Oxaliplatin transport mediated by organic cation/carnitine transporters OCTN1 and OCTN2 in overexpressing human embryonic kidney 293 cells and rat dorsal root ganglion neurons

Journal of Pharmacology and Experimental Therapeutics

Volumn 338, Issue 2, 2011, Pages 537-547

  Jong, Nancy N ^a,b   Nakanishi, Takeo ^b   Liu, Johnson J ^a   Tamai, Ikumi ^b   McKeage, Mark J ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b KANAZAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; CARBON 14; CARNITINE; MESSENGER RNA; ORGANIC CATION TRANSPORTER; ORGANIC CATION TRANSPORTER 1; ORGANIC CATION TRANSPORTER 2; ORGANIC CATION TRANSPORTER 3; OXALIPLATIN; PLATINUM; PROTEIN OCTN1; PROTEIN OCTN2; SODIUM; THIONEINE; TRITIUM; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STRAIN HEK293; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG TRANSPORT; EMBRYO; FEMALE; HUMAN; HUMAN CELL; NERVE CELL; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL GANGLION; TEMPERATURE;

ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CELLS, CULTURED; FEMALE; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; NEURONS; ORGANIC CATION TRANSPORT PROTEINS; ORGANOPLATINUM COMPOUNDS; RATS; RATS, WISTAR;

EID: 79960525836     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.111.181297     Document Type: Article

References (48)

