Islet cell hyperexpression of HLA class I antigens: a defining feature in type 1 diabetes

Diabetologia

Volumn 59, Issue 11, 2016, Pages 2448-2458

  Richardson, Sarah J ^a   Rodriguez Calvo, Teresa ^b   Gerling, Ivan C ^c   Mathews, Clayton E ^d   Kaddis, John S ^e   Russell, Mark A ^a   Zeissler, Marie ^a   Leete, Pia ^a   Krogvold, Lars ^f,g   Dahl Jørgensen, Knut ^f,g   von Herrath, Matthias ^b   Pugliese, Alberto ^h   Atkinson, Mark A ^d   Morgan, Noel G ^a  

^a UNIVERSITY OF EXETER MEDICAL SCHOOL   (United Kingdom)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

^e CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^f OSLO UNIVERSITY HOSPITAL   (Norway)

^g UNIVERSITY OF OSLO   (Norway)

^h UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

DiViD; HLA class I; HLA F; Islet cell; nPOD; Pancreas; STAT1; Type 1 diabetes

Indexed keywords

BETA 2 MICROGLOBULIN; HLA A ANTIGEN; HLA ANTIGEN CLASS 1; HLA B ANTIGEN; HLA C ANTIGEN; HLA F ANTIGEN; INSULIN; NLR FAMILY CARD DOMAIN CONTAINING 5; PROTEIN; STAT1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETIC PATIENT; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; INSULIN DEPENDENT DIABETES MELLITUS; LASER CAPTURE MICRODISSECTION; PANCREAS ISLET CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA EXTRACTION; UPREGULATION; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; METABOLISM; PANCREAS; PANCREAS ISLET; PATHOLOGY;

DIABETES MELLITUS, TYPE 1; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOHISTOCHEMISTRY; IN VITRO TECHNIQUES; INSULIN; ISLETS OF LANGERHANS; MALE; PANCREAS; STAT1 TRANSCRIPTION FACTOR;

EID: 84981244952     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-016-4067-4     Document Type: Article

References (43)

