Table of Contents Author Guidelines Submit a Manuscript
Scientifica
Volume 2012, Article ID 513192, 14 pages
http://dx.doi.org/10.6064/2012/513192
Review Article

Regulatory Mechanisms of Injury and Repair after Hepatic Ischemia/Reperfusion

Department of Surgery, College of Medicine, University of Cincinnati, 231 Albert Sabin Way, ML 0558, Cincinnati, OH 45267-0558, USA

Received 1 August 2012; Accepted 12 September 2012

Academic Editors: F. Afaq, S. Nitecki, C. Peralta, and A. G. Zapata

Copyright © 2012 Alex B. Lentsch. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. Delva, Y. Camus, B. Nordlinger et al., “Vascular occlusions for liver resections. Operative management and tolerance to hepatic ischemia: 142 cases,” Annals of Surgery, vol. 209, no. 2, pp. 211–218, 1989. View at Google Scholar · View at Scopus
  2. C. Huguet, A. Gavelli, and S. Bona, “Hepatic resection with ischemia of the liver exceeding one hour,” Journal of the American College of Surgeons, vol. 178, no. 5, pp. 454–458, 1994. View at Google Scholar · View at Scopus
  3. F. Serracino-Inglott, N. A. Habib, and R. T. Mathie, “Hepatic ischemia-reperfusion injury,” American Journal of Surgery, vol. 181, no. 2, pp. 160–166, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Jaeschke, C. V. Smith, and J. R. Mitchell, “Reactive oxygen species during ischemia-reflow injury in isolated perfused rat liver,” Journal of Clinical Investigation, vol. 81, no. 4, pp. 1240–1246, 1988. View at Google Scholar · View at Scopus
  5. H. Jaeschke and A. Farhood, “Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver,” American Journal of Physiology, vol. 260, no. 3, pp. G355–G362, 1991. View at Google Scholar · View at Scopus
  6. H. Jaeschke, “Reactive oxygen and ischemia/reperfusion injury of the liver,” Chemico-Biological Interactions, vol. 79, no. 2, pp. 115–136, 1991. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Jaeschke, A. Farhood, A. P. Bautista, Z. Spolarics, and J. J. Spitzer, “Complement activates Kupffer cells and neutrophils during reperfusion after hepatic ischemia,” American Journal of Physiology, vol. 264, no. 4, pp. G801–G809, 1993. View at Google Scholar · View at Scopus
  8. R. M. Zwacka, Y. Zhang, J. Halldorson, H. Schlossberg, L. Dudus, and J. F. Engelhardt, “CD4+ T-lymphocytes mediate ischemia/reperfusion-induced inflammatory responses in mouse liver,” Journal of Clinical Investigation, vol. 100, no. 2, pp. 279–289, 1997. View at Google Scholar · View at Scopus
  9. C. C. Caldwell, T. Okaya, A. Martignoni, T. Husted, R. Schuster, and A. B. Lentsch, “Divergent functions of CD4+ T lymphocytes in acute liver inflammation and injury after ischemia-reperfusion,” American Journal of Physiology, vol. 289, no. 5, pp. G969–G976, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. H. Oo, S. Shetty, and D. H. Adams, “The role of chemokines in the recruitment of lymphocytes to the liver,” Digestive Diseases, vol. 28, no. 1, pp. 31–44, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. Z. Yao, S. L. Painter, W. C. Fanslow et al., “Human IL-17: a novel cytokine derived from T cells,” Journal of Immunology, vol. 155, no. 12, pp. 5483–5486, 1995. View at Google Scholar · View at Scopus
  12. J. Witowski, K. Pawlaczyk, A. Breborowicz et al., “IL-17 stimulates intraperitoneal neutrophil infiltration through the release of GROα chemokine from mesothelial cells,” Journal of Immunology, vol. 165, no. 10, pp. 5814–5821, 2000. View at Google Scholar · View at Scopus
  13. M. Laan, Z. H. Cui, H. Hoshino et al., “Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways,” Journal of Immunology, vol. 162, no. 4, pp. 2347–2352, 1999. View at Google Scholar · View at Scopus
  14. S. Molet, Q. Hamid, F. Davoine et al., “IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines,” Journal of Allergy and Clinical Immunology, vol. 108, no. 3, pp. 430–438, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. M. J. Ruddy, F. Shen, J. B. Smith, A. Sharma, and S. L. Gaffen, “Interleukin-17 regulates expression of the CXC chemokine LIX/CXCL5 in osteoblasts: implications for inflammation and neutrophil recruitment,” Journal of Leukocyte Biology, vol. 76, no. 1, pp. 135–144, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Khandoga, M. Hanschen, J. S. Kessler, and F. Krombach, “CD4+ T cells contribute to postischemic liver injury in mice by interacting with sinusoidal endothelium and platelets,” Hepatology, vol. 43, no. 2, pp. 306–315, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. D. Takeuchi, H. Yoshidome, A. Kato et al., “Interleukin 18 causes hepatic ischemia/reperfusion injury by suppressing anti-inflammatory cytokine expression in mice,” Hepatology, vol. 39, no. 3, pp. 699–710, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. A. B. Lentsch, H. Yoshidome, A. Kato et al., “Requirement for interleukin-12 in the pathogenesis of warm hepatic ischemia/reperfusion injury in mice,” Hepatology, vol. 30, no. 6, pp. 1448–1453, 1999. View at Google Scholar · View at Scopus
  19. M. C. Leite-de-Moraes, A. Hameg, A. Arnould et al., “A distinct IL-18-induced pathway to fully activate NK T lymphocytes independently from TCR engagement,” Journal of Immunology, vol. 163, no. 11, pp. 5871–5876, 1999. View at Google Scholar · View at Scopus
