Liver regeneration: Focus on cell types and topographic differences

European Surgical Research

Volumn 44, Issue 1, 2010, Pages 1-12

  Kandilis, Apostolos N ^a,b   Koskinas, John ^b   Tiniakos, Dina G ^b   Nikiteas, Nikolaos ^b   Perrea, Despina N ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b UNIVERSITY OF ATHENS   (Greece)

Author keywords

Intralobular; Liver regeneration; Partial hepatectomy; Pericentral; Periportal

Indexed keywords

BETA GALACTOSIDASE; CARBON TETRACHLORIDE; COLLAGEN TYPE 1; COLLAGEN TYPE 3; COLLAGEN TYPE 4; COLLAGEN TYPE 5; CYCLIN DEPENDENT KINASE INHIBITOR; CYTOKINE; DEXAMETHASONE; DIPIN; DNA; EPIDERMAL GROWTH FACTOR; FIBRONECTIN; GALACTOSAMINE; GELATINASE B; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LAMININ; MATRIX METALLOPROTEINASE; N (2 FLUORENYL)ACETAMIDE; PARACETAMOL; PLASMINOGEN ACTIVATOR INHIBITOR; PROTEIN P27; PROTEINASE; PROTEOGLYCAN; SCATTER FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING 3; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA1;

CALCIUM SIGNALING; CELL CYCLE; CELL PROLIFERATION; CELL TYPE; DNA SYNTHESIS; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; HUMAN; ITO CELL; KUPFFER CELL; LIVER; LIVER DISEASE; LIVER FAILURE; LIVER INJURY; LIVER REGENERATION; LIVER RESECTION; LIVER SINUSOID; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; REVIEW; STEM CELL;

ANIMALS; HEPATECTOMY; LIVER; LIVER REGENERATION;

EID: 70350401899     PISSN: 0014312X     EISSN: None     Source Type: Journal    
DOI: 10.1159/000252770     Document Type: Review

References (84)

