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Abstract
Diabetes mellitus is one of the world’s most prevalent and complex metabolic disorders, and it is a rapidly growing global public health issue. It is characterized by hyperglycemia, a condition involving a high blood glucose level brought on by deficiencies in insulin secretion, decreased activity of insulin, or both. Prolonged effects of diabetes include cardiovascular problems, retinopathy, neuropathy, nephropathy, and vascular alterations in both macro- and micro-blood vessels. In vivo and in vitro models have always been important for investigating and characterizing disease pathogenesis, identifying targets, and reviewing novel treatment options and medications. Fully understanding these models is crucial for the researchers so this review summarizes the different experimental in vivo and in vitro model options used to study diabetes and its consequences. The most popular in vivo studies involves the small animal models, such as rodent models, chemically induced diabetogens like streptozotocin and alloxan, and the possibility of deleting or overexpressing a specific gene by knockout and transgenic technologies on these animals. Other models include virally induced models, diet/nutrition induced diabetic animals, surgically induced models or pancreatectomy models, and non-obese models. Large animals or non-rodent models like porcine (pig), canine (dog), nonhuman primate, and Zebrafish models are also outlined. The in vitro models discussed are murine and human beta-cell lines and pancreatic islets, human stem cells, and organoid cultures. The other enzymatic in vitro tests to assess diabetes include assay of amylase inhibition and inhibition of α-glucosidase activity.
Keywords
animal models
/
diabetes mellitus type I
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diabetes mellitus type II
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in vitro and in vivo models
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Yasodha Krishna Janapati, Sunil Junapudi.
Progress in experimental models to investigate the in vivo and in vitro antidiabetic activity of drugs.
Animal Models and Experimental Medicine, 2024, 7(3): 297-309 DOI:10.1002/ame2.12442
| [1] |
Roep BO, Thomaidou S, van Tienhoven R, Zaldumbide A. Type 1 diabetes mellitus as a disease of the β-cell (do not blame the immune system?). Nat Rev Endocrinol. 2021;17(3):150-161.
|
| [2] |
Wysham C, Shubrook J. Beta-cell failure in type 2 diabetes: mechanisms, markers, and clinical implications. Postgrad Med. 2020;132(8):676-686.
|
| [3] |
Unnikrishnan R, Anjana RM, Mohan V. Diabetes mellitus and its complications in India. Nat Rev Endocrinol. 2016;12(6):357-370.
|
| [4] |
Wang M, Liang Y, Chen K, et al. The management of diabetes mellitus by mangiferin: advances and prospects. Nanoscale. 2022;14(6):2119-2135.
|
| [5] |
https://diabetesatlas.org/
|
| [6] |
Bommer C, Heesemann E, Sagalova V, et al. The global economic burden of diabetes in adults aged 20-79 years: a cost-of-illness study. Lancet Diabetes Endocrinol. 2017;5(6):423-430.
|
| [7] |
Zhang P, Gregg E. Global economic burden of diabetes and its implications. Lancet Diabetes Endocrinol. 2017;5(6):404-405.
|
| [8] |
Https://Www.Statista.Com/Topics/6556/Diabetes-in-China/#topicHeader__wrapper
|
| [9] |
Pradeepa R, Mohan V. Epidemiology of type 2 diabetes in India. Indian J Ophthalmol. 2021;69(11):2932-2938.
|
| [10] |
Https://Diabetes.Org/
|
| [11] |
Kottaisamy CPD, Raj DS, Prasanth Kumar V, Sankaran U. Experimental animal models for diabetes and its related complications-a review. Lab Anim Res. 2021;37(1):23.
|
| [12] |
https://www.genome.gov/10001345/importance-of-mouse-genome
|
| [13] |
Archibald K. Animal Experimentation: Working Towards a Paradigm Change. Brill; 2019. https://brill.com/display/book/edcoll/9789004391192/BP000023.xml
|
| [14] |
Hernandez J. The FDA No Longer Requires All Drugs to Be Tested on Animals Before Human Trials; 2023. https://www.npr.org/2023/01/12/1148529799/fda-animal-testing-pharmaceuticals-drug-development
|
| [15] |
Banting FG, Best CH, Collip JB, Campbell WR, Fletcher AA. Pancreatic extracts in the treatment of diabetes mellitus. Can Med Assoc J. 1922;12(3):141-146.
|
| [16] |
Etuk EU. Animal models for studying diabetes mellitus. Agric Biol JN Am. 2010;1(2):130-134.
|
| [17] |
Rees DA, Alcolado JC. Animal models of diabetes mellitus. Diabet Med J Br Diabet Assoc. 2005;22(4):359-370.
