Fish Physiology and Biochemistry

, Volume 36, Issue 3, pp 677–686 | Cite as

Effects of fish CYP inducers on difloxacin N-demethylation in kidney cell of Chinese idle (Ctenopharyngodon idellus)

  • Ling Zhi Yu
  • Xian Le Yang
  • Xiang Ling Wang
  • Wen Juan Yu
  • Kun Hu
Article

Abstract

A drug–drug interaction occurs when the effect of one drug is altered by the presence of another drug which is generally associated with the induction of cytochrome P450s (CYPs) activity. Thus, unexpected treatment failures often happen resulting from inappropriate coadministration in fisheries. However, little information is available about CYP induction in fish. The reaction of difloxacin (DIF) biotransformation to sarafloxacin (SAR) belongs to N-demethylation catalyzed mainly by CYP(s). In order to supply useful information on CYP induction, the present study assessed the effects of fish-specific CYP inducers on DIF N-demethylation and enzyme kinetics in kidney cell of Chinese idle (CIK; grass carp (Ctenopharyngodon idellus)) by RP-HPLC. Results demonstrated that the amounts of SAR formation and enzymatic parameters Clint and Vmax were significantly increased due to β-naphthoflavone (BNF) pretreatment. Therefore, we suggest that CYP1A may be involved in DIF N-demethylation in CIK. This study provides instructive information to ensure treatment success via avoiding CYP induction in fisheries.

Keywords

Chinese idle CYP Difloxacin Grass carp Kinetics RP-HPLC Sarafloxacin 

Abbreviations

BNF

β-Naphthoflavone

CIK

Kidney cell of Chinese idle

CYPs

Cytochrome P450s

DIF

Difloxacin

EA

Ethyl alcohol

GCL

Grass carp liver cell line

RIF

Rifampicin

RP-HPLC

Reversed-phase high-performance liquid chromatography

SAR

Sarafloxacin

Notes

Acknowledgment

This work was financially supported by the National Natural Science Foundation of China (No. 30371109).

