Preclinical models for oral squamous cell carcinoma investigations – review

Marika Zurmukhtashvili, Avtandil Machavariani, Giorgi Menabde, Ketevan Gogilashvili

Abstract


 

Background

In the last two decades, the recent advances and discoveries in genomic technologies have dramatically expanded our views and understanding of molecular genetic mechanisms and genetic anomalies underlying oral squamous cell carcinoma. Further experiments with relevant in vitro and in vivo experimental models are very important to gain deep knowledge of disease progression and therapeutic response. A relevant animal model is an essential key for understanding processes underlying the initiation and progression of oral cancer. There is a number of studies on different animals which can be used for models.

Aim

Therefore, this review aims to provide a reference and direction for researchers working in the field of oral oncology.

Methods

Data were collected using the electronic search method in the following databases: PubMed/Medline, Scopus. Terms “oral carcinoma”, AND “animal model” were utilized. English articles published between 2010-2019, with available summary were included.

Results

Total 138 articles were found from different sources. Finally, 65 were selected for this review. After analysis and synthesis of information from articles, we have described different models currently used in oral oncology research and have provided details regarding their establishment and differences in their mechanisms, characteristics, and applications as well as regarding selection methods

Conclusion

Due to the characteristics of OSCC comprehensive understanding of model establishment is crucial for thorough investigations of these diseases. Unfortunately, it is impossible to completely replicate the natural situation of oral cancer. Every different model using different animals should be considered in regard to the field of planned studies. Generally, it was demonstrated that mice models can come most close.


Keywords


oral cancer, cell line, animal model,

Full Text:

PDF

References


Forman D, Bray F, Brewster DH, Gombe Mbalawa C, Kohler B, Piñeros M, et al., editors. Cancer incidence in five continents. Volume X. Lyon: International Agency for Research on Cancer; 2014.

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 Mar;136(5):E359–86.

Majchrzak E, Szybiak B, Wegner A, Pienkowski P, Pazdrowski J, Luczewski L, et al. Oral cavity and oropharyngeal squamous cell carcinoma in young adults: a review of the literature. Radiol Oncol. 2014 Jan;48(1):1–10.

Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016 Jan-Feb;66(1):7–30.

Cheon DJ, Orsulic S. Mouse models of cancer. Annu Rev Pathol. 2011;6(1):95–119.

van der Horst G, van der Pluijm G. Preclinical models that illuminate the bone metastasis cascade. Recent Results Cancer Res. 2012;192:1–31.

Barré-Sinoussi F, Montagutelli X. Animal models are essential to biological research: issues and perspectives. Future Sci OA. 2015 Nov;1(4): FSO63.

Al Moustafa AE, editor. Development of Oral Cancer, Springer International Publishing AG 2017 23 https://doi.org/10.1007/978-3-319-48054-1.

Ohnishi Y, Inoue H, Furukawa M, Kakudo K, Nozaki M. Heparin-binding epidermal growth factor-like growth factor is a potent regulator of invasion activity in oral squamous cell carcinoma. Oncol Rep. 2012 Apr;27(4):954–8.

Szaniszlo P, Fennewald SM, Qiu S, Kantara C, Shilagard T, Vargas G, et al. Temporal characterization of lymphatic metastasis in an orthotopic mouse model of oral cancer. Head Neck. 2014 Nov;36(11):1638–47.

Montague MJ, Li G, Gandolfi B, Khan R, Aken BL, Searle SM, et al. Comparative analysis of the domestic cat genome reveals genetic signatures underlying feline biology and domestication. Proc Natl Acad Sci USA. 2014 Dec;111(48):17230–5.

Warner BM, Casto BC, Knobloch TJ, Accurso BT, Weghorst CM. Chemoprevention of oral cancer by topical application of black raspberries on high at-risk mucosa. Oral Surg Oral Med Oral Pathol Oral Radiol. 2014 Dec;118(6):674–83.

Vincent-Chong VK, DeJong H, Attwood K, Hershberger PA, Seshadri M. Preclinical prevention trial of calcitriol: impact of stage of intervention and duration of treatment on oral carcinogenesis. Neoplasia. 2019 Apr;21(4):376–88.

Khiavi MM, Abdal K, Abbasi MM, Hamishehkar H, Aghbali AA, Salehi R, et al. Comparison of injectable doxorubicin & its nanodrug complex chemotherapy for the treatment of 4-nitroquinoline-1-oxide induced oral squamous cell carcinoma in rats. Indian J Med Res. 2017 Jan;145(1):112–7.

