Early prediction of polymyxin-induced nephrotoxicity with next-generation urinary kidney injury biomarkers

Toxicological Sciences

Volumn 137, Issue 2, 2014, Pages 278-291

  Keirstead, Natalie D ^a   Wagoner, Matthew P ^a   Bentley, Patricia ^a   Blais, Marie ^a   Brown, Crystal ^a   Cheatham, Letitia ^a   Ciaccio, Paul ^a,c   Dragan, Yvonne ^a   Ferguson, Douglas ^a   Fikes, Jim ^a   Galvin, Melanie ^b   Gupta, Anshul ^a   Hale, Michael ^a   Johnson, Nakpangi ^a   Luo, Wenli ^a   McGrath, Frank ^a   Pietras, Mark ^a   Price, Sally ^b   Sathe, Abhishek G ^a   Sasaki, Jennifer C ^a   Snow, Debra ^a   Walsky, Robert L ^a   Kern, Gunther ^a   more..

^a ASTRAZENECA   (United Kingdom)

^b AstraZenec UK Ltd   (United Kingdom)

^c CUBIST PHARMACEUTICALS INC   (United States)

Author keywords

AKI; Biomarkers; Colistin; Drug safety; Histopathology; HK 2; Immunohistochemistry; Infection; Kim 1; Nephrotoxicity; Polymyxin; RIFLE; Toxicology; Translation

Indexed keywords

BIOLOGICAL MARKER; COLISTIN; CREATININE; GLUTATHIONE TRANSFERASE ALPHA; KIM 1 PROTEIN; POLYMYXIN; POLYMYXIN B; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; CYTOTOXICITY; CYTOTOXICITY ASSAY; HISTOPATHOLOGY; IN VITRO STUDY; KIDNEY INJURY; KIDNEY TUBULE CELL; MALE; NEPHROTOXICITY; NONHUMAN; PREDICTION; RAT; UREA NITROGEN BLOOD LEVEL; WISTAR RAT;

AKI; BIOMARKERS; COLISTIN; DRUG SAFETY; HISTOPATHOLOGY; HK-2; IMMUNOHISTOCHEMISTRY; INFECTION; KIM-1; NEPHROTOXICITY; POLYMYXIN; RIFLE.; TOXICOLOGY; TRANSLATION;

ANIMALS; ANTI-BACTERIAL AGENTS; BIOLOGICAL MARKERS; CELL LINE; CELL SURVIVAL; COLISTIN; DATA INTERPRETATION, STATISTICAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EARLY DIAGNOSIS; KIDNEY DISEASES; MALE; POLYMYXIN B; PROGNOSIS; RATS; RATS, WISTAR;

EID: 84893352248     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kft247     Document Type: Article

References (46)

