Ivermectin toxicokinetics in rainbow trout (Oncorhynchus mykiss) following P-glycoprotein inhibition.

Cyclosporin A Inhibition Ivermectin P-glycoprotein Rainbow trout Toxicokinetics

Journal

Veterinary research communications
ISSN: 1573-7446
Titre abrégé: Vet Res Commun
Pays: Switzerland
ID NLM: 8100520

Informations de publication

Date de publication:
06 Aug 2024
Historique:
received: 11 12 2023
accepted: 22 07 2024
medline: 6 8 2024
pubmed: 6 8 2024
entrez: 6 8 2024
Statut: aheadofprint

Résumé

Changes to ivermectin (IVM [22,23-dihydro avermectin B1a + 22,23-dihydro avermectin B1b]) toxicokinetics (TK) with and without P-glycoprotein (P-gp) inhibition by cyclosporin A (CsA) were examined in rainbow trout (Oncorhynchus mykiss). Rainbow trout were injected with 175 μg/kg

Identifiants

pubmed: 39106005
doi: 10.1007/s11259-024-10480-3
pii: 10.1007/s11259-024-10480-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Antonić J, Grabnar I, Milčinski L et al (2011) Influence of P-glycoprotein inhibition on secretion of ivermectin and doramectin by milk in lactating sheep. Vet Parasitol 179:159–166. https://doi.org/10.1016/j.vetpar.2011.03.002
doi: 10.1016/j.vetpar.2011.03.002 pubmed: 21466921
Azevedo VC, Kennedy CJ (2022) P-glycoprotein inhibition affects ivermectin-induced behavioural alterations in fed and fasted zebrafish (Danio rerio). Fish Physiol Biochem 48:1267–1283. https://doi.org/10.1007/s10695-022-01111-2
doi: 10.1007/s10695-022-01111-2 pubmed: 36006557
Azevedo VC, Johnston CU, Kennedy CJ (2023) Ivermectin Toxicokinetics in Rainbow Trout (Oncorhynchus mykiss) following P-glycoprotein Induction. Arch Environ Contam Toxicol. https://doi.org/10.1007/s00244-023-01045-7
doi: 10.1007/s00244-023-01045-7
Baraka OZ, Mahmoud BM, Marschke CK et al (1996) Ivermectin distribution in the plasma and tissues of patients infected with Onchocerca volvulus. Eur J Clin Pharmacol 50:407–410. https://doi.org/10.1007/s002280050131
doi: 10.1007/s002280050131 pubmed: 8839664
Bard SM, Gadbois S (2007) Assessing neuroprotective P-glycoprotein activity at the blood-brain barrier in killifish (Fundulus heteroclitus) using behavioural profiles. Mar Environ Res 64:679–682. https://doi.org/10.1016/j.marenvres.2007.05.001
doi: 10.1016/j.marenvres.2007.05.001 pubmed: 17889328
Bardelmeijer HA, Ouwehand M, Beijnen JH et al (2004) Efficacy of novel P-glycoprotein inhibitors to increase the oral uptake of paclitaxel in mice. Invest New Drugs 22:219–229. https://doi.org/10.1023/B:DRUG.0000026248.45084.21
doi: 10.1023/B:DRUG.0000026248.45084.21 pubmed: 15122069
Barron MG, Tarr BD, Hayton WL (1987) Temperature-dependence of cardiac output and regional blood flow in rainbow trout, Salmo gairdneri Richardson. J Fish Biol 31:735–744. https://doi.org/10.1111/j.1095-8649.1987.tb05276.x
doi: 10.1111/j.1095-8649.1987.tb05276.x
Bauer B, Hartz AMS, Fricker G, Miller DS (2005) Modulation of p-Glycoprotein Transport Function at the Blood-Brain Barrier. Exp Biol Med 230:118–127. https://doi.org/10.1177/153537020523000206
doi: 10.1177/153537020523000206
Baumgarner BL, Bharadwaj AS, Inerowicz D et al (2013) Proteomic analysis of rainbow trout (Oncorhynchus mykiss) intestinal epithelia: Physiological acclimation to short-term starvation. Comp Biochem Physiol Part D Genomics Proteomics 8:58–64. https://doi.org/10.1016/j.cbd.2012.11.001
