A morphological and functional comparison of proximal tubule cell lines established from human urine and kidney tissue

Experimental Cell Research

Volumn 323, Issue 1, 2014, Pages 87-99

  Jansen, J ^a   Schophuizen, C M S ^a   Wilmer, M J ^a   Lahham, S H M ^b   Mutsaers, H A M ^a   Wetzels, J F M ^a   Bank, R A ^b   Van den Heuvel, L P ^a,c   Hoenderop, J G ^a   Masereeuw, R ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Bioartificial kidney; ECM; Regenerative nephrology; Transport

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; COLLAGEN TYPE 1; COLLAGEN TYPE 4; FIBRONECTIN; INULIN; KALININ; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 4; ORGANIC CATION TRANSPORTER 2; UVOMORULIN;

ARTICLE; CELL CLONE; CELL FUNCTION; CELL LINE; CELL STRUCTURE; CONDITIONALLY IMMORTALIZED PROXIMAL TUBULAR EPITHELIAL CELL LINE 1; CONDITIONALLY IMMORTALIZED PROXIMAL TUBULAR EPITHELIAL CELL LINE 2; CONDITIONALLY IMMORTALIZED PROXIMAL TUBULAR EPITHELIAL CELL LINE URINE; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOCYTOCHEMISTRY; KIDNEY PARENCHYMA; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; REAL TIME POLYMERASE CHAIN REACTION; URINE; WESTERN BLOTTING;

BIOARTIFICIAL KIDNEY; ECM; REGENERATIVE NEPHROLOGY; TRANSPORT;

ATP-BINDING CASSETTE TRANSPORTERS; BIOARTIFICIAL ORGANS; CADHERINS; CELL ADHESION MOLECULES; CELL CULTURE TECHNIQUES; CELL LINE; COLLAGEN TYPE I; FIBRONECTINS; HUMANS; INULIN; KIDNEY TUBULES, PROXIMAL; KIDNEYS, ARTIFICIAL; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NEOPLASM PROTEINS; OCTAMER TRANSCRIPTION FACTOR-2; P-GLYCOPROTEIN; TISSUE ENGINEERING; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; URINE;

EID: 84896494157     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.02.011     Document Type: Article

References (58)

