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International Journal of Hepatology
Volume 2012, Article ID 785786, 14 pages
http://dx.doi.org/10.1155/2012/785786
Research Article

Combined Stimulation with the Tumor Necrosis Factor and the Epidermal Growth Factor Promotes the Proliferation of Hepatocytes in Rat Liver Cultured Slices

1Covance Laboratory SAS, 2-8 rue de Rouen, Z.I. de Limay-Porcheville, 78440 Porcheville, France
2Laboratoire d'Hématologie, Hôpital Pontchaillou, 2 rue Henri Le Guilloux, 35033 Rennes Cedex, France
3Inserm UMR-S 991, Université de Rennes 1, Hôpital Pontchaillou, 35033 Rennes Cedex, France
4Noscira SA, 52 Avendia de la Industria 38760 Tres Cantos, Spain

Received 1 June 2012; Revised 6 September 2012; Accepted 7 September 2012

Academic Editor: Anne Corlu

Copyright © 2012 Francis Finot et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. Guguen-Guillouzo and A. Guillouzo, “General review on in vitro hepatocyte models and their applications,” Methods in Molecular Biology, vol. 640, pp. 1–40, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. P. Loyer, S. Cariou, D. Glaise, M. Bilodeau, G. Baffet, and C. Guguen-Guillouzo, “Growth factor dependence of progression through G1 and S phases of adult rat hepatocytes in vitro: evidence of a mitogen restriction point in mid-late G1,” The Journal of Biological Chemistry, vol. 271, no. 19, pp. 11484–11492, 1996. View at Google Scholar · View at Scopus
  3. B. Bailly-Maitre, G. de Sousa, N. Zucchini, J. Gugenheim, K. E. Boulukos, and R. Rahmani, “Spontaneous apoptosis in primary cultures of human and rat hepatocytes: molecular mechanisms and regulation by dexamethasone,” Cell Death and Differentiation, vol. 9, no. 9, pp. 945–955, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. D. Gilot, P. Loyer, A. Corlu et al., “Liver protection from apoptosis requires both blockage of initiator caspase activities and inhibition of ASK1/JNK pathway via glutathione S-transferase regulation,” The Journal of Biological Chemistry, vol. 277, no. 51, pp. 49220–49229, 2002. View at Publisher · View at Google Scholar · View at Scopus
  5. H. C. Isom, T. Secott, I. Georgoff, C. Woodworth, and J. Mummaw, “Maintenance of differentiated rat hepatocytes in primary culture,” Proceedings of the National Academy of Sciences of the United States of America, vol. 82, no. 10, pp. 3252–3256, 1985. View at Google Scholar · View at Scopus
  6. C. Guguen Guillouzo, B. Clement, G. Baffet et al., “Maintenance and reversibility of active albumin secretion by adult rat hepatocytes co-cultured with another liver epithelial cell type,” Experimental Cell Research, vol. 143, no. 1, pp. 47–54, 1983. View at Google Scholar · View at Scopus
  7. D. J. Waxman, J. J. Morrissey, S. Naik, and H. O. Jauregui, “Phenobarbital induction of cytochromes P-450. High-level long-term responsiveness of primary rat hepatocyte cultures to drug induction, and glucocorticoid dependence of the phenobarbital response,” Biochemical Journal, vol. 271, no. 1, pp. 113–119, 1990. View at Google Scholar · View at Scopus
  8. D. M. Bissell, D. M. Arenson, J. J. Maher, and F. J. Roll, “Support of cultured hepatocytes by a laminin-rich gel. Evidence for a functionally significant subendothelial matrix in normal rat liver,” Journal of Clinical Investigation, vol. 79, no. 3, pp. 801–812, 1987. View at Google Scholar · View at Scopus
  9. T. Kojima, T. Mitaka, D. L. Paul, M. Mori, and Y. Mochizuki, “Reappearance and long-term maintenance of connexin32 in proliferated adult rat hepatocytes: use of serum-free L-15 medium supplemented with EGF and DMSO,” Journal of Cell Science, vol. 108, part 4, pp. 1347–1357, 1995. View at Google Scholar · View at Scopus
  10. A. Corlu, G. Ilyin, S. Cariou, I. Lamy, P. Loyer, and C. Guguen-Guillouzo, “The coculture: a system for studying the regulation of liver differentiation/proliferation activity and its control,” Cell Biology and Toxicology, vol. 13, no. 4-5, pp. 235–242, 1997. View at Publisher · View at Google Scholar · View at Scopus
  11. L. K. Hansen and J. H. Albrecht, “Regulation of the hepatocyte cell cycle by type I collagen matrix: role of cyclin D1,” Journal of Cell Science, vol. 112, part 17, pp. 2971–2981, 1999. View at Google Scholar · View at Scopus