1. Michalopoulos GK, DeFrances MC: Liver regeneration. Science 1997; 276: 60-66.
2. Taub R: Liver regeneration: from myth to mechanism. Nat Rev Mol Cell Biol 2004; 5: 836-847.
3. Fausto N, Campbell JS, Riehle KJ: Liver regeneration. Hepatology 2006; 43(suppl 1):45-53.
4. Michalopoulos GK: Liver regeneration. J Cell Physiol 2007; 213: 286-300.
5. Malik R, Selden C, Hodgson H: The role of non-parenchymal cells in liver growth. Semin Cell Dev Biol 2002; 13: 425-431.
6. Burt AD, Portmann BC, Ferrell LD (eds): MacSween's Pathology of the Liver, ed 5. London, Churchill Livingstone, 2006.
7. Palmes D, Spiegel HU: Animal models of liver regeneration. Biomaterials 2004; 25: 1601-1611.
8. Fausto N, Campbell JS: The role of hepatocytes and oval cells in liver regeneration and repopulation. Mech Develop 2003; 120: 117-130.
9. Fausto N: Liver regeneration and repair: hepatocytes, progenitor cells and stem cells. Hepatology 2004; 39: 1478-1487.
10. Nagy P, Teramoto T, Factor VM, Sanchez A, Schnur J, Paku S, et al: Reconstitution of liver mass via cellular hypertrophy in the rat. Hepatology 2001; 33: 339-345.
11. Higgins GM, Anderson RM: Experimental pathology of the liver. I. Restoration of the liver of the white rat following partial surgical removal. Arch Pathol 1931; 12: 186-202.
12. Fausto N, Riehle KJ: Mechanisms of liver regeneration and their clinical implications. J Hepatobiliary Pancreat Surg 2005; 12: 181-189.
13. Koniaris, LG, McKillop IA, Schwartz, SI, Zimmers TA: Liver regeneration. J Amer Coll Surg 2003; 197: 634-659.
14. Iwai M, Cui TX, Kitamura H, Saito M, Shimazu T: Increased secretion of tumor necrosis factor and interleukin 6 from isolated, perfused liver of rats after partial hepatectomy. Cytokine 2001; 13: 60-64.
15. Nagata Y, Tanaka N, Orita K: Endotoxin-induced liver injury after extended hepatectomy and the role of Kupffer cells in the rat. Surg Today 2004; 24: 441-448.
16. Cornell RP, Lilijequist BL, Bartizal KF: Depressed liver regeneration after partial hepatectomy in germ-free athymic and lipopolysaccharide- resistant mice. Hepatology 1990; 11: 916-922.
17. Strey CW, Markiewski M, Mastellos D, Tudoran R, Spruce LA, Greenbaum LE, et al: The proinflammatory mediators C3a and C5a are essential for liver regeneration. J Exp Med 2003; 198: 913-923.
18. Selzner N, Selzner M, Odermatt B, Tia Y, van Rooijen N, Clavein PA: ICAM-1 triggers liver regeneration through leukocyte recruitment and Kupffer cell-dependent release of TNF/IL-6 in mice. Gastroenterology 2003; 124: 692-700.
19. Mead JE, Fausto N: Transforming growth factor may be a physiological regulator of liver regeneration by means of an autocrine mechanism. Proc Natl Acad Sci USA 1989; 86: 1558-1562.
20. Noguchi S, Ohba Y, Oka T: Influence of epidermal growth factor on liver regeneration after partial hepatectomy in mice. J Endocrinol 1991; 128: 425-431.
21. Jones DE Jr, Tran-Patterson R, Cui DM, Davin D, Estell KP, Miller DM: Epidermal growth factor secreted from the salivary gland is necessary for liver regeneration. Am J Physiol Gastrointest Liver Physiol 1995; 268: 872-878.
22. Steer CJ: Liver regeneration. FASEB J 1995; 9: 1396-1400.
23. Grisham JW: A morphologic study of deoxyribonucleic acid synthesis and cell proliferation in regenerating rat liver: autoradiography with thymidine-H. Cancer Res 1962; 22: 842-849.
24. Rabes HM, Wirsching R, Tuczek HV, Iseler G: Analysis of cell cycle compartments of hepatocytes after partial hepatectomy. Cell Tissue Kinet 1976; 9: 517-532.
25. Baratta B, Rizzoli R, Galliani I, Vitale M, Rizzi E, Matteucci A, et al: Early events of liver regeneration in rats: a multiparametric analysis. Histochem Cell Biol 1996; 105: 61-69.
26. Ohtake Y, Maruko A, Kojima S, Ono T, Nagashima T, Fukumoto M, et al: Zonal differences in DNA synthesis and in transglutaminase activity between perivenous versus periportal regions of regenerating rat liver. Biol Pharm Bull 2004; 27: 1758-1762.
27. Ohtake Y, Maruko A, Abe S, Nagashima T, Fukumoto M, Ohkubo Y: Involvement of retinoic acid-induced transglutaminase activity in zonal differences of hepatocyte proliferation after partial hepatectomy. J Gastroentrol Hepatol 2006; 21: 1726-1730.
28. Grisham JW: Migration of hepatocytes along hepatic plates and stem cell-fed hepatocyte lineages. Am J Pathol 1994; 144: 849-854.
29. Zajicek G, Oren R, Weinreb M Jr: The streaming liver. Liver 1985; 5: 293-300.
30. Zajicek G, Arber N, Schwartz-Arad D: Streaming liver. VIII. Cell production rates following partial hepatectomy. Liver 1991; 11: 347-351.
31. Bralet MP, Branchereau S, Brechot C, Ferry N: Cell lineage study in the liver using retroviral mediated gene transfer. Am J Pathol 1994; 144: 896-905.
32. Bedossa P, Paradis V: Liver extracellular matrix in health and disease. J Pathol 2003; 200: 504-515.
