Overexpression of SOCS3 mediated by adenovirus vector in mouse and human castration-resistant prostate cancer cells increases the sensitivity to NK cells in vitro and in vivo.
Adenoviridae
/ genetics
Animals
Apoptosis
/ genetics
Biomarkers, Tumor
Cell Cycle
/ genetics
Cell Line, Tumor
Disease Models, Animal
Gene Expression
Gene Transfer Techniques
Genetic Vectors
/ genetics
Humans
Interleukin-6
/ metabolism
Killer Cells, Natural
/ immunology
Male
Mice
Prostatic Neoplasms, Castration-Resistant
/ genetics
Signal Transduction
Suppressor of Cytokine Signaling 3 Protein
/ genetics
Transduction, Genetic
Tumor Microenvironment
/ genetics
Journal
Cancer gene therapy
ISSN: 1476-5500
Titre abrégé: Cancer Gene Ther
Pays: England
ID NLM: 9432230
Informations de publication
Date de publication:
11 2019
11 2019
Historique:
received:
01
08
2018
accepted:
09
12
2018
revised:
30
11
2018
pubmed:
5
1
2019
medline:
31
7
2020
entrez:
5
1
2019
Statut:
ppublish
Résumé
Prostate cancer is one of the most common cancers in men. The overactivation of IL-6/JAK/STAT3 signaling and silencing of SOCS3 are frequently observed in prostate cancer. In the present study we undertook to develop Ad-SOCS3 gene therapy for the treatment of prostate cancer and also investigated whether Ad-SOCS3 increased sensitivity to NK cells. We demonstrated that Ad-SOCS3 could significantly inhibit growth of castration-resistant prostate cancer (CRPC) cell lines expressing pSTAT3, DU-145 (at 10, 20, and 40 MOI), and TRAMP-C2 (at 40 MOI), but not the PC-3 CRPC cell line with the STAT3 gene deleted. Ad-SOCS3 (40 MOI) could suppress IL-6 production in DU-145 cells and PD-L1 expression induced by IFN-γ in TRAMP-C2 cells, and increased the NK cell sensitivity of both TRAMP-C2 and DU-145 cells. In the DU-145 mouse xenograft tumor model, intratumoral injections (twice/week for 3 weeks) of 1 × 10
Identifiants
pubmed: 30607005
doi: 10.1038/s41417-018-0075-5
pii: 10.1038/s41417-018-0075-5
doi:
Substances chimiques
Biomarkers, Tumor
0
Interleukin-6
0
SOCS3 protein, human
0
Suppressor of Cytokine Signaling 3 Protein
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
388-399Commentaires et corrections
Type : CommentIn
Références
Chikuma S, Kanamori M, Mise-Omata S, Yoshimura A. Suppressors of cytokine signaling: potential immune checkpoint molecules for cancer immunotherapy. Cancer Sci. 2017;108:574–80.
doi: 10.1111/cas.13194
Iwahori K, Serada S, Fujimoto M, Nomura S, Osaki T, Lee CM, et al. Overexpression of SOCS3 exhibits preclinical antitumor activity against malignant pleural mesothelioma. Int J Cancer. 2011;129:1005–17.
doi: 10.1002/ijc.25716
Yu H, Jove R. The STATs of cancer--new molecular targets come of age. Nat Rev Cancer. 2004;4:97–105.
doi: 10.1038/nrc1275
Zhang J, Li H, Yu JP, Wang SE, Ren XB. Role of SOCS1 in tumor progression and therapeutic application. Int J Cancer. 2012;130:1971–80.
doi: 10.1002/ijc.27318
Kim MH, Kim MS, Kim W, Kang MA, Cacalano NA, Kang SB, et al. Suppressor of cytokine signaling (SOCS) genes are silenced by DNA hypermethylation and histone deacetylation and regulate response to radiotherapy in cervical cancer cells. PLoS ONE. 2015;10:e0123133.
doi: 10.1371/journal.pone.0123133
He B, You L, Xu Z, Mazieres J, Lee AY, Jablons DM. Activity of the suppressor of cytokine signaling-3 promoter in human non-small-cell lung cancer. Clin Lung Cancer. 2004;5:366–70.
doi: 10.3816/CLC.2004.n.015
Sugase T, Takahashi T, Serada S, Nakatsuka R, Fujimoto M, Ohkawara T, et al. Suppressor of cytokine signaling-1 gene therapy induces potent antitumor effect in patient-derived esophageal squamous cell carcinoma xenograft mice. Int J Cancer. 2017;140:2608–21.
