Abstract
The immunopathology of type 1 diabetes (T1D) has proved difficult to study in man because of the limited availability of appropriate samples, but we now report a detailed study charting the evolution of insulitis in human T1D. Pancreas samples removed post-mortem from 29 patients (mean age 11.7 years) with recent-onset T1D were analysed by immunohistochemistry. The cell types constituting the inflammatory infiltrate within islets (insulitis) were determined in parallel with islet insulin content. CD8(+) cytotoxic T cells were the most abundant population during insulitis. Macrophages (CD68(+)) were also present during both early and later insulitis, although in fewer numbers. CD20(+) cells were present in only small numbers in early insulitis but were recruited to islets as beta cell death progressed. CD138(+) plasma cells were infrequent at all stages of insulitis. CD4(+) cells were present in the islet infiltrate in all patients but were less abundant than CD8(+) or CD68(+) cells. Forkhead box protein P3(+) regulatory T cells were detected in the islets of only a single patient. Natural killer cells were detected rarely, even in heavily inflamed islets. The results suggest a defined sequence of immune cell recruitment in human T1D. They imply that both CD8(+) cytotoxic cells and macrophages may contribute to beta cell death during early insulitis. CD20(+) cells are recruited in greatest numbers during late insulitis, suggesting an increasing role for these cells as insulitis develops. Natural killer cells and forkhead box protein P3(+) T cells do not appear to be required for beta cell death.
MeSH Terms
Adolescent
Child
Child, Preschool
Diabetes Mellitus, Type 1/immunology,metabolism,pathology
Disease Progression
Female
Humans
Infant
Insulin/analysis
Insulin-Secreting Cells/immunology,pathology
Islets of Langerhans/chemistry,immunology,pathology
Killer Cells, Natural/immunology
Male
Pancreatitis/immunology,pathology
Plasma Cells/immunology
T-Lymphocytes, Regulatory/immunology
Young Adult
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Willcox A
Institute of Biomedical and Clinical Sciences, Peninsula Medical School, Tamar Science Park, Plymouth, UK.
Richardson S J
Bone A J
Foulis A K
Morgan N G
References (28)
28 references, click to expand
-
Coxsackie B4 virus infection of beta cells and natural killer cell insulitis in recent-onset type 1 diabetic patients.
Proc Natl Acad Sci U S A. 2007 Mar 20;104(12):5115-20
PMID: 17360338
-
Fas and Fas ligand expression in inflamed islets in pancreas sections of patients with recent-onset Type I diabetes mellitus.
Diabetologia. 1999 Nov;42(11):1332-40
PMID: 10550417
-
Human natural killer cells.
Blood. 2008 Aug 1;112(3):461-9
PMID: 18650461
-
Cellular and molecular pathogenesis of type 1A diabetes.
Cell Mol Life Sci. 2007 Apr;64(7-8):865-72
PMID: 17429581
-
C. L. Oakley lecture (1987). The pathogenesis of beta cell destruction in type I (insulin-dependent) diabetes mellitus.
J Pathol. 1987 Jul;152(3):141-8
PMID: 3309229
-
B-cells promote intra-islet CD8+ cytotoxic T-cell survival to enhance type 1 diabetes.
Diabetes. 2008 Apr;57(4):909-17
PMID: 18184927
-
Identification of tissue-infiltrating lymphocytes expressing PEN5, a mucin-like glycoprotein selectively expressed on natural killer cells.
Am J Pathol. 1995 Feb;146(2):409-18
PMID: 7531954
-
Beta cells are responsible for CXCR3-mediated T-cell infiltration in insulitis.
Nat Med. 2002 Dec;8(12):1414-20
PMID: 12415259
-
Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production.
Int Immunol. 2007 Apr;19(4):345-54
PMID: 17329235
-
Natural history of beta-cell function in type 1 diabetes.
Diabetes. 2005 Dec;54 Suppl 2:S32-9
PMID: 16306337
-
Increased number of islet-associated macrophages in type 2 diabetes.
Diabetes. 2007 Sep;56(9):2356-70
PMID: 17579207
-
Natural killer cell signaling pathways.
Science. 2004 Nov 26;306(5701):1517-9
PMID: 15567854
-
Apoptosis and disease progression in the spontaneously diabetic BB/S rat.
Diabetologia. 2001 Mar;44(3):320-4
PMID: 11317663
-
Phenotypic difference of normal plasma cells from mature myeloma cells.
Blood. 1993 May 15;81(10):2658-63
PMID: 8490175
-
Mononuclear cell infiltration and its relation to the expression of major histocompatibility complex antigens and adhesion molecules in pancreas biopsy specimens from newly diagnosed insulin-dependent diabetes mellitus patients.
J Clin Invest. 1993 Nov;92(5):2313-22
PMID: 8227346
-
Lessons on autoimmune diabetes from animal models.
Clin Sci (Lond). 2006 Jun;110(6):627-39
PMID: 16689681
-
The natural history of lymphocyte subsets infiltrating the pancreas of NOD mice.
Diabetologia. 1989 May;32(5):282-9
PMID: 2666213
-
Imbalance in Th cell polarization and its relevance in type 1 diabetes mellitus.
Rev Diabet Stud. 2005 Winter;2(4):182-6
PMID: 17491692
-
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. 1987 May;30(5):333-43
PMID: 3301484
-
In situ characterization of autoimmune phenomena and expression of HLA molecules in the pancreas in diabetic insulitis.
N Engl J Med. 1985 Aug 8;313(6):353-60
PMID: 3159965
-
Macrophage infiltration precedes and is a prerequisite for lymphocytic insulitis in pancreatic islets of pre-diabetic BB rats.
Diabetologia. 1989 Feb;32(2):126-34
PMID: 2656351
-
Immune cell infiltration, cytokine expression, and beta-cell apoptosis during the development of type 1 diabetes in the spontaneously diabetic LEW.1AR1/Ztm-iddm rat.
Diabetes. 2005 Jul;54(7):2041-52
PMID: 15983205
-
The target tissue in autoimmunity--an influential niche.
Eur J Immunol. 2007 Mar;37(3):589-97
PMID: 17301949
-
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. 1986 May;29(5):267-74
PMID: 3522324
-
Analysis of FOXP3 protein expression in human CD4+CD25+ regulatory T cells at the single-cell level.
Eur J Immunol. 2005 Jun;35(6):1681-91
PMID: 15902688
-
Mechanisms of pancreatic beta-cell death in type 1 and type 2 diabetes: many differences, few similarities.
Diabetes. 2005 Dec;54 Suppl 2:S97-107
PMID: 16306347
-
Pancreatic islets under attack: cellular and molecular effectors.
Curr Pharm Des. 2007;13(7):749-60
PMID: 17346189
-
Natural history of type 1 diabetes.
Diabetes. 2005 Dec;54 Suppl 2:S25-31
PMID: 16306336