Amphiregulin stimulates liver regeneration after small-for-size mouse liver transplantation

American Journal of Transplantation

Volumn 12, Issue 8, 2012, Pages 2052-2061

  Liu, Q ^a,b   Rehman, H ^a   Krishnasamy, Y ^a   Haque, K ^a   Schnellmann, R G ^a,c   Lemasters, J J ^a,d   Zhong, Z ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b DALIAN MEDICAL UNIVERSITY   (China)

^c RALPH H JOHNSON VA MEDICAL CENTER   (United States)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Growth factor; liver graft survival; liver regeneration; liver transplantation; living donor transplantation; small for size syndrome

Indexed keywords

4 (3 BROMOANILINO) 6,7 DIMETHOXYQUINAZOLINE; AMPHIREGULIN; BROXURIDINE; CYCLIN D1; CYCLIN E; CYCLINE; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HYPERBILIRUBINEMIA; HYPOALBUMINEMIA; LIVER FUNCTION; LIVER REGENERATION; LIVER TRANSPLANTATION; MALE; MITOSIS INDEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SMALL FOR SIZE MOUSE LIVER TRANSPLANTATION; SURVIVAL;

ANIMALS; GLYCOPROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER REGENERATION; MALE; MICE; MICE, INBRED C57BL; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84864463927     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2012.04069.x     Document Type: Article

References (64)

