Hepatocyte transplantation in animal models

Liver Transplantation

Volumn 15, Issue 1, 2009, Pages 7-14

  Weber, Anne ^a   Groyer Picard, Marie Thérèse ^a   Franco, Dominique ^a,b   Dagher, Ibrahim ^a,b  

^a INSERM   (France)

^b HÔPITAL ANTOINE BÉCLÈRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; CRE RECOMBINASE; CYTOCHROME P450; INTERLEUKIN 2 RECEPTOR GAMMA; RETROVIRUS VECTOR;

APOPTOSIS; CELL ADHESION; CELL IMMORTALIZATION; CELL SURVIVAL; CELL VIABILITY; CRIGLER NAJJAR SYNDROME; CRYOPRESERVATION; ENGRAFTMENT; EXPERIMENTAL TRANSPLANTATION; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSDUCTION; HEPATOCYTE TRANSPLANTATION; ISOLATION PROCEDURE; LIVER CELL CULTURE; LIVER DISEASE; LIVER GRAFT REJECTION; LIVER REGENERATION; NONHUMAN; PORTAL VEIN OBSTRUCTION; PRIORITY JOURNAL; REVIEW; SAFETY; SIMIAN VIRUS 40; THAWING; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; CELL TRANSPLANTATION; CRIGLER-NAJJAR SYNDROME; DISEASE MODELS, ANIMAL; HEPATOCYTES; HUMANS; LIVER; LIVER REGENERATION; MICE; RATS; STEM CELLS; SYNDROME; TISSUE ENGINEERING; TISSUE THERAPY;

EID: 64049113151     PISSN: 15276465     EISSN: 15276473     Source Type: Journal    
DOI: 10.1002/lt.21670     Document Type: Review

References (82)

