Cited by 229Pancreatic function and diabetesCell death mechanisms and regulationDiabetes and associated disorders

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Cell Loss in Isolated Human Islets Occurs by Apoptosis

Paraskevas, Steven, Maysinger, Dusica, Wang, Rennien, Duguid, William P, Rosenberg, Lawrence·2000·Pancreas

DOI 10.1097/00006676-200004000-00008

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Abstract

Purified islet allografts have largely failed to maintain long-term glucose homeostasis in human recipients, and the reasons for this are unclear. It is noteworthy, however, that islet isolation destroys or removes cellular and noncellular elements of the pancreas that could play an important role in supporting islet survival. The purpose of this study was to determine whether human islet isolation leads to the induction of programmed cell death. Human islets were enzymatically isolated from cadaveric donor pancreata using Liberase or Collagenase P, purified over a discontinuous BSA gradient, then cultured in RPMI 1640 at 37 degrees C in 5% CO2 for < or = 7 days. Islets were examined daily by routine histology and immunocytochemistry for islet hormones, DNA fragmentation [cell death; enzyme-linked immunosorbent assay (ELISA) and TUNEL assay] and for transglutaminase (TG) activity, two indicators of apoptosis. TG activity and DNA fragmentation increased by 1,000% and 1,890%, respectively (p < 0.05) This corresponded to the appearance of pyknotic nuclei on light microscopy, the presence of apoptotic bodies on electron microscopy, and the demonstration of TUNEL-positive cells. These were present primarily in a distribution that corresponded to the insulin-immunoreactive cells. At 5 days, 31.4 +/- 2.2% of islet cells were TUNEL positive. In summary, apoptosis of islet cells appears soon after islet isolation, and involves primarily the beta cell. This is the first report of apopt…

