Oncolytic Vaccinia Virus Expressing White-Spotted Charr Lectin Regulates Antiviral Response in Tumor Cells and Inhibits Tumor Growth In Vitro and In Vivo
Abstract
:1. Introduction
2. Results
2.1. Cytotoxicity of oncoVV-WCL in Cancer Cells
2.2. Apoptotic Effect of oncoVV-WCL in Huh-7 Cells
2.3. Replication of Oncolytic Vaccinia Virus Improved by WCL
2.4. Onco VV-WCL Stimulated the Production of Type I IFNs
2.5. OncoVV-WCL Regulated the IFN-Induced Signaling and the Expression of IFN-Stimulated Genes
2.6. OncoVV-WCL Suppressed Hepatocellular Carcinoma Cell Growth In Vivo
3. Discussion
4. Materials and Methods
4.1. Cell Culture
4.2. Recombination of oncoVV-WCL
4.3. Western Blot
4.4. Animal Experiments
4.5. Cell Viability Detection and Flow Cytometry Assay
4.6. Virus Replication Assay
4.7. Reporter Assay
4.8. RNA Extraction and Semi-Quantitative PCR
4.9. qRT-PCR
4.10. Transcriptomic Analysis
4.11. Immunohistochemistry
4.12. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Sharon, N. Lectins: Carbohydrate-specific Reagents and Biological Recognition Molecules. J. Biol. Chem. 2007, 282, 2753–2764. [Google Scholar] [CrossRef] [Green Version]
- Catanzaro, E.; Calcabrini, C.; Bishayee, A.; Fimognari, C. Antitumor Potential of Marine and Freshwater Lectins. Mar. Drugs 2019, 18, 11. [Google Scholar] [CrossRef] [Green Version]
- Yau, T.; Dan, X.; Ng, C.C.; Ng, T.B. Lectins with potential for anti-cancer therapy. Molecules 2015, 20, 3791–3810. [Google Scholar] [CrossRef] [Green Version]
- Hayashi, K.; Walde, P.; Miyazaki, T.; Sakayama, K.; Nakamura, A.; Kameda, K.; Masuda, S.; Umakoshi, H.; Kato, K. Active Targeting to Osteosarcoma Cells and Apoptotic Cell Death Induction by the Novel Lectin Eucheuma serra Agglutinin Isolated from a Marine Red Alga. J. Drug Deliv. 2012, 2012, 842785. [Google Scholar] [CrossRef] [Green Version]
- Sugahara, T.; Ohama, Y.; Fukuda, A.; Hayashi, M.; Kawakubo, A.; Kato, K. The cytotoxic effect of Eucheuma serra agglutinin (ESA) on cancer cells and its application to molecular probe for drug delivery system using lipid vesicles. Cytotechnology 2001, 36, 93–99. [Google Scholar] [CrossRef]
- Omokawa, Y.; Miyazaki, T.; Walde, P.; Akiyama, K.; Sugahara, T.; Masuda, S.; Inada, A.; Ohnishi, Y.; Saeki, T.; Kato, K. In vitro and in vivo anti-tumor effects of novel Span 80 vesicles containing immobilized Eucheuma serra agglutinin. Int. J. Pharm. 2010, 389, 157–167. [Google Scholar] [CrossRef]
- Chernikov, O.; Kuzmich, A.; Chikalovets, I.; Molchanova, V.; Hua, K.-F. Lectin CGL from the sea mussel Crenomytilus grayanus induces Burkitt’s lymphoma cells death via interaction with surface glycan. Int. J. Biol. Macromol. 2017. [Google Scholar] [CrossRef]
- Liao, J.-H.; Chien, C.-T.H.; Wu, H.-Y.; Wu, K.-F.; Wang, I.; Ho, M.-R.; Tu, I.-F.; Lee, I.-M.; Li, W.; Shih, Y.-L. A Multivalent Marine Lectin from Crenomytilus grayanus Possesses Anti-cancer Activity through Recognizing Globotriose Gb3. J. Am. Chem. Soc. 2016, 138, 4787–4795. [Google Scholar] [CrossRef]
- Fujii, Y.; Fujiwara, T.; Koide, Y.; Hasan, I.; Sugawara, S.; Rajia, S.; Kawsar, S.M.A.; Yamamoto, D.; Araki, D.; Kanaly, R.A. Internalization of a novel, huge lectin from Ibacus novemdentatus (slipper lobster) induces apoptosis of mammalian cancer cells. Glycoconj. J. 2017. [Google Scholar] [CrossRef]
- Shen, Y.; Nemunaitis, J. Fighting cancer with vaccinia virus: teaching new tricks to an old dog. Mol. Ther. J. Am. Soc. Gene Ther. 2005, 11, 180–195. [Google Scholar] [CrossRef] [PubMed]
