Advanced Biomedical Research

Current status and patent prospective of animal models in diabetic research

Authors

1 Department of Pharmaceutical Sciences, Guru Nanak Dev University, Amritsar, India

2 School of Pharmaceutical Sciences, Lovely Professional University, Phagwara, Punjab, India

Abstract

Diabetes mellitus is a heterogeneous complex metabolic disorder with multiple etiology which characterized by chronic hyperglycemia resulting from defects in insulin secretion, insulin action or both. The widespread occurrence of diabetes throughout the world has increased dramatically over the past few years. For better understanding, appropriate animal models that closely mimic the changes in humans needed, as vital tool for understanding the etiology and pathogenesis of the disease at the cellular/molecular level and for preclinical testing of drugs. This review aims to describe the animal models of type-1 diabetes (T1Ds) and T2Ds to mimic the causes and progression of the disease in humans. And also we highlight patent applications published in the last few years related to animal models in diabetes as an important milestone for future therapies that are aim to treating diabetes with specific symptoms and complications.

Keywords

1.
Danaei G, Finucane MM, Lu Y, Singh GM, Cowan MJ, Paciorek CJ, et al. National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet 2011;378:31-40.  Back to cited text no. 1
    
2.
Mathers CD, Loncar D. Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 2006;3:e442.  Back to cited text no. 2
    
3.
Wang X. Translational Animal Models in Drug Discovery and Development. USA: Agennix Incorporated; 2012.  Back to cited text no. 3
    
4.
Etuk EU. Animals models for studying diabetes mellitus. Agr Biol J N Am  2010;1:130-4.  Back to cited text no. 4
    
5.
American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2010;33:62-9.  Back to cited text no. 5
    
6.
King AJ. The use of animal models in diabetes research. Br J Pharmacol 2012;166:877-94.  Back to cited text no. 6
    
7.
Hau J. Animal models for human diseases. In: Conn PM, editor. Sourcebook of Models for Biomedical Research. New Jersey: Human Press; 2008. p. 3-8.  Back to cited text no. 7
    
8.
Hansen K, Khanna C. Spontaneous and genetically engineered animal models; use in preclinical cancer drug development. Eur J Cancer 2004;40:858-80.  Back to cited text no. 8
    
9.
Chatzigeorgiou A, Halapas A, Kalafatakis K, Kamper E. The use of animal models in the study of diabetes mellitus. In Vivo 2009;23:245-58.  Back to cited text no. 9
    
10.
Polychronakos C. Animal models of spontaneous autoimmune diabetes: notes on their relevance to the human disease. Curr Diab Rep 2004;4:151-4.  Back to cited text no. 10
    
11.
Makino S, Kunimoto K, Muraoka Y, Mizushima Y, Katagiri K, Tochino Y. Breeding of a non-obese, diabetic strain of mice. Jikken Dobutsu 1980;29:1-13.  Back to cited text no. 11
    
12.
Mathews CE. Utility of murine models for the study of spontaneous autoimmune type 1 diabetes. Pediatr Diabetes 2005;6:165-77.  Back to cited text no. 12
    
13.
Atkinson MA, Leiter EH. The NOD mouse model of type 1 diabetes: as good as it gets? Nat Med 1999;5:601-4.  Back to cited text no. 13
    
14.
Giarratana N, Penna G, Adorini L. Animal models of spontaneous autoimmune disease: type 1 diabetes in the nonobese diabetic mouse. Methods Mol Biol 2007;380:285-311.  Back to cited text no. 14
    
15.
Mordes JP, Bortell R, Blankenhorn EP, Rossini AA, Greiner DL. Rat models of type 1 diabetes: genetics, environment, and autoimmunity. ILAR J 2004;45:278-91.  Back to cited text no. 15
    
16.
Nakhooda AF, Like AA, Chappel CI, Murray FT, Marliss EB. The spontaneously diabetic Wistar rat. Metabolic and morphologic studies. Diabetes 1977;26:100-12.  Back to cited text no. 16
    
17.
Rees DA, Alcolado JC. Animal models of diabetes mellitus. Diabet Med 2005;22:359-70.  Back to cited text no. 17
    
18.
Crisá L, Mordes JP, Rossini AA. Autoimmune diabetes mellitus in the BB rat. Diabetes Metab Rev 1992;8:4-37.  Back to cited text no. 18
    
19.
Jun HS, Yoon JW. A new look at viruses in type 1 diabetes. Diabetes Metab Res Rev 2003;19:8-31.  Back to cited text no. 19
    
