UVB Induced Skin Cancer Development in Experimental Mouse Model: A Review

Authors

  • Muhammad Wahizul Haswan Abdul Aziz ᵃCentre for Toxicology and Health Risk Studies (CORE), Faculty of Health Sciences, Universiti Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur, Malaysia; ᵇDepartment of Para-clinical Sciences, Faculty of Medicine and Health Sciences, Universiti Malaysia Sarawak, Jalan Datuk Mohammad Musa, 94300 Kota Samarahan, Sarawak, Malaysia https://orcid.org/0000-0001-8943-3934
  • Dayang Fredalina Basri Centre for Diagnostic, Therapeutic & Investigative Studies (CODTIS), Faculty of Health Sciences, Universiti Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur, MalaysiaUniversiti Kebangsaan Malaysia https://orcid.org/0000-0001-6667-9253
  • Siti Fathiah Masre Centre for Toxicology and Health Risk Studies (CORE), Faculty of Health Sciences, Universiti Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur, Malaysia https://orcid.org/0000-0002-4202-2289
  • Ahmad Rohi Ghazali Centre for Toxicology and Health Risk Studies (CORE), Faculty of Health Sciences, Universiti Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur, Malaysia https://orcid.org/0000-0001-9064-2178

DOI:

https://doi.org/10.11113/mjfas.v19n5.2968

Keywords:

Mice model, carcinogenesis, chemoprevention, skin cancer, UVB

Abstract

Skin cancer is a widespread global issue, with ultraviolet (UV) radiation being a significant risk factor. Researchers often use the mouse skin cancer model to develop novel therapeutic chemoprevention strategies. This model involves exposing mice to UVB radiation to induce skin carcinogenesis. In this short communication, we found that 69.57% of studies used female SKH-1 hairless mice, 17.39% used BALB/c mice, 8.69% used Swiss albino mice, and 4.35% used HRS/J hairless mice. All studies used mice aged 5-8 weeks. Different models of mice were exposed to varying doses of UVB radiation. SKH-1 hairless mice received UVB radiation twice a week for 10-18 weeks, while Swiss albino mice were exposed to UVB radiation three times a week for 30 weeks. HRS/J hairless mice received UVB radiation five times a week for 15 weeks. BALB/c mice were treated with DMBA and exposed to UVB radiation for 10-16 weeks to induce skin tumors. However, using SKH-1 hairless mice is costly. In conclusion, we can suggest BALB/c mice treated with DMBA and exposed to UVB radiation three times a week for 16 weeks for UVB-induced skin cancer model, as it is more cost-effective than other hairless mouse models.

References

Siegel, R. L, Miller, K. D., & Jemal, A. (2018). Cancer statistics, 2018. CA: A Cancer Journal for Clinicians, 68(1), 7-30. https://doi.org/10.3322/caac.21442.

Robertson, F. M. (2008). Skin carcinogenesis. In: Schwab M. (eds). Encyclopedia of Cancer, Springer, Berlin, Heidelberg, pp. 2751. https://doi.org/10.1007/978-3-540-47648-1_5340.

Poswar, F. O., Fraga, C. A., Farias, L. C., Feltenberger, J. D., Cruz, V. P., Santos, S. H., Silveira, C. M., de Paula, A. M., & Guimarães, A. L. (2013). Immunohistochemical analysis of TIMP-3 and MMP-9 in actinic keratosis, squamous cell carcinoma of the skin, and basal cell carcinoma. Pathology Research and Practice, 209, 705-709. https://doi.org/10.1016/j.prp.2013.08.002.

Ishida, M., Kojima, F. & Okabe, H. (2013). Cathepsin-K expression in basal cell carcinoma. Journal of the European Academy of Dermatology and Venereology, 27, e128–e130. https://doi.org/10.1111/j.1468-3083.2011.04436.x.

D'Orazio, J. A., Jarrett, S. G., Amaro-Ortiz, A. & Scott, T. L. (2013). UV Radiation and the Skin. International Journal of Molecular Sciences, 14, 12222-11248. https://doi.org/10.3390%2Fijms140612222.

Chhabra, G., Ndiaye, M. A., Garcia-Peterson, L. M. & Ahmad, N. (2017). Melanoma chemoprevention: Current status and future prospects. Photochemistry and Photobiology, 93, 975-989. https://doi.org/10.1111/php.12749.

Skobowiat, C., Sayre, R. M., Dowdy, J. C. & Slominski, A. T. (2013). Ultraviolet radiation regulates cortisol activity in a waveband-dependent manner in human skin ex vivo. British Journal of Dermatology, 168, 595-601. https://doi.org/10.1111/bjd.12096.

