EVALUATION OF ANIMAL MODELS BY COMPARISON WITH HUMAN DIABETES MELLITUS: A REVIEW
Keywords:
diabetes, human, animal model, dietAbstract
Animal models are widely used to imitate human diseases to improve the understanding of the pathophysiology of disease and to test treatment interventions. A chronic disease, such as diabetes mellitus, is a fast-growing epidemy worldwide connected with obesity, lack of physical exercise, aging and genetics. This review brings an introduction to diabetes mellitus and compares individual animal models, mainly rodents, with respect to this disease. The selection of a suitable model is important and essential for the progression of new therapeutic methods of preclinical and clinical studies.
References
<div align="justify">Acharjee, S., Ghosh, B., Al-Dhubiab, B. E. & Nair, A. B. (2013). Understanding type 1 diabetes: etiology and models. Canadian Journal of Diabetes, 37(4), 269–276. https://doi.org/ 10.1016/j.jcjd.2013.05.001
<br>American Diabetes Association (2018). Classification and diagnosis of diabetes: standards of medical care in diabetes. Diabetes Care, 41, 13–27.
<br>American Diabetes Association (2015). Classification and diagnosis of diabetes. Diabetes Care, 38, 8–16.
<br>Artasensi, A., Pedretti, A., Vistoli, G. & Fumagalli, L. (2020). Type 2 diabetes mellitus: a review of multi-target drugs. Molecules, 25(8), 1987–2007. https://doi.org/ 10.3390/molecules25081987
<br>Atkinson, M. A. & Leiter, E. H. (1999). The NOD mouse model of type 1 diabetes: as good as it gets? Nature Medicine, 5(6), 601–604. https://doi.org/10.1038/9442
<br>Baribault, H. (2016). Mouse models of type 2 diabetes mellitus in drug discovery. Methods in Molecular Biology, 1438, 153–175. https://doi.org/10.1007/978-1-4939-3661-8_10
<br>Bnouham, M., Ziyyat, A., Mekhfi, H., Tahri A. & Legssyer, A. (2006). Medicinal plants with potential antidiabetic activity – a review of ten years of herbal medicine research (1990-2000). International Journal of Diabetes and Metabolism, 14(1), 1–25. https://doi.org/10.1159/000497588
<br>Boden, G. (2003). Effects of free fatty acids (FFA) on glucose metabolism: significance for insulin resistance and type 2 diabetes. Experimental and Clinical Endocrinology & Diabetes, 111(3), 121–124. https://doi.org/10.1055/s-2003-39781
<br>Capcarova, M., Kalafova, A., Schwarzova, M., Schneidgenova, M., Prnova, M. S., Slovak, L., Kovacik, A., Lory, V. & Zorad, S. (2019). Cornelian cherry fruit improves glycaemia and manifestations of diabetes in obese zucker diabetic fatty rats. Research of Veterinary Science, 126, 118–123. https://doi.org/10.1016/j.rvsc.2019.08.024
<br>Chatzigeorgiou, A., Halapas, A., Kalafatakis, K. & Kamper, E. (2009). Animal Models of Diabetes: a Synopsis. In Vivo, 23, 245–258.
<br>Chehab, F. F., Lim, M. E. & Lu, R. (1996). Correction of the sterility defect in homozygous obese female mice by treatment with the human recombinant leptin. Nature Genetics, 12(3), 318–320. https://doi.org/10.1038/ng0396-318
<br>Cho, N. H., Shaw, J. E., Karunga, S., Huang, Y., Fernandes, J. D. R., Ohlrogge, A. W. & Malanda, B. (2018). IDF Diabetes atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Research and Clinical Practice, 138, 271–281. https://doi.org/ 10.1016/j.diabres.2018.02.023
<br>Clark, J. B., Palmer, C. J. & Shaw, W. N. (1983). The diabetic Zucker fatty rat. Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine, 173(1), 68–75. https://doi.org/10.3181/00379727-173-41611
<br>Deckert, T. & Poulsen, J. E. (1981). Diabetic nephropathy: fault or destiny? Diabetologia, 21(3), 178–183. https://doi.org/10.1007/BF00252651
<br>Dupak, R., Kalafova, A., Schneidgenova, M., Ivanisova, E., Brindza, J. & Capcarova, M. (2020). Antioxidant activity and hypoglycaemic effect of cornelian cherry stone in diabetic rats. Lucrări ştiinţifice. Zootehnie şi Biotehnologii, 53(6), 164–167.