1. Atkinson MA (2012) The pathogenesis and natural history of type 1 diabetes. Cold Spring Harb Perspect Med 2:2:a007641
2. Atkinson MA, Eisenbarth GS, Michels AW (2014) Type 1 diabetes. Lancet 383:69–82
3. Patterson CC, Dahlquist GG, Gyurus E, Green A, Soltesz G, Group ES (2009) Incidence trends for childhood type 1 diabetes in Europe during 1989-2003 and predicted new cases 2005-20: a multicentre prospective registration study. Lancet 373:2027–2033
4. Foulis AK, Liddle CN, Farquharson MA, Richmond JA, Weir RS (1986) The histopathology of the pancreas in type 1 (insulin-dependent) diabetes mellitus: a 25-year review of deaths in patients under 20 years of age in the United Kingdom. Diabetologia 29:267–274
5. Campbell-Thompson M (2015) What can organ donor specimens tell us about type 1 diabetes? Pediatr Diabetes 16:320–330
6. Campbell-Thompson M, Wasserfall C, Kaddis J et al (2012) Network for Pancreatic Organ Donors with Diabetes (nPOD): developing a tissue biobank for type 1 diabetes. Diabetes Metab Res Rev 28:608–617
7. Krogvold L, Edwin B, Buanes T et al (2014) Pancreatic biopsy by minimal tail resection in live adult patients at the onset of type 1 diabetes: experiences from the DiViD study. Diabetologia 57:841–843
8. In’t Veld P (2011) Insulitis in human type 1 diabetes: the quest for an elusive lesion. Islets 3:131–138
9. Richardson SJ, Morgan NG, Foulis AK (2014) Pancreatic pathology in type 1 diabetes mellitus. Endocr Pathol 25:80–92
10. Arif S, Leete P, Nguyen V et al (2014) Blood and islet phenotypes indicate immunological heterogeneity in type 1 diabetes. Diabetes 63:3835–3845
11. Willcox A, Richardson SJ, Bone AJ, Foulis AK, Morgan NG (2009) Analysis of islet inflammation in human type 1 diabetes. Clin Exp Immunol 155:173–181
12. Morgan NG, Leete P, Foulis AK, Richardson SJ (2014) Islet inflammation in human type 1 diabetes mellitus. IUBMB Life 66:723–734
13. Gomez-Tourino I, Arif S, Eichmann M, Peakman M (2015) T cells in type 1 diabetes: instructors, regulators and effectors: a comprehensive review. J Autoimmun 66:7–16
14. Coppieters KT, Dotta F, Amirian N et al (2012) Demonstration of islet-autoreactive CD8 T cells in insulitic lesions from recent onset and long-term type 1 diabetes patients. J Exp Med 209:51–60
15. Foulis AK, Farquharson MA, Hardman R (1987) Aberrant expression of class II major histocompatibility complex molecules by B cells and hyperexpression of class I major histocompatibility complex molecules by insulin containing islets in type 1 (insulin-dependent) diabetes mellitus. Diabetologia 30:333–343
16. Bottazzo GF, Dean BM, McNally JM, MacKay EH, Swift PG, Gamble DR (1985) In situ characterization of autoimmune phenomena and expression of HLA molecules in the pancreas in diabetic insulitis. N Engl J Med 313:353–360
17. Pujol-Borrell R, Todd I, Doshi M, Gray D, Feldmann M, Bottazzo GF (1986) Differential expression and regulation of MHC products in the endocrine and exocrine cells of the human pancreas. Clin Exp Immunol 65:128–139
18. Skog O, Korsgren S, Wiberg A et al (2014) Expression of human leukocyte antigen class I in endocrine and exocrine pancreatic tissue at onset of type 1 diabetes. Am J Pathol 185:129–138
19. Kaddis JS, Pugliese A, Atkinson MA (2015) A run on the biobank: what have we learned about type 1 diabetes from the nPOD tissue repository? Curr Opin Endocrinol Diabetes Obes 22:290–295
20. Pugliese A, Vendrame F, Reijonen H, Atkinson MA, Campbell-Thompson M, Burke GW (2014) New insight on human type 1 diabetes biology: nPOD and nPOD-transplantation. Curr Diab Rep 14:530
21. Krogvold L, Edwin B, Buanes T et al (2015) Detection of a low-grade enteroviral infection in the islets of Langerhans of living patients newly diagnosed with type 1 diabetes. Diabetes 64:1682–1687
22. Rodriguez-Calvo T, Suwandi JS, Amirian N et al (2015) Heterogeneity and lobularity of pancreatic pathology in type 1 diabetes during the prediabetic phase. J Histochem Cytochem 63:626–636
23. Marselli L, Sgroi DC, Bonner-Weir S, Weir GC (2009) Laser capture microdissection of human pancreatic β-cells and RNA preparation for gene expression profiling. Methods Mol Biol 560:87–98
24. Wu J, Kakoola DN, Lenchik NI, Desiderio DM, Marshall DR, Gerling IC (2012) Molecular phenotyping of immune cells from young NOD mice reveals abnormal metabolic pathways in the early induction phase of autoimmune diabetes. PLoS One 7, e46941
25. Wu Z, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F (2004) A model-based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 99:909–917
26. Quackenbush J (2002) Microarray data normalization and transformation. Nat Genet 32(Suppl):496–501
27. Irizarry RA, Hobbs B, Collin et al (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249–264
28. Horton R, Gibson R, Coggill P et al (2008) Variation analysis and gene annotation of eight MHC haplotypes: the MHC Haplotype Project. Immunogenetics 60:1–18
29. Krogvold L, Wiberg A, Edwin B et al (2015) Insulitis and characterisation of infiltrating T cells in surgical pancreatic tail resections from patients at onset of type 1 diabetes. Diabetologia 59:492–501
30. Leete P, Willcox A, Krogvold L et al (2016) Differential insulitic profiles determine the extent of β-cell destruction and the age of onset of type 1 diabetes. Diabetes 65:1362–1369
31. Meissner TB, Li A, Biswas A et al (2010) NLR family member NLRC5 is a transcriptional regulator of MHC class I genes. Proc Natl Acad Sci U S A 107:13794–13799
32. Wainwright SD, Biro PA, Holmes CH (2000) HLA-F is a predominantly empty, intracellular, TAP-associated MHC class Ib protein with a restricted expression pattern. J Immunol 164:319–328
33. Goodridge JP, Burian A, Lee N, Geraghty DE (2010) HLA-F complex without peptide binds to MHC class I protein in the open conformer form. J Immunol 184:6199–6208
34. Goodridge JP, Lee N, Burian A et al (2013) HLA-F and MHC-I open conformers cooperate in a MHC-I antigen cross-presentation pathway. J Immunol 191:1567–1577
35. Foulis AK, Farquharson MA, Meager A (1987) Immunoreactive α-interferon in insulin-secreting β cells in type 1 diabetes mellitus. Lancet 2:1423–1427
36. Devendra D, Eisenbarth GS (2004) Interferon alpha—a potential link in the pathogenesis of viral-induced type 1 diabetes and autoimmunity. Clin Immunol 111:225–233
37. Thomas HE, Parker JL, Schreiber RD, Kay TW (1998) IFN-gamma action on pancreatic beta cells causes class I MHC upregulation but not diabetes. J Clin Investig 102:1249–1257
38. von Herrath MG, Oldstone MB (1997) Interferon-γ is essential for destruction of beta cells and development of insulin-dependent diabetes mellitus. J Exp Med 185:531–539
39. Foulis AK (1996) The pathology of the endocrine pancreas in type 1 (insulin-dependent) diabetes mellitus. APMIS 104:161–167
40. Richardson SJ, Willcox A, Bone AJ, Morgan NG, Foulis AK (2011) Immunopathology of the human pancreas in type-I diabetes. Semin Immunopathol 33:9–21
41. Eizirik DL, Moore F, Flamez D, Ortis F (2008) Use of a systems biology approach to understand pancreatic β-cell death in Type 1 diabetes. Biochem Soc Trans 36:321–327
42. Marroqui L, Dos Santos RS, Floyel T et al (2015) TYK2, a candidate gene for type 1 diabetes, modulates apoptosis and the innate immune response in human pancreatic β-cells. Diabetes 64:3808–3817
43. Moore F, Naamane N, Colli ML et al (2011) STAT1 is a master regulator of pancreatic β-cell apoptosis and islet inflammation. J Biol Chem 286:929–941