33. Mars WM, Liu ML, Kitson RP, Goldfarb RH, Gabauer MK, Michalopoulos GK: Immediate early detection of urokinase receptor after partial hepatectomy and its implications for initiation of liver regeneration. Hepatology 1995; 21: 1695-1701.
34. Woessner JF Jr: Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J 1991; 5: 2145-2154.
35. Springman EB, Angleton EL, Birkedal-Hansen H, Van Wart HE: Multiple modes of activation of latent human fibroblast collagenase: evidence for the role of a Cys73 active-site zinc complex in latency and a 'cysteine switch' mechanism for activation. Proc Natl Acad Sci USA 1990; 87: 364-368.
36. Werb Z, Mainardi CL, Vater CA, Harris ED Jr: Endogenous activation of latent collagenase by rheumatoid synovial cells: evidence for a role of plasminogen activator. N Engl J Med 1977; 296: 1017-1023.
37. Birkedal-Hansen H, Moore WGI, Bodden MK, Windsor LJ, Birkedal-Hansen B, De- Carlo A, et al: Matrix metalloproteinases: a review. Crit Rev Oral Biol Med 1993; 4: 197-250.
38. Martinez-Hernandez A, Amenta PS: The extracellular matrix in hepatic regeneration. FASEB J 1995; 9: 1401-1410.
39. Kim TH, Mars WM, Stolz DB, Petersen BE, Michalopoulos GK: Extracellular matrix remodeling at the early stages of liver regeneration in the rat. Hepatology 1997; 26: 896-904.
40. Budny T, Palmes D, Stratmann U, Mini E, Herbst H, Spiegel HU: Morphologic features in the regenerating liver - a comparative intravital, light microscopical and ultrastructural analysis with focus on hepatic stellate cells. Virchow Arch 2007; 451: 781-791.
41. Zimmermann A: Regulation of liver regeneration. Nephrol Dial Transplant 2004; 19 (suppl 4):6-10.
42. Ross MA, Sander CM, Kleeb TB, Watkins SC, Stolz DB: Spatiotemporal expression of angiogenesis growth factor receptors during the revascularization of regenerating rat liver. Hepatology 2001; 34: 1135-1148.
43. Drixler TA, Vogten MJ, Ritchie ED, van Vroonhoven TJMV, Gebbink MFBG, Voest EE, et al: Liver regeneration is an angiogenesis- associated phenomenon. Ann Surg 2002; 236: 703-712.
44. Shimizu H, Miyazaki M, Wakabayashi Y, Mitsuhashi N, Kato A, Ito H, et al: Vascular endothelial growth factor and angiopoietins regulate sinusoidal regeneration and remodeling after partial hepatectomy in rats. World J Gastroenterol 2005; 11: 7254-7260.
45. Higashi N, Senoo H: Distribution of vitamin A-storing lipid droplets in hepatic stellate cells in liver lobules: a comparative study. Anat Rec A Discov Mol Cell Evol Biol 2003; 271: 240-248.
46. Sato M, Suzuki S, Senoo H: Hepatic stellate cells: unique characteristics in cell biology and phenotype. Cell Struct Funct 2003; 28: 105-112.
47. Mabuchi A, Mullaney I, Sheard P, Hessian P, Zimmermann A, Senoo H, et al: Role of hepatic stellate cells in the early phase of liver regeneration in rats: formation of tight adhesion to parenchymal cells. Comp Hepatol 2004; 3(suppl 1):29.
48. Higashi N, Sato M, Kojima N, Irie T, Kawamura K, Mabuchi A, et al: Vitamin A storage in hepatic stellate cells in the regenerating rat liver: with special reference to zonal heterogeneity. Anat Rec A Discov Mol Cell Evol Biol 2005; 286: 899-907.
49. Bilzer M, Roggel F, Gerbes AL: Role of Kupffer cells in host defense and liver disease. Liver Int 2006; 26: 1175-1186.
50. Sleyster EC, Knook DL: Relation between localization and function of rat liver Kupffer cells. Lab Invest 1982; 47: 484-490.
51. Rai RM, Yang SQ, McClain C, Karp CL, Klein AS, Diehl AM: Kupffer cell depletion by gadolinium chloride enhances liver regeneration after partial hepatectomy in rats. Am J Physiol Gastrointest Liver Physiol 1996; 270: 909-918.
52. Rai RM, Loffreda S, Karp CL, Yang SQ, Lin HZ, Diehl AM: Kupffer cell depletion abolishes induction of interleukin-10 and permits sustained overexpression of tumor necrosis factor messenger RNA in the regenerating rat liver. Hepatology 1997; 25: 889-895
53. Boulton RA, Alison MR, Golding M, Selden C, Hodgson HJF: Augmentation of the early phase of liver regeneration after 70% partial hepatectomy in rats following selective Kupffer cell depletion. J Hepatol 1998; 29: 271-280.
54. Takeishi T, Hirano K, Kobayashi T, Hasegawa G, Hatakeyama K, Naito M: The role of Kupffer cells in liver regeneration. Arch Histol Cytol 1999; 62: 413-422.
55. Häussinger D: Nitrogen metabolism in liver: structural and functional organization and physiological relevance. Biochem J 1990; 267: 281-290.
56. Jungermann K, Kietzmann T: Oxygen: modulator of metabolic zonation and disease of the liver. Hepatology 2000; 31: 255-260.
57. Gebhardt R: Metabolic zonation of the liver: regulation and implications for liver function. Pharmacol Ther 1992; 53: 275-354.
