Advances in liver regeneration

Expert Review of Gastroenterology and Hepatology

Volumn 8, Issue 8, 2014, Pages 897-907

  Michalopoulos, George K ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

EGFR; Extracellular matrix; Facultative stem cell; HGF; Integrin linked kinase; Liver regeneration

Indexed keywords

BETA CATENIN; CARBON TETRACHLORIDE; DNA; EPIDERMAL GROWTH FACTOR RECEPTOR; GLYPICAN 3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; METALLOPROTEINASE; NORADRENALIN; NOTCH1 RECEPTOR; PARACETAMOL; PLASMIN; PLASMINOGEN; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; STAT3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UROKINASE;

BILE DUCT; BODY WEIGHT; CELL PROLIFERATION; CELL TRANSDIFFERENTIATION; CONVALESCENCE; DNA SYNTHESIS; EPITHELIUM CELL; EXTRACELLULAR MATRIX; HEPATITIS A; HEPATITIS B; HEPATITIS C; HUMAN; LIVER CELL; LIVER REGENERATION; LIVER TOXICITY; LIVER WEIGHT; MAMMAL; NONHUMAN; PARTIAL HEPATECTOMY; PORTAL VEIN BLOOD FLOW; PROTEIN EXPRESSION; RECEPTOR BINDING; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; WNT SIGNALING PATHWAY; ANIMAL; COMPLICATION; LIVER DISEASES; LIVER RESECTION; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CELL PROLIFERATION; HEPATECTOMY; HEPATOCYTES; HUMANS; LIVER DISEASES; LIVER REGENERATION; SIGNAL TRANSDUCTION;

EID: 84911437031     PISSN: 17474124     EISSN: 17474132     Source Type: Journal    
DOI: 10.1586/17474124.2014.934358     Document Type: Review

References (99)