- Kirn, D.H.; Thorne, S.H. Targeted and armed oncolytic poxviruses: A novel multi-mechanistic therapeutic class for cancer. Nat. Rev. Cancer 2009, 9, 64–71. [Google Scholar] [CrossRef] [PubMed]
- Ekeke, C.N.; Russell, K.L.; Joubert, K.; Bartlett, D.L.; Luketich, J.D.; Soloff, A.C.; Guo, Z.S.; Lotze, M.T.; Dhupar, R. Fighting Fire with Fire: Oncolytic Virotherapy for Thoracic Malignancies. Ann. Surg. Oncol. 2021. [Google Scholar] [CrossRef]
- Heo, J.; Reid, T.; Ruo, L.; Breitbach, C.J.; Rose, S.; Bloomston, M.; Cho, M.; Lim, H.Y.; Chung, H.C.; Kim, C.W.; et al. Randomized dose-finding clinical trial of oncolytic immunotherapeutic vaccinia JX-594 in liver cancer. Nat. Med. 2013, 19, 329–336. [Google Scholar] [CrossRef] [PubMed]
- Aitcheson, G.; Pillai, A.; Dahman, B.; John, B.V. Recent Advances in Systemic Therapies for Advanced Hepatocellular Carcinoma. Curr. Hepatol. Rep. 2021, 1–11. [Google Scholar] [CrossRef]
- Breitbach, C.J.; Thorne, S.H.; Bell, J.C.; Kirn, D.H. Targeted and armed oncolytic poxviruses for cancer: The lead example of JX-594. Curr. Pharm. Biotechnol. 2012, 13, 1768–1772. [Google Scholar] [CrossRef]
- Kim, S.-G.; Ha, H.K.; Lim, S.-n.; Silva, N.S.D.; Pelusio, A.; Mun, J.H.; Patt, R.H.; Breitbach, C.J.; Burke, J.M. Phase II trial of pexa-vec (pexastimogene devacirepvec; JX-594), an oncolytic and immunotherapeutic vaccinia virus, in patients with metastatic, refractory renal cell carcinoma (RCC). J. Clin. Oncol. 2018, 36 (Suppl. 6), 671–671. [Google Scholar] [CrossRef]
- Breitbach, C.J.; Moon, A.; Burke, J.; Hwang, T.H.; Kirn, D.H. A Phase 2, Open-Label, Randomized Study of Pexa-Vec (JX-594) Administered by Intratumoral Injection in Patients with Unresectable Primary Hepatocellular Carcinoma. Methods Mol. Biol. 2015, 1317, 343–357. [Google Scholar]
- Li, G.; Cheng, J.; Mei, S.; Wu, T.; Ye, T. Tachypleus tridentatus Lectin Enhances Oncolytic Vaccinia Virus Replication to Suppress In Vivo Hepatocellular Carcinoma Growth. Mar. Drugs 2018, 16, 200. [Google Scholar] [CrossRef] [Green Version]
- Wu, T.; Xiang, Y.; Liu, T.; Wang, X.; Ren, X.; Ye, T.; Li, G. Oncolytic Vaccinia Virus Expressing Aphrocallistes vastus Lectin as a Cancer Therapeutic Agent. Mar. Drugs 2019, 17, 363. [Google Scholar] [CrossRef] [Green Version]
- Tateno, H.; Ogawa, T.; Muramoto, K.; Kamiya, H.; Saneyoshi, M. Distribution and molecular evolution of rhamnose-binding lectins in Salmonidae: isolation and characterization of two lectins from white-spotted Charr (Salvelinus leucomaenis) eggs. Biosci. Biotechnol. Biochem. 2002, 66, 1356–1365. [Google Scholar] [CrossRef]
- Vázquez, M.I.; Rivas, G.; Cregut, D.; Serrano, L.; Esteban, M. The vaccinia virus 14-kilodalton (A27L) fusion protein forms a triple coiled-coil structure and interacts with the 21-kilodalton (A17L) virus membrane protein through a C-terminal alpha-helix. J. Virol. 1998, 72, 10126–10137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smith, G.L.; Talbot-Cooper, C.; Lu, Y. How Does Vaccinia Virus Interfere with Interferon? Adv. Virus Res. 2018, 100, 355–378. [Google Scholar] [PubMed]
- Aaronson, D.S.; Horvath, C.M. A road map for those who don’t know JAK-STAT. Science 2002, 296, 1653–1655. [Google Scholar] [CrossRef]
- Puhlmann, M.; Gnant, M.; Brown, C.K.; Alexander, H.R.; Bartlett, D.L. Thymidine kinase-deleted vaccinia virus expressing purine nucleoside phosphorylase as a vector for tumor-directed gene therapy. Hum. Gene Ther. 1999, 10, 649–657. [Google Scholar] [CrossRef]
