دورية أكاديمية

Long-term efficacy and safety of porcine islet macrobeads in nonimmunosuppressed diabetic cynomolgus macaques.

التفاصيل البيبلوغرافية
العنوان: Long-term efficacy and safety of porcine islet macrobeads in nonimmunosuppressed diabetic cynomolgus macaques.
المؤلفون: Holdcraft RW; The Rogosin Institute, Xenia Division, Xenia, Ohio, USA., Graham MJ; Preclinical Research Center, University of Minnesota, St. Paul, Minnesota, USA., Bemrose MA; The Rogosin Institute, Xenia Division, Xenia, Ohio, USA., Mutch LA; Preclinical Research Center, University of Minnesota, St. Paul, Minnesota, USA., Martis PC; The Rogosin Institute, Xenia Division, Xenia, Ohio, USA., Janecek JL; Preclinical Research Center, University of Minnesota, St. Paul, Minnesota, USA., Hall RD; Bob Evans Farms, New Albany, Ohio, USA., Smith BH; The Rogosin Institute, New York, New York, USA., Gazda LS; The Rogosin Institute, Xenia Division, Xenia, Ohio, USA.
المصدر: Xenotransplantation [Xenotransplantation] 2022 May; Vol. 29 (3), pp. e12747. Date of Electronic Publication: 2022 Apr 06.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Munksgaard International Publishers Country of Publication: Denmark NLM ID: 9438793 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1399-3089 (Electronic) Linking ISSN: 0908665X NLM ISO Abbreviation: Xenotransplantation Subsets: MEDLINE
أسماء مطبوعة: Publication: Copenhagen : Munksgaard International Publishers
Original Publication: Copenhagen : Munksgaard, c1994-
مواضيع طبية MeSH: Diabetes Mellitus, Experimental*/therapy , Islets of Langerhans Transplantation*, Animals ; Humans ; Insulin/therapeutic use ; Macaca ; Swine ; Transplantation, Heterologous
مستخلص: Although human islet transplantation has proven to provide clinical benefits, especially the near complete amelioration of hypoglycemia, the supply of human islets is limited and insufficient to meet the needs of all people that could benefit from islet transplantation. Porcine islets, secreting insulin nearly identical to that of human insulin, have been proposed as a viable supply of unlimited islets. Further, encapsulation of the porcine islets has been shown to reduce or eliminate the use of immunosuppressive therapy that would be required to prevent rejection of the foreign islet tissue. The goal of the current study was to determine the long-term safety and efficacy of agarose encapsulated porcine islets (macrobeads) in diabetic cynomolgus macaques, in a study emulating a proposed IND trial in which daily exogenous insulin therapy would be reduced by 50% with no loss of glucose regulation. Four of six animals implanted with macrobeads demonstrated ≥ 30% reduction in insulin requirements in year 1 of follow-up. Animals were followed for 2, 3.5, and 7.4 years with no serious adverse events, mortality or evidence of pathogen transmission. This study supports the continued pursuit of encapsulated porcine islet therapy as a promising treatment option for diabetes mellitus.
(© 2022 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.)
References: 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;343:230-238.
Ricordi C, Goldstein JS, Balamurugan AN, et al. National Institutes of Health-Sponsored Clinical Islet Transplantation Consortium Phase 3 Trial: Manufacture of a complex cellular product at eight processing facilities. Diabetes. 2016;65:3418-3428.
Ryan EA, Paty BW, Senior PA, et al. Five-year follow-up after clinical islet transplantation. Diabetes. 2005;54:2060-2069.
Ahearn AJ, Parekh JR, Posselt AM. Islet transplantation for Type 1 diabetes: Where are we now? Expert Rev Clin Immunol. 2015;11:59-68.
Marfil-Garza BA, Shapiro AMJ, Kin T. Clinical islet transplantation: Current progress and new frontiers. J Hepatobiliary Pancreat Sci. 2021;28:23-254.
Hering BJ, Clarke WR, Bridges ND, et al. Phase 3 trial of transplantation of human islets in type 1 diabetes complicated by severe hypoglycemia. Diabetes Care. 2016;39:1230-1240.
Witkowski P, Philipson LH, Kaufman DB, et al. The demise of islet allotransplantation in the United States: A call for an urgent regulatory update. Am J Transplant. 2020;21(4):1365-1375.