|
| [18] |
Eddouks M, Chattopadhyay D, Zeggwagh NA. Animal models as tools to investigate antidiabetic and anti-inflammatory plants. Evid Based Complement Alternat Med. 2012;2012:142087.
|
| [19] |
Renner S, Blutke A, Clauss S, et al. Porcine models for studying complications and organ crosstalk in diabetes mellitus. Cell Tissue Res. 2020;380(2):341-378.
|
| [20] |
Pöppl AG, de Carvalho GLC, Vivian IF, Corbellini LG, González FHD. Canine diabetes mellitus risk factors: a matched case-control study. Res Vet Sci. 2017;114:469-473.
|
| [21] |
Pound LD, Kievit P, Grove KL. The nonhuman primate as a model for type 2 diabetes. Curr Opin Endocrinol Diabetes Obes. 2014;21(2):89-94.
|
| [22] |
Salehpour A, Rezaei M, Khoradmehr A, Tahamtani Y, Tamadon A. Which hyperglycemic model of zebrafish (Danio rerio) suites my type 2 diabetes mellitus research? A scoring system for available methods. Front Cell Dev Biol. 2021;9:652061.
|
| [23] |
Adin CA, Gilor C. The diabetic dog as a translational model for human islet transplantation. Yale J Biol Med. 2017;90(3):509-515.
|
| [24] |
Heeley AM, O’Neill DG, Davison LJ, Church DB, Corless EK, Brodbelt DC. Diabetes mellitus in dogs attending UK primary-care practices: frequency, risk factors and survival. Canine Med Genet. 2020;7(1):6.
|
| [25] |
Wang TN, Hu XG, Chen GX. Uses of knockout, knockdown, and transgenic models in the studies of glucose transporter 4. World J Meta-Anal. 2022;10(1):1-11.
|
| [26] |
Lenzen S. The mechanisms of alloxan-and streptozotocin-induced diabetes. Diabetologia. 2008;51:216-226.
|
| [27] |
Ledoux SP, Wilson GL. Effects of streptozotocin on a clonal isolate of rat insulinoma cells. Biochim Biophys Acta BBA-Mol Cell Res. 1984;804(4):387-392.
|
| [28] |
Lenzen S, Tiedge M, Elsner M, et al. The LEW.1AR1/Ztm-iddm rat: a new model of spontaneous insulin-dependent diabetes mellitus. Diabetologia. 2001;44(9):1189-1196.
|
| [29] |
King AJ. The use of animal models in diabetes research: animal models of diabetes. Br J Pharmacol. 2012;166(3):877-894.
|
| [30] |
van der Werf N, Kroese FGM, Rozing J, Hillebrands JL. Viral infections as potential triggers of type 1 diabetes. Diabetes Metab Res Rev. 2007;23(3):169-183.
|
| [31] |
Xiao Y, Karam C, Yi J, et al. ROS-related mitochondrial dysfunction in skeletal muscle of an ALS mouse model during the disease progression. Pharmacol Res. 2018;138:25-36.
|
| [32] |
Han J, Liu YQ. Reduction of islet pyruvate carboxylase activity might be related to the development of type 2 diabetes mellitus in agouti-K mice. J Endocrinol. 2010;204(2):143-152.
|
| [33] |
Rider BJ. Streptozotocin. In: Enna SJ, Bylund DB, eds. xPharm: The Comprehensive Pharmacology Reference. Elsevier; 2007:1-4.
|
| [34] |
Mostafavinia A, Amini A, Ghorishi SK, Pouriran R, Bayat M. The effects of dosage and the routes of administrations of streptozotocin and alloxan on induction rate of type1 diabetes mellitus and mortality rate in rats. Lab Anim Res. 2016;32(3):160-165.
|
| [35] |
Srinivasan K, Ramarao P. Animal models in type 2 diabetes research: an overview. Indian J Med Res. 2007;125(3):451-472.
|
| [36] |
White MG, Shaw JAM, Taylor R. Type 2 diabetes: the pathologic basis of reversible β-cell dysfunction. Diabetes Care. 2016;39(11):2080-2088.
|
| [37] |
Sheshala R, Peh KK, Darwis Y. Preparation, characterization, and in vivo evaluation of insulin-loaded PLA-PEG microspheres for controlled parenteral drug delivery. Drug Dev Ind Pharm. 2009;35(11):1364-1374.
|
| [38] |
Jansson L, Eizirik DL, Pipeleers DG, Borg LA, Hellerström C, Andersson A. Impairment of glucose-induced insulin secretion in human pancreatic islets transplanted to diabetic nude mice. J Clin Invest. 1995;96(2):721-726.
|
| [39] |
Graham ML, Janecek JL, Kittredge JA, Hering BJ, Schuurman HJ. The streptozotocin-induced diabetic nude mouse model: differences between animals from different sources. Comp Med. 2011;61(4):356-360.
