Activation of nuclear factor-κB during orthotopic liver transplantation in rats is protective and does not require Kupffer cells

Liver Transplantation and Surgery

Volumn 5, Issue 4, 1999, Pages 282-293

  Bradham, C A ^a   Schemmer, P ^a   Stachlewitz, R F ^a   Thurman, R G ^a   Brenner, D A ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; GADOLINIUM CHLORIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 6; LUCIFERASE; MESSENGER RNA; PLASMA PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; GENE TRANSFER; KUPFFER CELL; LIVER CELL DAMAGE; LIVER TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; TISSUE INJURY; TISSUE PERFUSION;

EID: 0033065273     PISSN: 10743022     EISSN: None     Source Type: Journal    
DOI: 10.1002/lt.500050401     Document Type: Article

References (66)

1. 1 Caldwell‐Kenkel JC, Currin RT, Tanaka Y, Thurman RG, Lemasters JJ. Kupffer cell activation and endothelial cell damage after storage of rat livers: Effects of reperfusion. Hepatology 1991 ; 13: 83–95. MEDLINE
2. 2 Lindert KA, Caldwell‐Kenkel JC, Nukina S, Lemasters JJ, Thurman RG. Activation of Kupffer cells on reperfusion following hypoxia: Particle phagocytosis in a low‐flow, reflow model. Am J Physiol 1992 ; 262: G345–G350. MEDLINE
3. 3 Furukawa H, Todo S, Imventarza O, Casavilla A, Wu YM, Scotti‐Foglieni C, et al. Effect of cold ischemia time on the early outcome of human hepatic allografts preserved with UW solution. Transplantation 1991 ; 51: 1000–1004. MEDLINE
4. 4 Nathan CF. Secretory products of macrophages. J Clin Invest 1987 ; 79: 319–326. MEDLINE
5. 5 Gao W, Takei Y, Marzi I, Lindert KA, Caldwell‐Kenkel JC, Currin RT, et al. Carolina rinse solution: A new strategy to increase survival time after orthotopic liver transplantation in the rat. Transplantation 1991 ; 52: 417–424. MEDLINE
6. 6 Marzi I, Cowper K, Takei Y, Lindert K, Lemasters JJ, Thurman RG. Methyl palmitate prevents Kupffer cell activation and improves survival after orthotopic liver transplantation in the rat. Transplant Int 1991 ; 4: 215–220.
7. 7 Shiatori Y, Kiriyama H, Fukushi Y, Nagura T, Takada H, Hai K, et al. Modulation of ischemia‐reperfusion–induced hepatic injury by Kupffer cells. Dig Dis Sci 1994 ; 39: 1265–1272. MEDLINE
8. 8 Motoyama K, Kamei T, Nakafusa Y, Ueki M, Hirano T, Arima T, et al. Donor treatment with gadolinium chloride improves survival after transplantation of cold‐stored livers by reducing Kupffer cell tumor necrosis factor production in rats. Transplant Proc 1995 ; 27: 762–764. MEDLINE
9. 9 Sankary HN, Chong A, Foster P, Brown E, Shen J, Kimura R, et al. Inactivation of Kupffer cells after prolonged donor fasting improves viability of transplanted hepatic allografts. Hepatology 1995 ; 22: 1236–1242. MEDLINE
10. 10 Zhong Z, Conner H, Mason RP, Qu W, Stachlewitz RF, Gao W, et al. Destruction of Kupffer cells increases survival and reduces graft injury after transplantation of fatty livers from ethanol‐treated rats. Liver Transpl Surg 1996 ; 2: 383–387. MEDLINE
11. 11 Niwano M, Arii S, Monden K, Ishiguro S, Nakamura T, Mizumoto M, et al. Amelioration of sinusoidal endothelial cell damage by Kupffer cell blockade during cold preservation of rat liver. J Surg Res 1997 ; 72: 36–48. MEDLINE
12. 12 Shibuya H, Ohkohchi N, Seya K, Satomi S. Kupffer cells generate superoxide anions and modulate reperfusion injury in rat livers after cold preservation. Hepatology 1997 ; 25: 356–360. MEDLINE
13. 13 Imamura H, Sutto F, Brault A, Huet P‐M. Role of Kupffer cells in cold ischemia/reperfusion injury of rat liver. Gastroenterology 1995 ; 109: 189–197. MEDLINE
14. 14 Hardonk MJ, Dijkhuis FWJ, Hulstaert CE, Koudstaal J. Heterogeneity of rat liver and spleen macrophages in gadolinium chloride–induced elimination and repopulation. J Leukoc Biol 1992 ; 52: 296–302. MEDLINE
15. 15 Colletti LM, Burtch GD, Remick DG, Kunkel SL, Strieter RM, Guicce KS, et al. The production of tumor necrosis factor alpha and the development of a pulmonary capillary injury following hepatic ischemia/reperfusion. Transplantation 1990 ; 49: 268–272. MEDLINE
16. 16 Bradham CA, Stachlewitz R, Gao W, Qian T, Jayadev S, Jenkins G, et al. Reperfusion after liver transplantation in rats differentially activates the mitogen‐activated protein kinases. Hepatology 1997 ; 25: 1128–1135. MEDLINE
17. 17 Takei Y, Marzi I, Kauffman FC, Currin RT, Lemasters JJ, Thurman RG. Increase in survival time of liver transplants by protease inhibitors and a calcium channel blocker, nisoldipine. Transplantation 1990 ; 50: 14–20. MEDLINE
18. 18 Bachman S, Caldwell‐Kenkel JC, Currin RT, Lichtman SN, Steffen R, Thurman RG, et al. Protection by pentoxifylline against graft failure from storage injury after orthotopic liver transplantation. Transplant Int 1992 ; 5: S345–S350.
