Ex vivo liver-directed gene therapy for the treatment of metabolic diseases: Advances in hepatocyte transplantation and retroviral vectors

Current Gene Therapy

Volumn 9, Issue 2, 2009, Pages 136-149

  Nguyen, Tuan Huy ^a   Mainot, Sylvie ^b   Lainas, Panagiotis ^b,c   Groyer Picard, Marie Thérèse ^b   Franco, Dominique ^b,c   Dagher, Ibrahim ^b,c   Weber, Anne ^b  

^a HÔTEL DIEU   (France)

^b INSERM   (France)

^c HÔPITAL ANTOINE BÉCLÈRE   (France)

Author keywords

Animal models; Gene therapy; Lentiviral vectors; Liver disease

Indexed keywords

ALPHA TOCOPHEROL; GANCICLOVIR; GLUCURONOSYLTRANSFERASE 1A1; GREEN FLUORESCENT PROTEIN; LENTIVIRUS VECTOR; PARVOVIRUS VECTOR; RETROVIRUS VECTOR; THYMIDINE KINASE;

APOPTOSIS; ARTIFICIAL EMBOLISM; CELL DIFFERENTIATION; CRYOPRESERVATION; DISEASE MODEL; ENGRAFTMENT; EX VIVO GENE TRANSFER; FAMILIAL HYPERCHOLESTEROLEMIA; GENE EXPRESSION; GENETIC TRANSDUCTION; GRAFT REJECTION; GRAFT SURVIVAL; HEPATITIS VIRUS; HEPATOCYTE TRANSPLANTATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HYPERBILIRUBINEMIA; IMMUNOSUPPRESSIVE TREATMENT; IN VIVO STUDY; LIVER DISEASE; LIVER PARENCHYMA; LIVER REGENERATION; LIVER TRANSPLANTATION; METABOLIC DISORDER; MUTAGENESIS; NONHUMAN; PORTAL VEIN OBSTRUCTION; PRIMATE; REVIEW;

ANIMALS; GENE THERAPY; GENETIC VECTORS; HEPATOCYTES; HUMANS; LIVER; LIVER DISEASES; METABOLIC DISEASES; RETROVIRIDAE;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS 1; LENTIVIRUS; PRIMATES;

EID: 65949115488     PISSN: 15665232     EISSN: None     Source Type: Journal    
DOI: 10.2174/156652309787909481     Document Type: Review

References (145)