doi: 10.1002/ijc.30666
Wen W, Wu J, Liu L, Tian Y, Buettner R, Hsieh MY, et al. Synergistic anti-tumor effect of combined inhibition of EGFR and JAK/STAT3 pathways in human ovarian cancer. Mol Cancer. 2015;14:100.
doi: 10.1186/s12943-015-0366-5
Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–386.
doi: 10.1002/ijc.29210
Karantanos T, Corn PG, Thompson TC. Prostate cancer progression after androgen deprivation therapy: mechanisms of castrate resistance and novel therapeutic approaches. Oncogene. 2013;32:5501–11.
doi: 10.1038/onc.2013.206
Lou W, Ni Z, Dyer K, Tweardy DJ, Gao AC. Interleukin-6 induces prostate cancer cell growth accompanied by activation of stat3 signaling pathway. Prostate. 2000;42:239–42.
doi: 10.1002/(SICI)1097-0045(20000215)42:3<239::AID-PROS10>3.0.CO;2-G
Ribas A, Dummer R, Puzanov I, VanderWalde A, Andtbacka RHI, Michielin O, et al. Oncolytic virotherapy promotes intratumoral T cell infiltration and improves anti-PD-1 immunotherapy. Cell . 2017;170:1109–19.
doi: 10.1016/j.cell.2017.08.027
Chesney J, Puzanov I, Collichio F, Singh P, Milhem MM, Glaspy J, et al. Randomized, open-label phase II study evaluating the efficacy and safety of talimogene laherparepvec in combination with ipilimumab versus ipilimumab alone in patients with advanced, unresectable melanoma. J Clin Oncol. 2018;36:1658–67.
doi: 10.1200/JCO.2017.73.7379
Hiwatashi K, Tamiya T, Hasegawa E, Fukaya T, Hashimoto M, Kakoi K, et al. Suppression of SOCS3 in macrophages prevents cancer metastasis by modifying macrophage phase and MCP2/CCL8 induction. Cancer Lett. 2011;308:172–80.
doi: 10.1016/j.canlet.2011.04.024
Kitamura H, Ohno Y, Toyoshima Y, Ohtake J, Homma S, Kawamura H, et al. Interleukin-6/STAT3 signaling as a promising target to improve the efficacy of cancer immunotherapy. Cancer Sci. 2017;108:1947–52.
doi: 10.1111/cas.13332
Zhang X, Zeng Y, Qu Q, Zhu J, Liu Z, Ning W, et al. PD-L1 induced by IFN-γ from tumor-associated macrophages via the JAK/STAT3 and PI3K/AKT signaling pathways promoted progression of lung cancer. Int J Clin Oncol. 2017;22:1026–33.
doi: 10.1007/s10147-017-1161-7
Miyake S, Makimura M, Kanegae Y, Harada S, Sato Y, Takamori K, et al. Efficient generation of recombinant adenoviruses using adenovirus DNAterminal protein complex and a cosmid bearing the full-length virus genome. Proc Natl Acad Sci USA. 1996;93:1320–4.
doi: 10.1073/pnas.93.3.1320
Goto H, Osaki T, Kijima T, Nishino K, Kumagai T, Funakoshi T, et al. Gene therapy utilizing the Cre/loxP system selectively suppresses tumor growth of disseminated carcinoembryonic antigen-producing cancer cells. Int J Cancer. 2001;94:414–9.
doi: 10.1002/ijc.1474
Nishino K, Osaki T, Kumagai T, Kijima T, Tachibana I, Goto H, et al. Adenovirus-mediated gene therapy specific for small cell lung cancer cells using a Myc-Max binding motif. Int J Cancer. 2001;91:851–6.
doi: 10.1002/1097-0215(200002)9999:9999<::AID-IJC1120>3.0.CO;2-1
Kijima T, Osaki T, Nishino K, Kumagai T, Funakoshi T, Goto H, et al. Application of the Cre recombinase/loxP system further enhances antitumor effects in cell type-specific gene therapy against carcinoembryonic antigen-producing cancer. Cancer Res. 1999;59:4906–11.
pubmed: 10519403
Saito H, Kitagawa K, Yoneda T, Fukui Y, Fujsawa M, Bautista D, et al. Combination of p53-DC vaccine and rAd-p53 gene therapy induced CTLs cytotoxic against p53-deleted human prostate cancer cells in vitro. Cancer Gene Ther. 2017;24:289–96.
doi: 10.1038/cgt.2017.21
Kanegae Y, Makimura M, Saito I. A simple and efficient method for purification of infectious recombinant adenovirus. Jpn J Med Sci Biol. 1994;47:157–66.
doi: 10.7883/yoken1952.47.157
Riccardi C, Nicoletti I. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat Protoc. 2006;1:1458–61.
