The NF-κB Subunit RelA/p65 Is Dispensable for Successful Liver Regeneration after Partial Hepatectomy in Mice

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Ringelhan, Marc ^a   Schmid, Roland M ^a   Geisler, Fabian ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE PROGRESSION; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; FEMALE; GEL MOBILITY SHIFT ASSAY; HISTOLOGY; IMMUNOBLOTTING; KNOCKOUT MOUSE; KUPFFER CELL; LIVER CELL; LIVER INJURY; LIVER REGENERATION; MALE; MOUSE; NONHUMAN; PARTIAL HEPATECTOMY; PROTEIN ISOLATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; CELL CYCLE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HEPATECTOMY; HEPATOCYTES; IMMUNOBLOTTING; KUPFFER CELLS; LIVER REGENERATION; MICE; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTOR RELA;

MUS;

EID: 84866995256     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046469     Document Type: Article

References (51)

1. Fausto N, Campbell JS, Riehle KJ, (2006) Liver regeneration. Hepatology 43: S45-53.
2. Taub R, (2004) Liver regeneration: from myth to mechanism. Nat Rev Mol Cell Biol 5: 836-847.
3. Michalopoulos GK, (2007) Liver regeneration. J Cell Physiol 213: 286-300.
4. Cressman DE, Greenbaum LE, Haber BA, Taub R, (1994) Rapid activation of post-hepatectomy factor/nuclear factor kappa B in hepatocytes, a primary response in the regenerating liver. J Biol Chem 269: 30429-30435.
5. Chen LF, Greene WC, (2004) Shaping the nuclear action of NF-kappaB. Nat Rev Mol Cell Biol 5: 392-401.
6. Hayden MS, Ghosh S, (2004) Signaling to NF-kappaB. Genes Dev 18: 2195-2224.
7. Iimuro Y, Nishiura T, Hellerbrand C, Behrns KE, Schoonhoven R, et al. (1998) NFkappaB prevents apoptosis and liver dysfunction during liver regeneration. J Clin Invest 101: 802-811.
8. Yang L, Magness ST, Bataller R, Rippe RA, Brenner DA, (2005) NF-kappaB activation in Kupffer cells after partial hepatectomy. Am J Physiol Gastrointest Liver Physiol 289: G530-538.
9. Chaisson ML, Brooling JT, Ladiges W, Tsai S, Fausto N, (2002) Hepatocyte-specific inhibition of NF-kappaB leads to apoptosis after TNF treatment, but not after partial hepatectomy. J Clin Invest 110: 193-202.
10. Maeda S, Chang L, Li ZW, Luo JL, Leffert H, et al. (2003) IKKbeta is required for prevention of apoptosis mediated by cell-bound but not by circulating TNFalpha. Immunity 19: 725-737.
11. Maeda S, Kamata H, Luo JL, Leffert H, Karin M, (2005) IKKbeta couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell 121: 977-990.
12. Malato Y, Sander LE, Liedtke C, Al-Masaoudi M, Tacke F, et al. (2008) Hepatocyte-specific inhibitor-of-kappaB-kinase deletion triggers the innate immune response and promotes earlier cell proliferation during liver regeneration. Hepatology 47: 2036-2050.
13. Koch KS, Maeda S, He G, Karin M, Leffert HL, (2009) Targeted deletion of hepatocyte Ikkbeta confers growth advantages. Biochem Biophys Res Commun 380: 349-354.
14. Luedde T, Assmus U, Wustefeld T, Meyer zu Vilsendorf A, Roskams T, et al. (2005) Deletion of IKK2 in hepatocytes does not sensitize these cells to TNF-induced apoptosis but protects from ischemia/reperfusion injury. J Clin Invest 115: 849-859.
