Innate immunity and heat shock response in islet transplantation

Clinical and Experimental Immunology

Volumn 157, Issue 1, 2009, Pages 1-8

  Lai, Y ^b   Chen, C ^c   Linn, T ^a,c  

^a Clinical Research Unit   (Germany)

^b University of Missouri   (United States)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Heat shock response; Inflammation; Innate immunity; Islet transplantation; Stress

Indexed keywords

ADENOVIRUS VECTOR; CHEMOKINE RECEPTOR CCR2; CLODRONIC ACID; GADOLINIUM CHLORIDE; GAMMA INTERFERON; HEAT SHOCK PROTEIN 70; HEME OXYGENASE 1; INSULIN; INTERLEUKIN 1BETA; INTERLEUKIN 2 RECEPTOR ANTIBODY; MACROPHAGE INFLAMMATORY PROTEIN 1; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 1 ANTIBODY; PROTEIN ANTIBODY; RANTES; RAPAMYCIN; TACROLIMUS; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; BLOOD GLUCOSE MONITORING; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COMPLEMENT ACTIVATION; CYTOKINE PRODUCTION; DENDRITIC CELL; GRAFT REJECTION; GRAFT SURVIVAL; HEAT SHOCK; HUMAN; INFLAMMATION; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; LOW DRUG DOSE; MACROPHAGE; NATURAL KILLER T CELL; NEUTROPHIL; NONHUMAN; PANCREAS ISLET TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; THROMBOCYTE; TRANSPLANTATION TOLERANCE;

ANIMALS; BLOOD PLATELETS; COMPLEMENT SYSTEM PROTEINS; CYTOKINES; DIABETES MELLITUS, TYPE 1; GRAFT SURVIVAL; HEAT-SHOCK RESPONSE; HUMANS; IMMUNITY, INNATE; ISLETS OF LANGERHANS TRANSPLANTATION; POSTOPERATIVE COMPLICATIONS; TREATMENT OUTCOME;

EID: 66849132584     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2009.03899.x     Document Type: Review

References (90)

