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Molecular and Cellular Biochemistry

, Volume 428, Issue 1–2, pp 101–108 | Cite as

MATE-1 modulation by kinin B1 receptor enhances cisplatin efflux from renal cells

  • Gabriel R. Estrela
  • Frederick Wasinski
  • Raphael J. F. Felizardo
  • Laura L. Souza
  • Niels O. S. Câmara
  • Michael Bader
  • Ronaldo C. Araujo
Article

Abstract

Cisplatin is a drug widely used in chemotherapy that frequently causes severe renal dysfunction. Organic transporters have an important role to control the absorption and excretion of cisplatin in renal cells. Deletion and blockage of kinin B1 receptor has already been show to protect against cisplatin-induced acute kidney injury. To test whether it exerts its protective function by modulating the organic transporters in kidney, we studied kinin B1 receptor knockout mice and treatment with a receptor antagonist at basal state and in presence of cisplatin. Cisplatin administration caused downregulation of renal organic transporters; in B1 receptor knockout mice, this downregulation of organic transporters in kidney was absent; and treatment by a B1 receptor antagonist attenuated the downregulation of the transporter MATE-1. Moreover, kinin B1 receptor deletion and blockage at basal state resulted in higher renal expression of MATE-1. Moreover we observed that kinin B1 receptor deletion and blockage result in less accumulation of platinum in renal tissue. Thus, we propose that B1 receptor deletion and blockage protect the kidney from cisplatin-induced acute kidney injury by upregulating the expression of MATE-1, thereby increasing the efflux of cisplatin from renal cells.

Keywords

Cisplatin nephrotoxicity Organic transporters Kinins 

Notes

Acknowledgements

This work was supported by FAPESP grants 2013/06207-6, 2015/20082-7 and by CAPES/PROBRAL grant 7191/15-4.

Compliance with ethical standards

Conflict of interest

All the authors declared no competing interests.

