A model of type 2 diabetes in the Guinea pig using sequential dietinduced glucose intolerance and streptozotocin treatment

DMM Disease Models and Mechanisms

Volumn 10, Issue 2, 2017, Pages 151-162

  Podell, Brendan K ^a   Ackart, David F ^a   Richardson, Michael A ^a   DiLisio, James E ^a   Pulford, Bruce ^a   Basaraba, Randall J ^a  

^a Veterinary Dentistry and Oral Surgery   (United States)

Author keywords

Animal model; Glucose intolerance; Guinea pig; Insulin independent diabetes; Streptozotocin; Type 2 diabetes

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR BLOCKING AGENT; GLIPIZIDE; INSULIN; METFORMIN; RECOMBINANT HUMAN INSULIN; STREPTOZOCIN; ANTIDIABETIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE DIET; CELL LOSS; CONTROLLED STUDY; CYTOTOXICITY; DIABETOGENESIS; DISEASE ASSOCIATION; DYSLIPIDEMIA; FEMALE; GUINEA PIG; HYPERINSULINEMIA; IMPAIRED GLUCOSE TOLERANCE; INSULIN BLOOD LEVEL; LIPID DIET; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL HYPERPLASIA; PRIORITY JOURNAL; STEATOSIS; WEIGHT GAIN; ANIMAL; CELL DEATH; COMPLICATION; DIET; DISEASE MODEL; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; FEEDING BEHAVIOR; GLUCOSE INTOLERANCE; HYPERGLYCEMIA; HYPERINSULINISM; HYPERPLASIA; METABOLISM; ORAL DRUG ADMINISTRATION; PATHOLOGY; SURVIVAL ANALYSIS;

ADMINISTRATION, ORAL; ADRENERGIC ALPHA-2 RECEPTOR ANTAGONISTS; ANIMALS; CELL DEATH; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DIET; DIETARY CARBOHYDRATES; DISEASE MODELS, ANIMAL; DYSLIPIDEMIAS; FEEDING BEHAVIOR; FEMALE; GLUCOSE INTOLERANCE; GUINEA PIGS; HYPERGLYCEMIA; HYPERINSULINISM; HYPERPLASIA; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN-SECRETING CELLS; STREPTOZOCIN; SURVIVAL ANALYSIS; WEIGHT GAIN;

EID: 85012124605     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.025593     Document Type: Article

References (71)

