Inflammation-Related Carcinogenesis: Lessons from Animal Models to Clinical Aspects

Futoshi Okada, Runa Izutsu, Keisuke Goto, Mitsuhiko Osaki, Futoshi Okada, Runa Izutsu, Keisuke Goto, Mitsuhiko Osaki

Abstract

Inflammation-related carcinogenesis has long been known as one of the carcinogenesis patterns in humans. Common carcinogenic factors are inflammation caused by infection with pathogens or the uptake of foreign substances from the environment into the body. Inflammation-related carcinogenesis as a cause for cancer-related death worldwide accounts for approximately 20%, and the incidence varies widely by continent, country, and even region of the country and can be affected by economic status or development. Many novel approaches are currently available concerning the development of animal models to elucidate inflammation-related carcinogenesis. By learning from the oldest to the latest animal models for each organ, we sought to uncover the essential common causes of inflammation-related carcinogenesis. This review confirmed that a common etiology of organ-specific animal models that mimic human inflammation-related carcinogenesis is prolonged exudation of inflammatory cells. Genotoxicity or epigenetic modifications by inflammatory cells resulted in gene mutations or altered gene expression, respectively. Inflammatory cytokines/growth factors released from inflammatory cells promote cell proliferation and repair tissue injury, and inflammation serves as a "carcinogenic niche", because these fundamental biological events are common to all types of carcinogenesis, not just inflammation-related carcinogenesis. Since clinical strategies are needed to prevent carcinogenesis, we propose the therapeutic apheresis of inflammatory cells as a means of eliminating fundamental cause of inflammation-related carcinogenesis.

Keywords: animal models; inflammation-related carcinogenesis; therapeutic apheresis.

Conflict of interest statement

We declare that there are no financial or other interests with regards to this manuscript that might be construed as a conflict of interest.

References

    1. Okada F. Gaseous molecules as an endogenous factor in the inflammation-related carcinogenesis model. In: Takaaki Akaike, editor. Inflammation and Cancer Metabolism, Persulfide Conference 2019, Proceedings pf the 1st International Conference on Persulfide and Sulfur Metabolism in Biology and Medicine, Sendai, Japan, 9–11 September 2019. Redox Week Sendai Office; Sendai, Japan: 2019. pp. 76–77.
    1. Touati E. When bacteria become mutagenic and carcinogenic: Lessons from H. pylori. Mutat. Res. 2010;703:66–70. doi: 10.1016/j.mrgentox.2010.07.014.
    1. Okada F. Inflammation-related carcinogenesis: Current findings in epidemiological trends, causes and mechanisms. Yonago Acta Med. 2014;57:65–72.
    1. Corrêa L.H., Heyn G.S., Magalhaes K.G. The impact of the adipose organ plasticity on inflammation and cancer progression. Cells. 2019;8:662. doi: 10.3390/cells8070662.
    1. Wang Y., Zhu N., Zhang C., Wang Y., Wu H., Li Q., Du K., Liao D., Qin L. Friend or foe: Multiple roles of adipose tissue in cancer formation and progression. J. Cell. Physiol. 2019;234:21436–21449. doi: 10.1002/jcp.28776.
    1. Quail D.F., Dannenberg A.J. The obese adipose tissue microenvironment in cancer development and progression. Nat. Rev. Endocrinol. 2019;15:139–154. doi: 10.1038/s41574-018-0126-x.
    1. Okada F. Beyond foreign-body-induced carcinogenesis: Impact of reactive oxygen species derived from inflammatory cells in tumorigenic conversion and tumor progression. Int. J. Cancer. 2007;121:2364–2372. doi: 10.1002/ijc.23125.
    1. Page A., Cascallana J.L., Casanova M.L., Navarro M., Alameda J.P., Pérez P., Bravo A., Ramírez A. IKKβ overexpression leads to pathologic lesions in stratified epithelia and exocrine glands and to tumoral transformation of oral epithelia. Mol. Cancer Res. 2011;9:1329–1338. doi: 10.1158/1541-7786.MCR-11-0168.
    1. Soffritti M., Belpoggi F., Cevolani D., Guarino M., Padovani M., Maltoni C. Results of long-term experimental studies on the carcinogenicity of methyl alcohol and ethyl alcohol in rats. Ann. N. Y. Acad. Sci. 2002;982:46–69. doi: 10.1111/j.1749-6632.2002.tb04924.x.
    1. Nachiappan V., Mufti S.I., Eskelson C.D. Ethanol-mediated promotion of oral carcinogenesis in hamsters: Association with lipid peroxidation. Nutr. Cancer. 1993;20:293–302. doi: 10.1080/01635589309514297.
    1. Guo Y., Wang X., Zhang X., Sun Z., Chen X. Ethanol promotes chemically induced oral cancer in mice through activation of the 5-lipoxygenase pathway of arachidonic acid metabolism. Cancer Prev. Res. 2011;4:1863–1872. doi: 10.1158/1940-6207.CAPR-11-0206.
    1. Li B., Hou D.Q., Xu S.B., Zhang J.Y., Zhu L.F., Wang Q., Pan L., Yu M., Shen W.L., Zhu W.W., et al. TLR2 deficiency enhances susceptibility to oral carcinogenesis by promoting an inflammatory environment. Am. J. Cancer Res. 2019;9:2599–2617.
    1. Corley D.A., Kubo A., Levin T.R., Block G., Habel L., Rumore G., Quesenberry C., Buffler P. Race, ethnicity, sex and temporal differences in Barrett’s oesophagus diagnosis: A large community-based study, 1994–2006. Gut. 2009;58:182–188. doi: 10.1136/gut.2008.163360.
    1. Goldstein S.R., Yang G.-Y., Curtis S.K., Reuhl K.R., Liu B.-C., Mirvish S.S., Newmark H.L., Yang C.S. Development of esophageal metaplasia and adenocarcinoma in a rat surgical model without the use of a carcinogen. Carcinogenesis. 1997;18:2265–2270. doi: 10.1093/carcin/18.11.2265.
    1. Fang H.-Y., Münch N.S., Schottelius M., Ingermann J., Liu H., Schauer M., Stangl S., Multhoff G., Steiger K., Gerngroß C., et al. CXCR4 is a potential target for diagnostic PET/CT imaging in Barrett’s dysplasia and esophageal adenocarcinoma. Clin. Cancer Res. 2018;24:1048–1061. doi: 10.1158/1078-0432.CCR-17-1756.
    1. Melkamu T., Qian X., Upadhyaya P., O’Sullivan M.G., Kassie F. Lipopolysaccharide enhances mouse lung tumorigenesis: A model for inflammation-driven lung cancer. Vet. Pathol. 2013;50:895–902. doi: 10.1177/0300985813476061.
    1. Gavett S.H., Parkinson C.U., Willson G.A., Wood C.E., Jarabek A.M., Roberts K.C., Kodavanti U.P., Dodd D.E. Persistent effects of Libby amphibole and amosite asbestos following subchronic inhalation in rats. Part. Fibre Toxicol. 2016;13:17. doi: 10.1186/s12989-016-0130-z.
    1. Blanco D., Vicent S., Fraga M.F., Fernandez-Garcia I., Freire J., Lujambio A., Esteller M., Ortiz-De-Solorzano C., Pio R., Lecanda F., et al. Molecular analysis of a multistep lung cancer model induced by chronic inflammation reveals epigenetic regulation of p16, activation of the DNA damage response pathway. Neoplasia. 2007;9:840–852. doi: 10.1593/neo.07517.
