Vascular endothelial growth factor improves liver regeneration and survival after 90% hepatectomy in a rat model of diet-induced steatosis

Digestion

Volumn 88, Issue 4, 2013, Pages 235-242

  Gu, Yanli ^a   Sowa, Jan Peter ^b   Paul, Andreas ^a   Gerken, Guido ^b   Schlaak, Joerg F ^b  

^a Departments of General Visceral and Transplantation Surgery   (Germany)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

Erythropoietin; Fatty liver disease; Gene expression; Liver regeneration; Liver resection; Vascular endothelial growth factor

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; ERYTHROPOIETIN; GLUCOSE; INTERLEUKIN 6; LACTATE DEHYDROGENASE; PROTEIN BCL 2; PUMA PROTEIN; RECOMBINANT ERYTHROPOIETIN; RECOMBINANT VASCULOTROPIN; RECOMBINANT VASCULOTROPIN 164; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BIOCHEMICAL MARKER; KI 67 ANTIGEN; SODIUM CHLORIDE; VASCULOTROPIN;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CONTROLLED STUDY; FATTY LIVER; GLUCOSE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; LACTATE DEHYDROGENASE BLOOD LEVEL; LIVER REGENERATION; LIVER RESECTION; MALE; NONHUMAN; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SURVIVAL RATE; TISSUE SURVIVAL; DISEASE SEVERITY; GENE EXPRESSION; HYPOGLYCEMIA; LIVER BIOPSY; LIVER CELL DAMAGE; LIVER FUNCTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL TIME; UPREGULATION;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; BLOOD GLUCOSE; DIET; DISEASE MODELS, ANIMAL; ERYTHROPOIETIN; FATTY LIVER; GENE EXPRESSION; GENES, BCL-2; GLUCONEOGENESIS; HEPATECTOMY; INTERLEUKIN-6; LIVER REGENERATION; MALE; RATS; RATS, WISTAR; SURVIVAL RATE; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84892148695     PISSN: 00122823     EISSN: 14219867     Source Type: Journal    
DOI: 10.1159/000355528     Document Type: Article

References (39)