<br>Dupak, R., Jaszcza, K., Kalafova, A., Schneidgenova, M., Ivanisova, E., Tokarova, K., Brindza, J. & Capcarova, M. (2020). Characterization of compounds in Cornelian cherry (Cornus mas L.) and its effect on interior milieu in ZDF. Emirates Journal of Food and Agriculture, 32(5), 368–375. https://doi.org/10.9755/ejfa.2020.v32.i5.2106
<br>Ehses, J. A., Lacraz, G., Giroix, M., Schmidlin, F., Coulaud, J., Kassis, N., Minger, J. C., Kergoat, M., Portha, B., Homo-Delarche, F. & Donath, M. Y. (2009). IL-1 antagonism reduces hyperglycemia and tissiu inflammation in the type 2 diabetic GK rat. Proceedings of the National Academy of Sciences of the United States of America, 106(33), 13998–14003. https://doi.org/10.1073/pnas.0810087106
<br>Fisher, S. J., Shi, Z. Q., Lickley, H. L., Efendic, S., Vranic, M. & Giacca, A. (2001). Low-dose IGF-I has no selective advantage over insulin in regulating glucose metabolism in hyperglycemic depancreatized dogs. The Journal of Endocrinology, 168(1), 49–58. https://doi.org/10.1677/joe.0.1680049
<br>Gault, V. A., Kerr, B. D., Harriott, P. & Flatt, P. R. (2011). Administration of an acylated GLP-1 and GIP preparation provides added beneficial glucose-lowering and insulinotropic actions over single incretins in mice with type 2 diabetes and obesity. Clinical Science, 121(3), 107–117. https://doi.org/10.1042/CS20110006
<br>Giroix, M. H., Irminger, J. C., Lacraz, G., Noll, C., Calderari, S., Ehses, J. A., Coulaud, J., Cornut, M., Kassis, N., Schmidlin, F., Paul, J. L., Kergoat, M., Janel, N., Halban, P. A. & Delarche, F. H. (2011). Hypercholesterolaemia, signs of islet microangiopathy and altered angiogenesis precede onset of type 2 diabetes in the Goto-Kakizaki (GK) rat. Diabetologia, 54(9), 2451–2462. https://doi.org/10.1007/s00125-011-2223-4
<br>Goto, Y., Kakizaki, M. & Masaki, N. (1976). Production of spontaneous diabetic rats by repetition of selective breeding. The Tohoku Journal of Experimental Medicine, 119(1), 85–90. https://doi.org/10.1620/tjem.119.85
<br>Guberski, D. L., Thomas, V. A., Shek, W. R., Like, A. A., Handler, E. S., Rossini, A. A., Wallace, J. E. & Welsh, R. M. (1991). Induction of type I diabetes by Kilham's rat virus in diabetes-resistant BB/Wor rats. Science, 254(5034), 1010–1013. https://doi.org/10.1126/science.1658938
<br>Han, J., Liu, Q. Y. (2010). Reduction of islet pyruvate carboxylase activity might be related to the development of type 2 diabetes mellitus in Agouti-K mice. The Journal of Endocrinology, 204(2), 143–152. https://doi.org/10.1677/JOE-09-0391
<br>Hasan, M. M., Ahmed, Q. U., Soad, S. Z. M. & Tunna, T. S. (2018). Animal models and natural products to investigate in vivo and in vitro antidiabetic activity. Biomedicine & Pharmacotherapy, 101, 833–841. https://doi.org/10.1016/j.biopha.2018.02.137
<br>He, S., Chen, Y., Wei, L., Jin, X., Zeng, L., Ren, Y., Zhang, J., Wang, L., Li, H., Lu, Y. & Cheng, J. (2011). Treatment and risk factor analysis of hypoglycemia in diabetic rhesus monkeys. Experimental Biology and Medicine, 236(2), 212–218. https://doi.org/10.1258/ebm.2010.010208
<br>Herrath, M., Filippi, C. & Coppieters, K. (2011). How viral infections enhance or prevent type 1 diabetes-from mouse to man. Journal of Medical Virology, 83(9), 1672. https://doi.org/10.1002/jmv.22063
<br>Hemmes, R. B. & Schoch, R. (1988). High dosage testosterone propionate induces copulatory behavior in the obese male Zucker rat. Physiology & Behavior, 43(3), 321–324. https://doi.org/10.1016/0031-9384(88)90195-3
<br>Heydemann, A. (2016). An overview of murine high fat diet as a model for type 2 diabetes mellitus. Journal of Diabetes Research, 2016, 1–14. https://doi.org/10.1155/2016/2902351
<br>Homo-Delarche F., Calderari, S., Irminger, J. C., Gangnerau, M. N., Coulaud, J., Rickenbach, K., Dolz, M., Halban, P., Portha, B. & Serradas, P. (2006). Islet inflammation and fibrosis in a spontaneous model of type 2 diabetes, the GK rat. Diabetes, 55(6), 1625–1633.
