In vitro exposure of pig neonatal isletlike cell clusters to human blood

Xenotransplantation

Volumn 22, Issue 4, 2015, Pages 317-324

  Nagaraju, Santosh ^a   Bertera, Suzanne ^b   Tanaka, Takayuki ^a   Hara, Hidetaka ^a,e   Rayat, Gina R ^c   Wijkstrom, Martin ^a   Ayares, David ^d   Trucco, Massimo ^b   Cooper, David K C ^a,e   Bottino, Rita ^b  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

^d REVIVICOR INC   (United States)

^e ALLEGHENY HEALTH NETWORK   (United States)

Author keywords

diabetes mellitus; genetically engineered; instant blood mediated inflammatory reaction; islets; neonatal; pigs; xenotransplantation

Indexed keywords

C PEPTIDE; GLUTAMATE DECARBOXYLASE; ALPHA-1,3-GALACTOSYLTRANSFERASE 1, PORCINE; APYRASE; CD39 ANTIGEN; CD46 PROTEIN, HUMAN; GALACTOSYLTRANSFERASE; LEUKOCYTE ANTIGEN; MEMBRANE COFACTOR PROTEIN; RECOMBINANT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; BLOOD; BLOOD CLOTTING; BLOOD MEDIATED INFLAMMATORY REACTION; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME RELEASE; EXPOSURE; GALACTOSYLTRANSFERASE GENE KNOCKOUT PIG; GRAFT FAILURE; HUMAN; HUMAN TISSUE; HUMORAL IMMUNITY; IN VITRO STUDY; INFLAMMATION; NEONATAL ISLETLIKE CELL CLUSTER; NONHUMAN; PIGLET; PRIORITY JOURNAL; TISSUE GRAFT; WILD TYPE; XENOTRANSPLANTATION; ADVERSE EFFECTS; ANIMAL; DEFICIENCY; GENE INACTIVATION; GENETICS; IMMUNOLOGY; NEWBORN; PANCREAS ISLET TRANSPLANTATION; PATHOLOGY; PIG; PROCEDURES; TRANSGENIC ANIMAL; XENOGRAFT;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANIMALS, NEWBORN; ANTIGENS, CD; ANTIGENS, CD46; APYRASE; BLOOD; BLOOD COAGULATION; COMPLEMENT ACTIVATION; DIABETES MELLITUS; GALACTOSYLTRANSFERASES; GENE KNOCKOUT TECHNIQUES; HUMANS; IN VITRO TECHNIQUES; ISLETS OF LANGERHANS TRANSPLANTATION; RECOMBINANT PROTEINS; SUS SCROFA; TRANSPLANTATION, HETEROLOGOUS;

EID: 84938090940     PISSN: 0908665X     EISSN: 13993089     Source Type: Journal    
DOI: 10.1111/xen.12178     Document Type: Article

References (53)