1. Rosenberg SA, Aebersold P, Cornetta K, et al. Gene transfer into humans - immunotherapy of patients with advanced melanoma, using tumor-infiltrating lymphocytes modified by retroviral gene transduction. N Engl J Med 1990; 323: 570-78.
2. Groth CG, Arborgh B, Bjorken C, Sundberg B, Lundgren G. Correction of hyperbilirubinemia in the glucuronyltransferase-deficient rat by intraportal hepatocyte transplantation. Transplant Proc 1977; 9: 313-16.
3. Raper SE, Chirmule N, Lee FS, et al. Fatal systemic inflammatory response syndrome in a ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol Genet Metab 2003; 80: 148-58.
4. Manno CS, Arruda VR, Pierce GF, et al. Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat Med 2006; 12: 342-7.
5. Fisher RA, Strom SC. Human hepatocyte transplantation: world-wide results. Transplantation 2006; 82: 441-9.
6. 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: 1317-23.
7. Lee KW, Lee JH, Shin SW, et al. Hepatocyte transplantation for glycogen storage disease type Ib. Cell Transplant 2007; 16: 629-37.
8. 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.
9. Fox IJ, Chowdhury JR, Kaufman SS, et al. Treatment of the Crigler-Najjar syndrome type I with hepatocyte transplantation. N Engl J Med 1998; 338: 1422-6.
10. 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: 688-94.
11. Horne PH, Zimmerer JM, Fisher MG, et al. Critical role of effector macrophages in mediating CD4-dependent alloimmune injury of transplanted liver parenchymal cells. J Immunol 2008; 181: 1224-31.
12. Smets F, Najimi M, Sokal EM. Cell transplantation in the treatment of liver diseases. Pediatr Transplant 2008; 12: 6-13.
13. Puppi J, Tan N, Mitry RR, et al. Hepatocyte transplantation followed by auxiliary liver transplantation--a novel treatment for ornithine transcarbamylase deficiency. Am J Transplant 2008; 8: 452-7.
14. Alison MR, Choong C, Lim S. Application of liver stem cells for cell therapy. Semin Cell Dev Biol 2007; 18: 819-26.
15. Schmelzer E, Zhang L, Bruce A, et al. Human hepatic stem cells from fetal and postnatal donors. J Exp Med 2007; 204: 1973-87.
16. Brulport M, Schormann W, Bauer A, et al. Fate of extrahepatic human stem and precursor cells after transplantation into mouse livers. Hepatology 2007; 46: 861-70.
17. Grossman M, Rader DJ, Muller DWM, et al. A pilot study of ex vivo gene therapy for homozygous familial hypercholesterolemia. Nat Med 1995; 1: 1148-54.
18. Ledley FD, Darlington GJ, Hahn T, Woo SL. Retroviral gene transfer into primary hepatocytes: implications for genetic therapy of liver-specific functions. Proc Natl Acad Sci USA 1987; 84: 5335-9.
19. Roe T, Reynolds TC, Yu G, Brown PO. Integration of murine leukemia virus DNA depends on mitosis. EMBO J 1993; 12: 2099-108.
20. Lorand I, Vons C, Nguyen TH, et al. Portal branch ligation induces efficient retrovirus-mediated gene delivery in rat liver. J Gene Med 2004; 6: 507-13.
21. Grossman M, Raper SE, Kozarsky K, et al. Successful ex vivo gene therapy directed to liver in a patient with familial hypercholesterolaemia. Nat Genet 1994; 6: 335-41.
22. Nguyen TH, Pages JC, Farge D, Briand P, Weber A. Amphotropic retroviral vectors displaying hepatocyte growth factor-envelope fusion proteins improve transduction efficiency of primary hepatocytes. Hum Gene Ther 1998; 9: 2469-79.
23. Solly SK, Nguyen TH, Weber A, Horellou P. Targeting of c-Met and urokinase expressing human glioma cell lines by retrovirus vector displaying single-chain variable fragment antibody. Cancer Biol Ther 2005; 4: 987-92.
24. Cosset FL, Russell SJ. Targeting retrovirus entry. Gene Ther 1996; 3: 946-56.
25. Verhoeyen E, Dardalhon V, Ducrey-Rundquist O, Trono D, Taylor N, Cosset FL. IL-7 surface-engineered lentiviral vectors promote survival and efficient gene transfer in resting primary T lymphocytes. Blood 2003; 101: 2167-74.
26. Verhoeyen E, Wiznerowicz M, Olivier D, et al. Novel lentiviral vectors displaying "early-acting cytokines" selectively promote survival and transduction of NOD/SCID repopulating human hematopoietic stem cells. Blood 2005; 106: 3386-95.