20.
Kawano K, Hirashima T, Mori S, Saitoh Y, Kurosumi M, Natori T. New inbred strain of Long-Evans Tokushima lean rats with IDDM without lymphopenia. Diabetes 1991;40:1375-81.  Back to cited text no. 20
    
21.
Komeda K, Noda M, Terao K, Kuzuya N, Kanazawa M, Kanazawa Y. Establishment of two substrains, diabetes-prone and non-diabetic, from Long-Evans Tokushima Lean (LETL) rats. Endocr J 1998;45:737-44.  Back to cited text no. 21
    
22.
Yokoi N, Namae M, Fuse M, Wang HY, Hirata T, Seino S, et al. Establishment and characterization of the Komeda diabetes-prone rat as a segregating inbred strain. Exp Anim 2003;52:295-301.  Back to cited text no. 22
    
23.
Yokoi N, Komeda K, Wang HY, Yano H, Kitada K, Saitoh Y, et al. Cblb is a major susceptibility gene for rat type 1 diabetes mellitus. Nat Genet 2002;31:391-4.  Back to cited text no. 23
    
24.
Yokoi N, Hayashi C, Fujiwara Y, Wang HY, Seino S. Genetic reconstitution of autoimmune type 1 diabetes with two major susceptibility genes in the rat. Diabetes 2007;56:506-12.  Back to cited text no. 24
    
25.
Lenzen S, Tiedge M, Elsner M, Lortz S, Weiss H, Jörns A, et al. The LEW.1AR1/Ztm-iddm rat: a new model of spontaneous insulin-dependent diabetes mellitus. Diabetologia 2001;44:1189-96.  Back to cited text no. 25
    
26.
Jörns A, Günther A, Hedrich HJ, Wedekind D, Tiedge M, Lenzen S. Immune cell infiltration, cytokine expression, and beta-cell apoptosis during the development of type 1 diabetes in the spontaneously diabetic LEW.1AR1/Ztm-iddm rat. Diabetes 2005;54:2041-52.  Back to cited text no. 26
    
27.
Dufrane D, van Steenberghe M, Guiot Y, Goebbels RM, Saliez A, Gianello P. Streptozotocin-induced diabetes in large animals (pigs/primates): role of GLUT2 transporter and beta-cell plasticity. Transplantation 2006;81:36-45.  Back to cited text no. 27
    
28.
Bansal R, Ahmad N, Kidwai JR. Alloxan-glucose interaction: effect on incorporation of 14C-leucine into pancreatic islets of rat. Acta Diabetol Lat 1980;17:135-43.  Back to cited text no. 28
    
29.
Federiuk IF, Casey HM, Quinn MJ, Wood MD, Ward WK. Induction of type-1 diabetes mellitus in laboratory rats by use of alloxan: route of administration, pitfalls, and insulin treatment. Comp Med 2004;54:252-7.  Back to cited text no. 29
    
30.
Jederström G, Gråsjö, Nordin A, Sjöholm I, Andersson A. Blood glucose-lowering activity of a hyaluronan-insulin complex after oral administration to rats with diabetes. Diabetes Technol Ther 2005;7:948-57.  Back to cited text no. 30
    
31.
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;35:1364-74.  Back to cited text no. 31
    
32.
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;96:721-6.  Back to cited text no. 32
    
33.
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;61:356-60.  Back to cited text no. 33
    
34.
Makhlouf L, Duvivier-Kali VF, Bonner-Weir S, Dieperink H, Weir GC, Sayegh MH. Importance of hyperglycemia on the primary function of allogeneic islet transplants. Transplantation 2003;76:657-64.  Back to cited text no. 34
    
35.
Lee JH, Yang SH, Oh JM, Lee MG. Pharmacokinetics of drugs in rats with diabetes mellitus induced by alloxan or streptozocin: comparison with those in patients with type I diabetes mellitus. J Pharm Pharmacol 2010;62:1-23.  Back to cited text no. 35
    
36.
Bono VH Jr. Review of mechanism of action studies of the nitrosoureas. Cancer Treat Rep 1976;60:699-702.  Back to cited text no. 36
    
37.
Sandler S, Swenne I. Streptozotocin, but not alloxan, induces DNA repair synthesis in mouse pancreatic islets in vitro. Diabetologia 1983;25:444-7.  Back to cited text no. 37
    