1. Abdelraouf, K., Braggs, K. H., Yin, T., Truong, L. D., Hu, M., and Tam, V. H. (2012). Characterization of polymyxin B-induced nephrotoxicity: Implications for dosing regimen design. Antimicrob. Agents Chemother. 56, 4625-4629.
2. Alessio, L., Berlin, A., Dell'Orto, A., Toffoletto, F., and Ghezzi, I. (1985). Reliability of urinary creatinine as a parameter used to adjust values of urinary biological indicators. Int. Arch. Occup. Environ. Health 55, 99-106.
3. Astashkina, A. I., Mann, B. K., Prestwich, G. D., and Grainger, D. W. (2012). Comparing predictive drug nephrotoxicity biomarkers in kidney 3-D primary organoid culture and immortalized cell lines. Biomaterials 33, 4712-4721.
4. Azad, M. K., Finnin, B. A., Poudyal, A., Davis K., Li, J., Hill, P. A., Nation, R. L., Velkov, T., and Li, J. (2013). Polymyxin B induces apoptosis in kidney proximal tubular cells. Antimicrob. Agents Chemother. 57, 4329-4335.
5. Bailly, V., Zhang, Z., Meier, W., Cate, R., Sanicola, M., and Bonventre, J. V. (2002). Shedding of kidney injury molecule-1, a putative adhesion protein involved in renal regeneration. J. Biol. Chem. 277, 39739-39748.
6. Bellomo, R., Ronco, C., Kellum, J. A., Mehta, R. L., and Palevsky, P. (2004). Acute renal failure-definition, outcome measures, animal models, fluid therapy and information technology needs: The Second International Consensus Conference of the Acute Dialysis Quality Initiative (ADQI) Group. Crit. Care 8, R204-R212.
7. Bonventre, J. V., Vaidya, V. S., Schmouder, R., Feig, P., and Dieterle, F. (2010). Next-generation biomarkers for detecting kidney toxicity. Nat. Biotechnol. 28, 436-440.
8. Chertow, G. M., Burdick, E., Honour, M., Bonventre, J. V., and Bates, D. W. (2005). Acute kidney injury, mortality, length of stay, and costs in hospitalized patients. J. Am. Soc. Nephr. 16, 3365-3370.
9. Christensen, E. I., and Willnow, T. E. (1999). Essential role of megalin in renal proximal tubule for vitamin homeostasis. J. Am. Soc. Nephr. 10, 2224-2236.
10. Cui, S., Verroust, P. J., Moestrup, S. K., and Christensen, E. I. (1996). Megalin/gp330 mediates uptake of albumin in renal proximal tubule. Am. J. Physiol. 271(4 Pt 2), F900-F907.
11. Danner, R. L., Joiner, K. A., Rubin, M., Patterson, W. H., Johnson, N., Ayers, K. M., and Parrillo, J. E. (1989). Purification, toxicity, and antiendotoxin activity of polymyxin B nonapeptide. Antimicrob. Agents Chemother. 33, 1428-1434.
12. DesRochers, T. M., Suter, L., Roth, A., and Kaplan, D. L. (2013). Bioengineered 3D human kidney tissue, a platform for the determination of nephrotoxicity. PLoS One 8, e59219.
13. Dieterle, F., Sistare, F., Goodsaid, F., Papaluca, M., Ozer, J. S., Webb, C. P., Baer, W., Senagore, A., Schipper, M. J., Vonderscher, J., et al. (2010). Renal biomarker qualification submission: A dialog between the FDA-EMEA and Predictive Safety Testing Consortium. Nat. Biotechnol. 28, 455-462.
14. Falagas, M. E., Fragoulis, K. N., Kasiakou, S. K., Sermaidis, G. J., and Michalopoulos, A. (2005). Nephrotoxicity of intravenous colistin: A prospective evaluation. Int. J. Antimicrob. Agents 26, 504-507.
15. Garonzik, S. M., Li, J., Thamlikitkul, V., Paterson, D. L., Shoham, S., Jacob, J., Silveira, F. P., Forrest, A., and Nation, R. L. (2011). Population pharmacokinetics of colistin methanesulfonate and formed colistin in critically ill patients from a multicenter study provide dosing suggestions for various categories of patients. Antimicrob. Agents Chemother. 55, 3284-3294.