    1. Xu J., Futakuchi M., Iigo M., Fukamachi K., Alexander D.B., Shimizu H., Sakai Y., Tamano S., Furukawa F., Uchino T., et al. Involvement of macrophage inflammatory protein 1α (MIP1α) in promotion of rat lung and mammary carcinogenic activity of nanoscale titanium dioxide particles administered by intra-pulmonary spraying. Carcinogenesis. 2010;31:927–935. doi: 10.1093/carcin/bgq029.
    1. Balansky R., Ganchev G., Iltcheva M., Nikolov M., Maestra S., Micale R., D’Agostini F., Steele V., Flora S. Modulation by licofelone and celecoxib of experimentally induced cancer and preneoplastic lesions in mice exposed to cigarette smoke. Curr. Cancer Drug Targets. 2015;15:188–195. doi: 10.2174/1568009615666150216170008.
    1. Moghaddam S.J., Li H., Cho S.-N., Dishop M.K., Wistuba I.I., Ji L., Kurie J.M., Dickey B.F., DeMayo F.J. Promotion of lung carcinogenesis by chronic obstructive pulmonary disease–like airway inflammation in a K-ras–induced mouse model. Am. J. Respir. Cell Mol. Biol. 2009;40:443–453. doi: 10.1165/rcmb.2008-0198OC.
    1. Freire J., Ajona D., De Biurrun G., Agorreta J., Segura V., Guruceaga E., Bleau A.-M., Pio R., Blanco D., Montuenga L.M. Silica-induced chronic inflammation promotes lung carcinogenesis in the context of an immunosuppressive microenvironment. Neoplasia. 2013;15:913–924. doi: 10.1593/neo.13310.
    1. Gao M., Zhang P., Huang L., Shao H., Duan S., Li C., Zhang Q., Wang W., Wu Y., Wang J., et al. Is NLRP3 or NLRP6 inflammasome activation associated with inflammation-related lung tumorigenesis induced by benzo(a)pyrene and lipopolysaccharide? Ecotoxicol. Environ. Saf. 2019;185:109687. doi: 10.1016/j.ecoenv.2019.109687.
    1. Huang L., Zhang P., Duan S., Shao H., Gao M., Zhang Q., Feng F. The comparison of two mouse models of inflammation-related lung tumorigenesis induced by benzo(a)pyrene and lipopolysaccharide. Exp. Anim. 2019;68:301–306. doi: 10.1538/expanim.18-0159.
    1. Malkinson A.M., Koski K.M., Evans W.A., Festing M.F. Butylated hydroxytoluene exposure is necessary to induce lung tumors in BALB mice treated with 3-methylcholanthrene. Cancer Res. 1997;57:2832–2834.
    1. Liu J., Cho S.-N., Wu S.-P., Jin N., Moghaddam S.J., Gilbert J.L., Wistuba I., DeMayo F.J. Mig-6 deficiency cooperates with oncogenic Kras to promote mouse lung tumorigenesis. Lung Cancer. 2017;112:47–56. doi: 10.1016/j.lungcan.2017.08.001.
    1. Li Y., Du H., Qin Y., Roberts J., Cummings O.W., Yan C. Activation of the signal transducers and activators of the transcription 3 pathway in alveolar epithelial cells induces inflammation and adenocarcinomas in mouse lung. Cancer Res. 2007;67:8494–8503. doi: 10.1158/0008-5472.CAN-07-0647.
    1. Bullock F.D., Curtis M.R. Spontaneous tumors of the rat. J. Cancer Res. 1930;14:1–115. doi: 10.1158/jcr.1930.1.
    1. Nozaki K., Shimizu N., Ikehara Y., Inoue M., Tsukamoto T., Inada K.-I., Tanaka H., Kumagai T., Kaminishi M., Tatematsu M. Effect of early eradication on Helicobacter pylori-related gastric carcinogenesis in Mongolian gerbils. Cancer Sci. 2003;94:235–239. doi: 10.1111/j.1349-7006.2003.tb01426.x.
    1. Weis V.G., Goldenring J.R. Current understanding of SPEM and its standing in the preneoplastic process. Gastric Cancer. 2009;12:189–197. doi: 10.1007/s10120-009-0527-6.
    1. Peek R.M., Jr. Helicobacter pylori strain-specific modulation of gastric mucosal cellular turnover: Implications for carcinogenesis. J. Gastroenterol. 2002;37:10–16. doi: 10.1007/BF02990093.
    1. Hahm K.-B., Song Y.-J., Oh T.-Y., Lee J.-S., Surh Y.-J., Kim Y.-B., Yoo B.-M., Kim J.-H., Ha S.-U., Nahm K.-T., et al. Chemoprevention of Helicobacter pylori-associated Gastric Carcinogenesis in a mouse model; is it possible? J. Biochem. Mol. Biol. 2003;36:82–94. doi: 10.5483/BMBRep.2003.36.1.082.
    1. Peek R.M. Helicobacter pylori infection and disease: From humans to animal models. Dis. Model. Mech. 2008;1:50–55. doi: 10.1242/dmm.000364.
    1. Lee C.-W., Rao V.P., Rogers A.B., Ge Z., Erdman S.E., Whary M.T., Fox J.G. Wild-type and interleukin-10-deficient regulatory T cells reduce effector T-cell-mediated gastroduodenitis in Rag2−/− mice, but only wild-type regulatory T cells suppress helicobacter pylori gastritis. Infect. Immun. 2007;75:2699–2707. doi: 10.1128/IAI.01788-06.
    1. Kodama Y., Ozaki K., Sano T., Matsuura T., Akagi H., Narama I. Induction of squamous cell carcinoma of forestomach in diabetic rats by single alloxan treatment. Cancer Sci. 2006;97:1023–1030. doi: 10.1111/j.1349-7006.2006.00279.x.
    1. Mason R.C., Taylor P.R., Filipe M.I., McColl I. Pancreaticoduodenal secretions and the genesis of gastric stump carcinoma in the rat. Gut. 1988;29:830–834. doi: 10.1136/gut.29.6.830.
    1. Tebbutt N.C., Giraud A.S., Inglese M., Jenkins B., Waring P., Clay F.J., Malki S., Alderman B.M., Grail D., Hollande F., et al. Reciprocal regulation of gastrointestinal homeostasis by SHP2 and STAT-mediated trefoil gene activation in gp130 mutant mice. Nat. Med. 2002;8:1089–1097. doi: 10.1038/nm763.
    1. Tu S., Bhagat G., Cui G., Takaishi S., Kurt-Jones E.A., Rickman B., Betz K.S., Penz-Oesterreicher M., Bjorkdahl O., Fox J.G., et al. Overexpression of interleukin-1β induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell. 2008;14:408–419. doi: 10.1016/j.ccr.2008.10.011.
    1. El-Omar E.M., Carrington M., Chow W.H., McColl K.E., Bream J.H., Young H.A., Herrera J., Lissowska J., Yuan C.C., Rothman N., et al. The role of interleukin-1 polymorphisms in the pathogenesis of gastric cancer. Nature. 2001;412:99–100. doi: 10.1038/35083631.
    1. Li X., Liu C., Ip B.C., Hu K.-Q., Smith D.E., Greenberg A.S., Wang X.-D. Tumor progression locus 2 ablation suppressed hepatocellular carcinoma development by inhibiting hepatic inflammation and steatosis in mice. J. Exp. Clin. Cancer Res. 2015;34:138. doi: 10.1186/s13046-015-0254-2.