  20. G. Martino, F. Grohovaz, E. Brambilla et al., “Proinflammatory cytokines regulate antigen-independent T-cell activation by two separate calcium-signaling pathways in multiple sclerosis patients,” Annals of Neurology, vol. 43, no. 3, pp. 340–349, 1998. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Sugaya, K. Nakamura, and K. Tamaki, “Interleukins 18 and 12 synergistically upregulate interferon-γ production by murine dendritic epidermal T cells,” Journal of Investigative Dermatology, vol. 113, no. 3, pp. 350–354, 1999. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Sugiura, S. Lee, T. Nagahama, Y. Adachi, J. Ishikawa, and S. Ikehara, “Tolerance induction across Mls and minor histocompatibility complex by inhibiting activation of T helper type 1 in early period,” Immunology Letters, vol. 77, no. 1, pp. 25–30, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Zhang, E. M. Alicot, I. Chiu et al., “Identification of the target self-antigens in reperfusion injury,” Journal of Experimental Medicine, vol. 203, no. 1, pp. 141–152, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. R. A. Kroczek, H. W. Mages, and A. Hutloff, “Emerging paradigms of T-cell co-stimulation,” Current Opinion in Immunology, vol. 16, no. 3, pp. 321–327, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. X. D. Shen, B. Ke, Y. Zhai et al., “CD154-CD40 T-cell costimulation pathway is required in the mechanism of hepatic ischemia/reperfusion injury, and its blockade facilitates and depends on heme oxygenase-1 mediated cytoprotection,” Transplantation, vol. 74, no. 3, pp. 315–319, 2002. View at Google Scholar · View at Scopus
  26. N. Kojima, M. Sato, A. Suzuki et al., “Enhanced expression of B7-1, B7-2, and intercellular adhesion molecule 1 in sinusoidal endothelial cells by warm ischemia/reperfusion injury in rat liver,” Hepatology, vol. 34, no. 4, pp. 751–757, 2001. View at Publisher · View at Google Scholar · View at Scopus
  27. A. S. R. Bartlett, J. L. McCall, R. Ameratunga, M. L. Yeong, E. Gane, and S. R. Munn, “Analysis of Intragraft Gene and Protein Expression of the Costimulatory Molecules, CD80, CD86 and CD154, in Orthotopic Liver Transplant Recipients,” American Journal of Transplantation, vol. 3, no. 11, pp. 1363–1368, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. D. K. Ysebaert, K. E. De Greef, A. De Beuf et al., “T cells as mediators in renal ischemia/reperfusion injury,” Kidney International, vol. 66, no. 2, pp. 491–496, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Limmer and P. A. Knolle, “Liver sinusoidal endothelial cells: a new type of organ-resident antigen-presenting cell,” Archivum Immunologiae et Therapiae Experimentalis, vol. 49, supplement 1, pp. S7–S11, 2001. View at Google Scholar · View at Scopus
  30. P. A. Knolle and A. Limmer, “Neighborhood politics: the immunoregulatory function of organ-resident liver endothelial cells,” Trends in Immunology, vol. 22, no. 8, pp. 432–437, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. P. A. Knolle, E. Schmitt, S. Jin et al., “Induction of cytokine production in naive CD4+ T cells by antigen- presenting murine liver sinusoidal endothelial cells but failure to induce differentiation toward T(h1) cells,” Gastroenterology, vol. 116, no. 6, pp. 1428–1440, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. S. C. Katz, V. G. Pillarisetty, J. I. Bleier, A. B. Shah, and R. P. DeMatteo, “Liver sinusoidal endothelial cells are insufficient to activate T cells,” Journal of Immunology, vol. 173, no. 1, pp. 230–235, 2004. View at Google Scholar · View at Scopus
  33. T. L. Husted, J. Blanchard, R. Schuster, H. Shen, and A. B. Lentsch, “Potential role for IL-23 in hepatic ischemia/reperfusion injury,” Inflammation Research, vol. 55, no. 5, pp. 177–178, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. L. Leifeld, S. Cheng, J. Ramakers et al., “Imbalanced intrahepatic expression of interleukin 12, interferon gamma, and interleukin 10 in fulminant hepatitis B,” Hepatology, vol. 36, no. 4, pp. 1001–1008, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. W. E. Thierfelder, J. M. Van Deursen, K. Yamamoto et al., “Requirement for Stat4 in interleukin-12-mediated responses of natural killer and T cells,” Nature, vol. 382, no. 6587, pp. 171–174, 1996. View at Publisher · View at Google Scholar · View at Scopus
  36. W. T. Watford, B. D. Hissong, J. H. Bream, Y. Kanno, L. Muul, and J. J. O'Shea, “Signaling by IL-12 and IL-23 and the immunoregulatory roles of STAT4,” Immunological Reviews, vol. 202, pp. 139–156, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Kato, A. Graul-Layman, M. J. Edwards, and A. B. Lentsch, “Promotion of hepatic ischemia/reperfusion injury by IL-12 is independent of STAT4,” Transplantation, vol. 73, no. 7, pp. 1142–1145, 2002. View at Google Scholar · View at Scopus
  38. L. M. Colletti, D. G. Remick, G. D. Burtch, S. L. Kunkel, R. M. Strieter, and D. A. Campbell Jr, “Role of tumor necrosis factor-α in the pathophysiologic alterations after hepatic ischemia/reperfusion injury in the rat,” Journal of Clinical Investigation, vol. 85, no. 6, pp. 1936–1943, 1990. View at Google Scholar · View at Scopus
  39. S. Suzuki and L. H. Toledo-Pereyra, “Interleukin 1 and tumor necrosis factor production as the initial stimulants of liver ischemia and reperfusion injury,” Journal of Surgical Research, vol. 57, no. 2, pp. 253–258, 1994. View at Publisher · View at Google Scholar · View at Scopus
  40. G. A. Wanner, W. Ertel, P. Müller et al., “Liver ischemia and reperfusion induces a systemic inflammatory response through Kupffer cell activation,” Shock, vol. 5, no. 1, pp. 34–40, 1996. View at Google Scholar · View at Scopus
  41. M. Shito, G. Wakabayashi, M. Ueda et al., “Interleukin 1 receptor blockade reduces tumor necrosis factor production, tissue injury, and mortality after hepatic ischemia-reperfusion in the rat,” Transplantation, vol. 63, no. 1, pp. 143–148, 1997. View at Publisher · View at Google Scholar · View at Scopus
  42. L. M. Colletti, G. D. Burtch, D. G. Remick et al., “The production of tumor necrosis factor alpha and the development of a pulmonary capillary injury following hepatic ischemia/reperfusion,” Transplantation, vol. 49, no. 2, pp. 268–272, 1990. View at Google Scholar · View at Scopus