1. Michalopoulos GK. Principles of liver regeneration and growth homeostasis. Compr Physiol 2013;3(1):485-513
2. Michalopoulos GK, DeFrances MC. Liver regeneration. Science 1997;276(5309): 60-6
3. Michalopoulos GK. Liver regeneration. J Cell Physiol 2007;213(2):286-300
4. Michalopoulos GK. Liver regeneration after partial hepatectomy: critical analysis of mechanistic dilemmas. Am J Pathol 2010; 176(1):2-13
5. Evarts RP, Nagy P, Marsden E, Thorgeirsson SS. A precursor-product relationship exists between oval cells and hepatocytes in rat liver. Carcinogenesis 1987;8(11):1737-40
6. Evarts RP, Nagy P, Nakatsukasa H, et al. In vivo differentiation of rat liver oval cells into hepatocytes. Cancer Res 1989;49(6): 1541-7
7. Yanger K, Zong Y, Maggs LR, et al. Robust cellular reprogramming occurs spontaneously during liver regeneration. Genes Dev 2013;27(7):719-24
8. Limaye PB, Bowen WC, Orr AV, et al. Mechanisms of hepatocyte growth factor-mediated and epidermal growth factor-mediated signaling in transdifferentiation of rat hepatocytes to biliary epithelium. Hepatology 2008;47(5): 1702-13
9. Michalopoulos GK, Barua L, Bowen WC. Transdifferentiation of rat hepatocytes into biliary cells after bile duct ligation and toxic biliary injury. Hepatology 2005;41(3): 535-44
10. Hattoum A, Rubin E, Orr A, Michalopoulos GK. Expression of hepatocyte epidermal growth factor receptor, FAS and glypican 3 in EpCAM-positive regenerative clusters of hepatocytes, cholangiocytes, and progenitor cells in human liver failure. Hum Pathol 2013; 44(5):743-9
11. Limaye PB, Alarcon G, Walls AL, et al. Expression of specific hepatocyte and cholangiocyte transcription factors in human liver disease and embryonic development. Lab Invest 2008;88(8):865-72
12. Wang L, Wang X, Xie G, et al. Liver sinusoidal endothelial cell progenitor cells promote liver regeneration in rats. J Clin Invest 2012;122(4):1567-73
13. Marubashi S, Sakon M, Nagano H, et al. Effect of portal hemodynamics on liver regeneration studied in a novel portohepatic shunt rat model. Surgery 2004;136(5): 1028-37
14. Kohler C, Bell AW, Bowen WC, et al. Expression of Notch-1 and its ligand Jagged-1 in rat liver during liver regeneration. Hepatology 2004;39(4):1056-65
15. Monga SP, Pediaditakis P, Mule K, et al. Changes in WNT/beta-catenin pathway during regulated growth in rat liver regeneration. Hepatology 2001;33(5): 1098-109
16. Kim TH, Mars WM, Stolz DB, et al. Extracellular matrix remodeling at the early stages of liver regeneration in the rat. Hepatology 1997;26(4):896-904
17. Kim TH, Mars WM, Stolz DB, Michalopoulos GK. Expression and activation of pro-MMP-2 and pro-MMP-9 during rat liver regeneration. Hepatology 2000;31(1):75-82
18. Stolz DB, Mars WM, Petersen BE, et al. Growth factor signal transduction immediately after two-thirds partial hepatectomy in the rat. Cancer Res 1999; 59(16):3954-60
19. Cruise JL, Knechtle SJ, Bollinger RR, et al. Alpha 1-adrenergic effects and liver regeneration. Hepatology 1987;7(6): 1189-94
20. Cruise JL, Houck KA, Michalopoulos GK. Induction of DNA synthesis in cultured rat hepatocytes through stimulation of alpha 1 adrenoreceptor by norepinephrine. Science 1985;227(4688):749-51
21. Broten J, Michalopoulos G, Petersen B, Cruise J. Adrenergic stimulation of hepatocyte growth factor expression. Biochem Biophys Res Commun 1999; 262(1):76-9
22. Olsen PS, Poulsen SS, Kirkegaard P. Adrenergic effects on secretion of epidermal growth factor from Brunner's glands. Gut 1985;26(9):920-7
23. Cressman DE, Greenbaum LE, DeAngelis RA, et al. Liver failure and defective hepatocyte regeneration in interleukin-6- deficient mice. Science 1996; 274(5291):1379-83
24. Yamada Y, Kirillova I, Peschon JJ, Fausto N. 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 1997;94(4): 1441-6
25. Webber EM, Bruix J, Pierce RH, Fausto N. Tumor necrosis factor primes hepatocytes for DNA replication in the rat. Hepatology 1998;28(5):1226-34
26. Mohn KL, Laz TM, Melby AE, Taub R. Immediate-early gene expression differs between regenerating liver, insulin-stimulated H-35 cells, and mitogen-stimulated Balb/c 3T3 cells. Liver-specific induction patterns of gene 33, phosphoenolpyruvate carboxykinase, and the jun, fos, and egr families. J Biol Chem 1990;265(35):21914-21
