Microwave ablation combined with anti-PD-1/CTLA-4 therapy induces an antitumor immune response to renal cell carcinoma in a murine model

References

• Deleuze A, Saout J, Dugay F, et al. Immunotherapy in renal cell carcinoma: the future is now. Int J Mol Sci. 2020 Apr 5;21(7):2532.
   PubMed Web of Science ®Google Scholar
• Gray RE, Harris GT Renal cell carcinoma: diagnosis and management. Am Fam Physician. 2019 Feb 1;99(3):179–184.
   PubMed Web of Science ®Google Scholar
• Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: globocan estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021 May;71(3):209–249.
   PubMed Web of Science ®Google Scholar
• Siegel RL, Miller KD, Fuchs HE, et al. Cancer statistics, 2021. CA Cancer J Clin. 2021 Jan;71(1):7–33.
   PubMed Web of Science ®Google Scholar
• Kahlmeyer A, Stöhr CG, Hartmann A, et al. Expression of PD-1 and CTLA-4 are negative prognostic markers in renal cell carcinoma. J Clin Med. 2019 May 24;8(5):743.
   PubMed Web of Science ®Google Scholar
• Schoenfeld JD, Giobbie-Hurder A, Ranasinghe S, et al. Durvalumab plus tremelimumab alone or in combination with low-dose or hypofractionated radiotherapy in metastatic non-small-cell lung cancer refractory to previous PD(L)-1 therapy: an open-label, multicentre, randomised, phase 2 trial. Lancet Oncol. 2022 Feb;23(2):279–291. 10.1016/S1470-2045(21)00658-6
   PubMed Web of Science ®Google Scholar
• Zhou J, Mahoney KM, Giobbie-Hurder A, et al. Soluble PD-L1 as a biomarker in malignant melanoma treated with checkpoint blockade. Cancer Immunol Res. 2017 Jun;5(6):480–492.
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Motzer RJ Systemic therapy for metastatic renal-cell carcinoma. N Engl J Med. 2017 Jan 26;376(4):354–366.
   PubMed Web of Science ®Google Scholar
• Bex A, Mulders P, Jewett M, et al. Comparison of immediate vs deferred cytoreductive nephrectomy in patients with synchronous metastatic renal cell carcinoma receiving sunitinib: the SURTIME randomized clinical trial. JAMA Oncol. 2019 Feb 1;5(2):164–170.
   PubMed Web of Science ®Google Scholar
• Löffler MW, Nussbaum B, Jäger G, et al. A non-interventional clinical trial assessing immune responses after radiofrequency ablation of liver metastases from colorectal cancer. Front Immunol. 2019;10:2526.
   PubMed Web of Science ®Google Scholar
• Acksteiner C, Steinke K Percutaneous microwave ablation for early-stage non-small cell lung cancer (NSCLC) in the elderly: a promising outlook. J Med Imaging Radiat Oncol. 2015 Feb;59(1):82–90.
   PubMed Web of Science ®Google Scholar
• Matsui Y, Hiraki T, Gobara H, et al. Percutaneous thermal ablation for renal cell carcinoma in patients with birt-hogg-dubé syndrome. Diagn Interv Imaging. 2019 Nov;100(11):671–677.
   PubMed Web of Science ®Google Scholar
• Takaki H, Cornelis F, Kako Y, et al. Thermal ablation and immunomodulation: from preclinical experiments to clinical trials. Diagn Interv Imaging. 2017 Sep;98(9):651–659.
   PubMed Web of Science ®Google Scholar
• Rao P, Escudier B, de Baere T Spontaneous regression of multiple pulmonary metastases after radiofrequency ablation of a single metastasis. Cardiovasc Intervent Radiol. 2011 Apr;34(2):424–430.