    1. Chiu A.P., Tschida B.R., Sham T.-T., Lo L.H., Moriarity B.S., Li X.-X., Lo R.C., Hinton D.E., Rowlands D.K., Chan C.-O., et al. HBx-K130M/V131I promotes liver cancer in transgenic mice via AKT/FOXO1 signaling pathway and arachidonic acid metabolism. Mol. Cancer Res. 2019;17:1582–1593. doi: 10.1158/1541-7786.MCR-18-1127.
    1. Buendia M.-A., Neuveut C. Hepatocellular carcinoma. Cold Spring Harb. Perspect. Med. 2015;5:a021444. doi: 10.1101/cshperspect.a021444.
    1. Anfuso B., El-Khobar K.E., Ie S.I., Avellini C., Radillo O., Raseni A., Tiribelli C., Sukowati C.H.C. Activation of hepatic stem cells compartment during hepatocarcinogenesis in a HBsAg HBV-transgenic mouse model. Sci. Rep. 2018;8:13168. doi: 10.1038/s41598-018-31406-5.
    1. Hussain S.P., Hofseth L.J., Harris C.C. Radical causes of cancer. Nat. Rev. Cancer. 2003;3:276–285. doi: 10.1038/nrc1046.
    1. Koike K. Molecular basis of hepatitis C virus-associated hepatocarcinogenesis: Lessons from animal model studies. Clin. Gastroenterol. Hepatol. 2005;3:S132–S135. doi: 10.1016/S1542-3565(05)00700-7.
    1. McGivern D.R., Lemon S.M. Virus-specific mechanisms of carcinogenesis in hepatitis C virus associated liver cancer. Oncogene. 2011;30:1969–1983. doi: 10.1038/onc.2010.594.
    1. Li Y., Togashi Y., Sato S., Emoto T., Kang J.-H., Takeichi N., Kobayashi H., Kojima Y., Une Y., Uchino J. Abnormal copper accumulation in non-cancerous and cancerous liver tissues of LEC rats developing hereditary hepatitis and spontaneous hepatoma. Jpn. J. Cancer Res. 1991;82:490–492. doi: 10.1111/j.1349-7006.1991.tb01876.x.
    1. Li Y., Togashi Y., Sato S., Emoto T., Kang J.H., Takeichi N., Kobayashi H., Kojima Y., Une Y., Uchino J. Spontaneous hepatic copper accumulation in Long-Evans Cinnamon rats with hereditary hepatitis. A model of Wilson’s disease. J. Clin. Investig. 1991;87:1858–1861. doi: 10.1172/JCI115208.
    1. Yamaguchi Y., Heiny M.E., Shimizu N., Aoki T., Gitlin J.D. Expression of the Wilson disease gene is deficient in the Long-Evans Cinnamon rat. Biochem. J. 1994;301:1–4. doi: 10.1042/bj3010001.
    1. Gouveia M.J., Pakharukova M.Y., Laha T., Sripa B., Maksimova G.A., Rinaldi G., Brindley P.J., Mordvinov V.A., Amaro T., Santos L.L., et al. Infection with Opisthorchis felineus induces intraepithelial neoplasia of the biliary tract in a rodent model. Carcinogenesis. 2017;38:929–937. doi: 10.1093/carcin/bgx042.
    1. Khoontawad J., Pairojkul C., Rucksaken R., Pinlaor P., Wongkham C., Yongvanit P., Pugkhem A., Jones A., Plieskatt J., Potriquet J., et al. Differential protein expression marks the transition from infection withopisthorchis viverrinito cholangiocarcinoma. Mol. Cell. Proteom. 2017;16:911–923. doi: 10.1074/mcp.M116.064576.
    1. Prakobwong S., Khoontawad J., Yongvanit P., Pairojkul C., Hiraku Y., Sithithaworn P., Pinlaor P., Aggarwal B.B., Pinlaor S. Curcumin decreases cholangiocarcinogenesis in hamsters by suppressing inflammation-mediated molecular events related to multistep carcinogenesis. Int. J. Cancer. 2011;129:88–100. doi: 10.1002/ijc.25656.
    1. Chan I.S., Guy C.D., Machado M.V., Wank A., Kadiyala V., Michelotti G., Choi S., Swiderska-Syn M., Karaca G., Pereira T.A., et al. Alcohol Activates the hedgehog pathway and induces related procarcinogenic processes in the alcohol-preferring rat model of hepatocarcinogenesis. Alcohol. Clin. Exp. Res. 2014;38:787–800. doi: 10.1111/acer.12279.
    1. Yip-Schneider M.T., Doyle C.J., McKillop I.H., Wentz S.C., Brandon-Warner E., Matos J.M., Sandrasegaran K., Saxena R., Hennig M.E., Wu H., et al. Alcohol induces liver neoplasia in a novel alcohol-preferring rat model. Alcohol. Clin. Exp. Res. 2011;35:2216–2225. doi: 10.1111/j.1530-0277.2011.01568.x.
    1. Ip B.C., Wang X.-D. Non-alcoholic steatohepatitis and hepatocellular carcinoma: Implications for lycopene intervention. Nutrients. 2013;6:124–162. doi: 10.3390/nu6010124.
    1. Miyazaki T., Shirakami Y., Kubota M., Ideta T., Kochi T., Sakai H., Tanaka T., Moriwaki H., Shimizu M. Sodium alginate prevents progression of non-alcoholic steatohepatitis and liver carcinogenesis in obese and diabetic mice. Oncotarget. 2016;7:10448–10458. doi: 10.18632/oncotarget.7249.
    1. Sasaki Y., Suzuki W., Shimada T., Iizuka S., Nakamura S., Nagata M., Fujimoto M., Tsuneyama K., Hokao R., Miyamoto K.-I., et al. Dose dependent development of diabetes mellitus and non-alcoholic steatohepatitis in monosodium glutamate-induced obese mice. Life Sci. 2009;85:490–498. doi: 10.1016/j.lfs.2009.07.017.
    1. Ma C., Kesarwala A.H., Eggert T., Medina-Echeverz J., Kleiner D.E., Jin P., Stroncek D.F., Terabe M., Kapoor V., Elgindi M., et al. NAFLD causes selective CD4+ T lymphocyte loss and promotes hepatocarcinogenesis. Nature. 2016;531:253–257. doi: 10.1038/nature16969.
    1. Shachaf C.M., Kopelman A.M., Arvanitis C., Karlsson Å., Beer S., Mandl S., Bachmann M.H., Borowsky A.D., Ruebner B., Cardiff R.D., et al. MYC inactivation uncovers pluripotent differentiation and tumour dormancy in hepatocellular cancer. Nature. 2004;431:1112–1117. doi: 10.1038/nature03043.
    1. Sagawa H., Naiki-Ito A., Kato H., Naiki T., Yamashita Y., Suzuki S., Sato S., Shiomi K., Kato A., Kuno T., et al. Connexin 32 and luteolin play protective roles in non-alcoholic steatohepatitis development and its related hepatocarcinogenesis in rats. Carcinogenesis. 2015;36:1539–1549. doi: 10.1093/carcin/bgv143.
    1. Nakae D. Endogenous liver carcinogenesis in the rat. Pathol. Int. 1999;49:1028–1042. doi: 10.1046/j.1440-1827.1999.00990.x.
    1. Coia H., Ma N., Hou Y., Dyba M.D., Fu Y., Cruz M.I., Benitez C., Graham G.T., McCutcheon J.N., Zheng Y.-L., et al. Prevention of lipid peroxidation–derived cyclic DNA adduct and mutation in high-fat diet–induced hepatocarcinogenesis by Theaphenon E. Cancer Prev. Res. 2018;11:665–676. doi: 10.1158/1940-6207.CAPR-18-0160.
