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Thymectomy and Radiation-Induced Type 1 Diabetes in Nonlymphopenic BB Rats Sheela Ramanathan,1,2,3 Marie-Therese Bihoreau,4 Andrew D

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Thymectomy and Radiation-Induced Type 1 Diabetes in Nonlymphopenic BB Rats Sheela Ramanathan,1,2,3 Marie-Therese Bihoreau,4 Andrew D Thymectomy and Radiation-Induced Type 1 Diabetes in Nonlymphopenic BB Rats Sheela Ramanathan,1,2,3 Marie-Therese Bihoreau,4 Andrew D. Paterson,5 Leili Marandi,1,2,3 Dominique Gauguier,4 and Philippe Poussier1,2,3 Spontaneous type 1 diabetes in BB rats is dependent on It remains unclear when and how this peripheral T- the RT1u MHC haplotype and homozygosity for an allele lymphopenia contributes to the development of diabetes, at the Lyp locus, which is responsible for a peripheral although its contribution is likely multifactorial. T-lymphopenia. Genetic studies have shown that there Our understanding of the pathogenic role of the BBDP are other, as yet unidentified, genetic loci contributing T-lymphopenia is further complicated by the demonstra- to diabetes susceptibility in this strain. BB rats carrying tion that autoimmune diabetes can develop in nonlym- wild-type Lyp alleles are not lymphopenic and are resis- tant to spontaneous diabetes (DR). Here we show that phopenic BBDR rats, a strain that is genetically related to thymectomy and exposure to one sublethal dose of BBDP rats (6,7; www-genome.wi.mit.edu/rat/public/). ␥-irradiation (TX-R) at 4 weeks of age result in the BBDR rats are not lymphopenic and do not develop rapid development of insulitis followed by diabetes in diabetes when maintained in a specific pathogen–free ؉ ؊ 100% of DR rats. Administration of CD4 45RC T-cells (SPF) environment (8). Although there is Ͼ15% genetic from unmanipulated, syngeneic donors immediately af- polymorphism between BBDP and BBDR rats (www- ter irradiation prevents the disease. Splenic T-cells genome.wi.mit.edu/rat/public/), spontaneous diabetes co- from TX-R–induced diabetic animals adoptively transfer type 1 diabetes to T-deficient recipients. ACI, WF, WAG, segregates as a single gene with the T-lymphopenia BN, LEW, PVG, and PVG.RT1u strains are resistant to between these two lines (9). Experimental induction of a TX-R–induced insulitis/diabetes. Genetic analyses re- peripheral T-lymphopenia in BBDR rats, through the ad- vealed linkage between regions on chromosomes 1, 3, 4, ministration of a depleting monoclonal antibody, cyclo- 6, 9, and 16, and TX-R–induced type 1 diabetes in a phosphamide, or sublethal ␥-irradiation, is followed by the ؋ cohort of nonlymphopenic F2 (Wistar Furth BBDP) rapid development of diabetes in a conventional environ- animals. This novel model of TX-R–induced diabetes in nonlymphopenic BB rats can be used to identify envi- ment (10). However, diabetes can also occur in unmanipu- ronmental and cellular factors that are responsible for lated BBDR rats after infection with Kilham’s rat virus the initiation of antipancreatic autoimmunity. Diabetes (KRV), a single-stranded DNA parvovirus with no tropism 51:2975–2981, 2002 for ␤-cells, or injection of polyinosinic-polycytidylic acid (poly[I:C]), an interferon-␣–inducing agent (11,12). Induc- tion of diabetes by administration of poly(I:C) is observed he BioBreeding (BBDP) rat spontaneously devel- both in SPF conditions and in conventional environment ops a T-cell–mediated, autoimmune diabetic syn- (12,13). Importantly, susceptibility to these experimentally drome that is similar to that observed in NOD induced type 1 diabetic syndromes is not restricted to BB- mice and humans (1). Two of the diabetes sus- related strains as long as the animals are haploidentical to T BB rats at the MHC class II locus (12,14). This observation ceptibility loci of the BB rat have been identified, Iddm1, which maps to the Lyp locus on chromosome 4, and suggests that diabetes susceptibility alleles are widespread Iddm2, which maps to the MHC class II haplotype RT1u of among laboratory rats. this animal (2,3). The Lyp allele carried by the BBDP rat This interpretation is further supported by the dem- shortens the life span of naı¨ve T-cells, resulting in a 5- to onstration that another type 1 diabetic syndrome can 10-fold decrease in the number of peripheral T-cells (4,5). be induced in various strains of rats, including some that do not carry the RT1u MHC haplotype (15). Specif- From the 1Sunnybrook and Women’s College Health Sciences Centre, Univer- ically, adult thymectomy followed by four subsequent, sity of Toronto, Toronto, Ontario, Canada; the 2Department of Medicine, sublethal doses of ␥-irradiation (TX-R) given 2 weeks University of Toronto, Toronto, Ontario, Canada; the 3Department of Immu- apart results in the development of diabetes 10 weeks nology, University of Toronto, Toronto, Ontario, Canada; 4the Welcome Trust Centre for Human