38.
Steiner H, Oelz O, Zahnd G, Foresch ER. Studies on islet cell regeneration, hyperplasia and intrainsular cellular interrelations in long lasting streptozotocin diabetes in rats. Diabetologia 1970;6:558-64.  Back to cited text no. 38
    
39.
Yamagami T, Miwa A, Takasawa S, Yamamoto H, Okamoto H. Induction of rat pancreatic B-cell tumors by the combined administration of streptozotocin or alloxan and poly (adenosine diphosphate ribose) synthetase inhibitors. Cancer Res 1985;45:1845-9.  Back to cited text no. 39
    
40.
Iwase M, Nunoi K, Wakisaka M, Kikuchi M, Maki Y, Sadoshima S, et al. Spontaneous recovery from non-insulin-dependent diabetes mellitus induced by neonatal streptozotocin treatment in spontaneously hypertensive rats. Metabolism 1991;40:10-4.  Back to cited text no. 40
    
41.
Kazumi T, Yoshino G, Fujii S, Baba S. Tumorigenic action of streptozotocin on the pancreas and kidney in male Wistar rats. Cancer Res 1978;38:2144-7.  Back to cited text no. 41
    
42.
Rerup CC. Drugs producing diabetes through damage of the insulin secreting cells. Pharmacol Rev 1970;22:485-518.  Back to cited text no. 42
    
43.
Like AA, Rossini AA. Streptozotocin-induced pancreatic insulitis: new model of diabetes mellitus. Science 1976;193:415-7.  Back to cited text no. 43
    
44.
Wang Z, Gleichmann H. GLUT2 in pancreatic islets: crucial target molecule in diabetes induced with multiple low doses of streptozotocin in mice. Diabetes 1998;47:50-6.  Back to cited text no. 44
    
45.
Lukic ML, Stosic-Grujicic S, Shahin A. Effector mechanisms in low-dose streptozotocin-induced diabetes. Dev Immunol 1998;6:119-28.  Back to cited text no. 45
    
46.
Reddy S, Wu D, Elliott RB. Low dose streptozotocin causes diabetes in severe combined immunodeficient (SCID) mice without immune cell infiltration of the pancreatic islets. Autoimmunity 1995;20:83-92.  Back to cited text no. 46
    
47.
Lenzen S. The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia 2008;51:216-26.  Back to cited text no. 47
    
48.
Nerup J, Mandrup-Poulsen T, Helqvist S, Andersen HU, Pociot F, Reimers JI, et al. On the pathogenesis of IDDM. Diabetologia 1994;37 Suppl 2:S82-9.  Back to cited text no. 48
    
49.
Szkudelski T. The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol Res 2001;50:537-46.  Back to cited text no. 49
    
50.
Malaisse WJ, Malaisse-Lagae F, Sener A, Pipeleers DG. Determinants of the selective toxicity of alloxan to the pancreatic B cell. Proc Natl Acad Sci U S A 1982;79:927-30.  Back to cited text no. 50
    
51.
Mathews CE, Leiter EH. Constitutive differences in antioxidant defense status distinguish alloxan-resistant and alloxan-susceptible mice. Free Radic Biol Med 1999;27:449-55.  Back to cited text no. 51
    
52.
im Walde SS, Dohle C, Schott-Ohly P, Gleichmann H. Molecular target structures in alloxan-induced diabetes in mice. Life Sci 2002;71:1681-94.  Back to cited text no. 52
    
53.
Kim HR, Rho HW, Park BH, Park JW, Kim JS, Kim UH, et al. Role of Ca2+in alloxan-induced pancreatic beta-cell damage. Biochim Biophys Acta 1994;1227:87-91.  Back to cited text no. 53
    
54.
Wang J, Wan R, Mo Y, Zhang Q, Sherwood LC, Chien S. Creating a long-term diabetic rabbit model. Exp Diabetes Res 2010;2010:289614.  Back to cited text no. 54
    
55.
Finch SC, Finch CA. Idiopathic hemochromatosis, an iron storage disease. A. Iron metabolism in hemochromatosis. Medicine (Baltimore) 1955;34:381-430.  Back to cited text no. 55
    
56.
Awai M, Narasaki M, Yamanoi Y, Seno S. Induction of diabetes in animals by parenteral administration of ferric nitrilotriacetate. A model of experimental hemochromatosis. Am J Pathol 1979;95:663-73.  Back to cited text no. 56
    