References

  1. Ackermann GE, Fent K (1998) The adaptation of the permanent fish cell lines PLHC-1 and RTG-2 to FCS-free media results in similar growth rates compared to FCS-containing conditions. Mar Environ Res 46:363–367CrossRefGoogle Scholar
  2. Ackermann GE, Schwaiger J, Negele RD, Fent K (2002) Effects of long-term nonylphenol exposure on gonadal development and biomarkers of estrogen exposure in juvenile rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 60:203–221CrossRefGoogle Scholar
  3. Araújo CSA, Marques SAF, Carrondo MJT, Goncalves LMD (2000) In vitro response of the brown bullhead catfish (BB) and rainbow trout (RTG-2) cell lines to benzo[a]pyrene. Sci Total Environ 247:127–135CrossRefGoogle Scholar
  4. Babín M, Casado S, Chana A, Herradón B et al (2005) Cytochrome P4501A induction caused by the imidazole derivative Prochloraz in a rainbow trout cell line. Toxicol In Vitro 19:899–902CrossRefGoogle Scholar
  5. Bainy ACD, Woodin BR, Stegeman JJ (1999) Elevated levels of multiple cytochrome P450 forms in tilapia from Billings Reservoir—Sao Paulo, Brazil. Aquat Toxicol 44:289–305CrossRefGoogle Scholar
  6. Bernhardt R (2004) Optimized chimeragenesis; creating diverse P450 functions. Chem Biol 11:287–288CrossRefGoogle Scholar
  7. Bhakta KY, Jiang W, Couroucli XI et al (2008) Regulation of cytochrome P4501A1 expression by hyperoxia in human lung cell lines: Implications for hyperoxic lung injury. Toxicol Appl Pharmacol 233:169–178CrossRefGoogle Scholar
  8. Billiard SM, Bols NC, Hodson PV (2004) In vitro and in vivo comparisons of fish-specific CYP1A induction relative potency factors for selected polycyclic aromatic hydrocarbons. Ecotoxicol Environ Saf 59:292–299CrossRefGoogle Scholar
  9. Brandon EFA, Raap CD, Meijerman I, Beijnen JH, Schellens JHM (2003) An update on in vitro test methods in human hepatic drug biotransformation research: pros and cons. Toxicol Appl Pharmacol 189:233–246CrossRefGoogle Scholar
  10. Brouwers JR (1992) Drug interactions with quinolone antibacterials. Drug Saf 7:268–281CrossRefGoogle Scholar
  11. Caminada D, Escher C, Fent K et al (2006) Cytotoxicity of pharmaceuticals found in aquatic systems: comparison of PLHC-1 and RTG-2 fish cell lines. Aquat Toxicol 79:114–123CrossRefGoogle Scholar
  12. Celander M, Förlin L (1991) Catalytic activity and immunochemical quantification of hepatic cytochrome P-450 in β-naphthoflavone and isosafrol treated rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 9:189–197CrossRefGoogle Scholar
  13. Celander M, Hahn ME, Stegeman JJ (1996) Cytochromes P450 (CYP) in the Poeciliopsis lucida hepatocellular carcinoma cell line (PLHC-1): dose and time-dependent glucocorticoid potentiation of CYP1A induction without induction of CYP3A. Arch Biochem Biophys 329:113–122CrossRefGoogle Scholar
  14. Chung-Davidson YW, Rees CB, Wu H, Yun SS, Li W (2004) beta-naphthoflavone induction of CYP1A in brain of juvenile lake trout (Salvelinus namaycush Walbaum). J Exp Biol 207:1533–1542CrossRefGoogle Scholar
  15. Davies BI, Maesen FP (1989) Drug interactions with quinolones. Rev Infect Dis 11:S1083–S1090CrossRefGoogle Scholar
  16. Ding FK, Cao JY, Ma LB et al (2006) Pharmacokinetics and tissue residues of difloxacin in crucian carp (Carassius auratus) after oral administration. Aquaculture 256:121–128CrossRefGoogle Scholar
  17. Fent K (2001) Fish cell lines as versatile tools in ecotoxicology: asssessment of cytotoxicity, cytochrome P450 1A induction potential and estrogenic activity of chemicals and environmental samples. Toxicol In Vitro 15:477–488CrossRefGoogle Scholar
  18. Fent K, Woodin BR, Stegeman JJ (1998) Effects of triphenyltin and other organotins on hepatic monooxygenase system in fish. Comp Biochem Physiol C 121:277–288PubMedGoogle Scholar
  19. Förlin L, Celander M (1995) Studies of the inducibility of P450 1A in perch from the PCB-contaminated lake Järnsjön in Sweden. Mar Environ Res 39:85–88CrossRefGoogle Scholar