<br>Hummel, K. P., Dickie, M. M. & Coleman, D. L. (1966). Diabetes, a new mutation in the mouse. Science, 153(3740), 1127–1128. https://doi.org/10.1126/science.153.3740.1127
<br>Kim, Y., Keogh, J. B. & Clifton, P. M. (2017). Benefits of nut consumption on insulin resistance and cardiovascular risk factors: multiple potential mechanisms of actions.Nutrients, 9(11), 1271. https://doi.org/10.3390/nu9111271
<br>Jaidane, H., Sane, F., Gharbi, J., Aouni, M., Romond, M. B. & Hober, D. (2009). Coxsackievirus B4 and type 1 diabetes pathogenesis: contribution of animal models. Diabetes/Metabolism Research and Reviews, 25(7), 591–603. https://doi.org/10.1002/dmrr.995
<br>Jederstrom, G., Grasjo, J., Nordin, A., Sjoholm, I. & Andersson, A. (2005). Blood glucose-lowering activity of a hyaluronan-insulin complex after oral administration to rats with diabetes. Diabetes Technology & Therapeutics, 7(6), 948–957. https://doi.org/10.1089/dia.2005.7.948
<br>Jun, H. S. & Yoon, J. W. (2003). A new look at viruses in type 1 diabetes. Diabetes/Metabolism Research and Reviews, 19(1), 8–31. https://doi.org/10.1002/dmrr.337
<br>Kahn, S. E., Cooper, M. E & Del Prato, S. (2014). Pathophysiology and treatment of type 2 diabetes: perspectives on the past, present, and future. Lancet, 383, 1068–1083. https://doi.org/ 10.1016/S0140-6736(13)62154-6
<br>Kawano, K., Mori, S., Hirashima, T., Man, Z. W. & Natori, T. (1999). Examination of the pathogenesis of diabetic nephropathy in OLETF rats. The Journal of Veterinary Medical Science, 61(11), 1219–1228. https://doi.org/10.1292/jvms.61.1219
<br>King, A. J. F. (2012). The use of animal models in diabetes research. British Journal of Pharmacology, 166(3), 877–894. https://doi.org/10.1111/j.1476-5381.2012.01911.x
<br>Kleinert, M., Clemmensen, C., Hofmann, S. M., Moore, M. C., Renner, S., Woods, S. C., Huypens, P., Beckers, J., Angelis, M. H., Schurmann, A., Bakhti, M., Klingenspor, M., Heiman, M., Cherrington, A. D., Ristow, M., Lickert, H., Wolf, E., Havel, P. J., Muller, T. D. & Tschop, M. H. (2018). Animal models of obesity and diabetes mellitus. Nature Reviews Endocrinology, 14(3), 140–162. https://doi.org/10.1038/nrendo.2017.161
<br>Lee, J. H., Yang, S. H., Jung, M. O. & Lee, M. G. (2010). Pharmacokinetics of drugs in rats with diabetes mellitus induced by alloxan or streptozocin: comparison with those in patients with type I diabetes mellitus. The Journal of Pharmacy and Pharmacology, 62(1), 1–23. https://doi.org/10.1211/jpp.62.01.0001
<br>Lenzen, S., Tiedge, M., Elsner, M., Lortz, S., Weiss, H., Jorns, A., Kloppel, G., Wedekind, D., Prokop, C. M. & Hedrich, H. J. (2001). The LEW.1AR1/ZTm-iddm rat: a new model of spontaneous insulin-dependent diabetes mellitus. Diabetologia, 44(9), 1189–1196. https://doi.org/10.1007/s001250100625
<br>Lenzen, S. (2008). The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia, 51, 216–226. https://doi.org/10.1007/s00125-007-0886-7
<br>Lindstrom, P. (2007). The physiology of obese-hyperglycemic mice (ob/ob mice). The Scientific World Journal, 7, 666–685. https://doi.org/10.1100/tsw.2007.117
<br>Matsumoto, S. (2011). Autologous islet cell transplantation to prevent surgical diabetes. Journal of Diabetes, 3(4), 328–336. https://doi.org/10.1111/j.1753-0407.2011.00128.x
<br>Mellert, J., Hering, B. J., Liu, X., Brandhorst, D., Brandhorst, H., Brendel, M., Ernst, E., Gramberg, D., Bretzel, R. G. & Hopt, U. T. (1998). Transplantation, 66(2), 200–204. https://doi.org/10.1097/00007890-199807270-00010
<br>Millo, M. G. (2002). Adipose tissue hormones. Journal of Endocrinological Investigation, 25(10), 855–861. https://doi.org/10.1007/BF03344048
<br>Müller, G. (2016). Methods to induce experimental diabetes mellitus. Drug Discovery and Evaluation: Pharmacological Assays, 2569–2581. https://doi.org/10.1007/978-3-319-05392-9_63
<br>Okada, S., Saito, M., Kinoshita, Y., Satoh, I., Kawaba, Y., Hayashi, A., Oite, T., Satoh, K. & Kanzaki, S. (2010). Effects of cyclohexenonic long-chain fatty alcohol in type 2 diabetic rat nephropathy. Biomedical Research, 31(4), 219–230. https://doi.org/10.2220/biomedres.31.219
<br>Ostenson, C. G. & Efendic, S. (2007). Islet gene expression and function in type 2 diabetes; studies in the Goto-Kakizaki rat and humans. Diabetes, Obesity & Metabolism, 9(2), 180–186. https://doi.org/10.1111/j.1463-1326.2007.00787.x
<br>Panchal, S. K. & Brown, L. (2011). Rodent models for metabolic syndrome research. Journal of Biomedicine and Biotechnology, 2011(4), 1–14. https://doi.org/10.1155/2011/351982
<br>Pick, A., Clark J., Kubstrup, C., Levisetti, M., Pugh, W., Weir, S. B. & Polonsky, K. S. (1998). Role of apoptosis in failure of beta-cell mass compensation for insulin resistance and beta-cell defects in the male Zucker diabetic fatty rat. Diabetes, 47(3), 358–364. https://doi.org/ 10.2337/diabetes.47.3.358
<br>Pivari, F., Mingione, A., Brasacchio, C. & Soldati, L. (2019). Curcumin and type 2 diabetes mellitus: prevention and treatment. Nutrients, 11(8), 1837. https://doi.org/10.3390/nu11081837
<br>Pociot, F. & McDermott, M. F. (2002). Genetics of type 1 diabetes mellitus. Genes & Immununity, 3, 235–249. https://doi.org/10.1038/sj.gene.6363875
<br>Portha, B. (2005). Programmed disorders of beta-cell development and function as one cause for type 2 diabetes? The GK rat paradigm. Diabetes/Metabolism Research and Reviews, 21(6), 495–504. https://doi.org/10.1002/dmrr.566
<br>Pravenec, M. (2010). Use of rat genomics for investigating the metabolic syndrome. Methods in Molecular Biology, 597, 415–426. https:/doi.org/10.1007/978-1-60327-389-3_28
<br>Ro, S., Park, C., Jin, J., Zheng, H., Blair, P. J., Redelman, D., Ward, S. M., Yan, W. & Sanders, K. M. (2010). A model to study the phenotypic changes of interstitial cells of Cajal in gastrointestinal diseases. Gastroenterology, 138(3), 1068–1078. https:// 10.1053/j.gastro.2009.11.007
<br>Shibata, T., Takeuchi, S., Yokota, S., Kakimoto, K., Yonemori, F. & Wakitani, K. (2000). Effects of peroxisome proliferator-activated receptor-alpha and -gamma agonist, JTT-501, on diabetic complications in Zucker diabetic fatty rats. British Journal of Pharmacology, 130(3), 495–504. https://doi.org/10.1038/sj.bjp.0703328
<br>Shimada, A. & Maruyama, T. (2004). Encephalomyocarditis-virus-induced diabetes model resembles "fulminant" type 1 diabetes in humans. Diabetologia, 47(10), 1854–1855. https://doi.org/10.1007/s00125-004-1538-9
<br>Srinivasan, K. & Ramarao, P. (2007). Animal models in type 2 diabetes research: an overview. The Indian Journal of Medical Research, 125(3), 451–472.