1. Fox C.S., Matsushita K., Woodward M., Bilo H.J., Chalmers J., Heerspink H.J., et al. Associations of kidney disease measures with mortality and end-stage renal disease in individuals with and without diabetes: a meta-analysis. Lancet 2012, 380:1662.
2. Mahmoodi B.K., Matsushita K., Woodward M., Blankestijn P.J., Cirillo M., Ohkubo T., et al. Associations of kidney disease measures with mortality and end-stage renal disease in individuals with and without hypertension: a meta-analysis. Lancet 2012, 380:1649.
3. Winearls C.G., Glassock R.J. Classification of chronic kidney disease in the elderly: pitfalls and errors. Nephron Clin. Pract. 2011, 119(Suppl 1):c2.
4. Krieter D.H., Hackl A., Rodriguez A., Chenine L., Moragues H.L., Lemke H.D., et al. Protein-bound uraemic toxin removal in haemodialysis and post-dilution haemodiafiltration. Nephrol., Dial., Transplant.: Off. Publ. Eur. Dial. Transplant Assoc.-Eur. Renal Assoc. 2010, 25:212.
5. Vanholder R., Van Laecke S., Glorieux G. What is new in uremic toxicity?. Pediatr. Nephrol. 2008, 23:1211.
6. Vanholder R., De Smet R. Pathophysiologic effects of uremic retention solutes. J. Am. Soc. Nephrol. 1999, 10:1815.
7. Morgan B.R., Ibrahim H.N. Long-term outcomes of kidney donors. Curr. Opin. Nephrol. Hypertens. 2011, 20:605.
8. Wolfe R.A., Ashby V.B., Milford E.L., Ojo A.O., Ettenger R.E., Agodoa L.Y., et al. Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant. N. Engl. J. Med. 1999, 341:1725.
9. Artz M.A., Boots J.M., Ligtenberg G., Roodnat J.I., Christiaans M.H., Vos P.F., et al. Conversion from cyclosporine to tacrolimus improves quality-of-life indices, renal graft function and cardiovascular risk profile. Am. J. Transplant.: Off. J. Am. Soc. Transplant. Am. Soc. Transplant Surg. 2004, 4:937.
10. Hoorn E.J., Walsh S.B., McCormick J.A., Furstenberg A., Yang C.L., Roeschel T., et al. The calcineurin inhibitor tacrolimus activates the renal sodium chloride cotransporter to cause hypertension. Nat. Med. 2011, 17:1304.
11. Segev D.L. Innovative strategies in living donor kidney transplantation. Nat. Rev. Nephrol. 2012, 8:332.
12. Humes H.D., Buffington D., Westover A.J., Roy S., Fissell W.H. The bioartificial kidney: current status and future promise. Pediatr. Nephrol. 2013.
13. Koepsell H., Endou H. The SLC22 drug transporter family. Pflugers Arch.: Eur. J. Physiol. 2004, 447:666.
14. Masereeuw R., Russel F.G. Regulatory pathways for ATP-binding cassette transport proteins in kidney proximal tubules. AAPS J. 2012, 14:883.
15. Anzai N., Ichida K., Jutabha P., Kimura T., Babu E., Jin C.J., et al. Plasma urate level is directly regulated by a voltage-driven urate efflux transporter URATv1 (SLC2A9) in humans. J. Biol. Chem. 2008, 283:26834.
16. Forster I.C., Hernando N., Biber J., Murer H. Proximal tubular handling of phosphate: a molecular perspective. Kidney Int. 2006, 70:1548.
17. Gekle M. Renal tubule albumin transport. Annu. Rev. Physiol. 2005, 67:573.
18. Triplitt C.L. Understanding the kidneys[U+05F3] role in blood glucose regulation. Am. J. Managed Care 2012, 18:S11.
19. Wilmer M.J., Saleem M.A., Masereeuw R., Ni L., van der Velden T.J., Russel F.G., et al. Novel conditionally immortalized human proximal tubule cell line expressing functional influx and efflux transporters. Cell Tissue Res. 2010, 339:449.
20. Gorvin C.M., Wilmer M.J., Piret S.E., Harding B., van den Heuvel L.P., Wrong O., et al. Receptor-mediated endocytosis and endosomal acidification is impaired in proximal tubule epithelial cells of Dent disease patients. Proc. Ntl. Acad. Sci. USA 2013, 110:7014.
21. 2+ release. Cell Calcium 2012, 51:452.
22. Mutsaers H.A., Wilmer M.J., Reijnders D., Jansen J., van den Broek P.H., Forkink M., et al. Uremic toxins inhibit renal metabolic capacity through interference with glucuronidation and mitochondrial respiration. Biochim. Biophys. Acta 2013, 1832:142.