Genetics, University of Oxford, Oxford, U.K.; and the after irradiation. Strains susceptible to TX-R–induced 5Program in Genetics and Genomics Biology, Hospital for Sick Children, diabetes include PVG (RT1c), PVG (RT1u), WAG (RT1u), Toronto, Ontario, Canada. ϫ c/u Address correspondence and reprint requests to Philippe Poussier, Sunny- and (PVG WF)F1 (RT1 ) (15,16). Therefore, it seems brook and Women’s Health Sciences Centre, 2075 Bayview Ave., Room A3 38, that most of the experimentally induced type 1 diabetic Toronto, Ontario, Canada M4N 3M5. E-mail: [email protected]. syndromes require the BB rat MHC class II haplo- utoronto.ca. Received for publication 1 April 2002 and accepted in revised form 26 June type, but none requires the BB rat genetic background 2002. exclusively. Here we describe a novel model of experi- FACS, fluorescence-activated cell sorting; KRV, Kilham’s rat virus; mAb, monoclonal antibody; MNC, mononuclear cell; PE, phycoethrin; SPF, specific mentally induced diabetes that is restricted to nonlym- pathogen free; TX-R, ␥-irradiation; VAF, virus antibody free. phopenic, BB-related strains. DIABETES, VOL. 51, OCTOBER 2002 2975 THYMECTOMY AND RADIATION-INDUCED TYPE 1 DIABETES RESEARCH DESIGN AND METHODS TABLE 1 Animals. Diabetes-resistant BBDR and diabetes-prone BBDP rats were TX-R induces type 1 diabetes in nonlymphopenic rats with a BB purchased from BRM (Worchester, MA) and maintained in our colony under genetic background SPF and virus antibody–free (VAF) conditions. Specifically, all immunocom- petent sentinels remained serologically negative for the KRV as well as for Mean day other viruses (SDAV, Sendai, PVM, Reo3, TMEV, GDVII, MAD1, parvovirus, MHC Type 1 of onset and LCMV) during the course of the study. Diabetes-prone BB.7b rats that are Strain haplotype diabetes Insulitis after R congenic for the RT7b allele of rat CD45 were derived in our laboratory by u/u introducing the RT7b allele of Wistar Furth (WF) rats into BBDP rats, followed BBDR RT1 31/31 NA 28 Ϯ 6 u/u by Ͼ10 backcrosses to BBDP rats (17). The cumulative incidence of diabetes DR.Lyp/ϩ RT1 6/6 NA 34 Ϯ 5 u/u in BB.7b animals is similar to that observed in BBDP rats originating from the Non-lyp BB/W RT1 7/7 NA 31 Ϯ 3 BRM colony (data not shown). Nonlymphopenic and hence diabetes-resistant ACI RT1a/a 0/5 0/5 (nonlyp BB/W) rats have been generated by introgressing the wild-type Lyp RT1u/u 0/7 0/7 allele from BBDR into BBDP rats, followed by systematic backcrossing to BN RT1n/n 0/5 0/5 BBDP rats. Nonlyp BB/W animals used in this study were the progeny of the LEW RT1l/l 0/4 0/4 seventh backcross. Diabetes-prone and lymphopenic DR.Lyp/Lyp as well as PVG RT1c/c 0/4 0/4 Ϯ diabetes-resistant and nonlymphopenic DR.Lyp/ congenic lines were ob- RT1u/u 1/6 1/5 47 tained from Dr. A. Lernmark (Washington University, Seattle, WA) and have WAG RT1u/u 0/3 0/3 been previously described (9). Other rat strains were purchased from Harlan u/u u u WF RT1 0/9 0/9 Sprague-Dawley (Indianapolis, IN). ACI rats congenic for RT1 and ACI.1 .lyp u/u u (WF ϫ BBDP) RT1 7/8 1/1 48 Ϯ 8 rats congenic for both RT1 and the Lyp allele of BBDP rats have been u/u previously described (18). F and F rats were generated in our animal colony. (BBDP ϫ WF) RT1 4/4 NA 45 Ϯ 4 1 2 u/u Thymectomy, sham thymectomy, and whole-body irradiation of rats were (WF ϫ BBDR) RT1 6/16 5/10 37 Ϯ 1 performed as previously described (5). Rats were tested three times a week (WF ϫ DR.Lyp/ϩ) RT1u/u 8/11 0/3 35 Ϯ 5 for the presence of glycosuria and ketonuria. Once the animals became (ACI.1* ϫ BBDR) RT1u/u 0/4 0/4 glycosuric, the diagnosis of type 1 diabetes was made on the basis of (ACI.1u ϫ BBDR) RT1u/u 0/5 0/5 hyperglycemia (blood glucose Ͼ16.7 mmol/l) for two consecutive days. Diabetic rats were treated with subcutaneous implants of insulin (Linplant; *Insulitis in nondiabetic animals. NA, not applicable. University of Toronto, ON, Canada). After the rats were killed, pancreas, lung, kidney, and liver were fixed in 10% formalin for histology. All of the animal protocols were approved by the Animal Care Committee of our institution. noted. Probabilities were independently confirmed using ANOVA. Basically, it Monoclonal antibodies, three-color immunofluorescence, and fluores- is an ANOVA test followed by permutation tests that provide exact signifi- cence-activated cell sorter analysis. The monoclonal antibodies (mAbs) cance thresholds for each pair of genotype/phenotype, regardless of the used in this study have been previously described (5). Suspensions of MNC phenotype distribution in the cross. This method that is therefore particularly were incubated with a biotinylated mAb, followed by streptavidin-phycoethrin appropriate for nonparametric analyses was developed by Churchill and (PE)/Texas Red Tandem. PE-labeled and FITC-conjugated mAbs were then Doerge (22) and was used recently by Martin et al.
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