<br>Suleiman, J. B., Mohamed, M. & Bakar, A. B. A. (2020). A systematic review on different models of inducing obesity in animals: Advantages and limitations. Journal of Advanced Veterinary and Animal Research, 7(1), 103–114. http://doi.org/10.5455/javar.2020.g399
<br>Surwit, R. S., Feinglos, M. N., Rodin, J., Sutherland, A., Petro, A. E., Opara, E. C., Kuhn, C. M. & Scrive, M. R. (1995). Differential effects of fat and sucrose on the development of obesity and diabetes in C57BL/6J and A/J mice. Metabolism, 44(5), 645–651. https://doi.org/ 10.1016/0026-0495(95)90123-x
<br>Toumilehto, J., Johnsen, K. B., Molarius, A., Forsén, T., Rastenyte, D., Sarti, C. & Reunanen, A. (1998). Incidence of cardiocascular disease in type 1 (insulin-dependent) diabetic subjects with and without diabetic nephropathy in Finland. Diabetologia, 41(7), 784–790. https://doi.org/10.1007/s001250050988
<br>Udler, M. S., Kim, J., Grotthuss, M., Guarch, S. B., Cole, J. B., Chiou, J., Anderson, C. D., Boehnke, M., Laakso, M., Atzmon, G., Glaser, B., Mercader, J. M., Gaulton, K., Flannick, J., Getz, G. & Florez, J. C. (2018). Type 2 diabetes genetic loci informed by multi-trait associations point to disease mechanisms and subtypes: a soft clustering analysis. PLoS Medicine, 15(9). e1002654. https://doi.org/10.1371/journal.pmed.1002654
<br>Vedtofte, L., Bodvarsdottir, T. B., Gotfredsen, C. F., Karlsen, A. E., Knudsen, L. B & Heller, R. S. (2010). Liraglutide, but not vildagliptin, restores normoglycaemia and insulin content in the animal model of type 2 diabetes, Psammomy obesus. Regulatory Peptides, 160 (1), 106–114. https://doi.org/10.1016/j.regpep.2009.12.005
<br>Wang, Y. J., Fu, G. S., Chen, F. M. & Wang, H. (2009). The effect of valsartan and fluvastatin on the connective tissue growth factor expression in experimental diabetic cardiomyopathy. Zhonghua Nei Ke Za Zhi, 48(8), 660-665.
<br>Weir, S. B., Trent, D. F. & Weir, G. C. (1983). Partial pancreatectomy in the rat and subsequent defect in glucose-induced insulin release. The Journal of Clinical Investigation, 71(6), 1544–1553.
<br>Werf, N., Kroese, F. G. M., Rozing, J. & Hillebrands, J. L. (2007). Viral infections as potential triggers of type 1 diabetes. Diabetes/Metabolism Research and Reviews, 23(3), 169–183. https://doi.org/10.1002/dmrr.695
<br>Winzell, M. S. & Ahren, B. (2004). The high-fat diet-fed mouse: a model for studying mechanisms and treatment of impaired glucose tolerance and type 2 diabetes. Diabetes, 53(3), 215–219. https://doi.org/10.2337/diabetes.53.suppl_3.s215
<br>Xu, L., Li, Y., Dai, Y. & Peng, J. (2018). Natural products for the treatment of type 2 diabetes mellitus: pharmacology and mechanisms. Pharmacological Research, 130, 451–465. https://doi.org/10.1016/j.phrs.2018.01.015
<br>Yadav, A., Jyoti, P., Jain, S. K. & Bhattacharjee, J. (2011). Correlation of adiponectin and leptin with insulin resistance: a pilot study in healthy north Indian population. Indian Journal of Clinical Biochemistry, 26(2), 193–196. https://doi.org/10.1007/s12291-011-0119-1
<br>Yang, Y. & Santamaria, P. (2006). Lessons on autoimmune diabetes from animal models. Clinical Science, 110(6), 627–639. https://doi.org/10.1042/CS20050330
<br>Yasuda, K., Nishikawa, W., Iwanaka, N., Nakamura, E., Seino, Y., Tsuda, K. & Ishihara, A. (2002). Abnormality in fibre type distribution of soleus and plantaris muscles in non-obese diabetic Goto-Kakizaki rats. Clinical and Experimental Pharmacology & Physiology, 29(11), 1001–1008. https://doi.org/10.1046/j.1440-1681.2002.03757.x
<br>Yoshioka, M., Kayo, T., Ikeda, T. & Koizuni, A. A. (1997). Novel locus, Mody4, Distal to D7Mit189 on chromosome 7 determines early-onset NIDDM in nonobese C57BL/6(Akita) mutant mice. Diabetes, 46(5), 887–894. https://doi.org/10.2337/diab.46.5.887
<br>Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L. & Friedman, J. M. (1994). Positional cloning of the mouse obese gene and its human homologue. Nature, 372(6505), 425–432. https://doi.org/10.1038/372425a0</div>
<br>American Diabetes Association (2018). Classification and diagnosis of diabetes: standards of medical care in diabetes. Diabetes Care, 41, 13–27.
