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Impact of intracellular chloride concentration on cisplatin accumulation in sensitive and resistant GLC4 cells

  • Milena Salerno
  • Dalila Yahia
  • Simplice Dzamitika
  • Elisabeth de Vries
  • Elene Pereira-Maia
  • Arlette Garnier-Suillerot
Original Paper

Abstract

Resistance to cisplatin [cis-diamminedichloroplatinum(II), CDDP] chemotherapy is a major problem in the clinic. Understanding the molecular basis of the intracellular accumulation of CDDP and other platinum-based anticancer drugs is of importance in delineating the mechanism of resistance to these clinically important therapies. Different molecular mechanisms may coexist, but defective uptake of CDDP is one of the most consistently identified characteristics of cells selected for CDDP resistance. We have studied the impact of intracellular chloride concentration on platinum-based compound accumulation in the human GLC4, GLC4/CDDP, and K562 tumor cell lines. We show that (1) a decrease of intracellular chloride concentration yielded an increase of CDDP accumulation and vice versa and (2) the intracellular chloride concentration in GLC4/CDDP cells is higher than in sensitive cells, whereas CDDP accumulation shows the opposite behavior. The identification of chloride as a critical determinant of CDDP intracellular accumulation and the molecular mechanisms by which CDDP-resistant cells modulate chloride concentration may allow alternative therapeutic approaches. Our findings indicate that increase of intracellular chloride concentration may be a major determinant of CDDP resistance.

Keywords

Cisplatin Resistance Chloride 

Notes

Acknowledgments

This research was supported by grants from Université Paris 13 and CNRS. We thank to Ricarda Riina for her help.