57.
Hansen WA, Christie MR, Kahn R, Norgaard A, Abel I, Petersen AM, et al. Supravital dithizone staining in the isolation of human and rat pancreatic islets. Diabetes Res 1989;10:53-7.  Back to cited text no. 57
    
58.
Goldberg ED, Eshchenko VA, Bovt VD. The diabetogenic and acidotropic effects of chelators. Exp Pathol 1991;42:59-64.  Back to cited text no. 58
    
59.
Yoon JW, London WT, Curfman BL, Brown RL, Notkins AL. Coxsackie virus B4 produces transient diabetes in nonhuman primates. Diabetes 1986;35:712-6.  Back to cited text no. 59
    
60.
Jaïdane H, Sané F, Gharbi J, Aouni M, Romond MB, Hober D. Coxsackievirus B4 and type 1 diabetes pathogenesis: contribution of animal models. Diabetes Metab Res Rev 2009;25:591-603.  Back to cited text no. 60
    
61.
Craighead JE, McLane MF. Diabetes mellitus: induction in mice by encephalomyocarditis virus. Science 1968;162:913-4.  Back to cited text no. 61
    
62.
Baek HS, Yoon JW. Direct involvement of macrophages in destruction of beta-cells leading to development of diabetes in virus-infected mice. Diabetes 1991;40:1586-97.  Back to cited text no. 62
    
63.
Guberski DL, Thomas VA, Shek WR, Like AA, Handler ES, Rossini AA, et al. Induction of type I diabetes by Kilham's rat virus in diabetes-resistant BB/Wor rats. Science 1991;254:1010-3.  Back to cited text no. 63
    
64.
Ellerman KE, Richards CA, Guberski DL, Shek WR, Like AA. Kilham rat triggers T-cell-dependent autoimmune diabetes in multiple strains of rat. Diabetes 1996;45:557-62.  Back to cited text no. 64
    
65.
Oldstone MB, Nerenberg M, Southern P, Price J, Lewicki H. Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: role of anti-self (virus) immune response. Cell 1991;65:319-31.  Back to cited text no. 65
    
66.
Yoon JW, Onodera T, Notkins AL. Virus-induced diabetes mellitus. XV. Beta cell damage and insulin-dependent hyperglycemia in mice infected with coxsackie virus B4. J Exp Med 1978;148:1068-80.  Back to cited text no. 66
    
67.
Lin JH. Applications and limitations of genetically modified mouse models in drug discovery and development. Curr Drug Metab 2008;9:419-38.  Back to cited text no. 67
    
68.
Available from: http://www.apps.nhlbi.nih.gov/transgenic/default.htm. [Last accessed on 2013 Mar 15].  Back to cited text no. 68
    
69.
Mathews CE, Langley SH, Leiter EH. New mouse model to study islet transplantation in insulin-dependent diabetes mellitus. Transplantation 2002;73:1333-6.  Back to cited text no. 69
    
70.
Chen H, Zheng C, Zhang X, Li J, Li J, Zheng L, et al. Apelin alleviates diabetes-associated endoplasmic reticulum stress in the pancreas of Akita mice. Peptides 2011;32:1634-9.  Back to cited text no. 70
    
71.
Jun H, Bae HY, Lee BR, Koh KS, Kim YS, Lee KW, et al. Pathogenesis of non-insulin-dependent (type II) diabetes mellitus (NIDDM) - Genetic predisposition and metabolic abnormalities. Adv Drug Deliv Rev 1999;35:157-77.  Back to cited text no. 71
    
72.
Yap IS, Giddings G, Pocock E, Chantler JK. Lack of islet neogenesis plays a key role in beta-cell depletion in mice infected with a diabetogenic variant of coxsackievirus B4. J Gen Virol 2003;84:3051-68.  Back to cited text no. 72
    
73.
Drel VR, Mashtalir N, Ilnytska O, Shin J, Li F, Lyzogubov VV, et al. The leptin-deficient (ob/ob) mouse: a new animal model of peripheral neuropathy of type 2 diabetes and obesity. Diabetes 2006;55:3335-43.  Back to cited text no. 73
    
74.
Coleman DL. A historical perspective on leptin. Nat Med 2010;16:1097-9.  Back to cited text no. 74
    
75.
Bell RH Jr, Hye RJ. Animal models of diabetes mellitus: physiology and pathology. J Surg Res 1983;35:433-60.  Back to cited text no. 75
    