Freige C, McCormack S, Ford C. Islet Cell Transplantation for Patients with Unstable or Uncontrollable Diabetes Mellitus: A Review of Clinical Effectiveness, Cost-Effectiveness and Guidelines. Ottawa; 2020.
Chinnuswami RHA, Gopalakrishnan L, Porter GD, Balamurugan AN. In: Miyagawa S, ed. Xenotransplantation: Comprehensive Study. IntechOpen; 2020.
Manell E, Hedenqvist P, Svensson A, Jensen-Waern M. Establishment of a refined oral glucose tolerance test in pigs, and assessment of insulin, glucagon and glucagon-like peptide-1 responses. PLoS One. 2016;11:e0148896.
Desai T, Shea LD. Advances in islet encapsulation technologies. Nat Rev Drug Discov. 2017;16:367.
Espona-Noguera A, Ciriza J, Cañibano-Hernánde A, et al. Review of advanced hydrogel-based cell encapsulation systems for insulin delivery in type 1 diabetes mellitus. Pharmaceutics. 2019;11:597.
Hu S, de Vos P. Polymeric approaches to reduce tissue responses against devices applied for islet-cell encapsulation. Front Bioeng Biotechnol. 2019;7:134.
Vaithilingam V, Bal S, Tuch BE. Encapsulated islet transplantation: Where do we stand? Rev Diabetes Stud. 2017;14:51-78.
Wiggins SC, Abuid NJ, Gattas-Asfura KM, Kar S, Stabler CL. Nanotechnology approaches to modulate immune responses to cell-based therapies for type 1 diabetes. J Diabetes Sci Technol. 2020;14:212-225.
Jain K, Asina S, Yang H, et al. Glucose control and long-term survival in biobreeding/Worcester rats after intraperitoneal implantation of hydrophilic macrobeads containing porcine islets without immunosuppression. Transplantation. 1999;68:1693-1700.
Gazda LS, Adkins H, Bailie JA, et al. The use of pancreas biopsy scoring provides reliable porcine islet yields while encapsulation permits the determination of microbiological safety. Cell Transplant. 2005;14:427-439.
Denner J. Transspecies transmission of gammaretroviruses and the origin of the Gibbon ape leukaemia virus (GaLV) and the Koala retrovirus (KoRV). Viruses. 2016;8:336.
Patience C, Takeuchi Y, Weiss RA. Infection of human cells by an endogenous retrovirus of pigs. Nat Med. 1997;3:282-286.
Moalic Y, Blanchard Y, Felix H, Jestin A. Porcine endogenous retrovirus integration sites in the human genome: Features in common with those of murine leukemia virus. J Virol. 2006;80:10980-10988.
Bendinelli M, Matteucci D, Friedman H. Retrovirus-induced acquired immunodeficiencies. Adv Cancer Res. 1985;45:125-181.
Wilson CA. Porcine endogenous retroviruses and xenotransplantation. Cell Mol Life Sci. 2008;65:3399-3412.
McGregor CGA, Takeuchi Y, Scobie L, Byrne G. PERVading strategies and infectious risk for clinical xenotransplantation. Xenotransplantation. 2018;25:e12402.
Elliott RB, Escobar L, Garkavenko O, et al. No evidence of infection with porcine endogenous retrovirus in recipients of encapsulated porcine islet xenografts. Cell Transplant. 2000;9:895-901.
Wang W, Mo Z, Ye B, Hu P, Liu S, Yi S. A clinical trial of xenotransplantation of neonatal pig islets for diabetic patients. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 2011;36:1134-1140.
Valdes-Gonzalez RA, Dorantes LM, Garibay GN, et al. Xenotransplantation of porcine neonatal islets of Langerhans and Sertoli cells: A 4-year study. Eur J Endocrinol. 2005;153:419-427.
Valdes-Gonzalez R, Dorantes LM, Bracho-Blanchet E, Rodriguez-Ventura A, White DJ. No evidence of porcine endogenous retrovirus in patients with type 1 diabetes after long-term porcine islet xenotransplantation. J Med Virol. 2010;82:331-334.
Matsumoto S, Tan P, Baker J, et al. Clinical porcine islet xenotransplantation under comprehensive regulation. Transplant Proc. 2014;46:1992-1995.
