Carbon monoxide enhances early liver regeneration in mice after hepatectomy

Hepatology

Volumn 53, Issue 6, 2011, Pages 2016-2026

  Kuramitsu, Kaori ^a   Gallo, David ^a   Yoon, Myunghee ^b   Chin, Beek Y ^a   Csizmadia, Eva ^a   Hanto, Douglas W ^a   Otterbein, Leo E ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Kosin University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON MONOXIDE; CYCLIN D1; CYCLIN E; HISTONE H3; PHOSPHO HISTONE 3; SCATTER FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; GENE EXPRESSION; HISTOPATHOLOGY; LIVER CELL; LIVER FUNCTION; LIVER REGENERATION; LIVER RESECTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BODY WEIGHT; CARBON MONOXIDE; CELL CYCLE; CELL PROLIFERATION; CYTOKINES; HEME OXYGENASE-1; HEPATECTOMY; HEPATOCYTE GROWTH FACTOR; KAPLAN-MEIER ESTIMATE; LIVER; LIVER REGENERATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, ANIMAL; SIGNAL TRANSDUCTION;

EID: 79957441392     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.24317     Document Type: Article

References (50)

1. Michalopoulos GK, deFrances MC. Liver regeneration. Science 1997; 276: 60-66.
2. Fausto N. Liver regeneration. J Hepatol 2000; 32: 19-31.
3. Michalopoulos GK. Liver regeneration. J Cell Physiol 2007; 213: 286-300.
4. Karp SJ. Clinical implications of advances in the basic science of liver repair and regeneration. Am J Transplant 2009; 9: 1973-1980.
5. Pomfret EA, Pomposelli JJ, Erbay N, Lyn Price L, Lewis WD, et al. Liver regeneration and surgical outcome in donors of right-lobe liver grafts. Transplantation 2003; 76: 5-10.
6. Child CG, Turcotte JC. Surgery and portal hypertension. In: Child CG, ed. The Liver and Portal Hypertension. Philadelphia, PA: Saunders; 1964; 50-51.
7. Pugh RN, Murray-Lyon IM, Pietroni MC, Williams R. Transection of the oesophagus for bleeding oesophageal varices. Br J Surg 1973; 60: 646-649.
8. Malinchoc M, Kamath PS, Peine CJ, Rank J, ter Borg PC. A model to predict poor survival in patients undergoing transjugular intrahepatic portosystemic shunts. HEPATOLOGY 2000; 31: 864-871.
9. Kamath PS, Wiesner RH, Malinchoc M, Kremers W, Therneau TM, Kosberg CL, et al. A model to predict survival in patients with end-stage liver disease. HEPATOLOGY 2001; 33: 464-470.
10. Shirabe K, Shimada M, Gion T, Hasegawa H, Takenaka K, Utunomiya T, et al. Postoperative liver failure after major hepatic resection for hepatocellular carcinoma in the modern era with special reference to remnant liver volume. J Am Coll Surg 1999; 188: 304-309.
11. Vauthey JN, Chaoui A, Do KA, Fenstermacher MJ, Charnsangavej C, et al. Standardized measurement of the future liver remnant prior to extended liver resection: methodology and clinical associations. Surgery 2000; 127: 512-519.
12. Fausto N, Riehle KJ. Mechanisms of liver regeneration and their clinical implications. J Hepatobiliary Pancreat Surg 2005; 12: 181-189.
13. Su AI, Guidotti LG, Chisari FV, Shultz PG. Gene expression during the priming phase of liver regeneration after partial hepatectomy in mice. Proc Natl Acad Sci U S A 2002; 99: 11181-11186.
14. Higgins GM, Anderson RM. Experimental pathology of the liver. Arch Pathol 1931; 12: 186-202.