    1. Ip B.C., Hu K.-Q., Liu C., Smith D.E., Obin M.S., Ausman L.M., Wang X.-D. Lycopene metabolite, apo-10′-lycopenoic acid, inhibits diethylnitrosamine-initiated, high fat diet–promoted hepatic inflammation and tumorigenesis in mice. Cancer Prev. Res. 2013;6:1304–1316. doi: 10.1158/1940-6207.CAPR-13-0178.
    1. Patterson M.M., Rogers A.B., Fox J.G. Experimental Helicobacter marmotae infection in A/J mice causes enterohepatic disease. J. Med. Microbiol. 2010;59:1235–1241. doi: 10.1099/jmm.0.020479-0.
    1. Chen N., Nishio N., Ito S., Tanaka Y., Sun Y., Isobe K.-I. Growth arrest and DNA damage-inducible protein (GADD34) enhanced liver inflammation and tumorigenesis in a diethylnitrosamine (DEN)-treated murine model. Cancer Immunol. Immunother. 2015;64:777–789. doi: 10.1007/s00262-015-1690-8.
    1. Fujii Y., Segawa R., Kimura M., Wang L., Ishii Y., Yamamoto R., Morita R., Mitsumori K., Shibutani M. Inhibitory effect of α-lipoic acid on thioacetamide-induced tumor promotion through suppression of inflammatory cell responses in a two-stage hepatocarcinogenesis model in rats. Chem. Biol. Interactions. 2013;205:108–118. doi: 10.1016/j.cbi.2013.06.017.
    1. Sun L., Beggs K., Borude P., Edwards G., Bhushan B., Walesky C., Roy N., Manley M.W., Gunewardena S., O’Neil M., et al. Bile acids promote diethylnitrosamine-induced hepatocellular carcinoma via increased inflammatory signaling. Am. J. Physiol. Gastrointest. l Liver Physiol. 2016;311:G91–G104. doi: 10.1152/ajpgi.00027.2015.
    1. Nagano K., Sasaki T., Umeda Y., Nishizawa T., Ikawa N., Ohbayashi H., Arito H., Yamamoto S., Fukushima S. Inhalation carcinogenicity and chronic toxicity of carbon tetrachloride in rats and mice. Inhal. Toxicol. 2007;19:1089–1103. doi: 10.1080/08958370701628770.
    1. Ni H.-M., Woolbright B.L., Williams J., Copple B., Cui W., Luyendyk J.P., Jaeschke H., Ding W.-X. Nrf2 promotes the development of fibrosis and tumorigenesis in mice with defective hepatic autophagy. J. Hepatol. 2014;61:617–625. doi: 10.1016/j.jhep.2014.04.043.
    1. Mitra A., Yan J., Xia X., Zhou S., Chen J., Mishra L., Li S. IL6-mediated inflammatory loop reprograms normal to epithelial-mesenchymal transition+metastatic cancer stem cells in preneoplastic liver of transforming growth factor beta-deficient β2-spectrin+/−mice. Hepatology. 2017;65:1222–1236. doi: 10.1002/hep.28951.
    1. Kim I., Morimura K., Shah Y., Yang Q., Ward J.M., Gonzalez F.J. Spontaneous hepatocarcinogenesis in farnesoid X receptor-null mice. Carcinogenesis. 2006;28:940–946. doi: 10.1093/carcin/bgl249.
    1. Zhao X., Fu J., Xu A., Yu L., Zhu J., Dai R., Su B., Luo T., Li N., Qin W., et al. Gankyrin drives malignant transformation of chronic liver damage-mediated fibrosis via the Rac1/JNK pathway. Cell Death Dis. 2015;6:e1751. doi: 10.1038/cddis.2015.120.
    1. Shimizu M., Sakai H., Shirakami Y., Iwasa J., Yasuda Y., Kubota M., Takai K., Tsurumi H., Tanaka T., Moriwaki H. Acyclic retinoid inhibits diethylnitrosamine-induced liver tumorigenesis in obese and diabetic C57BLKS/J- +Leprdb/+Leprdb Mice. Cancer Prev. Res. 2011;4:128–136. doi: 10.1158/1940-6207.CAPR-10-0163.
    1. Faggioli F., Palagano E., Di Tommaso L., Donadon M., Marrella V., Recordati C., Mantero S., Villa A., Vezzoni P., Cassani B. B lymphocytes limit senescence-driven fibrosis resolution and favor hepatocarcinogenesis in mouse liver injury. Hepatology. 2018;67:1970–1985. doi: 10.1002/hep.29636.
    1. Takai A., Toyoshima T., Uemura M., Kitawaki Y., Marusawa H., Hiai H., Yamada S., Okazaki I.M., Honjo T., Chiba T., et al. A novel mouse model of hepatocarcinogenesis triggered by AID causing deleterious p53 mutations. Oncogene. 2008;28:469–478. doi: 10.1038/onc.2008.415.
    1. Carrière C., Young A.L., Gunn J.R., Longnecker D.S., Korc M. Acute pancreatitis markedly accelerates pancreatic cancer progression in mice expressing oncogenic Kras. Biochem. Biophys. Res. Commun. 2009;382:561–565. doi: 10.1016/j.bbrc.2009.03.068.
    1. Ding L., Liou G.-Y., Schmitt D.M., Storz P., Zhang J.-S., Billadeau D.D. Glycogen synthase kinase-3β ablation limits pancreatitis-induced acinar-to-ductal metaplasia. J. Pathol. 2017;243:65–77. doi: 10.1002/path.4928.
    1. Philip B., Roland C.L., Daniluk J., Liu Y., Chatterjee D., Gomez S.B., Ji B., Huang H., Wang H., Fleming J.B., et al. A High-fat diet activates oncogenic kras and COX2 to induce development of pancreatic ductal adenocarcinoma in mice. Gastroenterology. 2013;145:1449–1458. doi: 10.1053/j.gastro.2013.08.018.
    1. Kohno H., Suzuki R., Sugie S., Tanaka T. Beta-Catenin mutations in a mouse model of inflammation-related colon carcinogenesis induced by 1,2-dimethylhydrazine and dextran sodium sulfate. Cancer Sci. 2005;96:69–76. doi: 10.1111/j.1349-7006.2005.00020.x.
    1. Tanaka T., Kohno H., Suzuki R., Yamada Y., Sugie S., Mori H. A novel inflammation-related mouse colon carcinogenesis model induced by azoxymethane and dextran sodium sulfate. Cancer Sci. 2003;94:965–973. doi: 10.1111/j.1349-7006.2003.tb01386.x.
    1. Yamada M., Ohkusa T., Okayasu I. Occurrence of dysplasia and adenocarcinoma after experimental chronic ulcerative colitis in hamsters induced by dextran sulphate sodium. Gut. 1992;33:1521–1527. doi: 10.1136/gut.33.11.1521.
    1. Zak S., Treven J., Nash N., Gutierrez L.S. Lack of thrombospondin-1 increases angiogenesis in a model of chronic inflammatory bowel disease. Int. J. Colorectal Dis. 2007;23:297–304. doi: 10.1007/s00384-007-0397-5.
    1. Okayasu I., Ohkusa T., Kajiura K., Kanno J., Sakamoto S. Promotion of colorectal neoplasia in experimental murine ulcerative colitis. Gut. 1996;39:87–92. doi: 10.1136/gut.39.1.87.
    1. Fazio V.M., De Robertis M., Massi E., Poeta M.L., Carotti S., Morini S., Cecchetelli L., Signori E. The AOM/DSS murine model for the study of colon carcinogenesis: From pathways to diagnosis and therapy studies. J. Carcinog. 2011;10:9. doi: 10.4103/1477-3163.78279.
