EVALUATION OF ANIMAL MODELS BY COMPARISON WITH HUMAN DIABETES MELLITUS: A REVIEW

Main Article Content

Rudolf DUPAK
Marcela CAPCAROVA

Abstract

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.

Keywords
  • diabetes
  • human
  • animal model
  • diet
  • Article Details

    Section
    Reviews

    References

    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

    American Diabetes Association (2018). Classification and diagnosis of diabetes: standards of medical care in diabetes. Diabetes Care, 41, 13–27.

    American Diabetes Association (2015). Classification and diagnosis of diabetes. Diabetes Care, 38, 8–16.

    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

    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

    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

    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

    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

    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

    Chatzigeorgiou, A., Halapas, A., Kalafatakis, K. & Kamper, E. (2009). Animal Models of Diabetes: a Synopsis. In Vivo, 23, 245–258.

    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

    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

    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

    Deckert, T. & Poulsen, J. E. (1981). Diabetic nephropathy: fault or destiny? Diabetologia, 21(3), 178–183. https://doi.org/10.1007/BF00252651

    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.

    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

    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

    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

    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

    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

    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

    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

    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

    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

    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

    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

    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

    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

    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.

    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

    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

    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

    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

    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

    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

    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

    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

    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

    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

    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

    Lenzen, S. (2008). The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia, 51, 216–226. https://doi.org/10.1007/s00125-007-0886-7

    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

    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

    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

    Millo, M. G. (2002). Adipose tissue hormones. Journal of Endocrinological Investigation, 25(10), 855–861. https://doi.org/10.1007/BF03344048

    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

    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

    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

    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

    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

    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

    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

    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

    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

    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

    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

    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

    Srinivasan, K. & Ramarao, P. (2007). Animal models in type 2 diabetes research: an overview. The Indian Journal of Medical Research, 125(3), 451–472.

    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

    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

    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

    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

    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

    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.

    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.

    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

    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

    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

    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

    Yang, Y. & Santamaria, P. (2006). Lessons on autoimmune diabetes from animal models. Clinical Science, 110(6), 627–639. https://doi.org/10.1042/CS20050330

    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

    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

    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

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