Acta Med. 2016, 59: 35-42

https://doi.org/10.14712/18059694.2016.87

Does Simple Steatosis Affect Liver Regeneration after Partial Hepatectomy in Rats?

Tomáš Garnol, Otto Kučera, Pavla Staňková, Halka Lotková, Zuzana Červinková

Department of Physiology, Charles University in Prague, Faculty of Medicine in Hradec Králové, Hradec Králové, Czech Republic

Received May 23, 2016
Accepted June 6, 2016

References

1. Bucher NL, Swaffield MN. The rate of incorporation of labelled thymidine into the deoxyribonucleic acid of regenerating rat liver in relation to the amount of liver excised. Cancer Res 1964; 24: 1611–25.
2. Michalopoulos GK, DeFrances MC. Liver regeneration. Science 1997; 276: 60–6. <https://doi.org/10.1126/science.276.5309.60>
3. Higgins G, Anderson R. Experimental pathology of the liver. I. Restoration of the liver of the white rat following partial surgical removal. Archives of pathology (Chic) 1931; 12: 186–202.
4. Fausto N. Liver regeneration. J Hepatol 2000; 32: 19–31. <https://doi.org/10.1016/S0168-8278(00)80412-2>
5. Fausto N, Campbell JS, Riehle KJ. Liver regeneration. Hepatology 2006; 43: S45–53. <https://doi.org/10.1002/hep.20969>
6. Mangnall D, Bird NC, Majeed AW. The molecular physiology of liver regeneration following partial hepatectomy. Liver Int 2003; 23: 124–38. <https://doi.org/10.1034/j.1600-0676.2003.00812.x>
7. Rychtrmoc D, Hubalkova L, Viskova A, Libra A, Buncek M, Cervinkova Z. Transcriptome temporal and functional analysis of liver regeneration termination. Physiol Res 2012; 61 Suppl 2: S77–92.
8. Trevisani F, Colantoni A, Caraceni P, Van Thiel DH. The use of donor fatty liver for liver transplantation: a challenge or a quagmire? J Hepatol 1996; 24: 114–21. <https://doi.org/10.1016/S0168-8278(96)80195-4>
9. Behrns KE, Tsiotos GG, DeSouza NF, Krishna MK, Ludwig J, Nagorney DM. Hepatic steatosis as a potential risk factor for major hepatic resection. J Gastrointest Surg 1998; 2: 292–8. <https://doi.org/10.1016/S1091-255X(98)80025-5>
10. Erickson SK. Nonalcoholic fatty liver disease. J Lipid Res 2009; 50 Suppl: S412–6. <https://doi.org/10.1194/jlr.R800089-JLR200> <PubMed>
11. Chalasani N, Younossi Z, Lavine JE, et al. The diagnosis and management of non-alcoholic fatty liver disease: Practice guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Am J Gastroenterol 2012; 107: 811–26. <https://doi.org/10.1038/ajg.2012.128>
12. Vendemiale G, Grattagliano I, Caraceni P, et al. Mitochondrial oxidative injury and energy metabolism alteration in rat fatty liver: effect of the nutritional status. Hepatology 2001; 33: 808–15. <https://doi.org/10.1053/jhep.2001.23060>
13. Mantena SK, Vaughn DP, Andringa KK, et al. High fat diet induces dysregulation of hepatic oxygen gradients and mitochondrial function in vivo. Biochem J 2009; 417: 183–93. <https://doi.org/10.1042/BJ20080868> <PubMed>
14. Kucera O, Garnol T, Lotkova H, et al. The effect of rat strain, diet composition and feeding period on the development of a nutritional model of non-alcoholic fatty liver disease in rats. Physiol Res 2011; 60: 317–28.
15. Paradies G, Paradies V, Ruggiero FM, Petrosillo G. Oxidative stress, cardiolipin and mitochondrial dysfunction in nonalcoholic fatty liver disease. World J Gastroenterol 2014; 20: 14205–18. <https://doi.org/10.3748/wjg.v20.i39.14205> <PubMed>
16. Sanyal AJ, Campbell-Sargent C, Mirshahi F, et al. Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities. Gastroenterology 2001; 120: 1183–92. <https://doi.org/10.1053/gast.2001.23256>
17. Kawahara H, Fukura M, Tsuchishima M, Takase S. Mutation of mitochondrial DNA in livers from patients with alcoholic hepatitis and nonalcoholic steatohepatitis. Alcohol Clin Exp Res 2007; 31: S54–60. <https://doi.org/10.1111/j.1530-0277.2006.00287.x>
18. Gao D, Wei C, Chen L, Huang J, Yang S, Diehl AM. Oxidative DNA damage and DNA repair enzyme expression are inversely related in murine models of fatty liver disease. Am J Physiol Gastrointest Liver Physiol 2004; 287: G1070–7. <https://doi.org/10.1152/ajpgi.00228.2004>