27. Vons C, Beaudoin S, Helmy N, Dagher I, Weber A, Franco D. First description of the surgical anatomy of the cynomolgus monkey liver. Am J Primatol 2009; Feb 4. [Epub ahead of print].
28. Andreoletti M, Loux N, Vons C, 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: 169-79.
29. Nguyen TH, Loux N, Dagher I, et al. Improved gene transfer selectivity to hepatocarcinoma cells by retrovirus vector displaying single-chain variable fragment antibody against c-Met. Cancer Gene Ther 2003; 10: 840-9.
30. Vons C, Loux N, Simon L, et al. Transplantation of hepatocytes in nonhuman primates: a preclinical model for the treatment of hepatic metabolic diseases. Transplantation 2001; 72: 811-8.
31. Naldini L, Blomer U, Gallay P, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 1996; 272: 263-7.
32. Frecha C, Szecsi J, Cosset FL, Verhoeyen E. Strategies for targeting lentiviral vectors. Curr Gene Ther 2008; 8: 449-60.
33. Bartosch B, Dubuisson J, Cosset FL. Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J Exp Med 2003; 197: 633-42.
34. Funke S, Maisner A, Muhlebach MD, et al. Targeted cell entry of lentiviral vectors. Mol Ther 2008; 16: 1427-36.
35. Frecha C, Costa C, Negre D, et al. Stable transduction of quiescent T-cells without induction of cycle progression by a novel lentiviral vector pseudotyped with measles virus glycoproteins. Blood 2008; 112: 4843-52.
36. Farson D, Witt R, McGuinness R, et al. A new-generation stable inducible packaging cell line for lentiviral vectors. Hum Gene Ther 2001; 12: 981-97.
37. Klages N, Zufferey R, Trono D. A stable system for the high-titer production of multiply attenuated lentiviral vectors. Mol Ther 2000; 2: 170-6.
38. Ni Y, Sun S, Oparaocha I, et al. Generation of a packaging cell line for prolonged large-scale production of high-titer HIV-1-based lentiviral vector. J Gene Med 2005; 7: 818-34.
39. Pacchia AL, Adelson ME, Kaul M, Ron Y, Dougherty JP. An inducible packaging cell system for safe, efficient lentiviral vector production in the absence of HIV-1 accessory proteins. Virology 2001; 282: 77-86.
40. Xu K, Ma H, McCown TJ, Verma IM, Kafri T. Generation of a stable cell line producing high-titer self-inactivating lentiviral vectors. Mol Ther 2001; 3: 97-104.
41. Broussau S, Jabbour N, Lachapelle G, et al. Inducible packaging cells for large-scale production of lentiviral vectors in serum-free suspension culture. Mol Ther 2008; 16: 500-7.
42. Suzuki Y, Craigie R. The road to chromatin - nuclear entry of retroviruses. Nat Rev 2007; 5: 187-96.
43. Christ F, Thys W, De Rijck J, et al. Transportin-SR2 imports HIV into the nucleus. Curr Biol 2008; 18: 1192-202.
44. Follenzi A, Ailles L, Bakovic S, Geuna M, Naldini L. Gene transfer by lentiviral vectors is limited by nuclear translocation and rescued by HIV-1 pol sequences. Nat Genet 2000; 25: 217-22.
45. Zennou V, Petit C, Guetard D, Nerhbass U, Montagnier L, Charneau P. HIV-1 genome nuclear import is mediated by a central DNA flap. Cell 2000; 10: 173-85.
46. Strang BL, Ikeda Y, Cosset FL, Collins MK, Takeuchi Y. Characterization of HIV-1 vectors with gammaretrovirus envelope glycoproteins produced from stable packaging cells. Gene Ther 2004; 11: 591-8.
47. Zufferey R, Dull T, Mandel RJ, et al. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 1998; 72: 9873-80.
48. Imren S, Fabry ME, Westerman KA, et al. High-level beta-globin expression and preferred intragenic integration after lentiviral transduction of human cord blood stem cells. J Clin Invest 2004; 114: 953-62.
49. Recillas-Targa F, Pikaart MJ, Burgess-Beusse B, et al. Position-effect protection and enhancer blocking by the chicken beta-globin insulator are separable activities. Proc Natl Acad Sci USA 2002; 99: 6883-8.
50. Zhang F, Thornhill SI, Howe SJ, et al. Lentiviral vectors containing an enhancer-less ubiquitously acting chromatin opening element (UCOE) provide highly reproducible and stable transgene expression in hematopoietic cells. Blood 2007; 110: 1448-57.