58. Katz NR: Metabolic heterogeneity of hepatocytes across the liver acinus. J Nutr 1992; 122(suppl 3):843-849.
59. Brinkmann A, Katz N, Sasse D, Jungermann K: Increase of the gluconeogenic and decrease of the glycolytic capacity of rat liver with a change of the metabolic zonation after partial hepatectomy. Hoppe Seylers Z Physiol Chem 1978; 359: 1561-1571.
60. Sasse D, Katz N, Jungermann K: Functional heterogeneity of rat liver parenchyma and of isolated hepatocytes. FEBS Lett 1975; 57: 83-88.
61. Andersen B, Zierz S, Jungermann K: Alteration in zonation of succinate dehydrogenase, phosphoenolpyruvate carboxykinase and glucose-6-phosphatase in regenerating rat liver. Histochemistry 1984; 80: 97-101.
62. Cheng HC, Yang CM, Shiao M: Zonation of cholesterol and glycerolipid synthesis in regenerating rat livers. Hepatology 1993; 17: 280-286.
63. Van Noorden CJF, Vogels IMC, Houtkooper JM: Cytophotometric analysis of alkaline phosphatase and 5-nucleotidase activity in regenerating rat liver after partial hepatectomy. Cell Biochem Funct 1988; 6: 53-60.
64. Gebhardt R: Altered acinar distribution of glutamine synthetase and different growth response of cultured enzyme-positive and -negative hepatocytes after partial hepatectomy. Cancer Res 1990; 50: 4407-4410.
65. Gebhardt R, Baldysiak-Figiel A, Krügel V, Ueberham E, Gaunitz F: Hepatocellular expression of glutamine synthetase: an indicator of morphogen actions as master regulators of zonation in adult liver. Prog Histochem Cytochem 2007; 41: 201-266.
66. Wack KE, Ross MA, Zegarra V, Sycko LR, Watkins SC, Stolz DB: Sinusoidal ultrastructure evaluated during the revascularization of regenerating rat liver. Hepatology 2001; 33: 363-378.
67. Braet F, Shleper M, Paizi M, Brodsky S, Kopeiko N, Resnick N, et al: Liver sinusoidal endothelial cell modulation upon resection and shear stress in vitro. Comp Hepatol 2004; 3: 7.
68. Gertsch P, Stipa F, Ho J, Yuen ST, Luk I, Lauder IJ: Changes in hepatic portal resistance and in liver morphology during regeneration: in vitro study in rats. Eur J Surg 1997; 163: 297-304.
69. Taniguchi E, Sakisaka S, Matsuo K, Tanikawa K, Sata M: Expression and role of vascular endothelial growth factor in liver regeneration after partial hepatectomy in rats. J Histochem Cytochem 2001; 49: 121-129.
70. Maeno H, Ono T, Dhar DK, Sato T, Yamanoi A, Nagasue N: Expression of hypoxia-inducible factor-1 during liver regeneration induced by partial hepatectomy in rats. Liver Int 2005; 25: 1002-1009.
71. 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: 75-82.
72. Rudolph KL, Trautwein C, Kubicka S, Rakemann T, Bahr MJ, Sedlaczek N, et al: Differential regulation of extracellular matrix synthesis during liver regeneration after partial hepatectomy in rats. Hepatology 1999; 30: 1159-1166.
73. Baier P, Wolf-Vorbeck G, Hempel S, Hopt UT, von Dobschuetz E: Effect of liver regeneration after partial hepatectomy and ischemia- reperfusion on expression of growth factor receptors. World J Gastroenterol 2006; 12: 3835-3840.
74. Jirtle RL, Carr BL, Scott CD: Modulation of insulin-like growth factor-II/mannose 6- phosphate receptors and transforming growth factor 1 during liver regeneration. J Biol Chem 1991; 266: 22444-22450.
75. 2+ signaling during liver regeneration: an interplay stimulating liver growth and bile flow. FASEB J 2003; 17: 1901-1903.
76. Nicou A, Serriére V, Hilly M, Prigent S, Combettes L, Guillon G, et al: Remodelling of calcium signalling during liver regeneration in the rat. J Hepatol 2007; 46: 247-256.
77. Guerrieri F, Pellecchia G, Lopriore B, Papa S, Liquori GE, Ferri D, et al: Changes in ultrastructure and the occurrence of permeability transition in mitochondria during rat liver regeneration. Eur J Biochem 2002; 269: 3304-3312.
78. Ferri D, Moro L, Mastrodonato M, Capuano F, Marra E, Liquori GE, et al: Ultrastructural zonal heterogeneity of hepatocytes and mitochondria within the hepatic acinus during liver regeneration after partial hepatectomy. Biol Cell 2005; 97: 277-288.
79. Simpson GEC, Finckh ES: The pattern of regeneration of rat liver after repeated partial hepatectomies. J Path Bact 1963; 86: 361-370.
80. Yashina IN: Formation of hepatic lobules in the regenerating liver. Byull Eksperiment Biol Med 1970; 70: 95-98.
81. Wagenaar GTM, Chamuleau RAFM, Pool CW, de Haan JG, Maas MAW, Korfage HAM, et al: Distribution and activity of glutamine synthase and carbamoylphosphate synthase upon enlargement of the liver lobule by repeated partial hepatectomies. J Hepatol 1993; 17: 397-407.
82. Iatropoulos MJ: Cytoarchitecture of rat liver during compensatory growth. Anat Rec 1970; 169: 509-514.
83. Sidorova VF: The structure of the regenerating liver in rats. Byul Eksptl Biol Med 1959; 48: 1020-1024.
84. Diehl AM: Liver regeneration. Front Biosci 2002; 7: 301-1134