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“Abbreviations: ACRg, acute C-peptide response to glucose; AE, adverse event; AIRg, acute insulin response to glucose; AUC, area under the curve; DI, deposition index; DPP-4, dipeptidyl peptidase 4; FSIVGTT, frequent sample intravenous glucose tolerance test; GIP, glucose-dependent insulinotropic peptide; GLP-1, glucag…”
Influential
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“Apoptosis also mediates beta cell loss in islet transplantation both during isolation of the islets [4] and during engraftment [5,6].”
Background
Block-copolymer micelles as carriers of cell signaling modulators for the inhibition of JNK in human islets of Langerhans.
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Background
Culturing with modified EGM2 medium enhances porcine neonatal islet‐like cell clusters resistance to apoptosis in islet xenotransplantation
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“Studies have indicated that islet isolation by collagenase treatment exposes them to various cellular stresses that soon lead to apoptosis.(4) This is caused by several factors, including destruction of the basement membrane (BM) around the islets and loss of vasculature.”
Background
Increased Albumin Concentration Reduces Apoptosis and Improves Functionality of Human Islets
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“The low frequency of islet grafting results from poor islet recovery from donors (23) and early islet loss during the first hours after grafting (6,30).”
Background
Liraglutide protects Rin-m5f β cells by reducing procoagulant tissue factor activity and apoptosis prompted by microparticles under conditions mimicking Instant Blood-Mediated Inflammatory Reaction
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“In particular, cell apoptosis during the isolation procedure or in the conservation medium before infusion [5,6], and the Instant Blood-Mediated Inflammatory Reaction (IBMIR) immediately after transplantation are thought to be early causes of the loss of graft function [7].”
Background
Regulation of the JNK3 Signaling Pathway during Islet Isolation: JNK3 and c-fos as New Markers of Islet Quality for Transplantation
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“Indeed, pancreas procurement, enzymatic digestion and mechanical purification damage the tissue and reduce beta-cell function and viability, compromising long-term islet graft function [8–10].”
Background
In Vitro and in Vivo Prevention of Human CD8+ CTL‐Mediated Xenocytotoxicity by Pig c‐FLIP Expression in Porcine Endothelial Cells
Tanemura, M., Saga, A., Kawamoto, K., Deguchi, T., Machida, T., Nishida, T., Sawa, Y., & Ito, T. (2008) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2007.02077.x · Cited by 9
“Several investigators have reported that islet cell death, especially of insulin-producing b-cells, is triggered by apoptosis, immediately after the islet isolation (47,48).”
Background
Red Ginseng Administration Before Islet Isolation Attenuates Apoptosis and Improves Islet Function and Transplant Outcome in a Syngeneic Mouse Marginal Islet Mass Model.
Kim, J. S., Jang, H., Kim, S. S., Oh, M., Kim, H., Lee, S. Y., Eom, D., Ham, J., & Han, D. (2016) · Transplantation Proceedings · doi:10.1016/j.transproceed.2016.01.025 · Cited by 8
Bone marrow increases human islets insulin positive cells in co-culture: quantification with flow cytometry
Wang, Z., Xiong, F., Hassani, M., Luo, J. Z. Q., & Luo, L.-G. (2011) · doi:10.4236/jdm.2011.14015 · Cited by 8
“Extending the duration of culture beyond this period usually results in a significant loss of structural integrity within the islets and a decline in glucose-stimulated insulin release [6-8].”
Mechanistic Insights into Ferroptotic Cell Death in Pancreatic Islets
Schepp, F., Schubert, U., Schmid, J., Lehmann, S., Latunde-Dada, G., Kose, T., Steenblock, C., Bornstein, S. R., Linkermann, A., & Ludwig, B. (2023) · Hormone and Metabolic Research · doi:10.1055/a-2190-2803 · Cited by 7
“It has been described that apoptotic cell death peaks after five days in culture and mainly affects beta cells [17].”
Background
Development of scaffold-free vascularized pancreatic beta-islets in vitro models by the anchoring of cell lines to a bioligand-functionalized gelatine substrate
Perugini, V., Flaherty, S. M., & Santin, M. (2022) · Journal of materials science. Materials in medicine · doi:10.1007/s10856-022-06658-3 · Cited by 7
Polymyxin B, scavenger of endotoxin, enhances isolation yield and in vivo function of islets
Park, S. G., Kim, J. H., Oh, J., Lee, H.-N., Park, H. S., Chung, S. S., Lee, Y., Lee, Y.-O.-Y., Jung, H., & Park, K. (2010) · Transplant International · doi:10.1111/j.1432-2277.2009.00987.x · Cited by 7
“The low probability of islet engraftment might be resulting from poor islet recovery from donors [3] and early islet losses [4] for instant blood-mediated inflammatory responses (IBMIR) [5,6].”
Background
Effect of Pretransplant Preconditioning by Whole Body Hyperthermia on Islet Graft Survival
