Human proximal tubule epithelial cells cultured on hollow fibers: Living membranes that actively transport organic cations

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Jansen, J ^a,b   De Napoli, I E ^c   Fedecostante, M ^a,b   Schophuizen, C M S ^a,b   Chevtchik, N V ^c   Wilmer, M J ^a   Van Asbeck, A H ^a   Croes, H J ^a   Pertijs, J C ^a   Wetzels, J F M ^b   Hilbrands, L B ^b   Van Den Heuvel, L P ^b,d   Hoenderop, J G ^a   Stamatialis, D ^c   Masereeuw, R ^a,e  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF TWENTE   (Netherlands)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

4-(4-(DIMETHYLAMINO)STYRYL)-1-METHYLPYRIDINIUM IODIDE; ARTIFICIAL MEMBRANE; CATION; CIMETIDINE; HISTAMINE H2 RECEPTOR ANTAGONIST; METHYLAMINE; ORGANIC CATION TRANSPORTER; PROTEIN ZO1; PYRIDINIUM DERIVATIVE; SLC22A2 PROTEIN, HUMAN; TJP1 PROTEIN, HUMAN;

ARTIFICIAL MEMBRANE; CELL ADHESION; CELL LINE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; EPITHELIUM CELL; HUMAN; IMMUNOHISTOCHEMISTRY; ION TRANSPORT; KIDNEY PROXIMAL TUBULE; METABOLISM; PERMEABILITY; TIGHT JUNCTION;

CATIONS; CELL ADHESION; CELL LINE; CIMETIDINE; EPITHELIAL CELLS; HISTAMINE H2 ANTAGONISTS; HUMANS; IMMUNOHISTOCHEMISTRY; ION TRANSPORT; KIDNEY TUBULES, PROXIMAL; MEMBRANES, ARTIFICIAL; METHYLAMINES; ORGANIC CATION TRANSPORT PROTEINS; PERMEABILITY; PYRIDINIUM COMPOUNDS; TIGHT JUNCTIONS; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84947079585     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep16702     Document Type: Article

References (54)