15. Geisler F, Algul H, Paxian S, Schmid RM, (2007) Genetic inactivation of RelA/p65 sensitizes adult mouse hepatocytes to TNF-induced apoptosis in vivo and in vitro. Gastroenterology 132: 2489-2503.
16. Algul H, Treiber M, Lesina M, Nakhai H, Saur D, et al. (2007) Pancreas-specific RelA/p65 truncation increases susceptibility of acini to inflammation-associated cell death following cerulein pancreatitis. J Clin Invest 117: 1490-1501.
17. Postic C, Magnuson MA, (2000) DNA excision in liver by an albumin-Cre transgene occurs progressively with age. Genesis 26: 149-150.
18. Kuhn R, Schwenk F, Aguet M, Rajewsky K, (1995) Inducible gene targeting in mice. Science 269: 1427-1429.
19. Geisler F, Nagl F, Mazur PK, Lee M, Zimber-Strobl U, et al. (2008) Liver-specific inactivation of Notch2, but not Notch1, compromises intrahepatic bile duct development in mice. Hepatology 48: 607-616.
20. Weisend CM, Kundert JA, Suvorova ES, Prigge JR, Schmidt EE, (2009) Cre activity in fetal albCre mouse hepatocytes: Utility for developmental studies. Genesis 47: 789-792.
21. Yamada Y, Kirillova I, Peschon JJ, Fausto N, (1997) Initiation of liver growth by tumor necrosis factor: deficient liver regeneration in mice lacking type I tumor necrosis factor receptor. Proc Natl Acad Sci U S A 94: 1441-1446.
22. Liu H, Lo CR, Czaja MJ, (2002) NF-kappaB inhibition sensitizes hepatocytes to TNF-induced apoptosis through a sustained activation of JNK and c-Jun. Hepatology 35: 772-778.
23. Schwabe RF, Bradham CA, Uehara T, Hatano E, Bennett BL, et al. (2003) c-Jun-N-terminal kinase drives cyclin D1 expression and proliferation during liver regeneration. Hepatology 37: 824-832.
24. He G, Yu GY, Temkin V, Ogata H, Kuntzen C, et al. (2010) Hepatocyte IKKbeta/NF-kappaB inhibits tumor promotion and progression by preventing oxidative stress-driven STAT3 activation. Cancer Cell 17: 286-297.
25. Cataldegirmen G, Zeng S, Feirt N, Ippagunta N, Dun H, et al. (2005) RAGE limits regeneration after massive liver injury by coordinated suppression of TNF-alpha and NF-kappaB. J Exp Med 201: 473-484.
26. Trautwein C, Rakemann T, Niehof M, Rose-John S, Manns MP, (1996) Acute-phase response factor, increased binding, and target gene transcription during liver regeneration. Gastroenterology 110: 1854-1862.
27. Cressman DE, Greenbaum LE, DeAngelis RA, Ciliberto G, Furth EE, et al. (1996) Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science 274: 1379-1383.
28. Fausto N, (2000) Liver regeneration. J Hepatol 32: 19-31.
29. Chakraborty JB, Mann DA, (2010) NF-kappaB signalling: embracing complexity to achieve translation. J Hepatol 52: 285-291.
30. Pasparakis M, (2009) Regulation of tissue homeostasis by NF-kappaB signalling: implications for inflammatory diseases. Nat Rev Immunol 9: 778-788.
31. Malato Y, Beraza N, Gassler N, Al-Masaoudi M, Liedtke C, et al. (2009) Activation of Progenitor Cells Triggers the Repopulation of Conditional Nemo Ko Livers during Liver Regeneration in Mice. Journal of Hepatology 50: S310-S310.
32. Beraza N, Ludde T, Assmus U, Roskams T, Vander Borght S, et al. (2007) Hepatocyte-specific IKK gamma/NEMO expression determines the degree of liver injury. Gastroenterology 132: 2504-2517.
33. Bettermann K, Vucur M, Haybaeck J, Koppe C, Janssen J,et al. TAK1 suppresses a NEMO-dependent but NF-kappaB-independent pathway to liver cancer. Cancer Cell 17: 481-496.