1. Aomine, M., Nobe, S. and Arita, M. (1990). The making of diabetic guinea pigs by streptozotocin and high incidence of triggered activity in the ventricular muscle. Jpn. J. Physiol. 40, 651-663.
2. Ar'Rajab, A. and Ahren, B. (1991). Effects of yohimbine and nicotinic acid on insulin secretion in islet transplanted streptozotocin-diabetic rats. Diabetes Res. Clin. Pract. 11, 81-87.
3. Aslan, M., Ozcan, F. and Kucuksayan, E. (2013). Increased small dense LDL and decreased paraoxonase enzyme activity reveals formation of an atherogenic risk in streptozotocin-induced diabetic guinea pigs. J. Diabetes Res. 2013, 860190.
4. Beagley, J., Guariguata, L., Weil, C. and Motala, A. A. (2014). Global estimates of undiagnosed diabetes in adults. Diabetes Res. Clin. Pract. 103, 150-160.
5. Bell,R.H., Jr. and Hye, R. J.(1983). Animal modelsofdiabetes mellitus: physiology and pathology. J. Surg. Res. 35, 433-460.
6. Bell,G.I., Kayano, T., Buse,J. B., Burant, C. F., Takeda,J., Lin, D., Fukumoto, H. and Seino, S. (1990). Molecular biology of mammalian glucose transporters. Diabetes Care 13, 198-208.
7. Bruning, J. C., Winnay, J., Bonner-Weir, S., Taylor, S. I., Accili, D. and Kahn, C. R. (1997). Development of a novel polygenic model of NIDDM in mice heterozygous for IR and IRS-1 null alleles. Cell 88, 561-572.
8. Butler, A. E., Janson, J., Bonner-Weir, S., Ritzel, R., Rizza, R. A. and Butler, P. C. (2003). Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52, 102-110.
9. Butler, P. C., Meier, J. J., Butler, A. E. and Bhushan, A. (2007). The replication of beta cells in normal physiology, in disease and for therapy. Nat. Clin. Pract. Endocrinol. Metab. 3, 758-768.
10. Ceylan-Isik, A. F., LaCour, K. H. and Ren, J. (2006). Sex difference in cardiomyocyte function in normal and metallothionein transgenic mice: the effect of diabetes mellitus. J. Appl. Physiol. 100, 1638-1646.
11. Chan, S. J., Episkopou, V., Zeitlin, S., Karathanasis, S. K., MacKrell, A., Steiner, D. F. and Efstratiadis, A. (1984). Guinea pig preproinsulin gene: an evolutionary compromise? Proc. Natl. Acad. Sci. USA 81, 5046-5050.
12. de la Garza-Rodea, A. S., Knaan-Shanzer, S., den Hartigh, J. D., Verhaegen, A. P. and van Bekkum, D. W. (2010). Anomer-equilibrated streptozotocin solution for the induction of experimental diabetesin mice (Mus musculus). J. Am. Assoc. Lab. Anim. Sci. 49, 40-44.
13. Elsner, M., Guldbakke, B., Tiedge, M., Munday, R. and Lenzen, S. (2000). Relative importance of transport and alkylation for pancreatic beta-cell toxicity of streptozotocin. Diabetologia 43, 1528-1533.
14. Ensign, W. Y., McNamara, D. J. and Fernandez, M. L. (2002). Exercise improves plasma lipid profiles and modifies lipoprotein composition in guinea pigs. J. Nutr. Biochem. 13, 747-753.
15. Fernandez, M. L. and Volek, J. S. (2006). Guinea pigs: a suitable animal model to study lipoprotein metabolism, atherosclerosis and inflammation. Nutr. Metab. 3, 17.
16. Fernandez, M. L., Wilson, T. A., Conde, K., Vergara-Jimenez, M. and Nicolosi, R. J. (1999). Hamsters and guinea pigs differ in their plasma lipoprotein cholesterol distribution when fed diets varying in animal protein, soluble fiber, or cholesterol content. J. Nutr. 129, 1323-1332.
17. Ferrannini, E., Gastaldelli, A., Miyazaki, Y., Matsuda, M., Mari, A. and DeFronzo, R. A. (2005). beta-Cell function in subjects spanning the range from normal glucose tolerance to overt diabetes: a new analysis. J. Clin. Endocrinol. Metab. 90, 493-500.
18. Garofano, A., Czernichow, P. and Breant, B. (2000). Impaired beta-cell regeneration in perinatally malnourished rats: a study with STZ. FASEB J. 14, 2611-2617.
19. Griffiths, M. (1948). The mechanism of the hypoglycemic action of alloxan. Aust. J. Exp. Biol. Med. Sci. 26, 339-346.
20. Guariguata, L., Whiting, D. R., Hambleton, I., Beagley, J., Linnenkamp, U. and Shaw, J. E. (2014). Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res. Clin. Pract. 103, 137-149.
21. Gurley, S. B., Clare, S. E., Snow, K. P., Hu, A., Meyer, T. W. and Coffman, T. M. (2006). Impact of genetic background on nephropathy in diabetic mice. Am. J. Physiol. Renal Physiol. 290, F214-F222.
22. Haughton, C. L., Dillehay, D. L. and Phillips, L. S. (1999). Insulin replacement therapy for the rat model of streptozotocin-induced diabetes mellitus. Lab. Anim. Sci. 49, 639-644.
23. Hegde, K. R., Henein, M. G. and Varma, S. D. (2003). Establishment of mouse as an animal model for study of diabetic cataracts: biochemical studies. Diab. Obes. Metab. 5, 113-119.