1. Gonzalez HD, Liu ZW, Cashman S, Fusai GK,. Small for size syndrome following living donor and split liver transplantation. World J Gastrointest Surg 2010; 2: 389-394.
2. Hong JC, Yersiz H, Busuttil RW,. Where are we today in split liver transplantation? Curr Opin Organ Transplant 2011; 16: 269-273.
3. Wertheim JA, Petrowsky H, Saab S, Kupiec-Weglinski JW, Busuttil RW,. Major challenges limiting liver transplantation in the United States. Am J Transplant 2011; 11: 1773-1784.
4. Testa G, Malago M, Broelsch CE,. Living-donor liver transplantation in adults. Langenbecks Arch Surg 1999; 384: 536-543.
5. Sugawara Y, Makuuchi M, Takayama T, et al,. Small-for-size grafts in living-related liver transplantation. J Am Coll Surg 2001; 192: 510-513.
6. Zhong Z, Schwabe RF, Kai Y, et al,. Liver regeneration is suppressed in small-for-size liver grafts after transplantation: Involvement of JNK, cyclin D1 and defective energy supply. Transplantation 2006; 82: 241-250.
7. Zhong Z, Tsukada S, Rehman H, et al,. Inhibition of transforming growth factor-beta/Smad signaling improves regeneration of small-for-size rat liver grafts. Liver Transpl 2010; 16: 181-190.
8. Tian Y, Graf R, Jochum W, Clavien PA,. Arterialized partial orthotopic liver transplantation in the mouse: A new model and evaluation of the critical liver mass. Liver Transpl 2003; 9: 789-795.
9. Tian Y, Jochum W, Georgiev P, Moritz W, Graf R, Clavien PA,. Kupffer cell-dependent TNF-alpha signaling mediates injury in the arterialized small-for-size liver transplantation in the mouse. Proc Natl Acad Sci USA 2006; 103: 4598-4603.
10. Zhong Z, Theruvath TP, Currin RT, Waldmeier PC, Lemasters JJ,. NIM811, a mitochondrial permeability transition inhibitor, prevents mitochondrial depolarization in small-for-size rat liver grafts. Am J Transplant 2007; 7: 1103-1111.
11. Zhong Z, Connor HD, Froh M, et al,. Free radical-dependent dysfunction of small-for-size rat liver grafts: Prevention by plant polyphenols. Gastroenterology 2005; 129: 652-664.
12. Streetz KL, Luedde T, Manns MP, Trautwein C,. Interleukin 6 and liver regeneration. Gut 2000; 47: 309-312.
13. Riehle KJ, Dan YY, Campbell JS, Fausto N,. New concepts in liver regeneration. J Gastroenterol Hepatol 2011; 26 (Suppl 1): 203-212.
14. Michalopoulos GK, Khan Z,. Liver regeneration, growth factors, and amphiregulin. Gastroenterology 2005; 128: 503-506.
15. Fausto N,. Liver regeneration. J Hepatol 2000; 32 (Suppl 1): 19-31.
16. Rehman H, Sun J, Shi Y, et al,. NIM811 prevents mitochondrial dysfunction, attenuates liver injury, and stimulates liver regeneration after massive hepatectomy. Transplantation 2011; 91: 406-412.
17. Kohler C, Bell AW, Bowen WC, Monga SP, Fleig W, Michalopoulos GK,. Expression of Notch-1 and its ligand Jagged-1 in rat liver during liver regeneration. Hepatology 2004; 39: 1056-1065.
18. Ren X, Hogaboam C, Carpenter A, Colletti L,. Stem cell factor restores hepatocyte proliferation in IL-6 knockout mice following 70% hepatectomy. J Clin Invest 2003; 112: 1407-1418.
19. Berasain C, Garcia-Trevijano ER, Castillo J, et al,. Amphiregulin: An early trigger of liver regeneration in mice. Gastroenterology 2005; 128: 424-432.
20. Sternlicht MD, Sunnarborg SW,. The ADAM17-amphiregulin-EGFR axis in mammary development and cancer. J Mammary Gland Biol Neoplasia 2008; 13: 181-194.
21. Bellezza I, Bracarda S, Caserta C, Minelli A,. Targeting of EGFR tyrosine kinase by ZD1839 ("Iressa") in androgen-responsive prostate cancer in vitro. Mol Genet Metab 2006; 88: 114-122.
22. Jorissen RN, Walker F, Pouliot N, Garrett TP, Ward CW, Burgess AW,. Epidermal growth factor receptor: Mechanisms of activation and signalling. Exp Cell Res 2003; 284: 31-53.
23. Theruvath TP, Czerny C, Ramshesh VK, Zhong Z, Chavin KD, Lemasters JJ,. C-Jun N-terminal kinase 2 promotes graft injury via the mitochondrial permeability transition after mouse liver transplantation. Am J Transplant 2008; 8: 1819-1828.