  12. K. De Smet, P. Loyer, D. Gilot, A. Vercruysse, V. Rogiers, and C. Guguen-Guillouzo, “Effects of epidermal growth factor on CYP inducibility by xenobiotics, DNA replication, and caspase activations in collagen I gel sandwich cultures of rat hepatocytes,” Biochemical Pharmacology, vol. 61, no. 10, pp. 1293–1303, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. C. L. Krumdieck, E. Dos Santos, and K. J. Ho, “A new instrument for the rapid preparation of tissue slices,” Analytical Biochemistry, vol. 104, no. 1, pp. 118–123, 1980. View at Google Scholar · View at Scopus
  14. H. Clouzeau-Girard, C. Guyot, C. Combe et al., “Effects of bile acids on biliary epithelial cell proliferation and portal fibroblast activation using rat liver slices,” Laboratory Investigation, vol. 86, no. 3, pp. 275–285, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. M. van de Bovenkamp, G. M. M. Groothuis, D. K. F. Meijer, and P. Olinga, “Precision-cut fibrotic rat liver slices as a new model to test the effects of anti-fibrotic drugs in vitro,” Journal of Hepatology, vol. 45, no. 5, pp. 696–703, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. A. E. M. Vickers and R. L. Fisher, “Organ slices for the evaluation of human drug toxicity,” Chemico-Biological Interactions, vol. 150, no. 1, pp. 87–96, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. V. Moronvalle-Halley, B. Sacré-Salem, V. Sallez, G. Labbe, and J. C. Gautier, “Evaluation of cultured, precision-cut rat liver slices as a model to study drug-induced liver apoptosis,” Toxicology, vol. 207, no. 2, pp. 203–214, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. M. G. L. Elferink, P. Olinga, E. M. van Leeuwen et al., “Gene expression analysis of precision-cut human liver slices indicates stable expression of ADME-Tox related genes,” Toxicology and Applied Pharmacology, vol. 253, no. 1, pp. 57–69, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. A. M. Neyrinck, C. Gomez, and N. M. Delzenne, “Precision-cut liver slices in culture as a tool to assess the physiological involvement of Kupffer cells in hepatic metabolism,” Comparative Hepatology, vol. 3, supplement 1, p. S45, 2004. View at Google Scholar
  20. C. Guyot, S. Lepreux, C. Combe et al., “Fibrogenic cell phenotype modifications during remodelling of normal and pathological human liver in cultured slices,” Liver International, vol. 30, no. 10, pp. 1529–1540, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. A. E. M. Vickers, R. Fisher, P. Olinga, and S. Dial, “Repair pathways evident in human liver organ slices,” Toxicology in Vitro, vol. 25, no. 7, pp. 1485–1492, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. A. E. M. Vickers, J. R. Sinclair, R. L. Fisher, S. R. Morris, and W. Way, “Blood cell oxidative stress precedes hemolysis in whole blood-liver slice co-cultures of rat, dog, and human tissues,” Toxicology and Applied Pharmacology, vol. 244, no. 3, pp. 354–365, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Lagaye, H. Shen, B. Saunier, M. Nascimbeni, J. Gaston, P. Bourdoncle et al., “Efficient replication of primary or culture hepatitis C virus isolates in human liver slices: a relevant ex vivo model of liver infection,” Hepatology, vol. 56, pp. 861–8672, 2012. View at Google Scholar
  24. A. Lupp, M. Danz, and D. Müller, “Histomorphological changes and cytochrome P450 isoforms expression and activities in precision-cut liver slices from neonatal rats,” Toxicology, vol. 206, no. 3, pp. 427–438, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. J. R. Catania, B. P. McGarrigle, K. Rittenhouse-Olson, and J. R. Olson, “Induction of CYP2B and CYP2E1 in precision-cut rat liver slices cultured in defined medium,” Toxicology in Vitro, vol. 21, no. 1, pp. 109–115, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Lupp, R. Glöckner, M. Danz, and D. Müller, “Cryopreserved precision-cut rat liver slices: morphology and cytochrome P450 isoforms expression after prolonged incubation,” Toxicology in Vitro, vol. 16, no. 6, pp. 