Development of lung metastases in mouse models of tongue squamous cell carcinoma.
animal models
distant metastases
head and neck cancer
lymph node metastases
oral cancer
Journal
Oral diseases
ISSN: 1601-0825
Titre abrégé: Oral Dis
Pays: Denmark
ID NLM: 9508565
Informations de publication
Date de publication:
Apr 2021
Apr 2021
Historique:
received:
06
06
2020
revised:
14
07
2020
accepted:
16
07
2020
pubmed:
9
8
2020
medline:
3
3
2021
entrez:
9
8
2020
Statut:
ppublish
Résumé
Oral squamous cell carcinoma (OSCC) represents 3%-4% of all cancers. Despite the increasing incidence of OSCC distant metastasis and poor prognosis, few animal models of OSCC distant metastasis have been reported. In this study, we established mouse models of OSCC lung metastasis by orthotopic and tail vein injection of new OSCC cell lines. For the tail vein model, we used a novel cell line isolated from lung metastases reproduced in vivo after intravenous injection of HSC-3 GFP/luciferase cells and sorted for GFP expression (HSC-3 M1 GFP/luciferase). Lung metastases were assessed by imaging techniques and further confirmed by histology. For the orthotopic model, HSC-3 GFP/luciferase cells were injected into the tongue of athymic nude mice. The primary tumor and metastases were assessed by in vivo imaging, histology, and immunohistochemistry. The orthotopic model presented spontaneous lung metastases in 50% of the animals and lymph node metastases were present in 83% of cases. In the tail vein model, a lung metastasis rate of 60% was observed. Lung metastases were successfully reproduced by orthotopic and tail vein injection. Since lymph node metastases were present, the orthotopic model with HSC-3 GFP/luciferase cells may be suitable to investigate metastatic dissemination in OSCC.
Types de publication
Journal Article
Langues
eng
Pagination
494-505Informations de copyright
© 2020 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd. All rights reserved.
Références
Bais, M. V., Kukuruzinska, M., & Trackman, P. C. (2015). Orthotopic non-metastatic and metastatic oral cancer mouse models. Oral Oncology, 51(5), 476-482. https://doi.org/10.1016/j.oraloncology.2015.01.012
Bernier, J., Domenge, C., Ozsahin, M., Matuszewska, K., Lefèbvre, J.-L., Greiner, R. H., … European Organization for Research and Treatment of Cancer Trial 22931 (2004). Postoperative irradiation with or without concomitant chemotherapy for locally advanced head and neck cancer. The New England Journal of Medicine, 350(19), 1945-1952. https://doi.org/10.1056/NEJMoa032641
Braks, J. A. M., Spiegelberg, L., Koljenovic, S., Ridwan, Y., Keereweer, S., Kanaar, R., … Essers, J. (2015). Optical imaging of tumor response to hyperbaric oxygen treatment and irradiation in an orthotopic mouse model of head and neck squamous cell carcinoma. Molecular Imaging and Biology, 17(5), 633-642. https://doi.org/10.1007/s11307-015-0834-8
Chen, Y.-F., Chang, K.-W., Yang, I.-T., Tu, H.-F., & Lin, S.-C. (2019). Establishment of syngeneic murine model for oral cancer therapy. Oral Oncology, 95, 194-201. https://doi.org/10.1016/j.oraloncology.2019.06.026
Chen, Y.-F., Liu, C.-J., Lin, L.-H., Chou, C.-H., Yeh, L.-Y., Lin, S.-C., & Chang, K.-W. (2019). Establishing of mouse oral carcinoma cell lines derived from transgenic mice and their use as syngeneic tumorigenesis models. BMC Cancer, 19(1), 281. https://doi.org/10.1186/s12885-019-5486-7
Chi, A. C., Day, T. A., & Neville, B. W. (2015). Oral cavity and oropharyngeal squamous cell carcinoma - An update. CA: A Cancer Journal for Clinicians, 65(5), 401-421. https://doi.org/10.3322/caac.21293