27. Mullany LK, White P, Hanse EA, et al. Distinct proliferative and transcriptional effects of the D-type cyclins in vivo. Cell Cycle 2008;7(14):2215-24
28. Paranjpe S, Bowen WC, Tseng GC, et al. A interference against hepatic epidermal growth factor receptor has suppressive effects on liver regeneration in rats. Am J Pathol 2010;176(6):2669-81
29. Nejak-Bowen K, Orr A, Bowen WC Jr, Michalopoulos GK. Conditional genetic elimination of hepatocyte growth factor in mice compromises liver regeneration after partial hepatectomy. PLoS One 2013;8(3): e59836
30. Paranjpe S, Bowen WC, Bell AW, et al. Cell cycle effects resulting from inhibition of hepatocyte growth factor and its receptor c-Met in regenerating rat livers by RNA interference. Hepatology 2007;45(6): 1471-7
31. Ma J, Zou C, Guo L, et al. Novel death defying domain in met entraps the active site of caspase-3 and blocks apoptosis in hepatocytes. Hepatology 2014;59(5): 2010-21
32. Wang X, DeFrances MC, Dai Y, et al. A mechanism of cell survival: sequestration of fas by the HGF receptor met. Mol Cell 2002;9(2):411-21
33. Rabes HM. Kinetics of hepatocellular proliferation as a function of the microvascular structure and functional state of the liver. Ciba Found Symp 1977(55): 31-53
34. Volk A, Michalopoulos G, Weidner M, Gebhardt R. Different proliferative responses of periportal and pericentral rat hepatocytes to hepatocyte growth factor. Biochem Biophys Res Commun 1995; 207(2):578-84
35. Mead JE, Fausto N. Transforming growth factor alpha may be a physiological regulator of liver regeneration by means of an autocrine mechanism. Proc Natl Acad Sci USA 1989;86(5):1558-62
36. LeCouter J, Moritz DR, Li B, et al. Angiogenesis-independent endothelial protection of liver: role of VEGFR-1. Science 2003;299(5608):890-3
37. Yanagita K, Nagaike M, Ishibashi H, et al. Lung may have an endocrine function producing hepatocyte growth factor in response to injury of distal organs. Biochem Biophys Res Commun 1992; 182(2):802-9
38. Kono S, Nagaike M, Matsumoto K, Nakamura T. Marked induction of hepatocyte growth factor mRNA in intact kidney and spleen in response to injury of distant organs. Biochem Biophys Res Commun 1992;186(2):991-8
39. Pediaditakis P, Lopez-Talavera JC, Petersen B, et al. The processing and utilization of hepatocyte growth factor/ scatter factor following partial hepatectomy in the rat. Hepatology 2001;34(4 Pt 1): 688-93
40. Weymann A, Hartman E, Gazit V, et al. p21 is required for dextrose-mediated inhibition of mouse liver regeneration. Hepatology 2009;50(1):207-15
41. Omenetti A, Choi S, Michelotti G, Diehl AM. Hedgehog signaling in the liver. J Hepatol 2011;54(2):366-73
42. Ochoa B, Syn WK, Delgado I, et al. Hedgehog signaling is critical for normal liver regeneration after partial hepatectomy in mice. Hepatology 2010; 51(5):1712-23
43. Bhave VS, Mars W, Donthamsetty S, et al. Regulation of liver growth by glypican 3, CD81, hedgehog, and Hhex. Am J Pathol 2013;183(1):153-9
44. Omenetti A, Choi S, Michelotti G, Diehl AM. Hedgehog signaling in the liver. J Hepatol 2011;54(2):366-73
45. Monga SP, Mars WM, Pediaditakis P, et al. Hepatocyte growth factor induces Wnt-independent nuclear translocation of beta-catenin after Met-beta-catenin dissociation in hepatocytes. Cancer Res 2002;62(7):2064-71
46. Yang J, Mowry LE, Nejak-Bowen KN, et al. Beta-catenin signaling in murine liver zonation and regeneration: a Wnt-Wnt situation! Hepatology. 2014. [Epub ahead of print]
47. Apte U, Zeng G, Muller P, et al. Activation of Wnt/beta-catenin pathway during hepatocyte growth factor-induced hepatomegaly in mice. Hepatology 2006; 44(4):992-1002
48. Tan X, Apte U, Micsenyi A, et al. Epidermal growth factor receptor: a novel target of the Wnt/beta-catenin pathway in liver. Gastroenterology 2005;129(1): 285-302
49. Zeng G, Awan F, Otruba W, et al. Wnt'er in liver: expression of Wnt and frizzled genes in mouse. Hepatology 2007;45(1): 195-204
50. Tan X, Behari J, Cieply B, et al. Conditional deletion of beta-catenin reveals its role in liver growth and regeneration. Gastroenterology 2006;131(5):1561-72
