Oxidative stress and extracellular matrices after hepatectomy and liver transplantation in rats

World Journal of Hepatology

Volumn 6, Issue 2, 2014, Pages 72-84

  Hori, Tomohide ^a   Uemoto, Shinji ^a   Chen, Feng ^b   Gardner, Lindsay B ^b   Baine, Ann Marie T ^b   Hata, Toshiyuki ^b   Kogure, Takayuki ^c   Nguyen, Justin H ^d  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b MAYO GRADUATE SCHOOL   (United States)

^c TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d MAYO CLINIC   (United States)

Author keywords

Akt; Free radicals; Matrix metalloproteinase; Phosphatidylinositol 3 kinase; Tissue inhibitors of metalloproteinase

Indexed keywords

EID: 84894427691     PISSN: None     EISSN: 19485182     Source Type: Journal    
DOI: 10.4254/wjh.v6.i2.72     Document Type: Article

References (56)

1. Bachellier P, Rosso E, Pessaux P, Oussoultzoglou E, Nobili C, Panaro F, Jaeck D. Risk factors for liver failure and mortality after hepatectomy associated with portal vein resection. Ann Surg 2011; 253: 173-179 [PMID: 21233614 DOI: 10.1097/SLA.0b013e3181f193ba]
2. Fan ST, Mau Lo C, Poon RT, Yeung C, Leung Liu C, Yuen WK, Ming Lam C, Ng KK, Ching Chan S. Continuous improvement of survival outcomes of resection of hepatocellular carcinoma: a 20-year experience. Ann Surg 2011; 253: 745-758 [PMID: 21475015 DOI: 10.1097/SLA.0b013e3182111195]
3. Lemasters J, Bunzendahl H, Thurman R. Preservation of the liver. In: Maddrey W, Sorrell M. Transplantation of the liver. 7th ed. East Norwalk: Appleton & Lange, 1995: 297-321
4. Hori T, Uemoto S, Gardner LB, Sibulesky L, Ogura Y, Nguyen JH. Left-sided grafts for living-donor liver transplantation and split grafts for deceased-donor liver transplantation: their impact on long-term survival. Clin Res Hepatol Gastroenterol 2012; 36: 47-52 [PMID: 21955515 DOI: 10.1016/j.clinre.2011.08.008]
5. Busuttil RW, Goss JA. Split liver transplantation. Ann Surg 1999; 229: 313-321 [PMID: 10077042]
6. Wang F, Pan KT, Chu SY, Chan KM, Chou HS, Wu TJ, Lee WC. Preoperative estimation of the liver graft weight in adult right lobe living donor liver transplantation using maximal portal vein diameters. Liver Transpl 2011; 17: 373-380 [PMID: 21445920 DOI: 10.1002/lt.22274]
7. Ogura Y, Hori T, El Moghazy WM, Yoshizawa A, Oike F, Mori A, Kaido T, Takada Y, Uemoto S. Portal pressure & lt; 15 mm Hg is a key for successful adult living donor liver transplantation utilizing smaller grafts than before. Liver Transpl 2010; 16: 718-728 [PMID: 20517905 DOI: 10.1002/lt.22059]
8. Hori T, Ogura Y, Ogawa K, Kaido T, Segawa H, Okajima H, Kogure T, Uemoto S. How transplant surgeons can overcome the inevitable insufficiency of allograft size during adult living-donor liver transplantation: strategy for donor safety with a smaller-size graft and excellent recipient results. Clin Transplant 2012; 26: E324-E334 [PMID: 22686957 DOI: 10.1111/j.1399-0012.2012.01664.x]
9. Acuña Castroviejo D, López LC, Escames G, López A, García JA, Reiter RJ. Melatonin-mitochondria interplay in health and disease. Curr Top Med Chem 2011; 11: 221-240 [PMID: 21244359]
10. Ghosh N, Ghosh R, Mandal SC. Antioxidant protection: A promising therapeutic intervention in neurodegenerative disease. Free Radic Res 2011; 45: 888-905 [PMID: 21615270 DOI: 10.3109/10715762.2011.574290]
11. Turan B. Role of antioxidants in redox regulation of diabetic cardiovascular complications. Curr Pharm Biotechnol 2010; 11: 819-836 [PMID: 20874678]
12. Defamie V, Laurens M, Patrono D, Devel L, Brault A, Saint-Paul MC, Yiotakis A, Barbry P, Gugenheim J, Crenesse D, Dive V, Huet PM, Mari B. Matrix metalloproteinase inhibition protects rat livers from prolonged cold ischemia-warm reperfusion injury. Hepatology 2008; 47: 177-185 [PMID: 18008367]