1. Garcea G, Maddern GJ: Liver failure after major hepatic resection. J Hepatobiliary Pancreat Surg 2009; 16: 145-155.
2. Belghiti J, Ogata S: Assessment of hepatic reserve for the indication of hepatic resection. J Hepatobiliary Pancreat Surg 2005; 12: 1-3.
3. Morris-Stiff G, Gomez D, Prasad R: Quantitative assessment of hepatic function and its relevance to the liver surgeon. J Gastrointest Surg 2009; 13: 374-385.
4. Rudich N, Zamir G, Pappo O, Shlomai Z, Faroja M, Weiss ID, Wald H, Galun E, Peled A, Wald O: Focal liver necrosis appears early after partial hepatectomy and is dependent on T cells and antigen delivery from the gut. Liver Int 2009; 29: 1273-1284.
5. Hsu K-Y, Chau G-Y, Lui W-Y, Tsay S-H, King K-L, Wu C-W: Predicting morbidity and mortality after hepatic resection in patients with hepatocellular carcinoma: the role of Model for End-Stage Liver Disease score. World J Surg 2009; 33: 2412-2419.
6. Ronco MT, Frances D, De Lujan Alvarez M, Quiroga A, Monti J, Parody JP, Pisani G, Carrillo MC, Carnovale CE: Vascular endothelial growth factor and nitric oxide in rat liver regeneration. Life Sci 2007; 81: 750-755.
7. Beaudry P, Hida Y, Udagawa T, Alwayn IP, Greene AK, Arsenault D, Folkman J, Heymach JV, Ryeom S, Puder M: Endothelial progenitor cells contribute to accelerated liver regeneration. J Pediatr Surg 2007; 42: 1190-1198.
8. Bockhorn M, Goralski M, Prokofiev D, Dammann P, Grunewald P, Trippler M, Biglarnia A, Kamler M, Niehues EM, Frilling A, Broelsch CE, Schlaak JF: VEGF is important for early liver regeneration after partial hepatectomy. J Surg Res 2007; 138: 291-299.
9. Schmeding M, Boas-Knoop S, Lippert S, Ruehl M, Somasundaram R, Dagdelen T, Neuhaus P, Neumann UP: Erythropoietin promotes hepatic regeneration after extended liver resection in rats. J Gastroenterol Hepatol 2008; 23: 1125-1131.
10. Bockhorn M, Fingas CD, Rauen U, Canbay A, Sotiropoulos GC, Frey U, Sheu S-Y, Wohlschlager J, Broelsch CE, Schlaak JF: Erythropoietin treatment improves liver regeneration and survival in rat models of extended liver resection and living donor liver transplantation. Transplantation 2008; 86: 1578-1585.
11. Naughton GK, Naughton BA, Gordon AS: Erythropoietin production by macrophages in the regenerating liver. J Surg Oncol 1985; 30: 184-197.
12. Klemm K, Eipel C, Cantre D, Abshagen K, Menger MD, Vollmar B: Multiple doses of erythropoietin impair liver regeneration by increasing TNF-alpha, the Bax to Bcl-xL ratio and apoptotic cell death. PLoS One 2008; 3:e3924.
13. Van den Esschert JW, De Graaf W, Van Lienden KP, Busch OR, Heger M, Van Delden OM, Gouma DJ, Bennink RJ, Lameris JS, Van Gulik TM: Volumetric and functional recovery of the remnant liver after major liver resection with prior portal vein embolization: recovery after PVE and liver resection. J Gastrointest Surg 2009; 13: 1464-1469.
14. Florman S, Miller CM: Live donor liver transplantation. Liver Transpl 2006; 12: 499-510.
15. Levene AP, Goldin RD: The epidemiology, pathogenesis and histopathology of fatty liver disease. Histopathology 2012; 61: 141-152.
16. Heuer M, Kaiser GM, Kahraman A, Banysch M, Saner FH, Mathe Z, Gerken G, Paul A, Canbay A, Treckmann JW: Liver transplantation in nonalcoholic steatohepatitis is associated with high mortality and post-transplant complications: a single-center experience. Digestion 2012; 86: 107-113.
17. Pathak S, Tang JMF, Terlizzo M, Poston GJ, Malik HZ: Hepatic steatosis, body mass index and long term outcome in patients undergoing hepatectomy for colorectal liver metastases. Eur J Surg Oncol 2010; 36: 52-57.
18. Gomez D, Malik HZ, Bonney GK, Wong V, Toogood GJ, Lodge JPA, Prasad KR: Steatosis predicts postoperative morbidity following hepatic resection for colorectal metastasis. Br J Surg 2007; 94: 1395-1402.
19. Bockhorn M, Schollmann S, Opitz B, Sotiropoulos GC, Sheu S-Y, Niehaus E, Trippler M, Frilling A, Broelsch CE, Schlaak JF: Vascular endothelial growth factor does not improve liver regeneration and survival after 90% subtotal liver resection. Hepatol Res 2007; 37: 353-359.
20. Emond J, Capron-Laudereau M, Meriggi F, Bernuau J, Reynes M, Houssin D: Extent of hepatectomy in the rat. Evaluation of basal conditions and effect of therapy. Eur Surg Res 1989; 21: 251-259.
21. Gu Y, Dirsch O, Dahmen U, Ji Y, He Q, Chi H, Broelsch CE: Impact of donor gender on male rat recipients of small-for-size liver grafts. Liver Transpl 2005; 11: 669-678.