51. Nejak-Bowen KN, Thompson MD, Singh S, et al. Accelerated liver regeneration and hepatocarcinogenesis in mice overexpressing serine-45 mutant beta-catenin. Hepatology 2010;51(5):1603-13
52. 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(4):2562-8
53. Haga S, Ogawa W, Inoue H, et al. Compensatory recovery of liver mass by Akt-mediated hepatocellular hypertrophy in liver-specific STAT3-deficient mice. J Hepatol 2005;43(5):799-807
54. Nagy P, Teramoto T, Factor VM, et al. Reconstitution of liver mass via cellular hypertrophy in the rat. Hepatology 2001; 33(2):339-45
55. Miyaoka Y, Miyajima A. To divide or not to divide: revisiting liver regeneration. Cell Div 2013;8(1):8
56. Miyaoka Y, Ebato K, Kato H, et al. Hypertrophy and unconventional cell division of hepatocytes underlie liver regeneration. Curr Biol 2012;22(13): 1166-75
57. Itoh T, Miyajima A. Liver regeneration by stem/progenitor cells. Hepatology 2014; 59(4):1617-26
58. Webber EM, FitzGerald MJ, Brown PI, et al. 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(6):1422-31
59. Luetteke NC, Qiu TH, Peiffer RL, et al. F alpha deficiency results in hair follicle and eye abnormalities in targeted and waved-1 mice. Cell 1993;73(2):263-78
60. Norris CA, He M, Kang LI, et al. Synthesis of IL-6 by hepatocytes is a normal response to common hepatic stimuli. PLoS One 2014;9(4):e96053
61. Schirmacher P, Geerts A, Pietrangelo A, et al. Hepatocyte growth factor/ hepatopoietin A is expressed in fat-storing cells from rat liver but not myofibroblast-like cells derived from fatstoring cells. Hepatology 1992;15(1):5-11
62. Houck KA, Cruise JL, Michalopoulos G. Norepinephrine modulates the growth-inhibitory effect of transforming growth factor-beta in primary rat hepatocyte cultures. J Cell Physiol 1988;135(3):551-5
63. Jirtle RL, Carr BI, Scott CD. Modulation of insulin-like growth factor-II/mannose 6-phosphate receptors and transforming growth factor-beta 1 during liver regeneration. J Biol Chem 1991;266(33): 22444-50. Erratum in J Biol Chem 1991; 266(36):24860
64. Ichikawa T, Zhang YQ, Kogure K, et al. Transforming growth factor beta and activin tonically inhibit DNA synthesis in the rat liver. Hepatology 2001;34(5):918-25
65. Jakowlew SB, Mead JE, Danielpour D, et al. Transforming growth factor-beta (TGF-beta) isoforms in rat liver regeneration: messenger RNA expression and activation of latent TGF- beta. Cell Regul 1991;2(7):535-48
66. Chari RS, Price DT, Sue SR, et al. Down-regulation of transforming growth factor beta receptor type I, II, and III during liver regeneration. Am J Surg 1995; 169(1):126-31.discussion 131-22
67. Roberts AB, McCune BK, Sporn MB. TGF-beta: regulation of extracellular matrix. Kidney Int 1992;41(3):557-9
68. Pepper MS, Vassalli JD, Orci L, Montesano R. Biphasic effect of transforming growth factor-beta 1 on in vitro angiogenesis. Exp Cell Res 1993; 204(2):356-63
69. Hu J, Srivastava K, Wieland M, et al. Endothelial cell-derived angiopoietin- 2 controls liver regeneration as a spatiotemporal rheostat. Science 2014; 343(6169):416-19
70. Oe S, Lemmer ER, Conner EA, et al. Intact signaling by transforming growth factor beta is not required for termination of liver regeneration in mice. Hepatology 2004; 40(5):1098-105
71. 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(14):5126-30
72. Gallai M, Sebestyen A, Nagy P, et al. Proteoglycan gene expression in rat liver after partial hepatectomy. Biochem Biophys Res Commun 1996;228(3):690-4
73. Block GD, Locker J, Bowen WC, et al. Population expansion, clonal growth, and specific differentiation patterns in primary cultures of hepatocytes induced by HGF/SF, EGF and TGF alpha in a chemically defined (HGM) medium. J Cell Biol 1996; 132(6):1133-49
74. Gkretsi V, Apte U, Mars WM, et al. Liver-specific ablation of integrin-linked kinase in mice results in abnormal histology, enhanced cell proliferation, and hepatomegaly. Hepatology 2008;48(6): 1932-41
75. Apte U, Gkretsi V, Bowen WC, et al. Enhanced liver regeneration following changes induced by hepatocyte-specific genetic ablation of integrin-linked kinase. Hepatology 2009;50(3):844-51