13. Ma ZY, Qian JM, Rui XH, Wang FR, Wang QW, Cui YY, Peng ZH. Inhibition of matrix metalloproteinase-9 attenuates acute small-for-size liver graft injury in rats. Am J Transplant 2010; 10: 784-795 [PMID: 20121733 DOI: 10.1111/j.1600-6143.2009.02993.x]
14. Hua H, Li M, Luo T, Yin Y, Jiang Y. Matrix metalloproteinases in tumorigenesis: an evolving paradigm. Cell Mol Life Sci 2011; 68: 3853-3868 [PMID: 21744247 DOI: 10.1007/s00018-011-0763-x]
15. Overall CM, López-Otín C. Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat Rev Cancer 2002; 2: 657-672 [PMID: 12209155]
16. Alwayn IP, Verbesey JE, Kim S, Roy R, Arsenault DA, Greene AK, Novak K, Laforme A, Lee S, Moses MA, Puder M. A critical role for matrix metalloproteinases in liver regeneration. J Surg Res 2008; 145: 192-198 [PMID: 18222481 DOI: 10.1016/j.jss.2007.04.002]
17. Olle EW, Ren X, McClintock SD, Warner RL, Deogracias MP, Johnson KJ, Colletti LM. Matrix metalloproteinase-9 is an important factor in hepatic regeneration after partial hepatectomy in mice. Hepatology 2006; 44: 540-549 [PMID: 16941692]
18. Padrissa-Altés S, Zaouali MA, Franco-Gou R, Bartrons R, Boillot O, Rimola A, Arroyo V, Rodés J, Peralta C, Roselló-Catafau J. Matrix metalloproteinase 2 in reduced-size liver transplantation: beyond the matrix. Am J Transplant 2010; 10: 1167-1177 [PMID: 20353474 DOI: 10.1111/j.1600-6143.2010.03092.x]
19. Kim TH, Mars WM, Stolz DB, Michalopoulos GK. Expression and activation of pro-MMP-2 and pro-MMP-9 during rat liver regeneration. Hepatology 2000; 31: 75-82 [PMID: 10613731]
20. Hori T, Uemoto S, Hata T, Gardner LB, Chen F, Baine AM, Nguyen JH. Matrix metalloproteinase-9 after the cold ischemia/reperfusion injury and/or shear stress with portal hypertension: an overview. Surg Today 2014; 44: 201-203 [PMID: 23525637]
21. Ten Hove WR, Korkmaz KS, op den Dries S, de Rooij BJ, van Hoek B, Porte RJ, van der Reijden JJ, Coenraad MJ, Dubbeld J, Hommes DW, Verspaget HW. Matrix metalloproteinase 2 genotype is associated with nonanastomotic biliary strictures after orthotopic liver transplantation. Liver Int 2011; 31: 1110-1117 [PMID: 21745270 DOI: 10.1111/j.1478-3231.2011.02459.x]
22. Chirco R, Liu XW, Jung KK, Kim HR. Novel functions of TIMPs in cell signaling. Cancer Metastasis Rev 2006; 25: 99-113 [PMID: 16680576]
23. Yamamoto S, Nguyen JH. TIMP-1/MMP-9 imbalance in brain edema in rats with fulminant hepatic failure. J Surg Res 2006; 134: 307-314 [PMID: 16488444]
24. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2002; 2: 161-174 [PMID: 11990853]
25. Ikebuchi Y, Ishida C, Okamoto K, Murawaki Y. Association of TIMP-1 and TIMP-2 gene polymorphisms with progression of liver fibrosis in patients with type C chronic liver disease. Biochem Genet 2013; 51: 564-574 [PMID: 23563628 DOI: 10.1007/s10528-013-9587-8]
26. Rath T, Menendez KM, Kügler M, Hage L, Wenzel C, Schulz R, Graf J, Nährlich L, Roeb E, Roderfeld M. TIMP-1/-2 and transient elastography allow non invasive diagnosis of cystic fibrosis associated liver disease. Dig Liver Dis 2012; 44: 780-787 [PMID: 22652148 DOI: 10.1016/j.dld.2012.04.008]
27. Kuyvenhoven JP, Molenaar IQ, Verspaget HW, Veldman MG, Palareti G, Legnani C, Moolenburgh SE, Terpstra OT, Lamers CB, van Hoek B, Porte RJ. Plasma MMP-2 and MMP-9 and their inhibitors TIMP-1 and TIMP-2 during human orthotopic liver transplantation. The effect of aprotinin and the relation to ischemia/reperfusion injury. Thromb Haemost 2004; 91: 506-513 [PMID: 14983226]