doi: 10.1016/j.cbd.2012.11.001 pubmed: 23261852
Bayen S, Giusti P, Lee HK et al (2005) Bioaccumulation of Ddt Pesticide in Cultured Asian Seabass Following Dietary Exposure. J Toxicol Environ Health A 68:51–65. https://doi.org/10.1080/15287390590524037
doi: 10.1080/15287390590524037 pubmed: 15739804
Bieczynski F, Painefilú JC, Venturino A, Luquet CM (2021) Expression and Function of ABC Proteins in Fish Intestine. Front Physiol 12. https://doi.org/10.3389/fphys.2021.791834
Bleasby K, Chauhan S, Brown CDA (2000) Characterization of MPP+ secretion across human intestinal Caco-2 cell monolayers: role of P-glycoprotein and a novel Na+-dependent organic cation transport mechanism. Br J Pharmacol 129:619–625. https://doi.org/10.1038/sj.bjp.0703078
doi: 10.1038/sj.bjp.0703078 pubmed: 10711363 pmcid: 1571862
Boer R, Haas S, Schödl A (1994) Influence of dexniguldipine-HCl on rhodamine-123 accumulation in a multidrug-resistant leukaemia cell line: Comparison with other chemosensitisers. Eur J Cancer 30:1117–1123. https://doi.org/10.1016/0959-8049(94)90469-3
doi: 10.1016/0959-8049(94)90469-3
Caminada D, Zaja R, Smital T, Fent K (2008) Human pharmaceuticals modulate P-gp1 (ABCB1) transport activity in the fish cell line PLHC-1. Aquat Toxicol 90:214–222. https://doi.org/10.1016/j.aquatox.2008.08.013
doi: 10.1016/j.aquatox.2008.08.013 pubmed: 18950875
Chen L (2020) Visual system: An understudied target of aquatic toxicology. Aquat Toxicol 225:105542. https://doi.org/10.1016/j.aquatox.2020.105542
doi: 10.1016/j.aquatox.2020.105542 pubmed: 32585539
Chiu SHL, Green ML, Baylis FP et al (1990) Absorption, tissue distribution, and excretion of tritium-labeled ivermectin in cattle, sheep, and rat. J Agric Food Chem 38:2072–2078. https://doi.org/10.1021/jf00101a015
doi: 10.1021/jf00101a015
Conklin DJ, Chavas A, Duff DW et al (1997) Cardiovascular effects of arginine vasotocin in the rainbow trout Oncorhynchus mykiss. J Exp Biol 200:2821–2832. https://doi.org/10.1242/jeb.200.22.2821
doi: 10.1242/jeb.200.22.2821 pubmed: 9344967
Craven J, Bjørn H, Hennessy DR, Friis C (2002) The effects of body composition on the pharmacokinetics of subcutaneously injected ivermectin and moxidectin in pigs. J Vet Pharmacol Ther 25:227–232. https://doi.org/10.1046/j.1365-2885.2002.00400.x
doi: 10.1046/j.1365-2885.2002.00400.x pubmed: 12081618
Dumas A, de Lange CFM, France J, Bureau DP (2007) Quantitative description of body composition and rates of nutrient deposition in rainbow trout (Oncorhynchus mykiss). Aquaculture 273:165–181. https://doi.org/10.1016/j.aquaculture.2007.09.026
doi: 10.1016/j.aquaculture.2007.09.026
Edhlund I, Lee C (2019) A Petri Net Approach to Physiologically Based Toxicokinetic Modeling. Environ Toxicol Chem 38:978–987. https://doi.org/10.1002/etc.4390
doi: 10.1002/etc.4390 pubmed: 30756430
Elazab ST, Hsu WH (2021) Effects of verapamil on the pharmacokinetics of ivermectin in rabbits. J Vet Pharmacol Ther 44:397–405. https://doi.org/10.1111/jvp.12919
doi: 10.1111/jvp.12919 pubmed: 33070345
Fernández C, Porcel MA, Alonso A et al (2011) Semifield assessment of the runoff potential and environmental risk of the parasiticide drug ivermectin under Mediterranean conditions. Environ Sci Pollut Res 18:1194–1201. https://doi.org/10.1007/s11356-011-0474-8
doi: 10.1007/s11356-011-0474-8
