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Islet Interleukin-1Β Immunoreactivity Is an Early Feature of Cystic Fibrosis That May Contribute to Β-Cell Failure

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Islet Interleukin-1Β Immunoreactivity Is an Early Feature of Cystic Fibrosis That May Contribute to Β-Cell Failure Diabetes Care 1 Islet Interleukin-1b Rebecca L. Hull,1 Ronald L. Gibson,2 Sharon McNamara,2 Gail H. Deutsch,3 Immunoreactivity Is an Early Corinne L. Fligner,3 Charles W. Frevert,1,4 Bonnie W. Ramsey,2 and Srinath Sanda5,6 Feature of Cystic Fibrosis That May Contribute to b-Cell Failure https://doi.org/10.2337/dc17-1387 OBJECTIVE Cystic fibrosis–related diabetes (CFRD) is a common complication of cystic fibrosis (CF), increasing patient morbidity and mortality. Poor understanding of CFRD path- ogenesis limits the development of targeted therapies to treat and/or prevent the disease. The aim of this study was to evaluate islet pathology, specifically, inflam- mation, amyloid deposition, and endocrine cell composition in subjects with CF with diabetes and with CF without diabetes. RESEARCH DESIGN AND METHODS A retrospective analysis of archived pancreas tissue collected at autopsy was con- ducted using pancreas tissue from subjects with CF and diabetes (CFRD) (n = 18) and PATHOPHYSIOLOGY/COMPLICATIONS CF without diabetes (CF-no DM) (n = 17). Two cohorts of control non-CF subjects were identified, each matched to CFRD and CF-no DM subjects for age, sex, and BMI (non-CF older, n = 20, and non-CF younger, n = 20), respectively. Immunohistochem- istry was performed to assess IL-1b and islet hormone (insulin, glucagon, somato- statin, and pancreatic polypeptide) immunoreactivity; histochemistry was performed 1Department of Medicine, University of Wash- to quantify amyloid deposition. ington, Seattle, WA 2Department of Pediatrics, University of Wash- RESULTS ington, Seattle, WA 3Department of Pathology, University of Wash- Islet IL-1b immunoreactivity was substantially increased in both CFRD and CF-no DM ington, Seattle, WA subjects compared with non-CF subjects and was common in young subjects with CF 4Department of Comparative Medicine, Univer- (£10 years of age). In contrast, islet amyloid deposition was increased only in CFRD sity of Washington, Seattle, WA 5Department of Pediatrics, University of Califor- subjects. We also observe abnormal islet hormone immunoreactivity, characterized nia, San Francisco, San Francisco, CA by increased glucagon immunoreactivity, in CF-no DM and CFRD subjects compared 6Diabetes Center, University of California, San with non-CF subjects. Francisco, San Francisco, CA Corresponding author: Rebecca L. Hull, rhull@ CONCLUSIONS uw.edu, or Srinath Sanda, srinath.sanda@ucsf These findings reveal novel molecular pathways and therapeutic targets underlying .edu. islet pathology in CF subjects and may be important in developing new approaches to Received 11 July 2017 and accepted 6 January treat CFRD. 2018. This article contains Supplementary Data online at http://care.diabetesjournals.org/lookup/ Cystic fibrosis–related diabetes (CFRD) occurs in up to 50% of adults with cystic fibrosis suppl/doi:10.2337/dc17-1387/-/DC1. (CF), with the highest incidence occurring during the second to third decade of life (1), © 2018 by the American Diabetes Association. although abnormal glucose tolerance is common even in very young children with the Readers may use this article as long as the work disease (2–4). CFRD is associated with increased morbidity and mortality in both males is properly cited, the use is educational and not for profit, and the work is not altered. More infor- and females (5). Insulin therapy is the current standard of care for CFRD. Unlike type 1 mation is available at http://www.diabetesjournals diabetes, CFRD does not appear to be the result of islet autoimmunity; HLA .org/content/license. Diabetes Care Publish Ahead of Print, published online February 1, 2018 2 Islet IL-1b Immunoreactivity in Cystic Fibrosis Diabetes Care susceptibility alleles are not observed that CFRD would be characterized not 3 from the JDRF nPOD registry) were iden- with greater frequency, although studies only by islet amyloid but also by islet ex- tified. These, designated “non-CF (youn- differ with respect to the prevalence of pression of the inflammatory cytokine ger)” (n = 20) and “non-CF (older)” (n = islet autoantibodies (6,7). Physiologically, IL-1b. We conducted a histologic study 21), were matched for age, sex, and BMI CFRD appears to have more in common to test this hypothesis. We observed to CF-no DM and CFRD subjects, respec- with type 2 diabetes. Genetic susceptibil- greater IL-1b immunoreactivity in islets tively, and to the extent possible, given ity loci for type 2 diabetes appear to con- subjects with CF with or without diabetes that autopsies were performed over fer risk for CFRD (8–10), and, similar to compared with control subjects without many years, these were also matched to type 2 diabetes, CFRD is characterized CF, while islet amyloid deposition was the time of autopsy. One non-CF control by a mixture of peripheral, particularly only increased in those individuals diag- subject [from the non-CF cohort (older)] hepatic, insulin resistance and