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 8.
2. Shapiro AM, Ricordi C, Hering BJ et al. International trial of the Edmonton protocol for islet transplantation. N Engl J Med 2006 355 : 1318 30.
3. Lai Y, Schneider D, Kidszun A et al. Vascular endothelial growth factor increases functional beta-cell mass by improvement of angiogenesis of isolated human and murine pancreatic islets. Transplantation 2005 79 : 1530 6.
4. Linn T, Schmitz J, Hauck-Schmalenberger I et al. Ischaemia is linked to inflammation and induction of angiogenesis in pancreatic islets. Clin Exp Immunol 2006 144 : 179 87.
5. Yokoyama WM, Kim S, French AR. The dynamic life of natural killer cells. Annu Rev Immunol 2004 22 : 405 29.
6. Raulet DH. Interplay of natural killer cells and their receptors with the adaptive immune response. Nat Immunol 2004 5 : 996 1002. (Pubitemid 41057716)
7. Hamerman JA, Ogasawara K, Lanier LL. NK cells in innate immunity. Curr Opin Immunol 2005 17 : 29 35. (Pubitemid 40094010)
8. Sun W, He X, Guo Z et al. IL-12p40-overexpressing immature dendritic cells induce T cell hyporesponsiveness in vitro but accelerate allograft rejection in vivo: role of NK cell activation and interferon-gamma production. Immunol Lett 2004 94 : 191 9.
9. Beilke JN, Kuhl NR, Van Kaer L, Gill RG. NK cells promote islet allograft tolerance via a perforin-dependent mechanism. Nat Med 2005 11 : 1059 65.
10. Ramirez-Victorio F, Beilke JN, Gill RG. Both innate and adaptive major histocompatibility complex class I-dependent immunity impair long-term islet xenograft survival. Transplant Proc 2008 40 : 557 8.
11. Devos T, Shengqiao L, Gysemans C et al. Late CD8+ T cell-dependent xenoantibody production in innate tolerant nude rats after hamster islet grafting but not after hamster heart grafting. Transplantation 2008 85 : 1489 95.
12. Devos T, Yan Y, Segers C et al. Role of CD4+ and CD8+ T cells in the rejection of heart or islet xenografts in recipients with xenotolerance in the innate immune compartment. Transplant Proc 2005 37 : 516 17.
13. Murray AG, Nelson RC, Rayat GR et al. Neonatal porcine islet cells induce human CD4+, but not CD8+, lymphocyte proliferation and resist cell-mediated cytolytic injury in vitro. Diabetes 1999 48 : 1713 19.
14. Kumagai-Braesch M, Satake M, Qian Y et al. Human NK cell and ADCC reactivity against xenogeneic porcine target cells including fetal porcine islet cells. Xenotransplantation 1998 5 : 132 45.
15. Uppaluri R, Sheehan KC, Wang L et al. Prolongation of cardiac and islet allograft survival by a blocking hamster anti-mouse CXCR3 monoclonal antibody. Transplantation 2008 86 : 137 47.
16. Yasunami Y, Kojo S, Kitamura H et al. Valpha14 NK T cell-triggered IFN-gamma production by Gr-1+CD11b+ cells mediates early graft loss of syngeneic transplanted islets. J Exp Med 2005 202 : 913 18.
17. Piemonti L, Leone BE, Nano R et al. Human pancreatic islets produce and secrete MCP-1/CCL2: relevance in human islet transplantation. Diabetes 2002 51 : 55 65. (Pubitemid 34517980)
18. Ehrnfelt C, Kumagai-Braesch M, Uzunel M, Holgersson J. Adult porcine islets produce MCP-1 and recruit human monocytes in vitro. Xenotransplantation 2004 11 : 184 94.
19. Omer A, Keegan M, Czismadia E et al. Macrophage depletion improves survival of porcine neonatal pancreatic cell clusters contained in alginate macrocapsules transplanted into rats. Xenotransplantation 2003 10 : 240 51.
20. de Vos P, Smedema I, van Goor H et al. Association between macrophage activation and function of micro-encapsulated rat islets. Diabetologia 2003 46 : 666 73.
21. Yi S, Ouyang L, Ha H et al. Involvement of CCR5 signaling in macrophage recruitment to porcine islet xenografts. Transplantation 2005 80 : 1468 75.
22. Solomon MF, Kuziel WA, Mann DA, Simeonovic CJ. The role of chemokines and their receptors in the rejection of pig islet tissue xenografts. Xenotransplantation 2003 10 : 164 77.