  43. L. M. Colletti, A. Cortis, N. Lukacs, S. L. Kunkel, M. Green, and R. M. Strieter, “Tumor necrosis factor up-regulates intercellular adhesion molecule 1, which is important in the neutrophil-dependent lung and liver injury associated with hepatic ischemia and reperfusion in the rat,” Shock, vol. 10, no. 3, pp. 182–191, 1998. View at Google Scholar · View at Scopus
  44. L. M. Colletti, S. L. Kunkel, A. Walz et al., “Chemokine expression during hepatic ischemia/reperfusion-induced lung injury in the rat. The role of epithelial neutrophil activating protein,” Journal of Clinical Investigation, vol. 95, no. 1, pp. 134–141, 1995. View at Google Scholar · View at Scopus
  45. A. B. Lentsch, H. Yoshidome, W. G. Cheadle, F. N. Miller, and M. J. Edwards, “Chemokine involvement in hepatic ischemia/reperfusion injury in mice: roles for macrophage inflammatory protein-2 and Kupffer cells,” Hepatology, vol. 27, no. 2, pp. 507–512, 1998. View at Publisher · View at Google Scholar · View at Scopus
  46. H. Yoshidome, A. B. Lentsch, W. G. Cheadle, F. N. Miller, and M. J. Edwards, “Enhanced pulmonary expression of CXC chemokines during hepatic ischemia/reperfusion-induced lung injury in mice,” Journal of Surgical Research, vol. 81, no. 1, pp. 33–37, 1999. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Kato, C. Gabay, T. Okaya, and A. B. Lentsch, “Specific role of interleukin-1 in hepatic neutrophil recruitment after ischemia/reperfusion,” American Journal of Pathology, vol. 161, no. 5, pp. 1797–1803, 2002. View at Google Scholar · View at Scopus
  48. H. L. Pahl, “Activators and target genes of Rel/NF-κB transcription factors,” Oncogene, vol. 18, no. 49, pp. 6853–6866, 1999. View at Google Scholar · View at Scopus
  49. A. Hoffmann and D. Baltimore, “Circuitry of nuclear factor κB signaling,” Immunological Reviews, vol. 210, pp. 171–186, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. A. S. Baldwin Jr, “The NF-kappa B and I kappa B proteins: new discoveries and insights,” Annual Review of Immunology, vol. 14, pp. 649–683, 1996. View at Publisher · View at Google Scholar
  51. N. D. Perkins, “Achieving transcriptional specificity with NF-κB,” International Journal of Biochemistry and Cell Biology, vol. 29, no. 12, pp. 1433–1448, 1997. View at Publisher · View at Google Scholar · View at Scopus
  52. T. Huxford, D. B. Huang, S. Malek, and G. Ghosh, “The crystal structure of the IκBα/NF-κB complex reveals mechanisms of NF-κB inactivation,” Cell, vol. 95, no. 6, pp. 759–770, 1998. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Scheidereit, “IκB kinase complexes: gateways to NF-κB activation and transcription,” Oncogene, vol. 25, no. 51, pp. 6685–6705, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. F. Mercurio, H. Zhu, B. W. Murray et al., “IKK-1 and IKK-2: cytokine-activated IκB kinases essential for NF-κB activation,” Science, vol. 278, no. 5339, pp. 860–866, 1997. View at Publisher · View at Google Scholar · View at Scopus
  55. Z. Chen, J. Hagler, V. J. Palombella et al., “Signal-induced site-specific phosphorylation targets IκBα to the ubiquitin-proteasome pathway,” Genes and Development, vol. 9, no. 13, pp. 1586–1597, 1995. View at Google Scholar · View at Scopus
  56. S. Ghosh, M. J. May, and E. B. Kopp, “NF-κB and rel proteins: evolutionarily conserved mediators of immune responses,” Annual Review of Immunology, vol. 16, pp. 225–260, 1998. View at Publisher · View at Google Scholar · View at Scopus
  57. V. Imbert, R. A. Rupec, A. Livolsi et al., “Tyrosine phosphorylation of IκB-α activates NF-κB without proteolytic degradation of IκB-α,” Cell, vol. 86, no. 5, pp. 787–798, 1996. View at Publisher · View at Google Scholar · View at Scopus
  58. C. Fan, Q. Li, D. Ross, and J. F. Engelhardt, “Tyrosine phosphorylation of IκBα activates NFκB through a redox-regulated and c-Src-dependent mechanism following hypoxia/reoxygenation,” Journal of Biological Chemistry, vol. 278, no. 3, pp. 2072–2080, 2003. View at Publisher · View at Google Scholar · View at Scopus
  59. R. M. Zwacka, Y. Zhang, W. Zhou, J. Halldorson, and J. E. Engelhardt, “Ischemia/reperfusion injury in the liver of BALB/c mice activates AP-1 and nuclear factor κB independently of IκB degradation,” Hepatology, vol. 28, no. 4, pp. 1022–1030, 1998. View at Publisher · View at Google Scholar · View at Scopus
  60. T. Okaya and A. B. Lentsch, “Hepatic expression of S32A/S36A IκBα does not reduce postischemic liver injury,” Journal of Surgical Research, vol. 124, no. 2, pp. 244–249, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. A. C. Koong, E. Y. Chen, and A. J. Giaccia, “Hypoxia causes the activation of nuclear factor κB through the phosphorylation of IκBα on tyrosine residues,” Cancer Research, vol. 54, no. 6, pp. 1425–1430, 1994. View at Google Scholar · View at Scopus
  62. S. C. Sun, P. A. Ganchi, D. W. Ballard, and W. C. Greene, “NF-κB controls expression of inhibitor IκBα: evidence for an inducible autoregulatory pathway,” Science, vol. 259, no. 5103, pp. 1912–1915, 1993. View at Google Scholar · View at Scopus
  63. M. L. Schmitz, I. Mattioli, H. Buss, and M. Kracht, “NF-κB: a multifaceted transcription factor regulated at several levels,” ChemBioChem, vol. 5, no. 10, pp. 1348–1358, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. P. Viatour, M. P. Merville, V. Bours, and A. Chariot, “Phosphorylation of NF-κB and IκB proteins: implications in cancer and inflammation,” Trends in Biochemical Sciences, vol. 30, no. 1, pp. 43–52, 2005. View at Publisher · View at Google Scholar · View at Scopus
  65. L. F. Chen and W. C. Greene, “Regulation of distinct biological activities of the NF-κB transcription factor complex by acetylation,” Journal of Molecular Medicine, vol. 81, no. 9, pp. 549–557, 2003. View at Publisher · View at Google Scholar · View at Scopus
