Entry of aminoglycosides into renal tubular epithelial cells via endocytosis-dependent and endocytosis-independent pathways

Biochemical Pharmacology

Volumn 90, Issue 4, 2014, Pages 331-337

  Nagai, Junya ^a   Takano, Mikihisa ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Aminoglycoside antibiotics; Cation channels; Endocytosis; Megalin; Renal tubular cells

Indexed keywords

4 AMINOHIPPURIC ACID; AMINOGLYCOSIDE DERIVATIVE; CATION CHANNEL; CHLORIDE CHANNEL; CLC 5 PROTEIN; CUBILIN; MEGALIN; ORGANIC ANION TRANSPORTER; ORGANIC CATION TRANSPORTER; PROBENECID; QUININE; UNCLASSIFIED DRUG;

CATION TRANSPORT; CELL TRANSPORT; DRUG DISTRIBUTION; DRUG EFFECT; DRUG PROTEIN BINDING; DRUG RECEPTOR BINDING; DRUG UPTAKE; ENDOCYTOSIS; HUMAN; KIDNEY DISTAL TUBULE; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SYSTEMIC THERAPY;

AMIKACIN (PUBCHEM CID: 37768); AMINOGLYCOSIDE ANTIBIOTICS; CATION CHANNELS; ENDOCYTOSIS; FUROSEMIDE (PUBCHEM CID: 3440); GADOLINIUM (PUBCHEM CID: 23982); GENTAMICIN (PUBCHEM CID: 3467); IODO-RESINIFERATOXIN (PUBCHEM CID: 6324614); MEGALIN; N-METHYLNICOTINEAMIDE (PUBCHEM CID: 64950); NETILMICIN (PUBCHEM CID: 441306); RENAL TUBULAR CELLS; RESINIFERATOXIN (PUBCHEM CID: 104826); STREPTOMYCIN (PUBCHEM CID: 5999); TOBRAMYCIN (PUBCHEM CID: 36294);

AMINOGLYCOSIDES; ANTI-BACTERIAL AGENTS; CARBOHYDRATE SEQUENCE; ENDOCYTOSIS; EPITHELIAL CELLS; HUMANS; KIDNEY TUBULES; MOLECULAR SEQUENCE DATA;

EID: 84904633516     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2014.05.018     Document Type: Note

References (75)

