2,554
Views
4
CrossRef citations to date
0
Altmetric
Research Paper

Poly(I:C) transfection induces a pro-inflammatory cascade in murine mammary carcinoma and fibrosarcoma cells

, , , , & ORCID Icon
Pages 841-851 | Received 04 Apr 2022, Accepted 27 May 2022, Published online: 23 Jun 2022

References

  • Li D, Wu M. Pattern recognition receptors in health and diseases. Signal Transduct Target Ther. 2021;6(1):291.
  • Alexopoulou L, Holt AC, Medzhitov R, et al. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature. 2001;413(6857):732–738.
  • Kato H, Takeuchi O, Sato S, et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature. 2006;441(7089):101–105.
  • Hornung V, Ellegast J, Kim S, et al. 5’-Triphosphate RNA is the ligand for RIG-I. Science. 2006;314(5801):994–997.
  • Thapa RJ, Ingram JP, Ragan KB, et al. DAI Senses Influenza A Virus Genomic RNA and Activates RIPK3-Dependent Cell Death. Cell Host Microbe. 2016;20(5):674–681.
  • Schlee M, Hartmann G. Discriminating self from non-self in nucleic acid sensing. Nat Rev Immunol. 2016;16(9):566–580.
  • Kim T, Pazhoor S, Bao M, et al. Aspartate-glutamate-alanine-histidine box motif (DEAH)/RNA helicase A helicases sense microbial DNA in human plasmacytoid dendritic cells. Proc Natl Acad Sci U S A. 2010;107(34):15181–15186.
  • Miyashita M, Oshiumi H, Matsumoto M, et al. DDX60, a DEXD/H box helicase, is a novel antiviral factor promoting RIG-I-like receptor-mediated signaling. Mol Cell Biol. 2011;31(18):3802–3819.
  • Jiang Z, Wei F, Zhang Y, et al. IFI16 directly senses viral RNA and enhances RIG-I transcription and activation to restrict influenza virus infection. Nat Microbiol. 2021;6(7):932–945.
  • Liu G, Gack MU. Distinct and Orchestrated Functions of RNA Sensors in Innate Immunity. Immunity. 2020;53(1):26–42.
  • Sayour EJ, Mitchell DA. Manipulation of Innate and Adaptive Immunity through Cancer Vaccines. J Immunol Res. 2017;2017:3145742.
  • Glavan TM, Pavelic J. The exploitation of Toll-like receptor 3 signaling in cancer therapy. Curr Pharm Des. 2014;20(42):6555–6564.
  • Ammi R, De Waele J, Willemen Y, et al. Poly(I:C) as cancer vaccine adjuvant: knocking on the door of medical breakthroughs. Pharmacol Ther. 2015;146:120–131.
  • Le Naour J, Galluzzi L, Zitvogel L, et al. Trial watch: TLR3 agonists in cancer therapy. Oncoimmunology. 2020;9(1):1771143.
  • Sultan H, Salazar AM, Celis E. Poly-ICLC, a multi-functional immune modulator for treating cancer. Semin Immunol. 2020;49:101414.
  • Vargason AM, Anselmo AC, Mitragotri S. The evolution of commercial drug delivery technologies. Nat Biomed Eng. 2021;5(9):951–967.
  • Neumann E, Schaefer-Ridder M, Wang Y, et al. Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J. 1982;1(7):841–845.
  • Marty M, Sersa G, Garbay JR, et al. Electrochemotherapy - An easy, highly effective and safe treatment of cutaneous and subcutaneous metastases: results of ESOPE (European Standard Operating Procedures of Electrochemotherapy) study. EJC Suppl. 2006;4(11):3–13.
  • Gehl J, Sersa G, Matthiessen LW, et al. Updated standard operating procedures for electrochemotherapy of cutaneous tumours and skin metastases. Acta oncologica. 2018;57(7):874–882.
  • Heller R, Heller LC. Gene electrotransfer clinical trials. Adv Genet. 2015;89:235–262.
  • Heller LC, Heller R. Gene Electrotransfer. In: Impellizeri JA, editor. Electroporation in Veterinary Oncology Practice: electrochemotherapy and Gene Electrotransfer for Immunotherapy. Cham: Springer International Publishing; 2021. p. 219–234.