   PubMed Web of Science ®Google Scholar
• Su T, Huang M, Liao J, et al. Insufficient radiofrequency ablation promotes hepatocellular carcinoma metastasis through N6-methyladenosine mRNA methylation-dependent mechanism. Hepatology. 2021 Sep;74(3):1339–1356. 10.1002/hep.31766
   PubMed Web of Science ®Google Scholar
• Yan P, Lyu X, Wang S, et al. Insufficient ablation promotes the metastasis of residual non-small cell lung cancer (NSCLC) cells via upregulating carboxypeptidase A4. Int J Hyperthermia. 2021;38(1):1037–1051.
   PubMed Web of Science ®Google Scholar
• Ahmad F, Gravante G, Bhardwaj N, et al. Changes in interleukin-1beta and 6 after hepatic microwave tissue ablation compared with radiofrequency, cryotherapy and surgical resections. Am J Surg. 2010 Oct;200(4):500–506.
   PubMed Web of Science ®Google Scholar
• Dolladille C, Ederhy S, Sassier M, et al. Immune checkpoint inhibitor rechallenge after immune-related adverse events in patients with cancer. JAMA Oncol. 2020 Jun 1;6(6):865–871.
   PubMed Web of Science ®Google Scholar
• Wang H, Guo X, Zhou J, et al. Clinical diagnosis and treatment of immune checkpoint inhibitor-associated pneumonitis. Thorac Cancer. 2020 Jan;11(1):191–197.
   PubMed Web of Science ®Google Scholar
• Amaria RN, Reddy SM, Tawbi HA, et al. Neoadjuvant immune checkpoint blockade in high-risk resectable melanoma. Nat Med. 2018 Nov;24(11):1649–1654.
   PubMed Web of Science ®Google Scholar
• Zhang H, Dai Z, Wu W, et al. Regulatory mechanisms of immune checkpoints PD-L1 and CTLA-4 in cancer. J Exp Clin Cancer Res. 2021 Jun 4;40(1):184.
   PubMed Web of Science ®Google Scholar
• Buchbinder EI, Desai A CTLA-4 and PD-1 pathways: similarities, differences, and implications of their inhibition. Am J Clin Oncol. 2016 Feb;39(1):98–106.
   PubMed Web of Science ®Google Scholar
• Gangaev A, Rozeman EA, Rohaan MW, et al. Differential effects of PD-1 and CTLA-4 blockade on the melanoma-reactive CD8 T cell response. Proc Natl Acad Sci U S a. 2021 Oct 26;118(43):e2102849118.
   PubMed Web of Science ®Google Scholar
• Duraiswamy J, Freeman GJ, Coukos G Therapeutic PD-1 pathway blockade augments with other modalities of immunotherapy T-cell function to prevent immune decline in ovarian cancer. Cancer Res. 2013 Dec 1;73(23):6900–6912.
   PubMed Web of Science ®Google Scholar
• Wei SC, Anang NAS, Sharma R, et al. Combination anti-CTLA-4 plus anti-PD-1 checkpoint blockade utilizes cellular mechanisms partially distinct from monotherapies. Proc Natl Acad Sci U S a. 2019 Nov 5;116(45):22699–22709.
   PubMed Web of Science ®Google Scholar
• Hamamoto S, Okuma T, Yamamoto A, et al. Radiofrequency ablation and immunostimulant OK-432: combination therapy enhances systemic antitumor immunity for treatment of VX2 lung tumors in rabbits. Radiology. 2013 May;267(2):405–413.
   PubMed Web of Science ®Google Scholar
• Raud B, McGuire PJ, Jones RG, et al. Fatty acid metabolism in CD8(+) T cell memory: challenging current concepts. Immunol Rev. 2018 May;283(1):213–231.
   PubMed Web of Science ®Google Scholar
• Tanaka A, Sakaguchi S Regulatory T cells in cancer immunotherapy. Cell Res. 2017 Jan;27(1):109–118.
   PubMed Web of Science ®Google Scholar
• Jorgovanovic D, Song M, Wang L, et al. Roles of IFN-γ in tumor progression and regression: a review. Biomark Res. 2020;8:49.