    1. Suzuki R., Kohno H., Sugie S., Nakagama H., Tanaka T. Strain differences in the susceptibility to azoxymethane and dextran sodium sulfate-induced colon carcinogenesis in mice. Carcinogenesis. 2006;27:162–169. doi: 10.1093/carcin/bgi205.
    1. de Moreno de Leblanc A., Perdigón G. The application of probiotic fermented milks in cancer and intestinal inflammation. Proc. Nutr. Soc. 2010;69:421–428. doi: 10.1017/S002966511000159X.
    1. Xiao Y., Dai X., Li K., Gui G., Liu J., Yang H. Clostridium butyricum partially regulates the development of colitis-associated cancer through miR-200c. Cell. Mol. Biol. 2017;63:59–66. doi: 10.14715/cmb/2017.63.4.10.
    1. Nyuyki K.D., Beiderbeck D.I., Lukas M., Neumann I.D., Reber S.O. Chronic subordinate colony housing (CSC) as a model of chronic psychosocial stress in male rats. PLoS ONE. 2012;7:e52371. doi: 10.1371/journal.pone.0052371.
    1. Reber S.O., Langgartner D., Foertsch S., Postolache T.T., Brenner L.A., Guendel H., Lowry C.A. Chronic subordinate colony housing paradigm: A mouse model for mechanisms of PTSD vulnerability, targeted prevention, and treatment—2016 Curt Richter Award Paper. Psychoneuroendocrinology. 2016;74:221–230. doi: 10.1016/j.psyneuen.2016.08.031.
    1. Peters S., Grunwald N., Rümmele P., Endlicher E., Lechner A., Neumann I.D., Obermeier F., Reber S.O. Chronic psychosocial stress increases the risk for inflammation-related colon carcinogenesis in male mice. Stress. 2012;15:403–415. doi: 10.3109/10253890.2011.631232.
    1. Shirakami Y., Shimizu M., Kubota M., Araki H., Tanaka T., Moriwaki H., Seishima M. Chemoprevention of colorectal cancer by targeting obesity-related metabolic abnormalities. World J. Gastroenterol. 2014;20:8939–8946.
    1. Matsui S., Okabayashi K., Tsuruta M., Shigeta K., Seishima R., Ishida T., Kondo T., Suzuki Y., Hasegawa H., Shimoda M., et al. Interleukin-13 and its signaling pathway is associated with obesity-related colorectal tumorigenesis. Cancer Sci. 2019;110:2156–2165. doi: 10.1111/cas.14066.
    1. Hintze K.J., Benninghoff A.D., Ward R.E. Formulation of the Total Western Diet (TWD) as a basal diet for rodent cancer studies. J. Agric. Food Chem. 2021;60:6736–6742. doi: 10.1021/jf204509a.
    1. Sido A., Radhakrishnan S., Kim S.W., Eriksson E., Shen F., Li Q., Bhat V., Reddivari L., Vanamala J.K. A food-based approach that targets interleukin-6, a key regulator of chronic intestinal inflammation and colon carcinogenesis. J. Nutr. Biochem. 2017;43:11–17. doi: 10.1016/j.jnutbio.2017.01.012.
    1. Newmark H., Yang K., Lipkin M., Kopelovich L., Liu Y., Fan K., Shinozaki H. A Western-style diet induces benign and malignant neoplasms in the colon of normal C57Bl/6 mice. Carcinogenesis. 2001;22:1871–1875. doi: 10.1093/carcin/22.11.1871.
    1. Hursting S.D., Slaga T.J., Fischer S.M., DiGiovanni J., Phang J.M. Mechanism-based cancer prevention approaches: Targets, examples, and the use of transgenic mice. J. Natl. Cancer Inst. 1999;91:215–225. doi: 10.1093/jnci/91.3.215.
    1. Yu S., Yin Y., Wang Q., Wang L. Dual gene deficient models of ApcMin/+ mouse in assessing molecular mechanisms of intestinal carcinogenesis. Biomed. Pharmacother. 2018;108:600–609. doi: 10.1016/j.biopha.2018.09.056.
    1. Tanaka T. Preclinical cancer chemoprevention studies using animal model of inflammation-associated colorectal carcinogenesis. Cancers. 2012;4:673–700. doi: 10.3390/cancers4030673.
    1. Fodde R., Smits R. Disease model: Familial adenomatous polyposis. Trends Mol. Med. 2001;7:369–373. doi: 10.1016/S1471-4914(01)02050-0.
    1. Wang L., Zhang Q. Application of the ApcMin/+ mouse model for studying inflammation-associated intestinal tumor. Biomed. Pharmacother. 2015;71:216–221. doi: 10.1016/j.biopha.2015.02.023.
    1. Slocum S.L., Kensler T.W. Nrf2: Control of sensitivity to carcinogens. Arch. Toxicol. 2011;85:273–284. doi: 10.1007/s00204-011-0675-4.
    1. Tomkovich S., Yang Y., Winglee K., Gauthier J., Mühlbauer M., Sun X., Mohamadzadeh M., Liu X., Martin P., Wang G.P., et al. Locoregional effects of microbiota in a preclinical model of colon carcinogenesis. Cancer Res. 2017;77:2620–2632. doi: 10.1158/0008-5472.CAN-16-3472.
    1. Ito K., Ishigamori R., Mutoh M., Ohta T., Imai T., Takahashi M. A y allele promotes azoxymethane-induced colorectal carcinogenesis by macrophage migration in hyperlipidemic/diabetic KK mice. Cancer Sci. 2013;104:835–843. doi: 10.1111/cas.12162.
    1. Ye Q., Zheng Y., Fan S., Qin Z., Li N., Tang A., Ai F., Zhang X., Bian Y., Dang W., et al. Lactoferrin deficiency promotes colitis-associated colorectal dysplasia in mice. PLoS ONE. 2014;9:e103298. doi: 10.1371/journal.pone.0103298.
    1. Osburn W.O., Kensler T.W. Nrf2 signaling: An adaptive response pathway for protection against environmental toxic insults. Mutat. Res. 2008;659:31–39. doi: 10.1016/j.mrrev.2007.11.006.
    1. Binder Gallimidi A., Nussbaum G., Hermano E., Weizman B., Meirovitz A., Vlodavsky I., Götte M., Elkin M. Syndecan-1 deficiency promotes tumor growth in a murine model of colitis-induced colon carcinoma. PLoS ONE. 2017;12:e0174343. doi: 10.1371/journal.pone.0174343.
    1. Zha L., Garrett S., Sun J. Salmonella infection in chronic inflammation and gastrointestinal cancer. Diseases. 2019;7:28. doi: 10.3390/diseases7010028.
    1. Okada F., Kawaguchi T., Habelhah H., Kobayashi T., Tazawa H., Takeichi N., Kitagawa T., Hosokawa M. Conversion of human colonic adenoma cells to adenocarcinoma cells through inflammation in nude mice. Lab. Investig. 2000;80:1617–1628. doi: 10.1038/labinvest.3780172.
    1. Kanda Y., Kawaguchi T., Kuramitsu Y., Kitagawa T., Kobayashi T., Takahashi N., Tazawa H., Habelhah H., Hamada J.-I., Kobayashi M., et al. Fascin regulates chronic inflammation-related human colon carcinogenesis by inhibiting cell anoikis. Proteomics. 2014;14:1031–1041. doi: 10.1002/pmic.201300414.