Bayerl, C., Taake, S., Moll, I. & Jung, E. G. (1995). Characterisation of sunburn cells after exposure to ultraviolet light. Photodermatology, Photoimmunology & Photomedicine, 11, 149-154. https://doi.org/10.1111/j.1600-0781.1995.tb00157.x.

Coelho, S. G., Choi, W., Brenner, M., Miyamura, Y., Yamaguchi, Y., Wolber, R., Smuda, C., Batzer, J., Kolbe, L., Ito, S., Wakamatsu, K., Zmudzka, B. Z., Beer, J. Z., Miller, S. A. & Hearing, V. J. (2009). Short- and long-term effects of UV radiation on the pigmentation of human skin. Journal of Investigative Dermatology Symposium Proceedings, 14(1), 32-35. https://doi.org/10.1038/jidsymp.2009.10.

Scott, T. L., Christian, P. A., Kesler, M. V., Donohue, K. M., Shelton, B., Wakamatsu, K., Ito, S. & D'Orazio, J. (2012). Pigment-independent cAMP-mediated epidermal thickening protects against cutaneous UV injury by keratinocyte proliferation. Experimental Dermatology, 21(10), 771-777. https://doi.org/10.1111/exd.12012.

Mitra, D. & Fisher, D. E. (2009). Transcriptional regulation in melanoma. Hematology/Oncology Clinics of North America, 23, 447-465. https://doi.org/10.1016/j.hoc.2009.03.003.

Sklar, L. R., Almutawa, F., Lim, H. W. & Hamzavi, I. (2013). Effects of ultraviolet radiation, visible light, and infrared radiation on erythema and pigmentation: A review. Photochemical & Photobiological Sciences, 12, 54-64. https://doi.org/10.1039/c2pp25152c.

Burke, K. E. (2010). Photoaging: The role of oxidative stress. Giornale italiano di dermatologia e venereologia, 145, 445-459.

Ikehata, H. & Ono, T. (2011). The mechanisms of UV mutagenesis. Journal of Radiation Research, 52, 115-125. https://doi.org/10.1269/jrr.10175.

George, B. P., Chandran, R., Abrahamse, H. (2021). Role of phytochemicals in cancer chemoprevention: Insights. Antioxidants. 10, 1455. https://doi.org/10.3390/antiox10091455.

Pyun, H. B.,Kim, M., Park, J., Numata, N., Shin, J. W., Shin, H. S., Kim, D. U. & Hwang, J. K. (2012). Effects of collagen tripeptide supplement on photoaging and epidermal skin barrier In Uvb-exposed hairless mice. Preventive Nutrition and Food Science, 4(17), 245-253. https://doi.org/10.3746/pnf.2012.17.4.245.

Ito, M., Liu, Y., Yang, Z., Nguyen, J. K., Liang, F., Morris, R. J. & Cotsarelis, G. (2005). Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nature Medicine, 12(11), 1351-1354. https://doi.org/10.1038/nm1328.

Singh, C. K., Mintie, C. A., Ndiaye, M. A., Chhabra, G., Dakup, P. P., Ye, T., Yu, M. & Ahmad, N. (2019). Chemoprotective effects of dietary grape powder on UVB radiation-mediated skin carcinogenesis in SKH-1 hairless mice. Journal of Investigative Dermatology, 139(3), 552-561. https://doi.org/10.1016/j.jid.2018.09.028.

Mirzoeva, S., Tong, X., Bridgeman, B. B., Plebanek, M. P. & Volpert, O. V. (2018). Apigenin inhibits UVB-induced skin carcinogenesis: the role of thrombospondin-1 as an anti-inflammatory factor. Neoplasia, 20(9), 930-942. https://doi.org/10.1016/j.neo.2018.07.005.

Dickinson, S. E., Janda, J., Criswell, J., Blohm-Mangone, K., Olson, E. R., Liu, Z., Barber, C., Petricoin, E. F. 3rd., Calvert, V. S., Einspahr, J., Dickinson, J. E., Stratton, S. P., Curiel-Lewandrowski, C., Saboda, K., Hu, C., Bode, A. M., Dong, Z., Alberts, D. S. & Timothy Bowden, G. (2016). Inhibition of Akt enhances the chemopreventive effects of topical rapamycin in mouse skin. Cancer Prevention Research (Philadelphia, Pa.), 9(3), 215-24. https://doi.org/10.1158/1940-6207.CAPR-15-0419.

