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Evolution of Metabolic and Renal Changes in the ZDF/Drt-Fa Rat Model of Type II Diabetes1’2

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Evolution of Metabolic and Renal Changes in the ZDF/Drt-Fa Rat Model of Type II Diabetes1’2 Evolution of Metabolic and Renal Changes in the ZDF/Drt-fa Rat Model of Type II Diabetes1’2 Jiten P. Vora, Stephanie M. Zimsen, Donald C. Houghton, and Sharon Anderson3 utility of this model for study of diabetic renal disease J.P. Vora, SM. Zimsen, S. Anderson, Division of Nephrol- Is compromised by the ubiquitous presence of other, ogy, Hypertension, and Clinical Pharmacology, De- nondlabetic renal lesions. partment of Medicine, Oregon Health Sciences Uni- Key Words: Albuminuria. hyperinsulinemia. pyelonophritis. hy- versity, Portland. OR, and Portland Veterans Administration Medical Center, Portland, OR dronephrosis. hyperilpidemia D.C. Houghton. Division of Anatomical Pathology. De- U nderstanding of the pathophysiobogy of renal partment of Pathology, Oregon Health Sciences Uni- disease In non-insulin- dependent diabetes mel- versity, Portland, OR litus (NIDDM) has been hampered by the lack of appropriate animal models of the disease. Over a (J. Am. Soc. Nephrol. 1996; 7:113-117) dozen putative models have been reported (1), but many are not truly representative of the human dis- ABSTRACT ease. For example, some models exhibit only mild hyperglycemia, whereas others do not develop any Studies of the pathophysiology of renal disease In renal manifestations. In most of these models, evolu- non-insulin-dependent diabetes mellitus (NIDDM) tion of diabetic nephropathic changes has not been have been hindered by the lack of an appropriate examIned (1). experimental model. We examined the natural history The partially Inbred Zucker Diabetic Fatty Rat of metabolic and renal changes in the partially in- (ZDF/Drt-fa) is a relatively new model that more bred Zucker Diabetic Falfy Rat (ZDF/Drt-fa), a model closely mimics the metabolic status of human MDDM that closely mimics the metabolic abnormalities of (2,3). DerIved from a few Zucker rats In which unusu- NIDDM. Lean nondiabetic fl#ermates served as con- ally high blood glucose levels developed, this strain trols. Body weights in the obese rats were higher has been selectively inbred for more than 16 genera- initially, but thereafter stabilized at values similar to tions (3). Affected obese males routinely develop stable those in lean controls. Blood glucose levels rose to hyperglycemia, and have been reported to exhibit diabetic neuropathy (4). Serum insulin levels are ini- overtly hyperglycemic levels in the obese group, tially high, but then decline as pancreatic 13cells cease stabilizing in the 300 to 400 mg/dL range. Serum to respond to the glucose stimulus (5). Accordingly, we insulin, cholesterol, and triglyceride levels were all sought to determine whether this strain might provide elevated in the obese group, though insulin levels an appropriate model of diabetic nephropathy. declined later in life. Values for systolic blood pressure rose slightly with age in both groups, but remained METHODS within the normal range, and did not differ between Longitudinal studies were performed in 20 obese male groups. Urinary albumin excretion values were higher ZDF/Drt-fa rats, obtained at the age of 5 wk from Genetic In the obese group at all time points, and rose pro- Models, Inc. (Indianapolis, IN). An addItional 20 male lean littermates served as controls. When unexpected changes gressively throughout the study. Morphologic exami- were found in rats followed to 40 wk of age (discussed below), nation revealed the presence of severe hydronephro- additional groups were obtained and followed to 12 (N = 9 sis in almost all animals, affecting lean as well as each) and 16 (N = 7 to 9) wk of age, to determine the timing obese rats. In some cases, complications were found, and onset of these abnormalities. All rats were fed tap water including tubular dilation, necrotizing granulomas, and Purina Rodent Chow 5008 (Ralston Purina, Richmond, inflammatory changes, and pyelonephritis, some of IN), containIng 6.5% fat, ad llbttum. The experimental proto- cols were approved by the Institutional Animal Care and Use which were fungal. Accordingly, the ZDF/Drt-fa rat Conunittee. appears to be an excellent model of the metabolic Blood glucose (BG) levels in tail venous blood were moni- changes that characterize NIDDM. Unfortunately, the tored weekly until the development of hyperglycemia, and then monthly thereafter. Monthly measurements were also 1 Received March 13, 1995. Accepted August 29. 