76.
Bates SH, Kulkarni RN, Seifert M, Myers MG Jr. Roles for leptin receptor/STAT3-dependent and -independent signals in the regulation of glucose homeostasis. Cell Metab 2005;1:169-78.  Back to cited text no. 76
    
77.
Berglund O, Frankel BJ, Hellman B. Development of the insulin secretory defect in genetically diabetic (db/db) mouse. Acta Endocrinol (Copenh) 1978;87:543-51.  Back to cited text no. 77
    
78.
Nakamura M, Yamada K. Studies on a diabetic (KK) strain of the mouse. Diabetologia 1967;3:212-21.  Back to cited text no. 78
    
79.
Ikeda H. KK mouse. Diabetes Res Clin Pract 1994;24 Suppl: S313-6.  Back to cited text no. 79
    
80.
Reddi AS, Camerini-Davalos RA. Hereditary diabetes in the KK mouse: an overview. Adv Exp Med Biol 1988;246:7-15.  Back to cited text no. 80
    
81.
Lenzen S, Panten U. Alloxan: history and mechanism of action. Diabetologia 1988;31:337-42.  Back to cited text no. 81
    
82.
Ramarao P, Kaul CL. Insulin resistance: current therapeutic approaches. Drugs Today (Barc) 1999;35:895-911.  Back to cited text no. 82
    
83.
Kato H, Ohue M, Kato K, Nomura A, Toyosawa K, Furutani Y, et al. Mechanism of amelioration of insulin resistance by beta3-adrenoceptor agonist AJ-9677 in the KK-Ay/Ta diabetic obese mouse model. Diabetes 2001;50:113-22.  Back to cited text no. 83
    
84.
Diani AR, Sawada G, Wyse B, Murray FT, Khan M. Pioglitazone preserves pancreatic islet structure and insulin secretory function in three murine models of type 2 diabetes. Am J Physiol Endocrinol Metab 2004;286:E116-22.  Back to cited text no. 84
    
85.
Shafrir E, Ziv E. A useful list of spontaneously arising animal models of obesity and diabetes. Am J Physiol Endocrinol Metab 2009;296:E1450-2.  Back to cited text no. 85
    
86.
Haskell BD, Flurkey K, Duffy TM, Sargent EE, Leiter EH. The diabetes-prone NZO/HlLt strain. I. Immunophenotypic comparison to the related NZB/BlNJ and NZW/LacJ strains. Lab Invest 2002;82:833-42.  Back to cited text no. 86
    
87.
Halaas JL, Boozer C, Blair-West J, Fidahusein N, Denton DA, Friedman JM. Physiological response to long-term peripheral and central leptin infusion in lean and obese mice. Proc Natl Acad Sci U S A 1997;94:8878-83.  Back to cited text no. 87
    
88.
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:S4-11.  Back to cited text no. 88
    
89.
Fang RC, Kryger ZB, Buck DW 2 nd , De la Garza M, Galiano RD, Mustoe TA. Limitations of the db/db mouse in translational wound healing research: Is the NONcNZO10 polygenic mouse model superior? Wound Repair Regen 2010;18:605-13.  Back to cited text no. 89
    
90.
Cho YR, Kim HJ, Park SY, Ko HJ, Hong EG, Higashimori T, et al. Hyperglycemia, maturity-onset obesity, and insulin resistance in NONcNZO10/LtJ males, a new mouse model of type 2 diabetes. Am J Physiol Endocrinol Metab 2007;293:E327-36.  Back to cited text no. 90
    
91.
Suzuki W, Iizuka S, Tabuchi M, Funo S, Yanagisawa T, Kimura M, et al. A new mouse model of spontaneous diabetes derived from ddY strain. Exp Anim 1999;48:181-9.  Back to cited text no. 91
    
92.
Miura T, Suzuki W, Ishihara E, Arai I, Ishida H, Seino Y, et al. Impairment of insulin-stimulated GLUT4 translocation in skeletal muscle and adipose tissue in the Tsumura Suzuki obese diabetic mouse: a new genetic animal model of type 2 diabetes. Eur J Endocrinol 2001;145:785-90.  Back to cited text no. 92
    
93.
Allan MF, Eisen EJ, Pomp D. The M16 mouse: an outbred animal model of early onset polygenic obesity and diabesity. Obes Res 2004;12:1397-407.  Back to cited text no. 93
    
94.
Augstein P, Salzsieder E. Morphology of pancreatic islets: a time course of pre-diabetes in Zucker fatty rats. Methods Mol Biol 2009;560:159-89.  Back to cited text no. 94
    
