Table of Contents Author Guidelines Submit a Manuscript
Journal of Toxicology
Volume 2017, Article ID 1907952, 5 pages
https://doi.org/10.1155/2017/1907952
Review Article

Hepatocyte CYP2B6 Can Be Expressed in Cell Culture Systems by Exerting Physiological Levels of Shear: Implications for ADME Testing

1Durham VA Medical Center, Research & Development Service, Durham, NC 27705, USA
2Nephrology Division, Department of Internal Medicine, Duke University School of Medicine, Durham, NC 27705, USA
3Space Policy Institute, Elliott School of International Affairs, George Washington University, Washington, DC 20052, USA
4Department of Veterans Affairs Office of Research and Development, Washington, DC 20420, USA
5Departments of Otorhinolaryngology, Immunology, and Psychiatry, Baylor College of Medicine, Houston, TX 77030, USA

Correspondence should be addressed to Timothy G. Hammond; moc.oohay@eciffofotuodnommah and Holly H. Birdsall; moc.liamg@llasdribhh

Received 24 June 2017; Revised 27 July 2017; Accepted 7 August 2017; Published 10 September 2017

Academic Editor: Lucio Guido Costa

Copyright © 2017 Timothy G. Hammond and Holly H. Birdsall. 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. T. Lang, K. Klein, J. Fischer et al., “Extensive genetic polymorphism in the human CYP2B6 gene with impact on expression and function in human liver,” Pharmacogenetics, vol. 11, no. 5, pp. 399–415, 2011. View at Publisher · View at Google Scholar
  2. H. Wang and L. M. Tompkins, “CYP2B6: New insights into a historically overlooked cytochrome P450 isozyme,” Current Drug Metabolism, vol. 9, no. 7, pp. 598–610, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. W. D. Hedrich, H. E. Hassan, and H. Wang, “Insights into CYP2B6-mediated drug-drug interactions,” Acta Pharmaceutica Sinica B, vol. 6, no. 5, pp. 413–425, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. U. M. Zanger, K. Klein, T. Saussele, J. Blievernicht, M. H. Hofmann, and M. Schwab, “Polymorphic CYP2B6: Molecular mechanisms and emerging clinical significance,” Pharmacogenomics, vol. 8, no. 7, pp. 743–759, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. L. A. Brown, L. M. Arterburn, A. P. Miller et al., “Maintenance of liver functions in rat hepatocytes cultured as spheroids in a rotating wall vessel,” In Vitro Cellular & Developmental Biology - Animal, vol. 39, no. 1, p. 13, 2003. View at Publisher · View at Google Scholar
  6. S.-F. Zhou, J.-P. Liu, and B. Chowbay, “Polymorphism of human cytochrome P450 enzymes and its clinical impact,” Drug Metabolism Reviews, vol. 41, no. 2, pp. 89–295, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. V. M. Lauschke, D. F. G. Hendriks, C. C. Bell, T. B. Andersson, and M. Ingelman-Sundberg, “Novel 3D Culture Systems for Studies of Human Liver Function and Assessments of the Hepatotoxicity of Drugs and Drug Candidates,” Chemical Research in Toxicology, vol. 29, no. 12, pp. 1936–1955, 2016. View at Publisher · View at Google Scholar · View at Scopus
  8. R. L. Sison-Young, V. M. Lauschke, E. Johann et al., “A multicenter assessment of single-cell models aligned to standard measures of cell health for prediction of acute hepatotoxicity,” Archives of Toxicology, vol. 91, no. 3, pp. 1385–1400, 2016. View at Publisher · View at Google Scholar
  9. National Research Council, Toxicity Testing in the 21st Century: A Vision and a Strategy, National Academy Press, Wash, USA, 2007.
  10. A. Guillouzo, A. Corlu, C. Aninat, D. Glaise, F. Morel, and C. Guguen-Guillouzo, “The human hepatoma HepaRG cells: A highly differentiated model for studies of liver metabolism and toxicity of xenobiotics,” Chemico-Biological Interactions, vol. 168, no. 1, pp. 66–73, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. A. P. Li, “Screening for human ADME/Tox drug properties in drug discovery,” Drug Discovery Today, vol. 6, no. 7, pp. 357–366, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. A. P. Li, “Human hepatocytes: Isolation, cryopreservation and applications in drug development,” Chemico-Biological Interactions, vol. 168, no. 1, pp. 16–29, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. C. C. Bell, D. F. G. Hendriks, S. M. L. Moro et al., “Characterization of primary human hepatocyte spheroids as a model system for drug-induced liver injury, liver function and disease,” Scientific Reports, vol. 6, p. 25187, 2016. View at Publisher · View at Google Scholar