1995. made of systolic blood pressure (SBP) by the conscious 2Poons of these studies were presented at the 1993 Annual Meeting of the tail-cuff method, body weight. and 24-h urinary albumin American Society of Nephrology, and published In abstract form (J Am Soc excretion value. Animals were followed until 40 wk of age. at Nephroi 1993;4:807). which time they were anesthetized with mactin (Research 3correspondence to Dr. S. Anderson, Div. of Nephroiogy and Hypertension Biochernicahs, Natick, MA; 100 mg/kg ip). Blood was taken in PP262, Oregon Health Sciences UniversIty, 3314 SW. U.S. Veterans Hospital Rd., non-fasting conditions for determination of serum glycosy- Portland, OR 97201. lated hemoglobin, insulin, cholesterol, and triglyceride lev- 10466673/0701-01 13103.00/0 Journal of the American Society of Nephrology els, after which the kidneys were fixed by perfusion for 5 mm Copyright © 1996 by the American Society of Nephroiogy at a pressure of 120mm Hg wIth 1.25% glutaraldehyde in 0.1 Journal of the American Society of Nephrology 113 Natural History of the ZDF/Drt-fa Diabetic Model M sodium cacodylate buffer (pH 7.4). After perfusion-fixa- tion, kidneys were immersed In the same fixative for 24 h and 600A then rinsed in Tyrodes solution for another 24 h. A series of 3 mm-thick transverse sections from each kidney were pro- 400 cessed and embedded in paraffin for light microscopy. Two to 4 micron-thIck sections were stained with periodic acid- 200 0 Schiff stain and examined by light microscopy. Incidence of hydronephrosis, tubular dilation, and focal and segmental glomerular sclerosis (FSGS) were assessed semiquantita- 500 B * tively. by using a score ranging from 0 (no lesions) to 3 .. 400 (extensive lesions). Specifically, the grading scale used was: 0 300 = absent/normal; 1 = minimal, few instances seen through- , 200 out the sections; 2 = moderate, instances easily found, most 10 areas normal; 3 = extensive, instances found In nearly all 400X fields. For hydronephrosis, the following criteria were used: 0 = normal (finger-in-glove configuration of the papilla 160 C and calyx); 1 = minimal (a narrow but definable fluid-ifiled 120 calyceal space with normal papillary contour): 2 = moderate (unequivocal dilatation of the calyx. with compression of the 80 papifia. but with preservation of its conical shape); 3 = a- w 40 marked (gross distension of the calyx, typically increasing (I, overall volume of the kidney by at least 50%. and resulting in 0 severe compression of the lateral cortex and distortion of the * 500 D papifia). ‘S Urinary albumin concentration was determined using a specific ELISA assay (Nephrat. Exocell, Inc., Philadelphia, 1 300 PA). Glycosylated hemoglobin was determined by afilnity w 200 * * column chromatography (Glyco-Gel B, Pierce Chemical Co., :: 100 Rockford, IL). Serum cholesterol and triglyceride levels were measured by enzymatic colorimetric methods (Cholesterol 6- * and Triglyceride GPO-Trlnder kits, Sigma Diagnostics. St. 4- Louis, MO) by using a centrifugal analyzer (Cobas#{174}-Bio. Roche Analytical Instruments. Inc., Nutley. NJ). Serum in- 2- sulin levels were measured by radioimmunoassay (Rat Insu- 0 lin RIA Kit, Linco Research, Inc., St. Louis, MO). Results are 6812162024283236 presented as means ± SE. Comparisons between lean and Age (weeks) obese groups were performed by repeated measures analysis of variance, followed by Tukey’s comparisons or the Mann- Figure 1. Serial measurements of (A) body weight. (B) blood Whitney test, as appropriate. Statistical significance was glucose. (C) systolic blood pressure (SBP), and (D) 24-h defined as P < 0.05. urinary albumin excretion (UAE), in nondiabetic lean (D) and diabetic obese () rats. Note the break in the scale in RESULTS Figure 1D. Values are means ± SE. * P < 0.05 versus lean at same time point. By 6 wk of age, the characteristic changes in body habitus that occur in obese rat strains were already apparent, and body weight was higher in the obese triglyceride (410 ± 43 versus 33 ± 2 mg/dL, P < group (lean, 138 ± 4 g; obese. 177 ± 5 g; each N 10: 0.00 1) levels, as compared with lean rats. By 36 wk of P < 0.01). Blood glucose levels (lean, 77 ± 3 mg/dL; age, serum cholesterol (423 ± 28 versus 106 ± 3 obese 82 ± 3 mg/dL; each N = 10; P>0.05) confirmed mg/dL, P < 0.00 1) and triglyceride (969 ± 157 versus that hyperglycemia was not yet present. Subsequent 74 ± 12 mg/dL, P < 0.00 1)levels remained elevated in changes in body weight, blood glucose level, systolic the obese diabetic rats. Though hyperglycemia was blood pressure, and albuminuria are summarized in sustaIned in the obese group, serum insulin levels Figure 1. Body weights remained higher in the obese were no longer different from those in lean control rats diabetic group during the first six months of age, but (48 ± 3 obese versus 96 ± 14 .tU/mL, NS). Systolic thereafter both groups were stable and body weights blood pressures were within the normal range in both converged (Figure 1A). Blood glucose levels were com- groups throughout the time course. They rose slightly parable in the two groups of rats at 8 wk of age. but with aging In both groups, but did not differ between thereafter uniformly rose to overtly hyperglycemic lev- groups (Figure 1C). Values for 24-h urinary albumin els in the obese diabetic group (Figure 1B). Other excretion in obese diabetic rats were slightly, though metabolic characteristics of NIDDM were apparent, as significantly, higher than those in the lean rats at 6 wk well.
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