1. Vanholder, R. et al. Chronic kidney disease as cause of cardiovascular morbidity and mortality. Nephrol Dial Transplant. 20, 1048-56 (2005).
2. Masereeuw, R. et al. The kidney and uremic toxin removal: glomerulus or tubule? Semin Nephrol. 34, 191-208 (2014).
3. Sun, H., Frassetto, L. & Benet, L. Z. Effects of renal failure on drug transport and metabolism. Pharmacol Therapeut. 109, 1-11 (2006).
4. Neirynck, N. et al. An update on uremic toxins. Int Urol Nephrol. 45, 139-50 (2013).
5. Vanholder, R., Schepers, E., Pletinck, A., Nagler, E. V. & Glorieux, G. The uremic toxicity of indoxyl sulfate and p-cresyl sulfate: a systematic review. J. Am Soc Nephrol. 25, 1897-907 (2014).
6. Poveda, J. et al. p-cresyl sulphate has pro-inflammatory and cytotoxic actions on human proximal tubular epithelial cells. Nephrol Dial Transplant. 29, 56-64 (2014).
7. Humes, H. D., Buffington, D., Westover, A. J., Roy, S. & Fissell, W. H. The bioartificial kidney: current status and future promise. Ped Nephrol. 29, 343-51 (2014).
8. Oo, Z. Y., Kandasamy, K., Tasnim, F. & Zink, D. A novel design of bioartificial kidneys with improved cell performance and haemocompatibility. J. Cell Mol Med. 17, 497-507 (2013).
9. Saito, A. et al. Evaluation of bioartificial renal tubule device prepared with lifespan-extended human renal proximal tubular epithelial cells. Nephrol Dial Transplant. 27, 3091-9 (2012).
10. Humes, H. D. et al. Metabolic replacement of kidney function in uremic animals with a bioartificial kidney containing human cells. Am J Kidney Dis. 39, 1078-87 (2002).
11. Humes, H. D. et al. Initial clinical results of the bioartificial kidney containing human cells in ICU patients with acute renal failure. Kidney Int. 66, 1578-88 (2004).
12. Tumlin, J. et al. Efficacy and safety of renal tubule cell therapy for acute renal failure. J. Am Soc Nephrol. 19, 1034-40 (2008).
13. Westover, A. J. et al. A bio-artificial renal epithelial cell system conveys survival advantage in a porcine model of septic shock. J. Tissue Eng Regen Med. doi:10.1002/term.1961 (2014).
14. Combes, A. N., Davies, J. A. & Little, M. H. Cell-cell interactions driving kidney morphogenesis. Curr Top Dev Biol. 112, 467-508 (2015).
15. Kruegel, J., Rubel, D. & Gross, O. Alport syndrome - insights from basic and clinical research. Nat Rev Nephrol. 9, 170-178 (2013).
16. Ni, M. et al. Characterization of membrane materials and membrane coatings for bioreactor units of bioartificial kidneys. Biomaterials. 32, 1465-76 (2011).
17. Zhang, H., Tasnim, F., Ying, J. Y. & Zink, D. The impact of extracellular matrix coatings on the performance of human renal cells applied in bioartificial kidneys. Biomaterials. 30, 2899-911 (2009).
18. Schophuizen, C. M. et al. Development of a living membrane comprising a functional human renal proximal tubule cell monolayer on polyethersulfone polymeric membrane. Acta Biomater. 14, 22-32 (2014).
19. Kimura, N. et al. Metformin is a superior substrate for renal organic cation transporter OCT2 rather than hepatic OCT1. Drug Metab Pharmacokinet. 20, 379-86 (2005).
20. Pietig, G. et al. Properties and regulation of organic cation transport in freshly isolated human proximal tubules. J. Biol Chem. 276, 33741-46 (2001).
21. Ciarimboli, G. et al. Cisplatin nephrotoxicity is critically mediated via the human organic cation transporter 2. Am J Pathol. 167, 1477-84 (2005).
22. Schophuizen, C. M. et al. Cationic uremic toxins affect human renal proximal tubule cell functioning through interaction with the organic cation transporter. Pflug Arch: Eur J Phy. 465, 1701-14 (2013).
23. Eloot, S. et al. Impact of hemodialysis duration on the removal of uremic retention solutes. Kidney Int. 73, 765-70 (2008).
24. D'Hooge, R. et al. Involvement of voltage- and ligand-gated Ca2+ channels in the neuroexcitatory and synergistic effects of putative uremic neurotoxins. Kidney Int. 63, 1764-75 (2003).
25. Glorieux, G. L. et al. In vitro study of the potential role of guanidines in leukocyte functions related to atherogenesis and infection. Kidney Int. 65, 2184-92 (2004).
26. Schepers, E. et al. Guanidino compounds as cause of cardiovascular damage in chronic kidney disease: an in vitro evaluation. Blood Purif. 30, 277-87 (2010).
27. Campbell, R. A., Grettie, D. P., Bartos, F., Bartos, D. & Marton, L. J. Uremic polyamine dysmetabolism. Proc Clin Dial Transplant Forum. 8, 194-8 (1978).
28. Dhondt, A., Vanholder, R., Van Biesen, W. & Lameire, N. The removal of uremic toxins. Kidney Int Suppl. 76, S47-59 (2000).
29. Igarashi, K., Ueda, S., Yoshida, K. & Kashiwagi, K. Polyamines in renal failure. Amino acids. 31, 477-83 (2006).
