Cytoprotective effects of a cyclic rgd peptide in steatotic liver cold ischemia and reperfusion injury

American Journal of Transplantation

Volumn 9, Issue 10, 2009, Pages 2240-2250

  Fondevila, C ^a   Shen, X D ^a   Duarte, S ^a   Busuttil, R W ^a   Coito, A J ^a  

^a UCLA MEDICAL CENTER   (United States)

Author keywords

Fibronectin; Hepatic steatosis; Inflammation; Integrin; Ischemia reperfusion injury; Liver transplantation

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; CYCLIC ARGINYLGLYCYLASPARTIC ACID; FIBRONECTIN RECEPTOR; GAMMA INTERFERON; GELATINASE B; INDUCIBLE NITRIC OXIDE SYNTHASE; MYELOPEROXIDASE; PROTEIN KINASE B; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ADHESION; CELL MIGRATION; COLD ISCHEMIA; CONTROLLED STUDY; DOWN REGULATION; FATTY LIVER; GRAFT SURVIVAL; IMMUNOHISTOCHEMISTRY; LIVER INJURY; LIVER ISCHEMIA; LIVER PROTECTION; LIVER TRANSPLANTATION; MALE; NEUTROPHIL CHEMOTAXIS; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SURVIVAL RATE; UPREGULATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; COLD TEMPERATURE; CYTOPROTECTION; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FATTY LIVER; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INTERFERON-GAMMA; MATRIX METALLOPROTEINASE 9; NEUTROPHILS; NITRIC OXIDE SYNTHASE TYPE II; OLIGOPEPTIDES; RATS; REPERFUSION INJURY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SURVIVAL RATE;

EID: 70349193665     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2009.02759.x     Document Type: Article

References (59)