95.
Frisbee JC. Hypertension-independent microvascular rarefaction in the obese Zucker rat model of the metabolic syndrome. Microcirculation 2005;12:383-92.  Back to cited text no. 95
    
96.
McIntosh CH, Pederson RA. Non-insulin dependent animalmodels of diabetes mellitus. In: McNeil JH, editor. Experimental Models of Diabetes. Florida, USA: CRC Press LLC; 1999. p. 337-98.  Back to cited text no. 96
    
97.
Michaelis OE 4 th , Patrick DH, Hansen CT, Canary JJ, Werner RM, Carswell N. Insulin-independent diabetes mellitus (type II). Spontaneous hypertensive/NIH-corpulent rat. Am J Pathol 1986;123:398-400.  Back to cited text no. 97
    
98.
Russel JC, Kelly SE, Proctor S. The JCR: LA-cp rat: animal model of the metabolic syndrome exhibiting micro-and macromolecular disease. In: Shafrir E, editor. Animal Models of Diabetes, Frontiers in Research. Boca Raton, FL: CRC Press; 2007. p. 159-83.  Back to cited text no. 98
    
99.
Kawano K, Hirashima T, Mori S, Saitoh Y, Kurosumi M, Natori T. Spontaneous long-term hyperglycemic rat with diabetic complications. Otsuka Long-Evans Tokushima Fatty (OLETF) strain. Diabetes 1992;41:1422-8.  Back to cited text no. 99
    
100.
Zhu M, Noma Y, Mizuno A, Sano T, Shima K. Poor capacity for proliferation of pancreatic beta-cells in Otsuka-Long-Evans-Tokushima Fatty rat: a model of spontaneous NIDDM. Diabetes 1996;45:941-6.  Back to cited text no. 100
    
101.
Kosegawa I, Chen S, Awata T, Negishi K, Katayama S. Troglitazone and metformin, but not glibenclamide, decrease blood pressure in Otsuka Long Evans Tokushima Fatty rats. Clin Exp Hypertens 1999;21:199-211.  Back to cited text no. 101
    
102.
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;50:2521-9.  Back to cited text no. 102
    
103.
Wechsler-Zangen S, Orlanski E, Zangen DH. Cohen diabetic rat. In: Shafrir E, editor. Animal Models of Diabetes, Frontiers in Research. Boca Raton, FL: CRC Press; 2007. p. 323-34.  Back to cited text no. 103
    
104.
Goto Y, Kakizaki M, Masaki N. Production of spontaneous diabetic rats by repetition of selective breeding. Tohoku J Exp Med 1976;119:85-90.  Back to cited text no. 104
    
105.
Picarel-Blanchot F, Berthelier C, Bailbé D, Portha B. Impaired insulin secretion and excessive hepatic glucose production are both early events in the diabetic GK rat. Am J Physiol 1996;271:E755-62.  Back to cited text no. 105
    
106.
Shinohara M, Masuyama T, Shoda T, Takahashi T, Katsuda Y, Komeda K, et al. A new spontaneously diabetic non-obese Torii rat strain with severe ocular complications. Int J Exp Diabetes Res 2000;1:89-100.  Back to cited text no. 106
    
107.
Shinohara M. Establishment and clinical features in spontaneously diabetic Torii rat. Open Diabetes J 2011;4:18-20.  Back to cited text no. 107
    
108.
Srinivasan K, Ramarao P. Animal models in type 2 diabetes research: an overview. Indian J Med Res 2007;125:451-72.  Back to cited text no. 108
[PUBMED]  Medknow Journal  
109.
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 Suppl 1:S125-9.  Back to cited text no. 109
    
110.
Reed MJ, Scribner KA. In-vivo and in-vitro models of type 2 diabetes in pharmaceutical drug discovery. Diabetes Obes Metab 1999;1:75-86.  Back to cited text no. 110
    
111.
Masiello P, Broca C, Gross R, Roye M, Manteghetti M, Hillaire-Buys D, et al. Experimental NIDDM: development of a new model in adult rats administered streptozotocin and nicotinamide. Diabetes 1998;47:224-9.  Back to cited text no. 111
    
112.
Larsen MO, Wilken M, Gotfredsen CF, Carr RD, Svendsen O, Rolin B. Mild streptozotocin diabetes in the Göttingen minipig. A novel model of moderate insulindeficiency and diabetes. Am J Physiol Endocrinol Metab 2002;282:E1342-51.  Back to cited text no. 112
    