doi: 10.1038/nprot.2006.238
Sansone P, Bromberg J. Targeting the interleukin-6/Jak/stat pathway in human malignancies. J Clin Oncol. 2012;30:1005–01014.
doi: 10.1200/JCO.2010.31.8907
Adler HL, McCurdy MA, Kattan MW, Timme TL, Scardino PT, Thompson TC. Elevated levels of circulating interleukin-6 and transforming growth factor-beta1 in patients with metastatic prostatic carcinoma. J Urol. 1999;161:182–7.
doi: 10.1016/S0022-5347(01)62092-5
Heinrich PC, Behrmann I, Haan S, Hermanns HM, Müller-Newen G, Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J. 2003;374:1–20.
doi: 10.1042/bj20030407
Don-Doncow N, Marginean F, Coleman I, Nelson PS, Ehrnström R, Krzyzanowska A, et al. Expression of STAT3 in prostate cancer metastases. Eur Urol. 2017;71:313–6.
doi: 10.1016/j.eururo.2016.06.018
Kroon P, Berry PA, Stower MJ, Rodrigues G, Mann VM, Simms M, Bhasin D, Chettiar S, Li C, Li PK, Maitland NJ, Collins AT. JAK-STAT blockade inhibits tumor initiation and clonogenic recovery of prostate cancer stem-like cells. Cancer Res. 2013;73:5288–98.
doi: 10.1158/0008-5472.CAN-13-0874
Huang S, Liu Q, Liao Q, Wu Q, Sun B, Yang Z, et al. Interleukin-6/signal transducer and activator of transcription 3 promotes prostate cancer resistance to androgen deprivation therapy via regulating pituitary tumor transforming gene 1 expression. Cancer Sci. 2018;109:678–87.
doi: 10.1111/cas.13493
Chung TD, Yu JJ, Spiotto MT, Bartkowski M, Simons JW. Characterization of the role of IL-6 in the progression of prostate cancer. Prostate. 1999;38:199–207.
doi: 10.1002/(SICI)1097-0045(19990215)38:3<199::AID-PROS4>3.0.CO;2-H
Clark J, Edwards S, Feber A, Flohr P, John M, Giddings I, et al. Genome-wide screening for complete genetic loss in prostate cancer by comparative hybridization onto cDNA microarrays. Oncogene. 2003;22:1247–52.
doi: 10.1038/sj.onc.1206247
Keller ET, Chang C, Ershler WB. Inhibition of NFkappaB activity through maintenance of IkappaBalpha levels contributes to dihydrotestosterone-mediated repression of the interleukin-6 promoter. J Biol Chem. 1996;271:26267–75.
doi: 10.1074/jbc.271.42.26267
Asbagh LA, Uzunoglu S, Cal C. Zoledronic acid effects interleukin-6 expression in hormone-independent prostate cancer cell lines. Int Braz J Urol. 2008;34:355–63.
doi: 10.1590/S1677-55382008000300013
Zitvogel L, Kroemer G. Targeting PD-1/PD-L1 interactions for cancer immunotherapy. Oncoimmunology. 2012;1:1223–5.
doi: 10.4161/onci.21335
Beldi-Ferchiou A, Caillat-Zucman S. Control of NK cell activation by immune checkpoint molecules. Int J Mol Sci. 2017;18:pii: E2129.
doi: 10.3390/ijms18102129
Rozali EN, Hato SV, Robinson BW, Lake RA, Lesterhuis WJ. Programmed death ligand 2 in cancer-induced immune suppression. Clin Dev Immunol. 2012;2012:656340.
doi: 10.1155/2012/656340
Mandai M, Hamanishi J, Abiko K, Matsumura N, Baba T, Konishi I. Dual faces of IFNγ in cancer progression: a role of PD-L1 induction in the determination of pro- and antitumor immunity. Clin Cancer Res. 2016;22:2329–34.
doi: 10.1158/1078-0432.CCR-16-0224
Kang YJ, Jeung IC, Park A, Park YJ, Jung H, Kim TD, et al. An increased level of IL-6 suppresses NK cell activity in peritoneal fluid of patients with endometriosis via regulation of SHP-2 expression. Hum Reprod. 2014;29:2176–89.
doi: 10.1093/humrep/deu172
Nakagawa S, Serada S, Kakubari R, Hiramatsu K, Sugase T, Matsuzaki S, et al. Intratumoral delivery of an adenoviral vector carrying the SOCS-1 gene enhances T cell-mediated anti-tumor immunity by suppressing PD-L1. Mol. Cancer Ther. 2018;17:1941–50.