1. Wight C, Cohen B. Shortage of organs for transplantation. BMJ 1996 312 : 989 990.
2. Koneru B, Dikdan G. Hepatic steatosis and liver transplantation current clinical and experimental perspectives. Transplantation 2002 73 : 325 330.
3. Strasberg SM, Howard TK, Molmenti EP, Hertl M. Selecting the donor liver: Risk factors for poor function after orthotopic liver transplantation. Hepatology 1994 20 : 829 838.
4. Taneja C, Prescott L, Koneru B. Critical preservation injury in rat fatty liver is to hepatocytes, not sinusoidal lining cells. Transplantation 1998 65 : 167 172.
5. Caraceni P, Nardo B, Domenicali M et al. Ischemia-reperfusion injury in rat fatty liver: Role of nutritional status. Hepatology 1999 29 : 1139 1146.
6. Selzner M, Clavien PA. Fatty liver in liver transplantation and surgery. Semin Liver Dis 2001 21 : 105 113.
7. Jaeschke H, Hasegawa T. Role of neutrophils in acute inflammatory liver injury. Liver Int 2006 26 : 912 919. (Pubitemid 44323408)
8. Bianchi E, Bender JR, Blasi F, Pardi R. Through and beyond the wall: Late steps in leukocyte transendothelial migration. Immunol Today 1997 18 : 586 591.
9. Jarnagin WR, Rockey DC, Koteliansky VE, Wang SS, Bissell DM. Expression of variant fibronectins in wound healing: Cellular source and biological activity of the EIIIA segment in rat hepatic fibrogenesis. J Cell Biol 1994 127 : 2037 2048.
10. Amersi F, Shen XD, Moore C et al. Fibronectin-alpha 4 beta 1 integrin-mediated blockade protects genetically fat Zucker rat livers from ischemia/reperfusion injury. Am J Pathol 2003 162 : 1229 1239.
11. Coito AJ, de Sousa M, Kupiec-Weglinski JW. Fibronectin in immune responses in organ transplant recipients. Dev Immunol 2000 7 : 239 248.
12. Yi M, Ruoslahti E. A fibronectin fragment inhibits tumor growth, angiogenesis, and metastasis. Proc Natl Acad Sci USA 2001 98 : 620 624.
13. Elices MJ, Tsai V, Strahl D et al. Expression and functional significance of alternatively spliced CS1 fibronectin in rheumatoid arthritis microvasculature. J Clin Invest 1994 93 : 405 416.
14. Coito AJ, Brown LF, Peters JH, Kupiec-Weglinski JW, Van De WL. Expression of fibronectin splicing variants in organ transplantation: A differential pattern between rat cardiac allografts and isografts. Am J Pathol 1997 150 : 1757 1772.
15. Hynes RO. Cell-matrix adhesion in vascular development. J Thromb Haemost 2007 5 (Suppl 1 32 40.
16. Hynes RO. Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 1992 69 : 11 25.
17. Matsuyama T, Yamada A, Kay J et al. Activation of CD4 cells by fibronectin and anti-CD3 antibody. A synergistic effect mediated by the VLA-5 fibronectin receptor complex. J Exp Med 1989 170 : 1133 1148.
18. Shang XZ, Lang BJ, Issekutz AC. Adhesion molecule mechanisms mediating monocyte migration through synovial fibroblast and endothelium barriers: Role for CD11/CD18, very late antigen-4 (CD49d/CD29), very late antigen-5 (CD49e/CD29), and vascular cell adhesion molecule-1 (CD106). J Immunol 1998 160 : 467 474.
19. Bohnsack JF, Chang J, Zhou X, Yednock TA. Mechanisms of beta 1 integrin-dependent adherence of granulocytic HL60 to fibronectin. J Leukoc Biol 1995 57 : 592 599.
20. Koivunen E, Wang B, Ruoslahti E. Phage libraries displaying cyclic peptides with different ring sizes: Ligand specificities of the RGD-directed integrins. Biotechnology (NY) 1995 13 : 265 270.
21. Kamada N, Calne RY. A surgical experience with five hundred thirty liver transplants in the rat. Surgery 1983 93 : 64 69.
22. Pierschbacher MD, Ruoslahti E. Influence of stereochemistry of the sequence Arg-Gly-Asp-Xaa on binding specificity in cell adhesion. J Biol Chem 1987 262 : 17294 17298.
23. Suzuki S, Toledo-Pereyra LH, Rodriguez FJ, Cejalvo D. Neutrophil infiltration as an important factor in liver ischemia and reperfusion injury. Modulating effects of FK506 and cyclosporine. Transplantation 1993 55 : 1265 1272.
24. Kato A, Yoshidome H, Edwards MJ, Lentsch AB. Regulation of liver inflammatory injury by signal transducer and activator of transcription-6. Am J Pathol 2000 157 : 297 302.
25. Moore C, Shen XD, Gao F, Busuttil RW, Coito AJ. Fibronectin-alpha4beta1 integrin interactions regulate metalloproteinase-9 expression in steatotic liver ischemia and reperfusion injury. Am J Pathol 2007 170 : 567 577.
26. Hamada T, Fondevila C, Busuttil RW, Coito AJ. Metalloproteinase-9 deficiency protects against hepatic ischemia/reperfusion injury. Hepatology 2008 47 : 186 198.
27. Hamada T, Tsuchihashi S, Avanesyan A et al. Cyclooxygenase-2 deficiency enhances Th2 immune responses and impairs neutrophil recruitment in hepatic ischemia/reperfusion injury. J Immunol 2008 180 : 1843 1853.
28. Han S, Ritzenthaler JD, Sitaraman SV, Roman J. Fibronectin increases matrix metalloproteinase 9 expression through activation of c-Fos via extracellular-regulated kinase and phosphatidylinositol 3-kinase pathways in human lung carcinoma cells. J Biol Chem 2006 281 : 29614 29624.
29. Nathan C. Inducible nitric oxide synthase: What difference does it make? J Clin Invest 1997 100 : 2417 2423.
30. Isobe M, Katsuramaki T, Hirata K, Kimura H, Nagayama M, Matsuno T. Beneficial effects of inducible nitric oxide synthase inhibitor on reperfusion injury in the pig liver. Transplantation 1999 68 : 803 813.
31. Lappas CM, Rieger JM, Linden J. A2A adenosine receptor induction inhibits IFN-gamma production in murine CD4+ T cells. J Immunol 2005 174 : 1073 1080.