1. H.F. Chambers The aminoglycosides J.G. Hardman, L.E. Limbird, A.G. Gilman, Goodman & Gilman's the pharmacological basis of therapeutics 10th ed. 2001 McGraw-Hill New York, NY 1219 1238
2. G.L. Drusano, P.G. Ambrose, S.M. Bhavnani, J.S. Bertino, A.N. Nafziger, and A. Louie Back to the future: using aminoglycosides again and how to dose them optimally Clin Infect Dis 45 2007 753 760 (Pubitemid 47378891)
3. E. Durante-Mangoni, A. Grammatikos, R. Utili, and M.E. Falagas Do we still need the aminoglycosides Int J Antimicrob Agents 33 2009 201 205
4. K.H. Tan, M. Mulheran, A.J. Knox, and A.R. Smyth Aminoglycoside prescribing and surveillance in cystic fibrosis Am J Respir Crit Care Med 167 2003 819 823 (Pubitemid 36801767)
5. M.P. Mingeot-Leclercq, and P.M. Tulkens Aminoglycosides: nephrotoxicity Antimicrob Agents Chemother 43 1999 1003 1012 (Pubitemid 29214718)
6. J.M. Lopez-Novoa, Y. Quiros, L. Vicente, A.I. Morales, and F.J. Lopez-Hernandez New insights into the mechanism of aminoglycoside nephrotoxicity: an integrative point of view Kidney Int 79 2011 33 45
7. O.W. Guthrie Aminoglycoside induced ototoxicity Toxicology 30 249 2008 91 96
8. R.L. Slaughter, and D.M. Cappelletty Economic impact of aminoglycoside toxicity and its prevention through therapeutic drug monitoring Pharmacoeconomics 14 1998 385 394 (Pubitemid 28455686)
9. H.D. Humes Aminoglycoside nephrotoxicity Kidney Int 33 1988 900 911
10. 1) J Pharmacol Exp Ther 238 1986 1071 1076 (Pubitemid 16033251)
11. 1) J Pharmacol Exp Ther 261 1992 1200 1205
12. 1 kidney epithelial cell line J Pharmacol Exp Ther 268 1994 669 674 (Pubitemid 24085862)
13. B.A. Molitoris Cell biology of aminoglycoside nephrotoxicity: newer aspects Curr Opin Nephrol Hypertens 6 1997 384 388 (Pubitemid 27305414)
14. G. Laurent, B.K. Kishore, and P.M. Tulkens Aminoglycoside-induced renal phospholipidosis and nephrotoxicity Biochem Pharmacol 40 1990 2383 2392
15. J. Nagai, and M. Takano Molecular aspects of renal handling of aminoglycosides and strategies for preventing the nephrotoxicity Drug Metab Pharmacokinet 19 2004 159 170
16. H. Servais, A. Ortiz, O. Devuyst, S. Denamur, P.M. Tulkens, and M.P. Mingeot-Leclercq Renal cell apoptosis induced by nephrotoxic drugs: cellular and molecular mechanisms and potential approaches to modulation Apoptosis 13 1 2008 11 32
17. F.J. Silverblatt, and C. Kuehn Autoradiography of gentamicin uptake by the rat proximal tubule cell Kidney Int 15 1979 335 345 (Pubitemid 10219854)
18. A. Vandewalle, N. Farman, J.P. Morin, J.P. Fillastre, P.Y. Hatt, and J.P. Bonvalet Gentamicin incorporation along the nephron: autoradiographic study on isolated tubules Kidney Int 19 1981 529 539 (Pubitemid 11120899)
19. R.P. Wedeen, V. Batuman, C. Cheeks, E. Marquet, and H. Sobel Transport of gentamicin in rat proximal tubule Lab Invest 48 1998 212 223
20. D. Beauchamp, P. Gourde, and M.G. Bergeron Subcellular distribution of gentamicin in proximal tubular cells, determined by immunogold labeling Antimicrob Agents Chemother 35 1991 2173 2179
21. F.C. Luft, and S.A. Kleit Renal parenchymal accumulation of aminoglycoside antibiotics in rats J Infect Dis 130 1974 656 659
22. J. Fabre, M. Rudhardt, P. Blanchard, and C. Regamey Persistence of sisomicin and gentamicin in renal cortex and medulla compared with other organs and serum of rats Kidney Int 10 1976 444 449 (Pubitemid 8031152)
