Pathology of an islet transplant 2 years after transplantation: Evidence for a nonimmunological loss

Transplantation

Volumn 86, Issue 1, 2008, Pages 54-62

  Smith, R Neal ^a   Kent, Sally C ^b   Nagle, Julie ^a   Selig, Martin ^a   Iafrate, A John ^a   Najafian, Nader ^b   Hafler, David A ^b   Auchincloss, Hugh ^a   Orban, Tihamer ^c   Cagliero, Enrico ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Autoimmunity; Islet; Rejection; Transplant

Indexed keywords

ALLOANTIBODY; C PEPTIDE; INSULIN; ANTIDIABETIC AGENT; GLYCOSYLATED HEMOGLOBIN; HEMOGLOBIN A1C PROTEIN, HUMAN;

ADULT; ARTICLE; AUTOIMMUNITY; AUTOPSY; CASE REPORT; DIABETES MELLITUS; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; KIDNEY ALLOGRAFT; PANCREAS ISLET TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN SECRETION; STROKE; ATROPHY; BLOOD; FATALITY; GRAFT REJECTION; GRAFT SURVIVAL; IMMUNOLOGY; INSULIN DEPENDENT DIABETES MELLITUS; METABOLISM; MIDDLE AGED; PANCREAS ISLET; PATHOLOGY; PORTAL VEIN; TREATMENT FAILURE;

ATROPHY; AUTOPSY; C-PEPTIDE; DIABETES MELLITUS, TYPE 1; FATAL OUTCOME; FEMALE; GRAFT REJECTION; GRAFT SURVIVAL; HEMOGLOBIN A, GLYCOSYLATED; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; ISLETS OF LANGERHANS; ISLETS OF LANGERHANS TRANSPLANTATION; MIDDLE AGED; PORTAL VEIN; TREATMENT FAILURE;

EID: 49849092250     PISSN: 00411337     EISSN: None     Source Type: Journal    
DOI: 10.1097/TP.0b013e318173a5da     Document Type: Article

References (59)