1. André T, Boni C, Mounedji-Boudiaf L, Navarro M, Tabernero J, Hickish T, Topham C, Zaninelli M, Clingan P, Bridgewater J, et al. (2004) Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer. N Engl J Med 350:2343-2351. (Pubitemid 38702845)
2. Bible KC, Boerner SA, and Kaufmann SH (1999) A one-step method for protein estimation in biological samples: nitration of tyrosine in nitric acid. Anal Biochem 267:217-221. (Pubitemid 29061825)
3. Burger H, Zoumaro-Djayoon A, Boersma AW, Helleman J, Berns EM, Mathijssen RH, Loos WJ, and Wiemer EA (2010) Differential transport of platinum compounds by the human organic cation transporter hOCT2 (hSLC22A2). Br J Pharmacol 159:898-908.
4. Cassidy J, Tabernero J, Twelves C, Brunet R, Butts C, Conroy T, Debraud F, Figer A, Grossmann J, Sawada N, et al. (2004) XELOX (capecitabine plus oxaliplatin): active first-line therapy for patients with metastatic colorectal cancer. J Clin Oncol 22:2084-2091. (Pubitemid 41095141)
5. Cavaletti G, Tredici G, Petruccioli MG, Dondè E, Tredici P, Marmiroli P, Minoia C, Ronchi A, Bayssas M, and Etienne GG (2001) Effects of different schedules of oxaliplatin treatment on the peripheral nervous system of the rat. Eur J Cancer 37:2457-2463. (Pubitemid 33097486)
6. Ciarimboli G, Deuster D, Knief A, Sperling M, Holtkamp M, Edemir B, Pavenstädt H, Lanvers-Kaminsky C, am Zehnhoff-Dinnesen A, Schinkel AH, et al. (2010) Organic cation transporter 2 mediates cisplatin-induced oto- and nephrotoxicity and is a target for protective interventions. Am J Pathol 176:1169-1180.
7. Ciarimboli G, Ludwig T, Lang D, Pavenstädt H, Koepsell H, Piechota HJ, Haier J, Jaehde U, Zisowsky J, and Schlatter E (2005) Cisplatin nephrotoxicity is critically mediated via the human organic cation transporter 2. Am J Pathol 167:1477-1484. (Pubitemid 41713303)
8. de Gramont A, Figer A, Seymour M, Homerin M, Hmissi A, Cassidy J, Boni C, Cortes-Funes H, Cervantes A, Freyer G, et al. (2000) Leucovorin and fluorouracil with or without oxaliplatin as first-line treatment in advanced colorectal cancer. J Clin Oncol 18:2938-2947. (Pubitemid 30644117)
9. Delree P, Leprince P, Schoenen J, and Moonen G (1989) Purification and culture of adult rat dorsal root ganglia neurons. J Neurosci Res 23:198-206. (Pubitemid 19178881)
10. Ehlert EM, Eggers R, Niclou SP, and Verhaagen J (2010) Cellular toxicity following application of adeno-associated viral vector-mediated RNA interference in the nervous system. BMC Neuroscience 11:20.
11. Fan X, Ross DD, Arakawa H, Ganapathy V, Tamai I, and Nakanishi T (2010) Impact of system L amino acid transporter 1 (LAT1) on proliferation of human ovarian cancer cells: a possible target for combination therapy with anti-proliferative aminopeptidase inhibitors. Biochem Pharmacol 80:811-818.
12. Filipski KK, Loos WJ, Verweij J, and Sparreboom A (2008) Interaction of cisplatin with the human organic cation transporter 2. Clin Cancer Res 14:3875-3880.
13. Filipski KK, Mathijssen RH, Mikkelsen TS, Schinkel AH, and Sparreboom A (2009) Contribution of organic cation transporter 2 (OCT2) to cisplatin-induced nephrotoxicity. Clin Pharmacol Ther 86:396-402.
14. Fujita M, Nakanishi T, Shibue Y, Kobayashi D, Moseley RH, Shirasaka Y, and Tamai I (2009) Hepatic uptake of γ-butyrobetaine, a precursor of carnitine biosynthesis, in rats. Am J Physiol Gastrointest Liver Physiol 297:G681-G686.
15. Gamelin L, Boisdron-Celle M, Delva R, Guérin-Meyer V, Ifrah N, Morel A, and Gamelin E (2004) Prevention of oxaliplatin-related neurotoxicity by calcium and magnesium infusions: a retrospective study of 161 patients receiving oxaliplatin combined with 5-Fluorouracil and leucovorin for advanced colorectal cancer. Clin Cancer Res 10:4055-4061. (Pubitemid 38812481)
16. Ghirardi O, Lo Giudice P, Pisano C, Vertechy M, Bellucci A, Vesci L, Cundari S, Miloso M, Rigamonti LM, Nicolini G, et al. (2005) Acetyl-L-carnitine prevents and reverts experimental chronic neurotoxicity induced by oxaliplatin, without altering its antitumor properties. Anticancer Res 25:2681-2687.
17. Green E, Sargent D, Goldberg R and Grothey A (2005) Detailed analysis of oxaliplatin-associated neurotoxicity in Intergroup trial N9741, in 2005 Gastrointestinal Cancers Symposium; 2005 Jan 25-29; Hollywood, FL. A182, American Society of Clinical Oncology, Alexandria, VA.
18. Grothey A (2003) Oxaliplatin-safety profile: neurotoxicity. Semin Oncol 30 (4 Suppl 15):5-13.
19. Hall MD, Okabe M, Shen DW, Liang XJ, and Gottesman MM (2008) The role of cellular accumulation in determining sensitivity to platinum-based chemotherapy. Annu Rev Pharmacol Toxicol 48:495-535. (Pubitemid 351738162)
20. Holmes J, Stanko J, Varchenko M, Ding H, Madden VJ, Bagnell CR, Wyrick SD, and Chaney SG (1998) Comparative neurotoxicity of oxaliplatin, cisplatin, and ormaplatin in a Wistar rat model. Toxicol Sci 46:342-351. (Pubitemid 29069619)
21. Ip V, Liu JJ, Mercer JF, and McKeage MJ (2010) Differential expression of ATP7A, ATP7B and CTR1 in adult rat dorsal root ganglion tissue. Mol Pain 6:53.
22. 2 in the blood plasma of colorectal cancer patients. J Anal At Spectrom 23:881-884.
23. Ishida S, Lee J, Thiele DJ, and Herskowitz I (2002) Uptake of the anticancer drug cisplatin mediated by the copper transporter Ctr1 in yeast and mammals. Proc Natl Acad Sci USA 99:14298-14302. (Pubitemid 35257666)
24. Kato Y, Kubo Y, Iwata D, Kato S, Sudo T, Sugiura T, Kagaya T, Wakayama T, Hirayama A, Sugimoto M, et al. (2010) Gene knockout and metabolome analysis of carnitine/organic cation transporter OCTN1. Pharm Res 27:832-840.