Fulton AJ, Nemec A, Murphy BG, Kass PH, Verstraete FJ. Risk factors associated with survival in dogs with nontonsillar oral squamous cell carcinoma 31 cases (1990-2010). J Am Vet Med Assoc. 2013 Sep;243(5):696–702.

Soltero-Rivera MM, Krick EL, Reiter AM, Brown DC, Lewis JR. Prevalence of regional and distant metastasis in cats with advanced oral squamous cell carcinoma: 49 cases (2005-2011). J Feline Med Surg. 2014 Feb;16(2):164–9.

Rossa C Jr, D’Silva NJ. Non-murine models to investigate tumor-immune interactions in head and neck cancer. Oncogene. 2019 Jun;38(25):4902–14.

Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009 Jul;6(7):e1000097.

Brenner JC, Graham MP, Kumar B, Saunders LM, Kupfer R, Lyons RH, et al. Genotyping of 73 UM-SCC head and neck squamous cell carcinoma cell lines. Head Neck. 2010 Apr;32(4):417–26.

Zhao M, Sano D, Pickering CR, Jasser SA, Henderson YC, Clayman GL, et al. Assembly and initial characterization of a panel of 85 genomically validated cell lines from diverse head and neck tumor sites. Clin Cancer Res. 2011 Dec;17(23):7248–64.

Möckelmann N, Rieckmann T, Busch CJ, Becker B, Gleißner L, Hoffer K, et al. Effect of sorafenib on cisplatin-based chemoradiation in head and neck cancer cells. Oncotarget. 2016 Apr;7(17):23542–51.

Laban S, Steinmeister L, Gleißner L, Grob TJ, Grénman R, Petersen C, et al. Sorafenib sensitizes head and neck squamous cell carcinoma cells to ionizing radiation. Radiother Oncol 2013;109:286–92. . radonc.2013.07.003. https://doi.org/10.1016/j.radonc.2013.07.003.

Maushagen R, Reers S, Pfannerstill AC, Hahlbrock A, Stauber R, Rahmanzadeh R, et al. Effects of paclitaxel on permanent head and neck squamous cell carcinoma cell lines and identification of anti-apoptotic caspase 9b. J Cancer Res Clin Oncol. 2016 Jun;142(6):1261–71.

Shin YS, Cha HY, Lee BS, Kang SU, Hwang HS, Kwon HC, et al. Anti-cancer effect of luminacin, a marine microbial extract, in head and neck squamous cell carcinoma progression via autophagic cell death. Cancer Res Treat. 2016 Apr;48(2):738–52.

Kadletz L, Heiduschka G, Domayer J, Schmid R, Enzenhofer E, Thurnher D. Evaluation of spheroid head and neck squamous cell carcinoma cell models in comparison to monolayer cultures. Oncol Lett. 2015 Sep;10(3):1281–6.

Rossa C Jr, D’Silva NJ. Non-murine models to investigate tumor-immune interactions in head and neck cancer. Oncogene. 2019 Jun;38(25):4902–14.

Wypij JM. A naturally occurring feline model of head and neck squamous cell carcinoma [PubMed: 23970998]. Pathol Res Int. 2013;2013:502197.

Shield KD, Ferlay J, Jemal A, Sankaranarayanan R, Chaturvedi AK, Bray F, et al. The global incidence of lip, oral cavity, and pharyngeal cancers by subsite in 2012. CA Cancer J Clin. 2017 Jan;67(1):51–64.

Yoshikawa H, Ehrhart EJ, Charles JB, Thamm DH, Larue SM. Immunohistochemical characterization of feline oral squamous cell carcinoma [PubMed: 23106467]. Am J Vet Res. 2012 Nov;73(11):1801–6.

Soltero-Rivera MM, Krick EL, Reiter AM, Brown DC, Lewis JR. Prevalence of regional and distant metastasis in cats with advanced oral squamous cell carcinoma: 49 cases (2005-2011) [PubMed: 24027053]. J Feline Med Surg. 2014 Feb;16(2):164–9.

Mestrinho LA, Pissarra H, Carvalho S, Peleteiro MC, Gawor J, Niza MM. Comparison of Histological and Proliferation Features of Canine Oral Squamous Cell Carcinoma Based on Intraoral Location: 36 Cases [PubMed: 28631549]. J Vet Dent. 2017 Jun;34(2):92–9.

Liu D, Xiong H, Ellis AE, Northrup NC, Dobbin KK, Shin DM, et al. Canine spontaneous head and neck squamous cell carcinomas represent their human counterparts at the molecular level [PubMed: 26030765]. PLoS Genet. 2015 Jun;11(6):e1005277.