Niu D, Wei H-J, Lin L, et al. Inactivation of porcine endogenous retrovirus in pigs using CRISPR-Cas9. Science. 2017;357:1303-1307.
Fishman JA. Infectious disease risks in xenotransplantation. Am J Transplant. 2018;18:1857-1864.
Fishman JA. Assessment of infectious risk in clinical xenotransplantation: The lessons for clinical allotransplantation. Xenotransplantation. 2014;21:307-308.
Gazda LS, Collins J, Lovatt A, et al. A comprehensive microbiological safety approach for agarose encapsulated porcine islets intended for clinical trials. Xenotransplantation. 2016;23:444-463.
Gazda LS, Vinerean HV, Laramore MA, Hall RD, Carraway JW, Smith BH. No evidence of viral transmission following long-term implantation of agarose encapsulated porcine islets in diabetic dogs. J Diabetes Res. 2014;2014;727483.
Switzer WM, Michler RE, Shanmugam V, et al. Lack of cross-species transmission of porcine endogenous retrovirus infection to nonhuman primate recipients of porcine cells, tissues, or organs. Transplantation. 2001;71:959-965.
Cardona K, Korbutt GS, Milas Z, et al. Long-term survival of neonatal porcine islets in nonhuman primates by targeting costimulation pathways. Nat Med. 2006;12:304-306.
Wynyard S, Nathu D, Garkavenko O, Denner J, Elliott R. Microbiological safety of the first clinical pig islet xenotransplantation trial in New Zealand. Xenotransplantation. 2014;21:309-323.
Morozov VA, Wynyard S, Matsumoto S, Abalovich A, Denner J, Elliott R. No PERV transmission during a clinical trial of pig islet cell transplantation. Virus Res. 2017;227:34-40.
Matsumoto S, Wynyard S, Giovannangelo M, et al. Long-term follow-up for the microbiological safety of clinical microencapsulated neonatal porcine islet transplantation. Xenotransplantation. 2020;27:e12631.
I. f. L. A. R. Committee for the Update of the Guide for the Care and Use of Laboratory Animals, Division on Earth and Life Studies, & National Research Council. Guide for the Care and Use of Laboratory Animals. 8th ed. National Academies Press; 2010.
Graham ML, Rieke EF, Dunning M, et al. A novel alternative placement site and technique for totally implantable vascular access ports in non-human primates. J Med Primatol. 2009;38:204-212.
Graham ML, Mutch LA, Rieke EF, et al. Refinement of vascular access port placement in nonhuman primates: Complication rates and outcomes. Comp Med. 2010;60:479-485.
Graham ML, Rieke EF, Mutch LA, et al. Successful implementation of cooperative handling eliminates the need for restraint in a complex non-human primate disease model. J Med Primatol. 2012;41:89-106.
Graham ML. In: SJ Shapiro, ed. Handbook of Primate Behavioral Management. CRC Press, Boca Raton; 2017: 185-200.
Mutch LA, Klinker ST, Janecek JJ, Niewinski MN, Lee RMZ, Graham ML. Long-term management of vascular access ports in nonhuman primates used in preclinical efficacy and tolerability studies. J Invest Surg. 2020;33:493-504.
Graham ML, Mutch LA, Rieke EF, et al. Refining the high-dose streptozotocin-induced diabetic non-human primate model: An evaluation of risk factors and outcomes. Exp Biol Med. 2011;236:1218-1230.
Graham ML, Gresch SC, Hardy SK, Mutch LA, Janecek JL, Hegstad-Davies RL. Evaluation of commercial ELISA and RIA for measuring porcine C-peptide: Implications for research. Xenotransplantation. 2015;22:62-69.
Gresch SC, Mutch LA, Janecek JL, Hegstad-Davies RL, Graham ML. Cross-validation of commercial enzyme-linked immunosorbent assay and radioimmunoassay for porcine C-peptide concentration measurements in non-human primate serum. Xenotransplantation. 2017;24:e12320.
Marigliano M, Casu A, Bertera S, Trucco M, Bottino R. Hemoglobin A1C percentage in nonhuman primates: A useful tool to monitor diabetes before and after porcine pancreatic islet xenotransplantation. J Transplant. 2011;2011:1-8.