References

  1. 1.
    Brenner J, Magill GB, Sordillo PP, Cheng EW, Yagoda A (1982) Cancer 50:2031–2033PubMedCrossRefGoogle Scholar
  2. 2.
    Rozencweig M, von Hoff DD, Slavik M, Muggia FM (1977) Ann Intern Med 86:803–812PubMedGoogle Scholar
  3. 3.
    Kartalou M, Essigmann JM (2001) Mutat Res 478:23–43PubMedGoogle Scholar
  4. 4.
    Wernyj RP, Morin PJ (2004) Drug Resist Update 7:227–232CrossRefGoogle Scholar
  5. 5.
    Wang D, Lippard SJ (2005) Nat Rev Drug Discov 4:307–320PubMedCrossRefGoogle Scholar
  6. 6.
    Kelland LR (2000) Drug Resist Update 3:139–141CrossRefGoogle Scholar
  7. 7.
    Baird RD, Kaye SB (2003) Eur J Cancer 39:2450–2461PubMedCrossRefGoogle Scholar
  8. 8.
    Oldenburg J, Begg AC, van Vugt MJ, Ruevekamp M, Schornagel JH, Pinedo HM, Los G (1994) Cancer Res 54:487–493PubMedGoogle Scholar
  9. 9.
    Andrews PA, Howell SB (1990) Cancer Cells 2:35–43PubMedGoogle Scholar
  10. 10.
    Gately DP, Howell SB (1993) Br J Cancer 67:1171–1176PubMedGoogle Scholar
  11. 11.
    Pereira-Maia E, Garnier-Suillerot A (2003) J Biol Inorg Chem 8:626–634PubMedCrossRefGoogle Scholar
  12. 12.
    Lee EL, Shimizu T, Ise T, Numata T, Kohno K, Okada Y (2007) J Cell Physiol 211:513–521PubMedCrossRefGoogle Scholar
  13. 13.
    Zijlstra JG, de Vries EG, Mulder NH (1987) Cancer Res 47:1780–1784PubMedGoogle Scholar
  14. 14.
    Hospers GA, Mulder NH, de Jong B, de Ley L, Uges DR, Fichtinger-Schepman AM, Scheper RJ, de Vries EG (1988) Cancer Res 48:6803–6807PubMedGoogle Scholar
  15. 15.
    Lozzio CB, Lozzio BB (1975) Blood 45:321–334PubMedGoogle Scholar
  16. 16.
    Lim MC, Martin RB (1976) J Inorg Nucl Chem 38:1911CrossRefGoogle Scholar
  17. 17.
    Piwnica-Worms D, Jacob R, Horres CR, Lieberman M (1983) J Gen Physiol 81:731–748PubMedCrossRefGoogle Scholar
  18. 18.
    Verkman AS, Sellers MC, Chao AC, Leung T, Ketcham R (1989) Anal Biochem 178:355–361PubMedCrossRefGoogle Scholar
  19. 19.
    Garcia MA, Meizel S (1999) J Androl 20:88–93PubMedGoogle Scholar
  20. 20.
    El-Khateeb M, Appleton TG, Charles BG, Gahan LR (1999) J Pharm Sci 88:319–326PubMedCrossRefGoogle Scholar
  21. 21.
    Dzamitika S, Salerno M, Pereira-Maia E, Le Moyec L, Garnier-Suillerot A (2006) J Bioenerg Biomembr 38:11–21PubMedCrossRefGoogle Scholar
  22. 22.
    Chao AC, Dix JA, Sellers MC, Verkman AS (1989) Biophys J 56:1071–1081PubMedCrossRefGoogle Scholar
  23. 23.
    Koncz C, Daugirdas JT (1994) Am J Physiol 267:H2114–H2123PubMedGoogle Scholar
  24. 24.
    Amorino GP, Fox MH (1996) J Membr Biol 152:217–222PubMedCrossRefGoogle Scholar
  25. 25.
    Huang H, Zhu L, Reid BR, Drobny GP, Hopkins PB (1995) Science 270:1842–1845PubMedCrossRefGoogle Scholar
  26. 26.
    Jiang S, Song MJ, Shin EC, Lee MO, Kim SJ, Park JH (1999) Hepatology 29:101–110PubMedCrossRefGoogle Scholar
  27. 27.
    Wang D, Lippard SJ (2004) J Biol Chem 279:20622–20625PubMedCrossRefGoogle Scholar
  28. 28.
    Berners-Price SJ, Ronconi L, Sadler PJ (2006) Prog Nucl Magn Reson Spectrosc 49:65–98Google Scholar
  29. 29.
    Kishimoto S, Kawazoe Y, Ikeno M, Saitoh M, Nakano Y, Nishi Y, Fukushima S, Takeuchi Y (2006) Cancer Chemother Pharmacol 57:84–90PubMedCrossRefGoogle Scholar
  30. 30.
    Kalayda GV, Zhang G, Abraham T, Tanke HJ, Reedijk J (2005) J Med Chem 48:5191–5202PubMedCrossRefGoogle Scholar
  31. 31.
    Miller SE, House DA (1989) Inorg Chim Acta 161:131–137CrossRefGoogle Scholar
  32. 32.
    Berners-Price SJ, Apleton TG (2000) In: Kelland LR, Farrell NP (ed) Platinum-based drugs in cancer therapy. Humana Press, Totowa, pp 3–35Google Scholar
  33. 33.
    Reedijk J, Teuben JM (1999). In: Lippert B (ed) Cisplatin: chemistry and biochemistry of a leading anticancer drug. Wiley, Weinheim, pp 339–362Google Scholar