Mochizuki H, Breen M. Sequence analysis of RAS and RAF mutation hot spots in canine carcinoma [PubMed: 27714944]. Vet Comp Oncol. 2017 Dec;15(4):1598–605.

Martano M, Restucci B, Ceccarelli DM, Lo Muzio L, Maiolino P. Immunohistochemical expression of vascular endothelial growth factor in canine oral squamous cell carcinomas [PubMed: 26870224]. Oncol Lett. 2016 Jan;11(1):399–404.

Schook LB, Collares TV, Darfour-Oduro KA, De AK, Rund LA, Schachtschneider KM, et al. Unraveling the swine genome: implications for human health [PubMed: 25689318]. Annu Rev Anim Biosci. 2015;3(1):219–44.

Mair KH, Sedlak C, Käser T, Pasternak A, Levast B, Gerner W, et al. The porcine innate immune system: an update [PubMed: 24709051]. Dev Comp Immunol. 2014 Aug;45(2):321–43.

De Pelsmaeker S, Devriendt B, Leclercq G, Favoreel HW. Porcine NK cells display features associated with antigen-presenting cells [PubMed: 29345060]. J Leukoc Biol. 2018 Jan;103(1):129–40.

Bordignon V, El-Beirouthi N, Gasperin BG, Albornoz MS, Martinez-Diaz MA, Schneider C, et al. Production of cloned pigs with targeted attenuation of gene expression [PubMed: 23737990]. PLoS One. 2013 May;8(5):e64613.

Lillico SG, Proudfoot C, Carlson DF, Stverakova D, Neil C, Blain C, et al. Live pigs produced from genome edited zygotes [PubMed: 24108318]. Sci Rep. 2013 Oct;3(1):2847.

Watson AL, Carlson DF, Largaespada DA, Hackett PB, Fahrenkrug SC. Engineered Swine Models of Cancer [PubMed: 27242889]. Front Genet. 2016 May;7:78.

Li Y, Li Y, Cao X, Jin X, Jin T. Pattern recognition receptors in zebrafish provide functional and evolutionary insight into innate immune signaling pathways [PubMed: 27721456]. Cell Mol Immunol. 2017 Jan;14(1):80–9.

Yapijakis et al: Model of Sequential Oral Cancer (Review) in vivo 33: 1751-1755 (2019) doi:https://doi.org/10.21873/invivo.11665.

Monti Hughes A, Pozzi E, Thorp SI, Curotto P, Medina VA, Martinel Lamas DJ, et al. Histamine reduces boron neutron capture therapy-induced mucositis in an oral precancer model. Oral Dis. 2015 Sep;21(6):770–7.

Baldasquin-Caceres B, Gomez-Garcia FJ, López-Jornet P, Castillo-Sanchez J, Vicente-Ortega V. Chemopreventive potential of phenolic compounds in oral carcinogenesis. Arch Oral Biol. 2014 Oct;59(10):1101–7.

Marcazzan S, Varoni EM, Blanco E, Lodi G, Ferrari M. Nanomedicine, an emerging therapeutic strategy for oral cancer therapy. Oral Oncol. 2018 Jan;76:1–7.

Kumar P, Bhattacharjee T, Ingle A, Maru G, Krishna CM. Raman spectroscopy of experimental oral carcinogenesis. Technol Cancer Res Treat. 2016 Oct;15(5):NP60–72.

Ishida K, Tomita H, Nakashima T, Hirata A, Tanaka T, Shibata T, et al. Current mouse models of oral squamous cell carcinoma: genetic and chemically induced models. Oral Oncol. 2017 Oct;73:16–20.

Chen YF, Yang CC, Kao SY, Liu CJ, Lin SC, Chang KW. MicroRNA-211 enhances the oncogenicity of carcinogen-induced oral carcinoma by repressing TCF12 and increasing antioxidant activity. Cancer Res. 2016 Aug;76(16):4872–86.

Wu TF, Chen L, Bu LL, Gao J, Zhang WF, Jia J. CD44+ cancer cell-induced metastasis: A feasible neck metastasis model. Eur J Pharm Sci. 2017 Apr;101:243–50.

Pickering CR, Zhang J, Yoo SY, Bengtsson L, Moorthy S, Neskey DM, et al. Integrative genomic characterization of oral squamous cell carcinoma identifies frequent somatic drivers. Cancer Discov. 2013 Jul;3(7):770–81.

Iglesias-Bartolome R, Martin D, Gutkind JS. Exploiting the head and neck cancer oncogenome: widespread PI3K-mTOR pathway alterations and novel molecular targets. Cancer Discov. 2013 Jul;3(7):722–5.

