publication . Article . Other literature type . 2018

The Role of NOD Mice in Type 1 Diabetes Research: Lessons from the Past and Recommendations for the Future

Chen, Yi-Guang; Mathews, Clayton E.; Driver, John P.;
Open Access English
  • Published: 01 Feb 2018 Journal: Frontiers in Endocrinology, volume 9 (eissn: 1664-2392, Copyright policy)
  • Publisher: Frontiers Media S.A.
Abstract
For more than 35 years, the NOD mouse has been the primary animal model for studying autoimmune diabetes. During this time, striking similarities to the human disease have been uncovered. In both species, unusual polymorphisms in a major histocompatibility complex (MHC) class II molecule confer the most disease risk, disease is caused by perturbations by the same genes or different genes in the same biological pathways and that diabetes onset is preceded by the presence of circulating autoreactive T cells and autoantibodies that recognize many of the same islet antigens. However, the relevance of the NOD model is frequently challenged due to past failures transl...
Subjects
free text keywords: Endocrinology, Perspective, NOD mouse, type 1 diabetes, preclinical, congenic, genetics, gene editing, Diseases of the endocrine glands. Clinical endocrinology, RC648-665, Internal medicine, medicine.medical_specialty, medicine, Insulitis, medicine.disease, Antigen, Immune system, Nod, Disease, Autoantibody, Biology, Immunology, NOD mice
Funded by
NIH| Genetic engineering of the Idd3 type 1 diabetes locus
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R21AI110963-01
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| Mechanistic and Therapeutic Role of the CD137-CD137L Axis in Type 1 Diabetes
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R01DK107541-01A1
  • Funding stream: NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES
,
NIH| Genetic Regulation of Human Beta Cell Destruction
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1UC4DK104194-01
  • Funding stream: NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES
,
NIH| Administrative Core
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5P01AI042288-17
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| A new genetic approach to identify the Idd9.3 type 1 diabetes susceptibility gene
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R21AI125879-02
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
138 references, page 1 of 10

1 Melanitou E Devendra D Liu E Miao D Eisenbarth GS. Early and quantal (by litter) expression of insulin autoantibodies in the nonobese diabetic mice predict early diabetes onset. J Immunol (2004) 173:6603–10.10.4049/jimmunol.173.11.6603 15557150 [OpenAIRE] [PubMed] [DOI]

2 You S Belghith M Cobbold S Alyanakian MA Gouarin C Barriot S Autoimmune diabetes onset results from qualitative rather than quantitative age-dependent changes in pathogenic T-cells. Diabetes (2005) 54:1415–22.10.2337/diabetes.54.5.1415 15855328 [OpenAIRE] [PubMed] [DOI]

3 Gregori S Giarratana N Smiroldo S Adorini L. Dynamics of pathogenic and suppressor T cells in autoimmune diabetes development. J Immunol (2003) 171:4040–7.10.4049/jimmunol.171.8.4040 14530324 [OpenAIRE] [PubMed] [DOI]

4 Pugliese A Autoreactive T cells in type 1 diabetes. J Clin Invest (2017) 127:2881–91.10.1172/JCI94549 28762987 [OpenAIRE] [PubMed] [DOI]

5 Regnell SE LernmarkÅ. Early prediction of autoimmune (type 1) diabetes. Diabetologia (2017) 60:1370–81.10.1007/s00125-017-4308-1 28550517 [OpenAIRE] [PubMed] [DOI]

6 Wester A Skärstrand H Lind A Ramelius A Carlsson A Cedervall E An increased diagnostic sensitivity of truncated GAD65 autoantibodies in type 1 diabetes may be related to HLA-DQ8. Diabetes (2017) 66:735–40.10.2337/db16-0891 28028075 [OpenAIRE] [PubMed] [DOI]

7 Katsarou A Gudbjörnsdottir S Rawshani A Dabelea D Bonifacio E Anderson BJ Type 1 diabetes mellitus. Nat Rev Dis Primers (2017) 3:17016.10.1038/nrdp.2017.16 28358037 [PubMed] [DOI]

8 Mathews CE Xue S Posgai A Lightfoot YL Li X Lin A Acute versus progressive onset of diabetes in NOD mice: potential implications for therapeutic interventions in type 1 diabetes. Diabetes (2015) 64:3885–90.10.2337/db15-0449 26216853 [OpenAIRE] [PubMed] [DOI]