23. Chandra AP, Ouyang L, Yi S et al. Chemokine and Toll-like receptor signaling in macrophage mediated islet xenograft rejection. Xenotransplantation 2007 14 : 48 59. (Pubitemid 46051369)
24. Janeway CAJ, Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002 20 : 197 216. (Pubitemid 34293424)
25. Akira S, Takeda K, Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2001 2 : 675 80.
26. Aderem A, Ulevitch RJ. Toll-like receptors in the induction of the innate immune response. Nature 2000 406 : 782 7.
27. Yi S, Wang Y, Chandra AP et al. Requirement of MyD88 for macrophage-mediated islet xenograft rejection after adoptive transfer. Transplantation 2007 83 : 615 23.
28. Bottino R, Fernandez LA, Ricordi C et al. Transplantation of allogeneic islets of Langerhans in the rat liver: effects of macrophage depletion on graft survival and microenvironment activation. Diabetes 1998 47 : 316 23.
29. Rossi L, Migliavacca B, Pierige F et al. Prolonged islet allograft survival in diabetic mice upon macrophage depletion by clodronate-loaded erythrocytes. Transplantation 2008 85 : 648 50.
30. Andres A, Toso C, Morel P et al. Macrophage depletion prolongs discordant but not concordant islet xenograft survival. Transplantation 2005 79 : 543 9.
31. van der Windt DJ, Bottino R, Casu A et al. Rapid loss of intraportally transplanted islets: an overview of pathophysiology and preventive strategies. Xenotransplantation 2007 14 : 288 97.
32. Titus TT, Horton PJ, Badet L et al. Adverse outcome of human islet-allogeneic blood interaction. Transplantation 2003 75 : 1317 22.
33. 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 19.
34. Moberg L, Korsgren O, Nilsson B. Neutrophilic granulocytes are the predominant cell type infiltrating pancreatic islets in contact with ABO-compatible blood. Clin Exp Immunol 2005 142 : 125 31.
35. Moberg L. The role of the innate immunity in islet transplantation. Ups J Med Sci 2005 110 : 17 55. (Pubitemid 40342459)
36. Fiorina P, Jurewicz M, Tanaka K et al. Characterization of donor dendritic cells and enhancement of dendritic cell efflux with CC-chemokine ligand 21: a novel strategy to prolong islet allograft survival. Diabetes 2007 56 : 912 20.
37. Wang L, Han R, Lee I et al. Permanent survival of fully MHC-mismatched islet allografts by targeting a single chemokine receptor pathway. J Immunol 2005 175 : 6311 18.
38. Gunn MD. Chemokine mediated control of dendritic cell migration and function. Semin Immunol 2003 15 : 271 6.
39. Fiorina P, Jurewicz M, Vergani A et al. Phenotypic and functional differences between wild-type and CCR2-/- dendritic cells: implications for islet transplantation. Transplantation 2008 85 : 1030 8.
40. Zhu H, Qiu W, Lei P et al. IL-10 gene modified dendritic cells inhibit T helper type 1-mediated alloimmune responses and promote immunological tolerance in diabetes. Cell Mol Immunol 2008 5 : 41 6.
41. Tjernberg J, Ekdahl KN, Lambris JD et al. Acute antibody-mediated complement activation mediates lysis of pancreatic islets cells and may cause tissue loss in clinical islet transplantation. Transplantation 2008 85 : 1193 9.
42. Rood PP, Bottino R, Balamurugan AN et al. Reduction of early graft loss after intraportal porcine islet transplantation in monkeys. Transplantation 2007 83 : 202 10.
43. Schuurman HJ, Pierson RNR. Progress towards clinical xenotransplantation. Front Biosci 2008 13 : 204 20.
44. Kobayashi T, Harb G, Rajotte RV et al. Immune mechanisms associated with the rejection of encapsulated neonatal porcine islet xenografts. Xenotransplantation 2006 13 : 547 59.
45. Murakami Y, Iwata H, Kitano E et al. Interaction of poly(styrene sulfonic acid) with the classical pathway of the serum complement system. J Biomater Sci Polym Ed 2005 16 : 685 97.
46. Goto M, Johansson H, Maeda A et al. Low molecular weight dextran sulfate prevents the instant blood-mediated inflammatory reaction induced by adult porcine islets. Transplantation 2004 77 : 741 7.