  66. T. Okazaki, S. Sakon, T. Sasazuki et al., “Phosphorylation of serine 276 is essential for p65 NF-κB subunit-dependent cellular responses,” Biochemical and Biophysical Research Communications, vol. 300, no. 4, pp. 807–812, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. H. Zhong, R. E. Voll, and S. Ghosh, “Phosphorylation of NF-κB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300,” Molecular Cell, vol. 1, no. 5, pp. 661–671, 1998. View at Google Scholar · View at Scopus
  68. M. E. Gerritsen, A. J. Williams, A. S. Neish, S. Moore, Y. Shi, and T. Collins, “CREB-binding protein/p300 are transcriptional coactivators of p65,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 7, pp. 2927–2932, 1997. View at Publisher · View at Google Scholar · View at Scopus
  69. L. F. Chen, Y. Mu, and W. C. Greene, “Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-κB,” EMBO Journal, vol. 21, no. 23, pp. 6539–6548, 2002. View at Publisher · View at Google Scholar · View at Scopus
  70. R. Kiernan, V. Brès, R. W. M. Ng et al., “Post-activation turn-off of NF-κB-dependent transcription is regulated by acetylation of p65,” Journal of Biological Chemistry, vol. 278, no. 4, pp. 2758–2766, 2003. View at Publisher · View at Google Scholar · View at Scopus
  71. R. A. DeAngelis, K. Kovalovich, D. E. Cressman, and R. Taub, “Normal liver regeneration in p50/nuclear factor κB1 knockout mice,” Hepatology, vol. 33, no. 4, pp. 915–924, 2001. View at Publisher · View at Google Scholar · View at Scopus
  72. A. Kato, M. J. Edwards, and A. B. Lentsch, “Gene deletion of NF-κB p50 does not alter the hepatic inflammatory response to ischemia/reperfusion,” Journal of Hepatology, vol. 37, no. 1, pp. 48–55, 2002. View at Publisher · View at Google Scholar · View at Scopus
  73. K. P. Lu, Y. C. Liou, and X. Z. Zhou, “Pinning down proline-directed phosphorylation signaling,” Trends in Cell Biology, vol. 12, no. 4, pp. 164–172, 2002. View at Publisher · View at Google Scholar · View at Scopus
  74. A. Ryo, F. Suizu, Y. Yoshida et al., “Regulation of NF-κB Signaling by Pin1-Dependent Prolyl Isomerization and Ubiquitin-Mediated Proteolysis of p65/RelA,” Molecular Cell, vol. 12, no. 6, pp. 1413–1426, 2003. View at Publisher · View at Google Scholar · View at Scopus
  75. S. Kuboki, T. Okaya, R. Schuster et al., “Hepatocyte NF-κB activation is hepatoprotective during ischemia-reperfusion injury and is augmented by ischemic hypothermia,” American Journal of Physiology, vol. 292, no. 1, pp. G201–G207, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. K. D. Patel, S. L. Cuvelier, and S. Wiehler, “Selectins: critical mediators of leukocyte recruitment,” Seminars in Immunology, vol. 14, no. 2, pp. 73–81, 2002. View at Publisher · View at Google Scholar · View at Scopus
  77. I. Singh, G. B. Zibari, M. F. Brown et al., “Role of P-selectin expression in hepatic ischemia and reperfusion injury,” Clinical Transplantation, vol. 13, no. 1, pp. 76–82, 1999. View at Google Scholar · View at Scopus
  78. D. E. Sawaya Jr, G. B. Zibari, A. Minardi et al., “P-selectin contributes to the initial recruitment of rolling and adherent leukocytes in hepatic venules after ischemia/reperfusion,” Shock, vol. 12, no. 3, pp. 227–232, 1999. View at Google Scholar · View at Scopus
  79. J. Burke, G. B. Zibari, M. F. Brown et al., “Hepatic ischemia-reperfusion injury causes E-selectin upregulation,” Transplantation Proceedings, vol. 30, no. 5, pp. 2321–2323, 1998. View at Publisher · View at Google Scholar · View at Scopus
  80. S. S. Yadav, D. N. Howell, W. Gao, D. A. Steeber, R. C. Harland, and P. A. Clavien, “L-selectin and ICAM-1 mediate reperfusion injury and neutrophil adhesion in the warm ischemic mouse liver,” American Journal of Physiology, vol. 275, no. 6, pp. G1341–G1352, 1998. View at Google Scholar · View at Scopus
  81. K. Ley, “Integration of inflammatory signals by rolling neutrophils,” Immunological Reviews, vol. 186, pp. 8–18, 2002. View at Publisher · View at Google Scholar · View at Scopus
  82. H. Jaeschke, A. Farhood, A. P. Bautista, Z. Spolarics, J. J. Spitzer, and C. W. Smith, “Functional inactivation of neutrophils with a Mac-1 (CD11b/CD18) monoclonal antibody protects against ischemia-reperfusion injury in rat liver,” Hepatology, vol. 17, no. 5, pp. 915–923, 1993. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Farhood, G. M. McGuire, A. M. Manning, M. Miyasaka, C. W. Smith, and H. Jaeschke, “Intercellular adhesion molecule 1 (ICAM-1) expression and its role in neutrophil-induced ischemia-reperfusion injury in rat liver,” Journal of Leukocyte Biology, vol. 57, no. 3, pp. 368–374, 1995. View at Google Scholar · View at Scopus
  84. C. Peralta, L. Fernández, J. Panés et al., “Preconditioning protects against systemic disorders associated with hepatic ischemia-reperfusion through blockade of tumor necrosis factor-induced P-selectin up-regulation in the rat,” Hepatology, vol. 33, no. 1, pp. 100–113, 2001. View at Publisher · View at Google Scholar · View at Scopus
  85. S. S. Yadav, D. N. Howell, D. A. Steeber, R. C. Harland, T. F. Tedder, and P. A. Clavien, “P-selectin mediates reperfusion injury through neutrophil and platelet sequestration in the warm ischemic mouse liver,” Hepatology, vol. 29, no. 5, pp. 1494–1502, 1999. View at Publisher · View at Google Scholar · View at Scopus
  86. T. G. Diacovo, S. J. Roth, J. M. Buccola, D. F. Bainton, and T. A. Springer, “Neutrophil rolling, arrest, and transmigration across activated, surface-adherent platelets via sequential action of P-selectin and the β2- integrin CD11b/CD18,” Blood, vol. 88, no. 1, pp. 146–157, 1996. View at Google Scholar · View at Scopus
  87. D. Sindram, R. J. Porte, M. R. Hoffman, R. C. Bentley, and P. Clavien, “Platelets induce sinusoidal endothelial cell apoptosis upon reperfusion of the cold ischemic rat liver,” Gastroenterology, vol. 118, no. 1, pp. 183–191, 2000. View at Google Scholar · View at Scopus
  88. M. Baggiolini, “Chemokines in pathology and medicine,” Journal of Internal Medicine, vol. 250, no. 2, pp. 91–104, 2001. View at Publisher · View at Google Scholar · View at Scopus