30. Pegg, A. E. Toxicity of polyamines and their metabolic products. Chem Res Toxicol. 26, 1782-800 (2013).
31. Jansen, J. et al. A morphological and functional comparison of proximal tubule cell lines established from human urine and kidney tissue. Exp Cell Res. 323, 87-99 (2014).
32. Wilmer, M. J. et al. Novel conditionally immortalized human proximal tubule cell line expressing functional influx and efflux transporters. Cell Tissue Res. 339, 449-57 (2010).
33. Mutsaers, H. A. et al. Uremic toxins inhibit renal metabolic capacity through interference with glucuronidation and mitochondrial respiration. Biochim Biophys Acta. 1832, 142-50 (2013).
34. Bonandrini, B. et al. Recellularization of well-preserved acellular kidney scaffold using embryonic stem cells. Tissue Eng Part A. 20, 1486-98 (2014).
35. Giebisch, G. & Windhager, E. The urinary system in Medical Physiology (eds Boron, W. F. et al.) 743-4 (Saunders 2003).
36. Kirk, A., Campbell, S., Bass, P., Mason, J. & Collins, J. Differential expression of claudin tight junction proteins in the human cortical nephron. Nephrol Dial Transplant. 25, 2107-19 (2010).
37. Guckel, D., Ciarimboli, G., Pavenstadt, H. & Schlatter, E. Regulation of organic cation transport in isolated mouse proximal tubules involves complex changes in protein trafficking and substrate affinity. Cell Physiol Biochem. 1, 269-81 (2012).
38. Oo, Z. Y. et al. The performance of primary human renal cells in hollow fiber bioreactors for bioartificial kidneys. Biomaterials. 32, 8806-15 (2011).
39. McMahon, H. T. & Boucrot, E. Membrane curvature at a glance. J. Cell Sci. 6, 1065-1070 (2015).
40. Jang, K. J. et al. Human kidney proximal tubule-on-a-chip for drug transport and nephrotoxicity assessment. Integr Biol (Camb). 5, 1119-29 (2013).
41. Pelis, R. M. & Wright, S. H. SLC22, SLC44, and SLC47 transporters-oganic anion and cation transporters: molecular and cellular properties. Curr Top Membr. 73, 233-261 (2014).
42. Urakami, Y., Akazawa, M., Saito, H., Okuda, M. & Inui, K. cDNA cloning, functional characterization, and tissue distribution of an alternatively spliced variant of organic cation transporter hOCT2 predominantly expressed in the human kidney. J. Am Soc Nephrol. 13, 1703-10 (2002).
43. Kido, Y., Matsson, P. & Giacomini, K. M. Profiling of a prescription drug library for potential renal drug-drug interactions mediated by the organic cation transporter 2. J Med Chem. 54, 4548-58 (2011).
44. Kimura, N., Masuda, S., Katsura, T. & Inui, K. Transport of guanidine compounds by human organic cation transporters, hOCT1 and hOCT2. Biochem Pharm. 77, 1429-36 (2009).
45. Winter, T. N., Elmquist, W. F. & Fairbanks, C. A. OCT2 and MATE1 provide bidirectional agmatine transport. Mol Pharm. 8, 133-42 (2011).
46. Humes, H. D., Buffington, D. A., MacKay, S. M., Funke, A. J. & Weitzel, W. F. Replacement of renal function in uremic animals with a tissue-engineered kidney. Nature biotechnol. 17, 451-5 (1999).
47. Humes, H. D., MacKay, S. M., Funke, A. J. & Buffington, D. A. Tissue engineering of a bioartificial renal tubule assist device: in vitro transport and metabolic characteristics. Kidney Int. 55, 2502-14 (1999).
48. Kuteykin-Teplyakov, K., Luna-Tortos, C., Ambroziak, K. & Loscher, W. Differences in the expression of endogenous efflux transporters in MDR1-transfected versus wildtype cell lines affect P-glycoprotein mediated drug transport. Br J Pharmacol. 160, 1453-63 (2010).
49. Takada, T., Suzuki, H. & Sugiyama, Y. Characterization of polarized expression of point- or deletion-mutated human BCRP/ABCG2 in LLC-PK1 cells. Pharm Res. 22, 458-64 (2005).
50. Ryan, M. J. et al. HK-2: an immortalized proximal tubule epithelial cell line from normal adult human kidney. Kidney Int. 45, 48-57 (1994).
51. Jenkinson, S. E. et al. The limitations of renal epithelial cell line HK-2 as a model of drug transporter expression and function in the proximal tubule. Pflug Arch: Eur J Phy. 464, 601-11 (2012).
52. Miller, J. H. Sodium-sensitive, probenecid-insensitive p-aminohippuric acid uptake in cultured renal proximal tubule cells of the rabbit. Proc Soc Exp Biol Med. 199, 298-304 (1992).
53. Jansen, J. et al. Biotechnological challenges of bioartificial kidney engineering. Biotech Adv. 32, 1317-27 (2014).
54. European medicines agency: committee for advanced therapies, Classification of advanced therapy medicinal products. Reflection paper. (2012) Available at: http://www.ema.europa.eu/docs/en-GB/document-library/Scientific-guideline/2012/12/WC500136422.pdf. (Accessed: 7th December 2012).