Pancreas collagen digestion during islet of Langerhans isolation-a prospective study.
collagen
collagenase
extracellular matrix
islet isolation
islet of Langerhans
islet transplantation
outcomes
type 1 diabetes mellitus
Journal
Transplant international : official journal of the European Society for Organ Transplantation
ISSN: 1432-2277
Titre abrégé: Transpl Int
Pays: Switzerland
ID NLM: 8908516
Informations de publication
Date de publication:
11 2020
11 2020
Historique:
received:
31
05
2020
revised:
03
07
2020
accepted:
20
08
2020
pubmed:
28
8
2020
medline:
25
6
2021
entrez:
28
8
2020
Statut:
ppublish
Résumé
The success of pancreas islet isolation largely depends on donor characteristics, including extracellular matrix composition of which collagen is the main element. We hypothesized that isolation yields are proportional to collagen digestion percentage, and aimed to determine a threshold that predicts isolation success. The amount of pancreas collagen (I-V) was determined using colorimetry prior to and after the digestion process in 52 human islet isolations. Collagen I-V and VI were also assessed histologically. We identified a collagen digestion threshold of ≥ 60% as an independent factor beyond which an islet preparation has a ninefold increased odds of yielding ≥ 250 000 islet equivalents (IEQ) (P = 0.009) and a sixfold increased odds of being transplanted (P = 0.015). Preparations with ≥ 60% collagen digestion (n = 35) yielded 283 017 ± 164 214 IEQ versus 180 142 ± 85 397 in the < 60% collagen digestion group (n = 17) (P = 0.016); respectively 62.9% versus 29.4% of those were transplanted (P = 0.024). Common donor characteristics, initial collagen content, enzyme blend, and digestion times were not associated with collagen digestion percentage variations. Donor age positively correlated with the amount of collagen VI (P = 0.013). There was no difference in islet graft survival between high and low digestion groups. We determined that a 60% pancreas collagen digestion is the threshold beyond which an islet isolation is likely to be successful and transplanted.
Substances chimiques
Collagen
9007-34-5
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1516-1528Subventions
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
ID : P300PB_174500
Informations de copyright
© 2020 Steunstichting ESOT. Published by John Wiley & Sons Ltd.
Références
Shapiro AM, Lakey JR, Ryan EA, et al. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N Engl J Med 2000; 343: 230.
Shapiro AM, Ricordi C, Hering BJ, et al. International trial of the Edmonton protocol for islet transplantation. N Engl J Med 2006; 355: 1318.
Schuetz C, Anazawa T, Cross SE, et al. beta Cell Replacement Therapy: The Next 10 Years. Transplantation 2018; 102: 215.
Barton FB, Rickels MR, Alejandro R, et al. Improvement in outcomes of clinical islet transplantation: 1999-2010. Diabetes Care 2012; 35: 1436.
Niclauss N, Bosco D, Morel P, et al. Influence of donor age on islet isolation and transplantation outcome. Transplantation 2011; 91: 360.
Meier RP, Sert I, Morel P, et al. Islet of Langerhans isolation from pediatric and juvenile donor pancreases. Transpl Int 2014; 27: 949.
Meier RPH, Andrey DO, Sun P, et al. Pancreas preservation fluid microbial contamination is associated with poor islet isolation outcomes - a multi-centre cohort study. Transpl Int 2018; 31: 917.
Balamurugan AN, Naziruddin B, Lockridge A, et al. Islet product characteristics and factors related to successful human islet transplantation from the Collaborative Islet Transplant Registry (CITR) 1999-2010. Am J Transplant 2014; 14: 2595.
Szot GL, Lee MR, Tavakol MM, et al. Successful clinical islet isolation using a GMP-manufactured collagenase and neutral protease. Transplantation 2009; 88: 753.
Cross SE, Vaughan RH, Willcox AJ, et al. Key Matrix Proteins Within the Pancreatic Islet Basement Membrane Are Differentially Digested During Human Islet Isolation. Am J Transplant. 2017; 17: 451.
Hughes SJ, Clark A, McShane P, Contractor HH, Gray DW, Johnson PR. Characterisation of collagen VI within the islet-exocrine interface of the human pancreas: implications for clinical islet isolation? Transplantation 2006; 81: 423.
Sackett SD, Tremmel DM, Ma F, et al. Extracellular matrix scaffold and hydrogel derived from decellularized and delipidized human pancreas. Sci Rep 2018; 8: 10452.
Ma F, Tremmel DM, Li Z, et al. In Depth Quantification of Extracellular Matrix Proteins from Human Pancreas. J Proteome Res 2019; 18: 3156.
Stendahl JC, Kaufman DB, Stupp SI. Extracellular matrix in pancreatic islets: relevance to scaffold design and transplantation. Cell Transplant 2009; 18: 1.
Ris F, Niclauss N, Morel P, et al. Islet autotransplantation after extended pancreatectomy for focal benign disease of the pancreas. Transplantation 2011; 91: 895.
Kempf MC, Andres A, Morel P, et al. Logistics and transplant coordination activity in the GRAGIL Swiss-French multicenter network of islet transplantation. Transplantation 2005; 79: 1200.