28. Mohammed FF, Pennington CJ, Kassiri Z, Rubin JS, Soloway PD, Ruther U, Edwards DR, Khokha R. Metalloproteinase inhibitor TIMP-1 affects hepatocyte cell cycle via HGF activation in murine liver regeneration. Hepatology 2005; 41: 857-867 [PMID: 15726641]
29. He S, Atkinson C, Qiao F, Cianflone K, Chen X, Tomlinson S. A complement-dependent balance between hepatic ischemia/reperfusion injury and liver regeneration in mice. J Clin Invest 2009; 119: 2304-2316 [PMID: 19620784 DOI: 10.1172/JCI38289]
30. Jin X, Zhang Z, Beer-Stolz D, Zimmers TA, Koniaris LG. Interleukin-6 inhibits oxidative injury and necrosis after extreme liver resection. Hepatology 2007; 46: 802-812 [PMID: 17668886]
31. Panis Y, McMullan DM, Emond JC. Progressive necrosis after hepatectomy and the pathophysiology of liver failure after massive resection. Surgery 1997; 121: 142-149 [PMID: 9037225]
32. Hori T, Ohashi N, Chen F, Baine AM, Gardner LB, Hata T, Uemoto S, Nguyen JH. Simple and reproducible hepatectomy in the mouse using the clip technique. World J Gastroenterol 2012; 18: 2767-2774 [PMID: 22719184 DOI: 10.3748/wjg.v18.i22.2767]
33. Hori T, Nguyen JH, Zhao X, Ogura Y, Hata T, Yagi S, Chen F, Baine AM, Ohashi N, Eckman CB, Herdt AR, Egawa H, Takada Y, Oike F, Sakamoto S, Kasahara M, Ogawa K, Hata K, Iida T, Yonekawa Y, Sibulesky L, Kuribayashi K, Kato T, Saito K, Wang L, Torii M, Sahara N, Kamo N, Sahara T, Yasutomi M, Uemoto S. Comprehensive and innovative techniques for liver transplantation in rats: a surgical guide. World J Gastroenterol 2010; 16: 3120-3132 [PMID: 20593497]
34. Hori T, Uemoto S, Zhao X, Chen F, Baine AMT, Gardner LB, Ohashi N, Conkle F, Castanedes-Casey M, Phillips VR, Rousseau LG, Murray ME, Kamo N, Nguyen JH. Surgical guide including innovative techniques for orthotopic liver transplantation in the rat: Key techniques and pitfalls in whole and split liver grafts. Ann Gastroentol 2010; 23: 270-295
35. Awasthi YC, Sharma R, Sharma A, Yadav S, Singhal SS, Chaudhary P, Awasthi S. Self-regulatory role of 4-hydroxynonenal in signaling for stress-induced programmed cell death. Free Radic Biol Med 2008; 45: 111-118 [PMID: 18456001 DOI: 10.1016/j.freeradbiomed.2008.04.007]
36. Voulgaridou GP, Anestopoulos I, Franco R, Panayiotidis MI, Pappa A. DNA damage induced by endogenous aldehydes: current state of knowledge. Mutat Res 2011; 711: 13-27 [PMID: 21419140 DOI: 10.1016/j.mrfmmm.2011.03.006]
37. Irarrazabal CE, Liu JC, Burg MB, Ferraris JD. ATM, a DNA damage-inducible kinase, contributes to activation by high NaCl of the transcription factor TonEBP/OREBP. Proc Natl Acad Sci USA 2004; 101: 8809-8814 [PMID: 15173573]
38. Andäng M, Hjerling-Leffler J, Moliner A, Lundgren TK, Castelo-Branco G, Nanou E, Pozas E, Bryja V, Halliez S, Nishimaru H, Wilbertz J, Arenas E, Koltzenburg M, Charnay P, El Manira A, Ibañez CF, Ernfors P. Histone H2AX-dependent GABA(A) receptor regulation of stem cell proliferation. Nature 2008; 451: 460-464 [PMID: 18185516 DOI: 10.1038/nature06488]
39. Yuan J, Adamski R, Chen J. Focus on histone variant H2AX: to be or not to be. FEBS Lett 2010; 584: 3717-3724 [PMID: 20493860 DOI: 10.1016/j.febslet.2010.05.021]
40. Fernando RN, Eleuteri B, Abdelhady S, Nussenzweig A, Andäng M, Ernfors P. Cell cycle restriction by histone H2AX limits proliferation of adult neural stem cells. Proc Natl Acad Sci USA 2011; 108: 5837-5842 [PMID: 21436033 DOI: 10.1073/pnas.1014993108]
41. Fernando RN, Eleuteri B, Abdelhady S, Nussenzweig A, Andäng M, Ernfors P. Cell cycle restriction by histone H2AX limits proliferation of adult neural stem cells. Proc Natl Acad Sci USA 2011; 108: 5837-5842 [PMID: 21436033 DOI: 10.1073/pnas.1014993108]