51. Zufferey R, Donello JE, Trono D, Hope TJ. Woodchuck hepatitis virus posttranscriptional regulatory element enhances expression of transgenes delivered by retroviral vectors. J Virol 1999; 73: 2886-92.
52. Donello JE, Loeb JE, Hope TJ. Woodchuck hepatitis virus contains a tripartite posttranscriptional regulatory element. J Virol 1998; 72: 5085-92.
53. Mastroyiannopoulos NP, Feldman ML, Uney JB, Mahadevan MS, Phylactou LA. Woodchuck post-transcriptional element induces nuclear export of myotonic dystrophy 3' untranslated region transcripts. EMBO Rep 2005; 6: 458-63.
54. Costa RH, Grayson DR. Site-directed mutagenesis of hepatocyte nuclear factor (HNF) binding sites in the mouse transthyretin (TTR) promoter reveal synergistic interactions with its enhancer region. Nucleic Acids Res 1991; 19: 4139-45.
55. Brown BD, Cantore A, Annoni A, et al. A microRNA-regulated lentiviral vector mediates stable correction of hemophilia B mice. Blood 2007; 110: 4144-4152.
56. Nguyen TH, Bellodi-Privato M, Aubert D, et al. Therapeutic lentivirus-mediated neonatal in vivo gene therapy in hyperbilirubinemic Gunn rats. Mol Ther 2005; 12: 852-9.
57. Seppen J, Rijnberg M, Cooreman MP, Oude Elferink RP. Lentiviral vectors for efficient transduction of isolated primary quiescent hepatocytes. J Hepatol 2002; 36: 459-65.
58. Dagher I, Nguyen T, Groyer-Picard M, et al. Efficient hepatocyte engraftment and long-term transgene expression after reversible portal embolization in non-human primates. Hepatology 2009; 49: 950-9.
59. 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.
60. Hanawa H, Hematti P, Keyvanfar K, et al. Efficient gene transfer into rhesus repopulating hematopoietic stem cells using a simian immunodeficiency virus-based lentiviral vector system. Blood 2004; 103: 4062-9.
61. Saenz DT, Teo W, Olsen JC, Poeschla EM. Restriction of feline immunodeficiency virus by Ref1, Lv1, and primate TRIM5alpha proteins. J Virol 2005; 79: 15175-88.
62. An DS, Kung SK, Bonifacino A, et al. Lentivirus vector-mediated hematopoietic stem cell gene transfer of common gamma-chain cytokine receptor in rhesus macaques. J Virol 2001; 75: 3547-55.
63. An DS, Wersto RP, Agricola BA, et al. Marking and gene expression by a lentivirus vector in transplanted human and nonhuman primate CD34(+) cells. J Virol 2000; 74: 1286-95.
64. Horn PA, Topp MS, Morris JC, Riddell SR, Kiem HP. Highly efficient gene transfer into baboon marrow repopulating cells using GALV-pseudotype oncoretroviral vectors produced by human packaging cells. Blood 2002; 100: 3960-7.
65. Trobridge GD, Beard BC, Gooch C, et al. Efficient transduction of pigtailed macaque hematopoietic repopulating cells with HIV-based lentiviral vectors. Blood 2008; 111: 5537-43.
66. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 2004; 427: 848-53.
67. Stremlau M, Perron M, Lee M, et al. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc Natl Acad Sci USA 2006; 103: 5514-9.
68. Lin TY, Emerman M. Determinants of cyclophilin A-dependent TRIM5 alpha restriction against HIV-1. Virology 2008; 379: 335-41.
69. Munk C, Brandt SM, Lucero G, Landau NR. A dominant block to HIV-1 replication at reverse transcription in simian cells. Proc Natl Acad Sci USA 2002; 99: 13843-8.
70. Towers GJ, Hatziioannou T, Cowan S, Goff SP, Luban J, Bieniasz PD. Cyclophilin A modulates the sensitivity of HIV-1 to host restriction factors. Nat Med 2003; 9: 1138-43.
71. Parouchev A, Nguyen TH, Dagher I, et al. Efficient ex vivo gene transfer into non-human primate hepatocytes using HIV-1 derived lentiviral vectors. J Hepatol 2006; 45: 99-107.
72. Cowan S, Hatziioannou T, Cunningham T, Muesing MA, Gottlinger HG, Bieniasz PD. Cellular inhibitors with Fv1-like activity restrict human and simian immunodeficiency virus tropism. Proc Natl Acad Sci USA 2002; 99: 11914-9.
73. Kootstra NA, Munk C, Tonnu N, Landau NR, Verma IM. Abrogation of postentry restriction of HIV-1-based lentiviral vector transduction in simian cells. Proc Natl Acad Sci USA 2003; 100: 1298-303.