24. Hickey, A. J. (2011). Guinea pig model of infectious disease - viral infections. Curr. Drug Targets 12, 1018-1023.
25. Hootman, S. R., Jones, J. E., Kapoor, R., Nguyen, K.-L. and de Ondarza, J. (1998). Sodium, potassium-activated adenosine triphosphatase activity is impaired in the guinea pig pancreatic duct system in streptozotocin-induced diabetes. Biochem. Biophys. Res. Commun. 243, 869-873.
26. Hosokawa, M., Dolci, W. and Thorens, B. (2001). Differential sensitivityof GLUT1-and GLUT2-expressing beta cells to streptozotocin. Biochem. Biophys. Res. Commun. 289, 1114-1117.
27. International Diabetes Federation (2015). Diabetes Atlas, 7th ed. Brussels, Belgium.
28. Islam, M. S. and Loots, D. T. (2009). Experimental rodent models of type 2 diabetes: a review. Methods Find Exp. Clin. Pharmacol. 31, 249.
29. Islam, M. S. and Wilson, R. D. (2012). Experimentally induced rodent models of type 2 diabetes. Methods Mol. Biol. 933, 161-174.
30. Jansson, L. and Sandler, S. (1985). Pancreatic islet circulation in relation to the diabetogenic action of streptozotocin in the rat. Endocrinology 116, 896-900.
31. Jones, H. B., Nugent, D. and Jenkins, R. (2010). Variation in characteristics of islets of Langerhans in insulin-resistant, diabetic and non-diabetic-rat strains. Int. J. Exp. Pathol. 91, 288-301.
32. Kahn, S. E. (2001). Clinical review 135: The importance of beta-cell failure in the development and progression of type 2 diabetes. J. Clin. Endocrinol. Metab. 86, 4047-4058.
33. Kitamura, T. (2013). The role of FOXO1 in beta-cell failure and type 2 diabetes mellitus. Nat. Rev. Endocrinol. 9, 615-623.
34. Klein, R., Engerman, R. L. and Ernest, J. T. (1980). Fluorophotometry. II. Streptozocin-treated guinea pigs. Arch. Ophthalmol. 98, 2233-2234.
35. Kushner, B., Lazar, M., Furman, M., Lieberman, T. W. and Leopold, I. H. (1969). Resistance of rabbits and guinea pigs to the diabetogenic effect of streptozotocin. Diabetes 18, 542-544.
36. Lenzen, S. (2007). Alloxan and streptozotocin diabetes. In Time Structures of Endocrine Systems (ed. E. Peschke), pp. 119-138. Stuttgart.
37. Lenzen, S. (2008). The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia 51, 216-226.
38. LePard, K. J. (2005). Choline acetyltransferase and inducible nitric oxide synthase are increased in myenteric plexus of diabetic guinea pig. Auton. Neurosci. 118, 12-24.
39. Lim, E. L., Hollingsworth, K. G., Aribisala, B. S., Chen, M. J., Mathers, J. C. and Taylor, R. (2011). Reversal of type 2 diabetes: normalisation of beta cell function in association with decreased pancreas and liver triacylglycerol. Diabetologia 54, 2506-2514.
40. Losert, W., Rilke, A., Loge, O. and Richter, K. D. (1971). [Comparative biochemical study on the diabetogenic effect of streptozotocin in mice, rats, Chinese hamsters and guinea pigs]. Arzneim-Forsch. 21, 1643-1653.
41. Madsen, C. S., Janovitz, E., Zhang, R., Van Nguyen-Tran, V., Ryan, C. S., Yin, X., Monshizadegan, H., Chang, M., D'Arienzo, C., Scheer, S. et al. (2008). The Guinea pig as a preclinical model for demonstrating the efficacy and safety of statins. J. Pharmacol. Exp. Ther. 324, 576-586.
42. Maimon, J., Mauro, M., Gorray, K. C. and Schneider, B. S. (1991). Synthetic guinea pig insulin B-chain C-terminal decapeptide: a novel immunogen for generating immunocytochemical-grade antisera. J. Histochem. Cytochem. 39, 1571-1574.
43. Mazza, A., Fruci, B., Garinis, G. A., Giuliano, S., Malaguarnera, R. and Belfiore, A. (2012). The role of metformin in the management of NAFLD. Exp. Diabetes Res. 2012, 716404.
44. Movassat, J., Saulnier, C. and Portha, B. (1997). Insulin administration enhances growth of the beta-cell mass in streptozotocin-treated newborn rats. Diabetes 46, 1445-1452.
45. Nakadate, T., Nakaki, T., Muraki, T. and Kato, R. (1981). Adrenergic receptors and the onset of streptozotocin-induced diabetes in mice. Eur. J. Pharmacol. 75, 45-51.
46. Ordway, D. J., Shanley, C. A., Caraway, M. L., Orme, E. A., Busy, D. S., Hascal-Dove, L., Henao-Tamayo, M., Harton, M. R., Shang, S., Ackart, D., Kraft, S. L., Lenaerts, A. J., Basaraba, R. J. and Orme, I. M. (2010). Evaluation of standard chemotherapy in the guinea pig model of tuberculosis. Antimicrob. Agents Chemother. 54, 1820-1833.
47. Padilla-Carlin,D.J., McMurray,D. N. and Hickey,A.J. (2008). The guinea pigasa model of infectious diseases. Comp. Med. 58, 324-340.