Szaniszlo P, Fennewald SM, Qiu S, Kantara C, Shilagard T, Vargas G, et al. Temporal characterization of lymphatic metastasis in an orthotopic mouse model of oral cancer. Head Neck. 2014 Nov;36(11):1638–47.

Rossa C Jr, D’Silva NJ. Immune-relevant aspects of murine models of head and neck cancer. Oncogene. 2019 May;38(21):3973–88.

Szadvari I, Krizanova O, Babula P. Athymic nude mice as an experimental model for cancer treatment [PubMed: 28006926]. Physiol Res. 2016 Dec;65 Suppl 4:S441–53.

Albanesi M, Mancardi DA, Jönsson F, Iannascoli B, Fiette L, Di Santo JP, et al. Neutrophils mediate antibody-induced antitumor effects in mice [PubMed: 23980063]. Blood. 2013 Oct;122(18):3160–4.

Liu B, Chen P, Xi D, Zhu H, Gao Y. ATF4 regulates CCL2 expression to promote endometrial cancer growth by controlling macrophage infiltration [PubMed: 28843961]. Exp Cell Res. 2017 Nov;360(2):105–12.

Niu Z, Shi Q, Zhang W, Shu Y, Yang N, Chen B, et al. Caspase-1 cleaves PPARγ for potentiating the pro-tumor action of TAMs. Nat Commun. 2017 Oct;8(1):766.

Shinohara H, Kuranaga Y, Kumazaki M, Sugito N, Yoshikawa Y, Takai T, et al. Regulated Polarization of Tumor-Associated Macrophages by miR-145 via Colorectal Cancer-Derived Extracellular Vesicles. J Immunol. 2017 Aug;199(4):1505–15.

Li Q, Dong H, Yang G, Song Y, Mou Y, Ni Y. Mouse Tumor-Bearing Models as Preclinical Study Platforms for Oral Squamous Cell Carcinoma. Front Oncol. 2020 Feb;10:212.

Chen WC, Lai CH, Chuang HC, Lin PY, Chen MF. Inflammation-induced myeloid-derived suppressor cells associated with squamous cell carcinoma of the head and neck. Head Neck. 2017 Feb;39(2):347–55.

Oghumu S, Knobloch TJ, Terrazas C, Varikuti S, Ahn-Jarvis J, Bollinger CE, et al. Deletion of macrophage migration inhibitory factor inhibits murine oral carcinogenesis: potential role for chronic pro-inflammatory immune mediators. Int J Cancer. 2016 Sep;139(6):1379–90. https://doi.org/10.1002/ijc.30177

Wu JS, Li L, Wang SS, Pang X, Wu JB, Sheng SR, et al. Autophagy is positively associated with the accumulation of myeloid‑derived suppressor cells in 4‑nitroquinoline‑1‑oxide‑induced oral cancer. Oncol Rep. 2018 Dec;40(6):3381–91. https://doi.org/10.3892/or.2018.6747

Wen L, Lu H, Li Q, Li Q, Wen S, Wang D, et al. Contributions of T cell dysfunction to the resistance against anti-PD-1 therapy in oral carcinogenesis. J Exp Clin Cancer Res. 2019 Jul;38(1):299. https://doi.org/10.1186/s13046-019-1185-0

Sun S, Zhang Z. Patient-derived xenograft platform of OSCC: a renewable human bio-bank for preclinical cancer research and a new co-clinical model for treatment optimization. Front Med. 2016 Mar;10(1):104–10. https://doi.org/10.1007/s11684-016-0432-4

Rivera C, Zandonadi FS, Sánchez-Romero C, Soares CD, Granato DC, González-Arriagada WA, et al. Agrin has a pathological role in the progression of oral cancer. Br J Cancer. 2018 Jun;118(12):1628–38. https://doi.org/10.1038/s41416-018-0135-5

Kerk SA, Finkel KA, Pearson AT, Warner KA, Zhang Z, Nör F, et al. 5T4-targeted therapy ablates cancer stem cells and prevents recurrence of head and neck squamous cell carcinoma. Clin Cancer Res. 2017 May;23(10):2516–27. https://doi.org/10.1158/1078-0432.CCR-16-1834

Rich LJ, Seshadri M. Photoacoustic monitoring of tumor and normal tissue response to radiation. Sci Rep. 2016 Feb;6(1):21237. https://doi.org/10.1038/srep21237

Fang Z, Zhao J, Xie W, Sun Q, Wang H, Qiao B. LncRNA UCA1 promotes proliferation and cisplatin resistance of oral squamous cell carcinoma by sunppressing miR-184 expression. Cancer Med. 2017 Dec;6(12):2897–908. https://doi.org/10.1002/cam4.1253