   PubMed Web of Science ®Google Scholar
• Lee HT, Lee SH, Heo YS Molecular interactions of antibody drugs targeting PD-1, PD-L1, and CTLA-4 in immuno-oncology. Molecules. 2019 Mar 26;24(6):1190.
   PubMed Web of Science ®Google Scholar
• Wei SC, Levine JH, Cogdill AP, et al. Distinct cellular mechanisms underlie anti-CTLA-4 and anti-PD-1 checkpoint blockade. Cell. 2017 Sep 7;170(6):1120–1133.e17.
   PubMed Web of Science ®Google Scholar
• Okazaki T, Iwai Y, Honjo T New regulatory co-receptors: Inducible co-stimulator and PD-1. Curr Opin Immunol. 2002 Dec;14(6):779–782.
   PubMed Web of Science ®Google Scholar
• Okazaki T, Honjo T PD-1 and PD-1 ligands: from discovery to clinical application. Int Immunol. 2007 Jul;19(7):813–824.
   PubMed Web of Science ®Google Scholar
• Yu Z, Geng J, Zhang M, et al. Treatment of osteosarcoma with microwave thermal ablation to induce immunogenic cell death. Oncotarget. 2014 Aug 15;5(15):6526–6539.
   PubMedGoogle Scholar
• Yu J, Liang P, Yu XL, et al. US-Guided percutaneous microwave ablation versus open radical nephrectomy for small renal cell carcinoma: intermediate-term results. Radiology. 2014 Mar;270(3):880–887.
   PubMed Web of Science ®Google Scholar
• Ahmad F, Gravante G, Bhardwaj N, et al. Renal effects of microwave ablation compared with radiofrequency, cryotherapy and surgical resection at different volumes of the liver treated. Liver Int. 2010 Oct;30(9):1305–1314.
   PubMed Web of Science ®Google Scholar
• Takahashi H, Berber E Role of thermal ablation in the management of colorectal liver metastasis. Hepatobiliary Surg Nutr. 2020 Feb;9(1):49–58.
   PubMed Web of Science ®Google Scholar
• Flynn MJ, Sayed AA, Sharma R, et al. Challenges and opportunities in the clinical development of immune checkpoint inhibitors for hepatocellular carcinoma. Hepatology. 2019 May;69(5):2258–2270.
   PubMed Web of Science ®Google Scholar
• Delaunay M, Cadranel J, Lusque A, et al. Immune-Checkpoint inhibitors associated with interstitial lung disease in cancer patients. Eur Respir J. 2017 Aug;50(2):1700050.
   PubMed Web of Science ®Google Scholar
• Slovak R, Ludwig JM, Gettinger SN, et al. Immuno-Thermal ablations - boosting the anticancer immune response. J Immunother Cancer. 2017 Oct 17;5(1):78.
   PubMedGoogle Scholar
• den Brok MHMGM, Sutmuller RPM, Nierkens S, et al. Efficient loading of dendritic cells following cryo and radiofrequency ablation in combination with immune modulation induces anti-tumour immunity. Br J Cancer. 2006 Oct 9;95(7):896–905.
   PubMed Web of Science ®Google Scholar
• Levy MY, Sidana A, Chowdhury WH, et al. Cyclophosphamide unmasks an antimetastatic effect of local tumor cryoablation. J Pharmacol Exp Ther. 2009 Aug;330(2):596–601.
   PubMed Web of Science ®Google Scholar
• Kong Y, Zhao X, Xu M, et al. PD-1 inhibitor combined with radiotherapy and GM-CSF (PRaG) in patients with metastatic solid tumors: an open-label phase II study. Front Immunol. 2022;13:952066.
   PubMed Web of Science ®Google Scholar
• Lin RA, Lin JK, Lin SY. Mechanisms of immunogenic cell death and immune checkpoint blockade therapy. Kaohsiung J Med Sci. 2021 Jun;37(6):448–458.
   PubMed Web of Science ®Google Scholar
• Legrand AJ, Konstantinou M, Goode EF, et al. The diversification of cell death and immunity: memento mori. Mol Cell. 2019 Oct 17;76(2):232–242.