References

  1. 1.
    Arany I, Safirstein RL (2003) Cisplatin nephrotoxicity. Semin Nephrol 23:460–464CrossRefPubMedGoogle Scholar
  2. 2.
    Miller RP, Tadagavadi RK, Ramesh G, Reeves WB (2010) Mechanisms of Cisplatin nephrotoxicity. Toxins (Basel) 2:2490–2518CrossRefGoogle Scholar
  3. 3.
    Thadhani R, Pascual M, Bonventre JV (1996) Acute renal failure. N Engl J Med 334:1448–1460CrossRefPubMedGoogle Scholar
  4. 4.
    Morisaki T, Matsuzaki T, Yokoo K, Kusumoto M, Iwata K, Hamada A, Saito H (2008) Regulation of renal organic ion transporters in cisplatin-induced acute kidney injury and uremia in rats. Pharm Res 25:2526–2533CrossRefPubMedGoogle Scholar
  5. 5.
    Yao X, Panichpisal K, Kurtzman N, Nugent K (2007) Cisplatin nephrotoxicity: a review. Am J Med Sci 334:115–124CrossRefPubMedGoogle Scholar
  6. 6.
    Motohashi H, Inui K (2013) Organic cation transporter OCTs (SLC22) and MATEs (SLC47) in the human kidney. Aaps J 15: 581–588.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Wang L, Sweet DH (2013) Renal organic anion transporters (SLC22 family): expression, regulation, roles in toxicity, and impact on injury and disease. Aaps J 15:53–69.CrossRefPubMedGoogle Scholar
  8. 8.
    Matsuzaki T, Morisaki T, Sugimoto W, Yokoo K, Sato D, Nonoguchi H, Tomita K, Terada T, Inui K, Hamada A, Saito H (2008) Altered pharmacokinetics of cationic drugs caused by down-regulation of renal rat organic cation transporter 2 (Slc22a2) and rat multidrug and toxin extrusion 1 (Slc47a1) in ischemia/reperfusion-induced acute kidney injury. Drug Metab Dispos 36:649–654CrossRefPubMedGoogle Scholar
  9. 9.
    Nies AT, Koepsell H, Damme K and Schwab M (2011) Organic cation transporters (OCTs, MATEs), in vitro and in vivo evidence for the importance in drug therapy. Handb Exp Pharmacol:105–67.Google Scholar
  10. 10.
    Ciarimboli G, Lancaster CS, Schlatter E, Franke RM, Sprowl JA, Pavenstadt H, Massmann V, Guckel D, Mathijssen RH, Yang W, Pui CH, Relling MV, Herrmann E, Sparreboom A (2012) Proximal tubular secretion of creatinine by organic cation transporter OCT2 in cancer patients. Clin Cancer Res 18:1101–1108CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Ludwig T, Riethmuller C, Gekle M, Schwerdt G, Oberleithner H (2004) Nephrotoxicity of platinum complexes is related to basolateral organic cation transport. Kidney Int 66:196–202CrossRefPubMedGoogle Scholar
  12. 12.
    Filipski KK, Mathijssen RH, Mikkelsen TS, Schinkel AH, Sparreboom A (2009) Contribution of organic cation transporter 2 (OCT2) to cisplatin-induced nephrotoxicity. Clin Pharmacol Ther 86:396–402CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Kido Y, Matsson P, Giacomini KM (2011) Profiling of a prescription drug library for potential renal drug-drug interactions mediated by the organic cation transporter 2. J Med Chem 54:4548–4558CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Masuda Y, Inoue M, Miyata A, Mizuno S, Nanba H (2009) Maitake beta-glucan enhances therapeutic effect and reduces myelosupression and nephrotoxicity of cisplatin in mice. Int Immunopharmacol 9:620–626CrossRefPubMedGoogle Scholar
  15. 15.
    Otsuka M, Matsumoto T, Morimoto R, Arioka S, Omote H, Moriyama Y (2005) A human transporter protein that mediates the final excretion step for toxic organic cations. Proc Natl Acad Sci USA 102:17923–17928CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Tsuda M, Terada T, Mizuno T, Katsura T, Shimakura J, Inui K (2009) Targeted disruption of the multidrug and toxin extrusion 1 (mate1) gene in mice reduces renal secretion of metformin. Mol Pharmacol 75:1280–1286CrossRefPubMedGoogle Scholar
  17. 17.
    Nakamura T, Yonezawa A, Hashimoto S, Katsura T, Inui K (2010) Disruption of multidrug and toxin extrusion MATE1 potentiates cisplatin-induced nephrotoxicity. Biochem Pharmacol 80:1762–1767CrossRefPubMedGoogle Scholar
  18. 18.
    Marceau F, Bachvarov DR (1998) Kinin receptors. Clin Rev Allergy Immunol 16:385–401CrossRefPubMedGoogle Scholar
  19. 19.
    Regoli D, Barabe J (1980) Pharmacology of bradykinin and related kinins. Pharmacol Rev 32:1–46PubMedGoogle Scholar
  20. 20.
    Pereira RL, Buscariollo BN, Correa-Costa M, Semedo P, Oliveira CD, Reis VO, Maquigussa E, Araujo RC, Braga TT, Soares MF, Moura IC, Malheiros DM, Filho AP, Keller AC, Camara NO (2011) Bradykinin receptor 1 activation exacerbates experimental focal and segmental glomerulosclerosis. Kidney Int 79:1217–1227CrossRefPubMedGoogle Scholar
  21. 21.
    Klein J, Gonzalez J, Duchene J, Esposito L, Pradere JP, Neau E, Delage C, Calise D, Ahluwalia A, Carayon P, Pesquero JB, Bader M, Schanstra JP and Bascands JL (2009) Delayed blockade of the kinin B1 receptor reduces renal inflammation and fibrosis in obstructive nephropathy. Faseb J 23:134–142.CrossRefPubMedGoogle Scholar
  22. 22.
    Klein J, Gonzalez J, Decramer S, Bandin F, Neau E, Salant DJ, Heeringa P, Pesquero JB, Schanstra JP, Bascands JL (2010) Blockade of the kinin B1 receptor ameloriates glomerulonephritis. J Am Soc Nephrol 21:1157–1164CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Wang PH, Campanholle G, Cenedeze MA, Feitoza CQ, Goncalves GM, Landgraf RG, Jancar S, Pesquero JB, Pacheco-Silva A, Camara NO (2008) Bradykinin [corrected] B1 receptor antagonism is beneficial in renal ischemia–reperfusion injury. PLoS ONE 3:e3050CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Wang PH, Cenedeze MA, Pesquero JB, Pacheco-Silva A, Camara NO (2006) Influence of bradykinin B1 and B2 receptors in the immune response triggered by renal ischemia–reperfusion injury. Int Immunopharmacol 6:1960–1965CrossRefPubMedGoogle Scholar
  25. 25.
    Estrela GR, Wasinski F, Almeida DC, Amano MT, Castoldi A, Dias CC, Malheiros DM, Almeida SS, Paredes-Gamero EJ, Pesquero JB, Barros CC, Camara NO, Araujo RC (2014) Kinin B1 receptor deficiency attenuates cisplatin-induced acute kidney injury by modulating immune cell migration. J Mol Med (Berl) 92:399–409Google Scholar
  26. 26.
    Estrela GR, Wasinski F, Bacurau RF, Malheiros DM, Camara NO, Araujo RC (2014) Kinin B2 receptor deletion and blockage ameliorates cisplatin-induced acute renal injury. Int Immunopharmacol 22:115–119CrossRefPubMedGoogle Scholar
  27. 27.
    Inui KI, Masuda S, Saito H (2000) Cellular and molecular aspects of drug transport in the kidney. Kidney Int 58:944–958CrossRefPubMedGoogle Scholar
  28. 28.
    Pabla N, Dong Z (2008) Cisplatin nephrotoxicity: mechanisms and renoprotective strategies. Kidney Int 73:994–1007CrossRefPubMedGoogle Scholar
  29. 29.
    Pohlen U, Rieger H, Meyer BT, Loddenkemper C, Buhr HJ, Heitland P, Koester HD, Schneider P (2007) Chemoembolization of lung metastases–pharmacokinetic behaviour of carboplatin in a rat model. Anticancer Res 27:809–815PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Gabriel R. Estrela
    • 1
    • 2
  • Frederick Wasinski
    • 1
    • 2
  • Raphael J. F. Felizardo
    • 2
  • Laura L. Souza
    • 4
  • Niels O. S. Câmara
    • 3
  • Michael Bader
    • 4
  • Ronaldo C. Araujo
    • 1
    • 2
  1. 1.Department of BiophysicsFederal University of São PauloSão PauloBrazil
  2. 2.Department of Medicine, Division of NephrologyFederal University of São PauloSão PauloBrazil
  3. 3.Department of Immunology, Laboratory of Transplantation Immunobiology, Institute of Biomedical SciencesUniversity of São PauloSão PauloBrazil
  4. 4.Max Delbrück Center for Molecular MedicineBerlinGermany

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