Ozawa H, Ranaweera RS, Izumchenko E, Makarev E, Zhavoronkov A, Fertig EJ, et al. SMAD4 loss is associated with cetuximab resistance and induction of MAPK/JNK activation in head and neck cancer cells. Clin Cancer Res. 2017 Sep;23(17):5162–75. https://doi.org/10.1158/1078-0432.CCR-16-1686

Su H, Luo Q, Xie H, Huang X, Ni Y, Mou Y, et al. Therapeutic antitumor efficacy of tumor-derived autophagosome (DRibble) vaccine on head and neck cancer. Int J Nanomedicine. 2015 Mar;10:1921–30. https://doi.org/10.2147/IJN.S74204

Su H, Luo Q, Xie H, Huang X, Ni Y, Mou Y, et al. Therapeutic antitumor efficacy of tumor-derived autophagosome (DRibble) vaccine on head and neck cancer. Int J Nanomedicine. 2015 Mar;10:1921–30.

72 Dong H, Su H, Chen L, Liu K, Hu HM, Yang W, et al. Immunocompetence and mechanism of the DRibble-DCs vaccine for oral squamous cell carcinoma. Cancer Manag Res. 2018 Mar;10:493–501.

73 Nagaya T, Nakamura Y, Okuyama S, Ogata F, Maruoka Y, Choyke PL, et al. Syngeneic mouse models of oral cancer are effectively targeted by anti-CD44-based NIR-PIT. Mol Cancer Res. 2017 Dec;15(12):1667–77.

74 Chung MK, Jung YH, Lee JK, Cho SY, Murillo-Sauca O, Uppaluri R, et al. CD271 confers an invasive and metastatic phenotype of head and neck squamous cell carcinoma through the upregulation of slug. Clin Cancer Res. 2018 Feb;24(3):674–83.

75 Adachi M, Mizuno-Kamiya M, Takayama E, Kawaki H, Inagaki T, Sumi S, et al. Gene expression analyses associated with malignant phenotypes of metastatic sub-clones derived from a mouse oral squamous cell carcinoma Sq-1979 cell line. Oncol Lett. 2018 Mar;15(3):3350–6.

76 De La Rochere P, Guil-Luna S, Decaudin D, Azar G, Sidhu SS, Piaggio E. Humanized mice for the study of immuno-oncology. Trends Immunol. 2018 Sep;39(9):748–63.

77 Morton JJ, Bird G, Refaeli Y, Jimeno A. Humanized mouse xenograft models: narrowing the tumor-microenvironment gap. Cancer Res. 2016 Nov;76(21):6153–8.

78 Greenblatt MB, Vrbanac V, Tivey T, Tsang K, Tager AM, Aliprantis AO. Graft versus host disease in the bone marrow, liver and thymus humanized mouse model. PLoS One. 2012;7(9):e44664.

Lampreht Tratar U, Horvat S, Cemazar M. Transgenic mouse models in cancer research. Front Oncol. 2018 Jul;8:268.

Bian Y, Hall B, Sun ZJ, Molinolo A, Chen W, Gutkind JS, et al. Loss of TGF- β signaling and PTEN promotes head and neck squamous cell carcinoma through cellular senescence evasion and cancer-related inflammation. Oncogene. 2012 Jul 12. 31:3322–32. doi: 10.1038/onc.2011.494

Li Z, Gonzalez CL, Wang B, Zhang Y, Mejia O, Katsonis P, et al. Cdkn2a suppresses metastasis in squamous cell carcinomas induced by the gain-of-function mutant p53(R172H). J Pathol. 2016 Jul 22. 240:224– 34. doi: 10.1002/path.4770

Chen W, Kang KL, Alshaikh A, Varma S, Lin YL, Shin KH, et al. Grainyhead- like 2. (GRHL2) knockout abolishes oral cancer development through reciprocal regulation of the MAP kinase and TGF-β signaling pathways. Oncogenesis. 2018 May 08. 7:38. doi: 10.1038/s41389-018-0047-5

El-Bayoumy K, Chen KM, Zhang SM, Sun YW, Amin S, Stoner G, et al. Carcinogenesis of the oral cavity: environmental causes and potential prevention by black raspberry. Chem Res Toxicol. 2017 Jan 17. 30:126– 44. doi: 10.1021/acs.chemrestox.6b00306


Refbacks

  • There are currently no refbacks.




 

Become a REVIEWER 

 

ISSN: 2346-8491 (online)