25. Kawasaki Y, Kato Y, Sai Y, and Tsuji A (2004) Functional characterization of human organic cation transporter OCTN1 single nucleotide polymorphisms in the Japanese population. J Pharm Sci 93:2920-2926. (Pubitemid 39657796)
26. Koepsell H, Lips K, and Volk C (2007) Polyspecific organic cation transporters: structure, function, physiological roles, and biopharmaceutical implications. Pharm Res 24:1227-1251. (Pubitemid 46876495)
27. Komatsu M, Sumizawa T, Mutoh M, Chen ZS, Terada K, Furukawa T, Yang XL, Gao H, Miura N, Sugiyama T, et al. (2000) Copper-transporting P-type adenosine triphosphatase (ATP7B) is associated with cisplatin resistance. Cancer Res 60: 1312-1316. (Pubitemid 30152000)
28. Liu JJ, Jamieson SM, Subramaniam J, Ip V, Jong NN, Mercer JF, and McKeage MJ (2009) Neuronal expression of copper transporter 1 in rat dorsal root ganglia: association with platinum neurotoxicity. Cancer Chemother Pharmacol 64:847-856.
29. Liu W and Saint DA (2002) Validation of a quantitative method for real time PCR kinetics. Biochem Biophys Res Commun 294:347-353. (Pubitemid 34694101)
30. -ΔΔCT method. Methods 25:402-408.
31. Luo FR, Wyrick SD, and Chaney SG (1999) Comparative neurotoxicity of oxaliplatin, ormaplatin, and their biotransformation products utilizing a rat dorsal root ganglia in vitro explant culture model. Cancer Chemother Pharmacol 44:29-38. (Pubitemid 29246322)
32. Nakamura T, Yoshida K, Yabuuchi H, Maeda T, and Tamai I (2008) Functional characterization of ergothioneine transport by rat organic cation/carnitine transporter Octn1 (slc22a4). Biol Pharm Bull 31:1580-1584.
33. Pisano C, Pratesi G, Laccabue D, Zunino F, Lo Giudice P, Bellucci A, Pacifici L, Camerini B, Vesci L, Castorina M, et al. (2003) Paclitaxel and cisplatin-induced neurotoxicity: a protective role of acetyl-L-carnitine. Clin Cancer Res 9:5756-5767. (Pubitemid 37499500)
34. Read ML, Mir S, Spice R, Seabright RJ, Suggate EL, Ahmed Z, Berry M, and Logan A (2009) Profiling RNA interference (RNAi)-mediated toxicity in neural cultures for effective short interfering RNA design. J Gene Med 11:523-534.
35. Samimi G, Safaei R, Katano K, Holzer AK, Rochdi M, Tomioka M, Goodman M, and Howell SB (2004) Increased expression of the copper efflux transporter ATP7A mediates resistance to cisplatin, carboplatin, and oxaliplatin in ovarian cancer cells. Clin Cancer Res 10:4661-4669. (Pubitemid 38955516)
36. Screnci D, Er HM, Hambley TW, Galettis P, Brouwer W, and McKeage MJ (1997) Stereoselective peripheral sensory neurotoxicity of diaminocyclohexane platinum enantiomers related to ormaplatin and oxaliplatin. Br J Cancer 76:502-510. (Pubitemid 27331216)
37. Screnci D, McKeage MJ, Galettis P, Hambley TW, Palmer BD, and Baguley BC (2000) Relationships between hydrophobicity, reactivity, accumulation and peripheral nerve toxicity of a series of platinum drugs. Br J Cancer 82:966-972. (Pubitemid 30085253)
38. Sekine T, Kusuhara H, Utsunomiya-Tate N, Tsuda M, Sugiyama Y, Kanai Y, and Endou H (1998) Molecular cloning and characterization of high-affinity carnitine transporter from rat intestine. Biochem Biophys Res Commun 251:586-591. (Pubitemid 28505066)
39. Song TY, Chen CL, Liao JW, Ou HC, and Tsai MS (2010) Ergothioneine protects against neuronal injury induced by cisplatin both in vitro and in vivo. Food Chem Toxicol 48:3492-3499.
40. Sugiura T, Kato Y, Kubo Y, and Tsuji A (2006) Mutation in an adaptor protein PDZK1 affects transport activity of organic cation transporter OCTNs and oligopeptide transporter PEPT2. Drug Metab Pharmacokinet 21:375-383.
41. Ta LE, Espeset L, Podratz J, and Windebank AJ (2006) Neurotoxicity of oxaliplatin and cisplatin for dorsal root ganglion neurons correlates with platinum-DNA binding. Neurotoxicology 27:992-1002. (Pubitemid 44838955)
42. +-coupled transport of L-carnitine via high-affinity carnitine transporter OCTN2 and its subcellular localization in kidney. Biochim Biophys Acta 1512: 273-284.
43. Tamai I, Ohashi R, Nezu J, Yabuuchi H, Oku A, Shimane M, Sai Y, and Tsuji A (1998) Molecular and functional identification of sodium ion-dependent, high affinity human carnitine transporter OCTN2. J Biol Chem 273:20378-20382. (Pubitemid 28377603)
44. Tamai I, Yabuuchi H, Nezu J, Sai Y, Oku A, Shimane M, and Tsuji A (1997) Cloning and characterization of a novel human pH-dependent organic cation transporter, OCTN1. FEBS Lett 419:107-111. (Pubitemid 28011227)
45. Yokoo S, Masuda S, Yonezawa A, Terada T, Katsura T, and Inui K (2008) Significance of organic cation transporter 3 (SLC22A3) expression for the cytotoxic effect of oxaliplatin in colorectal cancer. Drug Metab Dispos 36:2299-2306.
46. Yonezawa A, Masuda S, Nishihara K, Yano I, Katsura T, and Inui K (2005) Association between tubular toxicity of cisplatin and expression of organic cation transporter rOCT2 (Slc22a2) in the rat. Biochem Pharmacol 70:1823-1831. (Pubitemid 41612013)
47. Yonezawa A, Masuda S, Yokoo S, Katsura T, and Inui K (2006) Cisplatin and oxaliplatin, but not carboplatin and nedaplatin, are substrates for human organic cation transporters (SLC22A1-3 and multidrug and toxin extrusion family). J Pharmacol Exp Ther 319:879-886.
48. Zhang S, Lovejoy KS, Shima JE, Lagpacan LL, Shu Y, Lapuk A, Chen Y, Komori T, Gray JW, Chen X, et al. (2006) Organic cation transporters are determinants of oxaliplatin cytotoxicity. Cancer Res 66:8847-8857. (Pubitemid 44449203)