1. Shapiro AM, Lakey JR, Ryan EA, et al. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free im-munosuppressive regimen. N Engl J Med 2000; 343: 230.
2. Shapiro AM, Ricordi C, Hering B. Edmonton's islet success has indeed been replicated elsewhere. Lancet 2003; 362: 1242.
3. Shapiro AM, Ricordi C, Hering BJ, et al. International trial of the Edmonton protocol for islet transplantation. N Engl J Med 2006; 355: 1318.
4. Froud T, Ricordi C, Baidal DA, et al. Islet transplantation in type 1 diabetes mellitus using cultured islets and steroid-free immunosup-pression: Miami experience. Am J Transplant 2005; 5: 2037.
5. Ryan EA, Paty BW, Senior PA, et al. Five-year follow-up after clinical islet transplantation. Diabetes 2005; 54: 2060.
6. Smith RN, Brousaides N, Grazette L, et al. C4d deposition in cardiac allografts correlates with alloantibody. J Heart Lung Transplant 2005; 24: 1202.
7. Collins AB, Schneeberger EE, Pascual MA, et al. Complement activation in acute humoral renal allograft rejection: Diagnostic significance of C4d deposits in peritubular capillaries. J Am Soc Nephrol 1999; 10: 2208.
8. Davalli AM, Maffi P, Socci C, et al. Insights from a successful case of intrahepatic islet transplantation into a type 1 diabetic patient. J Clin Endocrinol Metab 2000; 85: 3847.
9. Verge CF, Gianani R, Kawasaki E, et al. Prediction of type I diabetes in first-degree relatives using a combination of insulin, GAD, and ICA512bdc/IA-2 autoantibodies. Diabetes 1996; 45: 926.
10. Sayegh MH. Why do we reject a graft? Role of indirect allorecognition in graft rejection. Kidney Int 1999; 56: 1967.
11. Najafian N, Salama AD, Fedoseyeva EV, et al. Enzyme-linked immu-nosorbent spot assay analysisof peripheral blood lymphocyte reactivity to donor HLA-DR peptides: Potential novel assay for prediction of outcomes for renal transplant recipients. J Am Soc Nephrol 2002; 13: 252.
12. Cardarelli F, Pascual M, Tolkoff-Rubin N, et al. Prevalence and significance of anti-HLA and donor-specific antibodies long-term after renal transplantation. Transpl Int 2005; 18: 532.
13. Racusen LC, Solez K, Colvin RB, et al. The Banff 97 working classification of renal allograft pathology. Kidney Int 1999; 55: 713.
14. Colvin RB, Smith RN. Antibody-mediated organ-allograft rejection. Nat Rev Immunol 2005; 5: 807.
15. Griffith RC, Scharp DW, Hartman BK, et al. A morphologic study of intrahepatic portal-vein islet isografts. Diabetes 1977; 26: 201.
16. Ricordi C, Tzakis A, Alejandro R, et al. Detection of pancreatic islet tissue following islet allotransplantation in man. Transplantation 1991; 52: 1079.
17. Sever CE, Demetris AJ, Zeng Y, et al. Islet cell allotransplantation in diabetic patients. Histologic findings in four adults simultaneously receiving kidney or liver transplants. Am J Pathol 1992; 140: 1255.
18. Lacy PE. The pancreatic beta cell. Structure and function. N Engl J Med 1967; 276: 187.
19. Finzi G, Davalli A, Placidi C, et al. Morphological and ultrastructural features of human islet grafts performed in diabetic nude mice. Ultra-struct Pathol 2005; 29: 525.
20. Hart TK, Pino RM. Pseudoislet vascularization. Induction of diaphragm-fenestrated endothelia from the hepatic sinusoids. Lab Invest 1986; 54: 304.
21. Vajkoczy P, Olofsson AM, Lehr HA, et al. Histogenesis and ultrastruc-ture of pancreatic islet graft microvasculature. Evidence for graft revas-cularization by endothelial cells of host origin. Am J Pathol 1995; 146: 1397.
22. Hyon SH, Ceballos MC, Barbich M, et al. Effect of the embolization of completely unpurified islets on portal vein pressure and hepatic biochemistry in clinical practice. Cell Transplant 2004; 13: 61.
23. Casey JJ, Lakey JR, Ryan EA, et al. Portal venous pressure changes after sequential clinical islet transplantation. Transplantation 2002; 74: 913.
24. White SA, Davies JE, Pollard C, et al. Pancreas resection and islet autotransplantation for end-stage chronic pancreatitis. Ann Surg 2001; 233: 423.
25. Colvin RB, Nickeleit V. Renal transplant pathology. In: Jennette JC, Olson JL, Schwartz MM, et al., eds. Heptinstall's pathology of the kidney, vol. 2. Philadelphia, Lippincott-Raven 2006, p 1347.
26. Lohr M, Kloppel G. Residual insulin positivity and pancreatic atrophy in relation to duration of chronic type 1 (insulin-dependent) diabetes mellitus and microangiopathy. Diabetologia 1987; 30: 757.
27. Foulis AK, Stewart JA. The pancreas in recent-onset type 1 (insulin-dependent) diabetes mellitus: Insulin content of islets, insulitis and associated changes in the exocrine acinar tissue. Diabetologia 1984; 26: 456.
28. Meier JJ, Bhushan A, Butler AE, et al. Sustained beta cell apoptosis in patients with long-standing type 1 diabetes: Indirect evidence for islet regeneration? Diabetologia 2005; 48: 2221.
29. Koulmanda M, Smith RN, Qipo A, et al. Prolonged survival of alloge-neic islets in cynomolgus monkeys after short-term anti-CD154-based therapy: Nonimmunologic graft failure? Am J Transplant 2006; 6: 687.