Blohm-Mangone, K., Burkett, N. B., Tahsin, S., Myrdal, P. B., Aodah, A., Ho, B., Janda, J., McComas, M., Saboda, K., Roe, D. J., Dong, Z., Bode, A. M., Petricoin, E. F. 3rd., Calvert, V. S., Curiel-Lewandrowski, C., Alberts, D. S., Wondrak, G. T. & Dickinson, S. E. (2018). Pharmacological TLR4 antagonism using topical resatorvid blocks solar UV-induced skin tumorigenesis in SKH-1 mice. Cancer Prevention Research (Philadelphia, Pa.), 11(5), 265-278. https://doi.org/10.1158/1940-6207.CAPR-17-0349.

Huang, K. M., Liang, S., Yeung, S., Oiyemhonlan, E., Cleveland, K. H., Parsa, C., Orlando, R., Meyskens, F. L. Jr., Andresen, B. T. & Huang, Y. (2017). Topically applied carvedilol attenuates solar ultraviolet radiation induced skin carcinogenesis. Cancer Prevention Research (Philadelphia, Pa.), 10(10), 598-606. https://doi.org/10.1158/1940-6207.CAPR-17-0132.

Gao, G., Zhang, T., Wang, Q., Reddy, K., Chen, H., Yao, K., Wang, K., Roh, E., Zykova, T., Ma, W., Ryu, J., Curiel-Lewandrowski, C., Alberts, D., Dickinson, S. E., Bode, A. M., Xing, Y. & Dong, Z. (2017). ADA-07 suppresses solar ultraviolet-induced skin carcinogenesis by directly inhibiting TOPK. Molecular Cancer Therapeutics, 16(9), 1843-1854. https://doi.org/10.1158/1535-7163.MCT-17-0212.

Ngo, S. N. (2018). Reduction of UV-induced skin tumours in hairless mice by topical non-steroidal anti-inflammatory drugs. Journal of Cancer and Tumor International, 7(2), 1-7. https://doi.org/10.9734/JCTI/2018/39590.

Qiang, L., Sample, A., Shea, C. R., Soltani, K., Macleod, K. F. & He, Y.Y. (2017). Autophagy gene ATG7 regulates ultraviolet radiation-induced inflammation and skin tumorigenesis. Autophagy, 13(12), 2086-2103. https://doi.org/10.1080/15548627.2017.1380757.

Rigby, C. M., Roy, S., Deep, G., Guillermo-Lagae, R., Jain, A. K., Dhar, D., Orlicky, D. J., Agarwal, C. & Agarwal, R. (2017). Role of p53 in silibinin-mediated inhibition of ultraviolet B radiation-induced DNA damage, inflammation and skin carcinogenesis. Carcinogenesis, 38(1), 40-50. https://doi,org/10.1093/carcin/bgw106.

Carrara, I. M., Melo, G. P., Bernardes, S. S., Neto, F. S., Ramalho, L. N. Z., Marinello, P. C., Luiz, R. C., Cecchini, R. & Cecchini, A. L. (2019). Looking beyond the skin: Cutaneous and systemic oxidative stress in UVB-induced squamous cell carcinoma in hairless mice. Journal of Photochemistry and Photobiology B: Biology, 195, 17-26. https://doi.org/10.1016/j.jphotobiol.2019.04.007.

Hou, G. R., Zeng, K., Lan, H. M. & Wang, Q. (2018). Juglanin ameliorates UVB induced skin carcinogenesis via anti-inflammatory and proapoptotic effects in vivo and in vitro. International Journal of Molecular Medicine, 42(1), 41-52. https://doi.org/10.3892%2Fijmm.2018.3601.

Chandrakesan, A., Muruhan, S. & Sayanam, R. R. A. (2018). Morin inhibiting photocarcinogenesis by targeting ultraviolet-B-induced oxidative stress and inflammatory cytokines expression in Swiss Albino mice. International Journal of Nutrition, Pharmacology, Neurological Diseases, 8(2), 41.

Boakye, C. H. A., Patel, K., Doddapaneni, R., Bagde, A., Behl, G., Chowdhury, N., Safe, S. & Singh, M. (2016). Ultra-flexible nanocarriers for enhanced topical delivery of a highly lipophilic antioxidative molecule for skin cancer chemoprevention. Colloids and Surfaces B: Biointerfaces, 143, 156-167. https://doi.org/10.1016/j.colsurfb.2016.03.036.

Chaudhary, S. C., Waseem, M., Rana, M., Xu, H., Kopelovich, L., Elmets, C. A. & Athar, M. (2017). Naproxen inhibits UVB-induced Basal cell and squamous cell carcinoma development in Ptch1+/- /SKH-1 hairless mice. Photochemistry and Photobiology, 93(4), 1016-1024. https://doi.org/10.1111/php.12758.

Lee, J., Ha, S. J., Park, J., Kim, Y. H., Lee, N. H., Kim, Y. E., Kim, Y., Song, K. M. & Jung, S. K. (2017). 1,8-cineole prevents UVB-induced skin carcinogenesis by targeting the aryl hydrocarbon receptor. Oncotarget, 8(62), 105995-106008. https://doi.org/10.18632/oncotarget.22519.