48. Podell, B. K., Ackart, D. F., Kirk, N. M., Eck, S. P., Bell, C. and Basaraba, R. J. (2012). Non-diabetic hyperglycemia exacerbates disease severity in Mycobacterium tuberculosis infected guinea pigs. PLoS ONE 7, e46824
49. Qi, Z., Fujita, H., Jin, J., Davis, L. S., Wang, Y., Fogo, A. B. and Breyer, M. D. (2005). Characterization of susceptibility of inbred mouse strains to diabetic nephropathy. Diabetes 54, 2628-2637.
50. Rahier, J., Guiot, Y., Goebbels, R. M., Sempoux, C. and Henquin, J. C. (2008). Pancreatic beta-cell mass in European subjects with type 2 diabetes. Diabetes Obes. Metab. 10 Suppl. 4, 32-42.
51. Reaven, G. M. and Ho, H. (1991). Low-dose streptozotocin-induced diabetes in the spontaneously hypertensive rat. Metabolism 40, 335-337.
52. Reed, M. J., Meszaros, K., Entes, L. J., Claypool, M. D., Pinkett, J. G., Gadbois, T. M. and Reaven, G. M. (2000). A new rat model of type 2 diabetes: the fat-fed, streptozotocin-treated rat. Metabolism 49, 1390-1394.
53. Rees, D. A. and Alcolado, J. C. (2005). Animal models of diabetes mellitus. Diabet. Med. 22, 359-370.
54. Remais, J. V., Zeng, G., Li, G., Tian, L. and Engelgau, M. M. (2013). Convergence of non-communicable and infectious diseases in low- and middle-income countries. Int. J. Epidemiol. 42, 221-227.
55. Rosengren, A. H., Jokubka, R., Tojjar, D., Granhall, C., Hansson, O., Li, D.-Q., Nagaraj, V., Reinbothe, T. M., Tuncel, J., Eliasson, L. et al. (2010). Overexpression of alpha2A-adrenergic receptors contributes to type 2 diabetes. Science 327, 217-220.
56. Saidullah, B., Muralidhar, K. and Fahim, M. (2014). Onset of diabetes modulates the airway smooth muscle reactivity of guinea pigs: role of epithelial mediators. J. Smooth Muscle Res. 50, 29-38.
57. Savontaus, E., Fagerholm, V., Rahkonen, O. and Scheinin, M. (2008). Reduced blood glucose levels, increased insulin levels and improved glucose tolerance in alpha2A-adrenoceptor knockout mice. Eur. J. Pharmacol. 578, 359-364.
58. Schlosser, M. J., Kapeghian, J. C. and Verlangieri, A. J. (1984). Effects of streptozotocin in the male guinea pig: a potential animal model for studying diabetes. Life Sci. 35, 649-655.
59. Schlosser, M. J., Kapeghian, J. C. and Verlangieri, A. J. (1987). Selected physical and biochemical parameters in the streptozotocin-treated guinea pig: insights into the diabetic guinea pig model. Life Sci. 41, 1345-1353.
60. Schnedl, W. J., Ferber, S., Johnson, J. H. and Newgard, C. B. (1994). STZ transport and cytotoxicity: specific enhancement in GLUT2-expressing cells. Diabetes 43, 1326-1333.
61. Shoelson, S. E., Lee, J. and Goldfine, A. B. (2006). Inflammation and insulin resistance. J. Clin. Invest. 116, 1793-1801.
62. Skovsø, S. (2014). Modeling type 2 diabetes in rats using high fat diet and streptozotocin. J. Diabetes Investig. 5, 349-358.
63. Srinivasan, K. and Ramarao, P. (2007). Animal models in type 2 diabetes research: an overview. Ind. J. Med. Res. 125, 451-472.
64. Surwit, R. S., Kuhn, C. M., Cochrane, C., McCubbin, J. A. and Feinglos, M. N. (1988). Diet-induced type II diabetes in C57BL/6J mice. Diabetes 37, 1163-1167.
65. Taylor, R. (2013). Type 2 diabetes: etiology and reversibility. Diabetes Care 36, 1047-1055.
66. Tocchetti, C. G., Stanley, B. A., Sivakumaran, V., Bedja, D., O'Rourke, B., Paolocci, N., Cortassa, S.and Aon, M.A.(2015). Impaired mitochondrialenergy supply coupled to increased H2O2 emission under energy/redox stress leads to myocardial dysfunction during Type I diabetes. Clin. Sci. 129, 561-574.
67. Wehner, H. and Majorek, B. (1975). Early glomerular changes in streptozotocin diabetes of the guinea pig. Virchows Arch. 368, 179-189.
68. Weir, G. C. and Bonner-Weir, S. (2013). Islet beta cell mass in diabetes and how it relates to function, birth, and death. Ann. N. Y. Acad. Sci. 1281, 92-105.
69. West, K. L. and Fernandez, M. L. (2004). Guinea pigs as models to study the hypocholesterolemic effects of drugs. Cardiovasc. Drug Rev. 22, 55-70.
70. Xie, C., Biary, N., Tocchetti, C. G., Aon, M. A., Paolocci, N., Kauffman, J. and Akar, F. G. (2013). Glutathione oxidation unmasks proarrhythmic vulnerability of chronically hyperglycemic guinea pigs. Am. J. Physiol. Heart Circ. Physiol. 304, H916-H926.
71. Ye, P., Cheah, I. K. and Halliwell, B. (2013). High fat diets and pathology in the guinea pig. Atherosclerosis or liver damage? Biochim. Biophys. Acta 1832, 355-364.