1. Berry MN, Friend DS. High-yield preparation of isolated rat liver parenchymal cells: a biochemical and fine structural study. J Cell Biol 1969;43:506-520.
2. Seglen PO. Preparation of isolated rat liver cells. Methods Cell Biol 1976;13:29-83.
3. Groth CG, Arborgh B, Bjorken C, Sundberg B, Lundgren G. Correction of hyperbilirubinemia in the glucuronyl-transferase-deficient rat by intraportal hepatocyte transplantation. Transplant Proc 1977;9:313-316.
4. Minato M, Houssin D, Demma I, Morin J, Gigou M, Szekely AM, et al. Transplantation of hepatocytes for treatment of surgically induced acute hepatic failure in the rat. Eur Surg Res 1984;16:162-169.
5. Sutherland DE, Numata M, Matas AJ, Simmons RL, Najarian JS. Hepatocellular transplantation in acute liver failure. Surgery 1977;82:124-132.
6. Rajvanshi P, Kerr A, Bhargava KK, Burk RD, Gupta S. Studies of liver repopulation using the dipeptidyl peptidase IV-deficient rat and other rodent recipients: cell size and structure relationships regulate capacity for increased transplanted hepatocyte mass in the liver lobule. Hepatology 1996;23:482-496.
7. Rajvanshi P, Kerr A, Bhargava KK, Burk RD, Gupta S. Efficacy and safety of repeated hepatocyte transplantation for significant liver repopulation in rodents. Gastroenterology 1996;111:1092-1102.
8. Joseph B, Malhi H, Bhargava KK, Palestro CJ, McCuskey RS, Gupta S. Kupffer cells participate in early clearance of syngeneic hepatocytes transplanted in the rat liver. Gastroenterology 2002;123:1677-1685.
9. Gupta S, Rajvanshi P, Sokhi R, Slehria S, Yam A, Kerr A, et al. Entry and integration of transplanted hepatocytes in rat liver plates occur by disruption of hepatic sinusoidal endothelium. Hepatology 1999;29:509-519.
10. Joseph B, Kumaran V, Berishvili E, Bhargava KK, Palestro CJ, Gupta S. Monocrotaline promotes transplanted cell engraftment and advances liver repopulation in rats via liver conditioning. Hepatology 2006;44:1411-1420.
11. Slehria S, Rajvanshi P, Ito Y, Sokhi RP, Bhargava KK, Palestro CJ, et al. Hepatic sinusoidal vasodilators improve transplanted cell engraftment and ameliorate microcirculatory perturbations in the liver. Hepatology 2002;35: 1320-1328.
12. Allen KJ, Soriano HE. Liver cell transplantation: the road to clinical application. J Lab Clin Med 2001;138:298-312.
13. Grompe M. Principles of therapeutic liver repopulation. J Inherit Metab Dis 2006;29:421-425.
14. Grossman M, Raper SE, Kozarsky K, Stein EA, Engelhardt JF, Muller D, et al. Successful ex vivo gene therapy directed to liver in a patient with familial hypercholesterolaemia. Nat Genet 1994;6:335-341.
15. Fisher RA, Strom SC. Human hepatocyte transplantation: worldwide results. Transplantation 2006;82:441-449.
16. Stephenne X, Najimi M, Sibille C, Nassogne MC, Smets F, Sokal EM. Sustained engraftment and tissue enzyme activity after liver cell transplantation for argininosuccinate lyase deficiency. Gastroenterology 2006;130:1317-1323.
17. Benten D, Kumaran V, Joseph B, Schattenberg J, Popov Y, Schuppan D, et al. Hepatocyte transplantation activates hepatic stellate cells with beneficial modulation of cell engraftment in the rat. Hepatology 2005;42:1072-1081.
18. Kumaran V, Joseph B, Benten D, Gupta S. Integrin and extracellular matrix interactions regulate engraftment of transplanted hepatocytes in the rat liver. Gastroenterology 2005;129:1643-1653.
19. Stephenne X, Vosters O, Najimi M, Beuneu C, Dung KN, Wijns W, et al. Tissue factor-dependent procoagulant activity of isolated human hepatocytes: relevance to liver cell transplantation. Liver Transpl 2007;13:599-606.
20. Boudreau N, Sympson CJ, Werb Z, Bissell MJ. Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 1995;267:891-893.
21. Frisch SM, Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 1994;124:619-626.
22. Frisch SM, Ruoslahti E. Integrins and anoikis. Curr Opin Cell Biol 1997;9:701-706.