    1. Kanda Y., Kawaguchi T., Osaki M., Onuma K., Ochiya T., Kitagawa T., Okada F. Fascin protein stabilization by miR-146a implicated in the process of a chronic inflammation-related colon carcinogenesis model. Inflamm. Res. 2018;67:839–846. doi: 10.1007/s00011-018-1175-2.
    1. Steiner J.L., Davis J.M., McClellan J., Guglielmotti A., Murphy E. Effects of the MCP-1 synthesis inhibitor bindarit on tumorigenesis and inflammatory markers in the C3(1)/SV40Tag mouse model of breast cancer. Cytokine. 2014;66:60–68. doi: 10.1016/j.cyto.2013.12.011.
    1. Santiago L., Castro M., Pardo J., Arias M. Mouse model of colitis-associated colorectal cancer (CAC): Isolation and characterization of mucosal-associated lymphoid cells. Methods Mol. Biol. 2019;1884:189–202. doi: 10.1007/978-1-4939-8885-3_13.
    1. Hamada J., Takeichi N., Okada F., Ren J., Li X., Hosokawa M., Kobayashi H. Progression of weakly malignant clone cells derived from rat mammary carcinoma by host cells reactive to plastic plates. Jpn. J. Cancer Res. 1992;83:483–490. doi: 10.1111/j.1349-7006.1992.tb01953.x.
    1. Hamada J.-I., Nakata D., Nakae D., Kobayashi Y., Akai H., Konishi Y., Okada F., Shibata T., Hosokawa M., Moriuchi T. Increased oxidative DNA damage in mammary tumor cells by continuous epidermal growth factor stimulation. J. Natl. Cancer Inst. 2001;93:214–219. doi: 10.1093/jnci/93.3.214.
    1. Nagayasu H., Hamada J., Nakata D., Shibata T., Kobayashi M., Hosokawa M., Takeichi N. Reversible and irreversible tumor progression of a weakly malignant rat mammary carcinoma cell line by in vitro exposure to epidermal growth factor. Int. J. Oncol. 1998;12:197–399. doi: 10.3892/ijo.12.1.197.
    1. Lucchini F., Sacco M.G., Hu N., Villa A., Brown J., Cesano L., Mangiarini L., Rindi G., Kindl S., Sessa F., et al. Early and multifocal tumors in breast, salivary, Harderian and epididymal tissues developed in MMTY-Neu transgenic mice. Cancer Lett. 1992;64:203–209. doi: 10.1016/0304-3835(92)90044-V.
    1. Calogero R.A., Cordero F., Forni G., Cavallo F. Inflammation and breast cancer. Inflammatory component of mammary carcinogenesis in ErbB2 transgenic mice. Breast Cancer Res. 2007;9:211. doi: 10.1186/bcr1745.
    1. Sangaletti S., Tripodo C., Ratti C., Piconese S., Porcasi R., Salcedo R., Trinchieri G., Colombo M.P., Chiodoni C. Oncogene-driven intrinsic inflammation induces leukocyte production of tumor necrosis factor that critically contributes to mammary carcinogenesis. Cancer Res. 2010;70:7764–7775. doi: 10.1158/0008-5472.CAN-10-0471.
    1. Guy C.T., Cardiff R.D., Muller W.J. Induction of mammary tumors by expression of polyomavirus middle T oncogene: A transgenic mouse model for metastatic disease. Mol. Cell. Biol. 1992;12:954–961. doi: 10.1128/MCB.12.3.954.
    1. Franklin R.A., Liao W., Sarkar A., Kim M.V., Bivona M.R., Liu K., Pamer E.G., Li M.O. The cellular and molecular origin of tumor-associated macrophages. Science. 2014;344:921–925. doi: 10.1126/science.1252510.
    1. Yamashita S., Suzuki S., Nomoto T., Kondo Y., Wakazono K., Tsujino Y., Sugimura T., Shirai T., Homma Y., Ushijima T. Linkage and microarray analyses of susceptibility genes in ACI/Seg rats: A model for prostate cancers in the aged. Cancer Res. 2005;65:2610–2616. doi: 10.1158/0008-5472.CAN-04-2932.
    1. Reyes I., Reyes N., Iatropoulos M., Mittelman A., Geliebter J. Aging-associated changes in gene expression in the ACI rat prostate: Implications for carcinogenesis. Prostate. 2005;63:169–186. doi: 10.1002/pros.20164.
    1. Özten N., Horton L., Lasano S., Bosland M.C. Selenomethionine and α-tocopherol do not inhibit prostate carcinogenesis in the testosterone plus estradiol–treated NBL rat model. Cancer Prev. Res. 2010;3:371–380. doi: 10.1158/1940-6207.CAPR-09-0152.
    1. Lesovaya E.A., Kirsanov K.I., Antoshina E.E., Trukhanova L.S., Gorkova T.G., Shipaeva E.V., Salimov R.M., Belitsky G.A., Blagosklonny M.V., Yakubovskaya M.G., et al. Rapatar, a nanoformulation of rapamycin, decreases chemically-induced benign prostate hyperplasia in rats. Oncotarget. 2015;6:9718–9727. doi: 10.18632/oncotarget.3929.
    1. Smith D.A., Kiba A., Zong Y., Witte O.N. Interleukin-6 and oncostatin-M synergize with the PI3K/AKT pathway to promote aggressive prostate malignancy in mouse and human tissues. Mol. Cancer Res. 2013;11:1159–1165. doi: 10.1158/1541-7786.MCR-13-0238.
    1. Ray D., Nelson T.A., Fu C.-L., Patel S., Gong D.N., Odegaard J.I., Hsieh M.H. Transcriptional profiling of the bladder in urogenital schistosomiasis reveals pathways of inflammatory fibrosis and urothelial compromise. PLOS Neglected Trop. Dis. 2012;6:e1912. doi: 10.1371/journal.pntd.0001912.
    1. Ebina Y., Okada S., Hamazaki S., Ogino F., Midorikawa O., Li J.-L. Nephrotoxicity and renal cell carcinoma after use of iron- and aluminum-nitrilotriacetate complexes in rats. J. Natl. Cancer Inst. 1986;76:107–113. doi: 10.1093/jnci/76.1.107.
    1. Kasprzak K.S., Diwan B.A., Rice J.M. Iron accelerates while magnesium inhibits nickel-induced carcinogenesis in the rat kidney. Toxicology. 1994;90:129–140. doi: 10.1016/0300-483X(94)90211-9.
    1. Chaudhary S.C., Waseem M., Rana M., Xu H., Kopelovich L., Elmets C.A., Athar M. Naproxen inhibits UVB-induced Basal cell and squamous cell carcinoma development in Ptch1+/−/SKH-1 hairless mice. Photochem. Photobiol. 2017;93:1016–1024. doi: 10.1111/php.12758.
    1. Kong Y.-H., Xu S.-P. Salidroside prevents skin carcinogenesis induced by DMBA/TPA in a mouse model through suppression of inflammation and promotion of apoptosis. Oncol. Rep. 2018;39:2513–2526. doi: 10.3892/or.2018.6381.
    1. Bishayee A. Cancer prevention and treatment with resveratrol: From rodent studies to clinical trials. Cancer Prev. Res. 2009;2:409–418. doi: 10.1158/1940-6207.CAPR-08-0160.
    1. Marks F., Fürstenberger G., Heinzelmann T., Müller-Decker K. Mechanisms in tumor promotion: Guidance for risk assessment and cancer chemoprevention. Toxicol. Lett. 1995;82–83:907–917. doi: 10.1016/0378-4274(95)03529-X.