23. Wilmer M.J., Kluijtmans L.A., van der Velden T.J., Willems P.H., Scheffer P.G., Masereeuw R., et al. Cysteamine restores glutathione redox status in cultured cystinotic proximal tubular epithelial cells. Biochim. Biophys. Acta 2011, 1812:643.
24. Dankers A.C., Mutsaers H.A., Dijkman H.B., van den Heuvel L.P., Hoenderop J.G., Sweep F.C., et al. Hyperuricemia influences tryptophan metabolism via inhibition of multidrug resistance protein 4 (MRP4) and breast cancer resistance protein (BCRP). Biochim. Biophys. Acta 2013.
25. Mutsaers H.A., van den Heuvel L.P., Ringens L.H., Dankers A.C., Russel F.G., Wetzels J.F., et al. Uremic toxins inhibit transport by breast cancer resistance protein and multidrug resistance protein 4 at clinically relevant concentrations. PLoS One 2011, 6:e18438.
26. Schophuizen C.M., Wilmer M.J., Jansen J., Gustavsson L., Hilgendorf C., Hoenderop J.G., et al. Cationic uremic toxins affect human renal proximal tubule cell functioning through interaction with the organic cation transporter. Pflugers Arch.: Eur. J. Physiol. 2013, 465:1701.
27. Rosenblatt J., Raff M.C., Cramer L.P. An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr. Biol. 2001, 11:1847.
28. Eisenhoffer G.T., Loftus P.D., Yoshigi M., Otsuna H., Chien C.B., Morcos P.A., et al. Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia. Nature 2012, 484:546.
29. van Setten P.A., van Hinsbergh V.W., van der Velden T.J., van de Kar N.C., Vermeer M., Mahan J.D., et al. Effects of TNF alpha on verocytotoxin cytotoxicity in purified human glomerular microvascular endothelial cells. Kidney Int. 1997, 51:1245.
30. Reubsaet F.A., Veerkamp J.H., Monnens L.A. Sulfated glycosaminoglycan content of glomerular and tubular basement membranes of individuals of different ages. Nephron 1985, 41:344.
31. Saleem M.A., O'Hare M.J., Reiser J., Coward R.J., Inward C.D., Farren T., et al. A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression. J. Am. Soc. Nephrol. 2002, 13:630.
32. Hills C.E., Jin T., Siamantouras E., Liu I.K., Jefferson K.P., Squires P.E. [U+05F3]Special k' and a loss of cell-to-cell adhesion in proximal tubule-derived epithelial cells: modulation of the adherens junction complex by ketamine. PLoS One. e71819 2013, 8.
33. van Aubel R.A., Smeets P.H., Peters J.G., Bindels R.J., Russel F.G. The MRP4/ABCC4 gene encodes a novel apical organic anion transporter in human kidney proximal tubules: putative efflux pump for urinary cAMP and cGMP. J. Am.Soc. Nephrol. 2002, 13:595.
34. Koenderink J.B., Geibel S., Grabsch E., De Pont J.J., Bamberg E., Friedrich T. Electrophysiological analysis of the mutated Na,K-ATPase cation binding pocket. J Biol. Chem. 2003, 278:51213.
35. van de Water F.M., Boleij J.M., Peters J.G., Russel F.G., Masereeuw R. Characterization of P-glycoprotein and multidrug resistance proteins in rat kidney and intestinal cell lines. Eur. J. Pharm. Sci.: Off. J. Eur. Fed. Pharm. Sci. 2007, 30:36.
36. Huls M., Brown C.D., Windass A.S., Sayer R., van den Heuvel J.J., Heemskerk S., et al. The breast cancer resistance protein transporter ABCG2 is expressed in the human kidney proximal tubule apical membrane. Kidney Int. 2008, 73:220.
37. Allen J.D., van Loevezijn A., Lakhai J.M., van der Valk M., van Tellingen O., Reid G., et al. Potent and specific inhibition of the breast cancer resistance protein multidrug transporter in vitro and in mouse intestine by a novel analogue of fumitremorgin C. Mol. Cancer Ther. 2002, 1:417.
38. Luders A.K., Saborowski R., Bickmeyer U. Inhibition of multidrug/xenobiotic resistance transporter by MK571 improves dye (Fura 2) accumulation in crustacean tissues from lobster, shrimp, and isopod. Comp. Biochem. Physiol. Toxicol. Pharmacol.: CBP 2009, 150:368.