19. 19 Colletti LM, Remick DG, Burtch GD, Kunkel SL, Strieter RM, Campbell DA. Role of tumor necrosis factor‐α in the pathophysiological alterations after ischemia/reperfusion injury in the rat. J Clin Invest 1990 ; 85: 1936–1943. MEDLINE
20. 20 Goto M, Takei Y, Kawano S, Tsuji S, Fukui H, Fushimi H, et al. Tumor necrosis factor and endotoxin in the pathogenesis of liver and pulmonary injuries after orthotopic liver transplantation in the rat. Hepatology 1992 ; 16: 487–493. MEDLINE
21. 21 Eason JD, Wee S, Kawai T, Hong HZ, Powelson JA, Widmer MB, et al. Inhibition of the effects of TNF in renal allograft recipients using recombinant human dimeric tumor necrosis factor receptors. Transplantation 1995 ; 59: 300–305. MEDLINE
22. 22 Brenner DA, O'Hara M, Angel P, Chojkier M, Karin M. Prolonged activation of jun and collagenase genes by tumor necrosis factor‐α. Nature 1989 ; 337: 661–663. MEDLINE
23. 23 Lowenthal JW, Ballard DW, Bogerd H, Böhnlein E, Greene WC. Tumor necrosis factor‐α activation of the IL‐2 receptor‐α gene involves the induction of κB‐specific DNA binding proteins. J Immunol 1989 ; 142: 3121–3128. MEDLINE
24. 24 Westwick JK, Weitzel C, Minden A, Karin M, Brenner DA. Tumor necrosis factor‐α stimulates AP‐1 activity through prolonged activation of the c‐jun kinase. J Biol Chem 1994 ; 269: 26369–26401.
25. 25 Derijard B, Hibi M, Wu I‐H, Barret T, Su B, Deng T, et al. JNK‐1: A protein kinase stimulated by UV light and Ha‐Ras that binds and phosphorylates the c‐Jun activation domain. Cell 1994 ; 76: 1025–1037. MEDLINE
26. 26 Gille H, Sharrocks AD, Shaw PE. Phosphorylation of transcription factor p62‐TCF by MAP kinase stimulated ternary complex formation at the c‐ fos promoter. Nature 1992 ; 358: 414–417. MEDLINE
27. 27 Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME. Opposing effects of ERK and JNK‐p38 MAP kinases on apoptosis. Science 1995 ; 270: 1326–1331. MEDLINE
28. 28 Verheij M, Bose R, Lin XH, Yao B, Jarvis WD, Grant S, et al. Requirement for ceramide‐initiated SAPK/JNK signaling in stress‐induced apoptosis. Nature 1996 ; 380: 75–79. MEDLINE
29. 29 Liu Z‐G, Hsu H, Goeddel DV, Karin M. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF‐κB activation prevents cell death. Cell 1996 ; 87: 565–576. MEDLINE
30. 30 Natoli G, Costanzo A, Ianni A, Templeton DJ, Woodjet JR, Balsano C, et al. Activation of SAPK/JNK by TNF receptor 1 through a nontoxic TRAF2‐dependent pathway. Science 1997 ; 275: 200–203. MEDLINE
31. 31 Wang C‐Y, Mayo MW, Baldwin ASJ. TNF‐ and cancer therapy–induced apoptosis: Potentiation by inhibiting NF‐κB. Science 1996 ; 274: 784–787. MEDLINE
32. 32 DiDonato JA, Hayakawa M, Rothwarf DM, Zandi E, Karin M. A cytokine‐responsive IκB kinase that activates the transcription factor NF‐κB. Nature 1997 ; 388: 548–554. MEDLINE
33. 33 Malinin NL, Boldin MP, Kovalenko AV, Wallach D. MAP3K‐related kinase involved in NF‐κB induction by TNF, CD‐95, and IL‐1. Nature 1997 ; 385: 540–544. MEDLINE
34. 34 Brown K, Gerstberger S, Carlson L, Franzoso G, Siebenlist U. Control of IκB‐α proteolysis by site‐specific, signal‐induced phosphorylation. Science 1995 ; 267: 1485–1488. MEDLINE
35. 35 Bergmeyer HU. Methods of enzymatic analysis. New York: Academic. 1988.