34. Greten FR, Arkan MC, Bollrath J, Hsu LC, Goode J, et al. (2007) NF-kappaB is a negative regulator of IL-1beta secretion as revealed by genetic and pharmacological inhibition of IKKbeta. Cell 130: 918-931.
35. Fujita J, Marino MW, Wada H, Jungbluth AA, Mackrell PJ, et al. (2001) Effect of TNF gene depletion on liver regeneration after partial hepatectomy in mice. Surgery 129: 48-54.
36. Hayashi H, Nagaki M, Imose M, Osawa Y, Kimura K, et al. (2005) Normal liver regeneration and liver cell apoptosis after partial hepatectomy in tumor necrosis factor-alpha-deficient mice. Liver Int 25: 162-170.
37. Sakamoto T, Liu Z, Murase N, Ezure T, Yokomuro S, et al. (1999) Mitosis and apoptosis in the liver of interleukin-6-deficient mice after partial hepatectomy. Hepatology 29: 403-411.
38. Wuestefeld T, Klein C, Streetz KL, Betz U, Lauber J, et al. (2003) Interleukin-6/glycoprotein 130-dependent pathways are protective during liver regeneration. J Biol Chem 278: 11281-11288.
39. Seki E, Tsutsui H, Iimuro Y, Naka T, Son G, et al. (2005) Contribution of Toll-like receptor/myeloid differentiation factor 88 signaling to murine liver regeneration. Hepatology 41: 443-450.
40. Campbell JS, Riehle KJ, Brooling JT, Bauer RL, Mitchell C, et al. (2006) Proinflammatory cytokine production in liver regeneration is Myd88-dependent, but independent of Cd14, Tlr2, and Tlr4. J Immunol 176: 2522-2528.
41. Vaquero J, Campbell JS, Haque J, McMahan RS, Riehle KJ, et al. (2011) Toll-like receptor 4 and myeloid differentiation factor 88 provide mechanistic insights into the cause and effects of interleukin-6 activation in mouse liver regeneration. Hepatology 54: 597-608.
42. Higgins GM, Anderson RM, (1931) Experimental pathology of the liver I. Restoration of the liver of the white rat following partial surgical removal. Arch Pathol 12: 186-202.
43. Yokoyama HO, Wilson ME, Tsuboi KK, Stowell RE, (1953) Regeneration of mouse liver after partial hepatectomy. Cancer Res 13: 80-85.
44. Doerr RJ, Castillo MH, Luchette FA, Caruna J, (1990) Partial Hepatectomy in the Mouse. Clinical Anatomy 3: 279-286.
45. Paulsen JE, (1990) Variations in regenerative growth of mouse liver following partial hepatectomy. In Vivo 4: 235-238.
46. Greene AK, Puder M, (2003) Partial hepatectomy in the mouse: technique and perioperative management. J Invest Surg 16: 99-102.
47. Mitchell C, Willenbring H, (2008) A reproducible and well-tolerated method for 2/3 partial hepatectomy in mice. Nat Protoc 3: 1167-1170.
48. Boyce S, Harrison D, (2008) A detailed methodology of partial hepatectomy in the mouse. Lab Anim (NY) 37: 529-532.
49. Blindenbacher A, Wang X, Langer I, Savino R, Terracciano L, et al. (2003) Interleukin 6 is important for survival after partial hepatectomy in mice. Hepatology 38: 674-682.
50. Huh CG, Factor VM, Sanchez A, Uchida K, Conner EA, et al. (2004) Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc Natl Acad Sci U S A 101: 4477-4482.
51. Factor VM, Seo D, Ishikawa T, Kaposi-Novak P, Marquardt JU, et al. (2010) Loss of c-Met disrupts gene expression program required for G2/M progression during liver regeneration in mice. PLoS One 5: e12739.