  89. J. J. Oppenheim, C. O. C. Zachariae, N. Mukaida, and K. Matsushima, “Properties of the novel proinflammatory supergene ”intercrine” cytokine family,” Annual Review of Immunology, vol. 9, pp. 617–648, 1991. View at Google Scholar · View at Scopus
  90. A. Mantovani, R. Bonecchi, and M. Locati, “Tuning inflammation and immunity by chemokine sequestration: decoys and more,” Nature Reviews Immunology, vol. 6, no. 12, pp. 907–918, 2006. View at Publisher · View at Google Scholar · View at Scopus
  91. I. F. Charo and R. M. Ransohoff, “Mechanisms of disease: the many roles of chemokines and chemokine receptors in inflammation,” New England Journal of Medicine, vol. 354, no. 6, pp. 610–621, 2006. View at Publisher · View at Google Scholar · View at Scopus
  92. R. M. Strieter, P. J. Polverini, S. L. Kunkel et al., “The functional role of the ELR motif in CXC chemokine-mediated angiogenesis,” Journal of Biological Chemistry, vol. 270, no. 45, pp. 27348–27357, 1995. View at Publisher · View at Google Scholar · View at Scopus
  93. J. A. Belperio, M. P. Keane, D. A. Arenberg et al., “CXC chemokines in angiogenesis,” Journal of Leukocyte Biology, vol. 68, no. 1, pp. 1–8, 2000. View at Google Scholar · View at Scopus
  94. A. D. Luster, “Mechanisms of disease: chemokines-chemotactic cytokines that mediate inflammation,” New England Journal of Medicine, vol. 338, no. 7, pp. 436–445, 1998. View at Publisher · View at Google Scholar · View at Scopus
  95. K. Bacon, M. Baggiolini, H. Broxmeyer et al., “Chemokine/chemokine receptor nomenclature,” Cytokine, vol. 21, no. 1, pp. 48–49, 2003. View at Publisher · View at Google Scholar · View at Scopus
  96. I. Clark-Lewis, B. Dewald, T. Geiser, B. Moser, and M. Baggiolini, “Platelet factor 4 binds to interleukin 8 receptors and activates neutrophils when its N terminus is modified with Glu-Leu-Arg,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 8, pp. 3574–3577, 1993. View at Google Scholar · View at Scopus
  97. C. A. Hebert, R. V. Vitangcol, and J. B. Baker, “Scanning mutagenesis of interleukin-8 identifies a cluster of residues required for receptor binding,” Journal of Biological Chemistry, vol. 266, no. 28, pp. 18989–18994, 1991. View at Google Scholar · View at Scopus
  98. L. M. Colletti, M. E. Green, M. D. Burdick, and R. M. Strieter, “The ratio of ELR+ to ELR- CXC chemokines affects the lung and liver injury following hepatic ischemia/reperfusion in the rat,” Hepatology, vol. 31, no. 2, pp. 435–445, 2000. View at Google Scholar · View at Scopus
  99. R. Stillie, S. M. Farooq, J. R. Gordon, and A. W. Stadnyk, “The functional significance behind expressing two IL-8 receptor types on PMN,” Journal of Leukocyte Biology, vol. 86, no. 3, pp. 529–543, 2009. View at Publisher · View at Google Scholar · View at Scopus
  100. C. Clarke, S. Kuboki, N. Sakai et al., “CXC chemokine receptor-1 is expressed by hepatocytes and regulates liver recovery after hepatic ischemia/reperfusion injury,” Hepatology, vol. 53, no. 1, pp. 261–271, 2011. View at Publisher · View at Google Scholar · View at Scopus
  101. C. M. Hogaboam, C. L. Bone-Larson, M. L. Steinhauser et al., “Novel CXCR2-dependent liver regenerative qualities of ELR-containing CXC chemokines,” FASEB Journal, vol. 13, no. 12, pp. 1565–1574, 1999. View at Google Scholar · View at Scopus
  102. A. R. Nagendra, J. K. Mickelson, and C. W. Smith, “CD18 integrin and CD54-dependent neutrophil adhesion to cytokine- stimulated human hepatocytes,” American Journal of Physiology, vol. 272, no. 3, pp. G408–G416, 1997. View at Google Scholar · View at Scopus
  103. N. M. Boury and C. J. Czuprynski, “Listeria monocytogenes infection increases neutrophil adhesion and damage to a murine hepatocyte cell line in vitro,” Immunology Letters, vol. 46, no. 1-2, pp. 111–116, 1995. View at Publisher · View at Google Scholar · View at Scopus
  104. H. Jaeschke, A. P. Bautista, Z. Spolarics, and J. J. Spitzer, “Superoxide generation by Kupffer cells and priming of neutrophils during reperfusion after hepatic ischemia.,” Free radical research communications, vol. 15, no. 5, pp. 277–284, 1991. View at Google Scholar · View at Scopus
  105. T. W. Wu, N. Hashimoto, J. X. Au, J. Wu, D. A. G. Mickle, and D. Carey, “Trolox protects rat hepatocytes against oxyradical damage and the ischemic rat liver from reperfusion injury,” Hepatology, vol. 13, no. 3, pp. 575–580, 1991. View at Publisher · View at Google Scholar · View at Scopus
  106. P. Mavier, B. Guigui, A. M. Preaux et al., “In vitro toxicity of hydrogen peroxide against normal vs. tumor rat hepatocytes: role of catalase and of the glutathione redox cycle,” Hepatology, vol. 8, no. 6, pp. 1673–1678, 1988. View at Google Scholar · View at Scopus
  107. X. K. Li, A. F. M. Matin, H. Suzuki, T. Uno, T. Yamaguchi, and Y. Harada, “Effect of protease inhibitor on ischemia/reperfusion injury of the rat liver,” Transplantation, vol. 56, no. 6, pp. 1331–1336, 1993. View at Google Scholar · View at Scopus
  108. J. S. Kim, L. He, and J. J. Lemasters, “Mitochondrial permeability transition: A common pathway to necrosis and apoptosis,” Biochemical and Biophysical Research Communications, vol. 304, no. 3, pp. 463–470, 2003. View at Publisher · View at Google Scholar · View at Scopus
  109. E. Bonfoco, D. Krainc, M. Ankarcrona, P. Nicotera, and S. A. Lipton, “Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 16, pp. 7162–7166, 1995. View at Publisher · View at Google Scholar · View at Scopus
  110. Y. Eguchi, S. Shimizu, and Y. Tsujimoto, “Intracellular ATP levels determine cell death fate by apoptosis or necrosis,” Cancer Research, vol. 57, no. 10, pp. 1835–1840, 1997. View at Google Scholar · View at Scopus
  111. M. Leist, B. Single, A. F. Castoldi, S. Kühnle, and P. Nicotera, “Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis,” Journal of Experimental Medicine, vol. 185, no. 8, pp. 1481–1486, 1997. View at Publisher · View at Google Scholar · View at Scopus