749–758, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Martignoni, M. Monshouwer, R. De Kanter, D. Pezzetta, A. Moscone, and P. Grossi, “Phase I and phase II metabolic activities are retained in liver slices from mouse, rat, dog, monkey and human after cryopreservation,” Toxicology in Vitro, vol. 18, no. 1, pp. 121–128, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. I. A. M. De Graaf and H. J. Koster, “Cryopreservation of precision-cut tissue slices for application in drug metabolism research,” Toxicology in Vitro, vol. 17, no. 1, pp. 1–17, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Olinga, K. Groen, I. H. Hof et al., “Comparison of five incubation systems for rat liver slices using functional and viability parameters,” Journal of Pharmacological and Toxicological Methods, vol. 38, no. 2, pp. 59–69, 1997. View at Publisher · View at Google Scholar · View at Scopus
  30. M. VandenBranden, S. A. Wrighton, S. Ekins et al., “Alterations of the catalytic activities of drug-metabolizing enzymes in cultures of human liver slices,” Drug Metabolism and Disposition, vol. 26, no. 11, pp. 1063–1068, 1998. View at Google Scholar · View at Scopus
  31. M. S. Gokhale, T. E. Bunton, J. Zurlo, and J. D. Yager, “Cytochrome P450 isoenzyme activities in cultured rat and mouse liver slices,” Xenobiotica, vol. 27, no. 4, pp. 341–355, 1997. View at Google Scholar · View at Scopus
  32. H. P. Behrsing, A. E. M. Vickers, and C. A. Tyson, “Extended rat liver slice survival and stability monitored using clinical biomarkers,” Biochemical and Biophysical Research Communications, vol. 312, no. 1, pp. 209–213, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Zimmermann, J. Lampe, S. Lange et al., “Improved reproducibility in preparing precision-cut liver tissue slices,” Cytotechnology, vol. 61, no. 3, pp. 145–152, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Lerche-Langrand and H. J. Toutain, “Precision-cut liver slices: characteristics and use for in vitro pharmaco-toxicology,” Toxicology, vol. 153, no. 1–3, pp. 221–253, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. P. M. van Midwoud, M. T. Merema, N. Verweij, G. M. Groothuis, and E. Verpoorte, “Hydrogel embedding of precision-cut liver slices in a microfluidic device improves drug metabolic activity,” Biotechnology and Bioengineering, vol. 108, no. 6, pp. 1404–1412, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Yoshida, Y. Arisaka, S. Nakagawa, and H. Takahashi, “Rotation culture with a newly developed holder enables long-term liver slice culture for study of liver fibrosis,” Hepatology Research, vol. 28, no. 4, pp. 198–206, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. E. Hashemi, M. Dobrota, C. Till, and C. Ioannides, “Structural and functional integrity of precision-cut liver slices in xenobiotic metabolism: a comparison of the dynamic organ and multiwell plate culture procedures,” Xenobiotica, vol. 29, no. 1, pp. 11–25, 1999. View at Publisher · View at Google Scholar · View at Scopus
  38. H. J. Toutain, V. Moronvalle-Halley, J. P. Sarsat, C. Chelin, D. Hoet, and D. Leroy, “Morphological and functional integrity of precision-cut rat liver slices in rotating organ culture and multiwell plate culture: effects of oxygen tension,” Cell Biology and Toxicology, vol. 14, no. 3, pp. 175–190, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Verrill, J. Davies, H. Millward-Sadler, L. Sundstrom, and N. Sheron, “Organotypic liver culture in a fluid-air interface using slices of neonatal rat and adult human tissue—A model of fibrosis in vitro,” Journal of Pharmacological and Toxicological Methods, vol. 48, no. 2, pp. 103–110, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. I. A. M. De Graaf, O. Tajima, J. P. Groten, and A. P. M. Wolterbeek, “Intercellular communication and cell proliferation in precision-cut rat liver slices: effect of medium composition and DDT,” Cancer Letters, vol. 154, no. 1, pp. 53–62, 2000. View at Publisher · View at Google Scholar · View at Scopus