113.
Kasiviswanath R, Ramesh A, Kumar KE. Hypoglycemic and antihyperglycemic effect of Gmelina asiatica LINN. in normal and in alloxan induced diabetic rats. Biol Pharm Bull 2005;28:729-32.  Back to cited text no. 113
    
114.
Le Marchand-Brustel Y. Molecular mechanisms of insulin action in normal and insulin-resistant states. Exp Clin Endocrinol Diabetes 1999;107:126-32.  Back to cited text no. 114
    
115.
Le Marchand-Brustel Y, Jeanrenaud B, Freychet P. Insulin binding and effects in isolated soleus muscle of lean and obese mice. Am J Physiol 1978;234:E348-58.  Back to cited text no. 115
    
116.
Karasawa H, Takaishi K, Kumagae Y. Obesity-induced diabetes in mouse strains treated with gold thioglucose: a novel animal model for studying ß-cell dysfunction. Obesity (Silver Spring) 2011;19:514-21.  Back to cited text no. 116
    
117.
Bonner-Weir S, Trent DF, Weir GC. Partial pancreatectomy in the rat and subsequent defect in glucose-induced insulin release. J Clin Invest 1983;71:1544-53.  Back to cited text no. 117
    
118.
Choi SB, Park CH, Choi MK, Jun DW, Park S. Improvement of insulin resistance and insulin secretion by water extracts of Cordyceps militaris, Phellinus linteus, and Paecilomyces tenuipes in 90% pancreatectomized rats. Biosci Biotechnol Biochem 2004;68:2257-64.  Back to cited text no. 118
    
119.
Luft R. Oskar Minkowski: discovery of the pancreatic origin of diabetes, 1889. Diabetologia 1989;32:399-401.  Back to cited text no. 119
    
120.
Kurup S, Bhonde RR. Combined effect of nicotinamide and streptozotocin on diabetic status in partially pancreatectomized adult BALB/c mice. Horm Metab Res 2000;32:330-4.  Back to cited text no. 120
    
121.
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;47:212-24.  Back to cited text no. 121
    
122.
Noda K, Melhorn MI, Zandi S, Frimmel S, Tayyari F, Hisatomi T, et al. An animal model of spontaneous metabolic syndrome: Nile grass rat. FASEB J 2010;24:2443-53.  Back to cited text no. 122
    
123.
Surwit RS, Kuhn CM, Cochrane C, McCubbin JA, Feinglos MN. Diet-induced type II diabetes in C57BL/6J mice. Diabetes 1988;37:1163-7.  Back to cited text no. 123
    
124.
Heled Y, Shapiro Y, Shani Y, Moran DS, Langzam L, Braiman L, et al. Physical exercise prevents the development of type 2 diabetes mellitus in Psammomys obesus. Am J Physiol Endocrinol Metab 2002;282:E370-5.  Back to cited text no. 124
    
125.
Coscun T, Chen Y, Sindelar D, Heiman M. Animal models to study obesity and type 2 diabetes induced by diet. In: Shafrir E, editor. Animal Models of Diabetes, Frontiers of Research. Boca Raton, FL: CRC Press; 2007. p. 349-57.  Back to cited text no. 125
    
126.
Ziv E, Shafrir E, Kalman R, Galer S, Bar-On H. Changing pattern of prevalence of insulin resistance in Psammomys obesus, a model of nutritionally induced type 2 diabetes. Metabolism 1999;48:1549-54.  Back to cited text no. 126
    
127.
Marquié G, Hadjiisky P, Arnaud O, Duhault J. Development of macroangiopathy in sand rats (Psammomys obesus), an animal model of non-insulin-dependent diabetes mellitus: effect of gliclazide. Am J Med 1991 24;90:55S-61.  Back to cited text no. 127
    
128.
Matveyenko AV, Butler PC. Islet amyloid polypeptide (IAPP) transgenic rodents as models for type 2 diabetes. ILAR J 2006;47:225-33.  Back to cited text no. 128
    
129.
Matveyenko AV, Gurlo T, Daval M, Butler AE, Butler PC. Successful versus failed adaptation to high-fat diet-induced insulin resistance: the role of IAPP-induced beta-cell endoplasmic reticulum stress. Diabetes 2009;58:906-16.  Back to cited text no. 129
    