Brandhorst, H., Olbrich, M., Neumann, A., Jahr, H., & Brandhorst, D. (2007) · Cell Transplantation · doi:10.3727/000000007783465163 · Cited by 7
The Pig as the Donor of Pancreatic Islets for Men
Trucco, M., Casu, A., & Bottino, R. (2007) · Veterinary research communications · doi:10.1007/s11259-007-0006-7 · Cited by 6
“Besides the limited number of cadaveric organ donors, the current procedure used to isolate islets from their pancreata activates metabolic processes that promote the loss of b cells in the islets by apoptosis and/or necrosis ( Paraskevas et al., 2000; Okamoto and Takasawa, 2002).”
Method
Inflammatory and hypoxic stress-induced islet exosomes released during isolation are associated with poor transplant outcomes in islet autotransplantation
Saravanan, P. B., Kalivarathan, J., McClintock, K., Mohammed, S., Burch, E., Morecock, C., Liu, J., Khan, A. A., Levy, M. F., & Kanak, M. A. (2024) · American Journal of Transplantation · doi:10.1016/j.ajt.2024.02.011 · Cited by 6
The loss of pancreatic islet NADPH oxidase (NOX)2 improves islet transplantation
Wrublewsky, S., Glas, J., Carlein, C., Nalbach, L., Hoffmann, M. D. A., Pack, M., Vilas‐Boas, E. A., Ribot, N., Kappl, R., Menger, M. D., et al. (2022) · Redox Biology · doi:10.1016/j.redox.2022.102419 · Cited by 7
“Several studies already reported that oxidative stress resulting from the islet isolation procedure leads to islet cell damage, which in turn impairs the islets’ function after transplantation [10,45,46].”
Background
α-cell loss from islet impairs its insulin secretion in vitro and in vivo
Wang, H., Zhang, W.-J., Cai, H.-Q., Xu, S.-Q., Sui, W.-G., Jiang, Y.-W., Deng, S., & Lou, J. (2011) · Islets · doi:10.4161/isl.3.2.15036 · Cited by 5
"The matrix unloaded": implications for cytokine signaling in islets?
Lowe, W. (2003) · Endocrinology · doi:10.1210/en.2003-0884 · Cited by 5
Augmenting engraftment of beta cell replacement therapies for T1DM
Aggarwal, S., Pepper, A. R., & Jahdhami, N. A. (2021) · Journal of Immunology and Regenerative Medicine · doi:10.1016/j.regen.2021.100058 · Cited by 5
A Preconditioning Regimen with a PKCε Activator Improves Islet Graft Function in a Mouse Transplant Model
Hamilton, D., Rugg, C., Davis, N. E., Kvezereli, M., Tafti, B., Busque, S., & Fontaine, M. (2014) · Cell Transplantation · doi:10.3727/096368913x665567 · Cited by 4
Significant Improvement in Islet Yield and Survival with Modified ET-Kyoto Solution: ET-Kyoto/Neutrophil Elastase Inhibitor
Machida, T., Tanemura, M., Ohmura, Y., Tanida, T., Wada, H., Kobayashi, S., Marubashi, S., Eguchi, H., Ito, T., Nagano, H., et al. (2012) · Cell Transplantation · doi:10.3727/096368912x637028 · Cited by 6
“Indeed, the islet isolation procedure itself can lead to tissue destruction and activation of cellular and noncellular components of the pancreas, including resident neutrophils, macrophages, and T cells, which probably play an important role in impairment of islet survival (1,4,31,37,42).”
Background
Mitomycin C Treatment Significantly Reduces Central Damage of Islets in Culture
Saito, T., Saito, T., Sato, Y., Ise, K., Anazawa, T., Oshibe, I., Haga, J., Yamamoto, M., Waguri, S., & Gotoh, M. (2012) · Pancreas · doi:10.1097/mpa.0b013e31822461c7 · Cited by 4
Improved Islet Yield and Function by Use of a Chloride Channel Blocker During Collagenase Digestion
Anazawa, T., Sato, Y., Saito, T., Tsuchiya, T., Kenjo, A., Kimura, T., Haga, J., Miyake, M., Waguri, S., Hazama, A., et al. (2011) · Transplantation · doi:10.1097/tp.0b013e31822e6eb4 · Cited by 4
“(31) reported that cell loss in islets that were isolated using the human islet isolation procedure occurs by apoptosis.”
Background
Design and fabrication of large area nano-structured substrates for use in pancreatic beta-cell engineering
Bakeine, G., Bertolotti, A., Zennaro, C., Grenci, G., Pozzato, A., Zilio, S. D., Prasciolu, M., Carraro, M., Businaro, L., Tormen, M., et al. (2009) · doi:10.1016/j.mee.2008.12.059 · Cited by 4
APOPTOSIS OF HUMAN FETAL PANCREATIC ISLETS DURING SHORT-TERM CULTURE
Djordjević, P., Dimitrijevic-Sreckovic, V., Bumbaširević, V., Čolović, R., Nikolic, D., Raketic, N., & Canović, F. (2009) · doi:10.2298/abs0901009d · Cited by 4
“The influence of apoptosis of HAIs after Tx has also been cited (Paraskevas et al., 2000).”
Background
Clinical Islet Transplantation Covered by Health Insurance in Japan
Noguchi, H. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11143977 · Cited by 3
Improvement of human pancreatic islet quality after co-culture with human adipose-derived stem cells.
de Souza, B. D., Rodrigues, M., de Oliveira, F. S., da Silva, L. A., Bouças, A. P., Portinho, C. P., Santos, B. P. D., Camassola, M., Rocha, D., Lysakowski, S., et al. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.110729 · Cited by 3
Selective Osmotic Shock for Islet Isolation in the Cadaveric Canine Pancreas
Thompson, E., Sollinger, J., Opara, E., & Adin, C. (2018) · Cell Transplantation · doi:10.1177/0963689717752947 · Cited by 3
Molecular shielding of porcine islets by tissue-adhesive chitosan-catechol for enhancement of in-vitro stability