23. C. Josepovitz, E. Pastoriza-Munoz, D. Timmerman, M. Scott, S. Feldman, and G.J. Kaloyanides Inhibition of gentamicin uptake in rat renal cortex in vivo by aminoglycosides and organic polycations J Pharmacol Exp Ther 223 1982 314 321 (Pubitemid 12005727)
24. R.A. Giuliano, G.A. Verpooten, L. Verbist, R.P. Wedeen, and M.E. De Broe In vivo uptake kinetics of aminoglycosides in the kidney cortex of rats J Pharmacol Exp Ther 236 1986 470 475 (Pubitemid 16184244)
25. J. Schacht Isolation of an aminoglycoside receptor from guinea pig inner ear tissues and kidney Arch Otorhinolaryngol 224 1979 129 134 (Pubitemid 9254382)
26. M. Sastrasinh, T.C. Knauss, J.M. Weinberg, and H.D. Humes Identification of the aminoglycoside binding site in rat renal brush border membranes J Pharmacol Exp Ther 222 1982 350 358 (Pubitemid 12047263)
27. S.K. Moestrup, S. Cui, H. Vorum, C. Bregengård, S.E. Bjørn, and K. Norris et al. Evidence that epithelial glycoprotein 330/megalin mediates uptake of polybasic drugs J Clin Invest 96 1995 1404 1413
28. E.I. Christensen, and H. Birn Megalin and cubilin: multifunctional endocytic receptors Nat Rev Mol Cell Biol 3 2002 256 266 (Pubitemid 34619261)
29. E.I. Christensen, H. Birn, T. Storm, K. Weyer, and R. Nielsen Endocytic receptors in the renal proximal tubule Physiology (Bethesda) 27 2012 223 236
30. S. Cui, P.J. Verroust, S.K. Moestrup, and E.I. Christensen Megalin/gp330 mediates uptake of albumin in renal proximal tubule Am J Physiol 271 4 Pt 2 1996 F900 F907
31. H. Birn, J.C. Fyfe, C. Jacobsen, F. Mounier, P.J. Verroust, and H. Orskov et al. Cubilin is an albumin binding protein important for renal tubular albumin reabsorption J Clin Invest 105 2000 1353 1361 (Pubitemid 30322401)
32. J. Tauris, E.I. Christensen, A. Nykjaer, C. Jacobsen, C.M. Petersen, and T. Ovesen Cubilin and megalin co-localize in the neonatal inner ear Audiol Neurootol 14 2009 267 278
33. J. Nagai, H. Tanaka, N. Nakanishi, T. Murakami, and M. Takano Role of megalin in renal handling of aminoglycosides Am J Physiol Renal Physiol 281 2001 F337 F344
34. J. Nagai, T. Katsube, T. Murakami, and M. Takano Effect of gentamicin on pharmacokinetics of lysozyme in rats: interaction between megalin substrates in the kidney J Pharm Pharmacol 54 2002 1491 1496 (Pubitemid 35339315)
35. C. Schmitz, J. Hilpert, C. Jacobsen, C. Boensch, E.I. Christensen, and F.C. Luft et al. Megalin deficiency offers protection from renal aminoglycoside accumulation J Biol Chem 277 2002 618 622 (Pubitemid 34952099)
36. J. Gburek, H. Birn, P.J. Verroust, B. Goj, C. Jacobsen, and S.K. Moestrup et al. Renal uptake of myoglobin is mediated by the endocytic receptors megalin and cubilin Am J Physiol Renal Physiol 285 2003 F451 F458
37. J. Nagai, T. Komeda, R. Yumoto, and M. Takano Effect of protamine on the accumulation of gentamicin in opossum kidney epithelial cells J Pharm Pharmacol 65 3 2013 441 446
38. J. Nagai, T. Komeda, Y. Katagiri, R. Yumoto, and M. Takano Characterization of protamine uptake by opossum kidney epithelial cells Biol Pharm Bull 36 2013 1942 1949
39. R. Dagil, C. O'Shea, A. Nykjær, A.M. Bonvin, and B.B. Kragelund Gentamicin binds to the megalin receptor as a competitive inhibitor using the common ligand binding motif of complement type repeats: insight from the NMR structure of the 10th complement type repeat domain alone and in complex with gentamicin J Biol Chem 288 2013 4424 4435
40. E.I. Christensen, O. Devuyst, G. Dom, R. Nielsen, P. Van der Smissen, and P. Verroust et al. Loss of chloride channel ClC-5 impairs endocytosis by defective trafficking of megalin and cubilin in kidney proximal tubules Proc Nat Acad Sci USA 100 2003 8472 8477 (Pubitemid 36842569)