47. Johansson U, Elgue G, Nilsson B, Korsgren O. Composite islet-endothelial cell grafts: a novel approach to counteract innate immunity in islet transplantation. Am J Transplant 2005 5 : 2632 9.
48. Gysemans C, Callewaert H, Overbergh L, Mathieu C. Cytokine signalling in the beta-cell: a dual role for IFNgamma. Biochem Soc Trans 2008 36 : 328 33.
49. Monti P, Scirpoli M, Maffi P et al. Islet transplantation in patients with autoimmune diabetes induces homeostatic cytokines that expand autoreactive memory T cells. J Clin Invest 2008 118 : 1806 14.
50. Lee I, Wang L, Wells AD et al. Blocking the monocyte chemoattractant protein-1/CCR2 chemokine pathway induces permanent survival of islet allografts through a programmed death-1 ligand-1-dependent mechanism. J Immunol 2003 171 : 6929 35.
51. Abdi R, Means TK, Ito T et al. Differential role of CCR2 in islet and heart allograft rejection: tissue specificity of chemokine/chemokine receptor function in vivo. J Immunol 2004 172 : 767 75.
52. Schroppel B, Zhang N, Chen P et al. Role of donor-derived monocyte chemoattractant protein-1 in murine islet transplantation. J Am Soc Nephrol 2005 16 : 444 51.
53. Baker MS, Chen X, Rotramel AR et al. Genetic deletion of chemokine receptor CXCR3 or antibody blockade of its ligand IP-10 modulates posttransplantation graft-site lymphocytic infiltrates and prolongs functional graft survival in pancreatic islet allograft recipients. Surgery 2003 134 : 126 33.
54. Abdi R, Smith RN, Makhlouf L et al. The role of CC chemokine receptor 5 (CCR5) in islet allograft rejection. Diabetes 2002 51 : 2489 95.
55. Yang L, Liu YF, Wu G et al. Blocking the CC chemokine receptor 5 pathway by antisense peptide nucleic acid prolongs islet allograft survival. Transplant Proc 2007 39 : 185 90.
56. Akashi S, Sho M, Kashizuka H et al. A novel small-molecule compound targeting CCR5 and CXCR3 prevents acute and chronic allograft rejection. Transplantation 2005 80 : 378 84.
57. Kehrel BE, Jurk K. Platelets at the interface between hemostasis and innate immunity. Transfus Med Hemother 2004 31 : 379 86.
58. Bennet W, Sundberg B, Groth CG et al. Incompatibility between human blood and isolated islets of Langerhans: a finding with implications for clinical intraportal islet transplantation? Diabetes 1999 48 : 1907 14.
59. Moberg L, Johansson H, Lukinius A et al. Production of tissue factor by pancreatic islet cells as a trigger of detrimental thrombotic reactions in clinical islet transplantation. Lancet 2002 360 : 2039 45.
60. Ozmen L, Ekdahl KN, Elgue G et al. Inhibition of thrombin abrogates the instant blood-mediated inflammatory reaction triggered by isolated human islets: possible application of the thrombin inhibitor melagatran in clinical islet transplantation. Diabetes 2002 51 : 1779 84.
61. Moberg L, Olsson A, Berne C et al. Nicotinamide inhibits tissue factor expression in isolated human pancreatic islets: implications for clinical islet transplantation. Transplantation 2003 76 : 1285 8.
62. Sonna LA, Gaffin SL, Pratt RE et al. Effect of acute heat shock on gene expression by human peripheral blood mononuclear cells. J Appl Physiol 2002 92 : 2208 20.
63. Bellmann K, Wenz A, Radons J et al. Heat shock induces resistance in rat pancreatic islet cells against nitric oxide, oxygen radicals and streptozotocin toxicity in vitro. J Clin Invest 1995 95 : 2840 5.
64. Burkart V, Liu H, Bellmann K et al. Natural resistance of human beta cells toward nitric oxide is mediated by heat shock protein 70. J Biol Chem 2000 275 : 19521 8.
65. Bellmann K, Jaattela M, Wissing D et al. Heat shock protein hsp70 overexpression confers resistance against nitric oxide. FEBS Lett 1996 391 : 185 8.
66. Bellmann K, Hui L, Radons J et al. Low stress response enhances vulnerability of islet cells in diabetes-prone BB rats. Diabetes 1997 46 : 232 6.
67. Wachlin G, Heine L, Kloting I et al. Stress response of pancreatic islets from diabetes prone BB rats of different age. Autoimmunity 2002 35 : 389 95.