  14. R. Kostadinova, F. Boess, D. Applegate et al., “A long-term three dimensional liver co-culture system for improved prediction of clinically relevant drug-induced hepatotoxicity,” Toxicology and Applied Pharmacology, vol. 268, no. 1, pp. 1–16, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. J. J. Xu, P. V. Henstock, M. C. Dunn, A. R. Smith, J. R. Chabot, and D. de Graaf, “Cellular imaging predictions of clinical drug-induced liver injury,” Toxicological Sciences, vol. 105, no. 1, pp. 97–105, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. R. M. Tostões, S. B. Leite, M. Serra et al., “Human liver cell spheroids in extended perfusion bioreactor culture for repeated-dose drug testing,” Hepatology, vol. 55, no. 4, pp. 1227–1236, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Dash, M. B. Simmers, T. G. Deering et al., “Hemodynamic flow improves rat hepatocyte morphology, function, and metabolic activity in vitro,” American Journal of Physiology - Cell Physiology, vol. 304, no. 11, pp. C1053–C1063, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Choi, W. P. Pfund, M. E. Andersen, R. S. Thomas, H. J. Clewell, and E. L. Lecluyse, “Development of 3D dynamic flow model of human liver and its application to prediction of metabolic clearance of 7-ethoxycoumarin,” Tissue Engineering - Part C: Methods, vol. 20, no. 8, pp. 641–651, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. J. P. Miranda, S. B. Leite, U. Muller-Vieira, A. Rodrigues, M. J. T. Carrondo, and P. M. Alves, “Towards an extended functional hepatocyte in vitro culture,” Tissue Engineering C: Methods, vol. 15, no. 2, pp. 157–167, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Essig and G. Friedlander, “Tubular Shear Stress and Phenotype of Renal Proximal Tubular Cells,” Journal of the American Society of Nephrology, vol. 14, pp. S33–S35, 2003. View at Publisher · View at Google Scholar
  21. Y. Duan, N. Gotoh, Q. Yan et al., “Shear-induced reorganization of renal proximal tubule cell actin cytoskeleton and apical junctional complexes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 32, pp. 11418–11423, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. Z. Du, Y. Duan, Q. Yan, A. M. Weinstein, S. Weinbaum, and T. Wang, “Mechanosensory function of microvilli of the kidney proximal tubule,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 35, pp. 13068–13073, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. D. Maggiorani, R. Dissard, M. Belloy et al., “Shear stress-induced alteration of epithelial organization in human renal tubular cells,” PLoS ONE, vol. 10, no. 7, Article ID e0131416, pp. 1–21, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. K. A. Homan, D. B. Kolesky, M. A. Skylar-Scott et al., “Bioprinting of 3D Convoluted Renal Proximal Tubules on Perfusable Chips,” Scientific Reports, vol. 6, p. 34845, 2016. View at Publisher · View at Google Scholar · View at Scopus
  25. H. Rashidi, S. Alhaque, D. Szkolnicka, O. Flint, and D. C. Hay, “Fluid shear stress modulation of hepatocyte-like cell function,” Archives of Toxicology, vol. 90, no. 7, pp. 1757–1761, 2016. View at Publisher · View at Google Scholar · View at Scopus
  26. J. M. Pedersen, Y. Shim, V. Hans et al., “Fluid Dynamic Modeling to Support the Development of Flow-Based Hepatocyte Culture Systems for Metabolism Studies,” Frontiers in Bioengineering and Biotechnology, vol. 4, p. 72, 2016. View at Publisher · View at Google Scholar
  27. N. L. Cowger, E. Benes, P. L. Allen, and T. G. Hammond, “Expression of renal cell protein markers is dependent on initial mechanical culture conditions,” Journal of Applied Physiology, vol. 92, no. 2, pp. 691–700, 2002. View at Google Scholar