significant nosed with CFRD. Islet endocrine compo- was excluded from further analysis, as no defects in b-cell function (4,11–13). How- sition was also disturbed, with increased pancreas specimen was available, bringing ever, the cause of b-cell dysfunction in a-cell area observed in subjects with CF the sample size from the non-CF (older) CFRD is not known. with and without diabetes. Based on group to 20. The study was approved by Work in various animal models, includ- these observations, we propose that CF institutional review boards at the Univer- ing the recently developed pig and ferret is characterized by islet inflammation, sity of Washington and SCH. models, demonstrates abnormalities in which could predispose to b-cell failure, Pancreatic tissue was obtained during glucose metabolism and insulin release, and by islet a-cell expansion, while islet autopsies performed at the University of mostly in the newborn period (14–16). amyloid formation is mainly restricted to Washington and SCH or via the nPOD pro- Human autopsy studies have been infor- CFRD. gram. Histologic sampling from the body mative in describing islet cell histological of the pancreas was routinely performed, changes with clinical manifestations. although autopsy records did not always Some small studies have reported that RESEARCH DESIGN AND METHODS indicate the specific location of the sample. subjects with CFRD have a lower density Subjects Specimens were included in the study only of endocrine (islet) tissue compared with Forty-one patients with CF were identi- if they showed no or minimal autolysis, as fi patients with CF without diabetes (17) ed by retrospective screening of autopsy assessed by CLF and RLH (University of ’ and/or loss of b-cells with no change in records at the Seattle Children s Hospital Washington samples) or GHD and RLH glucagon-producing a-cells or somato- (SCH) and the University of Washington (SCH samples). Pancreatic weight was not statin-producing d-cells compared with Medical Center for a CF diagnosis. We available; therefore, endocrine cell data are CF subjects without diabetes (18,19). screened records from SCH between presented as relative area rather than mass. However, one larger study found no dif- 1977 and 2012 and at University of Wash- ference in b-cell area among subjects ington Medical Center between 1991 and with CF with or without diabetes (20). 2013. Available clinical data (Table 1), in- Immunohistochemistry Four-micron-thick sections of formalin- As in type 2 diabetes, pancreatic islet cluding history of lung transplantation, fixed, paraffin-embedded pancreas were amyloid deposition has been identified were extracted from the medical record subjected to immunohistochemistry (IHC) as a characteristic feature of CFRD in hu- and managed using REDCap electronic mans (19,20). Islet amyloid is a well- data capture tools hosted at the Univer- (LeicaBond Max; Leica Microsystems, Buf- described pathological feature of type 2 sity of Washington’s Institute of Transla- falo Grove, IL) as follows. The following diabetes, and consistent with the etiology tional Health Sciences. Three additional primary antisera were used, for each of of this form of diabetes, islet amyloid de- cases of CF were available from the which the host species is denoted in position is usually observed in older indi- JDRF-supported Network for Pancreatic square brackets: insulin (A0564 [guinea viduals (21–23). Islet amyloid deposition Organ Donors with Diabetes (nPOD). pig], 1:4,000; Dako, Carpenteria, CA), b is toxic to b-cells, correlating with both Nine were excluded from further analysis IL-1 (49-4960 [rabbit], 1:500; ProSci In- reduced b-cell area and increased b-cell based on the following criteria: incom- corporated, Poway, CA; and ab2105 [rab- apoptosis in patients with type 2 diabetes plete medical records (n = 1), lack of avail- bit], 1:1,000; Abcam, Cambridge, MA), (21–23). Recent data have linked islet am- ability or poor quality of pancreas tissue IL-1Ra (AF-280-NA [goat], 1:500; R&D Sys- yloid deposition to islet inflammation, (n =5),absenceofpancreaticisletsonthe tems, Minneapolis, MN; and NBP1-32568 namely, showing that islet amyloid indu- available pancreas sections (n = 2), or his- [rabbit], 2 mg/mL; Novus Biologicals, Little- ces inflammatory cytokine production, tory of islet antigen 2 antibodies and zinc ton, CO), CD68 (Clone 514H12 [mouse], 0.34 chiefly interleukin (IL)-1b,bymacrophages transporter 8 autoantibodies, suggestive mg/mL; Leica Biosystems/Novacastra), and dendritic cells (24,25). In a similar of the presence of type 1 diabetes (n =1). glucagon (EP3070 [rabbit], 1:10,000; fashion, the systemic inflammatory pro- Of the remaining 35 subjects with CF, Epitomics, Burlingame, CA), somatostatin cess observed in CF subjects also seems to 18 were classified as “CFRD” based on (SC-7819 [goat], 1:200; Santa Cruz Bio- be skewed toward IL-1b–regulated cyto- presence of diabetes diagnosis by the technology, Santa Cruz, CA) and pancre- kines such as IL-8 and IL-17 (26–28). treating physician and/or insulin use in atic polypeptide (PP) (NB100-1793 [goat], Given these previous observations of the medical record; the other 17 were des- 1:250; Novus).
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