|
| [40] |
Halim D, Khalifa K, Awadallah R, El-Hawary Z, El-Dessouky EA. Serum mineral changes in dithizone-induced diabetes before and after insulin treatment. Z Ernahrungswiss. 1977;16(1):22-26.
|
| [41] |
Penfornis A, Kury-Paulin S. Immunosuppressive drug-induced diabetes. Diabetes Metab. 2006;32(5 Pt 2):539-546.
|
| [42] |
Clemetson CA. Ascorbic acid and diabetes mellitus. Med Hypotheses. 1976;2(5):193-194.
|
| [43] |
Kadota I, Midorikawa O. Diabetogenic action of organic reagents: destructive lesions of islets of Langerhans caused by sodium diethyldithiocarbamate and potassium ethylxanthate. J Lab Clin Med. 1951;38(5):671-688.
|
| [44] |
Dhuria RS, Singh G, Kaur A, Kaur R, Kaur T. Current status and patent prospective of animal models in diabetic research. Adv Biomed Res. 2015;4:117.
|
| [45] |
Papich MG. Streptozocin. In: Papich MG, ed. Saunders Handbook of Veterinary Drugs. 4th ed. W.B. Saunders; 2016:742-743.
|
| [46] |
Wallig MA. Chapter 20: Endocrine system. In: Wallig MA, Haschek WM, Rousseaux CG, Bolon B, eds. Fundamentals of Toxicologic Pathology. 3rd ed. Academic Press; 2018:565-624.
|
| [47] |
Szkudelski T. The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol Res. 2001;50(6):537-546.
|
| [48] |
Islam M, Code Q. Streptozotocin is more convenient than Alloxan for the induction of type 2 diabetes. IJPR. 2017;7(1):10-7439.
|
| [49] |
Saleem Mir M, Maqbool Darzi M, Khalil Baba O, et al. Streptozotocin induced acute clinical effects in rabbits (Oryctolagus cuniculus). Iran J Pathol. 2015;10(3):206-213.
|
| [50] |
Janapti Y. Optimize diabetes by herbal medicine: a review. J Adv Med Pharm Sci. 2015;3(3):98-111.
|
| [51] |
Janapati YK, Junapudi S, Dachani SR. Optimization of diabetes by herbal medicine. Technol Innov Manag Rev. 2021;6:1-18.
|
| [52] |
Chen D, Thayer TC, Wen L, Wong FS. Mouse models of autoimmune diabetes: the nonobese diabetic (NOD) mouse. Methods Mol Biol. 2020;2128:87-92.
|
| [53] |
Bortell R, Yang C. The BB rat as a model of human type 1 diabetes. Methods Mol Biol. 2012;933:31-44.
|
| [54] |
Yokoi N, Namae M, Fuse M, et al. Establishment and characterization of the Komeda diabetes-prone rat as a segregating inbred strain. Exp Anim. 2003;52(4):295-301.
|
| [55] |
Weiss H, Bleich A, Hedrich HJ, et al. Genetic analysis of the LEW.1AR1-iddm rat: an animal model for spontaneous diabetes mellitus. Mamm Genome. 2005;16(6):432-441.
|
| [56] |
Conaway HH, Faas FH, Smith SD, Sanders LL. Spontaneous diabetes mellitus in the New Zealand white rabbit: physiologic characteristics. Metabolism. 1981;30(1):50-56.
|
| [57] |
Kramer JW. Animal model of human disease: inherited early-onset, insulin-requiring diabetes mellitus in keeshond dogs. Am J Pathol. 1981;105(2):194-196.
|
| [58] |
Gerritsen GC. The Chinese hamster as a model for the study of diabetes mellitus. Diabetes. 1982;31(suppl 1):14-23.
|
| [59] |
Harwood HJ Jr, Listrani P, Wagner JD. Nonhuman primates and other animal models in diabetes research. J Diabetes Sci Technol. 2012;6(3):503-514.
|
| [60] |
Hau J. Animal models for human diseases. In: Conn PM, ed. Sourcebook of Models for Biomedical Research. Humana Press; 2008:3-8.
|
| [61] |
Bnouham MM, Ziyyat AA, Mekhfi HH, Tahri AA, Legssyer AA. Medicinal plants with potential antidiabetic activity-a review of ten years of herbal medicine research (1990-2000). Int J Diabetes Metab. 2006;14(1):1-25.
|
| [62] |
Serreze DV, Niens M, Kulik J, Di Lorenzo TP. Bridging mice to men: using HLA transgenic mice to enhance the future prediction and prevention of autoimmune type 1 diabetes in humans. In: Proetzel G, Wiles MV, eds. Mouse Models for Drug Discovery. Vol 602. Methods in Molecular Biology. Humana Press; 2010:119-134.