Crossan C, O'Hara Z, Mourad N, Gianello P, Scobie L. Examining the potential for porcine-derived islet cells to harbour viral pathogens. Xenotransplantation. 2018;25:e12375.
Scobie L, Padler-Karavani V, Bas-Bernardet SL, et al. Long-term IgG response to porcine Neu5Gc antigens without transmission of PERV in burn patients treated with porcine skin xenografts. J Immunol. 2013;191:2907-2915.
Heneine W, Switzer WM, Soucie JM, et al. Evidence of porcine endogenous retroviruses in porcine factor VIII and evaluation of transmission to recipients with hemophilia. J Infect Dis. 2001;183:648-652.
Irgang M, Sauer IM, Karlas A, et al. Porcine endogenous retroviruses: No infection in patients treated with a bioreactor based on porcine liver cells. J Clin Virol. 2003;28:141-154.
Xu H, Sharma A, Okabe J, et al. Serologic analysis of anti-porcine endogenous retroviruses immune responses in humans after ex vivo transgenic pig liver perfusion. ASAIO J. 2003;49:407-416.
Di Nicuolo G, D'Alessandro A, Andria B, et al. Long-term absence of porcine endogenous retrovirus infection in chronically immunosuppressed patients after treatment with the porcine cell-based Academic Medical Center bioartificial liver. Xenotransplantation. 2010;17:431-439.
Scobie L, Galli C, Gianello P, Cozzi E, Schuurman HJ. Cellular xenotransplantation of animal cells into people: Benefits and risk. Rev Sci Tech. 2018;37:113-122.
Graham ML, Bellin MD, Papas KK, Hering BJ, Schuurman HJ. Species incompatibilities in the pig-to-macaque islet xenotransplant model affect transplant outcome: a comparison with allotransplantation. Xenotransplantation. 2011;18:328-342.
Holdcraft RW, Dumpala PR, Smith BH, Gazda LS. A model for determining an effective in vivo dose of transplanted islets based on in vitro insulin secretion. Xenotransplantation. 2018;25:e12443.
Gazda LS, Vinerean HV, Laramore MA, et al. Encapsulation of porcine islets permits extended culture time and insulin independence in spontaneously diabetic BB rats. Cell Transplant. 2007;16:609-620.
Nishimura M, Iizuka N, Fujita Y, Sawamoto O, Matsumoto S. Effects of encapsulated porcine islets on glucose and C-peptide concentrations in diabetic nude mice 6 months after intraperitoneal transplantation. Xenotransplantation. 2017;24:e12313.
Iizuka N, Nishimura M, Fujita Y, Sawamoto O, Matsumoto S. The pharmacokinetics of porcine C-peptide after intraperitoneal injection. Xenotransplantation. 2019;26:e12505.
Sima AA, Zhang W, Xu G, Sugimoto K, Guberski D, Yorek MA. A comparison of diabetic polyneuropathy in type II diabetic BBZDR/Wor rats and in type I diabetic BB/Wor rats. Diabetologia. 2000;43:786-793.
Zhang W, Yorek M, Pierson CR, Murakawa Y, Breidenbach A, Sima AA. Human C-peptide dose dependently prevents early neuropathy in the BB/Wor-rat. Int J Exp Diabetes Res. 2001;2:187-193.
Kamiya H, Zhang W, Sima AA. C-peptide prevents nociceptive sensory neuropathy in type 1 diabetes. Ann Neurol. 2004;56:827-835.
Jolivalt CG, Rodriguez M, Wahren J, Calcutt NA. Efficacy of a long-acting C-peptide analogue against peripheral neuropathy in streptozotocin-diabetic mice. Diabetes Obes Metab. 2015;17:781-788.
Johansson BL, Sjoberg S, Wahren J. The influence of human C-peptide on renal function and glucose utilization in type 1 (insulin-dependent) diabetic patients. Diabetologia. 1992;35:121-128.
Johansson BL, Kernell A, Sjoberg S, Wahren J. Influence of combined C-peptide and insulin administration on renal function and metabolic control in diabetes type 1. J Clin Endocrinol Metab. 1993;77:976-981.
Ryk A, Losiewicz A, Michalak A, Fendler W. Biological activity of C-peptide in microvascular complications of type 1 diabetes-time for translational studies or back to the basics? Int J Mol Sci. 2020;21:9723.