15. Cataldegirmen G, Zeng S, Ippagunta N, Dun H, Qu W, et al. RAGE limits regeneration after massive liver injury by coordinated suppression of TNF-alpha and NF-kappaB. J Exp Med 2005; 201: 473-484.
16. Mazzola S, Forni M, Albertini M, Bacci ML, Zannoni A, Gentilini F, et al. Carbon monoxide pretreatment prevents respiratory derangement and ameliorates hyperacute endotoxic shock in pigs. FASEB J 2005; 14: 2045-2047.
17. Moore BA, Overhaus M, Whitcomb J, Ifedigbo E, Choi AM, Otterbein LE, et al. Brief inhalation of low-dose carbon monoxide protects rodents and swine from postoperative ileus. Crit Care Med 2005; 6: 1317-26.
18. Neto JS, Nakao A, Stolz DB, Uchiyama T, et al. Protection of transplant-induced renal ischemia-reperfusion injury with carbon monoxide. Am J Physiol 2004; 287: F979-F989.
19. Ameredes BT, Otterbein LE, Gligonic AL, Calhoun WJ, Choi AM. Low-dose carbon monoxide reduces airway hyperresponsiveness in mice. Am J Physiol 2003; 285: L1270-L1276.
20. Zuckerbraun BS, Otterbein LE, Boyle P, Jaffe R, Upperman J, Zamora R, et al. Carbon monoxide protects against the development of experimental necrotizing enterocolitis. Am J Physiol 2005; 289: G607-G613.
21. Nakao A, Neto JS, Kanno S, Stolz DB, Kimizuka K, Liu F, et al. Protection against ischemia/reperfusion injury in cardiac and renal transplantation with carbon monoxide, biliverdin and both. Am J Transplant 2005; 5: 282-291.
22. Mori M, Suematsu M, Kyokane T, Sano T, Yamaguchi C, Suzuki H, et al. Carbon monoxide-mediated alterations in paracellular permeability and vesicular transport in acetaminophen-treated perfused rat liver. HEPATOLOGY 1999; 30: 160-168.
23. Zuckerbraun BS, Billiar TR, Otterbein SL, Liu F, Choi AM, et al. Carbon monoxide protects against liver failure through nitric oxide-induced heme oxygenase 1. J Exp Med 2003; 198: 1707-1716.
24. Gerdes J, Lemke H, Baisch H, Wacker H-H, Schwab U, Stein H. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol 1984; 133: 1710-1715.
25. Goto H, Tomono Y, Ajiro K, Kosako H, Fujita M, Sakurai M, et al. Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J Biol Chem 1999; 274: 25543-25549.
26. Michalopoulos GK, DeFrances MC. Liver regeneration. Nature 1997; 276: 60-66.
27. Paku S, Schnur J, Nagy P, Thorgeirsson SS. Origin and structural evolution of the early proliferating oval cells in rat liver. Am J Pathol 2001; 158: 1313-1323.
28. Russell WE, Coffey RJ Jr, Ouellette AJ, Moses HL. Type beta transforming growth factor reversibly inhibits the early proliferative response to partial hepatectomy in the rat. Proc Natl Acad Sci U S A 1988; 85: 5126-5130.
29. Cressman DE, Greenbaum LE, DeAngelis RA, Ciliberto G, Furth EE, Poli V, et al. Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science 1996; 22: 1379-1383.
30. Kovalovich K, DeAngelis RA, Furth E, Ciliberto G, Taub R. Increased toxin-induced liver injury and fibrosis in interleukin-6 deficient mice. HEPATOLOGY 2000; 31: 149-159.
31. Haga S, Ozaki M, Inoue H, Okamoto Y, Ogawa W, Takeda K, et al. 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.
32. Son G, Hirano T, Seki E, Nukiwa T, Iimuro Y, Matsumoto K, et al. Blockage of HGF/c-Met system by gene therapy (adenovirus-mediated NK4 gene) suppresses hepatocellular carcinoma in mice. J Hepatol 2006; 45: 688-695.