    1. Chaudhary S.C., Tang X., Arumugam A., Li C., Srivastava R.K., Weng Z., Xu J., Zhang X., Kim A.L., McKay K., et al. Shh and p50/Bcl3 signaling crosstalk drives pathogenesis of BCCs in gorlin syndrome. Oncotarget. 2015;6:36789–36814. doi: 10.18632/oncotarget.5103.
    1. Kunisada M., Hosaka C., Takemori C., Nakano E., Nishigori C. CXCL1 Inhibition regulates UVB-induced skin inflammation and tumorigenesis in Xpa-deficient mice. J. Investig. Dermatol. 2017;137:1975–1983. doi: 10.1016/j.jid.2017.04.034.
    1. Okada F., Hosokawa M., Hasegawa J., Ishikawa M., Chiba I., Nakamura Y., Kobayashi H. Regression mechanisms of mouse fibrosarcoma cells after in vitro exposure to quercetin: Diminution of tumorigenicity with a corresponding decrease in the production of prostaglandin E2. Cancer Immunol. Immunother. 1990;31:358–364. doi: 10.1007/BF01741407.
    1. Okada F., Hosokawa M., Hamada J.-I., Hasegawa J., Mizutani M., Takeichi N., Kobayashi H. Progression of a weakly tumorigenic mouse fibrosarcoma at the site of early phase of inflammation caused by plastic plates. Jpn. J. Cancer Res. 1993;84:1230–1236. doi: 10.1111/j.1349-7006.1993.tb02827.x.
    1. Okada F., Hosokawa M., Hamada J.-I., Hasegawa J., Kato M., Mizutani M., Ren J., Takeichi N., Kobayashi H. Malignant progression of a mouse fibrosarcoma by host cells reactive to a foreign body (gelatin sponge) Br. J. Cancer. 1992;66:635–639. doi: 10.1038/bjc.1992.329.
    1. Habelhah H., Okada F., Kobayashi M., Nakai K., Choi S., Hamada J.-I., Moriuchi T., Kaya M., Yoshida K., Fujinaga K., et al. Increased E1AF expression in mouse fibrosarcoma promotes metastasis through induction of MT1-MMP expression. Oncogene. 1999;18:1771–1776. doi: 10.1038/sj.onc.1202465.
    1. Kobayashi T., Okada F., Fujii N., Tomita N., Ito S., Tazawa H., Aoyama T., Choi S.K., Shibata T., Fujita H., et al. Thymosin-β4 regulates motility and metastasis of malignant mouse fibrosarcoma cells. Am. J. Pathol. 2002;160:869–882. doi: 10.1016/S0002-9440(10)64910-3.
    1. Tazawa H., Okada F., Kobayashi T., Tada M., Mori Y., Une Y., Sendo F., Kobayashi M., Hosokawa M. Infiltration of neutrophils is required for acquisition of metastatic phenotype of benign murine fibrosarcoma cells: Implication of inflammation-associated carcinogenesis and tumor progression. Am. J. Pathol. 2003;163:2221–2232. doi: 10.1016/S0002-9440(10)63580-8.
    1. Okada F., Kobayashi M., Tanaka H., Kobayashi T., Tazawa H., Iuchi Y., Onuma K., Hosokawa M., Dinauer M.C., Hunt N.H. The role of nicotinamide adenine dinucleotide phosphate oxidase-derived reactive oxygen species in the acquisition of metastatic ability of tumor cells. Am. J. Pathol. 2006;169:294–302. doi: 10.2353/ajpath.2006.060073.
    1. Ma Q., Cavallin L.E., Yan B., Zhu S., Duran E.M., Wang H., Hale L.P., Dong C., Cesarman E., Mesri E.A., et al. Antitumorigenesis of antioxidants in a transgenic Rac1 model of Kaposi’s sarcoma. Proc. Natl. Acad. Sci. USA. 2009;106:8683–8688. doi: 10.1073/pnas.0812688106.
    1. Tazawa H., Tatemichi M., Sawa T., Gilibert I., Ma N., Hiraku Y., Donehower L.A., Ohgaki H., Kawanishi S., Ohshima H. Oxidative and nitrative stress caused by subcutaneous implantation of a foreign body accelerates sarcoma development in Trp53+/- mice. Carcinogenesis. 2007;28:191–198. doi: 10.1093/carcin/bgl128.
    1. Guerra C., Schuhmacher A.J., Cañamero M., Grippo P.J., Verdaguer L., Pérez-Gallego L., Dubus P., Sandgren E.P., Barbacid M. Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice. Cancer Cell. 2007;11:291–302. doi: 10.1016/j.ccr.2007.01.012.
    1. Ashi K.W., Inagaki T., Fujimoto Y., Fukuda Y. Induction by degraded carrageenan of colorectal tumors in rats. Cancer Lett. 1978;4:171–176. doi: 10.1016/s0304-3835(78)94237-4.
    1. Devapatla B., Sanders J., Samuelson D.J. Genetically determined inflammatory-response related cytokine and chemokine transcript profiles between mammary carcinoma resistant and susceptible rat strains. Cytokine. 2012;59:223–227. doi: 10.1016/j.cyto.2012.04.037.
    1. Fabian R.J., Abraham R., Coulston F., Golberg L. Carrageenan-induced squamous metaplasia of the rectal mucosa in the rat. Gastroenterology. 1973;65:265–276. doi: 10.1016/S0016-5085(19)33108-7.
    1. Cater D.B. The carcinogenic action of carrageenin in rats. Br. J. Cancer. 1961;15:607–614. doi: 10.1038/bjc.1961.70.
    1. Okayasu I., Yamada M., Mikami T., Yoshida T., Kanno J., Ohkusa T. Dysplasia and carcinoma development in a repeated dextran sulfate sodium-induced colitis model. J. Gastroenterol. Hepatol. 2002;17:1078–1083. doi: 10.1046/j.1440-1746.2002.02853.x.
    1. Hirono I., Kuhara K., Yamaji T., Hosaka S., Golberg L. Induction of colorectal squamous cell carcinomas in rats by dextran sulfate sodium. Carcinogenesis. 1982;3:353–355. doi: 10.1093/carcin/3.3.353.
    1. Hirono I., Kuhara K., Hosaka S., Tomizawa S., Golberg L. Induction of intestinal tumors in rats by dextran sulfate sodium. J. Natl. Cancer Inst. 1981;66:579–583.
    1. Sugie S., Mori Y., Okumura A., Yoshimi N., Okamoto K., Sato S., Tanaka T., Mori H. Promoting and synergistic effects of chrysazin on 1,2-dimethylhydrazine-induced carcinogenesis in male ICR/CD-1 mice. Carcinogenesis. 1994;15:1175–1179. doi: 10.1093/carcin/15.6.1175.
    1. Tanaka T., Kohno H., Yoshitani S., Takashima S., Okumura A., Murakami A., Hosokawa M. Ligands for peroxisome proliferator-activated receptors alpha and gamma inhibit chemically induced colitis and formation of aberrant crypt foci in rats. Cancer Res. 2001;61:2424–2428.
    1. Khor T.O., Huang M.-T., Prawan A., Liu Y., Hao X., Yu S., Cheung W.K.L., Chan J.Y., Reddy B.S., Yang C.S., et al. Increased susceptibility of Nrf2 knockout mice to colitis-associated colorectal cancer. Cancer Prev. Res. 2008;1:187–191. doi: 10.1158/1940-6207.CAPR-08-0028.