30. Kenyon NS, Fernandez LA, Lehmann R, et al. Long-term survival and functionof intrahepatic islet allograftsin baboons treated with humanized anti-CD154. Diabetes 1999; 48: 1473.
31. Terasaki PI, Ozawa M. Predictive value of HLA antibodies and serum creatinine in chronic rejection: Results of a 2-year prospective trial. Transplantation 2005; 80: 1194.
32. Campbell PM, Salam A, Ryan EA, et al. Pretransplant HLA antibodies are associated with reduced graft survival after clinical islet transplantation. Am J Transplant 2007; 7: 1242.
33. Campbell PM, Senior PA, Salam A, et al. High risk of sensitization after failed islet transplantation. Am J Transplant 2007; 7: 2311.
34. Roep BO, Stobbe I, Duinkerken G, et al. Auto- and alloimmune reac- tivity to human islet allografts transplanted into type 1 diabetic patients. Diabetes 1999; 48: 484.
35. Lohmann T, Klemm T, Geissler F, et al. Islet cell-specific autoantibod-ies as potential markers for recurrence of autoimmune type 1 diabetes after simultaneous pancreas-kidney transplantation. Transplant Proc 2002; 34: 2249.
36. Repka J, Nicoluzzi J, Belila R, et al. Pancreatic islet cells antibodies in diabetic patients submitted to pancreas transplantation. Transplant Proc 2006; 38: 3031.
37. Alejandro R, Cutfield RG, Shienvold FL, et al. Natural history of intra-hepatic canine islet cell autografts. J Clin Invest 1986; 78: 1339.
38. Clayton HA, Davies JE, Pollard CA, et al. Pancreatectomy with islet autotransplantation for the treatment of severe chronic pancreatitis: The first 40 patients at the leicester general hospital. Transplantation 2003; 76: 92.
39. Robertson RP, Lanz KJ, Sutherland DE,etal. Prevention of diabetes for up to 13 years by autoislet transplantation after pancreatectomy for chronic pancreatitis. Diabetes 2001; 50: 47.
40. Teuscher AU, Kendall DM, Smets YF, et al. Successful islet autotransplantation in humans: Functional insulin secretory reserve as an estimate of surviving islet cell mass. Diabetes 1998; 47: 324.
41. Pyzdrowski KL, Kendall DM, Halter JB, et al. Preserved insulin secretion and insulin independence in recipients of islet autografts. N Engl J Med 1992; 327: 220.
42. Oberholzer J, Mathe Z, Bucher P, et al. Islet autotransplantation after left pancreatectomy for non-enucleable insulinoma. Am J Transplant 2003; 3: 1302.
43. Juang JH, Bonner-Weir S, Wu YJ, et al. Beneficial influence of glycemic control upon the growth and function of transplanted islets. Diabetes 1994; 43: 1334.
44. Melzi R, Battaglia M, Draghici E, et al. Relevance of hyperglycemia on the timing of functional loss of allogeneic islet transplants: Implication for mouse model. Transplantation 2007; 83: 167.
45. Makhlouf L, Duvivier-Kali VF, Bonner-Weir S, et al. Importance of hyperglycemia on the primary function of allogeneic islet transplants. Transplantation 2003; 76: 657.
46. Laybutt DR, Sharma A, Sgroi DC, et al. Genetic regulation of metabolic pathways in beta-cells disrupted by hyperglycemia. J Biol Chem 2002; 277: 10912.
47. Weir GC, Bonner-Weir S. Five stages of evolving beta-cell dysfunction during progression to diabetes. Diabetes 2004; 53(suppl 3): S16.
48. Ahn YB, Xu G, Marselli L, et al. Changes in gene expression in beta cells after islet isolation and transplantation using laser-capture microdis-section. Diabetologia 2007; 50: 334.
49. Desai NM, Goss JA, Deng S, et al. Elevated portal vein drug levels of sirolimus and tacrolimus in islet transplant recipients: Local immuno-suppression or islet toxicity? Transplantation 2003; 76: 1623.
50. Hyder A, Laue C, Schrezenmeir J. Effect of the immunosuppressive regime of Edmonton protocol on the long-term in vitro insulin secretion from islets of two different species and age categories. Toxicol In Vitro 2005; 19: 541.
51. Shapiro AM, Gallant HL, Hao EG,etal. The portal immunosuppressive storm: Relevancetoislet transplantation?Ther Drug Monit2005; 27: 35.
52. JanssonL,Carlsson PO. Graft vascular function after transplantation of pancreatic islets. Diabetologia 2002; 45: 749.
53. Brunicardi FC, Stagner J, Bonner-Weir S, et al. Microcirculation of the islets of Langerhans. Long Beach Veterans Administration Regional Medical Education Center Symposium. Diabetes 1996; 45: 385.
54. Vasir B, Reitz P, Xu G, et al. Effects of diabetes and hypoxia on gene markers of angiogenesis (HGF, cMET, uPA and uPAR, TGF-alpha, TGF-beta, bFGF and Vimentin) in cultured and transplanted rat islets. Diabetologia 2000; 43: 763.
55. Bonner-Weir S, Sharma A. Pancreatic stem cells. J Pathol 2002; 197: 519.
56. Dor Y, Brown J, Martinez OI, et al. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 2004; 429: 41.
57. Bouwens L, Rooman I. Regulation of pancreatic beta-cell mass. Physiol Rev 2005; 85: 1255.
58. Bouwens L, Lu WG, de Krijger R. Proliferation and differentiation in the human fetal endocrine pancreas. Diabetologia 1997; 40: 398.
59. Hayek A, Beattie GM, Cirulli V, et al. Growth factor/matrix-induced proliferation of human adult beta-cells. Diabetes 1995; 44: 1458.