76. Donthamsetty S, Bhave VS, Kliment CS, et al. Excessive hepatomegaly of mice with hepatocyte-targeted elimination of integrin linked kinase following treatment with 1,4-bis [2-(3,5-dichaloropyridyloxy)] benzene. Hepatology 2011;53(2):587-95
77. Donthamsetty S, Bhave VS, Mars WM, et al. Role of PINCH and its partner tumor suppressor Rsu-1 in regulating liver size and tumorigenesis. PLoS One 2013;8(9):e74625
78. Luo JH, Ren B, Keryanov S, et al. Transcriptomic and genomic analysis of human hepatocellular carcinomas and hepatoblastomas. Hepatology 2006;44(4): 1012-24
79. Filmus J, Capurro M. Glypican-3 and alphafetoprotein as diagnostic tests for hepatocellular carcinoma. Mol Diagn 2004; 8(4):207-12
80. Pilia G, Hughes-Benzie RM, MacKenzie A, et al. Mutations in GPC3, a glypican gene, cause the Simpson-Golabi-Behmel overgrowth syndrome. Nat Genet 1996; 12(3):241-7
81. Capurro MI, Xu P, Shi W, et al. Glypican-3 inhibits Hedgehog signaling during development by competing with patched for Hedgehog binding. Dev Cell 2008;14(5):700-11
82. Liu B, Paranjpe S, Bowen WC, et al. Investigation of the role of glypican 3 in liver regeneration and hepatocyte proliferation. Am J Pathol 2009;175(2): 717-24
83. Brazzoli M, Bianchi A, Filippini S, et al. CD81 is a central regulator of cellular events required for hepatitis C virus infection of human hepatocytes. J Virol 2008;82(17):8316-29
84. Liu B, Bell AW, Paranjpe S, et al. Suppression of liver regeneration and hepatocyte proliferation in hepatocyte-targeted glypican 3 transgenic mice. Hepatology 2010;52(3):1060-7
85. Papp V, Dezso K, Laszlo V, et al. Architectural changes during regenerative and ontogenic liver growth in the rat. Liver Transpl 2009;15(2):177-83
86. Jaeschke H, Williams CD, Ramachandran A, Bajt ML. Acetaminophen hepatotoxicity and repair: the role of sterile inflammation and innate immunity. Liver Int 2012;32(1): 8-20
87. Ware AJ, Eigenbrodt EH, Shorey J, Combes B. Viral hepatitis complicating the Dubin-Johnson syndrome. Gastroenterology 1972;63(2):331-9
88. Nagy P, Bisgaard HC, Thorgeirsson SS. Expression of hepatic transcription factors during liver development and oval cell differentiation. J Cell Biol 1994;126(1): 223-33
89. Bisgaard HC, Nagy P, Santoni-Rugiu E, Thorgeirsson SS. Proliferation, apoptosis, and induction of hepatic transcription factors are characteristics of the early response of biliary epithelial (oval) cells to chemical carcinogens. Hepatology 1996; 23(1):62-70
90. Huch M, Dorrell C, Boj SF, et al. In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration. Nature 2013;494(7436):247-50
91. Jakubowski A, Ambrose C, Parr M, et al. TWEAK induces liver progenitor cell proliferation. J Clin Invest 2005;115(9): 2330-40
92. Hu Z, Evarts RP, Fujio K, et al. Expression of transforming growth factor alpha/ epidermal growth factor receptor, hepatocyte growth factor/c-met and acidic fibroblast growth factor/fibroblast growth factor receptors during hepatocarcinogenesis. Carcinogenesis 1996;17(5):931-8
93. Evarts RP, Hu Z, Fujio K, et al. Activation of hepatic stem cell compartment in the rat: role of transforming growth factor alpha, hepatocyte growth factor, and acidic fibroblast growth factor in early proliferation. Cell Growth Differ 1993;4(7): 555-61
94. Isse K, Lesniak A, Grama K, et al. Preexisting epithelial diversity in normal human livers: a tissue-tethered cytometric analysis in portal/periportal epithelial cells. Hepatology 2013;57(4):1632-43
95. Clotman F, Jacquemin P, Plumb-Rudewiez N, et al. Control of liver cell fate decision by a gradient of TGF beta signaling modulated by Onecut transcription factors. Genes Dev 2005; 19(16):1849-54
96. Carpentier R, Suner RE, van Hul N, et al. Embryonic ductal plate cells give rise to cholangiocytes, periportal hepatocytes, and adult liver progenitor cells. Gastroenterology 2011;141(4):1432-8.e1431-4
97. Desmet VJ. Congenital diseases of intrahepatic bile ducts: variations on the theme "ductal plate malformation". Hepatology 1992;16(4): 1069-83
98. Roskams T, De Vos R, van den Oord JJ, Desmet V. Cells with neuroendocrine features in regenerating human liver. APMIS Suppl 1991;23:32-9
99. Desmet V, Roskams T, Van Eyken P. Ductular reaction in the liver. Pathol Res Pract 1995;191(6):513-24