|
| [63] |
Hasan MDM, Ahmed QU, Mat Soad SZ, Tunna TS. Animal models and natural products to investigate in vivo and in vitro antidiabetic activity. Biomed Pharmacother. 2018;101:833-841.
|
| [64] |
Müller G. Methods to induce experimental diabetes mellitus. In: Hock FJ, ed. Drug Discovery and Evaluation: Pharmacological Assays. Springer International Publishing; 2016:2569-2581.
|
| [65] |
Britsch S. Transgenic and knock-out animals. Encyclopedic Reference of Genomics and Proteomics in Molecular Medicine. Springer; 2006:1900-1903.
|
| [66] |
Habener JF, Kemp DM, Thomas MK. Minireview: transcriptional regulation in pancreatic development. Endocrinology. 2005;146(3):1025-1034.
|
| [67] |
Kahn CR. Knockout mice challenge our concepts of glucose homeostasis and the pathogenesis of diabetes. Exp Diabesity Res. 2003;4(3):169-182.
|
| [68] |
Wang Q, Jin T. The role of insulin signaling in the development of β-cell dysfunction and diabetes. Islets. 2009;1(2):95-101.
|
| [69] |
Neubauer N, Kulkarni RN. Molecular approaches to study control of glucose homeostasis. ILAR J. 2006;47(3):199-211.
|
| [70] |
Accili D, Drago J, Lee EJ, et al. Early neonatal death in mice homozygous for a null allele of the insulin receptor gene. Nat Genet. 1996;12(1):106-109.
|
| [71] |
Roncero I, Alvarez E, Acosta C, et al. Insulin-receptor substrate-2 (IRS-2) is required for maintaining glucokinase and glucokinase regulatory protein expression in mouse liver. PLoS ONE. 2013;8(4):e58797.
|
| [72] |
Yan R, Zhang Y, Yang Y, et al. Peroxisome proliferator-activated receptor gene knockout promotes podocyte injury in diabetic mice [retracted in: Biomed Res Int. 2022 Nov 23;2022:9764610]. Biomed Res Int. 2022;2022:9018379.
|
| [73] |
Baker DJ, Atkinson AM, Wilkinson GP, Coope GJ, Charles AD, Leighton B. Characterization of the heterozygous glucokinase knockout mouse as a translational disease model for glucose control in type 2 diabetes. Br J Pharmacol. 2014;171(7):1629-1641.
|
| [74] |
Jun HS, Yoon JW. A new look at viruses in type 1 diabetes. Diabetes Metab Res Rev. 2003;19(1):8-31.
|
| [75] |
Horwitz MS, Bradley LM, Harbertson J, Krahl T, Lee J, Sarvetnick N. Diabetes induced by Coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat Med. 1998;4(7):781-785.
|
| [76] |
Yoon JW, Jun HS. Viruses cause type 1 diabetes in animals. Ann N Y Acad Sci. 2006;1079:138-146.
|
| [77] |
Alkanani AK, Hara N, Gianani R, Zipris D. Kilham rat virus-induced type 1 diabetes involves beta cell infection and intra-islet JAK-STAT activation prior to insulitis. Virology. 2014;468-470:19-27.
|
| [78] |
von Herrath MG, Coon B, Wolfe T, Chatenoud L. Nonmitogenic CD3 antibody reverses virally induced (rat insulin promoter-lymphocytic choriomeningitis virus) autoimmune diabetes without impeding viral clearance. J Immunol. 2002;168(2):933-941.
|
| [79] |
Menser MA, Forrest JM, Bransby RD. Rubella infection and diabetes mellitus. Lancet. 1978;1(8055):57-60.
|
| [80] |
Craighead JE. Viral diabetes mellitus in man and experimental animals. Am J Med. 1981;70(1):127-134.
|
| [81] |
von Herrath M, Filippi C, Coppieters K. How viral infections enhance or prevent type 1 diabetes-from mouse to man. J Med Virol. 2011;83(9):1672.
|
| [82] |
Richardson SJ, Willcox A, Bone AJ, Foulis AK, Morgan NG. The prevalence of enteroviral capsid protein vp1 immunostaining in pancreatic islets in human type 1 diabetes. Diabetologia. 2009;52(6):1143-1151.
|
| [83] |
Morel P, Kaufmann DB, Matas AJ, et al. Total pancreatectomy in the pig for islet transplantation. Tech Altern Transplant. 1991;52(1):11-15.
|
| [84] |
Zettler S, Renner S, Kemter E, et al. A decade of experience with genetically tailored pig models for diabetes and metabolic research. Anim Reprod. 2020;17(3):e20200064.