  112. V. Kohli, M. Selzner, J. F. Madden, R. C. Bentley, and P. A. Clavien, “Endothelial cell and hepatocyte deaths occur by apoptosis after ischemia-reperfusion injury in the rat liver,” Transplantation, vol. 67, no. 8, pp. 1099–1105, 1999. View at Publisher · View at Google Scholar · View at Scopus
  113. R. Cursio, J. Gugenheim, J. E. Ricci et al., “A caspase inhibitor fully protects rats against lethal normothermic liver ischemia by inhibition of liver apoptosis,” FASEB Journal, vol. 13, no. 2, pp. 253–261, 1999. View at Google Scholar · View at Scopus
  114. J. S. Gujral, T. J. Bucci, A. Farhood, and H. Jaeschke, “Mechanism of cell death during warm hepatic ischemia-reperfusion in rats: apoptosis or necrosis?” Hepatology, vol. 33, no. 2, pp. 397–405, 2001. View at Publisher · View at Google Scholar · View at Scopus
  115. K. Yamabe, S. Shimizu, W. Kamiike et al., “Prevention of hypoxic liver cell necrosis by in vivo human bcl-2 gene transfection,” Biochemical and Biophysical Research Communications, vol. 243, no. 1, pp. 217–223, 1998. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Selzner, H. A. Rüdiger, N. Selzner, D. W. Thomas, D. Sindram, and P. A. Clavien, “Transgenic mice overexpressing human Bcl-2 are resistant to hepatic ischemia and reperfusion,” Journal of Hepatology, vol. 36, no. 2, pp. 218–225, 2002. View at Publisher · View at Google Scholar · View at Scopus
  117. H. A. Rüdiger and P. Clavien, “Tumor necrosis factor α, but not Fas, mediates hepatocellular apoptosis in the murine ischemic liver,” Gastroenterology, vol. 122, no. 1, pp. 202–210, 2002. View at Google Scholar · View at Scopus
  118. H. Hsu, H. B. Shu, M. G. Pan, and D. V. Goeddel, “TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways,” Cell, vol. 84, no. 2, pp. 299–308, 1996. View at Publisher · View at Google Scholar · View at Scopus
  119. C. Y. Wang, M. W. Mayo, R. G. Korneluk, D. V. Goeddel, and A. S. Baldwin Jr, “NF-B antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c- IAP2 to suppress caspase-8 activation,” Science, vol. 281, no. 5383, pp. 1680–1683, 1998. View at Publisher · View at Google Scholar · View at Scopus
  120. D. J. Van Antwerp, S. J. Martin, T. Kafri, D. R. Green, and I. M. Verma, “Suppression of TNF-α-induced apoptosis by NF-κB,” Science, vol. 274, no. 5288, pp. 787–789, 1996. View at Publisher · View at Google Scholar · View at Scopus
  121. C. Y. Wang, M. W. Mayo, and A. S. Baldwin Jr, “TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-κB,” Science, vol. 274, no. 5288, pp. 784–787, 1996. View at Publisher · View at Google Scholar · View at Scopus
  122. A. A. Beg, W. C. Sha, R. T. Bronson, S. Ghosh, and D. Baltimore, “Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-κB,” Nature, vol. 376, no. 6536, pp. 167–170, 1995. View at Google Scholar · View at Scopus
  123. D. Wallach, “Preparations of lymphotoxin induce resistance to their own cytotoxic effect,” Journal of Immunology, vol. 132, no. 5, pp. 2464–2469, 1984. View at Google Scholar · View at Scopus
  124. K. R. McCurry, D. A. Campbell Jr, W. E. Scales, J. S. Warren, and D. G. Remick, “Tumor necrosis factor, interleukin 6, and the acute phase response following hepatic ischemia/reperfusion,” Journal of Surgical Research, vol. 55, no. 1, pp. 49–54, 1993. View at Publisher · View at Google Scholar · View at Scopus
  125. A. Kato, T. Okaya, and A. B. Lentsch, “Endogenous IL-13 protects hepatocytes and vascular endothelial cells during ischemia/reperfusion injury,” Hepatology, vol. 37, no. 2, pp. 304–312, 2003. View at Publisher · View at Google Scholar · View at Scopus
  126. C. A. Camargo Jr, J. F. Madden, W. Gao, R. S. Selvan, and P. A. Clavien, “Interleukin-6 protects liver against warm ischemia/reperfusion injury and promotes hepatocyte proliferation in the rodent,” Hepatology, vol. 26, no. 6, pp. 1513–1520, 1997. View at Google Scholar · View at Scopus
  127. H. Yoshidome, A. Kato, M. J. Edwards, and A. B. Lentsch, “Interleukin-10 inhibits pulmonary NF-κB activation and lung injury induced by hepatic ischemia-reperfusion,” American Journal of Physiology, vol. 277, no. 5, pp. L919–L923, 1999. View at Google Scholar · View at Scopus
  128. H. Yoshidome, A. Kato, M. J. Edwards, and A. B. Lentsch, “Interleukin-10 suppresses hepatic ischemia/reperfusion injury in mice: implications of a central role for nuclear factor κB,” Hepatology, vol. 30, no. 1, pp. 203–208, 1999. View at Publisher · View at Google Scholar · View at Scopus
  129. H. Yoshidome, A. Kato, M. Miyazaki, M. J. Edwards, and A. B. Lentsch, “IL-13 activates STAT6 and inhibits liver injury induced by ischemia/reperfusion,” American Journal of Pathology, vol. 155, no. 4, pp. 1059–1064, 1999. View at Google Scholar · View at Scopus
  130. Y. Ohmori and T. A. Hamilton, “Interleukin-4/STAT6 represses STAT1 and NF-κB-dependent transcription through distinct mechanisms,” Journal of Biological Chemistry, vol. 275, no. 48, pp. 38095–38103, 2000. View at Publisher · View at Google Scholar · View at Scopus
  131. A. B. Lentsch, H. Yoshidome, R. L. Warner, P. A. Ward, and M. J. Edwards, “Secretory leukocyte protease inhibitor in mice regulates local and remote organ inflammatory injury induced by hepatic ischemia/reperfusion,” Gastroenterology, vol. 117, no. 4, pp. 953–961, 1999. View at Publisher · View at Google Scholar · View at Scopus
  132. A. B. Lentsch, J. A. Jordan, B. J. Czermak et al., “Inhibition of NF-κB activation and augmentation of IκBβ by secretory leukocyte protease inhibitor during lung inflammation,” American Journal of Pathology, vol. 154, no. 1, pp. 239–247, 1999. View at Google Scholar · View at Scopus