Fischer S, Klüver N, Burkhardt-Medicke K et al (2013) Abcb4 acts as multixenobiotic transporter and active barrier against chemical uptake in zebrafish (Danio rerio) embryos. BMC Biol 11:1–16. https://doi.org/10.1186/1741-7007-11-69
doi: 10.1186/1741-7007-11-69
Gélineau A, Corraze G, Boujard T et al (2001) Relation between dietary lipid level and voluntary feed intake, growth, nutrient gain, lipid deposition and hepatic lipogenesis in rainbow trout. Reprod Nutr Dev 41:487–503. https://doi.org/10.1051/rnd:2001103
doi: 10.1051/rnd:2001103 pubmed: 12126295
González Canga A, Sahagún Prieto AM, Diez Liébana MJ et al (2008) The Pharmacokinetics and Interactions of Ivermectin in Humans—A Mini-review. AAPS J 10:42–46. https://doi.org/10.1208/s12248-007-9000-9
doi: 10.1208/s12248-007-9000-9 pubmed: 18446504 pmcid: 2751445
González Canga A, Sahagún Prieto AM, José Diez Liébana M et al (2009) The pharmacokinetics and metabolism of ivermectin in domestic animal species. Vet J 179:25–37. https://doi.org/10.1016/j.tvjl.2007.07.011
doi: 10.1016/j.tvjl.2007.07.011 pubmed: 17851096
Gourley ME, Kennedy CJ (2009) Energy allocations to xenobiotic transport and biotransformation reactions in rainbow trout (Oncorhynchus mykiss) during energy intake restriction. Comp Biochem Physiol Part C Toxicol Pharmacol 150:270–278. https://doi.org/10.1016/j.cbpc.2009.05.003
doi: 10.1016/j.cbpc.2009.05.003
Guerreiro DD, de Lima LF, Mbemya GT et al (2018) ATP-binding cassette (ABC) transporters in caprine preantral follicles: gene and protein expression. Cell Tissue Res 372:611–620. https://doi.org/10.1007/s00441-018-2804-3
doi: 10.1007/s00441-018-2804-3 pubmed: 29488001
Hoar WS, Hickman CP (1975) A Laboratory Companion for General and Comparative Physiology, 2nd edn. Prentice-Hall, Englewood Cliffs
Høy T, Horsberg TE, Nafstad I (1990) The Disposition of Ivermectin in Atlantic Salmon (Salmo salar). Pharmacol Toxicol 67:307–312. https://doi.org/10.1111/j.1600-0773.1990.tb00835.x
doi: 10.1111/j.1600-0773.1990.tb00835.x pubmed: 2077522
Jaki T, Wolfsegger MJ (2020) PK: Basic non-compartmental pharmacokinetics. Version 1.3–5
Jouan E, Le Vée M, Mayati A et al (2016) Evaluation of P-Glycoprotein Inhibitory Potential Using a Rhodamine 123 Accumulation Assay. Pharmaceutics 8:12. https://doi.org/10.3390/pharmaceutics8020012
doi: 10.3390/pharmaceutics8020012 pubmed: 27077878 pmcid: 4932475
Kajikawa T, Mishima H, Mishima H et al (1999) Role of P-glycoprotein in distribution of rhodamine 123 into aqueous humor in rabbits. Curr Eye Res 18:240–246. https://doi.org/10.1076/ceyr.18.3.240.5365
doi: 10.1076/ceyr.18.3.240.5365 pubmed: 10342379
Katharios P, Iliopoulou-Georgudaki J, Antimisiaris S et al (2002) Pharmacokinetics of ivermectin in sea bream, Sparus aurata using a direct competitive ELISA. Fish Physiol Biochem 26:189–195. https://doi.org/10.1023/A:1025473904513
doi: 10.1023/A:1025473904513
Kennedy CJ, Tierney KB, Mittelstadt M (2014) Inhibition of P-glycoprotein in the blood–brain barrier alters avermectin neurotoxicity and swimming performance in rainbow trout. Aquat Toxicol 146:176–185. https://doi.org/10.1016/j.aquatox.2013.10.035
doi: 10.1016/j.aquatox.2013.10.035 pubmed: 24316435
Kiki-Mvouaka S, Ménez C, Borin C et al (2010) Role of P-Glycoprotein in the Disposition of Macrocyclic Lactones: A Comparison between Ivermectin, Eprinomectin, and Moxidectin in Mice. Drug Metab Dispos 38:573–580. https://doi.org/10.1124/dmd.109.030700