33. Motterlini R, Otterbein LE. The therapeutic potential of carbon monoxide. Nat Rev 2010; 9: 728-743.
34. Tomiyama K, Ikeda A, Ueki S, Nakao A, Stolz DB, Koike Y, et al. Inhibition of Kupffer cell-mediated early proinflammatory response with carbon monoxide in transplant-induced hepatic ischemia/reperfusion injury in rats. HEPATOLOGY 2008; 48: 1608-1620.
35. Glanemann M, Schirmeier A, Langrehr JM, Neuhaus P, Nussler AK. Cobalt-protoporphyrin induced heme oxygenase overexpression and its impact on liver regeneration. Transplant Proc 2005; 37: 3223-3225.
36. Wei AC, Tung-Ping Poon R, Wong J. Risk factors for perioperative morbidity and mortality after extended hepatectomy for hepatocellular carcinoma. Br J Surg 2003; 90: 33-41.
37. Myronovych A, Murata S, Chiba M, Matsuo R, Ikeda O, Watanabe M, et al. Role of platelets on liver regeneration after 90% hepatectomy in mice. J Hepatol 2008; 49: 363-372.
38. Zhong Z, Schwab RF, Kai Y, He L, Yang L, Bunzendahl H, et al. Liver regeneration is suppressed in small-for size liver grafts after transplantation. Transplantation 2006; 82: 241-250.
39. Kubota T, Takabe K, Sekido H, Endo I, Ichikawa Y, et al. Minimum size for remnant and transplanted livers in rats. J Hepatolbiliary Pancreat Surg 1997; 4: 398-404.
40. Turner A, Moore BA, Overhaus M, Kalff JC, Bauer AJ. Colonic postoperative inflammatory ileus in the rat. Ann Surg 2002; 236: 56-66.
41. Kalff JC, Strait WH, Simmons RL, Bauer AJ. Role of inducible nitric oxide synthase in postoperative intestinal smooth muscle dysfunction in rodents. Gastroenterology 2000; 118: 316-327.
42. Schwarz NT, Kalff JC, Turler A, Engel BM, Watkins SC, Billiar TR, et al. Prostanoid production via COX-2 as a causative mechanism of rodent postoperative ileus. Gastroenterology 2001; 121: 1354-1371.
43. Moore BA, Otterbein LE, Choi AM, Bauer AJ. Inhaled carbon monoxide suppresses the development of postoperative ileus in the murine small intestine. Gastroenterology 2003; 124: 377-391.
44. Taub R. Liver regeneration: from myth to mechanism. Nat Rev 2004; 5: 836-847.
45. Rigotti P, Peters JC, Transberg KG, Fischer JE. Effects of amino acid infusions on liver regeneration after partial hepatectomy in the rat. JPEN J Parenter Enteral Nutr 1986; 10: 17-20.
46. Zimmers TA, McKillop IH, Pierce RH, Yoo JY, Koniaris LG. Massive liver growth in mice induced by systemic interleukin 6 administration. HEPATOLOGY 2003; 38: 326-334.
47. Atta HM, Al-Hendy A, Shaker OG, Hammam OA. Low-dose simultaneous delivery of adenovirus encoding hepatocyte growth factor and vascular endothelial growth factor in dogs enhances liver proliferation. Liver Int 2009; 29: 1022-1030.
48. Safety and tolerability study of inhaled carbon monoxide in kidney transplant patients. Available at Accessed March 2010.
49. Sulliman HB, Carraway MS, Reynolds CM, Welty-Wolf KE, Piantadosi CA. The CO/HO system reverses inhibition of mitochondrial biogenesis and prevents murine doxorubicin cardiomyopathy. J Clin Invest 2007; 117: 3720-2741.
50. Haschemi A, Wagner O, Marculescu R, Wegiel B, Robson SC, Gagliani N, et al. Inhalation of carbon monoxide and the adenosine A2a receptor in macrophages. 2007; 178: 5921-5929.