Jeong, J.-H., Woo, Y.-J., Lee, M.-Y., Haque, M. R., Ahn, C., Lee, H., & Byun, Y. (2018) · doi:10.1016/j.jiec.2017.08.040 · Cited by 3
An Engineered Innate Repair Receptor Agonist, ARA 290, Protects Rat Islets from Cytokine-induced Apoptosis
Watanabe, M., Saito, Y., Wallmo, J., Takahashi, T., Diab, R., Yao, M. H., Brines, M. L., Cerami, A., Östenson, C. G., Lundgren, T., et al. (2016) · Journal of Diabetes & Metabolism · doi:10.4172/2155-6156.1000708 · Cited by 2
“In addition, the islet isolation process also triggers a cascade of stressful events in the islets involving apoptosis and the production of proinflammatory molecules that negatively influence islet function, producing detrimental effects following PITx [5-7].”
BackgroundInfluential
The IL-1 Receptor Antagonist Anakinra Enhances Survival and Function of Human Islets during Culture: Implications in Clinical Islet Transplantation
Park, Y., Zhang, Y., Ao, Z.-L., Meloche, M., Warnock, G., & Marzban, L. (2012) · doi:10.1016/j.jcjd.2012.08.003 · Cited by 3
Pancreas Biology, Pathology, and Tissue Engineering
Macfarlane, W. M., Bone, A. J., & Harrison, M. (2008) · Springer eBooks · doi:10.1007/978-0-387-74660-9_8 · Cited by 1
Pancreas Preservation with a Neutrophil Elastase Inhibitor, Alvelestat, Contributes to Improvement of Porcine Islet Isolation and Transplantation
Otsuka, R., Miyagi-Shiohira, C., Kuwae, K., Nishime, K., Tamaki, Y., Yonaha, T., Sakai-Yonaha, M., Yamasaki, I., Shinzato, M., Saitoh, I., et al. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11154290 · Cited by 2
Quercetin Enhances the Function and Reduces Apoptosis of Mouse Islets.
Kim, S. S., Jang, H., & Oh, M. (2019) · Transplantation Proceedings · doi:10.1016/j.transproceed.2019.03.022 · Cited by 2
Protective effect of rat pancreatic progenitors cells expressing Pdx1 and nestin on islets survival and function in vitro and in vivo
Zhou, S.-Y., Zhang, Y.-S., Li, Q., Zhang, Y., Qi, H., Zhou, H.-X., Deng, C.-Y., & Li, F.-R. (2012) · Journal of physiology and biochemistry · doi:10.1007/s13105-012-0180-0 · Cited by 2
“Scarcity of transplantable islets has been a major obstacle for widescale islet transplantation [17].”
Background
Cobalt Protoporpyhrin Reduces Caspase-3,-7 Enzyme Activity in Neonatal Porcine Islets, But Does Not Inhibit Cell Death Induced by TNF-α
Bosio, E., Seveso, M., Dedja, A., Luca, G., Calvitti, M., Calafiore, R., Rigotti, P., Busetto, R., Ancona, E., & Cozzi, E. (2008) · Cell Transplantation · doi:10.3727/096368908786092784 · Cited by 2
Culturing Free-Floating and Fibrin-Embedded Islets with Endothelial Cells: Effects on Insulin Secretion and Apoptosis
Dubiel, E. A., Lakey, J., Lamb, M. W., & Vermette, P. (2014) · Cellular and Molecular Bioengineering · doi:10.1007/s12195-014-0332-0 · Cited by 1
The Adrenal Gland and Pancreatic Islets – A Beneficial Endocrine Alliance
Schubert, U., Lehmann, S., Schmid, J., Morawietz, H., Bornstein, S. R., & Ludwig, B. (2024) · Hormone and Metabolic Research · doi:10.1055/a-2256-6344 · Cited by 1
“Oxidatively stressed cells are characterized by redox imbalance with accumulation of reduced pyridine nucleotides, depletion of ATP, mitochondrial membrane depolarization, cytochrome c release, and activation of apoptotic and necrotic pathways [13, 14].”
Background
The Effects of Cord Blood Serum on Survival of Rat Pancreatic Islets during In vitro Culturing
Karbek, B., PÄ-narlÄ-Fa, Erden, G., Çakal, E., & Delibaşı, T. (2016) · doi:10.4172/2161-1017.1000241 · Cited by 1
Rotational Transport of Islets: The Best Way for Islets to Get around?
Oberhuber, R., Mittermair, C., Zelger, B., Pirkebner, D., Draxl, A., Weissenbacher, A., Resch, T., Margreiter, C., Sucher, R., Margreiter, R., et al. (2013) · BioMed Research International · doi:10.1155/2013/975608 · Cited by 1
Total pancreatectomy with islet autotransplantation in children
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Islet Cell Transplant
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Development of a 3D subcutaneous construct containing insulin-producing beta cells using bioprinting
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Could Transplantation into the Thyroid Gland Benefit Pancreatic Islet Grafting in Unstable Type 1 Diabetes (T1DM), Complicated Type 2 Diabetes (T2DM), and Patients with Total Pancreatectomy?
Rosato, L., Lavorini, E., & Deandrea, M. (2023) · Stem Cell Reviews and Reports · doi:10.1007/s12015-023-10671-6
“The process of isolating islets from the pancreas, due to enzymatic (collagenase) and mechanical insults, is detrimental to the integrity of the islets themselves, whose cells may undergo necrosis and apoptosis [24].”
Stem Cell-Derived Insulin-Producing Cells in 3D Engineered Tissue in a Perfusion Flow Bioreactor
Ma, X.-T., Jain, N., Hitscherich, P., Seetamraju, S., & Lee, E. A. (2020) · Tissue Engineering. Part A · doi:10.1089/ten.tea.2020.0231
“6,7 To overcome the limitation of the donors and islet resources, derivation of insulin-producing cells (IPCs) from pluripotent stem cells has emerged as an attractive option.”