22. Jonas S, Thelen A, Benckert C, Biskup W, Neumann U, Rudolph B, Lopez-Haanninen E, Neuhaus P: Extended liver resection for intrahepatic cholangiocarcinoma: a comparison of the prognostic accuracy of the fifth and sixth editions of the TNM classification. Ann Surg 2009; 249: 303-309.
23. Kim SH, Cho SY, Park S-J, Lee KW, Han S-S, Lee S, Park J-W, Kim C-M: Learning curve for living-donor liver transplantation in a fledgling cancer center. Transpl Int 2009; 22: 1164-1171.
24. Hosohata K, Masuda S, Yonezawa A, Sugimoto M, Takada Y, Kaido T, Ogura Y, Oike F, Uemoto S, Inui K: Absence of influence of concomitant administration of rabeprazole on the pharmacokinetics of tacrolimus in adult living-donor liver transplant patients: a case-control study. Drug Metab Pharmacokinet 2009; 24: 458-463.
25. Cescon M, Vetrone G, Grazi GL, Ramacciato G, Ercolani G, Ravaioli M, Del Gaudio M, Pinna AD: Trends in perioperative outcome after hepatic resection: analysis of 1500 consecutive unselected cases over 20 years. Ann Surg 2009; 249: 995-1002.
26. Fausto N, Campbell JS, Riehle KJ: Liver regeneration. Hepatology 2006; 43:S45-S53.
27. Shimizu H, Mitsuhashi N, Ohtsuka M, Ito H, Kimura F, Ambiru S, Togawa A, Yoshidome H, Kato A, Miyazaki M: Vascular endothelial growth factor and angiopoietins regulate sinusoidal regeneration and remodeling after partial hepatectomy in rats. World J Gastroenterol 2005; 11: 7254-7260.
28. Shimizu H, Miyazaki M, Wakabayashi Y, Mitsuhashi N, Kato A, Ito H, Nakagawa K, Yoshidome H, Kataoka M, Nakajima N: Vascular endothelial growth factor secreted by replicating hepatocytes induces sinusoidal endothelial cell proliferation during regeneration after partial hepatectomy in rats. J Hepatol 2001; 34: 683-689.
29. Qiao J-G, Wu L, Lei D-X, Wang L: Insulin promotes sinusoidal endothelial cell proliferation mediated by upregulation of vascular endothelial growth factor in regenerating rat liver after partial hepatectomy. World J Gastroenterol 2005; 11: 5978-5983.
30. Oe H, Kaido T, Mori A, Onodera H, Imamura M: Hepatocyte growth factor as well as vascular endothelial growth factor gene induction effectively promotes liver regeneration after hepatectomy in Solt-Farber rats. Hepatogastroenterology 2005; 52: 1393-1397.
31. Lu X, Ji Y, Zhang L, Zhang Y, Zhang S, An Y, Liu P, Zheng Y: Resistance to obesity by repression of VEGF gene expression through induction of brown-like adipocyte differentiation. Endocrinology 2012; 153: 3123-3132.
32. Elias I, Franckhauser S, Ferre T, Vila L, Tafuro S, Munoz S, Roca C, Ramos D, Pujol A, Riu E, Ruberte J, Bosch F: Adipose tissue overexpression of vascular endothelial growth factor protects against diet-induced obesity and insulin resistance. Diabetes 2012; 61: 1801-1813.
33. Seitz O, Schurmann C, Hermes N, Muller E, Pfeilschifter J, Frank S, Goren I: Wound healing in mice with high-fat diet-or ob gene-induced diabetes-obesity syndromes: a comparative study. Exp Diabetes Res 2010; 2010: 476969.
34. Park H, Kim M, Kwon GT, Lim DY, Yu R, Sung M-K, Lee KW, Daily JW 3rd, Park JHY: A high-fat diet increases angiogenesis, solid tumor growth, and lung metastasis of CT26 colon cancer cells in obesity-resistant BALB/c mice. Mol Carcinog 2012; 51: 869-880.
35. Wada H, Ura S, Kitaoka S, Satoh-Asahara N, Horie T, Ono K, Takaya T, Takanabe-Mori R, Akao M, Abe M, Morimoto T, Murayama T, Yokode M, Fujita M, Shimatsu A, Hasegawa K: Distinct characteristics of circulating vascular endothelial growth factor-a and C levels in human subjects. PLoS One 2011; 6:e29351.
36. Yuceturk H, Yagmurdur MC, Gur G, Demirbilek M, Bilezikci B, Turan M, Karakayali H, Haberal M: Role of heparin on TNF-alpha and IL-6 levels in liver regeneration after partial hepatic resection. Eur Surg Res 2007; 39: 216-221.
37. Sudo K, Yamada Y, Saito K, Shimizu S, Ohashi H, Kato T, Moriwaki H, Ito H, Seishima M: TNF-alpha and IL-6 signals from the bone marrow derived cells are necessary for normal murine liver regeneration. Biochim Biophys Acta 2008; 1782: 671-679.
38. Fausto N, Laird AD, Webber EM: Liver regeneration. 2. Role of growth factors and cytokines in hepatic regeneration. FASEB J 1995; 9: 1527-1536.
39. Sydor S, Gu Y, Schlattjan M, Bechmann LP, Rauen U, Best J, Paul A, Baba HA, Sowa J-P, Gerken G, Canbay A: Steatosis does not impair liver regeneration after partial hepatectomy. Lab Invest 2013; 93: 20-30.