<br>American Diabetes Association (2015). Classification and diagnosis of diabetes. Diabetes Care, 38, 8–16.
<br>Artasensi, A., Pedretti, A., Vistoli, G. & Fumagalli, L. (2020). Type 2 diabetes mellitus: a review of multi-target drugs. Molecules, 25(8), 1987–2007. https://doi.org/ 10.3390/molecules25081987
<br>Atkinson, M. A. & Leiter, E. H. (1999). The NOD mouse model of type 1 diabetes: as good as it gets? Nature Medicine, 5(6), 601–604. https://doi.org/10.1038/9442
<br>Baribault, H. (2016). Mouse models of type 2 diabetes mellitus in drug discovery. Methods in Molecular Biology, 1438, 153–175. https://doi.org/10.1007/978-1-4939-3661-8_10
<br>Bnouham, M., Ziyyat, A., Mekhfi, H., Tahri A. & Legssyer, A. (2006). Medicinal plants with potential antidiabetic activity – a review of ten years of herbal medicine research (1990-2000). International Journal of Diabetes and Metabolism, 14(1), 1–25. https://doi.org/10.1159/000497588
<br>Boden, G. (2003). Effects of free fatty acids (FFA) on glucose metabolism: significance for insulin resistance and type 2 diabetes. Experimental and Clinical Endocrinology & Diabetes, 111(3), 121–124. https://doi.org/10.1055/s-2003-39781
<br>Capcarova, M., Kalafova, A., Schwarzova, M., Schneidgenova, M., Prnova, M. S., Slovak, L., Kovacik, A., Lory, V. & Zorad, S. (2019). Cornelian cherry fruit improves glycaemia and manifestations of diabetes in obese zucker diabetic fatty rats. Research of Veterinary Science, 126, 118–123. https://doi.org/10.1016/j.rvsc.2019.08.024
<br>Chatzigeorgiou, A., Halapas, A., Kalafatakis, K. & Kamper, E. (2009). Animal Models of Diabetes: a Synopsis. In Vivo, 23, 245–258.
<br>Chehab, F. F., Lim, M. E. & Lu, R. (1996). Correction of the sterility defect in homozygous obese female mice by treatment with the human recombinant leptin. Nature Genetics, 12(3), 318–320. https://doi.org/10.1038/ng0396-318
<br>Cho, N. H., Shaw, J. E., Karunga, S., Huang, Y., Fernandes, J. D. R., Ohlrogge, A. W. & Malanda, B. (2018). IDF Diabetes atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Research and Clinical Practice, 138, 271–281. https://doi.org/ 10.1016/j.diabres.2018.02.023
<br>Clark, J. B., Palmer, C. J. & Shaw, W. N. (1983). The diabetic Zucker fatty rat. Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine, 173(1), 68–75. https://doi.org/10.3181/00379727-173-41611
<br>Deckert, T. & Poulsen, J. E. (1981). Diabetic nephropathy: fault or destiny? Diabetologia, 21(3), 178–183. https://doi.org/10.1007/BF00252651
<br>Dupak, R., Kalafova, A., Schneidgenova, M., Ivanisova, E., Brindza, J. & Capcarova, M. (2020). Antioxidant activity and hypoglycaemic effect of cornelian cherry stone in diabetic rats. Lucrări ştiinţifice. Zootehnie şi Biotehnologii, 53(6), 164–167.