19. Perez-Carreras M, Del Hoyo P, Martin MA, et al. Defective hepatic mitochondrial respiratory chain in patients with nonalcoholic steatohepatitis. Hepatology 2003; 38: 999–1007. <https://doi.org/10.1002/hep.1840380426>
20. Garcia-Ruiz I, Rodriguez-Juan C, Diaz-Sanjuan T, et al. Uric acid and anti-TNF antibody improve mitochondrial dysfunction in ob/ob mice. Hepatology 2006; 44: 581–91. <https://doi.org/10.1002/hep.21313>
21. Vetelainen R, Bennink RJ, van Vliet AK, van Gulik TM. Mild steatosis impairs functional recovery after liver resection in an experimental model. Br J Surg 2007; 94: 1002–8. <https://doi.org/10.1002/bjs.5672>
22. Selzner M, Clavien PA. Failure of regeneration of the steatotic rat liver: disruption at two different levels in the regeneration pathway. Hepatology 2000; 31: 35–42. <https://doi.org/10.1002/hep.510310108>
23. Kele PG, van der Jagt EJ, Gouw AS, Lisman T, Porte RJ, de Boer MT. The impact of hepatic steatosis on liver regeneration after partial hepatectomy. Liver Int 2013; 33: 469–75. <https://doi.org/10.1111/liv.12089>
24. de Meijer VE, Kalish BT, Puder M, Ijzermans JN. Systematic review and meta-analysis of steatosis as a risk factor in major hepatic resection. Br J Surg 2010; 97: 1331–9. <https://doi.org/10.1002/bjs.7194>
25. Picard C, Lambotte L, Starkel P, et al. Steatosis is not sufficient to cause an impaired regenerative response after partial hepatectomy in rats. J Hepatol 2002; 36: 645–52. <https://doi.org/10.1016/S0168-8278(02)00038-7>
26. Sydor S, Gu Y, Schlattjan M, et al. Steatosis does not impair liver regeneration after partial hepatectomy. Lab Invest 2013; 93: 20–30. <https://doi.org/10.1038/labinvest.2012.142>
27. Cho JY, Suh KS, Kwon CH, Yi NJ, Lee KU. Mild hepatic steatosis is not a major risk factor for hepatectomy and regenerative power is not impaired. Surgery 2006; 139: 508–15. <https://doi.org/10.1016/j.surg.2005.09.007>
28. Lieber CS, Leo MA, Mak KM, et al. Model of nonalcoholic steatohepatitis. Am J Clin Nutr 2004; 79: 502–9. <https://doi.org/10.1093/ajcn/79.3.502>
29. Drahota Z, Palenickova E, Endlicher R, et al. Biguanides inhibit complex I, II and IV of rat liver mitochondria and modify their functional properties. Physiol Res 2014; 63: 1–11.
30. Cervinkova Z, Kucera O, Lotkova H, Drahota Z, Houstek J. [Oxygraphic evaluation of energy metabolism in isolated hepatocytes]. Acta Medica (Hradec Kralove) Suppl 2002; 45: 65–76.
31. Hissin PJ, Hilf R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Analytical biochemistry 1976; 74: 214–26. <https://doi.org/10.1016/0003-2697(76)90326-2>
32. Rousar T, Kucera O, Lotkova H, Cervinkova Z. Assessment of reduced glutathione: comparison of an optimized fluorometric assay with enzymatic recycling method. Anal Biochem 2012; 423: 236–40. <https://doi.org/10.1016/j.ab.2012.01.030>
33. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959; 37: 911–7. <https://doi.org/10.1139/o59-099>
34. Burton K. A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J 1956; 62: 315–23. <https://doi.org/10.1042/bj0620315> <PubMed>
35. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248–54. <https://doi.org/10.1016/0003-2697(76)90527-3>
36. Pilz J, Meineke I, Gleiter CH. Measurement of free and bound malondialdehyde in plasma by high-performance liquid chromatography as the 2,4-dinitrophenylhydrazine derivative. J Chromatogr B Biomed Sci Appl 2000; 742: 315–25. <https://doi.org/10.1016/S0378-4347(00)00174-2>
37. Bader A, Pavlica S, Deiwick A, et al. Proteomic analysis to display the effect of low doses of erythropoietin on rat liver regeneration. Life Sci 2011; 89: 827–33. <https://doi.org/10.1016/j.lfs.2011.08.002>
38. Bellentani S, Scaglioni F, Marino M, Bedogni G. Epidemiology of non-alcoholic fatty liver disease. Dig Dis 2010; 28: 155–61. <https://doi.org/10.1159/000282080>
