TLR4 mediates early graft failure after intraportal islet transplantation

American Journal of Transplantation

Volumn 10, Issue 7, 2010, Pages 1588-1596

  Gao, Q ^a   Ma, L L ^a   Gao, X ^a   Yan, W ^a   Williams, P ^a   Yin, Deng Ping ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Early graft failure; islet transplantation; mice; TLR

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 1BETA; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ENZYME INHIBITION; GRAFT FAILURE; GRAFT SURVIVAL; MOUSE; NONHUMAN; PANCREAS ISLET TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; GRAFT SURVIVAL; HMGB1 PROTEIN; INTERLEUKIN-1BETA; ISLETS OF LANGERHANS TRANSPLANTATION; KIDNEY; LIVER; LUMINESCENCE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4; TRANSPLANTATION, HETEROTOPIC; TREATMENT FAILURE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77954072462     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2010.03151.x     Document Type: Article

References (57)

1. Shapiro AM, Nanji SA, Lakey JR. Clinical islet transplant: Current and future directions towards tolerance. Immunol Rev 2003 196 : 219 236.
2. Fritschy WM, van Straaten JF, de Vos P, Strubbe JH, Wolters GH, van Schilfgaarde R. The efficacy of intraperitoneal pancreatic islet isografts in the reversal of diabetes in rats. Transplantation 1991 52 : 777 783.
3. Wahoff DC, Sutherland DE, Hower CD, Lloveras JK, Gores PF. Free intraperitoneal islet autografts in pancreatectomized dogs: Impact of islet purity and posttransplantation exogenous insulin. Surgery 1994 116 : 742 748 discussion 748 750.
4. Yasunami Y, Lacy PE, Finke EH. A new site for islet transplantation: A peritoneal-omental pouch. Transplantation 1983 36 : 181 182.
5. Ueki M, Yasunami Y, Ryu S, Ikeda S, Tanaka M. Peritoneal-omental pouch as a site for islet allotransplantation. Transplant Proc 1994 26 : 676 677.
6. Andersson A, Korsgren O, Jansson L. Intraportally transplanted pancreatic islets revascularized from hepatic arterial system. Diabetes 1989 38 (Suppl 1 192 195.
7. Bobzien B, Yasunami Y, Majercik M, Lacy PE, Davie JM. Intratesticular transplants of islet xenografts (rat to mouse). Diabetes 1983 32 : 213 216.
8. Selawry H, Fajaco R, Whittington K. Intratesticular islet allografts in the spontaneously diabetic BB/W rat. Diabetes 1985 34 : 1019 1024.
9. Leow CK, Gray DW, Morris PJ. The long-term metabolic function of intraportal and renal subcapsular islet isografts and the effect on glomerular basement membrane thickness in rats. Diabetologia 1995 38 : 1014 1024.
10. Leow CK, Shimizu S, Gray DW, Morris PJ. Successful pancreatic islet autotransplantation to the renal subcapsule in the cynomolgus monkey. Transplantation 1994 57 : 161 164.
11. Trimble ER, Karakash C, Malaisse-Lagae F, Vassutine I, Orci L, Renold AE. Effects of intraportal islet transplantation on the transplanted tissue and the recipient pancreas. I. Functional studies. Diabetes 1980 29 : 341 347.
12. Luzi L, Hering BJ, Socci C et al. Metabolic effects of successful intraportal islet transplantation in insulin-dependent diabetes mellitus. J Clin Invest 1996 97 : 2611 2618.
13. Ozmen L, Ekdahl KN, Elgue G, Larsson R, Korsgren O, Nilsson B. 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 1784.
14. Emamaullee JA, Merani S, Toso C et al. Porcine marginal mass islet autografts resist metabolic failure over time and are enhanced by early treatment with liraglutide. Endocrinology 2009 150 : 2145 2152.
15. Berney T, Molano RD, Cattan P et al. Endotoxin-mediated delayed islet graft function is associated with increased intra-islet cytokine production and islet cell apoptosis. Transplantation 2001 71 : 125 132.