  133. F. Y. Jin, C. Nathan, D. Radzioch, and A. Ding, “Secretory leukocyte protease inhibitor: a macrophage product induced by and antagonistic to bacterial lipopolysaccharide,” Cell, vol. 88, no. 3, pp. 417–426, 1997. View at Publisher · View at Google Scholar · View at Scopus
  134. H. Jaeschke and C. W. Smith, “Mechanisms of neutrophil-induced parenchymal cell injury,” Journal of Leukocyte Biology, vol. 61, no. 6, pp. 647–653, 1997. View at Google Scholar · View at Scopus
  135. M. S. Mulligan, A. B. Lentsch, M. Huber-Lang et al., “Anti-inflammatory effects of mutant forms of secretory leukocyte protease inhibitor,” American Journal of Pathology, vol. 156, no. 3, pp. 1033–1039, 2000. View at Google Scholar · View at Scopus
  136. C. D. Wright, J. A. Kennedy, R. J. Zitnik, and M. A. Kashem, “Inhibition of murine neutrophil serine proteinases by human and murine secretory leukocyte protease inhibitor,” Biochemical and Biophysical Research Communications, vol. 254, no. 3, pp. 614–617, 1999. View at Publisher · View at Google Scholar · View at Scopus
  137. H. Jaeschke, V. B. Schini, and A. Farhood, “Role of nitric oxide in the oxidant stress during ischemia/reperfusion injury of the liver,” Life Sciences, vol. 50, no. 23, pp. 1797–1804, 1992. View at Publisher · View at Google Scholar · View at Scopus
  138. B. G. Harbrecht and T. R. Billiar, “The role of nitric oxide in Kupffer cell-hepatocyte interactions.,” Shock, vol. 3, no. 2, pp. 79–87, 1995. View at Google Scholar · View at Scopus
  139. F. Esteban, J. Gomez-Jimenez, M. C. Martin et al., “Nitric oxide and hepatic ischemic injury in human orthotopic liver transplantation,” Transplantation Proceedings, vol. 27, no. 4, pp. 2283–2285, 1995. View at Google Scholar · View at Scopus
  140. H. Kobayashi, T. Nonami, T. Kurokawa et al., “Role of endogenous nitric oxide in ischemia-reperfusion injury in rat liver,” Journal of Surgical Research, vol. 59, no. 6, pp. 772–779, 1995. View at Publisher · View at Google Scholar · View at Scopus
  141. C. Peralta, G. Hotter, D. Closa, E. Gelpí, O. Bulbena, and J. Roselló-Catafau, “Protective effect of preconditioning on the injury associated to hepatic ischemia-reperfusion in the rat: role of nitric oxide and adenosine,” Hepatology, vol. 25, no. 4, pp. 934–937, 1997. View at Publisher · View at Google Scholar · View at Scopus
  142. T. A. Koeppel, J. C. Thies, P. Schemmer et al., “Inhibition of nitric oxide synthesis in ischemia/reperfusion of the rat liver is followed by impairment of hepatic microvascular blood flow,” Journal of Hepatology, vol. 27, no. 1, pp. 163–169, 1997. View at Publisher · View at Google Scholar · View at Scopus
  143. P. Liu, K. Yin, R. Nagele, and P. Y. K. Wong, “Inhibition of nitric oxide synthase attenuates peroxynitrite generation, but augments neutrophil accumulation in hepatic ischemia-reperfusion in rats,” Journal of Pharmacology and Experimental Therapeutics, vol. 284, no. 3, pp. 1139–1146, 1998. View at Google Scholar · View at Scopus
  144. B. H. J. Pannen, F. Al-Adili, M. Bauer, M. G. Clemens, and K. K. Geiger, “Role of endothelins and nitric oxide in hepatic reperfusion injury in the rat,” Hepatology, vol. 27, no. 3, pp. 755–764, 1998. View at Publisher · View at Google Scholar · View at Scopus
  145. B. S. Taylor, L. H. Alarcon, and T. R. Billiar, “Inducible nitric oxide synthase in the liver: regulation and function,” Biochemistry, vol. 63, no. 7, pp. 766–781, 1998. View at Google Scholar · View at Scopus
  146. H. Ohmori, D. K. Dhar, Y. Nakashima, M. Hashimoto, S. Masumura, and N. Nagasue, “Beneficial effects of FK409, a novel nitric oxide donor, on reperfusion injury of rat liver,” Transplantation, vol. 66, no. 5, pp. 579–585, 1998. View at Publisher · View at Google Scholar · View at Scopus
  147. T. Shimamura, Y. Zhu, S. Zhang et al., “Protective role of nitric oxide in ischemia and reperfusion injury of the liver,” Journal of the American College of Surgeons, vol. 188, no. 1, pp. 43–52, 1999. View at Publisher · View at Google Scholar · View at Scopus
  148. V. G. Lee, M. L. Johnson, J. Baust, V. E. Laubach, S. C. Watkins, and T. R. Billiar, “The roles of iNOS in liver ischemia-reperfusion injury,” Shock, vol. 16, no. 5, pp. 355–360, 2001. View at Google Scholar · View at Scopus
  149. I. N. Hines, S. Kawachi, H. Harada et al., “Role of nitric oxide in liver ischemia and reperfusion injury,” Molecular and Cellular Biochemistry, vol. 234-235, pp. 229–237, 2002. View at Publisher · View at Google Scholar · View at Scopus
  150. I. N. Hines, H. Harada, S. Flores, B. Gao, J. M. McCord, and M. B. Grisham, “Endothelial nitric oxide synthase protects the post-ischemic liver: potential interactions with superoxide,” Biomedicine and Pharmacotherapy, vol. 59, no. 4, pp. 183–189, 2005. View at Publisher · View at Google Scholar · View at Scopus
  151. M. R. Duranski, J. W. Elrod, J. W. Calvert, N. S. Bryan, M. Feelisch, and D. J. Lefer, “Genetic overexpression of eNOS attenuates hepatic ischemia-reperfusion injury,” American Journal of Physiology, vol. 291, no. 6, pp. H2980–H2986, 2006. View at Publisher · View at Google Scholar · View at Scopus
  152. A. Zimmermann, “Regulation of liver regeneration,” Nephrology Dialysis Transplantation, vol. 19, supplement 4, pp. iv6–iv10, 2004. View at Publisher · View at Google Scholar · View at Scopus
  153. N. Fausto, J. S. Campbell, and K. J. Riehle, “Liver regeneration,” Hepatology, vol. 43, no. 2, pp. S45–S53, 2006. View at Publisher · View at Google Scholar · View at Scopus
  154. G. K. Michalopoulos, “Liver regeneration,” Journal of Cellular Physiology, vol. 213, no. 2, pp. 286–300, 2007. View at Publisher · View at Google Scholar · View at Scopus
  155. E. M. Webber, J. Bruix, R. H. Pierce, and N. Fausto, “Tumor necrosis factor primes hepatocytes for DNA replication in the rat,” Hepatology, vol. 28, no. 5, pp. 1226–1234, 1998. View at Publisher · View at Google Scholar · View at Scopus