41. F. Jouret, A. Bernard, C. Hermans, G. Dom, S. Terryn, and T. Leal et al. Cystic fibrosis is associated with a defect in apical receptor-mediated endocytosis in mouse and human kidney J Am Soc Nephrol 18 2007 707 718 (Pubitemid 46434488)
42. C. Raggi, K. Fujiwara, T. Leal, F. Jouret, O. Devuyst, and S. Terryn Decreased renal accumulation of aminoglycoside reflects defective receptor-mediated endocytosis in cystic fibrosis and Dent's disease Pflugers Arch 462 2011 851 860
43. A. Whelton, and W.G. Walker Editorial intrarenal antibiotic distribution in health and disease Kidney Int 6 1974 131 137
44. W.M. Kluwe, and J.B. Hook Analysis of gentamicin uptake by rat renal cortical slices Toxicol Appl Pharmacol 45 1978 531 539 (Pubitemid 9001011)
45. E. Pastoriza-Munoz, R.L. Bowman, and G.J. Kaloyanides Renal tubular transport of gentamicin in the rat Kidney Int 16 1979 440 450 (Pubitemid 10195855)
46. 3H]gentamicin uptake in brush border and basolateral membrane vesicles from rat kidney cortex Biochem Pharmacol 35 1986 2253 2256 (Pubitemid 16069283)
47. K. Inui, S. Masuda, and H. Saito Cellular and molecular aspects of drug transport in the kidney Kidney Int 58 2000 944 958
48. S.E. Myrdal, K.C. Johnson, and P.S. Steyger Cytoplasmic and intra-nuclear binding of gentamicin does not require endocytosis Hear Res 204 2005 156 169 (Pubitemid 40733213)
49. R.M. Sandoval, and B.A. Molitoris Gentamicin traffics retrograde through the secretory pathway and is released in the cytosol via the endoplasmic reticulum Am J Physiol Renal Physiol 286 2004 F617 F624
50. S.E. Myrdal, and P.S. Steyger TRPV1 regulators mediate gentamicin penetration of cultured kidney cells Hear Res 204 2005 170 182 (Pubitemid 40733214)
51. G. Pethö, I. Izydorczyk, and P.W. Reeh Effects of TRPV1 receptor antagonists on stimulated iCGRP release from isolated skin of rats and TRPV1 mutant mice Pain 109 2004 284 290 (Pubitemid 38638705)
52. T. Karasawa, Q. Wang, Y. Fu, D.M. Cohen, and P.S. Steyger TRPV4 enhances the cellular uptake of aminoglycoside antibiotics J Cell Sci 121 Pt 17 2008 2871 2879
53. T. Voets, J. Prenen, J. Vriens, H. Watanabe, A. Janssens, and U. Wissenbach et al. Molecular determinants of permeation through the cation channel TRPV4 J Biol Chem 277 2002 33704 33710
54. W. Tian, M. Salanova, H. Xu, J.N. Lindsley, T.T. Oyama, and S. Anderson et al. Renal expression of osmotically responsive cation channel TRPV4 is restricted to water-impermeant nephron segments Am J Physiol Renal Physiol 287 2004 F17 F24
55. H. Servais, Y. Jossin, F. Van Bambeke, P.M. Tulkens, and M.P. Mingeot-Leclercq Gentamicin causes apoptosis at low concentrations in renal LLC-PK1 cells subjected to electroporation Antimicrob Agents Chemother 50 2006 1213 1221
56. S. Denamur, F. Van Bambeke, M.P. Mingeot-Leclercq, and P.M. Tulkens Apoptosis induced by aminoglycosides in LLC-PK1 cells: comparative study of neomycin, gentamicin, amikacin, and isepamicin using electroporation Antimicrob Agents Chemother 52 2008 2236 2238 (Pubitemid 351758566)
57. T. Sawada, J. Nagai, Y. Okada, R. Yumoto, and M. Takano Gadolinium modulates gentamicin uptake via an endocytosis-independent pathway in HK-2 human renal proximal tubular cell line Eur J Pharmacol 684 2012 146 153
58. A. Watanabe, J. Nagai, Y. Adachi, T. Katsube, Y. Kitahara, and T. Murakami et al. Targeted prevention of renal accumulation and toxicity of gentamicin by aminoglycoside binding receptor antagonists J Controlled Release 95 2004 423 433 (Pubitemid 38340493)