  • Znidar K, Bosnjak M, Cemazar M, et al. Cytosolic DNA Sensor Upregulation Accompanies DNA Electrotransfer in B16.F10 Melanoma Cells. Mol Ther Nucleic Acids. 2016;5:e322.
  • Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3(6):1101–1108.
  • Rueden CT, Schindelin J, Hiner MC, et al. ImageJ2: imageJ for the next generation of scientific image data. BMC Bioinformatics. 2017;18(1):529.
  • Panda D, Gjinaj E, Bachu M, et al. IRF1 Maintains Optimal Constitutive Expression of Antiviral Genes and Regulates the Early Antiviral Response. Front Immunol. 2019;10:1019.
  • Feng H, Zhang YB, Gui JF, et al. Interferon regulatory factor 1 (IRF1) and anti-pathogen innate immune responses. PLoS Pathog. 2021;17(1):e1009220.
  • Fujita T, Reis LF, Watanabe N, et al. Induction of the transcription factor IRF-1 and interferon-beta mRNAs by cytokines and activators of second-messenger pathways. Proc Natl Acad Sci U S A. 1989;86(24):9936–9940.
  • Nair P, O’Donnell CM, Janasek K, et al. Lipopolysacchride-treated mammary carcinomas secrete proinflammatory chemokines and exhibit reduced growth rates in vivo, but not in vitro. Immunol Invest. 2009;38(8):730–748.
  • Bernardo AR, Cosgaya JM, Aranda A, et al. Synergy between RA and TLR3 promotes type I IFN-dependent apoptosis through upregulation of TRAIL pathway in breast cancer cells. Cell Death Dis. 2013;4(1):e479.
  • Salaun B, Coste I, Rissoan MC, et al. TLR3 can directly trigger apoptosis in human cancer cells. J Immunol. 2006;176(8):4894–4901.
  • Inao T, Harashima N, Monma H, et al. Antitumor effects of cytoplasmic delivery of an innate adjuvant receptor ligand, poly(I:C), on human breast cancer. Breast Cancer Res Treat. 2012;134(1):89–100.
  • Ultimo A, Gimenez C, Bartovsky P, et al. Targeting Innate Immunity with dsRNA-Conjugated Mesoporous Silica Nanoparticles Promotes Antitumor Effects on Breast Cancer Cells. Chemistry. 2016;22(5):1582–1586.
  • Zigler M, Shir A, Joubran S, et al. HER2-Targeted Polyinosine/Polycytosine Therapy Inhibits Tumor Growth and Modulates the Tumor Immune Microenvironment. Cancer Immunol Res. 2016;4(8):688–697.
  • Colapicchioni V, Palchetti S, Pozzi D, et al. Killing cancer cells using nanotechnology: novel poly(I:C) loaded liposome-silica hybrid nanoparticles. J Mater Chem B. 2015;3(37):7408–7416.
  • Ultimo A, de la Torre C, Gimenez C, et al. Nanoparticle-cell-nanoparticle communication by stigmergy to enhance poly(I:C) induced apoptosis in cancer cells. Chem Commun (Camb). 2020;56(53):7273–7276.
  • Fang L, Zhao Z, Wang J, et al. Light-controllable charge-reversal nanoparticles with polyinosinic-polycytidylic acid for enhancing immunotherapy of triple negative breast cancer. Acta Pharm Sin B. 2022;12(1):353–363.
  • Znidar K, Bosnjak M, Semenova N, et al. Tumor cell death after electrotransfer of plasmid DNA is associated with cytosolic DNA sensor upregulation. Oncotarget. 2018;9(27):18665–18681.
  • Galli R, Paone A, Fabbri M, et al. Toll-like receptor 3 (TLR3) activation induces microRNA-dependent reexpression of functional RARbeta and tumor regression. Proc Natl Acad Sci U S A. 2013;110(24):9812–9817.
  • Bernardo AR, Cosgaya JM, Aranda A, et al. Pro-apoptotic signaling induced by Retinoic acid and dsRNA is under the control of Interferon Regulatory Factor-3 in breast cancer cells. Apoptosis. 2017;22(7):920–932.
  • Wiedbrauk DL, Burleson GR. Production and Characterization of Poly(I):Poly(C)-Induced Rat Interferons In Vitro. J Interferon Res. 1986;6(3):281–295.