Kalin, J. H., Eroglu, A., Liu, H., Holtzclaw, W. D., Leigh, I., Proby, C. M., Fahey, J. W., Cole, P. A. & Dinkova-Kostova, A. T. (2019). Investigation into the use of histone deacetylase inhibitor MS-275 as a topical agent for the prevention and treatment of cutaneous squamous cell carcinoma in an SKH-1 hairless mouse model. PLoS One, 14(3), e0213095. https://doi.org/10.1371/journal.pone.0213095.

Hosseini, M., Dousset, L., Michon, P., Mahfouf, W., Muzotte, E., Bergeron, V., Bortolotto, D., Rossignol, R., Moisan, F., Taieb, A., Bouzier-Sore, A. K. & Rezvani, H. R. (2019). UVB-induced DHODH upregulation, which is driven by STAT3, is a promising target for chemoprevention and combination therapy of photocarcinogenesis. Oncogenesis, 8(10), 52. https://doi.org/10.1038/s41389-019-0161-z.

Yum, H. W., Park, J., Park, H. J., Shin, J. W., Cho, Y. Y., Kim, S. J., Kang, J. X. & Surh, Y. J. (2017). Endogenous ω-3 fatty acid production by fat-1 transgene and topically applied docosahexaenoic acid protect against UVB-induced mouse skin carcinogenesis. Scientific Reports, 7, 11658. https://doi.org/10.1038/s41598-017-11443-2.

Gunaseelan, S., Balupillai, A., Govindasamy, K., Muthusamy, G., Ramasamy, K., Shanmugam, M. & Rajendra Prasad, N. (2019). Correction: The preventive effect of linalool on acute and chronic UVB-mediated skin carcinogenesis in Swiss albino mice. Photochemical & Photobiological Sciences, 18(11), 2816-2817. https://doi.org/10.1039/c9pp90051a.

Zhao, J. G. & Zhang, Y. Q. (2015). Inhibition of the flavonoid extract from silkworm cocoons on DMBA/UVB-induced skin damage and tumor promotion in BALB/c mice. Toxicology Research, 4(4), 1016-1024. https://doi.org/10.1039/c5tx00087d.

Tanveer, M. A., Rashid, H., Nazir, L. A., Archoo, S., Shahid, N. H., Ragni, G., Umar, S. A. & Tasduq, S. A. (2023). Trigonelline, a plant derived alkaloid prevents ultraviolet-B-induced oxidative DNA damage in primary human dermal fibroblasts and BALB/c mice via modulation of phosphoinositide 3-kinase-Akt-Nrf2 signalling axis. Experimental Gerontology, 171, 112028. https://doi.org/10.1016/j.exger.2022.112028.

Hussaana, A. (2013). Peran protein daun Mirabilis jalapa l sebagai kemoprevensi kanker kulit: penelusuran mekanisme antiinflamasi, restorasi supresi imun dan regulasi apoptosis. Doctoral dissertation, Universitas Gadjah Mada.

Listyawati, S. (2015) Potensi ekstrak terkuantifikasi rimpang Boesenbergia pandurata (Roxb.) Schlecht. sebagai agen kemoprevensi kanker kulit. Doctoral dissertation, Universitas Gadjah Mada.

Bowden, G. T. (2004). Prevention of non-melanoma skin cancer by targeting ultraviolet-B-light signalling. Nature Reviews Cancer, 4, 23-35. https://doi.org/10.1038/nrc1253.

Athanassiadou, A. M., Lazaris, A. C., Patsouris, E., Tsipis, A., Chelidonis, G. & Aroni, K. (2013). Significance of cyclooxygenase 2, EZH-2 polycomb group and p53 expression in actinic keratosis and squamous cell carcinomas of the skin. The American Journal of Dermatopathology, 35, 425-431. https://doi.org/10.1097/dad.0b013e318271292a.

Benavides, F., Oberyszyn, T. M., VanBuskirk, A. M., Reeve, V. E. & Kusewitt, D. F. (2009). The hairless mouse in skin research. Journal of Dermatological Science, 53(1), 10‐8. https://doi.org/10.1016/j.jdermsci.2008.08.012.

Konger, R. L., Derr‐Yellin, E., Hojati, D., Lutz, C. & Sundberg, J. P. (2016). Comparison of the acute ultraviolet photoresponse in congenic albino hairless C57BL/6J mice relative to outbred SKH1 hairless mice. Experimental Dermatology, 25, 688‐93. https://doi.org/10.1111/exd.13034.

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19-10-2023