<br>Dupak, R., Jaszcza, K., Kalafova, A., Schneidgenova, M., Ivanisova, E., Tokarova, K., Brindza, J. & Capcarova, M. (2020). Characterization of compounds in Cornelian cherry (Cornus mas L.) and its effect on interior milieu in ZDF. Emirates Journal of Food and Agriculture, 32(5), 368–375. https://doi.org/10.9755/ejfa.2020.v32.i5.2106
<br>Ehses, J. A., Lacraz, G., Giroix, M., Schmidlin, F., Coulaud, J., Kassis, N., Minger, J. C., Kergoat, M., Portha, B., Homo-Delarche, F. & Donath, M. Y. (2009). IL-1 antagonism reduces hyperglycemia and tissiu inflammation in the type 2 diabetic GK rat. Proceedings of the National Academy of Sciences of the United States of America, 106(33), 13998–14003. https://doi.org/10.1073/pnas.0810087106
<br>Fisher, S. J., Shi, Z. Q., Lickley, H. L., Efendic, S., Vranic, M. & Giacca, A. (2001). Low-dose IGF-I has no selective advantage over insulin in regulating glucose metabolism in hyperglycemic depancreatized dogs. The Journal of Endocrinology, 168(1), 49–58. https://doi.org/10.1677/joe.0.1680049
<br>Gault, V. A., Kerr, B. D., Harriott, P. & Flatt, P. R. (2011). Administration of an acylated GLP-1 and GIP preparation provides added beneficial glucose-lowering and insulinotropic actions over single incretins in mice with type 2 diabetes and obesity. Clinical Science, 121(3), 107–117. https://doi.org/10.1042/CS20110006
<br>Giroix, M. H., Irminger, J. C., Lacraz, G., Noll, C., Calderari, S., Ehses, J. A., Coulaud, J., Cornut, M., Kassis, N., Schmidlin, F., Paul, J. L., Kergoat, M., Janel, N., Halban, P. A. & Delarche, F. H. (2011). Hypercholesterolaemia, signs of islet microangiopathy and altered angiogenesis precede onset of type 2 diabetes in the Goto-Kakizaki (GK) rat. Diabetologia, 54(9), 2451–2462. https://doi.org/10.1007/s00125-011-2223-4
<br>Goto, Y., Kakizaki, M. & Masaki, N. (1976). Production of spontaneous diabetic rats by repetition of selective breeding. The Tohoku Journal of Experimental Medicine, 119(1), 85–90. https://doi.org/10.1620/tjem.119.85
<br>Guberski, D. L., Thomas, V. A., Shek, W. R., Like, A. A., Handler, E. S., Rossini, A. A., Wallace, J. E. & Welsh, R. M. (1991). Induction of type I diabetes by Kilham's rat virus in diabetes-resistant BB/Wor rats. Science, 254(5034), 1010–1013. https://doi.org/10.1126/science.1658938
<br>Han, J., Liu, Q. Y. (2010). Reduction of islet pyruvate carboxylase activity might be related to the development of type 2 diabetes mellitus in Agouti-K mice. The Journal of Endocrinology, 204(2), 143–152. https://doi.org/10.1677/JOE-09-0391
<br>Hasan, M. M., Ahmed, Q. U., Soad, S. Z. M. & Tunna, T. S. (2018). Animal models and natural products to investigate in vivo and in vitro antidiabetic activity. Biomedicine & Pharmacotherapy, 101, 833–841. https://doi.org/10.1016/j.biopha.2018.02.137
<br>He, S., Chen, Y., Wei, L., Jin, X., Zeng, L., Ren, Y., Zhang, J., Wang, L., Li, H., Lu, Y. & Cheng, J. (2011). Treatment and risk factor analysis of hypoglycemia in diabetic rhesus monkeys. Experimental Biology and Medicine, 236(2), 212–218. https://doi.org/10.1258/ebm.2010.010208
<br>Herrath, M., Filippi, C. & Coppieters, K. (2011). How viral infections enhance or prevent type 1 diabetes-from mouse to man. Journal of Medical Virology, 83(9), 1672. https://doi.org/10.1002/jmv.22063
<br>Hemmes, R. B. & Schoch, R. (1988). High dosage testosterone propionate induces copulatory behavior in the obese male Zucker rat. Physiology & Behavior, 43(3), 321–324. https://doi.org/10.1016/0031-9384(88)90195-3
<br>Heydemann, A. (2016). An overview of murine high fat diet as a model for type 2 diabetes mellitus. Journal of Diabetes Research, 2016, 1–14. https://doi.org/10.1155/2016/2902351
<br>Homo-Delarche F., Calderari, S., Irminger, J. C., Gangnerau, M. N., Coulaud, J., Rickenbach, K., Dolz, M., Halban, P., Portha, B. & Serradas, P. (2006). Islet inflammation and fibrosis in a spontaneous model of type 2 diabetes, the GK rat. Diabetes, 55(6), 1625–1633.
<br>Hummel, K. P., Dickie, M. M. & Coleman, D. L. (1966). Diabetes, a new mutation in the mouse. Science, 153(3740), 1127–1128. https://doi.org/10.1126/science.153.3740.1127
<br>Kim, Y., Keogh, J. B. & Clifton, P. M. (2017). Benefits of nut consumption on insulin resistance and cardiovascular risk factors: multiple potential mechanisms of actions.Nutrients, 9(11), 1271. https://doi.org/10.3390/nu9111271
<br>Jaidane, H., Sane, F., Gharbi, J., Aouni, M., Romond, M. B. & Hober, D. (2009). Coxsackievirus B4 and type 1 diabetes pathogenesis: contribution of animal models. Diabetes/Metabolism Research and Reviews, 25(7), 591–603. https://doi.org/10.1002/dmrr.995
<br>Jederstrom, G., Grasjo, J., Nordin, A., Sjoholm, I. & Andersson, A. (2005). Blood glucose-lowering activity of a hyaluronan-insulin complex after oral administration to rats with diabetes. Diabetes Technology & Therapeutics, 7(6), 948–957. https://doi.org/10.1089/dia.2005.7.948
<br>Jun, H. S. & Yoon, J. W. (2003). A new look at viruses in type 1 diabetes. Diabetes/Metabolism Research and Reviews, 19(1), 8–31. https://doi.org/10.1002/dmrr.337
<br>Kahn, S. E., Cooper, M. E & Del Prato, S. (2014). Pathophysiology and treatment of type 2 diabetes: perspectives on the past, present, and future. Lancet, 383, 1068–1083. https://doi.org/ 10.1016/S0140-6736(13)62154-6