- Kim, M. Replicating poxviruses for human cancer therapy. J. Microbiol. 2015, 53, 209–218. [Google Scholar] [CrossRef]
- Guo, Z.S.; Lu, B.; Guo, Z.; Giehl, E.; Feist, M.; Dai, E.; Liu, W.; Storkus, W.J.; He, Y.; Liu, Z.; et al. Vaccinia virus-mediated cancer immunotherapy: cancer vaccines and oncolytics. J. Immunother. Cancer 2019, 7, 6. [Google Scholar] [CrossRef]
- Jia, X.; Chen, Y.; Zhao, X.; Lv, C.; Yan, J. Oncolytic vaccinia virus inhibits human hepatocellular carcinoma MHCC97-H cell proliferation via endoplasmic reticulum stress, autophagy and Wnt pathways. J. Gene Med. 2016, 18, 211–219. [Google Scholar] [CrossRef]
- Maniatis, T.; Falvo, J.V.; Kim, T.H.; Kim, T.K.; Lin, C.H.; Parekh, B.S.; Wathelet, M.G. Structure and function of the interferon-beta enhanceosome. Cold Spring Harb. Symp. Quant. Biol. 1998, 63, 609–620. [Google Scholar] [CrossRef]
- Villarroya-Beltri, C.; Guerra, S.; Sánchez-Madrid, F. ISGylation—A key to lock the cell gates for preventing the spread of threats. J. Cell Sci. 2017, 130, 2961–2969. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Diamond, M.S. IFIT1: A dual sensor and effector molecule that detects non-2′-O methylated viral RNA and inhibits its translation. Cytokine Growth Factor Rev. 2014, 25, 543–550. [Google Scholar] [CrossRef]
- Pidugu, V.K.; Pidugu, H.B.; Wu, M.M.; Liu, C.J.; Lee, T.C. Emerging Functions of Human IFIT Proteins in Cancer. Front. Mol. Biosci. 2019, 6, 148. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, J.; Ghosh, A.; Sarkar, S.N. OASL-a new player in controlling antiviral innate immunity. Curr. Opin. Virol. 2015, 12, 15–19. [Google Scholar] [CrossRef] [Green Version]
- Asgari, S.; Schlapbach, L.J.; Anchisi, S.; Hammer, C.; Bartha, I.; Junier, T.; Mottet-Osman, G.; Posfay-Barbe, K.M.; Longchamp, D.; Stocker, M.; et al. Severe viral respiratory infections in children with IFIH1 loss-of-function mutations. Proc. Natl. Acad. Sci. USA 2017, 114, 8342–8347. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Euhus, D.M.; Hudd, C.; LaRegina, M.C.; Johnson, F.E. Tumor measurement in the nude mouse. J. Surg. Oncol. 1986, 31, 229–234. [Google Scholar] [CrossRef]
- Tomayko, M.M.; Reynolds, C.P. Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother. Pharmacol. 1989, 24, 148–154. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wang, X.; Zhou, N.; Liu, T.; Jia, X.; Ye, T.; Chen, K.; Li, G. Oncolytic Vaccinia Virus Expressing White-Spotted Charr Lectin Regulates Antiviral Response in Tumor Cells and Inhibits Tumor Growth In Vitro and In Vivo. Mar. Drugs 2021, 19, 292. https://doi.org/10.3390/md19060292
Wang X, Zhou N, Liu T, Jia X, Ye T, Chen K, Li G. Oncolytic Vaccinia Virus Expressing White-Spotted Charr Lectin Regulates Antiviral Response in Tumor Cells and Inhibits Tumor Growth In Vitro and In Vivo. Marine Drugs. 2021; 19(6):292. https://doi.org/10.3390/md19060292
Chicago/Turabian StyleWang, Xue, Ningning Zhou, Tingting Liu, Xiaoyuan Jia, Ting Ye, Kan Chen, and Gongchu Li. 2021. "Oncolytic Vaccinia Virus Expressing White-Spotted Charr Lectin Regulates Antiviral Response in Tumor Cells and Inhibits Tumor Growth In Vitro and In Vivo" Marine Drugs 19, no. 6: 292. https://doi.org/10.3390/md19060292
APA StyleWang, X., Zhou, N., Liu, T., Jia, X., Ye, T., Chen, K., & Li, G. (2021). Oncolytic Vaccinia Virus Expressing White-Spotted Charr Lectin Regulates Antiviral Response in Tumor Cells and Inhibits Tumor Growth In Vitro and In Vivo. Marine Drugs, 19(6), 292. https://doi.org/10.3390/md19060292