  34. 34.
    Bose RN, Ghosh SK, Moghaddas S (1997) J Inorg Biochem 65:199–205PubMedCrossRefGoogle Scholar
  35. 35.
    Kelland L (2007) Nat Rev Cancer 7:573–584PubMedCrossRefGoogle Scholar
  36. 36.
    Dabrowiak JC, Goodisman J, Souid AK (2002) Drug Metab Dispos 30:1378–1384PubMedCrossRefGoogle Scholar
  37. 37.
    Berners-Price S, Kuchel PW (1990) J Inorg Biochem 38:327–345CrossRefGoogle Scholar
  38. 38.
    Berners-Price S, Kuchel P (1990) J Inorg Chem 38:305–326Google Scholar
  39. 39.
    Ishikawa T, Ali-Osman F (1993) J Biol Chem 268:20116–20125PubMedGoogle Scholar
  40. 40.
    Arner ES, Nakamura H, Sasada T, Yodoi J, Holmgren A, Spyrou G (2001) Free Radic Biol Med 31:1170–1178PubMedCrossRefGoogle Scholar
  41. 41.
    Jennerwein M, Andrews PA (1995) Drug Metab Dispos 23:178–184PubMedGoogle Scholar
  42. 42.
    Yarbrough JW, Merryman JI, Barnhill MA, Hahn KA (1999) In Vivo 13:375–383PubMedGoogle Scholar
  43. 43.
    Kawabe T, Chen ZS, Wada M, Uchiumi T, Ono M, Akiyama S, Kuwano M (1999) FEBS Lett 456:327–331PubMedCrossRefGoogle Scholar
  44. 44.
    Nakayama K, Miyazaki K, Kanzaki A, Fukumoto M, Takebayashi Y (2001) Oncol Rep 8:1285–1287PubMedGoogle Scholar
  45. 45.
    Komatsu M, Sumizawa T, Mutoh M, Chen ZS, Terada K, Furukawa T, Yang XL, Gao H, Miura N, Sugiyama T, Akiyama S (2000) Cancer Res 60:1312–1316PubMedGoogle Scholar
  46. 46.
    Song IS, Savaraj N, Siddik ZH, Liu P, Wei Y, Wu CJ, Kuo MT (2004) Mol Cancer Ther 3:1543–1549PubMedGoogle Scholar
  47. 47.
    Beretta GL, Gatti L, Tinelli S, Corna E, Colangelo D, Zunino F, Perego P (2004) Biochem Pharmacol 68:283–291PubMedCrossRefGoogle Scholar
  48. 48.
    Holzer AK, Samimi G, Katano K, Naerdemann W, Lin X, Safaei R, Howell SB (2004) Mol Pharmacol 66:817–823PubMedCrossRefGoogle Scholar
  49. 49.
    Holzer AK, Katano K, Klomp LW, Howell SB (2004) Clin Cancer Res 10:6744–6749PubMedCrossRefGoogle Scholar
  50. 50.
    Zisowsky J, Koegel S, Leyers S, Devarakonda K, Kassack MU, Osmak M, Jaehde U (2007) Biochem Pharmacol 73:298–307PubMedCrossRefGoogle Scholar
  51. 51.
    Guo Y, Smith K, Petris MJ (2004) J Biol Chem 279:46393–46399PubMedCrossRefGoogle Scholar
  52. 52.
    Owatari S, Akune S, Komatsu M, Ikeda R, Firth SD, Che XF, Yamamoto M, Tsujikawa K, Kitazono M, Ishizawa T, Takeuchi T, Aikou T, Mercer JF, Akiyama S, Furukawa T (2007) Cancer Res 67:4860–4868PubMedCrossRefGoogle Scholar
  53. 53.
    Kabolizadeh P, Ryan J, Farrell N (2007) Biochem Pharmacol 73:1270–1279PubMedCrossRefGoogle Scholar
  54. 54.
    Safaei R, Katano K, Samimi G, Naerdemann W, Stevenson JL, Rochdi M, Howell SB (2004) Cancer Chemother Pharmacol 53:239–246PubMedCrossRefGoogle Scholar
  55. 55.
    Safaei R, Holzer A, Katano K, Samimi G, Howell S (2004) J Inorg Biochem 98:1607–1613PubMedCrossRefGoogle Scholar
  56. 56.
    Beretta GL, Righetti SC, Lombardi L, Zunino F, Perego P (2002) Ultrastruct Pathol 26:331–334PubMedCrossRefGoogle Scholar
  57. 57.
    Russell JM (2000) Physiol Rev 80:211–276PubMedGoogle Scholar

Copyright information

© SBIC 2008

Authors and Affiliations

  • Milena Salerno
    • 1
  • Dalila Yahia
    • 1
  • Simplice Dzamitika
    • 1
  • Elisabeth de Vries
    • 2
  • Elene Pereira-Maia
    • 3
  • Arlette Garnier-Suillerot
    • 1
  1. 1.Laboratoire de Biophysique Moléculaire Cellulaire et Tissulaire (BioMoCeTi)UMR-CNRS 7033, UMPC Université Paris 6 and Université Paris 13, UFR SMBH, Université Paris 13BobignyFrance
  2. 2.Department of Medical OncologyUniversity Medical Center GroningenGroningenThe Netherlands
  3. 3.Departamento de Quimica, ICExUniversidade Federal de Minas GeraisBelo HorizonteBrazil

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