  156. G. Michalopoulos, K. A. Houck, M. L. Dolan, and N. C. Luetteke, “Control of hepatocyte replication by two serum factors,” Cancer Research, vol. 44, no. 10, pp. 4414–4419, 1984. View at Google Scholar · View at Scopus
  157. T. Nakamura, K. Nawa, and A. Ichihara, “Partial formation and characterization of hepatocyte growth factor from serum of hepatectomized rats,” Biochemical and Biophysical Research Communications, vol. 122, no. 3, pp. 1450–1459, 1984. View at Google Scholar · View at Scopus
  158. E. Albi, G. Rossi, N. M. Maraldi et al., “Involvement of nuclear phosphatidylinositol-dependent phospholipases C in cell cycle progression during rat liver regeneration,” Journal of Cellular Physiology, vol. 197, no. 2, pp. 181–188, 2003. View at Publisher · View at Google Scholar · View at Scopus
  159. C. G. Nebigil, “Suppression of phospholipase C β, γ, and δ families alters cell growth and phosphatidylinositol 4,5-bisphosphate levels,” Biochemistry, vol. 36, no. 50, pp. 15949–15958, 1997. View at Publisher · View at Google Scholar · View at Scopus
  160. T. Adachi, S. Nakashima, S. Saji, T. Nakamura, and Y. Nozawa, “Mitogen-activated protein kinase activation in hepatocyte growth factor-stimulated rat hepatocytes: involvement of protein tyrosine kinase and protein kinase C,” Hepatology, vol. 23, no. 5, pp. 1244–1253, 1996. View at Google Scholar · View at Scopus
  161. A. Coutant, C. Rescan, D. Gilot, P. Loyer, C. Guguen-Guillouzo, and G. Baffet, “PI3K-FRAP/mTOR pathway is critical for hepatocyte proliferation whereas MEK/ERK supports both proliferation and survival,” Hepatology, vol. 36, no. 5, pp. 1079–1088, 2002. View at Publisher · View at Google Scholar · View at Scopus
  162. A. Watanabe, S. Nakashima, T. Adachi, S. Saji, and Y. Nozawa, “Changes the expression of lipid-mediated signal-transducing enzymes in the rat liver after partial hepatectomy,” Surgery Today, vol. 30, no. 7, pp. 622–630, 2000. View at Google Scholar · View at Scopus
  163. T. Adachi, S. Nakashima, S. Saji, T. Nakamura, and Y. Nozawa, “Possible involvement of pertussis toxin-sensitive G protein in hepatocyte growth factor-induced signal transduction in cultured rat hepatocytes: pertussis toxin treatment inhibits activation of phospholipid signaling, calcium oscillation, and mitogen-activated protein kinase,” Hepatology, vol. 26, no. 2, pp. 295–300, 1997. View at Publisher · View at Google Scholar · View at Scopus
  164. M. Refsnes, O. F. Dajani, D. Sandnes et al., “On the mechanisms of the growth-promoting effect of prostaglandins in hepatocytes: the relationship between stimulation of DNA synthesis and signaling mediated by adenylyl cyclase and phosphoinositide-specific phospholipase C,” Journal of Cellular Physiology, vol. 164, no. 3, pp. 465–473, 1995. View at Publisher · View at Google Scholar · View at Scopus
  165. D. C. Harrison, J. J. Lemasters, and B. Herman, “A pH-dependent phospholipase A2 contributes to loss of plasma membrane integrity during chemical hypoxia in rat hepatocytes1,” Biochemical and Biophysical Research Communications, vol. 174, no. 2, pp. 654–659, 1991. View at Google Scholar · View at Scopus
  166. H. Malhi, G. J. Gores, and J. J. Lemasters, “Apoptosis and necrosis in the liver: a tale of two deaths?” Hepatology, vol. 43, no. 2, pp. S31–S44, 2006. View at Publisher · View at Google Scholar · View at Scopus
  167. T. P. Reilly, J. N. Brady, M. R. Marchick et al., “A protective role for cyclooxygenase-2 in drug-induced liver injury in mice,” Chemical Research in Toxicology, vol. 14, no. 12, pp. 1620–1628, 2001. View at Publisher · View at Google Scholar · View at Scopus
  168. C. N. Clarke, S. Kuboki, A. Tevar, A. B. Lentsch, and M. Edwards, “CXC chemokines play a critical role in liver injury, recovery, and regeneration,” American Journal of Surgery, vol. 198, no. 3, pp. 415–419, 2009. View at Publisher · View at Google Scholar · View at Scopus
  169. L. M. Colletti, M. Green, M. D. Burdick, S. L. Kunkel, and R. M. Strieter, “Proliferative effects of CXC chemokines in rat hepatocytes in vitro and in vivo,” Shock, vol. 10, no. 4, pp. 248–257, 1998. View at Google Scholar · View at Scopus
  170. S. Kuboki, T. Shin, N. Huber et al., “Hepatocyte signaling through CXC chemokine receptor-2 is detrimental to liver recovery after ischemia/reperfusion in mice,” Hepatology, vol. 48, no. 4, pp. 1213–1223, 2008. View at Publisher · View at Google Scholar · View at Scopus
  171. L. Stefanovic and B. Stefanovic, “Mechanism of direct hepatotoxic effect of KC chemokine: sequential activation of gene expression and progression from inflammation to necrosis,” Journal of Interferon and Cytokine Research, vol. 26, no. 10, pp. 760–770, 2006. View at Publisher · View at Google Scholar · View at Scopus
  172. S. Barone, T. Okaya, S. Rudich et al., “Distinct and sequential upregulation of genes regulating cell growth and cell cycle progression during hepatic ischemia-reperfusion injury,” American Journal of Physiology, vol. 289, no. 4, pp. C826–C835, 2005. View at Publisher · View at Google Scholar · View at Scopus
  173. W. Fu, Y. Zhang, J. Zhang, and W. F. Chen, “Cloning and characterization of mouse homolog of the CXC chemokine receptor CXCR1,” Cytokine, vol. 31, no. 1, pp. 9–17, 2005. View at Publisher · View at Google Scholar · View at Scopus
  174. X. Fan, A. C. Patera, A. Pong-Kennedy et al., “Murine CXCR1 is a functional receptor for GCP-2/CXCL6 and interleukin-8/CXCL8,” Journal of Biological Chemistry, vol. 282, no. 16, pp. 11658–11666, 2007. View at Publisher · View at Google Scholar · View at Scopus
  175. C. L. Bone-Larson, C. M. Hogaboam, H. Evanhoff, R. M. Strieter, and S. L. Kunkel, “IFN-γ-inducible protein-10 (CXCL10) is hepatoprotective during acute liver injury through the induction of CXCR2 on hepatocytes,” Journal of Immunology, vol. 167, no. 12, pp. 7077–7083, 2001. View at Google Scholar · View at Scopus