23. Rivera DJ, Gores GJ, Misra SP, Hardin JA, Nyberg SL. Apoptosis by gel-entrapped hepatocytes in a bioartificial liver. Transplant Proc 1999;31:671-673.
24. Nishitai R, Koch CA, Ogata K, Knudsen BE, Plummer TB, Butters KA, et al. Toward the survival and function of xenogeneic hepatocyte grafts. Liver Transpl 2005;11:39-50.
25. Fox IJ, Chowdhury JR, Kaufman SS, Goertzen TC, Chowdhury NR, Warkentin PI, et al. Treatment of the Crigler-Najjar syndrome type I with hepatocyte transplantation. N Engl J Med 1998;338:1422-1426.
26. Hughes RD, Mitry RR, Dhawan A. Hepatocyte transplantation in the treatment of liver diseases - future seems bright after all. Pediatr Transplant 2008;12:4-5.
27. Terry C, Dhawan A, Mitry RR, Lehec SC, Hughes RD. Preincubation of rat and human hepatocytes with cytoprotectants prior to cryopreservation can improve viability and function upon thawing. Liver Transpl 2006;12:165-177.
28. Katenz E, Vondran FW, Schwartlander R, Pless G, Gong X, Cheng X, et al. Cryopreservation of primary human hepatocytes: the benefit of trehalose as an additional cryoprotective agent. Liver Transpl 2007;13:38-45.
29. Terry C, Dhawan A, Mitry RR, Hughes RD. Cryopreservation of isolated human hepatocytes for transplantation: state of the art. Cryobiology 2006;53:149-159.
30. Kunieda T, Maruyama M, Okitsu T, Shibata N, Takesue M, Totsugawa T, et al. Cryopreservation of primarily isolated porcine hepatocytes with UW solution. Cell Transplant 2003;12:607-616.
31. Yagi T, Hardin JA, Valenzuela YM, Miyoshi H, Gores GJ, Nyberg SL. Caspase inhibition reduces apoptotic death of cryopreserved porcine hepatocytes. Hepatology 2001;33: 1432-1440.
32. Parouchev A, Nguyen TH, Dagher I, Mainot S, Groyer-Picard MT, Branger J, et al. Efficient ex vivo gene transfer into non-human primate hepatocytes using HIV-1 derived lentiviral vectors. J Hepatol 2006;45:99-107.
33. Mai G, Nguyen TH, Morel P, Mei J, Andres A, Bosco D, et al. Treatment of fulminant liver failure by transplantation of microencapsulated primary or immortalized xenogeneic hepatocytes. Xenotransplantation 2005;12:457-464.
34. Liu ZC, Chang TM. Coencapsulation of hepatocytes and bone marrow cells: in vitro and in vivo studies. Biotechnol Annu Rev 2006;12:137-151.
35. Liu ZC, Chang TM. Transdifferentiation of bioencapsulated bone marrow cells into hepatocyte-like cells in the 90% hepatectomized rat model. Liver Transpl 2006;12: 566-572.
36. Aoki T, Jin Z, Nishino N, Kato H, Shimizu Y, Niiya T, et al. Intrasplenic transplantation of encapsulated hepatocytes decreases mortality and improves liver functions in fulminant hepatic failure from 90% partial hepatectomy in rats. Transplantation 2005;79:783-790.
37. Desille M, Mahler S, Seguin P, Malledant Y, Fremond B, Sebille V, et al. Reduced encephalopathy in pigs with ischemia-induced acute hepatic failure treated with a bioartificial liver containing alginate-entrapped hepatocytes. Crit Care Med 2002;30:658-663.
38. Nyberg SL, Yagi T, Matsushita T, Hardin J, Grande JP, Gibson LE, et al. Membrane barrier of a porcine hepatocyte bioartificial liver. Liver Transpl 2003;9:298-305.
39. Nagata H, Nishitai R, Shirota C, Zhang JL, Koch CA, Cai J, et al. Prolonged survival of porcine hepatocytes in cynomolgus monkeys. Gastroenterology 2007;132:321-329.
40. Cai J, Ito M, Nagata H, Westerman KA, Lafleur D, Chowdhury JR, et al. Treatment of liver failure in rats with end-stage cirrhosis by transplantation of immortalized hepatocytes. Hepatology 2002;36:386-394.
41. Smalley M, Leiper K, Tootle R, McCloskey P, O'Hare MJ, Hodgson H. Immortalization of human hepatocytes by temperature-sensitive SV40 large-T antigen. In Vitro Cell Dev Biol Anim 2001;37:166-168.
42. Westerman KA, Leboulch P. Reversible immortalization of mammalian cells mediated by retroviral transfer and sitespecific recombination. Proc Natl Acad Sci U S A 1996;93: 8971-8976.
43. Cai J, Ito M, Westerman KA, Kobayashi N, Leboulch P, Fox IJ. Construction of a non-tumorigenic rat hepatocyte cell line for transplantation: reversal of hepatocyte immortalization by site-specific excision of the SV40 T antigen. J Hepatol 2000;33:701-708.