130.
Ueda H, Ikegami H, Yamato E, Fu J, Fukuda M, Shen G, et al. The NSY mouse: a new animal model of spontaneous NIDDM with moderate obesity. Diabetologia 1995;38:503-8.  Back to cited text no. 130
    
131.
Henson MS, O'Brien TD. Feline models of type 2 diabetes mellitus. ILAR J 2006;47:234-42.  Back to cited text no. 131
    
132.
Hansen BC, Tigno XF. The rhesus monkey (Macaca mulatta) manifestsall the features of human type 2 diabetes. In: Shafrir E, editor. Animal Models of Diabetes, Frontiers in Research. Boca Raton, FL: CRC Press; 2007. p. 251-70.  Back to cited text no. 132
    
133.
Kim SY, Johnson MA, McLeod DS, Alexander T, Hansen BC, Lutty GA. Neutrophils are associated with capillary closure in spontaneously diabetic monkey retinas. Diabetes 2005;54:1534-42.  Back to cited text no. 133
    
134.
Tsukasa H, Kazuya K, Masao K, Yuichi S. Non-insulin-dependent diabetic rat. EP0491396; 1992.  Back to cited text no. 134
    
135.
Jongil K, Soonhee K, Jeongsun S. A transgenic nonhuman animal model for diabetes. EP 0712930; 1996.  Back to cited text no. 135
    
136.
Walter CS, Maynard DC, David KK. Transgenic animal models for type II diabetes mellitus. US6187991; 2001.  Back to cited text no. 136
    
137.
Luthman LH, Joakim LG. Congenic animal models of non-insulin dependent diabetes mellitus. EP1228094; 2002.  Back to cited text no. 137
    
138.
Fumitoshi I, Naoki M, Tomoko I, Minesuke Y, Shigeharu W. Mammalian model for diabetes. US 20040128707; 2004.  Back to cited text no. 138
    
139.
Helena E, Rubins N, Steneberg P, Michael DW. New diabetes type 2 animal model. EP1659860; 2006.  Back to cited text no. 139
    
140.
Rebecca ST, Edward HK, Joan FF, Dennis LG. Non-human animal models for diabetic complications and their uses. WO2006021006; 2006.  Back to cited text no. 140
    
141.
Lernmark A, Niklasson B. Diabetes model. EP1432990; 2008.  Back to cited text no. 141
    
142.
Hiromichi Y, Kunie M, Hiroshi S, Kenji K. Diabetes model animal. US20090217394; 2009.  Back to cited text no. 142
    
143.
Hitoshi S, Nobuhiro Y. Nonhuman transgenic animal as type 2 diabetes model. US20090320147; 2009.  Back to cited text no. 143
    
144.
Itsuki O, Masahiko S, Susumu M. Production of congenic mouse model of human type 2 diabetes. JP4588808; 2010.  Back to cited text no. 144
    
145.
Chengxin S, Yuying F, Xinzhi L. A vertical type 2 diabetes mellitus the animal model claims a method for the screening of reducing blood sugar application in the medicine CN102812921; 2012.  Back to cited text no. 145
    
146.
Chen Y, Cheng J, Lu Y, Liu J, Li Xi, Yang G, et al. A method for preparing rhesus non insulin dependent diabetes mellitus model. CN103314925; 2013.  Back to cited text no. 146
    
147.
Wang X, Hai C. High selenium-induced insulin resistance animal models, its application and construction method. CN103211834; 2013.  Back to cited text no. 147
    
148.
Danilova IG, Gette IF, Bulavintseva TS. Method for simulating alloxan diabetes. RU2534411; 2014.  Back to cited text no. 148
    
149.
Yang S, Kong S, Ruan J, Xin L, Li K. Diabetes mouse model using gene HSD11B1, CHOP and IAPP expression vectors. CN103966243; 2014.  Back to cited text no. 149
    
150.
Lan G, Yang H, Jiang Q, Guo Y, Chen J, Liang J. A method for preparing model of mini pig with non insulin dependent diabetes mellitus. CN103858820; 2014.  Back to cited text no. 150
    
151.
Schuele R, Duteil D, Metzger E, Guenther T. Animal models for type 2 diabetes and obesity having reduced LSD1 expression as well as transgenic animals over expressing human LSD1 gene. WO2014068033; 2014.  Back to cited text no. 151
    
152.
Eldridge JA, Campaigne WC. Diabetic animal model for diabetes research. WO 2014028737; 2014.  Back to cited text no. 152
Advanced Biomedical Research
Volume 2015, May
May 2015
Pages 1-14