoma induces lesion regression and cytotoxic T-cell responses. Blood94(3), 902–908 (1999).
  • Lenzi R , RosenblumM, VerschraegenCet al. Phase I study of intraperitoneal recombinant human interleukin 12 in patients with Mullerian carcinoma, gastrointestinal primary malignancies, and mesothelioma. Clin. Cancer Res.8(12), 3686–3695 (2002).
  • Lenzi R , EdwardsR, JuneCet al. Phase II study of intraperitoneal recombinant interleukin-12 (rhIL-12) in patients with peritoneal carcinomatosis (residual disease <1 cm) associated with ovarian cancer or primary peritoneal carcinoma. J. Transl. Med.5, 66 (2007).
  • Barrett JA , CaiH, MiaoJet al. Regulated intratumoral expression of IL-12 using a RheoSwitch Therapeutic System® (RTS®) gene switch as gene therapy for the treatment of glioma. Cancer Gene Ther.25, 106–116 (2018).
  • Brown DW , BahramiAJ, CantonDAet al. Development of an adaptive electroporation system for intratumoral plasmid DNA delivery. Bioelectrochemistry122, 191–198 (2018).
  • Imboden M , ShiF, PughTDet al. Safety of interleukin-12 gene therapy against cancer: a murine biodistribution and toxicity study. Hum. Gene Ther.14(11), 1037–1048 (2003).
  • Kang WK , ParkC, YoonHLet al. Interleukin 12 gene therapy of cancer by peritumoral injection of transduced autologous fibroblasts: outcome of a Phase I study. Hum. Gene Ther.12(6), 671–684 (2001).
  • Fewell JG , MatarM, SlobodkinGet al. Synthesis and application of a non-viral gene delivery system for immunogene therapy of cancer. J. Control Rel.109(1–3), 288–298 (2005).
  • Mahato RI , LeeM, HanS, MahatoRI, LeeM, HanS. Intratumoral delivery of p2CMVmIL-12 using water-soluble lipopolymers. Mol. Ther.4(2), 130–138 (2001).
  • Ogris M , BrunnerS, SchullerS, OgrisM, BrunnerS, SchullerS. PEGylated DNA/transferrin-PEI complexes: reduced interaction with blood components, extended circulation in blood and potential for systemic gene delivery. Gene Ther.6(4), 595–605 (1999).
  • Boussif O , Lezoualc’hF, ZantaMAet al. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc. Natl Acad. Sci. USA92(16), 7297–7301 (1995).
  • Fewell JG , MatarMM, RiceJSet al. Treatment of disseminated ovarian cancer using nonviral interleukin-12 gene therapy delivered intraperitoneally. J. Gene Med.11(8), 718–728 (2009).
  • Thaker PH , BradleyWH, LeathCAet al. Phase I study of the safety and activity of formulated IL-12 plasmid administered intraperitoneally in combination with standard neoadjuvant chemotherapy in patients with newly diagnosed advanced stage ovarian cancer. Presented at: American Society of Clinical Oncology – Society for Immunotherapy of Cancer. National Harbor, MD, USA, Abstract 155 (2017).
  • Anwer K , MatsuzakiJ, BsharaWet al. Immunological changes following intraperitoneal administration of a formulated IL-12 plasmid in combination with standard neoadjuvant chemo in newly diagnosed advanced stage ovarian cancer patients. Presented at: American Association of Cancer Research. Addressing Critical Questions in Ovarian Cancer Research and Treatment. Pittsburgh, PA, USA, Abstract A76 (2017).
  • Roby KF , TaylorCC, SweetwoodJPet al. Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis21(4), 585–591 (2000).
  • Hasko G , SzaboC. IL-12 as a therapeutic target for pharmacological modulation in immune-mediated and inflammatory diseases: regulation of T helper 1/T helper 2 responses. Br. J. Pharmacol.127(6), 1295–1304 (1999).
  • Fewell JG , MatarMM, RiceJKet al. Interleukin-12 gene therapy in combination with bevacizumab and PEGylated liposomal doxorubicin for treatment of disseminated ovarian cancer. Presented at: American Association for Cancer Research. New Orleans, LA, USA, Abstract 2078 (2016).
  • Sriratana P , NortonJ. New immunotherapies in oncology treatment and their side effect profiles. J. Am. Board Fam. Med.31(4), 620–627 (2018).
  • Anwer K , BarnesMN, FewellJ, LewisDH, AlvarezRD. Phase-I clinical trial of IL-12 plasmid/lipopolymer complexes for the treatment of recurrent ovarian cancer. Gene Ther.17(3), 360–369 (2010).
  • Alvarez RD , SillMW, DavidsonSAet al. A Phase II trial of intraperitoneal EGEN-001, an IL-12 plasmid formulated with PEG-PEI-cholesterol lipopolymer in the treatment of persistent or recurrent epithelial ovarian, fallopian tube or primary peritoneal cancer: a gynecologic oncology group study. Gynecol. Oncol.133(3), 433–438 (2014).
  • Anwer K , KellyFJ, ChuC, FewellJG, LewisD, AlvarezRD. Phase I trial of a formulated IL-12 plasmid in combination with carboplatin and docetaxel chemotherapy in the treatment of platinum-sensitive recurrent ovarian cancer. Gynecol. Oncol.131(1), 169–173 (2013).
  • Colombo N , KutarskaE, DimopoulosMet al. Randomized, open-label, Phase III study comparing patupilone (EPO906) with pegylated liposomal doxorubicin in platinum-refractory or -resistant patients with recurrent epithelial ovarian, primary fallopian tube, or primary peritoneal cancer. J. Clin. Oncol.30(31), 3841–3847 (2012).
  • Gordon AN , GranaiCO, RosePGet al. Phase II study of liposomal doxorubicin in platinum- and paclitaxel-refractory epithelial ovarian cancer. J. Clin. Oncol.18(17), 3093–3100 (2000).
  • Markman M , GordonAN, McGuireWP, MuggiaFM. Liposomal anthracycline treatment for ovarian cancer. Semin. Oncol.31(6 Suppl. 13), 91–105 (2004).
  • Kepp O , GalluzziL, MartinsIet al. Molecular determinants of immunogenic cell death elicited by anticancer chemotherapy. Cancer Metastasis Rev.30(1), 61–69 (2011).
  • Gadducci A , GuerrieriME. Immune checkpoint inhibitors in gynecological cancers: update of literature and perspectives of clinical research. Anticancer Res.37(11), 5955–5965 (2017).
  • Molina MD , ArmstrongTK, ZhangY, PatelMM, LentzYK, AnchordoquyTJ. The stability of lyophilized lipid/DNA complexes during prolonged storage. J. Pharm. Sci.93(9), 2259–2273 (2004).