|
| [85] |
Suriano F, Vieira-Silva S, Falony G, et al. Novel insights into the genetically obese (ob/ob) and diabetic (db/db) mice: two sides of the same coin. Microbiome. 2021;9(1):147.
|
| [86] |
Guest PC, Rahmoune H. Characterization of the db/db mouse model of type 2 diabetes. Methods Mol Biol. 2019;1916:195-201.
|
| [87] |
Fu C, Zhang X, Ye F, Yang J. High insulin levels in KK-ay diabetic mice cause increased cortical bone mass and impaired trabecular micro-structure. Int J Mol Sci. 2015;16(4):8213-8226.
|
| [88] |
Tomino Y. Lessons from the KK-ay mouse, a spontaneous animal model for the treatment of human type 2 diabetic nephropathy. Nephro-Urol Mon. 2012;4(3):524-529.
|
| [89] |
Kluge R, Scherneck S, Schürmann A, Joost HG. Pathophysiology and genetics of obesity and diabetes in the New Zealand obese mouse: a model of the human metabolic syndrome. Methods Mol Biol. 2012;933:59-73.
|
| [90] |
Leiter EH, Reifsnyder PC. Differential levels of diabetogenic stress in two new mouse models of obesity and type 2 diabetes. Diabetes. 2004;53(suppl_1):S4-S11.
|
| [91] |
Hirayama I, Yi Z, Izumi S, et al. Genetic analysis of obese diabetes in the TSOD mouse. Diabetes. 1999;48(5):1183-1191.
|
| [92] |
Allan MF, Eisen EJ, Pomp D. The M16 mouse: an outbred animal model of early onset polygenic obesity and diabesity. Obes Res. 2004;12(9):1397-1407.
|
| [93] |
Otani K, Funada H, Teranishi R, Okada M, Yamawaki H. Cardiovascular characteristics of Zucker fatty diabetes mellitus rats, an animal model for obesity and type 2 diabetes. Int J Mol Sci. 2022;23(8):4228.
|
| [94] |
Peterson RG, Shaw WN, Neel MA, Little LA, Eichberg J. Zucker diabetic fatty rat as a model for non-insulin-dependent diabetes mellitus. ILAR J. 1990;32(3):16-19.
|
| [95] |
Shiota M, Printz RL. Diabetes in Zucker diabetic fatty rat. Methods Mol Biol. 2012;933:103-123.
|
| [96] |
Greene SF, Johnson PR, Eiffert KC, Greenwoodt MR, Stern JS. The male obese Wistar diabetic fatty rat is a new model of extreme insulin resistance. Obes Res. 1994;2(5):432-443.
|
| [97] |
Augstein P, Salzsieder E. Morphology of pancreatic islets: a time course of pre-diabetes in Zucker fatty rats. Methods Mol Biol. 2009;560:159-189.
|
| [98] |
Frisbee JC. Hypertension-independent microvascular rarefaction in the obese Zucker rat model of the metabolic syndrome. Microcirculation. 2005;12(5):383-392.
|
| [99] |
Weir GC, Marselli L, Marchetti P, Katsuta H, Jung MH, Bonner-Weir S. Towards better understanding of the contributions of overwork and glucotoxicity to the beta-cell inadequacy of type 2 diabetes. Diabetes Obes Metab. 2009;11(suppl 4):82-90.
|
| [100] |
Suleiman JB, Mohamed M, Bakar ABA. A systematic review on different models of inducing obesity in animals: advantages and limitations. J Adv Vet Anim Res. 2019;7(1):103-114.
|
| [101] |
Akash M, Rehman K, Chen S. Goto-kakizaki rats: its suitability as non-obese diabetic animal model for spontaneous type 2 diabetes mellitus. Curr Diabetes Rev. 2013;9(5):387-396.
|
| [102] |
Cohen AM, Rosenmann E, Rosenthal T. The cohen diabetic (non-insulin-dependent) hypertensive rat model. Description of the model and pathologic findings. Am J Hypertens. 1993;6(12):989-995.
|
| [103] |
Mathews CE, Bagley R, Leiter EH. ALS/Lt: a new type 2 diabetes mouse model associated with low free radical scavenging potential. Diabetes. 2004;53(1):S125-S129.
|
| [104] |
Höppener JW, Jacobs HM, Wierup N, et al. Human islet amyloid polypeptide transgenic mice: in vivo and ex vivo models for the role of hIAPP in type 2 diabetes mellitus. Exp Diabetes Res. 2008;2008:697035.
|
| [105] |
Seal SV, Henry M, Pajot C, et al. A holistic view of the Goto-Kakizaki rat immune system: decreased circulating immune markers in non-obese type 2 diabetes. Front Immunol. 2022;13:896179.