74. Rits MA, van Dort KA, Munk C, Meijer AB, Kootstra NA. Efficient transduction of simian cells by HIV-1-based lentiviral vectors that contain mutations in the capsid protein. Mol Ther 2007; 15: 930-7.
75. Kahl CA, Cannon PM, Oldenburg J, Tarantal AF, Kohn DB. Tissue-specific restriction of cyclophilin A-independent HIV-1- and SIV-derived lentiviral vectors. Gene Ther 2008; 15: 1079-89.
76. Besnier C, Takeuchi Y, Towers G. Restriction of lentivirus in monkeys. Proc Natl Acad Sci USA 2002; 99: 11920-5.
77. Nguyen TH, Khakhoulina T, Simmons A, Morel P, Trono D. A simple and highly effective method for the stable transduction of uncultured porcine hepatocytes using lentiviral vector. Cell Transplant 2005; 14: 489-96.
78. Park F, Ohashi K, Kay MA. The effect of age on hepatic gene transfer with self-inactivating lentiviral vectors in vivo. Mol Ther 2003; 8: 314-23.
79. Park F, Ohashi K, Chiu W, Naldini L, Kay M. Efficient lentiviral transduction of liver requires cell cycling in vivo. Nat Genet 2000; 24: 49-52.
80. Chang AH, Stephan MT, Sadelain M. Stem cell-derived erythroid cells mediate long-term systemic protein delivery. Nat Biotechnol 2006; 24: 1017-21.
81. Santoni de Sio FR, Gritti A, Cascio P, et al. Lentiviral vector gene transfer is limited by the proteasome at postentry steps in various types of stem cells. Stem Cells 2008; 26: 2142-52.
82. Santoni de Sio FR, Cascio P, Zingale A, Gasparini M, Naldini L. Proteasome activity restricts lentiviral gene transfer into hematopoietic stem cells and is down-regulated by cytokines that enhance transduction. Blood 2006; 107: 4257-65.
83. Hacein-Bey-Abina S, Garrigue A, Wang GP, et al. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J Clin Invest 2008; 118: 3132-42.
84. Bauer G, Dao MA, Case SS, et al. In vivo biosafety model to assess the risk of adverse events from retroviral and lentiviral vectors. Mol Ther 2008; 16: 1308-15.
85. Montini E, Cesana D, Schmidt M, et al. Hematopoietic stem cell gene transfer in a tumor-prone mouse model uncovers low genotoxicity of lentiviral vector integration. Nat Biotechnol 2006; 24: 687-96.
86. Wu X, Li Y, Crise B, Burgess SM. Transcription start regions in the human genome are favored targets for MLV integration. Science 2003; 300: 1749-51.
87. Modlich U, Bohne J, Schmidt M, et al. Cell-culture assays reveal the importance of retroviral vector design for insertional genotoxicity. Blood 2006; 108: 2545-53.
88. Zychlinski D, Schambach A, Modlich U, et al. Physiological promoters reduce the genotoxic risk of integrating gene vectors. Mol Ther 2008; 16: 718-25.
89. Nasu Y, Saika T, Ebara S, et al. Suicide gene therapy with adenoviral delivery of HSV-tK gene for patients with local recurrence of prostate cancer after hormonal therapy. Mol Ther 2007; 15: 834-40.
90. Traversari C, Marktel S, Magnani Z, et al. The potential immunogenicity of the TK suicide gene does not prevent full clinical benefit associated with the use of TK-transduced donor lymphocytes in HSCT for hematologic malignancies. Blood 2007; 109: 4708-15.
91. Frank O, Rudolph C, Heberlein C, et al. Tumor cells escape suicide gene therapy by genetic and epigenetic instability. Blood 2004; 104: 3543-49.
92. Michalopoulos G, DeFrances M. Liver regeneration. Science 1997; 276: 60-6.
93. Baum C, Kustikova O, Modlich U, Li Z, Fehse B. Mutagenesis and oncogenesis by chromosomal insertion of gene transfer vectors. Hum Gene Ther 2006; 17: 253-63.
94. Nienhuis AW, Dunbar CE, Sorrentino BP. Genotoxicity of retroviral integration in hematopoietic cells. Mol Ther 2006; 13: 1031-49.
95. Forbes SJ, Themis M, Alison MR, Sarosi I, Coutelle C, Hodgson HJ. Synergistic growth factors enhance rat liver proliferation and enable retroviral gene transfer via a peripheral vein. Gastroenterology 2000; 118: 591-8.
96. Patijn GA, Lieber A, Schowalter DB, Schwall R, Kay MA. Hepatocyte growth factor induces hepatocyte proliferation in vivo and allows for efficient retroviral-mediated gene transfer in mice. Hepatology 1998; 28: 707-16.