59. J. Nagai, M. Saito, Y. Adachi, R. Yumoto, and M. Takano Inhibition of gentamicin binding to rat renal brush-border membrane by megalin ligands and basic peptides J Controlled Release 112 2006 43 50
60. K. Tousova, L. Vyklicky, K. Susankova, J. Benedikt, and V. Vlachova Gadolinium activates and sensitizes the vanilloid receptor TRPV1 through the external protonation sites Mol Cell Neurosci 30 2005 207 217 (Pubitemid 41319675)
61. 2+-activated potassium channels Cell Biochem Biophys 65 2013 381 398
62. W. Marcotti, S.M. van Netten, and C.J. Kros The aminoglycoside antibiotic dihydrostreptomycin rapidly enters mouse outer hair cells through the mechano-electrical transducer channels J Physiol 567 2005 505 521 (Pubitemid 41301048)
63. A. Alharazneh, L. Luk, M. Huth, A. Monfared, P.S. Steyger, and A.G. Cheng et al. Functional hair cell mechanotransducer channels are required for aminoglycoside ototoxicity PLoS One 6 2011 e22347
64. R.S. Stepanyan, A.A. Indzhykulian, A.C. Vélez-Ortega, E.T. Boger, P.S. Steyger, and T.B. Friedman et al. TRPA1-mediated accumulation of aminoglycosides in mouse cochlear outer hair cells J Assoc Res Otolaryngol 12 2011 729 740
65. J.H. Lee, C. Park, S.J. Kim, H.J. Kim, G.S. Oh, and A. Shen et al. Different uptake of gentamicin through TRPV1 and TRPV4 channels determines cochlear hair cell vulnerability Exp Mol Med 45 2013 e12
66. A.A. Vu, G.S. Nadaraja, M.E. Huth, L. Luk, J. Kim, and R. Chai et al. Integrity and regeneration of mechanotransduction machinery regulate aminoglycoside entry and sensory cell death PLoS One 8 2013 e54794
67. K. Mizuta, A. Saito, T. Watanabe, M. Nagura, M. Arakawa, and F. Shimizu et al. Ultrastructural localization of megalin in the rat cochlear duct Hear Res 129 1999 83 91 (Pubitemid 29111610)
68. H.E. Farris, C.L. LeBlanc, J. Goswami, and A.J. Ricci Probing the pore of the auditory hair cell mechanotransducer channel in turtle J Physiol 558 2004 769 792 (Pubitemid 39199104)
69. A. Jara-Oseguera, I. Llorente, T. Rosenbaum, and L.D. Islas Properties of the inner pore region of TRPV1 channels revealed by block with quaternary ammoniums J Gen Physiol 132 2008 547 562
70. 2+ permeation through the nociceptor cation channel TRPA1 Biophys J 98 2010 773 783
71. A.B. Kroese, A. Das, and A.J. Hudspeth Blockage of the transduction channels of hair cells in the bullfrog's sacculus by aminoglycoside antibiotics Hear Res 37 1989 203 217
72. D.P. Nicolau, C.D. Freeman, P.P. Belliveau, C.H. Nightingale, J.W. Ross, and R. Quintiliani Experience with a once-daily aminoglycoside program administered to 2,184 adult patients Antimicrob Agents Chemother 39 1995 650 655
73. C.D. Freeman, D.P. Nicolau, P.P. Belliveau, and C.H. Nightingale Once-daily dosing of aminoglycosides: review and recommendations for clinical practice J Antimicrob Chemother 39 1997 677 686 (Pubitemid 27296406)
74. M.J. Rybak, B.J. Abate, S.L. Kang, M.J. Ruffing, S.A. Lerner, and G.L. Drusano Prospective evaluation of the effect of an aminoglycoside dosing regimen on rates of observed nephrotoxicity and ototoxicity Antimicrob Agents Chemother 43 1999 1549 1555 (Pubitemid 29331226)
75. K.M. Olsen, M.I. Rudis, J.A. Rebuck, J. Hara, D. Gelmont, and R. Mehdian et al. Effect of once-daily dosing vs. multiple daily dosing of tobramycin on enzyme markers of nephrotoxicity Crit Care Med 32 2004 1678 1682 (Pubitemid 39050517)