36. 36 Hattori MA, Tugores A, Westwick JK, Veloz L, Leffert HL, Karin M, et al. Activation of activating protein 1 during hepatic acute phase response. Am J Physiol 1993 ; 264: G95–G103. MEDLINE
37. 37 Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 1979 ; 18: 5294–5299. MEDLINE
38. 38 Herfarth HH, Mohanty S, Rath HC, Sartor RB. IL‐10 therapy suppresses experimental chronic, granulomatous inflammation induced by bacterial cell wall polymers. Gut 1996 ; 39: 836–845. MEDLINE
39. 39 Iimura Y, Nishiura T, Hellerbrand C, Behrns KE, Schoonhoven R, Grisham JW, et al. NFκB prevents apoptosis and liver dysfunction during liver regeneration. J Clin Invest 1998 ; 101: 802–811. MEDLINE
40. 40 Graham FL, Prevec L. Manipulation of adenovirus vectors. Methods Enzymol 1991 ; 7: 109–128.
41. 41 Bradham CA, Qian T, Streetz K, Brenner DA, Lemasters JJ. The mitochondrial permeability transition is required for TNFα‐mediated apoptosis and cytochrome c release. Mol Cell Biol 1998 ; 18: 6353–6364. MEDLINE
42. 42 Bossy‐Wetzel E, Bakiri L, Yaniv M. Induction of apoptosis by the transcription factor c‐Jun. EMBO J 1997 ; 16: 1695–1709. MEDLINE
43. 43 Arii S, Monden K, Adachi Y, Higashitsuji H, Furutani M, Mise M, et al. Pathogenic role of Kupffer cell activation in the reperfusion injury of cold‐preserved liver. Transplantation 1994 ; 58: 1072–1077. MEDLINE
44. 44 Suzuki S, Nakamura S, Sakaguchi T, Ochiai H, Konno H, Baba S, et al. Alteration of reticuloendothelial phagocytic function and tumor necrosis factor‐alpha production after total hepatic ischemia. Transplantation 1997 ; 64: 821–827. MEDLINE
45. 45 Rai RM, Yang SQ, McClain C, Karp CL, Klein AS, Diehl AM. Kupffer cell depletion by gadolinium chloride enhances liver regeneration after partial hepatectomy in rats. Am J Physiol 1996 ; 270: G909–G918. MEDLINE
46. 46 Loffreda S, Rai R, Yang SQ, Lin HZ, Diehl AM. Bile ducts and portal and central veins are major producers of tumor necrosis factor alpha in regenerating rat liver. Gastroenterology 1997 ; 112: 2089–2098. MEDLINE
47. 47 Conner HD, Gao W, Nukina S, Lemasters JJ, Mason RP, Thurman RG. Evidence that free radicals are involved in graft failure following orthotopic liver transplantation in the rat—An electron paramagnetic resonance spin trapping study. Transplantation 1992 ; 54: 199–204. MEDLINE
48. 48 Qu W, Savier E, Thurman RG. Stimulation of monooxygenation and conjugation after liver transplantation in the rat: Involvement of Kupffer cells. Mol Pharmacol 1992 ; 41: 1149–1154. MEDLINE
49. 49 Dawson TL, Gores GJ, Nieminen A‐L, Herman B, Lemasters JJ. Mitochondria as a source of reactive oxygen species during reductive stress in rat hepatocytes. Am J Physiol 1993 ; 264: C961–C967. MEDLINE
50. 50 Hirose K, Longo DL, Oppenheim JJ, Matsushima K. Overexpression of mitochondrial manganese SOD promotes the survival of tumour cells exposed to interleukin‐1, tumor necrosis factor, selected anticancer drugs, and ionising radiation. FASEB J 1993 ; 7: 361–368. MEDLINE
51. 51 Zwacka RM, Zhou W, Zhang Y, Darby CJ, Dudas L, Halldorson J, et al. Redox gene therapy for ischemia/reperfusion of the liver reduces AP‐1 and NF‐κB activation. Nat Med 1998 ; 4: 698–704. MEDLINE