68. Scarim AL, Heitmeier MR, Corbett JA. Heat shock inhibits cytokine-induced nitric oxide synthase expression by rat and human islets. Endocrinology 1998 139 : 5050 7.
69. Desmard M, Boczkowski J, Poderoso J, Motterlini R. Mitochondrial and cellular heme-dependent proteins as targets for the bioactive function of the heme oxygenase/carbon monoxide system. Antioxid Redox Signal 2007 9 : 2139 55.
70. Lundquist I, Alm P, Salehi A et al. Carbon monoxide stimulates insulin release and propagates Ca2+ signals between pancreatic beta-cells. Am J Physiol Endocrinol Metab 2003 285 : E1055 63.
71. Ollinger R, Wang H, Yamashita K et al. Therapeutic applications of bilirubin and biliverdin in transplantation. Antioxid Redox Signal 2007 9 : 2175 85.
72. Soares MP, Bach FH. Heme oxygenase-1 in organ transplantation. Front Biosci 2007 12 : 4932 45.
73. Camara NO, Soares MP. Heme oxygenase-1 (HO-1), a protective gene that prevents chronic graft dysfunction. Free Radic Biol Med 2005 38 : 426 35.
74. Bach FH. Heme oxygenase-1 and transplantation tolerance. Hum Immunol 2006 67 : 430 2.
75. Won KC, Moon JS, Eun MJ et al. A protective role for heme oxygenase-1 in INS-1 cells and rat islets that are exposed to high glucose conditions. J Korean Med Sci 2006 21 : 418 24.
76. Abraham NG, Tsenovoy PL, McClung J, Drummond GS. Heme oxygenase: a target gene for anti-diabetic and obesity. Curr Pharm Des 2008 14 : 412 21.
77. Lee SS, Gao W, Mazzola S et al. Heme oxygenase-1, carbon monoxide, and bilirubin induce tolerance in recipients toward islet allografts by modulating T regulatory cells. FASEB J 2007 21 : 3450 7.
78. Brusko TM, Wasserfall CH, Agarwal A et al. An integral role for heme oxygenase-1 and carbon monoxide in maintaining peripheral tolerance by CD4+CD25+ regulatory T cells. J Immunol 2005 174 : 5181 6.
79. Wang H, Lee SS, Gao W et al. Donor treatment with carbon monoxide can yield islet allograft survival and tolerance. Diabetes 2005 54 : 1400 6.
80. Chen XB, Li YX, Jiao Y et al. Influence of heme oxygenase-1 gene transfer on the viability and function of rat islets in in vitro culture. World J Gastroenterol 2007 13 : 1053 9.
81. Li Y, Li G, Dong W et al. Transplantation of rat islets transduced with Hum heme oxygenase-1 gene using adenovirus vector. Pancreas 2006 33 : 280 6.
82. Lee DY, Lee S, Nam JH, Byun Y. Minimization of immunosuppressive therapy after islet transplantation: combined action of heme oxygenase-1 and PEGylation to islet. Am J Transplant 2006 6 : 1820 8.
83. Ribeiro MM, Klein D, Pileggi A et al. Heme oxygenase-1 fused to a TAT peptide transduces and protects pancreatic beta-cells. Biochem Biophys Res Commun 2003 305 : 876 81.
84. Ye J, Laychock SG. A protective role for heme oxygenase expression in pancreatic islets exposed to interleukin-1beta. Endocrinology 1998 139 : 4155 63.
85. Tobiasch E, Gunther L, Bach FH. Heme oxygenase-1 protects pancreatic beta cells from apoptosis caused by various stimuli. J Invest Med 2001 49 : 566 71.
86. Pileggi A, Molano RD, Berney T et al. Heme oxygenase-1 induction in islet cells results in protection from apoptosis and improved in vivo function after transplantation. Diabetes 2001 50 : 1983 91.
87. Brandhorst D, Hammes HP, Brandhorst H et al. Pretransplant induction of HSP-70 in isolated adult pig islets decreases early islet xenograft survival. Cell Transplant 2000 9 : 423 30.
88. Brandhorst D, Brandhorst H, Kumarasamy V et al. Hyperthermic preconditioning protects pig islet grafts from early inflammation but enhances rejection in immunocompetent mice. Cell Transplant 2003 12 : 859 65.
89. Brandhorst H, Olbrich M, Neumann A et al. Effect of pretransplant preconditioning by whole body hyperthermia on islet graft survival. Cell Transplant 2007 16 : 707 15.
90. Schramm R, Scheuer C, Yamauchi J et al. Heat shock preconditioning impairs revascularization of freely transplanted pancreatic islets. Transplantation 2002 74 : 1544 50.