Colevas, A. D., Yom, S. S., Pfister, D. G., Spencer, S., Adelstein, D., Adkins, D., … Darlow, S. D. (2018). NCCN guidelines insights: Head and neck cancers, version 1.2018. Journal of the National Comprehensive Cancer Network, 16(5), 479-490. https://doi.org/10.6004/jnccn.2018.0026
de Visscher, S. A. H. J., Melchers, L. J., Dijkstra, P. U., Karakullukcu, B., Tan, I. B., Hopper, C., … Witjes, M. J. H. (2013). mTHPC-mediated photodynamic therapy of early stage oral squamous cell carcinoma: A comparison to surgical treatment. Annals of Surgical Oncology, 20(9), 3076-3082. https://doi.org/10.1245/s10434-013-3006-6
Erdem, N. F., Carlson, E. R., Gerard, D. A., & Ichiki, A. T. (2007). Characterization of 3 oral squamous cell carcinoma cell lines with different invasion and/or metastatic potentials. Journal of Oral and Maxillofacial Surgery, 65(9), 1725-1733. https://doi.org/10.1016/j.joms.2006.11.034
Furness, S., Glenny, A.-M., Worthington, H. V., Pavitt, S., Oliver, R., Clarkson, J. E., Conway, D. I. (2011). Interventions for the treatment of oral cavity and oropharyngeal cancer: chemotherapy. Cochrane Database of Systematic Reviews, 4(4), CD006386. https://doi.org/10.1002/14651858.CD006386.pub3
Harrington, K. J., Ferris, R. L., Blumenschein, G., Colevas, A. D., Fayette, J., Licitra, L., … Guigay, J. (2017). Nivolumab versus standard, single-agent therapy of investigator’s choice in recurrent or metastatic squamous cell carcinoma of the head and neck (CheckMate 141): Health-related quality-of-life results from a randomised, phase 3 trial. The Lancet Oncology, 18(8), 1104-1115. https://doi.org/10.1016/S1470-2045(17)30421-7
Hasegawa, T., Shibuya, Y., Takeda, D., Iwata, E., Saito, I., Kakei, Y., … Komori, T. (2017). Prognosis of oral squamous cell carcinoma patients with level IV/V metastasis: An observational study. Journal of Cranio-Maxillo-Facial Surgery, 45(1), 145-149. https://doi.org/10.1016/j.jcms.2016.10.011
Hier, M. P., Black, M. J., Shenouda, G., Sadeghi, N., & Karp, S. E. (1995). A murine model for the immunotherapy of head and neck squamous cell carcinoma. The Laryngoscope, 105(10), 1077-1080. https://doi.org/10.1288/00005537-199510000-00013
Hyakusoku, H., Sano, D., Takahashi, H., Hatano, T., Isono, Y., Shimada, S., … Oridate, N. (2016). JunB promotes cell invasion, migration and distant metastasis of head and neck squamous cell carcinoma. Journal of Experimental & Clinical Cancer Research, 35(1), 6. https://doi.org/10.1186/s13046-016-0284-4
Irani, S. (2016). Distant metastasis from oral cancer: A review and molecular biologic aspects. Journal of International Society of Preventive & Community Dentistry, 6(4), 265-271. https://doi.org/10.4103/2231-0762.186805
Ishida, K., Tomita, H., Nakashima, T., Hirata, A., Tanaka, T., Shibata, T., & Hara, A. (2017). Current mouse models of oral squamous cell carcinoma: Genetic and chemically induced models. Oral Oncology, 73, 16-20. https://doi.org/10.1016/j.oraloncology.2017.07.028
Jouhi, L., Datta, N., Renkonen, S., Atula, T., Mäkitie, A., Haglund, C., … Hagström, J. (2015). Expression of toll-like receptors in HPV-positive and HPV-negative oropharyngeal squamous cell carcinoma - An in vivo and in vitro study. Tumour Biology, 36(10), 7755-7764. https://doi.org/10.1007/s13277-015-3494-z
Kauppila, J. H., Mattila, A. E., Karttunen, T. J., & Salo, T. (2013). Toll-like receptor 5 (TLR5) expression is a novel predictive marker for recurrence and survival in squamous cell carcinoma of the tongue. British Journal of Cancer, 108(3), 638-643. https://doi.org/10.1038/bjc.2012.589
Kawashiri, S., Kumagai, S., Kojima, K., Harada, H., Nakagawa, K., & Yamamoto, E. (1999). Reproduction of occult metastasis of head and neck cancer in nude mice. Clinical & Experimental Metastasis, 17(4), 277-282.