  20. Gingerich WH, Meinertz JR, Dawson VK et al (1995) Distribution and elimination of 14C sarafloxacin hydrochloride from tissues of juvenile channel catfish (Ictalurus punctatus). Aquaculture 131:23–36CrossRefGoogle Scholar
  21. Gooneratne R, Miranda CL, Henderson MC, Buhler DR (1997) Beta-naphthoflavone induced CYP1A1 and 1A3 proteins in the liver of rainbow trout (Oncorhynchus mykiss). Xenobiotica 27:175–187CrossRefGoogle Scholar
  22. Gravato C, Santos MA (2002) β-Naphthoflavone liver EROD and erythrocytic nuclear abnormality induction in juvenile (Dicentrarchus labrax L.). Ecotoxicol Environ Saf 52:69–74CrossRefGoogle Scholar
  23. Guengerich FP (2004) Cytochrome P450: what have we learned and what are the future issues? Drug Metab Rev 36:159–197CrossRefGoogle Scholar
  24. Harder S, Fuhr U, Staib AH, Wolff T (1989) Ciprofloxacin-caffeine: a drug interaction established using in vivo and in vitro investigations. Am J Med 87:89S–91SCrossRefGoogle Scholar
  25. Henczová M, Deér AK, Komlósi V, Mink J (2006) Detection of toxic effects of Cd2+ on different fish species via liver cytochrome P450-dependent monooxygenase activities and FTIR spectroscopy. Anal Bioanal Chem 385:652–659CrossRefGoogle Scholar
  26. Ho SH, Cheng CF, Wang WS (1999) Pharmacokinetics and depletion studies of sarafloxacin after oral administration to eel (Anguilla anguilla). J Vet Sci 61:459–463CrossRefGoogle Scholar
  27. Janošek J, Hilscherová K, Bláha L, Holoubek I (2006) Environmental xenobiotics and nuclear receptors-interactions, effects and in vitro assessment. Toxicol In Vitro 20:18–37CrossRefGoogle Scholar
  28. Khan MN, Reddy PK, Renaud RL, Leatherland JF (1997) Effect of cortisol on the metabolism of 17-hydroxyprogesterone by Arctic charr and rainbow trout embryos. Fish Physiol Biochem 16:197–209CrossRefGoogle Scholar
  29. Kim JH, Raisuddin S, Ki JS, Han KN (2008) Molecular cloning and beta-naphthoflavone-induced expression of a cytochrome P450 1A (CYP1A) gene from an anadromous river pufferfish. Takifugu obscurus. Mar Pollut Bull 57:433–440CrossRefGoogle Scholar
  30. Li D, Yang XL, Zhang SJ et al (2008) Effects of mammalian CYP3A inducers on CYP3A-related enzyme activities in grass carp (Ctenopharyngodon idellus): Possible implications for the establishment of a fish CYP3A induction model. Comp Biochem Physiol C 147:17–29Google Scholar
  31. Lin M, Yang XL, Fang WH et al (2006) Dose–response of inducers to effect on EROD in grass carp hepatocyte. J Fish China 30:311–315Google Scholar
  32. Lin M, Yang XL, Wang XL et al (2007) Enzymatic on deethlation metabolism of enrofloxacin in grass carp hepatocyte. High Technol Lett (Chinese version) 17:314–318Google Scholar
  33. Lorenzana RM, Hedstrom OR, Buhler DR (1988) Localization of cytochrome P-450 in the head and trunk kidney of rainbow trout (Salmo gairdneri). Toxicol Appl Pharmacol 96:159–167CrossRefGoogle Scholar
  34. Malmström CM, Koponen K, Lindström-Seppä P et al (2004) Induction and localization of hepatic CYP4501A in flounder and rainbow trout exposed to benzo[a]pyrene. Ecotoxicol Environ Saf 58:365–372CrossRefGoogle Scholar
  35. Martinsen B, Horsberg TE (1995) Comparative single-dose pharmacokinetics of four quinolones, oxolinic acid, flumequine, sarafloxacin and enrofloxacin in Atlantic salmon (Salmo salar) held in seawater at 10°C. Antimicrob Agents Chemother 39:1059–1064CrossRefGoogle Scholar
  36. Monod G, Saucier D, Perdu-Durand E et al (1994) Biotransformation enzyme activities in the olfactory organ of rainbow trout (Oncorhynchus mykiss). Immunocytochemical localization of cytochrome P4501A1 and its induction by β-naphthoflavone. Fish Physiol Biochem 13:433–444CrossRefGoogle Scholar
  37. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63CrossRefGoogle Scholar