<br>Kawano, K., Mori, S., Hirashima, T., Man, Z. W. & Natori, T. (1999). Examination of the pathogenesis of diabetic nephropathy in OLETF rats. The Journal of Veterinary Medical Science, 61(11), 1219–1228. https://doi.org/10.1292/jvms.61.1219
<br>King, A. J. F. (2012). The use of animal models in diabetes research. British Journal of Pharmacology, 166(3), 877–894. https://doi.org/10.1111/j.1476-5381.2012.01911.x
<br>Kleinert, M., Clemmensen, C., Hofmann, S. M., Moore, M. C., Renner, S., Woods, S. C., Huypens, P., Beckers, J., Angelis, M. H., Schurmann, A., Bakhti, M., Klingenspor, M., Heiman, M., Cherrington, A. D., Ristow, M., Lickert, H., Wolf, E., Havel, P. J., Muller, T. D. & Tschop, M. H. (2018). Animal models of obesity and diabetes mellitus. Nature Reviews Endocrinology, 14(3), 140–162. https://doi.org/10.1038/nrendo.2017.161
<br>Lee, J. H., Yang, S. H., Jung, M. O. & Lee, M. G. (2010). Pharmacokinetics of drugs in rats with diabetes mellitus induced by alloxan or streptozocin: comparison with those in patients with type I diabetes mellitus. The Journal of Pharmacy and Pharmacology, 62(1), 1–23. https://doi.org/10.1211/jpp.62.01.0001
<br>Lenzen, S., Tiedge, M., Elsner, M., Lortz, S., Weiss, H., Jorns, A., Kloppel, G., Wedekind, D., Prokop, C. M. & Hedrich, H. J. (2001). The LEW.1AR1/ZTm-iddm rat: a new model of spontaneous insulin-dependent diabetes mellitus. Diabetologia, 44(9), 1189–1196. https://doi.org/10.1007/s001250100625
<br>Lenzen, S. (2008). The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia, 51, 216–226. https://doi.org/10.1007/s00125-007-0886-7
<br>Lindstrom, P. (2007). The physiology of obese-hyperglycemic mice (ob/ob mice). The Scientific World Journal, 7, 666–685. https://doi.org/10.1100/tsw.2007.117
<br>Matsumoto, S. (2011). Autologous islet cell transplantation to prevent surgical diabetes. Journal of Diabetes, 3(4), 328–336. https://doi.org/10.1111/j.1753-0407.2011.00128.x
<br>Mellert, J., Hering, B. J., Liu, X., Brandhorst, D., Brandhorst, H., Brendel, M., Ernst, E., Gramberg, D., Bretzel, R. G. & Hopt, U. T. (1998). Transplantation, 66(2), 200–204. https://doi.org/10.1097/00007890-199807270-00010
<br>Millo, M. G. (2002). Adipose tissue hormones. Journal of Endocrinological Investigation, 25(10), 855–861. https://doi.org/10.1007/BF03344048
<br>Müller, G. (2016). Methods to induce experimental diabetes mellitus. Drug Discovery and Evaluation: Pharmacological Assays, 2569–2581. https://doi.org/10.1007/978-3-319-05392-9_63
<br>Okada, S., Saito, M., Kinoshita, Y., Satoh, I., Kawaba, Y., Hayashi, A., Oite, T., Satoh, K. & Kanzaki, S. (2010). Effects of cyclohexenonic long-chain fatty alcohol in type 2 diabetic rat nephropathy. Biomedical Research, 31(4), 219–230. https://doi.org/10.2220/biomedres.31.219
<br>Ostenson, C. G. & Efendic, S. (2007). Islet gene expression and function in type 2 diabetes; studies in the Goto-Kakizaki rat and humans. Diabetes, Obesity & Metabolism, 9(2), 180–186. https://doi.org/10.1111/j.1463-1326.2007.00787.x
<br>Panchal, S. K. & Brown, L. (2011). Rodent models for metabolic syndrome research. Journal of Biomedicine and Biotechnology, 2011(4), 1–14. https://doi.org/10.1155/2011/351982
<br>Pick, A., Clark J., Kubstrup, C., Levisetti, M., Pugh, W., Weir, S. B. & Polonsky, K. S. (1998). Role of apoptosis in failure of beta-cell mass compensation for insulin resistance and beta-cell defects in the male Zucker diabetic fatty rat. Diabetes, 47(3), 358–364. https://doi.org/ 10.2337/diabetes.47.3.358
<br>Pivari, F., Mingione, A., Brasacchio, C. & Soldati, L. (2019). Curcumin and type 2 diabetes mellitus: prevention and treatment. Nutrients, 11(8), 1837. https://doi.org/10.3390/nu11081837
<br>Pociot, F. & McDermott, M. F. (2002). Genetics of type 1 diabetes mellitus. Genes & Immununity, 3, 235–249. https://doi.org/10.1038/sj.gene.6363875
<br>Portha, B. (2005). Programmed disorders of beta-cell development and function as one cause for type 2 diabetes? The GK rat paradigm. Diabetes/Metabolism Research and Reviews, 21(6), 495–504. https://doi.org/10.1002/dmrr.566
<br>Pravenec, M. (2010). Use of rat genomics for investigating the metabolic syndrome. Methods in Molecular Biology, 597, 415–426. https:/doi.org/10.1007/978-1-60327-389-3_28
<br>Ro, S., Park, C., Jin, J., Zheng, H., Blair, P. J., Redelman, D., Ward, S. M., Yan, W. & Sanders, K. M. (2010). A model to study the phenotypic changes of interstitial cells of Cajal in gastrointestinal diseases. Gastroenterology, 138(3), 1068–1078. https:// 10.1053/j.gastro.2009.11.007
<br>Shibata, T., Takeuchi, S., Yokota, S., Kakimoto, K., Yonemori, F. & Wakitani, K. (2000). Effects of peroxisome proliferator-activated receptor-alpha and -gamma agonist, JTT-501, on diabetic complications in Zucker diabetic fatty rats. British Journal of Pharmacology, 130(3), 495–504. https://doi.org/10.1038/sj.bjp.0703328
<br>Shimada, A. & Maruyama, T. (2004). Encephalomyocarditis-virus-induced diabetes model resembles "fulminant" type 1 diabetes in humans. Diabetologia, 47(10), 1854–1855. https://doi.org/10.1007/s00125-004-1538-9
<br>Srinivasan, K. & Ramarao, P. (2007). Animal models in type 2 diabetes research: an overview. The Indian Journal of Medical Research, 125(3), 451–472.