39. Malmstrom K., Stange G., Murer H. Intracellular cascades in the parathyroid-hormone-dependent regulation of Na+/phosphate cotransport in OK cells. Biochem. J. 1988, 251:207.
40. 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.: Off. Publ. Eur. Dial. Transplant Assoc.-Eur. Renal Assoc. 2010, 25:2107.
41. Kwon O., Nelson W.J., Sibley R., Huie P., Scandling J.D., Dafoe D., et al. Backleak, tight junctions, and cell-cell adhesion in postischemic injury to the renal allograft. J. Clin. Invest. 1998, 101:2054.
42. Nony P.A., Schnellmann R.G. Interactions between collagen IV and collagen-binding integrins in renal cell repair after sublethal injury. Mol. Pharmacol. 2001, 60:1226.
43. Pozzi A., Zent R. Integrins in kidney disease. J. Am. Soc. Nephrol. 2013.
44. Giacomini K.M., Huang S.M. Transporters in drug development and clinical pharmacology. Clin. Pharmacol. Ther. 2013, 94:3.
45. Huls M., Schoeber J.P., Verfaillie C.M., Luttun A., Ulloa-Montoya F., Menke A.L., et al. Deficiency of either P-glycoprotein or breast cancer resistance protein protect against acute kidney injury. Cell Transplant. 2010, 19:1195.
46. Woroniecki R., Gaikwad A.B., Susztak K. Fetal environment, epigenetics, and pediatric renal disease. Pediatr. Nephrol. 2011, 26:705.
47. Terabayashi T., Sakaguchi M., Shinmyozu K., Ohshima T., Johjima A., Ogura T., et al. Phosphorylation of Kif26b promotes its polyubiquitination and subsequent proteasomal degradation during kidney development. PLoS One. e39714 2012, 7.
48. Uwai Y., Honjo H., Iwamoto K. Interaction and transport of kynurenic acid via human organic anion transporters hOAT1 and hOAT3. Pharmacol. Res.: Off. J. Italian Pharmacol. Soc. 2012, 65:254.
49. Hagos Y., Burckhardt G., Burckhardt B.C. Human organic anion transporter OAT1 is not responsible for glutathione transport but mediates transport of glutamate derivatives. Am. J. Physiol. Renal Physiol. 2013, 304:F403.
50. Wang L., Sweet D.H. Interaction of natural dietary and herbal anionic compounds and flavonoids with human organic anion transporters 1 (SLC22A6), 3 (SLC22A8), and 4 (SLC22A11). Evid.-Based Complementary Altern. Med.: eCAM 2013, 2013:612527.
51. Brown C.D., Sayer R., Windass A.S., Haslam I.S., De Broe M.E., D'Haese P.C., et al. Characterisation of human tubular cell monolayers as a model of proximal tubular xenobiotic handling. Toxicol. Appl. Pharmacol. 2008, 233:428.
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. Soc. Exp. Biol. Med. 1992, 199:298.
53. Yamaguchi H., Sugie M., Okada M., Mikkaichi T., Toyohara T., Abe T., et al. Transport of estrone 3-sulfate mediated by organic anion transporter OATP4C1: estrone 3-sulfate binds to the different recognition site for digoxin in OATP4C1. Drug Metab. Pharmacokinet. 2010, 25:314.
54. Ahlin G., Hilgendorf C., Karlsson J., Szigyarto C.A., Uhlen M., Artursson P. Endogenous gene and protein expression of drug-transporting proteins in cell lines routinely used in drug discovery programs. Drug Metab. Dispos.: Biol. Fate Chem. 2009, 37:2275.
55. Jenkinson S.E., Chung G.W., van Loon E., Bakar N.S., Dalzell A.M., Brown C.D. The limitations of renal epithelial cell line HK-2 as a model of drug transporter expression and function in the proximal tubule. Pflugers Arch.: Eur. J. Physiol. 2012, 464:601.
56. Lowenstein J. The anglerfish and uremic toxins. FASEB J.: Off. Publ. Fed. Am. Soc. Exp. Biol. 2011, 25:1781.
57. Marquez I.O., Tambra S., Luo F.Y., Li Y., Plummer N.S., Hostetter T.H., et al. Contribution of residual function to removal of protein-bound solutes in hemodialysis. Clin. J. Am. Soc. Nephrol. 2011, 6:290.
58. Wieser M., Stadler G., Jennings P., Streubel B., Pfaller W., Ambros P., et al. hTERT Alone immortalizes epithelial cells of renal proximal tubules without changing their functional characteristics. Am. J. Physiol. Renal Physiol. 2008, 295:F1365.