44. Kobayashi N, Fujiwara T, Westerman KA, Inoue Y, Sakaguchi M, Noguchi H, et al. Prevention of acute liver failure in rats with reversibly immortalized human hepatocytes. Science 2000;287:1258-1262.
45. Nguyen TH, Mai G, Villiger P, Oberholzer J, Salmon P, Morel P, et al. Treatment of acetaminophen-induced acute liver failure in the mouse with conditionally immortalized human hepatocytes. J Hepatol 2005;43:1031-1037.
46. Allain JE, Dagher I, Mahieu-Caputo D, Loux N, Andreoletti M, Westerman K, et al. Immortalization of a primate bipotent epithelial liver stem cell. Proc Natl Acad Sci U S A 2002;99:3639-3644.
47. Delgado JP, Parouchev A, Allain JE, Pennarun G, Gauthier LR, Dutrillaux AM, et al. Long-term controlled immortalization of a primate hepatic progenitor cell line after simian virus 40 T-antigen gene transfer. Oncogene 2005; 24:541-551.
48. Totsugawa T, Yong C, Rivas-Carrillo JD, Soto-Gutierrez A, Navarro-Alvarez N, Noguchi H, et al. Survival of liver failure pigs by transplantation of reversibly immortalized human hepatocytes with tamoxifen-mediated self-recombination. J Hepatol 2007;47:74-82.
49. Strom SC, Chowdhury JR, Fox IJ. Hepatocyte transplantation for the treatment of human disease. Semin Liver Dis 1999;19:39-48.
50. Uyama S, Kaufmann PM, Kneser U, Fiegel HC, Pollok JM, Kluth D, et al. Hepatocyte transplantation using biodegradable matrices in ascorbic acid-deficient rats: comparison with heterotopically transplanted liver grafts. Transplantation 2001;71:1226-1231.
51. Nagata H, Ito M, Shirota C, Edge A, McCowan TC, Fox IJ. Route of hepatocyte delivery affects hepatocyte engraftment in the spleen. Transplantation 2003;76:732-734.
52. Kobayashi N, Ito M, Nakamura J, Cai J, Gao C, Hammel JM, et al. Hepatocyte transplantation in rats with decompensated cirrhosis. Hepatology 2000;31:851-857.
53. Gupta S, Lee CD, Vemuru RP, Bhargava KK. 111Indium labeling of hepatocytes for analysis of short-term biodistribution of transplanted cells. Hepatology 1994;19:750-757.
54. Rajvanshi P, Fabrega A, Bhargava KK, Kerr A, Pollak R, Blanchard J, et al. Rapid clearance of transplanted hepatocytes from pulmonary capillaries in rats indicates a wide safety margin of liver repopulation and the potential of using surrogate albumin particles for safety analysis. J Hepatol 1999;30:299-310.
55. Benhamouche S, Decaens T, Godard C, Chambrey R, Rickman DS, Moinard C, et al. Apc tumor suppressor gene is the "zonation-keeper" of mouse liver. Dev Cell 2006;10: 759-770.
56. Gupta S, Rajvanshi P, Sokhi RP, Vaidya S, Irani AN, Gorla GR. Position-specific gene expression in the liver lobule is directed by the microenvironment and not by the previous cell differentiation state. J Biol Chem 1999;274:2157-2165.
57. Koenig S, Aurich H, Schneider C, Krause P, Haftendorn R, Becker H, et al. Zonal expression of hepatocytic marker enzymes during liver repopulation. Histochem Cell Biol 2007;128:105-114.
58. Shultz LD, Ishikawa F, Greiner DL. Humanized mice in translationalbiomedicalresearch.NatRevImmunol2007;7: 118-130.
59. DiSanto JP, Muller W, Guy-Grand D, Fischer A, Rajewsky K. Lymphoid development in mice with a targeted deletion of the interleukin 2 receptor gamma chain. Proc Natl Acad Sci U S A 1995;92:377-381.
60. Azuma H, Paulk N, Ranade A, Dorrell C, Al-Dhalimy M, Ellis E, et al. Robust expansion of human hepatocytes in Fah-/-/Rag2-/d/Il2rg-/- mice. Nat Biotechnol 2007; 25:903-910.
61. Meuleman P, Libbrecht L, De Vos R, de Hemptinne B, Gevaert K, Vandekerckhove J, et al. Morphological and biochemical characterization of a human liver in a uPASCID mouse chimera. Hepatology 2005;41:847-856.
62. Tateno C, Yoshizane Y, Saito N, Kataoka M, Utoh R, Yamasaki C, et al. Near completely humanized liver in mice shows human-type metabolic responses to drugs. Am J Pathol 2004;165:901-912.