9 DiLorenzo TP Graser RT Ono T Christianson GJ Chapman HD Roopenian DC Major histocompatibility complex class I-restricted T cells are required for all but the end stages of diabetes development in nonobese diabetic mice and use a prevalent T cell receptor alpha chain gene rearrangement. Proc Natl Acad Sci U S A (1998) 95:12538–43.10.1073/pnas.95.21.12538 9770521 [OpenAIRE] [PubMed] [DOI]

10 Campbell-Thompson M Fu A Kaddis JS Wasserfall C Schatz DA Pugliese A Insulitis and β-cell mass in the natural history of type 1 diabetes. Diabetes (2016) 65:719–31.10.2337/db15-0779 26581594 [OpenAIRE] [PubMed] [DOI]

11 Driver JP Chen YG Mathews CE. Comparative genetics: synergizing human and NOD mouse studies for identifying genetic causation of type 1 diabetes. Rev Diabet Stud (2012) 9:169–87.10.1900/RDS.2012.9.169 23804259 [OpenAIRE] [PubMed] [DOI]

12 Uchigata Y Okada T Gong JS Yamada Y Iwamoto Y Tanaka M A mitochondrial genotype associated with the development of autoimmune-related type 1 diabetes. Diabetes Care (2002) 25:2106 10.2337/diacare.25.11.2106 [OpenAIRE] [DOI]

13 Mathews CE Leiter EH Spirina O Bykhovskaya Y Gusdon AM Ringquist S mt-Nd2 Allele of the ALR/Lt mouse confers resistance against both chemically induced and autoimmune diabetes. Diabetologia (2005) 48:261–7.10.1007/s00125-004-1644-8 15692809 [OpenAIRE] [PubMed] [DOI]

14 Onengut-Gumuscu S Chen WM Burren O Cooper NJ Quinlan AR Mychaleckyj JC Fine mapping of type 1 diabetes susceptibility loci and evidence for colocalization of causal variants with lymphoid gene enhancers. Nat Genet (2015) 47:381–6.10.1038/ng.3245 25751624 [OpenAIRE] [PubMed] [DOI]

15 Vijayakrishnan L Slavik JM Illes Z Greenwald RJ Rainbow D Greve B An autoimmune disease-associated CTLA-4 splice variant lacking the B7 binding domain signals negatively in T cells. Immunity (2004) 20:563–75.10.1016/S1074-7613(04)00110-4 15142525 [OpenAIRE] [PubMed] [DOI]

138 references, page 1 of 10
Abstract
For more than 35 years, the NOD mouse has been the primary animal model for studying autoimmune diabetes. During this time, striking similarities to the human disease have been uncovered. In both species, unusual polymorphisms in a major histocompatibility complex (MHC) class II molecule confer the most disease risk, disease is caused by perturbations by the same genes or different genes in the same biological pathways and that diabetes onset is preceded by the presence of circulating autoreactive T cells and autoantibodies that recognize many of the same islet antigens. However, the relevance of the NOD model is frequently challenged due to past failures transl...
Subjects
free text keywords: Endocrinology, Perspective, NOD mouse, type 1 diabetes, preclinical, congenic, genetics, gene editing, Diseases of the endocrine glands. Clinical endocrinology, RC648-665, Internal medicine, medicine.medical_specialty, medicine, Insulitis, medicine.disease, Antigen, Immune system, Nod, Disease, Autoantibody, Biology, Immunology, NOD mice
Funded by
NIH| Genetic engineering of the Idd3 type 1 diabetes locus
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R21AI110963-01
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| Mechanistic and Therapeutic Role of the CD137-CD137L Axis in Type 1 Diabetes
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1R01DK107541-01A1
  • Funding stream: NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES
,
NIH| Genetic Regulation of Human Beta Cell Destruction
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 1UC4DK104194-01
  • Funding stream: NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES
,
NIH| Administrative Core
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5P01AI042288-17
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| A new genetic approach to identify the Idd9.3 type 1 diabetes susceptibility gene
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R21AI125879-02
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
138 references, page 1 of 10

1 Melanitou E Devendra D Liu E Miao D Eisenbarth GS. Early and quantal (by litter) expression of insulin autoantibodies in the nonobese diabetic mice predict early diabetes onset. J Immunol (2004) 173:6603–10.10.4049/jimmunol.173.11.6603 15557150 [OpenAIRE] [PubMed] [DOI]

2 You S Belghith M Cobbold S Alyanakian MA Gouarin C Barriot S Autoimmune diabetes onset results from qualitative rather than quantitative age-dependent changes in pathogenic T-cells. Diabetes (2005) 54:1415–22.10.2337/diabetes.54.5.1415 15855328 [OpenAIRE] [PubMed] [DOI]