  • Yang J, Hagan MK, Offermann MK. Induction of IL-6 gene expression in Kaposi’s sarcoma cells. J Immunol. 1994;152(2):943–955.
  • Livengood AJ, Wu CC, Carson DA. Opposing roles of RNA receptors TLR3 and RIG-I in the inflammatory response to double-stranded RNA in a Kaposi’s sarcoma cell line. Cell Immunol. 2007;249(2):55–62.
  • Wu M, Yuan F, Rao J. Membrane binding of plasmid DNA and endocytic pathways are involved in electrotransfection of mammalian cells. PLoS One. 2011;6(6):e20923.
  • Rosazza C, Phez E, Escoffre JM, et al. Cholesterol implications in plasmid DNA electrotransfer: evidence for the involvement of endocytotic pathways. Int J Pharm. 2012;423(1):134–143.
  • Chan CP, Jin DY. Cytoplasmic RNA sensors and their interplay with RNA-binding partners in innate antiviral response: theme and variations. Rna. 2022;28(4):449–477.
  • Wu Y, Wu X, Wu L, et al. The anticancer functions of RIG-I-like receptors, RIG-I and MDA5, and their applications in cancer therapy. Transl Res. 2017;190:51–60.
  • Kato H, Takeuchi O, Mikamo-Satoh E, et al. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J Exp Med. 2008;205(7):1601–1610.
  • Semenova N, Bosnjak M, Markelc B, et al. Multiple cytosolic DNA sensors bind plasmid DNA after transfection. Nucleic Acids Res. 2019;47(19):10235–10246.
  • Oshiumi H, Miyashita M, Okamoto M, et al. DDX60 Is Involved in RIG-I-Dependent and Independent Antiviral Responses, and Its Function Is Attenuated by Virus-Induced EGFR Activation. Cell Rep. 2015;11(8):1193–1207.
  • Zhang Z, Yuan B, Lu N, et al. DHX9 pairs with IPS-1 to sense double-stranded RNA in myeloid dendritic cells. J Immunol. 2011;187(9):4501–4508.
  • Su C, Tang YD, Zheng C. DExD/H-box helicases: multifunctional regulators in antiviral innate immunity. Cell Mol Life Sci. 2021;79(1):2.
  • Sato M, Suemori H, Hata N, et al. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity. 2000;13(4):539–548.
  • Guney Eskiler G, Deveci Ozkan A. The relationship between the efficacy of talazoparib and the functional toll-like receptors 3 and 9 in triple negative breast cancer. Mol Immunol. 2022;141:280–286.
  • Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140(6):805–820.
  • Takaoka A, Wang Z, Choi MK, et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature. 2007;448(7152):501–505.
  • Came PE, Moore DH. Inhibition of spontaneous mammary carcinoma of mice by treatment with interferon and poly I:C. Proc Soc Exp Biol Med. 1971;137(1):304–305.
  • Potmesil M, Goldfeder A. Inhibitory effect of polyinosinic:polycytidylic acid on the growth of transplantable mouse mammary carcinoma. Proc Soc Exp Biol Med. 1972;139(4):1392–1397.
  • Anderson KM, Evans A, Kellen JA. Unimpaired development of DMBA-induced mammary tumors in rats treated with poly(I)-poly(C). Res Commun Chem Pathol Pharmacol. 1972;4(1):193–202.
  • Borden EC, Balkwill FR. Preclinical and clinical studies of interferons and interferon inducers in breast cancer. Cancer. 1984;53:783–789.
  • Dillon PM, Petroni GR, Smolkin ME, et al. A pilot study of the immunogenicity of a 9-peptide breast cancer vaccine plus poly-ICLC in early stage breast cancer. J Immunother Cancer. 2017;5(1):92.
  • Bloksma N, Kuper CF, Hofhuis FM, et al. Antitumour activity of endotoxin, concanavalin A and poly I: c and their ability to elicit tumour necrosis factor, cytostatic factors, and interferon in vivo. Cancer Immunol Immunother. 1983;16(1):35–39.
  • Salazar AM, Erlich RB, Mark A, et al. Therapeutic In Situ Autovaccination against Solid Cancers with Intratumoral Poly-ICLC: case Report, Hypothesis, and Clinical Trial. Cancer Immunol Res. 2014;2(8):720–724.