Abstract
The cytoarchitecture of human islets has been examined, focusing on cellular associations that provide the anatomical framework for paracrine interactions. By using confocal microscopy and multiple immunofluorescence, we found that, contrary to descriptions of prototypical islets in textbooks and in the literature, human islets did not show anatomical subdivisions. Insulin-immunoreactive beta cells, glucagon-immunoreactive alpha cells, and somatostatin-containing delta cells were found scattered throughout the human islet. Human beta cells were not clustered, and most (71%) showed associations with other endocrine cells, suggesting unique paracrine interactions in human islets. Human islets contained proportionally fewer beta cells and more alpha cells than did mouse islets. In human islets, most beta, alpha, and delta cells were aligned along blood vessels with no particular order or arrangement, indicating that islet microcirculation likely does not determine the order of paracrine interactions. We further investigated whether the unique human islet cytoarchitecture had functional implications. Applying imaging of cytoplasmic free Ca2+ concentration, [Ca2+]i, we found that beta cell oscillatory activity was not coordinated throughout the human islet as it was in mouse islets. Furthermore, human islets responded with an increase in [Ca2+]i when lowering the glucose concentration to 1 mM, which can be attributed to the large contribution of alpha cells to the islet composition. We conclude that the unique cellular arrangement of human islets has functional implications for islet cell function.
MeSH Terms
Animals
Female
Humans
Islets of Langerhans/chemistry,cytology,physiology
Macaca fascicularis
Male
Mice
Microscopy, Confocal
Microscopy, Fluorescence
Middle Aged
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Cabrera Over
Diabetes Research Institute, Miller School of Medicine, University of Miami, Miami, FL 33136, USA.
Berman Dora M
Kenyon Norma S
Ricordi Camillo
Berggren Per-Olof
Caicedo Alejandro
References (27)
27 references, click to expand
-
Cellular composition of the human diabetic pancreas.
Diabetologia. 1983 May;24(5):366-71
PMID: 6347784
-
Quantitation of endocrine cell content in the pancreas of nondiabetic and diabetic humans.
Diabetes. 1982 Aug;31(8 Pt 1):694-700
PMID: 6131002
-
A new, simple method for cold storage of the pancreas using perfluorochemical.
Transplantation. 1988 Sep;46(3):457-60
PMID: 3047936
-
Islet amyloid, increased A-cells, reduced B-cells and exocrine fibrosis: quantitative changes in the pancreas in type 2 diabetes.
Diabetes Res. 1988 Dec;9(4):151-9
PMID: 3073901
-
Three-dimensional imaging of intact isolated islets of Langerhans with confocal microscopy.
Diabetes. 1989 Jun;38(6):808-14
PMID: 2656348
-
Glucose-induced oscillations of intracellular Ca2+ concentration resembling bursting electrical activity in single mouse islets of Langerhans.
FEBS Lett. 1989 Dec 18;259(1):19-23
PMID: 2689228
-
Islets of Langerhans: the puzzle of intraislet interactions and their relevance to diabetes.
J Clin Invest. 1990 Apr;85(4):983-7
PMID: 1969425
-
A morphological and immunohistochemical investigation of endocrine pancreata from obese ob+/ob+ mice.
Acta Histochem. 1991;90(1):93-101
PMID: 1675542
-
Widespread synchronous [Ca2+]i oscillations due to bursting electrical activity in single pancreatic islets.
Pflugers Arch. 1991 May;418(4):417-22
PMID: 1876486
-
Perfusion with anti-insulin gamma globulin indicates a B to A to D cellular perfusion sequence in the pancreas of the rhesus monkey, Macaca mulatta.
Pancreas. 1992;7(1):26-9
PMID: 1372978
-
Quantitative immunohistochemical changes in the endocrine pancreas of nonobese diabetic (NOD) mice.
Pancreas. 1995 Nov;11(4):396-401
PMID: 8532657
-
Microcirculation of the islets of Langerhans. Long Beach Veterans Administration Regional Medical Education Center Symposium.
Diabetes. 1996 Apr;45(4):385-92
PMID: 8603757
-
A comparative immunohistochemical study of pancreatic islets in laboratory animals (rats, dogs, minipigs, nonhuman primates).
Exp Toxicol Pathol. 1998 Jun;50(3):151-72
PMID: 9681646
-
Proportions of various endocrine cells in the pancreatic islets of wood mice (Apodemus speciosus).
Anat Histol Embryol. 1999 Mar;28(1):13-6
PMID: 10208028
-
Homologous and heterologous asynchronicity between identified alpha-, beta- and delta-cells within intact islets of Langerhans in the mouse.
J Physiol. 1999 May 15;517 ( Pt 1):85-93
PMID: 10226151
-
Long-term survival and function of intrahepatic islet allografts in rhesus monkeys treated with humanized anti-CD154.
Proc Natl Acad Sci U S A. 1999 Jul 6;96(14):8132-7
PMID: 10393960
-
Islet graft assessment in the Edmonton Protocol: implications for predicting long-term clinical outcome.
Diabetes. 2004 Dec;53(12):3107-14
PMID: 15561940
-
Loss of connexin36 channels alters beta-cell coupling, islet synchronization of glucose-induced Ca2+ and insulin oscillations, and basal insulin release.
Diabetes. 2005 Jun;54(6):1798-807
PMID: 15919802
-
A novel method for the assessment of cellular composition and beta-cell viability in human islet preparations.
Am J Transplant. 2005 Jul;5(7):1635-45
PMID: 15943621
-
Assessment of human pancreatic islet architecture and composition by laser scanning confocal microscopy.
J Histochem Cytochem. 2005 Sep;53(9):1087-97
PMID: 15923354
-
Different effects of tolbutamide and diazoxide in alpha, beta-, and delta-cells within intact islets of Langerhans.
Diabetes. 1999 Dec;48(12):2390-7
PMID: 10580428
-
Endotoxin-mediated delayed islet graft function is associated with increased intra-islet cytokine production and islet cell apoptosis.
Transplantation. 2001 Jan 15;71(1):125-32
PMID: 11211177
-
Reduced beta-cell mass and expression of oxidative stress-related DNA damage in the islet of Japanese Type II diabetic patients.
Diabetologia. 2002 Jan;45(1):85-96
PMID: 11845227
-
Functional subdivision of islets of Langerhans and possible role of D cells.
Lancet. 1975 Dec 20;2(7947):1243-4
PMID: 53729
-
Pancreatic polypeptide and glucagon : non-random distribution in pancreatic islets.
Life Sci. 1976 Dec 15;19(12):1811-5
PMID: 794610
-
New perspectives on the microvasculature of the islets of Langerhans in the rat.
Diabetes. 1982 Oct;31(10):883-9
PMID: 6759221
-
Automated method for isolation of human pancreatic islets.
Diabetes. 1988 Apr;37(4):413-20
PMID: 3288530