16. Brandhorst D, Brandhorst H, Zwolinski A, Nahidi F, Bretzel RG. Prevention of early islet graft failure by selective inducible nitric oxide synthase inhibitors after pig to nude rat intraportal islet transplantation. Transplantation 2001 71 : 179 184.
17. Goto M, Johansson H, Maeda A, Elgue G, Korsgren O, Nilsson B. Low molecular weight dextran sulfate prevents the instant blood-mediated inflammatory reaction induced by adult porcine islets. Transplantation 2004 77 : 741 747. (Pubitemid 38366981)
18. Rood PP, Bottino R, Balamurugan AN et al. Reduction of early graft loss after intraportal porcine islet transplantation in monkeys. Transplantation 2007 83 : 202 210.
19. Yin D, Ding JW, Shen J, Ma L, Hara M, Chong AS. Liver ischemia contributes to early islet failure following intraportal transplantation: Benefits of liver ischemic-preconditioning. Am J Transplant 2006 6 : 60 68.
20. Werts C, Girardin SE, Philpott DJ. TIR, CARD and PYRIN: Three domains for an antimicrobial triad. Cell Death Differ 2006 13 : 798 815.
21. Noulin N, Quesniaux VF, Schnyder-Candrian S et al. Both hemopoietic and resident cells are required for MyD88-dependent pulmonary inflammatory response to inhaled endotoxin. J Immunol 2005 175 : 6861 6869.
22. Jung DY, Lee H, Jung BY et al. TLR4, but not TLR2, signals autoregulatory apoptosis of cultured microglia: A critical role of IFN-beta as a decision maker. J Immunol 2005 174 : 6467 6476.
23. Shen XD, Ke B, Zhai Y et al. Absence of toll-like receptor 4 (TLR4) signaling in the donor organ reduces ischemia and reperfusion injury in a murine liver transplantation model. Liver Transpl 2007 13 : 1435 1443.
24. Tsung A, Hoffman RA, Izuishi K et al. Hepatic ischemia/reperfusion injury involves functional TLR4 signaling in nonparenchymal cells. J Immunol 2005 175 : 7661 7668.
25. Goldberg A, Parolini M, Chin BY et al. Toll-like receptor 4 suppression leads to islet allograft survival. FASEB J 2007 21 : 2840 2848.
26. Arumugam TV, Okun E, Tang SC, Thundyil J, Taylor SM, Woodruff TM. Toll-like receptors in ischemia-reperfusion injury. Shock 2009 32 : 4 16.
27. Tsan MF, Gao B. Endogenous ligands of Toll-like receptors. J Leukoc Biol 2004 76 : 514 519.
28. Barrat FJ, Meeker T, Gregorio J et al. Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J Exp Med 2005 202 : 1131 1139.
29. Tsung A, Klune JR, Zhang X et al. HMGB1 release induced by liver ischemia involves Toll-like receptor 4 dependent reactive oxygen species production and calcium-mediated signaling. J Exp Med 2007 204 : 2913 2923.
30. Tsung A, Sahai R, Tanaka H et al. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 2005 201 : 1135 1143.
31. Andersson A, Covacu R, Sunnemark D et al. Pivotal advance: HMGB1 expression in active lesions of human and experimental multiple sclerosis. J Leukoc Biol 2008 84 : 1248 1255.
32. Kawahara K, Biswas KK, Unoshima M et al. C-reactive protein induces high-mobility group box-1 protein release through activation of p38MAPK in macrophage RAW264.7 cells. Cardiovasc Pathol 2008 17 : 129 138.
33. Tang D, Shi Y, Kang R et al. Hydrogen peroxide stimulates macrophages and monocytes to actively release HMGB1. J Leukoc Biol 2007 81 : 741 747.
34. Ilmakunnas M, Tukiainen EM, Rouhiainen A et al. High mobility group box 1 protein as a marker of hepatocellular injury in human liver transplantation. Liver Transpl 2008 14 : 1517 1525.
35. Matsuoka N, Itoh T, Watarai H et al. High-mobility group box 1 is involved in the initial events of early loss of transplanted islets in mice. J Clin Invest 2009 120 : 735 743.