32. Rudiger HA, Graf R, Clavien PA. Liver ischemia: Apoptosis as a central mechanism of injury. J Invest Surg 2003 16 : 149 159.
33. Han Z, Hendrickson EA, Bremner TA, Wyche JH. A sequential two-step mechanism for the production of the mature p17:p12 form of caspase-3 in vitro. J Biol Chem 1997 272 : 13432 13436.
34. Mullonkal CJ, Toledo-Pereyra LH. Akt in ischemia and reperfusion. J Invest Surg 2007 20 : 195 203.
35. Lawrence MB, Springer TA. Leukocytes roll on a selectin at physiologic flow rates: Distinction from and prerequisite for adhesion through integrins. Cell 1991 65 : 859 873.
36. Wong J, Johnston B, Lee SS et al. A minimal role for selectins in the recruitment of leukocytes into the inflamed liver microvasculature. J Clin Invest 1997 99 : 2782 2790.
37. Gaboury JP, Kubes P. Reductions in physiologic shear rates lead to CD11/CD18-dependent, selectin-independent leukocyte rolling in vivo. Blood 1994 83 : 345 350.
38. Hayashi M, Tokunaga Y, Fujita T, Tanaka K, Yamaoka Y, Ozawa K. The effects of cold preservation on steatotic graft viability in rat liver transplantation. Transplantation 1993 56 : 282 287.
39. Gao W, Connor HD, Lemasters JJ, Mason RP, Thurman RG. Primary nonfunction of fatty livers produced by alcohol is associated with a new, antioxidant-insensitive free radical species. Transplantation 1995 59 : 674 679.
40. Noiri E, Gailit J, Sheth D et al. Cyclic RGD peptides ameliorate ischemic acute renal failure in rats. Kidney Int 1994 46 : 1050 1058.
41. Bruck R, Hershkoviz R, Lider O et al. Inhibition of experimentally- induced liver cirrhosis in rats by a nonpeptidic mimetic of the extracellular matrix-associated Arg-Gly-Asp epitope. J Hepatol 1996 24 : 731 738.
42. Bruck R, Hershkoviz R, Lider O, Shirin H, Aeed H, Halpern Z. The use of synthetic analogues of Arg-Gly-Asp (RGD) and soluble receptor of tumor necrosis factor to prevent acute and chronic experimental liver injury. Yale J Biol Med 1997 70 : 391 402.
43. Laskin DL, Pendino KJ. Macrophages and inflammatory mediators in tissue injury. Annu Rev Pharmacol Toxicol 1995 35 : 655 677.
44. Weber C, Alon R, Moser B, Springer TA. Sequential regulation of alpha 4 beta 1 and alpha 5 beta 1 integrin avidity by CC chemokines in monocytes: Implications for transendothelial chemotaxis. J Cell Biol 1996 134 : 1063 1073.
45. Elitok S, Brodsky SV, Patschan D et al. Cyclic arginine-glycine-aspartic acid peptide inhibits macrophage infiltration of the kidney and carotid artery lesions in apo-E-deficient mice. Am J Physiol Renal Physiol 2006 290 : F159 F166.
46. Bohnsack JF, Zhou XN. Divalent cation substitution reveals. J Immunol 1992 149 : 1340 1347.
47. Burns JA, Issekutz TB, Yagita H, Issekutz AC. The alpha 4 beta 1 (very late antigen (VLA)-4, CD49d/CD29) and alpha 5 beta 1 (VLA-5, CD49e/CD29) integrins mediate beta 2 (CD11/CD18) integrin-independent neutrophil recruitment to endotoxin-induced lung inflammation. J Immunol 2001 166 : 4644 4649.
48. Hamada T, Duarte S, Tsuchihashi S et al. Inducible nitric oxide synthase deficiency impairs matrix metalloproteinase-9 activity and disrupts leukocyte migration in hepatic ischemia/reperfusion injury. Am J Pathol 2009 174 : 2265 2277.
49. Xie B, Laouar A, Huberman E. Fibronectin-mediated cell adhesion is required for induction of 92-kDa type IV collagenase/gelatinase (MMP-9) gene expression during macrophage differentiation. The signaling role of protein kinase C-beta. J Biol Chem 1998 273 : 11576 11582.
50. Chana RS, Martin J, Rahman EU, Wheeler DC. Monocyte adhesion to mesangial matrix modulates cytokine and metalloproteinase production. Kidney Int 2003 63 : 889 898.
51. Anderson DG, Li X, Balian G. A fibronectin fragment alters the metabolism by rabbit intervertebral disc cells in vitro. Spine 2005 30 : 1242 1246.
52. Redondo-Munoz J, Escobar-Diaz E, Samaniego R, Terol MJ, Garcia-Marco JA, Garcia-Pardo A. MMP-9 in B-cell chronic lymphocytic leukemia is up-regulated by alpha4beta1 integrin or CXCR4 engagement via distinct signaling pathways, localizes to podosomes, and is involved in cell invasion and migration. Blood 2006 108 : 3143 3151.
53. Baskin-Bey ES, Canbay A, Bronk SF et al. Cathepsin B inactivation attenuates hepatocyte apoptosis and liver damage in steatotic livers after cold ischemia-warm reperfusion injury. Am J Physiol Gastrointest Liver Physiol 2005 288 : G396 G402.
54. Lemasters JJ. V. Necrapoptosis and the mitochondrial permeability transition: Shared pathways to necrosis and apoptosis. Am J Physiol 1999 276 : G1 G6.
55. Hierholzer C, Harbrecht B, Menezes JM et al. Essential role of induced nitric oxide in the initiation of the inflammatory response after hemorrhagic shock. J Exp Med 1998 187 : 917 928.
56. Sass G, Koerber K, Bang R, Guehring H, Tiegs G. Inducible nitric oxide synthase is critical for immune-mediated liver injury in mice. J Clin Invest 2001 107 : 439 447.
57. Nathan C, Calingasan N, Nezezon J et al. Protection from Alzheimer's-like disease in the mouse by genetic ablation of inducible nitric oxide synthase. J Exp Med 2005 202 : 1163 1169.
58. Serandour AL, Loyer P, Garnier D et al. TNFalpha-mediated extracellular matrix remodeling is required for multiple division cycles in rat hepatocytes. Hepatology 2005 41 : 478 486.
59. Yang SQ, Lin HZ, Lane MD, Clemens M, Diehl AM. Obesity increases sensitivity to endotoxin liver injury: Implications for the pathogenesis of steatohepatitis. Proc Natl Acad Sci USA 1997 94 : 2557 2562.