16. Gauthier, C., Nguyen-Simonnet, H., Vincent, C., Revillard, J. P., and Pellet, M. V. (1984). Renal tubular absorption of beta 2 microglobulin. Kidney Int. 26, 170-175.
17. Haase, M., Bellomo, R., Devarajan, P., Schlattmann, P., and Haase-Fielitz, A.; NGAL Meta-analysis Investigator Group. (2009). Accuracy of neutrophil gelatinase-associated lipocalin (NGAL) in diagnosis and prognosis in acute kidney injury: A systematic review and meta-analysis. Am. J. Kidney Dis. 54, 1012-1024.
18. Han, W. K., Bailly, V., Abichandani, R., Thadhani, R., and Bonventre, J. V. (2002). Kidney Injury Molecule-1 (KIM-1): A novel biomarker for human renal proximal tubule injury. Kidney Int. 62, 237-244.
19. Harrison, D. J., Kharbanda, R., Cunningham, D. S., McLellan, L. I., and Hayes, J. D. (1989). Distribution of glutathione S-transferase isoenzymes in human kidney: Basis for possible markers of renal injury. J. Clin. Pathol. 42, 624-628.
20. Hartzell, J. D., Neff, R., Ake, J., Howard, R., Olson, S., Paolino, K., Vishnepolsky, M., Weintrob, A., and Wortmann, G. (2009). Nephrotoxicity associated with intravenous colistin (colistimethate sodium) treatment at a tertiary care medical center. Clin. Infect. Dis. 48, 1724-1728.
21. Hvidberg, V., Jacobsen, C., Strong, R. K., Cowland, J. B., Moestrup, S. K., and Borregaard, N. (2005). The endocytic receptor megalin binds the iron transporting neutrophil-gelatinase-associated lipocalin with high affinity and mediates its cellular uptake. FEBS Lett. 579, 773-777.
22. Koyner, J. L., Vaidya, V. S., Bennett, M. R., Ma, Q., Worcester, E., Akhter, S. A., Raman, J., Jeevanandam, V., O'Connor, M. F., Devarajan, P., et al. (2010). Urinary biomarkers in the clinical prognosis and early detection of acute kidney injury. Clin. J. Am. Soc. Nephrol. 5, 2154-2165.
23. Landman, D., Georgescu, C., Martin, D. A., and Quale, J. (2008). Polymyxins revisited. Clin. Microbiol. Rev. 21, 449-465.
24. Li, J., Nation, R. L., Turnidge, J. D., Milne, R. W., Coulthard, K., Rayner, C. R., and Paterson, D. L. (2006). Colistin: The re-emerging antibiotic for multidrug-resistant Gram-negative bacterial infections. Lancet Infect. Dis. 6, 589-601.
25. Li, M., Balamuthusamy, S., Simon, E. E., and Batuman, V. (2008). Silencing megalin and cubilin genes inhibits myeloma light chain endocytosis and ameliorates toxicity in human renal proximal tubule epithelial cells. Am. J. Physiol. Renal Physiol. 295, F82-F90.
26. Lopez-Novoa, J. M., Quiros, Y., Vicente, L., Morales, A. I., and Lopez-Hernandez, F. J. (2011). New insights into the mechanism of aminoglycoside nephrotoxicity: An integrative point of view. Kidney Int. 79, 33-45.
27. Magee, T. V., Brown, M. F., Starr, J. T., Ackley, D. C., Abramite, J. A., Aubrecht, J., Butler, A., Crandon, J. L., Dib-Hajj, F., Flanagan, M. E., et al. (2013). Discovery of dap-3 polymyxin analogues for the treatment of multidrug-resistant gram-negative nosocomial infections. J. Med. Chem. 56, 5079-5093.
28. Mingeot-Leclercq, M. P., Tulkens, P. M., Denamur, S., Vaara, T., and Vaara, M. (2012). Novel polymyxin derivatives are less cytotoxic than polymyxin B to renal proximal tubular cells. Peptides 35, 248-252.
29. Moestrup, S. K., Cui, S., Vorum, H., Bregengård, C., Bjørn, S. E., Norris, K., Gliemann, J., and Christensen, E. I. (1995). Evidence that epithelial glycoprotein 330/megalin mediates uptake of polybasic drugs. J. Clin. Invest. 96, 1404-1413.
30. Mori, K., and Nakao, K. (2007). Neutrophil gelatinase-associated lipocalin as the real-time indicator of active kidney damage. Kidney Int. 71, 967-970.