97. Pichard V, Aubert D, Ferry N. Efficient retroviral gene transfer to the liver in vivo using nonpolypeptidic mitogens. Biochem Biophys Res Commun 2001; 286: 929-35.
98. Zimmers TA, McKillop IH, Pierce RH, Yoo JY, Koniaris LG. Massive liver growth in mice induced by systemic interleukin 6 administration. Hepatology 2003; 38: 326-34.
99. Bellodi-Privato M, Aubert D, Pichard V, Myara A, Trivin F, Ferry N. Successful gene therapy of the Gunn rat by in vivo neonatal hepatic gene transfer using murine oncoretroviral vectors. Hepatology 2005; 42: 431-8.
100. Overturf K, Al-Dhalimy M, Tanguay R, et al. Hepatocytes corrected by gene therapy are selected in vivo in a murine model of hereditary tyrosinaemia type I. Nat Genet 1996; 12: 266-73.
101. Themis M, Waddington SN, Schmidt M, et al. Oncogenesis following delivery of a nonprimate lentiviral gene therapy vector to fetal and neonatal mice. Mol Ther 2005; 12: 763-71.
102. Uyama S, Kaufmann PM, Kneser U, et al. Hepatocyte transplantation using biodegradable matrices in ascorbic acid-deficient rats: comparison with heterotopically transplanted liver grafts. Transplantation 2001; 71: 1226-31.
103. 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: 732-4.
104. Kobayashi N, Ito M, Nakamura J, et al. Hepatocyte transplantation in rats with decompensated cirrhosis. Hepatology 2000; 31: 851-7.
105. Ohashi K, Kay MA, Yokoyama T, et al. Stability and repeat regeneration potential of the engineered liver tissues under the kidney capsule in mice. Cell Transplant 2005; 14: 621-7.
106. Ohashi K, Waugh JM, Dake MD, et al. Liver tissue engineering at extrahepatic sites in mice as a potential new therapy for genetic liver diseases. Hepatology 2005; 41: 132-40.
107. Benhamouche S, Decaens T, Godard C, et al. Apc tumor suppressor gene is the "zonation-keeper" of mouse liver. Dev Cell 2006; 10: 759-70.
108. Koenig S, Aurich H, Schneider C, et al. Zonal expression of hepatocytic marker enzymes during liver repopulation. Histochem Cell Biol 2007; 128: 105-14.
109. 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: 1677-85.
110. Gupta S, Rajvanshi P, Sokhi R, et al. Entry and integration of transplanted hepatocytes in rat liver plates occur by disruption of hepatic sinusoidal endothelium. Hepatology 1999; 29: 509-19.
111. 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: 1411-20.
112. Slehria S, Rajvanshi P, Ito Y, et al. Hepatic sinusoidal vasodilators improve transplanted cell engraftment and ameliorate microcirculatory perturbations in the liver. Hepatology 2002; 35: 1320-8.
113. Grompe M, Laconi E, Shafritz DA. Principles of therapeutic liver repopulation. Semin Liver Dis 1999; 19: 7-14.
114. Koenig S, Krause P, Schmidt TK, et al. Irradiation as preparative regimen for hepatocyte transplantation causes prolonged cell cycle block. Int J Rad Biol 2008; 84: 285-98.
115. 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: 165-73.
116. Giannini C, Morosan S, Tralhao JG, et al. A highly efficient, stable, and rapid approach for ex vivo human liver gene therapy via a FLAP lentiviral vector. Hepatology 2003; 38: 114-22.
117. Birraux J, Menzel O, Wildhaber B, Jond C, Chardot C, Nguyen TH. A step toward liver gene therapy: efficient correction of the genetic defect of hepatocytes isolated from a patient with Crigler-Najjar syndrome type 1 with lentiviral vectors. Transplantation 2009; In press.
118. 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 USA 1995; 92: 377-81.
119. Nguyen TH, Birraux J, Wildhaber B, et al. Ex vivo lentivirus transduction and immediate transplantation of uncultured hepatocytes for treating hyperbilirubinemic Gunn rat. Transplantation 2006; 82: 794-803.
120. Brezillon N, Lambert-Blot M, Morosan S, et al. Transplanted hepatocytes over-expressing FoxM1B efficiently repopulate chronically injured mouse liver independent of donor age. Mol Ther 2007; 15: 1710-5.