52. 52 Jaeschke H, Farhood A. Neutrophil and Kupffer cell–induced oxidant stress and ischemia‐reperfusion injury in rat liver. Am J Physiol 1991 ; 260: G355–G362. MEDLINE
53. 53 Kushner I, Rzewnicki DL. The acute‐phase response: General aspects. Baillieres Clin Rheumatol 1994 ; 8: 513–530. MEDLINE
54. 54 Heinrich PC, Horn F, Graeve L, Dittrich E, Kerr I, Muller‐Newen G, et al. Interleukin‐6 and related cytokines: Effect on the acute phase reaction. Z Ernahrungswiss 1998 ; 37 (suppl 1): 43–49. MEDLINE
55. 55 Cosenza CA, Shirwin H, Cramer DV, Sher L, Podesta L, Makowka L. Intragraft cytokine gene expression in human liver allografts. Liver Transpl Surg 1995 ; 1: 16–22. MEDLINE
56. 56 Boros P, Suehiro T, Curtiss S, Sheiner P, Emre S, Guy S, et al. Differential contribution of graft and recipient to perioperative TNF‐alpha, IL‐1, IL‐6 and IL‐8 levels and correlation with early graft function in clinical liver transplantation. Clin Transplant 1997 ; 11: 588–592. MEDLINE
57. 57 Camargo CAJ, Madden JF, Gao W, Selvan RS, Clavien P‐A. Interleukin‐6 protects liver against warm ischemia/reperfusion injury and promotes hepatocyte proliferation in the rodent. Hepatology 1997 ; 26: 1513–1520. MEDLINE
58. 58 Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O'Garra A. IL‐10 inhibits cytokine production by activated macrophages. J Immunol 1991 ; 147: 3815–3822. MEDLINE
59. 59 Rai RM, Karp CL, Yang S‐Q, Lin H‐Z, Diehl AM. Kupffer cell depletion abolishes induction of interleukin‐10 and permits sustained expression of tumor necrosis factor α mRNA in the regenerating liver. Hepatology 1997 ; 25: 889–895. MEDLINE
60. 60 Wang P, Wu P, Siegel MI, Egan RW, Billah NM. Interleukin (IL)‐10 inhibits nuclear factor κB (NFκB) activation in human monocytes. J Biol Chem 1995 ; 270: 9558–9563. MEDLINE
61. 61 Knolle P, Lohr H, Triechel U, Dienes HP, Lohse A, Schlaak J, et al. Parenchymal and nonparenchymal liver cells and their interaction in the local immune response. Z Gastroenterol 1995 ; 33: 613–620. MEDLINE
62. 62 Sawai H, Okazaki T, Yamamoto H, Okano H, Takeda Y, Tashima M, et al. Requirement of AP‐1 for ceramide‐induced apoptosis in human leukemia HL‐60 cells. J Biol Chem 1995 ; 270: 27326–27331. MEDLINE
63. 63 Lenczowski JM, Dominguez L, Eder AE, King LB, Zacharchuk CM, Ashwell JD. Lack of a role for jun kinase and AP‐1 in Fas‐induced apoptosis. Mol Cell Biol 1997 ; 17: 170–181. MEDLINE
64. 64 Chu ZL, McKinsey TA, Liu L, Gentry JJ, Malim MH, Ballard DW. Suppression of tumor necrosis factor–induced cell death by inhibitor of apoptosis c‐IAP2 is under NF‐κB control. Proc Natl Acad Sci U S A 1997 ; 94: 10057–10062. MEDLINE
65. 65 You M, Ku PT, Hrdlickova R, Bose HRJ. ch‐IAP, a member of the inhibitor of apoptosis protein family, is a mediator of the antiapoptotic activities of the v‐Rel oncoprotein. Mol Cell Biol 1997 ; 17: 7328–7341. MEDLINE
66. 66 Schreck R, Rieber P, Baeuerle PA. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF‐κB transcription factor and HIV‐1. EMBO J 1991 ; 10: 2247–2258. MEDLINE