36. Fowler M, Virostko J, Chen Z et al. Assessment of pancreatic islet mass after islet transplantation using in vivo bioluminescence imaging. Transplantation 2005 79 : 768 776.
37. Sadikot RT, Blackwell TS. Bioluminescence: Imaging modality for in vitro and in vivo gene expression. Methods Mol Biol 2008 477 : 383 394.
38. Roth DJ, Jansen ED, Powers AC, Wang TG. A novel method of monitoring response to islet transplantation: Bioluminescent imaging of an NF-kB transgenic mouse model. Transplantation 2006 81 : 1185 1190.
39. Yull FE, Han W, Jansen ED et al. Bioluminescent detection of endotoxin effects on HIV-1 LTR-driven transcription in vivo. J Histochem Cytochem 2003 51 : 741 749.
40. Ma L, Xiang Z, Sherrill TP et al. Bioluminescence imaging visualizes activation of nuclear factor-kappaB in mouse cardiac transplantation. Transplantation 2008 85 : 903 910.
41. Ma LL, Gao X, Liu L et al. CpG oligodeoxynucleotide triggers the liver inflammatory reaction and abrogates spontaneous tolerance. Liver Transpl 2009 15 : 915 923.
42. Smith SJ, Zhang H, Clermont AO et al. in vivo monitoring of pancreatic beta-cells in a transgenic mouse model. Mol Imaging 2006 5 : 65 75.
43. Chen X, Zhang X, Larson CS, Baker MS, Kaufman DB. In vivo bioluminescence imaging of transplanted islets and early detection of graft rejection. Transplantation 2006 81 : 1421 1427.
44. Zhai Y, Shen XD, O'Connell R et al. Cutting edge: TLR4 activation mediates liver ischemia/reperfusion inflammatory response via IFN regulatory factor 3-dependent MyD88-independent pathway. J Immunol 2004 173 : 7115 7119.
45. Kruger B, Krick S, Dhillon N et al. Donor Toll-like receptor 4 contributes to ischemia and reperfusion injury following human kidney transplantation. Proc Natl Acad Sci U S A 2009 106 : 3390 3395.
46. Andrassy M, Volz HC, Igwe JC et al. High-mobility group box-1 in ischemia-reperfusion injury of the heart. Circulation 2008 117 : 3216 3226.
47. Wahamaa H, Vallerskog T, Qin S et al. HMGB1-secreting capacity of multiple cell lineages revealed by a novel HMGB1 ELISPOT assay. J Leukoc Biol 2007 81 : 129 136.
48. Hara M, Yin D, Dizon RF, Shen J, Chong AS, Bindokas VP. A mouse model for studying intrahepatic islet transplantation. Transplantation 2004 78 : 615 618.
49. Zhang N, Kruger B, Lal G et al. Inhibition of TLR4 signaling prolongs Treg-dependent murine islet allograft survival. Immunol Lett 2010 127 : 119 125.
50. Hutton MJ, Westwell-Roper C, Soukhatcheva G, Plesner A, Dutz JP, Verchere CB. Islet allograft rejection is independent of toll-like receptor signaling in mice. Transplantation 2009 88 : 1075 1080.
51. Ivanov S, Dragoi AM, Wang X et al. A novel role for HMGB1 in TLR9-mediated inflammatory responses to CpG-DNA. Blood 2007 110 : 1970 1981.
52. Klune JR, Dhupar R, Cardinal J, Billiar TR, Tsung A. HMGB1: Endogenous danger signaling. Mol Med 2008 14 : 476 484.
53. van Zoelen MA, Yang H, Florquin S et al. Role of toll-like receptors 2 and 4, and the receptor for advanced glycation end products in high-mobility group box 1-induced inflammation in vivo. Shock 2009 31 : 280 284.
54. Yu M, Wang H, Ding A et al. HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock 2006 26 : 174 179.
55. Park JS, Gamboni-Robertson F, He Q et al. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am J Physiol Cell Physiol 2006 290 : C917 C924.
56. Hreggvidsdottir HS, Ostberg T, Wahamaa H et al. The alarmin HMGB1 acts in synergy with endogenous and exogenous danger signals to promote inflammation. J Leukoc Biol 2009 86 : 655 662.
57. Park JS, Svetkauskaite D, He Q et al. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem 2004 279 : 7370 7377.