|
| [106] |
Weksler-Zangen S, Yagil C, Zangen DH, Ornoy A, Jacob HJ, Yagil Y. The newly inbred cohen diabetic rat: a nonobese normolipidemic genetic model of diet-induced type 2 diabetes expressing sex differences. Diabetes. 2001;50(11):2521-2529.
|
| [107] |
Sasase T, Ohta T, Masuyama T, Yokoi N, Kakehashi A, Shinohara M. The spontaneously diabetic torii rat: an animal model of nonobese type 2 diabetes with severe diabetic complications. J Diabetes Res. 2013;2013:976209.
|
| [108] |
Shinohara M, Oikawa T, Sato K, Kanazawa Y. Glucose intolerance and hyperlipidemia prior to diabetes onset in female spontaneously diabetic Torii (SDT) rats. Exp Diabesity Res. 2004;5(4):253-256.
|
| [109] |
Yamada K, Hosokawa M, Fujimoto S, et al. The spontaneously diabetic Torii rat with gastroenteropathy. Diabetes Res Clin Pract. 2007;75(2):127-134.
|
| [110] |
Stott NL, Marino JS. High fat rodent models of type 2 diabetes: from rodent to human. Nutrients. 2020;12(12):3650.
|
| [111] |
Wondmkun YT. Obesity, insulin resistance, and type 2 diabetes: associations and therapeutic implications. Diabetes Metab Syndr Obes. 2020;13:3611-3616.
|
| [112] |
Kaiser N, Cerasi E, Leibowitz G. Diet-induced diabetes in the sand rat (Psammomys obesus). In: Joost HG, Al-Hasani H, Schürmann A, eds. Animal Models in Diabetes Research. Humana Press; 2012:89-102.
|
| [113] |
Gouaref I, Detaille D, Wiernsperger N, Khan NA, Leverve X, Koceir EA. The desert gerbil Psammomys obesus as a model for metformin-sensitive nutritional type 2 diabetes to protect hepatocellular metabolic damage: impact of mitochondrial redox state. PLoS ONE. 2017;12(2):e0172053.
|
| [114] |
Sahraoui A, Dewachter C, de Medina G, Naeije R, Aouichat Bouguerra S, Dewachter L. Myocardial structural and biological anomalies induced by high fat diet in Psammomys obesus gerbils. PLoS ONE. 2016;11(2):e0148117.
|
| [115] |
Gaire J, Varholick JA, Rana S, et al. Spiny mouse (Acomys): an emerging research organism for regenerative medicine with applications beyond the skin. Npj Regen Med. 2021;6(1):1.
|
| [116] |
Shafrir E, Ziv E, Kalman R. Nutritionally induced diabetes in desert rodents as models of type 2 diabetes: Acomys cahirinus (spiny mice) and Psammomys obesus (desert gerbil). ILAR J. 2006;47(3):212-224.
|
| [117] |
Flanagan P. Nile grass rats see the light of day. Lab Anim. 2013;42(4):115.
|
| [118] |
Subramaniam A, Landstrom M, Luu A, Hayes KC. The Nile rat (Arvicanthis niloticus) as a superior carbohydrate-sensitive model for type 2 diabetes mellitus (T2DM). Nutrients. 2018;10(2):235.
|
| [119] |
Noda K, Melhorn MI, Zandi S, et al. An animal model of spontaneous metabolic syndrome: Nile grass rat. FASEB J. 2010;24(7):2443-2453.
|
| [120] |
Henson MS, O’Brien TD. Feline models of type 2 diabetes mellitus. ILAR J. 2006;47(3):234-242.
|
| [121] |
Samaha G, Beatty J, Wade CM, Haase B. The Burmese cat as a genetic model of type 2 diabetes in humans [published correction appears in Anim Genet. 2020 Feb;51(1):153]. Anim Genet. 2019;50(4):319-325.
|
| [122] |
Samaha G, Wade CM, Beatty J, Lyons LA, Fleeman LM, Haase B. Mapping the genetic basis of diabetes mellitus in the Australian Burmese cat (Felis catus). Sci Rep. 2020;10(1):19194.
|
| [123] |
Ramsey JJ, Laatsch JL, Kemnitz JW. Age and gender differences in body composition, energy expenditure, and glucoregulation of adult rhesus monkeys. J Med Primatol. 2000;29(1):11-19.
|
| [124] |
Smith AB, Schill JP, Gordillo R, et al. Ceramides are early responders in metabolic syndrome development in rhesus monkeys. Sci Rep. 2022;12(1):9960.
|
| [125] |
Lieschke GJ, Currie PD. Animal models of human disease: zebrafish swim into view. Nat Rev Genet. 2007;8(5):353-367.