  28. S. A. Hoffmann, U. Müller-Vieira, K. Biemel et al., “Analysis of drug metabolism activities in a miniaturized liver cell bioreactor for use in pharmacological studies,” Biotechnology and Bioengineering, vol. 109, no. 12, pp. 3172–3181, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. S. M. King, J. W. Higgins, C. R. Nino et al., “3D proximal tubule tissues recapitulate key aspects of renal physiology to enable nephrotoxicity testing,” Frontiers in Physiology, vol. 8, p. 123, 2017. View at Publisher · View at Google Scholar · View at Scopus
  30. D. A. Wolf and R. P. Schwarz, “Analysis of gravity-induced particle motion and fluid perfusion flow in the NASA-designed rotating zero-head-space tissue culture vessel,” Tech. Rep., NASA, 1991. View at Google Scholar
  31. T. G. Hammond and J. M. Hammond, “Optimized suspension culture: the rotating-wall vessel,” The American Journal of Physiology—Renal Physiology, vol. 281, no. 1, pp. F12–F25, 2001. View at Google Scholar · View at Scopus
  32. T. Niiya, M. Murakami, T. Aoki, N. Murai, Y. Shimizu, and M. Kusano, “Immediate increase of portal pressure, reflecting sinusoidal shear stress, induced liver regeneration after partial hepatectomy,” Journal of Hepato-Biliary-Pancreatic Surgery, vol. 6, no. 3, pp. 275–280, 1999. View at Publisher · View at Google Scholar · View at Scopus
  33. T. Hammond, P. Allen, and H. Birdsall, “Is There a Space-Based Technology Solution to Problems with Preclinical Drug Toxicity Testing?” Pharmaceutical Research, vol. 33, no. 7, pp. 1545–1551, 2016. View at Publisher · View at Google Scholar · View at Scopus
  34. T. G. Hammond, E. Benes, K. C. O’Reilly et al., “Mechanical culture conditions effect gene expression: gravity-induced changes on the space shuttle,” Physiological Genomics, vol. 3, no. 3, pp. 163–173, 2000. View at Google Scholar
  35. J. H. Kaysen, W. C. Campbell, R. R. Majewski et al., “Select de novo gene and protein expression during renal epithelial cell culture in rotating wall vessels is shear stress dependent,” Journal of Membrane Biology, vol. 168, no. 1, pp. 77–89, 1999. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Sukasem, M. Chamnanphon, N. Koomdee et al., “High plasma efavirenz concentration and CYP2B6 polymorphisms in Thai HIV-1 infections,” Drug Metabolism and Pharmacokinetics, vol. 28, no. 5, pp. 391–397, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. C. Sukasem, T. R. Cressey, P. Prapaithong et al., “Pharmacogenetic markers of CYP2B6 associated with efavirenz plasma concentrations in HIV-1 infected Thai adults,” British Journal of Clinical Pharmacology, vol. 74, no. 6, pp. 1005–1012, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Rohrbacher, A. Kirchhof, G. Geisslinger, and J. Lötsch, “Pyrosequencing™-based screening for genetic polymorphisms in cytochrome P450 2B6 of potential clinical relevance,” Pharmacogenomics, vol. 7, no. 7, pp. 995–1002, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. N. Yuce-Artun, G. Kose, and H. S. Suzen, “Allele and genotype frequencies of CYP2B6 in a Turkish population,” Molecular Biology Reports, vol. 41, no. 6, pp. 3891–3896, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. N. Yuce-Artun, B. Baskak, E. T. Ozel-Kizil et al., “Influence of CYP2B6 and CYP2C19 polymorphisms on sertraline metabolism in major depression patients,” International Journal of Clinical Pharmacy, vol. 38, no. 2, pp. 388–394, 2016. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Martignoni, G. M. Groothuis, and R. d. Kanter, “Species differences between mouse, rat, dog, monkey and human CYP-mediated drug metabolism, inhibition and induction,” Expert Opinion on Drug Metabolism & Toxicology, vol. 2, no. 6, pp. 875–894, 2006. View at Publisher · View at Google Scholar
  42. C. Sukasem and S. Sungkanuparph, “Would a CYP2B6 test help HIV patients being treated with efavirenz?” Pharmacogenomics, vol. 14, no. 9, pp. 999–1001, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. S.-F. Zhou, Y. M. Di, E. Chan et al., “Clinical pharmacogenetics and potential application in personalized medicine,” Current Drug Metabolism, vol. 9, no. 8, pp. 738–784, 2008. View at Publisher · View at Google Scholar · View at Scopus