Kawashiri, S., Noguchi, N., Tanaka, A., Nakaya, H., Kato, K., & Yamamoto, E. (2009). Inhibitory effect of neoadjuvant chemotherapy on metastasis of oral squamous cell carcinoma in a mouse model. Oral Oncology, 45(9), 794-797. https://doi.org/10.1016/j.oraloncology.2008.12.003
Li, P., Zhou, G., Zhu, X., Li, G., Yan, P., Shen, L., … Hamblin, M. R. (2012). Photodynamic therapy with hyperbranched poly(ether-ester) chlorin(e6) nanoparticles on human tongue carcinoma CAL-27 cells. Photodiagnosis and Photodynamic Therapy, 9(1), 76-82. https://doi.org/10.1016/j.pdpdt.2011.08.001
Li, Q., Dong, H., Yang, G., Song, Y., Mou, Y., & Ni, Y. (2020). Mouse tumor-bearing models as preclinical study platforms for oral squamous cell carcinoma. Frontiers in Oncology, 10, 212. https://doi.org/10.3389/fonc.2020.00212
Li, W., Zhu, D., & Qin, S. (2018). SIRT7 suppresses the epithelial-to-mesenchymal transition in oral squamous cell carcinoma metastasis by promoting SMAD4 deacetylation. Journal of Experimental & Clinical Cancer Research, 37(1), 148. https://doi.org/10.1186/s13046-018-0819-y
Lou, E., Kellman, R. M., Hutchison, R., & Shillitoe, E. J. (2003). Clinical and pathological features of the murine AT-84 orthotopic model of oral cancer. Oral Diseases, 9(6), 305-312. https://doi.org/10.1034/j.1601-0825.2003.00968.x
Lu, D. J., Luu, M., Mita, A., Scher, K., Shiao, S. L., Yoshida, E. P., Zumsteg, Z. S. (2018). Human papillomavirus-associated oropharyngeal cancer among patients aged 70 and older: Dramatically increased prevalence and clinical implications. European Journal of Cancer (Oxford, England: 1990), 103, 195-204. https://doi.org/10.1016/j.ejca.2018.08.015
Masood, R., Hochstim, C., Cervenka, B., Zu, S., Baniwal, S. K., Patel, V., … Sinha, U. K. (2013). A novel orthotopic mouse model of head and neck cancer and lymph node metastasis. Oncogenesis, 2(9), e68. https://doi.org/10.1038/oncsis.2013.33
Matsui, T., Ota, T., Ueda, Y., Tanino, M., & Odashima, S. (1998). Isolation of a highly metastatic cell line to lymph node in human oral squamous cell carcinoma by orthotopic implantation in nude mice. Oral Oncology, 34(4), 253-256. https://doi.org/10.1016/S1368-8375(98)80003-1
Mermod, M., Hiou-Feige, A., Bovay, E., Roh, V., Sponarova, J., Bongiovanni, M., … Simon, C. (2018). Mouse model of postsurgical primary tumor recurrence and regional lymph node metastasis progression in HPV-related head and neck cancer. International Journal of Cancer, 142(12), 2518-2528. https://doi.org/10.1002/ijc.31240
Mognetti, B., Di Carlo, F., & Berta, G. N. (2006). Animal models in oral cancer research. Oral Oncology, 42(5), 448-460. https://doi.org/10.1016/j.oraloncology.2005.07.014
Myers, J. N., Holsinger, F. C., Jasser, S. A., Bekele, B. N., & Fidler, I. J. (2002). An orthotopic nude mouse model of oral tongue squamous cell carcinoma. Clinical Cancer Research 8(1), 293-298. https://doi.org/10.1016/j.ejca.2018.08.015
Naruse, T., Yanamoto, S., Matsushita, Y., Sakamoto, Y., Morishita, K., Ohba, S., … Umeda, M. (2016). Cetuximab for the treatment of locally advanced and recurrent/metastatic oral cancer: An investigation of distant metastasis. Molecular and Clinical Oncology, 5(2), 246-252. https://doi.org/10.3892/mco.2016.928
Noguchi, N., Kawashiri, S., Tanaka, A., Kato, K., & Nakaya, H. (2003). Effects of fibroblast growth inhibitor on proliferation and metastasis of oral squamous cell carcinoma. Oral Oncology, 39(3), 240-247. https://doi.org/10.1016/S1368-8375(02)00092-1
Noguti, J., De Moura, C. F. G., De Jesus, G. P. P., Da Silva, V. H. P., Hossaka, T. A., Oshima, C. T. F., & Ribeiro, D. A. (2012). Metastasis from oral cancer: An overview. Cancer Genomics & Proteomics, 9(5), 329-335.