|
| [126] |
Oka T, Nishimura Y, Zang L, et al. Diet-induced obesity in zebrafish shares common pathophysiological pathways with mammalian obesity. BMC Physiol. 2010;10:21.
|
| [127] |
Teame T, Zhang Z, Ran C, et al. The use of zebrafish (Danio rerio) as biomedical models. Anim Front. 2019;9(3):68-77.
|
| [128] |
Papatheodorou K, Banach M, Bekiari E, Rizzo M, Edmonds M. Complications of diabetes 2017. J Diabetes Res. 2018;2018:3086167.
|
| [129] |
Choi JSY, De Haan JB, Sharma A. Animal models of diabetes-associated vascular diseases: an update on available models and experimental analysis. Br J Pharmacol. 2022;179(5):748-769.
|
| [130] |
Singh R, Farooq SA, Mannan A, et al. Animal models of diabetic microvascular complications: relevance to clinical features. Biomed Pharmacother. 2022;145:112305.
|
| [131] |
Hassan RH. Defect of insulin signal in peripheral tissues: important role of ceramide. World J Diabetes. 2014;5(3):244-257.
|
| [132] |
Ho HTB, Chung SK, Law JWS, et al. Aldose reductase-deficient mice develop nephrogenic diabetes insipidus. Mol Cell Biol. 2000;20(16):5840-5846.
|
| [133] |
Jiang X, Yang L, Luo Y. Animal models of diabetic retinopathy. Curr Eye Res. 2015;40(8):761-771.
|
| [134] |
Thomas AA, Biswas S, Feng B, Chen S, Gonder J, Chakrabarti S. lncRNA H19 prevents endothelial-mesenchymal transition in diabetic retinopathy. Diabetologia. 2019;62(3):517-530.
|
| [135] |
Cai X, McGinnis JF. Diabetic retinopathy: animal models, therapies, and perspectives. J Diabetes Res. 2016;2016:3789217.
|
| [136] |
B Arden G, Sivaprasad S. Hypoxia and oxidative stress in the causation of diabetic retinopathy. Curr Diabetes Rev. 2011;7(5):291-304.
|
| [137] |
Tang J, Du Y, Petrash JM, Sheibani N, Kern TS. Deletion of aldose reductase from mice inhibits diabetes-induced retinal capillary degeneration and superoxide generation. PLoS ONE. 2013;8(4):e62081.
|
| [138] |
Feldman E, Sullivan K, Lentz S, Roberts J Jr. Criteria for creating and assessing mouse models of diabetic neuropathy. Curr Drug Targets. 2008;9(1):3-13.
|
| [139] |
Drel VR, Mashtalir N, Ilnytska O, et al. The leptin-deficient (ob/ob) mouse. Diabetes. 2006;55(12):3335-3343.
|
| [140] |
Kennedy WR, Quick DC, Miyoshi T, Gerritsen GC. Peripheral neurology of the diabetic Chinese hamster. Diabetologia. 1982;23(5):445-451.
|
| [141] |
Bhatti R, Sharma S, Singh J, Ishar MPS. Ameliorative effect of Aegle marmelos leaf extract on early stage alloxan-induced diabetic cardiomyopathy in rats. Pharm Biol. 2011;49(11):1137-1143.
|
| [142] |
Lee WS, Kim J. Application of animal models in diabetic cardiomyopathy. Diabetes Metab J. 2021;45(2):129-145.
|
| [143] |
Jasińska-Stroschein M. The current state of preclinical modeling of human diabetic cardiomyopathy using rodents. Biomed Pharmacother. 2023;168:115843.
|
| [144] |
Rodrigues B, McNeill JH. Cardiac dysfunction in isolated perfused hearts from spontaneously diabetic BB rats. Can J Physiol Pharmacol. 1990;68(4):514-518.
|
| [145] |
Lilao-Garzón J, Valverde-Tercedor C, Muñoz-Descalzo S, Brito-Casillas Y, Wägner AM. In vivo and in vitro models of diabetes: a focus on pregnancy. In: Islam MDS, ed. Diabetes: from Research to Clinical Practice. Vol. 1307. Advances in Experimental Medicine and Biology. Springer International Publishing; 2020:553-576.
|
| [146] |
Reed MJ, Scribner KA. In-vivo and in-vitro models of type 2 diabetes in pharmaceutical drug discovery. Diabetes Obes Metab. 1999;1(2):75-86.
|
| [147] |
Sotelo JR, Horie H, Ito S, Benech C, Sango K, Takenaka T. An in vitro model to study diabetic neuropathy. Neurosci Lett. 1991;129(1):91-94.