Jeyam A, Colhoun H, McGurnaghan S, et al. Clinical impact of residual C-peptide secretion in type 1 diabetes on glycemia and microvascular complications. Diabetes Care. 2021;44:390-398.
Vantyghem MC, Raverdy V, Balavoine A-S, et al. Continuous glucose monitoring after islet transplantation in type 1 diabetes: An excellent graft function (beta-score greater than 7) Is required to abrogate hyperglycemia, whereas a minimal function is necessary to suppress severe hypoglycemia (beta-score greater than 3). J Clin Endocrinol Metab. 2012;97:E2078-2083.
Lachin JM, McGee P, Palmer JP, Group DER. Impact of C-peptide preservation on metabolic and clinical outcomes in the Diabetes Control and Complications Trial. Diabetes. 2014;63:739-748.
Brooks AM, Oram R, Home P, Steen N, Shaw JA. Demonstration of an intrinsic relationship between endogenous C-peptide concentration and determinants of glycemic control in type 1 diabetes following islet transplantation. Diabetes Care. 2015;38:105-112.
Olivares AM, Althoff K, Chen GF, et al. Animal models of diabetic retinopathy. Curr Diabetes Rep. 2017;17:93.
Bui HDT, Jing X, Lu R, et al. Prevalence of and factors related to microvascular complications in patients with type 2 diabetes mellitus in Tianjin, China: A cross-sectional study. Ann Transl Med. 2019;7:325-325.
Smith BH, Parikh T, Andrada ZP, et al. First-in-human phase 1 trial of agarose beads containing murine RENCA cells in advanced solid tumors. Cancer Growth Metastasis. 2016;9:9-20.
Smith BH, Gazda LS, Fahey TJ, et al. Clinical laboratory and imaging evidence for effectiveness of agarose-agarose macrobeads containing stem-like cells derived from a mouse renal adenocarcinoma cell population (RMBs) in treatment-resistant, advanced metastatic colorectal cancer: Evaluation of a biological-systems approach to cancer therapy (U.S. FDA IND-BB 10091; NCT 02046174, NCT 01053013). Chin J Cancer Res. 2018;30:72-83.
Hering BJ, Wijkstrom M, Graham ML, et al. Prolonged diabetes reversal after intraportal xenotransplantation of wild-type porcine islets in immunosuppressed nonhuman primates. Nat Med. 2006;12:301-303.
Thompson P, Cardona K, Russell M, et al. CD40-specific costimulation blockade enhances neonatal porcine islet survival in nonhuman primates. Am J Transplant. 2011;11:947-957.
Bottino R, Wijkstrom M, van der Windt DJ, et al. Pig-to-monkey islet xenotransplantation using multi-transgenic pigs. Am J Transplant. 2014;14:2275-2287.
Sun Y, Ma X, Zhou D, Vacek I, Sun AM. Normalization of diabetes in spontaneously diabetic cynomologus monkeys by xenografts of microencapsulated porcine islets without immunosuppression. J Clin Invest. 1996;98:1417-1422.
Elliott RB, Escobar L, Tan PLJ, et al. Intraperitoneal alginate-encapsulated neonatal porcine islets in a placebo-controlled study with 16 diabetic cynomolgus primates. Transplant Proc. 2005;37:3505-3508.
Dufrane D, Goebbels RM, Gianello P. Alginate macroencapsulation of pig islets allows correction of streptozotocin-induced diabetes in primates up to 6 months without immunosuppression. Transplantation. 2010;90:1054-1062.
Safley SA, Kenyon NS, Berman DM, et al. Microencapsulated adult porcine islets transplanted intraperitoneally in streptozotocin-diabetic non-human primates. Xenotransplantation. 2018;25:e12450.
فهرسة مساهمة: Keywords: diabetes; encapsulation; porcine islets; xenotransplantation
المشرفين على المادة: 0 (Insulin)
تواريخ الأحداث: Date Created: 20220406 Date Completed: 20220623 Latest Revision: 20220630
رمز التحديث: 20221213
DOI: 10.1111/xen.12747
PMID: 35384085
قاعدة البيانات: MEDLINE
الوصف
تدمد:1399-3089
DOI:10.1111/xen.12747