24. Zhong Z, Ramshesh VK, Rehman H, et al,. Activation of the oxygen-sensing signal cascade prevents mitochondrial injury after mouse liver ischemia-reperfusion. Am J Physiol Gastrointest Liver Physiol 2008; 295: G823-G832.
25. Rehman H, Ramshesh VK, Theruvath TP, et al,. NIM811, a mitochondrial permeability transition inhibitor, attenuates cholestatic liver injury but not fibrosis in mice. J Pharmacol Exp Ther 2008; 327: 699-706.
26. Leonardi E, Girlando S, Serio G, et al,. PCNA and Ki67 expression in breast carcinoma: Correlations with clinical and biological variables. J Clin Pathol 1992; 45: 416-419.
27. Galderisi U, Jori FP, Giordano A,. Cell cycle regulation and neural differentiation. Oncogene 2003; 22: 5208-5219.
28. Schwabe RF, Bradham CA, Uehara T, et al,. c-Jun-N-terminal kinase drives cyclin D1 expression and proliferation during liver regeneration. Hepatology 2003; 37: 824-832.
29. Buitrago-Molina LE, Pothiraju D, Lamle J, et al,. Rapamycin delays tumor development in murine livers by inhibiting proliferation of hepatocytes with DNA damage. Hepatology 2009; 50: 500-509.
30. Ravenhall C, Guida E, Harris T, Koutsoubos V, Stewart A,. The importance of ERK activity in the regulation of cyclin D1 levels and DNA synthesis in human cultured airway smooth muscle. Br J Pharmacol 2000; 131: 17-28.
31. Urata K, Kawasaki S, Matsunami H, et al,. Calculation of child and adult standard liver volume for liver transplantation. Hepatology 1995; 21: 1317-1321.
32. Ikegami T, Shimada M, Imura S, et al,. Current concept of small-for-size grafts in living donor liver transplantation. Surg Today 2008; 38: 971-982.
33. Lee S, Hwang S, Park K, et al,. An adult-to-adult living donor liver transplant using dual left lobe grafts. Surgery 2001; 129: 647-650.
34. LIU C, Lee RC, Loong CC, Hsia CY, Yeh YC, Chiou SY,. Increasing donor body weight to prevent small-for-size syndrome in living donor liver transplantation. World J Surg 2010; 34: 2401-2408.
35. Xu X, Man K, Zheng SS, et al,. Attenuation of acute phase shear stress by somatostatin improves small-for-size liver graft survival. Liver Transpl 2006; 12: 621-627.
36. Tian Y, Graf R, El-Badry AM, et al,. Activation of serotonin receptor-2B rescues small-for-size liver graft failure in mice. Hepatology 2011; 53: 253-262.
37. Zhao Y, Man K, Lo CM, et al,. Attenuation of small-for-size liver graft Injury by FTY720: Significance of cell survival Akt signaling pathway. Am J Transplant 2004; 4: 1399-1407.
38. Rehman H, Connor HD, Ramshesh VK, et al,. Ischemic preconditioning prevents free radical production and mitochondrial depolarization in small-for-size rat liver grafts. Transplantation 2008; 85: 1322-1331.
39. Webber EM, Godowski PJ, Fausto N,. In vivo response of hepatocytes to growth factors requires an initial priming stimulus. Hepatology 1994; 19: 489-497.
40. Pinkus R, Weiner LM, Daniel V,. Role of oxidants and antioxidants in the induction of AP-1, NF-kappaB, and glutathione S-transferase gene expression. J Biol Chem 1996; 271: 13422-13429.
41. Hsu D, Fukata M, Hernandez YG, et al,. Toll-like receptor 4 differentially regulates epidermal growth factor-related growth factors in response to intestinal mucosal injury. Lab Invest 2010; 90: 1295-1305.
42. Bordoli MR, Stiehl DP, Borsig L, et al,. Prolyl-4-hydroxylase. Oncogene 2011; 30: 548-560.
43. Berasain C, Castillo J, Perugorria MJ, Prieto J, Avila MA,. Amphiregulin: A new growth factor in hepatocarcinogenesis. Cancer Lett 2007; 254: 30-41.
44. Miyazaki Y, Shinomura Y, Tsutsui S, et al,. Oxidative stress increases gene expression of heparin-binding EGF-like growth factor and amphiregulin in cultured rat gastric epithelial cells. Biochem Biophys Res Commun 1996; 226: 542-546.