Ohara, T., Takaoka, M., Sakurama, K., Nagaishi, K., Takeda, H., Shirakawa, Y., … Naomoto, Y. (2010). The establishment of a new mouse model with orthotopic esophageal cancer showing the esophageal stricture. Cancer Letters, 293(2), 207-212. https://doi.org/10.1016/j.canlet.2010.01.017
Osaki, T., Yoneda, K., Yamamoto, T., Kimura, T., Matuoka, H., Sakai, H., & Ryoke, K. (2000). Clinical investigation on pulmonary metastasis of head and neck carcinomas. Oncology, 59(3), 196-203. https://doi.org/10.1159/000012161
Patel, V., Marsh, C. A., Dorsam, R. T., Mikelis, C. M., Masedunskas, A., Amornphimoltham, P., … Gutkind, J. S. (2011). Decreased lymphangiogenesis and lymph node metastasis by mTOR inhibition in head and neck cancer. Cancer Research, 71(22), 7103-7112. https://doi.org/10.1158/0008-5472.CAN-10-3192
Rossa, C., & D’Silva, N. J. (2019). Immune-relevant aspects of murine models of head and neck cancer. Oncogene, 38(21), 3973-3988. https://doi.org/10.1038/s41388-019-0686-9
Sano, D., & Myers, J. N. (2009). Xenograft models of head and neck cancers. Head & Neck Oncology, 1(1), 32. https://doi.org/10.1186/1758-3284-1-32
Sano, D., Xie, T.-X., Ow, T. J., Zhao, M., Pickering, C. R., Zhou, G., … Myers, J. N. (2011). Disruptive TP53 mutation is associated with aggressive disease characteristics in an orthotopic murine model of oral tongue cancer. Clinical Cancer Research, 17(21), 6658-6670. https://doi.org/10.1158/1078-0432.CCR-11-0046
Saxena, M., & Christofori, G. (2013). Rebuilding cancer metastasis in the mouse. Molecular Oncology, 7(2), 283-296. https://doi.org/10.1016/j.molonc.2013.02.009
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., … Cardona, A. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9(7), 676-682. https://doi.org/10.1038/nmeth.2019
Steeg, P. S. (2016). Targeting metastasis. Nature Reviews Cancer, 16(4), 201-218. https://doi.org/10.1038/nrc.2016.25
Sugiura, T., Inoue, Y., Matsuki, R., Ishii, K., Takahashi, M., Abe, M., & Shirasuna, K. (2009). VEGF-C and VEGF-D expression is correlated with lymphatic vessel density and lymph node metastasis in oral squamous cell carcinoma: Implications for use as a prognostic marker. International Journal of Oncology, 34(3), 673-680. https://doi.org/10.3892/ijo_00000193
Sugiyama, M., Bhawal, U. K., Dohmen, T., Ono, S., Miyauchi, M., & Ishikawa, T. (2003). Detection of human papillomavirus-16 and HPV-18 DNA in normal, dysplastic, and malignant oral epithelium. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics, 95(5), 594-600. https://doi.org/10.1067/moe.2003.36
Sutton, D., Brown, J., Rogers, S., Vaughan, E., & Woolgar, J. (2003). The prognostic implications of the surgical margin in oral squamous cell carcinoma. International Journal of Oral and Maxillofacial Surgery, 32(1), 30-34. https://doi.org/10.1054/ijom.2002.0313
Takahashi, M., Aoki, T., Nakamura, N., Carreras, J., Kajiwara, H., Kumaki, N., … Ota, Y. (2014). Clinicopathological analysis of 502 patients with oral squamous cell carcinoma with special interest to distant metastasis. The Tokai Journal of Experimental and Clinical Medicine, 39(4), 178-185.
Tamada, Y., Aoki, D., Nozawa, S., & Irimura, T. (2004). Model for paraaortic lymph node metastasis produced by orthotopic implantation of ovarian carcinoma cells in athymic nude mice. European Journal of Cancer, 40(1), 158-163. https://doi.org/10.1016/j.ejca.2003.08.008
Umeda, M., Yokoo, S., Komori, T., Nishimatsu, N., Shibuya, Y., & Fujioka, M. (2001). Experimental model of invasion and metastasis by orthotopic transplantation of oral squamous and adenoid cystic carcinomas into the tongue of nude mice. The British Journal of Oral & Maxillofacial Surgery, 39(5), 376-380. https://doi.org/10.1054/bjom.2000.0590
Wu, T.-F., Chen, L., Bu, L.-L., Gao, J., Zhang, W.-F., & Jia, J. (2017). CD44 + cancer cell-induced metastasis: A feasible neck metastasis model. European Journal of Pharmaceutical Sciences, 101, 243-250. https://doi.org/10.1016/j.ejps.2017.02.020
Xu, R., Zhang, G., Mai, J., Deng, X., Segura-Ibarra, V., Wu, S., … Shen, H. (2016). An injectable nanoparticle generator enhances delivery of cancer therapeutics. Nature Biotechnology, 34(4), 414-418. https://doi.org/10.1038/nbt.3506