42. Burgering BM, Coffer PJ. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 1995; 376: 599-602 [PMID: 7637810]
43. Franke TF, Yang SI, Chan TO, Datta K, Kazlauskas A, Morrison DK, Kaplan DR, Tsichlis PN. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 1995; 81: 727-736 [PMID: 7774014]
44. Haga S, Ozaki M, Inoue H, Okamoto Y, Ogawa W, Takeda K, Akira S, Todo S. The survival pathways phosphatidylinositol-3 kinase (PI3-K)/phosphoinositide-dependent protein kinase 1 (PDK1)/Akt modulate liver regeneration through hepatocyte size rather than proliferation. Hepatology 2009; 49: 204-214 [PMID: 19065678 DOI: 10.1002/hep.22583]
45. Khalil A, Morgan RN, Adams BR, Golding SE, Dever SM, Rosenberg E, Povirk LF, Valerie K. ATM-dependent ERK signaling via AKT in response to DNA double-strand breaks. Cell Cycle 2011; 10: 481-491 [PMID: 21263216]
46. Maulik N, Das DK. Emerging potential of thioredoxin and thioredoxin interacting proteins in various disease conditions. Biochim Biophys Acta 2008; 1780: 1368-1382 [PMID: 18206121 DOI: 10.1016/j.bbagen.2007.12.008]
47. Nguyen JH, Yamamoto S, Steers J, Sevlever D, Lin W, Shimojima N, Castanedes-Casey M, Genco P, Golde T, Richelson E, Dickson D, McKinney M, Eckman CB. Matrix metalloproteinase-9 contributes to brain extravasation and edema in fulminant hepatic failure mice. J Hepatol 2006; 44: 1105-1114 [PMID: 16458990]
48. Ohashi N, Hori T, Chen F, Jermanus S, Eckman CB, Nakao A, Uemoto S, Nguyen JH. Matrix metalloproteinase-9 contributes to parenchymal hemorrhage and necrosis in the remnant liver after extended hepatectomy in mice. World J Gastroenterol 2012; 18: 2320-2333 [PMID: 22654423 DOI: 10.3748/wjg.v18.i19.2320]
49. Chen F, Radisky ES, Das P, Batra J, Hata T, Hori T, Baine AM, Gardner L, Yue MY, Bu G, del Zoppo G, Patel TC, Nguyen JH. TIMP-1 attenuates blood-brain barrier permeability in mice with acute liver failure. J Cereb Blood Flow Metab 2013; 33: 1041-1049 [PMID: 23532086 DOI: 10.1038/jcbfm.2013.45]
50. Nguyen JH. Blood-brain barrier in acute liver failure. Neurochem Int 2012; 60: 676-683 [PMID: 22100566 DOI: 10.1016/j.neuint.2011.10.012]
51. Chen F, Hori T, Ohashi N, Baine AM, Eckman CB, Nguyen JH. Occludin is regulated by epidermal growth factor receptor activation in brain endothelial cells and brains of mice with acute liver failure. Hepatology 2011; 53: 1294-1305 [PMID: 21480332 DOI: 10.1002/hep.24161]
52. Nguyen JH. Subtle BBB alterations in brain edema associated with acute liver failure. Neurochem Int 2010; 56: 203-204; author reply 205-207 [PMID: 20201130]
53. Hori T, Gardner LB, Chen F, Baine AM, Hata T, Uemoto S, Nguyen JH. Liver graft pretreated in vivo or ex vivo by ?-aminobutyric acid receptor regulation. J Surg Res 2013; 182: 166-175 [PMID: 23010512 DOI: 10.1016/j.jss.2012.08.055]
54. Hori T, Gardner LB, Hata T, Chen F, Baine AM, Uemoto S, Nguyen JH. Pretreatment of liver grafts in vivo by ?-aminobutyric acid receptor regulation reduces cold ischemia/warm reperfusion injury in rat. Ann Transplant 2013; 18: 299-313 [PMID: 23792534 DOI: 10.12659/AOT.883955]
55. Ohashi N, Hori T, Chen F, Jermanus S, Nakao A, Uemoto S, Nguyen JH. Matrix metalloproteinase-9 in the initial injury after hepatectomy in mice. World J Gastroenterol 2013; 19: 3027-3042 [PMID: 23716982 DOI: 10.3748/wjg.v19.i20.3027]
56. Gardner LB, Hori T, Chen F, Baine AM, Hata T, Uemoto S, Nguyen JH. Effect of specific activation of γ-aminobutyric acid receptor in vivo on oxidative stress-induced damage after extended hepatectomy. Hepatol Res 2012; 42: 1131-1140 [PMID: 22583816 DOI: 10.1111/j.1872-034X.2012.01030.x]