  41. F. Desmots, M. Rissel, D. Gilot et al., “Pro-inflammatory cytokines tumor necrosis factor α and interleukin-6 and survival factor epidermal growth factor positively regulate the murine GSTA4 enzyme in hepatocytes,” The Journal of Biological Chemistry, vol. 277, no. 20, pp. 17892–17900, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. P. F. Smith, G. Krack, R. L. McKee et al., “Maintenance of adult rat liver slices in dynamic organ culture,” In Vitro Cellular and Developmental Biology, vol. 22, no. 12, pp. 706–712, 1986. View at Google Scholar · View at Scopus
  43. N. Fausto, “Liver regeneration,” Journal of Hepatology, vol. 32, no. 1, pp. 19–31, 2000. View at Google Scholar · View at Scopus
  44. H. Talarmin, C. Rescan, S. Cariou et al., “The mitogen-activated protein kinase kinase/extracellular signal- regulated kinase cascade activation is a key signalling pathway involved in the regulation of G1 phase progression in proliferating hepatocytes,” Molecular and Cellular Biology, vol. 19, no. 9, pp. 6003–6011, 1999. View at Google Scholar · View at Scopus
  45. H. Duval, S. F. Mbatchi, S. Grandadam et al., “Reperfusion stress induced during intermittent selective clamping accelerates rat liver regeneration through JNK pathway,” Journal of Hepatology, vol. 52, no. 4, pp. 560–569, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. F. Desmots, M. Rissel, C. Pigeon, P. Loyer, O. Loréal, and A. Guillouzo, “Differential effects of iron overload on GST isoform expression in mouse liver and kidney and correlation between GSTA4 induction and overproduction of free radicals,” Free Radical Biology and Medicine, vol. 32, no. 1, pp. 93–101, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. P. Loyer, G. Ilyin, S. Cariou, D. Glaise, A. Corlu, and C. Guguen-Guillouzo, “Progression through G1 and S phases of adult rat hepatocytes,” Progress in Cell Cycle Research, vol. 2, pp. 37–47, 1996. View at Google Scholar · View at Scopus
  48. D. Garnier, P. Loyer, C. Ribault, C. Guguen-Guillouzo, and A. Corlu, “Cyclin-dependent kinase 1 plays a critical role in DNA replication control during rat liver regeneration,” Hepatology, vol. 50, no. 6, pp. 1946–1956, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. A. L. Sérandour, P. Loyer, D. Garnier et al., “TNFα-mediated extracellular matrix remodeling is required for multiple division cycles in rat hepatocytes,” Hepatology, vol. 41, no. 3, pp. 478–486, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. F. Desmots, P. Loyer, M. Rissel, A. Guillouzo, and F. Morel, “Activation of C-Jun N-terminal kinase is required for glutathione transferase A4 induction during oxidative stress, not during cell proliferation, in mouse hepatocytes,” FEBS Letters, vol. 579, no. 25, pp. 5691–5696, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. D. E. Cressman, L. E. Greenbaum, R. A. DeAngelis et al., “Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice,” Science, vol. 274, no. 5291, pp. 1379–1383, 1996. View at Publisher · View at Google Scholar · View at Scopus
  52. E. M. Webber, J. Bruix, R. H. Pierce, and N. Fausto, “Tumor necrosis factor primes hepatocytes for DNA replication in the rat,” Hepatology, vol. 28, no. 5, pp. 1226–1234, 1998. View at Publisher · View at Google Scholar · View at Scopus
  53. T. H. Kim, W. M. Mars, D. B. Stolz, B. E. Petersen, and G. K. Michalopoulos, “Extracellular matrix remodeling at the early stages of liver regeneration in the rat,” Hepatology, vol. 26, no. 4, pp. 896–904, 1997. View at Google Scholar · View at Scopus
  54. T. H. Kim, W. M. Mars, D. B. Stolz, and G. K. Michalopoulos, “Expression and activation of pro-MMP-2 and pro-MMP-9 during rat liver regeneration,” Hepatology, vol. 31, no. 1, pp. 75–82, 2000. View at Google Scholar · View at Scopus
  55. E. S. Bour, L. K. Ward, G. A. Cornman, and H. C. Isom, “Tumor necrosis factor-α-induced apoptosis in hepatocytes in long-term culture,” The American Journal of Pathology, vol. 148, no. 2, pp. 485–495, 1996. View at Google Scholar · View at Scopus
  56. S. Thohan, M. C. Zurich, H. Chung, M. Weiner, A. S. Kane, and G. M. Rosen, “Tissue slices revisited: evaluation and development of a short-term incubation for integrated drug metabolism,” Drug Metabolism and Disposition, vol. 29, no. 10, pp. 1337–1342, 2001. View at Google Scholar · View at Scopus