1. 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.
2. 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.
3. 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.
4. Cardona K, Milas Z, Strobert E, et al.; Engraftment of adult porcine islet xenografts in diabetic nonhuman primates through targeting of costimulation pathways. Am J Transplant 2007; 7: 2260-2268.
5. van der Windt DJ, Bottino R, Casu A, et al.; Long-term controlled normoglycemia in diabetic non-human primates after transplantation with CD46 transgenic porcine islets. Am J Transplant 2009; 9: 2716-2726.
6. 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.
7. van der Windt DJ, Bottino R, Kumar G, et al.; Clinical islet xenotransplantation-how close are we? Diabetes 2012; 61: 3046-3055.
8. Groth CG, Korsgren O, Tibell A, et al.; Transplantation of porcine fetal pancreas to diabetic patients. Lancet 1994; 344: 1402-1404.
9. Elliott RB, Escobar L, Tan PL, et al.; Live encapsulated porcine islets from a type 1 diabetic patient 9.5 yr after xenotransplantation. Xenotransplantation 2007; 14: 157-161.
10. Elliott RB,. Towards xenotransplantation of pig islets in the clinic. Curr Opin Organ Transplant 2011; 16: 195-200.
11. Valdes-Gonzalez R, Rodriguez-Ventura AL, White DJ, et al.; Long-term follow-up of patients with type 1 diabetes transplanted with neonatal pig islets. Clin Exp Immunol 2010; 162: 537-542.
12. Wang W, Mo Z, Ye B, et al.; 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.
13. Bennet W, Sundberg B, Groth CG, et al.; Incompatibility between human blood and isolated islets of Langerhans: a finding with implications for clinical transplantation? Diabetes 1999; 48: 1907-1914.
14. Bennet W, Groth CG, Larsson R, Nilsson B, Korsgren O,. Isolated human islets trigger an instant blood mediated inflammatory reaction: implications for intraportal islet transplantation as a treatment for patients with type 1 diabetes. Ups J Med Sci 2000; 105: 125-133.
15. Korsgren O, Nilsson B, Berne C, et al.; Current status of clinical islet transplantation. Transplantation 2005; 79: 1289-1293.
16. van der Windt DJ, Bottino R, Casu A, Campanile N, Cooper DKC,. Rapid loss of intraportally-transplanted islets: an overview of pathophysiology and preventive strategies. Xenotransplantation 2007; 14: 288-297.
17. Naziruddin B, Iwahashi S, Kanak MA, et al.; Evidence for instant blood-mediated inflammatory reaction in clinical autologous islet transplantation. Am J Transplant 2014; 14: 428-437.
18. Nagaraju S, Bottino R, Wijkstrom M, Trucco M, Cooper DK,. Islet xenotransplantation: what is the optimal age of the islet-source pig? Xenotransplantation 2015; 22: 7-19.
19. Korbutt GS, Elliott JF, Ao Z, et al.; Large scale isolation, growth, and function of porcine neonatal islet cells. J Clin Invest 1996; 97: 2119-2129.
20. Juang JH, Hsu BRS, Kuo CH, et al.; Characteristics and transplantation of the porcine neonatal pancreatic cell clusters isolated from 1- to 3-day-old versus 1- month-old pigs. Transplant Proc 2004; 36: 1203-1205.
21. Luca G, Nastruzzi C, Calvitti M, et al.; Accelerated functional maturation of isolated neonatal porcine cell clusters: in vitro and In vivo results in NOD mice. Cell Transplant 2005; 14: 249-261.
22. Arefanian H, Tredget EB, Mok DCM, et al.; Characterization of the cell composition and function of islets isolated from different ages of newborn pigs. Xenotransplantation 2009; 16: 355.
23. Lamb M, Laugenour K, Liang O, et al.; In vitro maturation of viable islets from partially digested young pig pancreas. Cell Transplant 2014; 23: 263-272.
24. Vizzardelli C, Molano RD, Pileggi A, et al.; Neonatal porcine pancreatic cell clusters as a potential source for transplantation in humans: characterization of proliferation, apoptosis, xenoantigen expression and gene delivery with recombinant AAV. Xenotransplantation 2002; 9: 14-24.
25. Bloch K, Assa S, Lazard D, et al.; Neonatal pig islets induce a lower T-cell response than adult pig islets in IDDM patients. Transplantation 1999; 67: 748-752.
26. Emamaullee JA, Shapiro AM, Rajotte RV, Korbutt G, Elliott JF,. Neonatal porcine islets exhibit natural resistance to hypoxia-induced apoptosis. Transplantation 2006; 82: 945-952.
27. Ji M, Yi S, Smith-Hurst H, et al.; The importance of tissue factor expression by porcine NICC in triggering IBMIR in the xenograft setting. Transplantation 2011; 91: 841-846.
28. Elliott RB, Escobar L, Tan PL, et al.; Intraperitoneal alginate-encapsulated neonatal porcine islets in a placebo-controlled study with 16 diabetic cynomolgus primates. Transplant Proc 2005; 37: 3505-3508.