39. McCormack L, Petrowsky H, Jochum W, Furrer K, Clavien PA. Hepatic steatosis is a risk factor for postoperative complications after major hepatectomy: a matched case-control study. Ann Surg 2007; 245: 923–30. <https://doi.org/10.1097/01.sla.0000251747.80025.b7> <PubMed>
40. Vetelainen R, van Vliet AK, van Gulik TM. Severe steatosis increases hepatocellular injury and impairs liver regeneration in a rat model of partial hepatectomy. Ann Surg. 2007; 245: 44–50. <https://doi.org/10.1097/01.sla.0000225253.84501.0e> <PubMed>
41. Murata H, Yagi T, Iwagaki H, et al. Mechanism of impaired regeneration of fatty liver in mouse partial hepatectomy model. J Gastroenterol Hepatol 2007; 22: 2173–80. <https://doi.org/10.1111/j.1440-1746.2006.04798.x>
42. DeAngelis RA, Markiewski MM, Taub R, Lambris JD. A high-fat diet impairs liver regeneration in C57BL/6 mice through overexpression of the NF-kappaB inhibitor, IkappaBalpha. Hepatology 2005; 42: 1148–57. <https://doi.org/10.1002/hep.20879>
43. Rao MS, Papreddy K, Abecassis M, Hashimoto T. Regeneration of liver with marked fatty change following partial hepatectomy in rats. Dig Dis Sci 2001; 46: 1821–6. <https://doi.org/10.1023/A:1010654908938>
44. Rudnick DA, Davidson NO. Functional Relationships between Lipid Metabolism and Liver Regeneration. Int J Hepatol 2012; 2012: 549241. <https://doi.org/10.1155/2012/549241> <PubMed>
45. Yanger K, Knigin D, Zong Y, et al. Adult hepatocytes are generated by self-duplication rather than stem cell differentiation. Cell Stem Cell 2014; 15: 340–9. <https://doi.org/10.1016/j.stem.2014.06.003> <PubMed>
46. Fabrikant JI. The kinetics of cellular proliferation in regenerating liver. J Cell Biol 1968; 36: 551–65. <https://doi.org/10.1083/jcb.36.3.551> <PubMed>
47. Grisham JW. A morphologic study of deoxyribonucleic acid synthesis and cell proliferation in regenerating rat liver; autoradiography with thymidine-H3. Cancer Res 1962; 22: 842–9.
48. Yu CC, Woods AL, Levison DA. The assessment of cellular proliferation by immunohistochemistry: a review of currently available methods and their applications. Histochem J 1992; 24: 121–31. <https://doi.org/10.1007/BF01047461>
49. Weglarz TC, Sandgren EP. Timing of hepatocyte entry into DNA synthesis after partial hepatectomy is cell autonomous. Proc Natl Acad Sci U S A. 2000; 97: 12595–600. <https://doi.org/10.1073/pnas.220430497> <PubMed>
50. Streetz KL, Luedde T, Manns MP, Trautwein C. Interleukin 6 and liver regeneration. Gut 2000; 47: 309–12. <https://doi.org/10.1136/gut.47.2.309> <PubMed>
51. 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: 5126–30. <https://doi.org/10.1073/pnas.85.14.5126> <PubMed>
52. Gambino R, Musso G, Cassader M. Redox balance in the pathogenesis of nonalcoholic fatty liver disease: mechanisms and therapeutic opportunities. Antioxid Redox Signal 2011; 15: 1325–65. <https://doi.org/10.1089/ars.2009.3058>
53. Riehle KJ, Haque J, McMahan RS, Kavanagh TJ, Fausto N, Campbell JS. Sustained Glutathione Deficiency Interferes with the Liver Response to TNF-alpha and Liver Regeneration after Partial Hepatectomy in Mice. J Liver Disease Transplant 2013; 1.
54. Huang ZZ, Li H, Cai J, Kuhlenkamp J, Kaplowitz N, Lu SC. Changes in glutathione homeostasis during liver regeneration in the rat. Hepatology 1998; 27: 147–53. <https://doi.org/10.1002/hep.510270123>
55. Cortez-Pinto H, Chatham J, Chacko VP, Arnold C, Rashid A, Diehl AM. Alterations in liver ATP homeostasis in human nonalcoholic steatohepatitis: a pilot study. JAMA 1999; 282: 1659–64. <https://doi.org/10.1001/jama.282.17.1659>
56. Yang S, Tan TM, Wee A, Leow CK. Mitochondrial respiratory function and antioxidant capacity in normal and cirrhotic livers following partial hepatectomy. Cell Mol Life Sci 2004; 61: 220–9. <https://doi.org/10.1007/s00018-003-3357-4>
front cover

ISSN 1211-4286 (Print) ISSN 1805-9694 (Online)

Open access journal

Archive