45. Webber EM, Fitzgerald MJ, Brown PI, Bartlett MH, Fausto N,. Transforming growth factor-alpha expression during liver regeneration after partial hepatectomy and toxic injury, and potential interactions between transforming growth factor-alpha and hepatocyte growth factor. Hepatology 1993; 18: 1422-1431.
46. Russell WE, Dempsey PJ, Sitaric S, Peck AJ, Coffey RJ, Jr,. Transforming growth factor-alpha (TGF alpha) concentrations increase in regenerating rat liver: Evidence for a delayed accumulation of mature TGF alpha. Endocrinol 1993; 133: 1731-1738.
47. Russell WE, Kaufmann WK, Sitaric S, Luetteke NC, Lee DC,. Liver regeneration and hepatocarcinogenesis in transforming growth factor-alpha-targeted mice. Mol Carcinog 1996; 15: 183-189.
48. Mitchell C, Nivison M, Jackson LF, et al,. Heparin-binding epidermal growth factor-like growth factor links hepatocyte priming with cell cycle progression during liver regeneration. J Biol Chem 2005; 280: 2562-2568.
49. Paranjpe S, Bowen WC, Tseng GC, Luo JH, Orr A, Michalopoulos GK,. RNA interference against hepatic epidermal growth factor receptor has suppressive effects on liver regeneration in rats. Am J Pathol 2010; 176: 2669-2681.
50. Klapper LN, Glathe S, Vaisman N, et al,. The ErbB-2/HER2 oncoprotein of human carcinomas may function solely as a shared coreceptor for multiple stroma-derived growth factors. Proc Natl Acad Sci USA 1999; 96: 4995-5000.
51. Haga S, Ozaki M, Inoue H, 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.
52. Francavilla A, Starzl TE, Scotti C, et al,. Inhibition of liver, kidney, and intestine regeneration by rapamycin. Transplantation 1992; 53: 496-498.
53. Volarevic S, Stewart MJ, Ledermann B, et al,. Proliferation, but not growth, blocked by conditional deletion of 40S ribosomal protein S6. Science 2000; 288: 2045-2047.
54. Dennis PB, Jaeschke A, Saitoh M, Fowler B, Kozma SC, Thomas G,. Mammalian TOR: A homeostatic ATP sensor. Science 2001; 294: 1102-1105.
55. Wan YS, Wang ZQ, Voorhees J, Fisher G,. EGF receptor crosstalks with cytokine receptors leading to the activation of c-Jun kinase in response to UV irradiation in human keratinocytes. Cell Signal 2001; 13: 139-144.
56. Prada PO, Ropelle ER, Mourao RH, et al,. EGFR tyrosine kinase inhibitor (PD153035) improves glucose tolerance and insulin action in high-fat diet-fed mice. Diabetes 2009; 58: 2910-2919.
57. Leu JI, Crissey MA, Craig LE, Taub R,. Impaired hepatocyte DNA synthetic response posthepatectomy in insulin-like growth factor binding protein 1-deficient mice with defects in C/EBP beta and mitogen-activated protein kinase/extracellular signal-regulated kinase regulation. Mol Cell Biol 2003; 23: 1251-1259.
58. Bard-Chapeau EA, Yuan J, Droin N, Long S, Zhang EE, Nguyen TV, et al,. Concerted functions of Gab1 and Shp2 in liver regeneration and hepatoprotection. Mol Cell Biol 2006; 26: 4664-4674.
59. Scheving LA, Stevenson MC, Zhang X, Russell WE,. Cultured rat hepatocytes upregulate Akt and ERK in an ErbB-2-dependent manner. Am J Physiol Gastrointest Liver Physiol 2008; 295: G322-G331.
60. Bokemeyer D, Panek D, Kitahara M, et al,. The map kinase ERK regulates renal activity of cyclin-dependent kinase 2 in experimental glomerulonephritis. Nephrol Dial Transplant 2007; 22: 3431-3441.
61. Nelsen CJ, Rickheim DG, Timchenko NA, Stanley MW, Albrecht JH,. Transient expression of cyclin D1 is sufficient to promote hepatocyte replication and liver growth in vivo. Cancer Res 2001; 61: 8564-8568.
62. Tian Y, Rudiger HA, Jochum W, Clavien PA,. Comparison of arterialized and nonarterialized orthotopic liver transplantation in mice: Prowess or relevant model? Transplantation 2002; 74: 1242-1246.
63. Steger U, Sawitzki B, Gassel AM, Gassel HJ, Wood KJ,. Impact of hepatic rearterialization on reperfusion injury and outcome after mouse liver transplantation. Transplantation 2003; 76: 327-332.
64. Conzelmann LO, Zhong Z, Bunzendahl H, Wheeler MD, Lemasters JJ,. Reduced-size liver transplantation in the mouse. Transplantation 2003; 76: 496-501.