121. Delgado JP, Parouchev A, Allain JE, et al. Long-term controlled immortalization of a primate hepatic progenitor cell line after Simian virus 40 T-Antigen gene transfer. Oncogene 2005; 24: 541-51.
122. Allain JE, Dagher I, Mahieu-Caputo D, et al. Immortalization of a primate bipotent epithelial liver stem cell. Proc Natl Acad Sci USA 2002; 99: 3639-44.
123. Furrer K, Tian Y, Pfammatter T, et al. Selective portal vein embolization and ligation trigger different regenerative responses in the rat liver. Hepatology 2008; 47:1615-23.
124. Ise N, Sato T, Yasui O, et al. Enhanced proliferation of hepatic progenitor cells in rats after portal branch occlusion. Liver Transpl 2004; 10: 748-54.
125. Eguchi S, Rozga J, Lebow LT, et al. Treatment of hypercholesterolemia in the Watanabe rabbit using allogeneic hepatocellular transplantation under a regeneration stimulus. Transplantation 1996; 62: 588-93.
126. Yanez-Munoz RJ, Balaggan KS, MacNeil A, et al. Effective gene therapy with nonintegrating lentiviral vectors. Nat Med 2006; 12: 348-53.
127. Cara A, Cereseto A, Lori F, Reitz MS, Jr. HIV-1 protein expression from synthetic circles of DNA mimicking the extrachromosomal forms of viral DNA. J Biol Chem 1996; 271: 5393-7.
128. Engelman A, Englund G, Orenstein JM, Martin MA, Craigie R. Multiple effects of mutations in human immunodeficiency virus type 1 integrase on viral replication. J Virol 1995; 69: 2729-36.
129. Philippe S, Sarkis C, Barkats M, et al. Lentiviral vectors with a defective integrase allow efficient and sustained transgene expression in vitro and in vivo. Proc Natl Acad Sci USA 2006; 103: 17684-9.
130. Butler SL, Johnson EP, Bushman FD. Human immunodeficiency virus cDNA metabolism: notable stability of two-long terminal repeat circles. J Virol 2002; 76: 3739-47.
131. Pierson TC, Kieffer TL, Ruff CT, Buck C, Gange SJ, Siliciano RF. Intrinsic stability of episomal circles formed during human immunodeficiency virus type 1 replication. J Virol 2002; 76: 4138-44.
132. Apolonia L, Waddington SN, Fernandes C, et al. Stable gene transfer to muscle using non-integrating lentiviral vectors. Mol Ther 2007; 15: 1947-54.
133. Bayer M, Kantor B, Cockrell A, et al. A large U3 deletion causes increased in vivo expression from a nonintegrating lentiviral vector. Mol Ther 2008; 16: 1968-76.
134. Lombardo A, Genovese P, Beausejour CM, et al. Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat Biotechnol 2007; 25: 1298-306.
135. Ivics Z, Izsvak Z. Transposons for gene therapy! Curr Gene Ther 2006; 6: 593-607.
136. Ivics Z, Katzer A, Stuwe EE, Fiedler D, Knespel S, Izsvak Z. Targeted sleeping beauty transposition in human cells. Mol Ther 2007; 15: 1137-44.
137. Yant SR, Huang Y, Akache B, Kay MA. Site-directed transposon integration in human cells. Nucleic Acids Res 2007; 35: e50.
138. Liu L, Mah C, Fletcher BS. Sustained FVIII expression and phenotypic correction of hemophilia A in neonatal mice using an endothelial-targeted sleeping beauty transposon. Mol Ther 2006; 13: 1006-15.
139. Montini E, Held PK, Noll M, et al. In vivo correction of murine tyrosinemia type I by DNA-mediated transposition. Mol Ther 2002; 6: 759-69.
140. Ohlfest JR, Frandsen JL, Fritz S, et al. Phenotypic correction and long-term expression of factor VIII in hemophilic mice by immunotolerization and nonviral gene transfer using the sleeping beauty transposon system. Blood 2005; 105: 2691-8.
141. Yant SR, Meuse L, Chiu W, Ivics Z, Izsvak Z, Kay MA. Somatic integration and long-term transgene expression in normal and haemophilic mice using a DNA transposon system. Nat Genet 2000; 25: 35-41.
142. Wang X, Mani P, Sarkar DP, Roy-Chowdhury N, Roy-Chowdhury J. Ex vivo gene transfer into hepatocytes. Meth Mol Biol 2009; 481: 1-23.
143. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131: 861-72.
144. Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S. Generation of mouse induced pluripotent stem cells without viral vectors. Science 2008; 322: 949-53.
145. Yamanaka S. Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell stem cell 2007; 1: 39-49.