  38. Moutou KA, Burke MD, Houlihan DF (1998) Hepatic P450 monooxygenase response in rainbow trout (Oncorhynchus mykiss (Walbaum)) administered aquaculture antibiotics. Fish Physiol Biochem 18:97–106CrossRefGoogle Scholar
  39. Muto N, Hirai H, Tanaka T, Itoh N, Tanaka K (1997) Induction and inhibition of cytochrome P450 isoforms by imazalil, a food contaminant, in mouse small intestine and liver. Xenobiotica 27:1215–1223CrossRefGoogle Scholar
  40. Park ED, Lightner DV, Stamm JM, Bell TA (1994) Preliminary studies on the palatability, animal safety, and tissue residues of sarafloxacin–HCl in the penaeid shrimp, Penaeus vannamei. Aquaculture 126:231–241CrossRefGoogle Scholar
  41. Pesonen M, Celander M, Förlin L, Andersson T (1987) Comparison of xenobiotic biotransformation enzymes in kidney and liver of rainbow trout (Salmo gairdneri). Toxicol Appl Pharmacol 91:75–84CrossRefGoogle Scholar
  42. Plant NJ, Ogg MS, Crowder M, Gibson GG (2000) Control and statistical analysis of in vitro reporter gene assays. Anal Biochem 278:170–174CrossRefGoogle Scholar
  43. Ronisz D, Förlin L (1998) Interaction of isosafrole, beta-naphthoflavone and other CYP1A inducers in liver of rainbow trout (Oncorhynchus mykiss) and eelpout (Zoarces viviparus). Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 121:289–296CrossRefGoogle Scholar
  44. Seubert JM, Kennedy CJ (1997) The toxicokinetics of benzo[a]pyrene in juvenile coho salmon, Oncorhynchus kisutch, during smoltification. Fish Physiol Biochem 16:437–447CrossRefGoogle Scholar
  45. Snyder MJ (2000) Cytochrome P450 enzymes in aquatic invertebrates: recent advances and future directions. Aquat Toxicol 48:529–547CrossRefGoogle Scholar
  46. Sono M, Roach MP, Coulter ED, Dawson JH (1996) Heme-containing oxygenases. Chem Rev 96:2841–2888CrossRefGoogle Scholar
  47. Tan FX, Wang M, Wang WM, Lu YA (2008) Comparative evaluation of the cytotoxicity sensitivity of six fish cell lines to four heavy metals in vitro. Toxicol In Vitro 22:164–170CrossRefGoogle Scholar
  48. Tyrpenou AE, Iossfidou EG, Psomas IE et al (2003) Tissue distribution and depletion of sarafloxacin hydrochloride after in feed administration in gilthead seabream (Sparus aurata L.). Aquaculture 215:291–300CrossRefGoogle Scholar
  49. Wan XQ, Wu WZ, He JZ (2002) Evaluating toxic effects of PCDD/F using grass carp primary hepatocyte culture. China Environ Sci 22:114–117Google Scholar
  50. Wan XQ, Ma TW, Wu WZ, Wang ZJ (2004) EROD activities in a primary cell culture of grass carp (Ctenopharyngodon idellus) hepatocytes exposed to polychlorinated aromatic hydrocarbonas. Ecotoxicol Environ Saf 58:84–89CrossRefGoogle Scholar
  51. Wang XL, Yang XL, Lin M, Yu WJ et al (2007) Elimination of enrofloxacin and detection of metabol ic enzyme activity in Micropterus salmoides hepatocytes. J Fish Sci China 14:1004–1005Google Scholar
  52. Wang XL, Yang XL, Zhang N et al (2008) Induction of CYP2E1 activity in Ctenopharyngodon idellus hepatocyte. Acta Hydrobiol Sin 32:469–474CrossRefGoogle Scholar
  53. Werck-Reichhart D, Feyereisen R (2000) Cytochromes P450: a success story. Genome Biol 1: reviews 3003.1-3003.9CrossRefGoogle Scholar
  54. Winzer K, Noorden CJFV, Köhler A (2002) Sex-specific biotransformation and detoxification after xenobiotic exposure of primary cultured hepatocytes of European flounder (Platichthys flesus L.). Aquat Toxicol 59:17–33CrossRefGoogle Scholar
  55. Xu X, Liu HY, Liu L, Xie L, Liu XD (2008) The influence of a newly developed quinolone: antofloxacin, on CYP activity in rats. Eur J Drug Metab Pharmacokinet 33:1–7CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Ling Zhi Yu
    • 1
  • Xian Le Yang
    • 1
  • Xiang Ling Wang
    • 2
  • Wen Juan Yu
    • 1
  • Kun Hu
    • 1
  1. 1.Aquatic Pathogen Collection Centre of Ministry of AgricultureShanghai Ocean UniversityShanghaiChina
  2. 2.Shanghai Medicilon & MPI Inc.ShanghaiChina

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