    1. Lowe E.L., Crother T.R., Rabizadeh S., Hu B., Wang H., Chen S., Shimada K., Wong M.H., Michelsen K.S., Arditi M. Toll-like receptor 2 signaling protects mice from tumor development in a mouse model of colitis-induced cancer. PLoS One. 2010;5:e13027. doi: 10.1371/journal.pone.0013027.
    1. Chen X., Ding Y.W., Yang G.Y., Bondoc F., Lee M.J., Yang C.S. Oxidative damage in an esophageal adenocarcinoma model with rats. Carcinogenesis. 2000;21:257–263. doi: 10.1093/carcin/21.2.257.
    1. EhrnstrÖm R.A., Veress B., Arvidsson S., Sternby N.H., Andersson T., LindstrÖm C.G. Dietary supplementation of carbonate promotes spontaneous tumorigenesis in a rat gastric stump model. Scand. J. Gastroenterol. 2006;41:12–20. doi: 10.1080/00365520510024106.
    1. Ambade A., Satishchandran A., Gyongyosi B., Lowe P., Szabo G. Adult mouse model of early hepatocellular carcinoma promoted by alcoholic liver disease. World J. Gastroenterol. 2016;22:4091–4108. doi: 10.3748/wjg.v22.i16.4091.
    1. Escrich R., Costa I., Moreno M., Cubedo M., Vela E., Escrich E., Moral R. A high-corn-oil diet strongly stimulates mammary carcinogenesis, while a high-extra-virgin-olive-oil diet has a weak effect, through changes in metabolism, immune system function and proliferation/apoptosis pathways. J. Nutr. Biochem. 2019;64:218–227. doi: 10.1016/j.jnutbio.2018.11.001.
    1. Bosland M.C., Ford H., Horton L. Induction at high incidence of ductal prostate adenocarcinomas in NBL/Cr and Sprague-Dawley Hsd: SD rats treated with a combination of testosterone and estradiol-17 beta or diethylstilbestrol. Carcinogenesis. 1995;16:1311–1317. doi: 10.1093/carcin/16.6.1311.
    1. Mauad T.H., van Nieuwkerk C.M.J., Dingemans K.P., Smit J.J.M., Schinkel A.H., Notenboom R.G.E., van den Bergh Weerman M.A., Verkruisen R.P., Groen A.K., Elferink R.P.J.O., et al. Mice with homozygous disruption of the mdr2 P-glycoprotein gene. A novel animal model for studies of nonsuppurative inflammatory cholangitis and hepatocarcinogenesis. Am. J. Pathol. 1994;145:1237–1245.
    1. Green J.E., Shibata M.A., Yoshidome K., Liu M.L., Jorcyk C., Anver M.R., Wigginton J., Wiltrout R., Shibata E., Kaczmarczyk S., et al. The C3(1)/SV40 T-antigen transgenic mouse model of mammary cancer: Ductal epithelial cell targeting with multistage progression to carcinoma. Oncogene. 2000;19:1020–1027. doi: 10.1038/sj.onc.1203280.
    1. Isaacs J.T. The aging ACI/Seg versus Copenhagen male rat as a model system for the study of prostatic carcinogenesis. Cancer Res. 1984;44:5785–5796.
    1. Ward J.M., Reznik G., Stinson S.F., Lattuada C.P., Longfellow D.G., Cameron T.P. Histogenesis and morphology of naturally occurring prostatic carcinoma in the ACI/segHapBR rat. Lab. Invest. 1980;43:517–522.
    1. Nakane H., Takeuchi S., Yuba S., Saijo M., Nakatsu Y., Murai H., Nakatsuru Y., Ishikawa T., Hirota S., Kitamura Y., et al. High incidence of ultraviolet-B-or chemical-carcinogen-induced skin tumours in mice lacking the xeroderma pigmentosum group A gene. Nature. 1995;377:165–168. doi: 10.1038/377165a0.
    1. Cai X., Carlson J., Stoicov C., Li H., Wang T.C., Houghton J. Helicobacter felis eradication restores normal architecture and inhibits gastric cancer progression in C57BL/6 mice. Gastroenterology. 2005;128:1937–1952. doi: 10.1053/j.gastro.2005.02.066.
    1. Summers J., Smolec J.M., Snyder R. A virus similar to human hepatitis B virus associated with hepatitis and hepatoma in woodchucks. Proc. Natl. Acad. Sci. USA. 1978;75:4533–4537. doi: 10.1073/pnas.75.9.4533.
    1. Moriya K., Fujie H., Shintani Y., Yotsuyanagi H., Tsutsumi T., Ishibashi K., Matsuura Y., Kimura S., Miyamura T., Koike K. The core protein of hepatitis C virus induces hepatocellular carcinoma in transgenic mice. Nat. Med. 1998;4:1065–1067. doi: 10.1038/2053.
    1. Thamavit W., Bhamarapravati N., Sahaphong S., Vajrasthira S., Angsubhakorn S. Effects of dimethylnitrosamine on induction of cholangiocarcinoma in Opisthorchis viverrini-infected Syrian golden hamsters. Cancer Res. 1978;38:4634–4639.
    1. Lakatos H.F., Burgess H.A., Thatcher T.H., Redonnet M.R., Hernady E., Williams J.P., Sime P.J. Oropharyngeal aspiration of a silica suspension produces a superior model of silicosis in the mouse when compared to intratracheal instillation. Exp. Lung Res. 2006;32:181–199. doi: 10.1080/01902140600817465.
    1. Dupré A., Malik H.Z. Inflammation and cancer: What a surgical oncologist should know. Eur. J. Surg. Oncol. 2018;44:566–570. doi: 10.1016/j.ejso.2018.02.209.
    1. Asegaonkar S.B., Asegaonkar B.N., Takalkar U.V., Advani S.H., Thorat A.P. C-reactive protein and breast cancer: New insights from old molecule. Int. J. Breast Cancer. 2015;2015:145647. doi: 10.1155/2015/145647.
    1. Guo L., Liu S., Zhang S., Chen Q., Zhang M., Quan P., Lu J., Sun X. C-reactive protein and risk of breast cancer: A systematic review and meta-analysis. Sci. Rep. 2015;5:10508. doi: 10.1038/srep10508.
    1. Guo Y.-Z., Pan L., Du C.-J., Ren D.-Q., Xie X.-M. Association between c-reactive protein and risk of cancer: A meta-analysis of prospective cohort studies. Asian Pac. J. Cancer Prev. 2013;14:243–248. doi: 10.7314/APJCP.2013.14.1.243.
    1. Heikkilä K., Ebrahim S., Lawlor D.A. A systematic review of the association between circulating concentrations of C reactive protein and cancer. J. Epidemiol. Community Health. 2007;61:824–833. doi: 10.1136/jech.2006.051292.
    1. Krznarić Ž., Markoš P., Ćepulić B.G., Čuković-Čavka S., Domislović V., Bojanić I., Barišić A., Kekez D. Leukocytapheresis in the management of severe steroid-dependent ulcerative colitis. Acta Clin. Croat. 2019;58:529–534. doi: 10.20471/acc.2019.58.03.18.
    1. Kuzmina Z., Stroncek D., Pavletic S.Z. Extracorporeal photopheresis as a therapy for autoimmune diseases. J. Clin. Apher. 2015;30:224–237. doi: 10.1002/jca.21367.
    1. Reiche E.M.V., Morimoto H.K., Nunes S.M.V. Stress and depression-induced immune dysfunction: Implications for the development and progression of cancer. Int. Rev. Psychiatry. 2005;17:515–527. doi: 10.1080/02646830500382102.

Source: PubMed

Sponsorer och medarbetare

Medicinska tillstånd

Läkemedelsinterventioner

3
Prenumerera