31. Pappo, I., Bercovier, H., Berry, E., Gallilly, R., Feigin, E., and Freund, H. R. (1995). Antitumor necrosis factor antibodies reduce hepatic steatosis during total parenteral nutrition and bowel rest in the rat. J. Parenter. Enteral. Nutr. 19, 80-82.
32. Pinches, M. D., Betts, C. J., Bickerton, S. J., Beattie, L., Burdett, L. D., Thomas, H. T., Derbyshire, N. A., Moores, M., and Price, S. A. (2012). Evaluation of novel urinary renal biomarkers: Biological variation and reference change values. Toxicol. Pathol. 40, 541-549.
33. Prowle, J. R., Liu, Y. L., Licari, E., Bagshaw, S. M., Egi, M., Haase, M., Haase-Fielitz, A., Kellum, J. A., Cruz, D., Ronco, C., et al. (2011). Oliguria as predictive biomarker of acute kidney injury in critically ill patients. Crit. Care 15, R172.
34. Ricci, Z., Cruz, D., and Ronco, C. (2008). The RIFLE criteria and mortality in acute kidney injury: A systematic review. Kidney Int. 73, 538-546.
35. Rozell, B., Hansson, H. A., Guthenberg, C., Tahir, M. K., and Mannervik, B. (1993). Glutathione transferases of classes alpha, mu and pi show selective expression in different regions of rat kidney. Xenobiotica 23, 835-849.
36. Russo, L. M., Sandoval, R. M., McKee, M., Osicka, T. M., Collins, A. B., Brown, D., Molitoris, B. A., and Comper, W. D. (2007). The normal kidney filters nephrotic levels of albumin retrieved by proximal tubule cells: Retrieval is disrupted in nephrotic states. Kidney Int. 71, 504-513.
37. Servais, H., Ortiz, A., Devuyst, O., Denamur, S., Tulkens, P. M., and Mingeot-Leclercq, M. P. (2008). Renal cell apoptosis induced by nephrotoxic drugs: Cellular and molecular mechanisms and potential approaches to modulation. Apoptosis 13, 11-32.
38. Servais, H., Van Der Smissen, P., Thirion, G., Van der Essen, G., Van Bambeke, F., Tulkens, P. M., and Mingeot-Leclercq, M. P. (2005). Gentamicin-induced apoptosis in LLC-PK1 cells: Involvement of lysosomes and mitochondria. Toxicol. Appl. Pharmacol. 206, 321-333.
39. Smith, R., and Coast, J. (2013). The true cost of antimicrobial resistance. BMJ 346, f1493.
40. Stonard, M. D., Gore, C. W., Oliver, G. J., and Smith, I. K. (1987). Urinary enzymes and protein patterns as indicators of injury to different regions of the kidney. Fundam. Appl. Toxicol. 9, 339-351.
41. Takano, M., Nakanishi, N., Kitahara, Y., Sasaki, Y., Murakami, T., and Nagai, J. (2002). Cisplatin-induced inhibition of receptor-mediated endocytosis of protein in the kidney. Kidney Int. 62, 1707-1717.
42. Vaara, M., and Vaara, T. (2013). The novel polymyxin derivative NAB739 is remarkably less cytotoxic than polymyxin B and colistin to human kidney proximal tubular cells. Int. J. Antimicrob. Agents 41, 292-293.
43. Vaidya, V. S., Ozer, J. S., Dieterle, F., Collings, F. B., Ramirez, V., Troth, S., Muniappa, N., Thudium, D., Gerhold, D., Holder, D. J., et al. (2010). Kidney injury molecule-1 outperforms traditional biomarkers of kidney injury in preclinical biomarker qualification studies. Nat. Biotechnol. 28, 478-485.
44. Wadey, R. M., Pinches, M. G., Jones, H. B., Riccardi, D., and Price, S. A. (2013). Tissue expression and correlation of a panel of urinary biomarkers following cisplatin-induced kidney injury. Toxicol. Pathol. doi: 10.1177/0192623313492044.
45. Wallace, S. J., Li, J., Nation, R. L., Rayner, C. R., Taylor, D., Middleton, D., Milne, R. W., Coulthard, K., and Turnidge, J. D. (2008). Subacute toxicity of colistin methanesulfonate in rats: Comparison of various intravenous dosage regimens. Antimicrob. Agents Chemother. 52, 1159-1161.
46. Waterer, G. W., and Wunderink, R. G. (2001). Increasing threat of Gramnegative bacteria. Crit. Care Med. 29, N75-N81.