<br>Suleiman, J. B., Mohamed, M. & Bakar, A. B. A. (2020). A systematic review on different models of inducing obesity in animals: Advantages and limitations. Journal of Advanced Veterinary and Animal Research, 7(1), 103–114. http://doi.org/10.5455/javar.2020.g399
<br>Surwit, R. S., Feinglos, M. N., Rodin, J., Sutherland, A., Petro, A. E., Opara, E. C., Kuhn, C. M. & Scrive, M. R. (1995). Differential effects of fat and sucrose on the development of obesity and diabetes in C57BL/6J and A/J mice. Metabolism, 44(5), 645–651. https://doi.org/ 10.1016/0026-0495(95)90123-x
<br>Toumilehto, J., Johnsen, K. B., Molarius, A., Forsén, T., Rastenyte, D., Sarti, C. & Reunanen, A. (1998). Incidence of cardiocascular disease in type 1 (insulin-dependent) diabetic subjects with and without diabetic nephropathy in Finland. Diabetologia, 41(7), 784–790. https://doi.org/10.1007/s001250050988
<br>Udler, M. S., Kim, J., Grotthuss, M., Guarch, S. B., Cole, J. B., Chiou, J., Anderson, C. D., Boehnke, M., Laakso, M., Atzmon, G., Glaser, B., Mercader, J. M., Gaulton, K., Flannick, J., Getz, G. & Florez, J. C. (2018). Type 2 diabetes genetic loci informed by multi-trait associations point to disease mechanisms and subtypes: a soft clustering analysis. PLoS Medicine, 15(9). e1002654. https://doi.org/10.1371/journal.pmed.1002654
<br>Vedtofte, L., Bodvarsdottir, T. B., Gotfredsen, C. F., Karlsen, A. E., Knudsen, L. B & Heller, R. S. (2010). Liraglutide, but not vildagliptin, restores normoglycaemia and insulin content in the animal model of type 2 diabetes, Psammomy obesus. Regulatory Peptides, 160 (1), 106–114. https://doi.org/10.1016/j.regpep.2009.12.005
<br>Wang, Y. J., Fu, G. S., Chen, F. M. & Wang, H. (2009). The effect of valsartan and fluvastatin on the connective tissue growth factor expression in experimental diabetic cardiomyopathy. Zhonghua Nei Ke Za Zhi, 48(8), 660-665.
<br>Weir, S. B., Trent, D. F. & Weir, G. C. (1983). Partial pancreatectomy in the rat and subsequent defect in glucose-induced insulin release. The Journal of Clinical Investigation, 71(6), 1544–1553.
<br>Werf, N., Kroese, F. G. M., Rozing, J. & Hillebrands, J. L. (2007). Viral infections as potential triggers of type 1 diabetes. Diabetes/Metabolism Research and Reviews, 23(3), 169–183. https://doi.org/10.1002/dmrr.695
<br>Winzell, M. S. & Ahren, B. (2004). The high-fat diet-fed mouse: a model for studying mechanisms and treatment of impaired glucose tolerance and type 2 diabetes. Diabetes, 53(3), 215–219. https://doi.org/10.2337/diabetes.53.suppl_3.s215
<br>Xu, L., Li, Y., Dai, Y. & Peng, J. (2018). Natural products for the treatment of type 2 diabetes mellitus: pharmacology and mechanisms. Pharmacological Research, 130, 451–465. https://doi.org/10.1016/j.phrs.2018.01.015
<br>Yadav, A., Jyoti, P., Jain, S. K. & Bhattacharjee, J. (2011). Correlation of adiponectin and leptin with insulin resistance: a pilot study in healthy north Indian population. Indian Journal of Clinical Biochemistry, 26(2), 193–196. https://doi.org/10.1007/s12291-011-0119-1
<br>Yang, Y. & Santamaria, P. (2006). Lessons on autoimmune diabetes from animal models. Clinical Science, 110(6), 627–639. https://doi.org/10.1042/CS20050330
<br>Yasuda, K., Nishikawa, W., Iwanaka, N., Nakamura, E., Seino, Y., Tsuda, K. & Ishihara, A. (2002). Abnormality in fibre type distribution of soleus and plantaris muscles in non-obese diabetic Goto-Kakizaki rats. Clinical and Experimental Pharmacology & Physiology, 29(11), 1001–1008. https://doi.org/10.1046/j.1440-1681.2002.03757.x
<br>Yoshioka, M., Kayo, T., Ikeda, T. & Koizuni, A. A. (1997). Novel locus, Mody4, Distal to D7Mit189 on chromosome 7 determines early-onset NIDDM in nonobese C57BL/6(Akita) mutant mice. Diabetes, 46(5), 887–894. https://doi.org/10.2337/diab.46.5.887
<br>Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L. & Friedman, J. M. (1994). Positional cloning of the mouse obese gene and its human homologue. Nature, 372(6505), 425–432. https://doi.org/10.1038/372425a0</div>