Benhamou PY, Oberholzer J, Toso C, et al. Human islet transplantation network for the treatment of Type I diabetes: first data from the Swiss-French GRAGIL consortium (1999-2000). Groupe de Recherche Rhin Rhjne Alpes Geneve pour la transplantation d'Ilots de Langerhans. Diabetologia 2001; 44: 859.
Borot S, Niclauss N, Wojtusciszyn A, et al. Impact of the number of infusions on 2-year results of islet-after-kidney transplantation in the GRAGIL network. Transplantation 2011; 92: 1031.
Ricordi C, Lacy PE, Finke EH, Olack BJ, Scharp DW. Automated method for isolation of human pancreatic islets. Diabetes 1988; 37: 413.
Bucher P, Mathe Z, Morel P, et al. Assessment of a novel two-component enzyme preparation for human islet isolation and transplantation. Transplantation 2005; 79: 91.
Niclauss N, Wojtusciszyn A, Morel P, et al. Comparative impact on islet isolation and transplant outcome of the preservation solutions Institut Georges Lopez-1, University of Wisconsin, and Celsior. Transplantation 2012; 93: 703.
Niclauss N, Sgroi A, Morel P, et al. Computer-assisted digital image analysis to quantify the mass and purity of isolated human islets before transplantation. Transplantation 2008; 86: 1603.
Ricordi C, Gray DW, Hering BJ, et al. Islet isolation assessment in man and large animals. Acta Diabetol Lat 1990; 27: 185.
Meier RP, Seebach JD, Morel P, et al. Survival of free and encapsulated human and rat islet xenografts transplanted into the mouse bone marrow. PLoS One 2014; 9: e91268.
Toso C, Baertschiger R, Morel P, et al. Sequential kidney/islet transplantation: efficacy and safety assessment of a steroid-free immunosuppression protocol. Am J Transplant 2006; 6: 1049.
Badet L, Benhamou PY, Wojtusciszyn A, et al. Expectations and strategies regarding islet transplantation: metabolic data from the GRAGIL 2 trial. Transplantation 2007; 84: 89.
Benhamou PY, Milliat-Guittard L, Wojtusciszyn A, et al. Quality of life after islet transplantation: data from the GRAGIL 1 and 2 trials. Diabet Med 2009; 26: 617.
Lablanche S, Borot S, Wojtusciszyn A, et al. Five-Year Metabolic, Functional, and Safety Results of Patients With Type 1 Diabetes Transplanted With Allogenic Islets Within the Swiss-French GRAGIL Network. Diabetes Care 2015; 38: 1714.
van Deijnen JH, Hulstaert CE, Wolters GH, van Schilfgaarde R. Significance of the peri-insular extracellular matrix for islet isolation from the pancreas of rat, dog, pig, and man. Cell Tissue Res 1992; 267: 139.
Wang RN, Paraskevas S, Rosenberg L. Characterization of integrin expression in islets isolated from hamster, canine, porcine, and human pancreas. J Histochem Cytochem. 1999; 47: 499.
Daoud J, Petropavlovskaia M, Rosenberg L, Tabrizian M. The effect of extracellular matrix components on the preservation of human islet function in vitro. Biomaterials 2010; 31: 1676.
Van Deijnen JH, Van Suylichem PT, Wolters GH, Van Schilfgaarde R. Distribution of collagens type I, type III and type V in the pancreas of rat, dog, pig and man. Cell Tissue Res 1994; 277: 115.
Wang R, Li J, Lyte K, Yashpal NK, Fellows F, Goodyer CG. Role for beta1 integrin and its associated alpha3, alpha5, and alpha6 subunits in development of the human fetal pancreas. Diabetes 2005; 54: 2080.
Niclauss N, Meier R, Bedat B, Berishvili E, Berney T. Beta-Cell Replacement: Pancreas and Islet Cell Transplantation. Endocr Dev 2016; 31: 146.
Hilling DE, Rijkelijkhuizen JK, Tons HA, Terpstra OT, Bouwman E. Porcine islet isolation outcome is not affected by the amount and distribution of collagen in the pancreas. Xenotransplantation 2010; 17: 250.
Montanari E, Meier RPH, Mahou R, et al. Multipotent mesenchymal stromal cells enhance insulin secretion from human islets via N-cadherin interaction and prolong function of transplanted encapsulated islets in mice. Stem Cell Res Ther 2017; 8: 199.
Parnaud G, Gonelle-Gispert C, Morel P, et al. Cadherin engagement protects human beta-cells from apoptosis. Endocrinology 2011; 152: 4601.
Venkataramana NK, Kumar SK, Balaraju S, et al. Open-labeled study of unilateral autologous bone-marrow-derived mesenchymal stem cell transplantation in Parkinson's disease. Transl Res 2010; 155: 62.
Dowell JD, Rubart M, Pasumarthi KB, Soonpaa MH, Field LJ. Myocyte and myogenic stem cell transplantation in the heart. Cardiovasc Res 2003; 58: 336.
Meier RPH, Navarro-Alvarez N, Morel P, Schuurman HJ, Strom S, Buhler LH. Current status of hepatocyte xenotransplantation. Int J Surg 2015; 23: 273.
Meier RP, Muller YD, Morel P, Gonelle-Gispert C, Buhler LH. Transplantation of mesenchymal stem cells for the treatment of liver diseases, is there enough evidence? Stem Cell Res 2013; 11: 1348.