|
| [148] |
Verma A, Verma M, Singh A. Animal tissue culture principles and applications. Anim Biotechnol. 2020;269-293.
|
| [149] |
Poovitha S, Parani M. In vitro and in vivo α-amylase and α-glucosidase inhibiting activities of the protein extracts from two varieties of bitter gourd (Momordica charantia L.). BMC Complement Altern Med. 2016;16(S1):185.
|
| [150] |
Khadayat K, Marasini BP, Gautam H, Ghaju S, Parajuli N. Evaluation of the alpha-amylase inhibitory activity of Nepalese medicinal plants used in the treatment of diabetes mellitus. Clin Phytosci. 2020;6(1):34.
|
| [151] |
Hanson MS, Steffen A, Danobeitia JS, Ludwig B, Fernandez LA. Flow cytometric quantification of glucose-stimulated β-cell metabolic flux can reveal impaired islet functional potency. Cell Transplant. 2008;17(12):1337-1347.
|
| [152] |
Jones B, Bloom SR, Buenaventura T, Tomas A, Rutter GA. Control of insulin secretion by GLP-1. Peptides. 2018;100:75-84.
|
| [153] |
Kalwat MA, Wichaidit C, Nava Garcia AY, et al. Insulin promoter-driven Gaussia luciferase-based insulin secretion biosensor assay for discovery of β-cell glucose-sensing pathways. ACS Sens. 2016;1(10):1208-1212.
|
| [154] |
Nakajima Y, Ohmiya Y. Bioluminescence assays: multicolor luciferase assay, secreted luciferase assay and imaging luciferase assay. Expert Opin Drug Discovery. 2010;5(9):835-849.
|
| [155] |
Zhang H, Yang F, Qi J, et al. Homoisoflavonoids from the fibrous roots of Polygonatum odoratum with glucose uptake-stimulatory activity in 3T3-L1 adipocytes. J Nat Prod. 2010;73(4):548-552.
|
| [156] |
Yamamoto N, Ueda-Wakagi M, Sato T, et al. Measurement of glucose uptake in cultured cells. Curr Protoc Pharmacol. 2015;71(1):12-14.
|
| [157] |
Yamamoto N, Ashida H. Evaluation methods for facilitative glucose transport in cells and their applications. Food Sci Technol Res. 2012;18(4):493-503.
|
| [158] |
Vhora N, Naskar U, Hiray A, Kate AS, Jain A. Recent advances in in-vitro assays for type 2 diabetes mellitus: an overview. Rev Diabet Stud. 2020;16(1):13-23.
|
| [159] |
Efrat S, Leiser M, Surana M, Tal M, Fusco-Demane D, Fleischer N. Murine insulinoma cell line with normal glucose-regulated insulin secretion. Diabetes. 1993;42(6):901-907.
|
| [160] |
D’Ambra R, Surana M, Efrat S, Starr RG, Fleischer N. Regulation of insulin secretion from beta-cell lines derived from transgenic mice insulinomas resembles that of normal beta-cells. Endocrinology. 1990;126(6):2815-2822.
|
| [161] |
Scharfmann R, Staels W, Albagli O. The supply chain of human pancreatic βcell lines. J Clin Invest. 2019;129(9):3511-3520.
|
| [162] |
Szot GL, Koudria P, Bluestone JA. Murine pancreatic islet isolation. J Vis Exp. 2007;7:255.
|
| [163] |
Corbin KL, West HL, Brodsky S, Whitticar NB, Koch WJ, Nunemaker CS. A practical guide to rodent islet isolation and assessment revisited. Biol Proced Online. 2021;23(1):7.
|
| [164] |
Da Silva XG. The cells of the islets of Langerhans. J Clin Med. 2018;7(3):54.
|
| [165] |
Balboa D, Barsby T, Lithovius V, et al. Functional, metabolic and transcriptional maturation of human pancreatic islets derived from stem cells. Nat Biotechnol. 2022;40(7):1042-1055.
|
| [166] |
Bani Hamad FR, Rahat N, Shankar K, Tsouklidis N. Efficacy of stem cell application in diabetes mellitus: promising future therapy for diabetes and its complications. Cureus. 2021;13(2):e13563.
|
| [167] |
Chen S, Du K, Zou C. Current progress in stem cell therapy for type 1 diabetes mellitus. Stem Cell Res Ther. 2020;11(1):275.
|
| [168] |
Zhang X, Ma Z, Song E, Xu T. Islet organoid as a promising model for diabetes. Protein Cell. 2022;13(4):239-257.
|
| [169] |
Dayem AA, Lee SB, Kim K, Lim KM, Jeon TI, Cho SG. Recent advances in organoid culture for insulin production and diabetes therapy: methods and challenges. BMB Rep. 2019;52(5):295-303.
|
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