29. Isaac JR, Skinner S, Elliot R, et al.; Transplantation of neonatal porcine islets and sertoli cells into nonimmunosuppressed nonhuman primates. Transplant Proc 2005; 37: 487-488.
30. Thompson P, Badell IR, Lowe M, et al.; Islet xenotransplantation using Gal-deficient neonatal donors improves engraftment and function. Am J Transplant 2011; 11: 2593-2602.
31. Thompson P, Badell IR, Lowe M, et al.; Alternative immunomodulatory strategies for xenotransplantation: CD40/154 pathway-sparing regimens promote xenograft survival. Am J Transplant 2012; 12: 1765-1775.
32. Hawthorne WJ, Salvaris EJ, Phillips P, et al.; Control of IBMIR in neonatal porcine islet xenotransplantation in baboons. Am J Transplant 2014; 14: 1300-1309.
33. Phelps CJ, Koike C, Vaught TD, et al.; Production of alpha 1,3-galactosyltransferase-deficient pigs. Science 2003; 299: 411-414.
34. Rayat GR, Rajotte RV, Hering BJ, Binette TM, Korbutt GS,. In vitro and in vivo expression of Galalpha-(1,3)Gal on porcine islet cells is age dependent. J Endocrinol 2003; 177: 127-135.
35. Galili U, Rachmilewitz EA, Peleg A, Flechner I,. A unique natural human IgG antibody with anti-alpha-galactosyl specificity. J Exp Med 1984; 160: 1519-1531.
36. Cooper DKC,. Depletion of natural antibodies in non-human primates-a step towards successful discordant xenografting in humans. Clin Transplant 1992; 6: 178-183.
37. Good AH, Cooper DKC, Malcolm AJ, et al.; Identification of carbohydrate structures that bind human antiporcine antibodies: implications for discordant xenografting in man. Transplant Proc 1992; 24: 559-562.
38. van der Windt DJ, Marigliano M, He J, et al.; Early islet damage after direct exposure of pig islets to blood: has humoral immunity been underestimated? Cell Transplant 2012; 21: 1791-1802.
39. Rayat GR, Gill RG,. Indefinite survival of neonatal porcine islet xenografts by simultaneous targeting of LFA-1 and CD154 or CD45RB. Diabetes 2005; 54: 443-451.
40. Cowan PJ, d'Apice AJF,. Complement activation and coagulation in xenotransplantation. Immunol Cell Biol 2009; 87: 203-208.
41. Kang HJ, Lee H, Ha J, et al.; The role of the alternative complement pathway in early graft loss after intraportal porcine islet xenotransplantation. Transplantation 2014; 97: 999-1008.
42. Greene SA, Smith MA, Cartwright B, Baum JD,. Comparison of human versus porcine insulin in treatment of diabetes in children. Br Med J (Clin Res Ed) 1983; 287: 1578-1579.
43. Ekser B, Ezzelarab M, Hara H, et al.; Clinical xenotransplantation: the next medical revolution? Lancet 2012; 379: 672-683.
44. Rayat GR, Rajotte RV, Elliott JF, Korbutt GS,. Expression of Gal alpha(1,3)gal on neonatal porcine islet beta-cells and susceptibility to human antibody/complement lysis. Diabetes 1998; 47: 1406-1411.
45. Goto M, Tjernberg J, Dufrane D, et al.; Dissecting the instant blood mediated inflammatory reaction in islet xenotransplantation. Xenotransplantation 2008; 15: 225-234.
46. Bennet W, Sundberg B, Lundgren T, et al.; Damage to porcine islets of Langerhans after exposure to human blood in vitro, or after intraportal transplantation to cynomologus monkeys: protective effects of sCR1 and heparin. Transplantation 2000; 69: 711-719.
47. Komoda H, Miyagawa S, Kubo T, et al.; A study of the xenoantigenicity of adult pig islets cells. Xenotransplantation 2004; 11: 237-246.
48. Omori T, Nishida T, Komoda H, et al.; A study of the xenoantigenicity of neonatal porcine islet-like cell clusters (NPCC) and the efficiency of adenovirus-mediated DAF (CD55) expression. Xenotransplantation 2006; 13: 455-464.
49. Park JY, Park MR, Kwon DN, et al.; Alpha 1,3-Galactosyltransferase deficiency in pigs increases sialyltransferase activities that potentially raise non-Gal xenogenicity. J Biomed Biotechnol 2011; 2011: 56085.
50. Lutz AJ, Li P, Estrada JL, et al.; Double knockout pigs deficient in N-glycolylneuraminic acid and galactose α1,3-galactose reduce the humoral barrier to xenotransplantation. Xenotransplantation 2013; 20: 27-35.
51. Burlak C, Paris LL, Lutz AJ, et al.; Reduced binding of human antibodies to cells from GGTA1/CMAH KO pigs. Am J Transplant 2014; 14: 1895-1900.
52. Reddy S, Wu D, Poole CA,. Glutamic acid decarboxylase 65 and 67 isoforms in fetal, neonatal and adult porcine islets: predominant beta cell co-localization by light and confocal microscopy. J Autoimmun 1996; 9: 21-27.
53. Schlosser M, Walschus U, Klöting I, Walther R,. Determination of glutamic acid decarboxylase (GAD65) in pancreatic islets and its in vitro and in vivo degradation kinetics in serum using a highly sensitive enzyme immunoassay. Dis Markers 2008; 24: 191-198.