Authors: Paraskevas, S., Maysinger, D., Wang, R., Duguid, W. P., & Rosenberg, L.
Affiliations: Montreal General Hospital (CA)
Corresponding author: Rosenberg, Lawrence
ORCID: Paraskevas, Steven
Venue: Pancreas
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2000-04
Volume: 20
Issue: 3
Pages: 270-276
ISSN: 0885-3177 (ISSN-L)
DOI: 10.1097/00006676-200004000-00008
OpenAlex: W2046236577
Cited by: 229
References: 0
Citations by year: 2024: 6 · 2023: 7 · 2022: 6 · 2021: 8 · 2020: 7 · 2019: 7 · 2018: 15 · 2017: 10 · 2016: 11 · 2015: 9 · 2014: 7 · 2013: 14 · 2012: 12
FWCI: 7.56
Type: journal article
Language: en
Open access: closed
Locations: Pancreas (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Pancreatic function and diabetes
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Diabetes and associated disorders
Keywords: islet isolation, apoptosis, beta-cell death, human pancreatic islets, islet transplantation, transglutaminase activity, DNA fragmentation, TUNEL, Liberase, islet purification
MeSH terms: Adolescent, Adult, Cadaver, Cell Separation, Enzyme-Linked Immunosorbent Assay, Humans, Immunohistochemistry, Islets of Langerhans, Microscopy, Electron, Middle Aged, Transglutaminases, Thermolysin, Apoptosis, Collagenases, In Situ Nick-End Labeling, DNA Fragmentation

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Cell Loss in Isolated Human Islets Occurs by Apoptosis

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