3 Gregori S Giarratana N Smiroldo S Adorini L. Dynamics of pathogenic and suppressor T cells in autoimmune diabetes development. J Immunol (2003) 171:4040–7.10.4049/jimmunol.171.8.4040 14530324 [OpenAIRE] [PubMed] [DOI]

4 Pugliese A Autoreactive T cells in type 1 diabetes. J Clin Invest (2017) 127:2881–91.10.1172/JCI94549 28762987 [OpenAIRE] [PubMed] [DOI]

5 Regnell SE LernmarkÅ. Early prediction of autoimmune (type 1) diabetes. Diabetologia (2017) 60:1370–81.10.1007/s00125-017-4308-1 28550517 [OpenAIRE] [PubMed] [DOI]

6 Wester A Skärstrand H Lind A Ramelius A Carlsson A Cedervall E An increased diagnostic sensitivity of truncated GAD65 autoantibodies in type 1 diabetes may be related to HLA-DQ8. Diabetes (2017) 66:735–40.10.2337/db16-0891 28028075 [OpenAIRE] [PubMed] [DOI]

7 Katsarou A Gudbjörnsdottir S Rawshani A Dabelea D Bonifacio E Anderson BJ Type 1 diabetes mellitus. Nat Rev Dis Primers (2017) 3:17016.10.1038/nrdp.2017.16 28358037 [PubMed] [DOI]

8 Mathews CE Xue S Posgai A Lightfoot YL Li X Lin A Acute versus progressive onset of diabetes in NOD mice: potential implications for therapeutic interventions in type 1 diabetes. Diabetes (2015) 64:3885–90.10.2337/db15-0449 26216853 [OpenAIRE] [PubMed] [DOI]

9 DiLorenzo TP Graser RT Ono T Christianson GJ Chapman HD Roopenian DC Major histocompatibility complex class I-restricted T cells are required for all but the end stages of diabetes development in nonobese diabetic mice and use a prevalent T cell receptor alpha chain gene rearrangement. Proc Natl Acad Sci U S A (1998) 95:12538–43.10.1073/pnas.95.21.12538 9770521 [OpenAIRE] [PubMed] [DOI]

10 Campbell-Thompson M Fu A Kaddis JS Wasserfall C Schatz DA Pugliese A Insulitis and β-cell mass in the natural history of type 1 diabetes. Diabetes (2016) 65:719–31.10.2337/db15-0779 26581594 [OpenAIRE] [PubMed] [DOI]

11 Driver JP Chen YG Mathews CE. Comparative genetics: synergizing human and NOD mouse studies for identifying genetic causation of type 1 diabetes. Rev Diabet Stud (2012) 9:169–87.10.1900/RDS.2012.9.169 23804259 [OpenAIRE] [PubMed] [DOI]

12 Uchigata Y Okada T Gong JS Yamada Y Iwamoto Y Tanaka M A mitochondrial genotype associated with the development of autoimmune-related type 1 diabetes. Diabetes Care (2002) 25:2106 10.2337/diacare.25.11.2106 [OpenAIRE] [DOI]

13 Mathews CE Leiter EH Spirina O Bykhovskaya Y Gusdon AM Ringquist S mt-Nd2 Allele of the ALR/Lt mouse confers resistance against both chemically induced and autoimmune diabetes. Diabetologia (2005) 48:261–7.10.1007/s00125-004-1644-8 15692809 [OpenAIRE] [PubMed] [DOI]

14 Onengut-Gumuscu S Chen WM Burren O Cooper NJ Quinlan AR Mychaleckyj JC Fine mapping of type 1 diabetes susceptibility loci and evidence for colocalization of causal variants with lymphoid gene enhancers. Nat Genet (2015) 47:381–6.10.1038/ng.3245 25751624 [OpenAIRE] [PubMed] [DOI]

15 Vijayakrishnan L Slavik JM Illes Z Greenwald RJ Rainbow D Greve B An autoimmune disease-associated CTLA-4 splice variant lacking the B7 binding domain signals negatively in T cells. Immunity (2004) 20:563–75.10.1016/S1074-7613(04)00110-4 15142525 [OpenAIRE] [PubMed] [DOI]

138 references, page 1 of 10
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publication . Article . Other literature type . 2018

The Role of NOD Mice in Type 1 Diabetes Research: Lessons from the Past and Recommendations for the Future

Chen, Yi-Guang; Mathews, Clayton E.; Driver, John P.;