63. Smets F, Najimi M, Sokal EM. Cell transplantation in the treatment of liver diseases. Pediatr Transplant 2008;12:6-13.
64. Allen KJ, Mifsud NA, Williamson R, Bertolino P, Hardikar W. Cell-mediated rejection results in allograft loss after liver cell transplantation. Liver Transpl 2008;14:688-694.
65. Horne PH, Zimmerer JM, Fisher MG, Lunsford KE, Nadasdy G, Nadasdy T, et al. Critical role of effector macrophages in mediating CD4-dependent alloimmune injury of transplanted liver parenchymal cells. J Immunol 2008; 181:1224-1231.
66. Nguyen TH, Oberholzer J, Birraux J, Majno P, Morel P, Trono D. Highly efficient lentiviral vector-mediated transduction of nondividing, fully reimplantable primary hepatocytes. Mol Ther 2002;6:199-209.
67. Trono D. Lentiviral vectors: turning a deadly foe into a therapeutic agent. Gene Ther 2000;7:20-23.
68. Yuasa T, Yamamoto T, Rivas-Carrillo JD, Chen Y, Navarro-Alvarez N, Soto-Guiterrez A, et al. Laparoscopy-assisted creation of a liver failure model in pigs. Cell Transplant 2008;17:187-193.
69. Malhi H, Joseph B, Schilsky ML, Gupta S. Development of cell therapy strategies to overcome copper toxicity in the LEC rat model of Wilson disease. Regen Med 2008;3:165-173.
70. Koenig S, Krause P, Schmidt TK, Rave-Fraenk M, Rothe H, Hermann RM, et al. Irradiation as preparative regimen for hepatocyte transplantation causes prolonged cell cycle block. Int J Radiat Biol 2008;84:285-298.
71. De Vree JM, Ottenhoff R, Bosma PJ, Smith AJ, Aten J, Oude Elferink RP. Correction of liver disease by hepatocyte transplantation in a mouse model of progressive familial intrahepatic cholestasis. Gastroenterology 2000; 119:1720-1730.
72. Furrer K, Tian Y, Pfammatter T, Jochum W, El-Badry AM, Graf R, et al. Selective portal vein embolization and ligation trigger different regenerative responses in the rat liver. Hepatology 2008;47:1615-1623.
73. Ise N, Sato T, Yasui O, Watanabe G, Koyama K, Terada K, et al. Enhanced proliferation of hepatic progenitor cells in rats after portal branch occlusion. Liver Transpl 2004;10: 748-754.
74. Lorand I, Vons C, Nguyen T, Di Rico V, Coulomb A, Franco D, et al. Portal branch ligation induces efficient retrovirusmediated gene delivery in rat liver. J Gene Med 2004;6: 507-513.
75. Eguchi S, Rozga J, Lebow LT, Chen SC, Wang CC, Rosenthal R, et al. Treatment of hypercholesterolemia in the Watanabe rabbit using allogeneic hepatocellular transplantation under a regeneration stimulus. Transplantation 1996;62:588-593.
76. Andreoletti M, Loux N, Vons C, Nguyen TH, Lorand I, Mahieu D, et al. Engraftment of autologous retrovirally transduced hepatocytes after intraportal transplantation into nonhuman primates: implication for ex vivo gene therapy. Hum Gene Ther 2001;12:169-179.
77. Vons C, Loux N, Simon L, Mahieu-Caputo D, Dagher I, Andreoletti M, et al. Transplantation of hepatocytes in nonhuman primates: a preclinical model for the treatment of hepatic metabolic diseases. Transplantation 2001;72:811-818.
78. Dagher I, Boudechiche L, Branger J, Coulomb-Lhermine A, Parouchev A, Sentilhes L, et al. Efficient hepatocyte engraftment in a nonhuman primate model after partial portal vein embolization. Transplantation 2006;82:1067-1073.
79. Lainas P, Boudechiche L, Osorio A, Coulomb A, Weber A, Pariente D, et al. Liver regeneration and recanalization time course following reversible portal vein embolization. J Hepatol 2008;49:354-362.
80. Chan C, Berthiaume F, Nath BD, Tilles AW, Toner M, Yarmush ML. Hepatic tissue engineering for adjunct and temporary liver support: critical technologies. Liver Transpl 2004;10:1331-1342.
81. Yokoyama T, Ohashi K, Kuge H, Kanehiro H, Iwata H, Yamato M, et al. In vivo engineering of metabolically active hepatic tissues in a neovascularized subcutaneous cavity. Am J Transplant 2006;6:50-59.
82. Ohashi K, Yokoyama T, Yamato M, Kuge H, Kanehiro H, Tsutsumi M, et al. Engineering functional two- and threedimensional liver systems in vivo using hepatic tissue sheets. Nat Med 2007;13:880-885.