   PubMed Web of Science ®Google Scholar
• Hijaze N, Ledersnaider M, Simanovich E, et al. Inducing regulated necrosis and shifting macrophage polarization with anti-EMMPRIN antibody (161-pAb) and complement factors. J Leukoc Biol. 2021 Aug;110(2):343–356.
   PubMed Web of Science ®Google Scholar
• Ahmed A, Tait SWG. Targeting immunogenic cell death in cancer. Mol Oncol. 2020 Dec;14(12):2994–3006.
   PubMed Web of Science ®Google Scholar
• Efimova I, Catanzaro E, Van der Meeren L, et al. Vaccination with early ferroptotic cancer cells induces efficient antitumor immunity. J Immunother Cancer. 2020 Nov;8(2):e001369.
   PubMed Web of Science ®Google Scholar
• Tappe KA, Budida R, Stankov MV, et al. Immunogenic cell death of dendritic cells following modified vaccinia virus ankara infection enhances CD8(+) T cell proliferation. Eur J Immunol. 2018 Dec;48(12):2042–2054.
   PubMed Web of Science ®Google Scholar
• O’Malley DM, Neffa M, Monk BJ, et al. Dual PD-1 and CTLA-4 checkpoint blockade using balstilimab and zalifrelimab combination as second-line treatment for advanced cervical cancer: an open-label phase II study. J Clin Oncol. 2022 Mar 1;40(7):762–771.
   PubMed Web of Science ®Google Scholar
• Curran MA, Montalvo W, Yagita H, et al. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci U S a. 2010 Mar 2;107(9):4275–4280.
   PubMed Web of Science ®Google Scholar
• Topalian SL, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012 Jun 28;366(26):2443–2454.
   PubMed Web of Science ®Google Scholar
• Taube JM, Klein A, Brahmer JR, et al. Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy. Clin Cancer Res. 2014 Oct 1;20(19):5064–5074.
   PubMed Web of Science ®Google Scholar
• Twyman-Saint Victor C, Rech AJ, Maity A, et al. Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature. 2015 Apr 16;520(7547):373–377.
   PubMed Web of Science ®Google Scholar
• Tartarone A, Roviello G, Lerose R, et al. Anti-PD-1 versus anti-PD-L1 therapy in patients with pretreated advanced non-small-cell lung cancer: a meta-analysis. Future Oncol. 2019 Jul;15(20):2423–2433.
   PubMed Web of Science ®Google Scholar
• Passiglia F, Galvano A, Rizzo S, et al. Looking for the best immune-checkpoint inhibitor in pre-treated NSCLC patients: an indirect comparison between nivolumab, pembrolizumab and atezolizumab. Int J Cancer. 2018 Mar 15;142(6):1277–1284.
   PubMed Web of Science ®Google Scholar
• Zhang L, Xu L, Wang Y, et al. Antitumor immunity augmented by combining radiofrequency ablation with anti-CTLA-4 therapy in a subcutaneous murine hepatoma model. J Vasc Interv Radiol. 2020 Jul;31(7):1178–1186.
   PubMed Web of Science ®Google Scholar
• Sobhani N, Tardiel-Cyril DR, Davtyan A, et al. CTLA-4 in regulatory T cells for cancer immunotherapy. Cancers (Basel). 2021 Mar 22;13(6):1440.
   PubMed Web of Science ®Google Scholar
• NCCN clinical practice guidelines in oncology (NCCN Guidelines®) kidney cancer, version 1. 2022- July 1, 2021: National Comprehensive Cancer Network; 2021 [cited 2021 July 11]. Available from: https://www.nccn.org/professionals/physician_gls/pdf/kidney.pdf
   Google Scholar
• Nocera L, Karakiewicz PI, Wenzel M, et al. Clinical outcomes and adverse events after first-line treatment in metastatic renal cell carcinoma: a systematic review and network meta-analysis. J Urol. 2021 Sep 21; 207(1):16–24.
   PubMed Web of Science ®Google Scholar