doi: 10.1124/dmd.109.030700 pubmed: 20089736
Kropf C, Fent K, Fischer S et al (2020) ABC transporters in gills of rainbow trout (Oncorhynchus mykiss). J Exp Biol 223:jeb221069. https://doi.org/10.1242/jeb.221069
doi: 10.1242/jeb.221069 pubmed: 32532865
Kurelec B (1992) The Multixenobiotic Resistance Mechanism in Aquatic Organisms. Crit Rev Toxicol 22:23–43. https://doi.org/10.3109/10408449209145320
doi: 10.3109/10408449209145320 pubmed: 1352103
Kurelec B, Pivčević B (1991) Evidence for a multixenobiotic resistance mechanism in the mussel Mytilus galloprovincialis. Aquat Toxicol 19:291–301. https://doi.org/10.1016/0166-445X(91)90054-D
doi: 10.1016/0166-445X(91)90054-D
Kurth D, Brack W, Luckenbach T (2015) Is chemosensitisation by environmental pollutants ecotoxicologically relevant? Aquat Toxicol 167:134–142. https://doi.org/10.1016/j.aquatox.2015.07.017
doi: 10.1016/j.aquatox.2015.07.017 pubmed: 26281775
Leopoldo M, Nardulli P, Contino M et al (2019) An updated patent review on P-glycoprotein inhibitors (2011–2018). Expert Opin Ther Pat 29:455–461. https://doi.org/10.1080/13543776.2019.1618273
doi: 10.1080/13543776.2019.1618273 pubmed: 31079547
Leslie EM, Deeley RG, Cole SPC (2005) Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 204:216–237. https://doi.org/10.1016/j.taap.2004.10.012
doi: 10.1016/j.taap.2004.10.012 pubmed: 15845415
Liebig M, Fernandez ÁA, Blübaum-Gronau E et al (2010) Environmental risk assessment of ivermectin: A case study. Integr Environ Assess Manag 6:567–587. https://doi.org/10.1002/ieam.96
doi: 10.1002/ieam.96 pubmed: 20821718
Lifschitz A, Entrocasso C, Alvarez L et al (2010a) Interference with P-glycoprotein improves ivermectin activity against adult resistant nematodes in sheep. Vet Parasitol 172:291–298. https://doi.org/10.1016/j.vetpar.2010.04.039
doi: 10.1016/j.vetpar.2010.04.039 pubmed: 20605686
Lifschitz A, Suarez VH, Sallovitz J et al (2010b) Cattle nematodes resistant to macrocyclic lactones: Comparative effects of P-glycoprotein modulation on the efficacy and disposition kinetics of ivermectin and moxidectin. Exp Parasitol 125:172–178. https://doi.org/10.1016/j.exppara.2010.01.009
doi: 10.1016/j.exppara.2010.01.009 pubmed: 20109455
Lončar J, Popović M, Zaja R, Smital T (2010) Gene expression analysis of the ABC efflux transporters in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol Part C Toxicol Pharmacol 151:209–215. https://doi.org/10.1016/j.cbpc.2009.10.009
doi: 10.1016/j.cbpc.2009.10.009
Love RC, Osachoff HL, Kennedy CJ (2021) Short communication: Tissue-specific transcript expression of P-glycoprotein isoforms abcb1a and abcb1b in rainbow trout (Oncorhynchus mykiss) following induction with clotrimazole. Comp Biochem Physiol B Biochem Mol Biol 252:110538. https://doi.org/10.1016/j.cbpb.2020.110538
doi: 10.1016/j.cbpb.2020.110538 pubmed: 33227421
Luckenbach T, Fischer S, Sturm A (2014) Current advances on ABC drug transporters in fish. Comp Biochem Physiol Part C Toxicol Pharmacol 165:28–52. https://doi.org/10.1016/j.cbpc.2014.05.002
doi: 10.1016/j.cbpc.2014.05.002
Manor ML, Weber GM, Salem M et al (2012) Effect of sexual maturation and triploidy on chemical composition and fatty acid content of energy stores in female rainbow trout, Oncorhynchus mykiss. Aquaculture 364–365:312–321. https://doi.org/10.1016/j.aquaculture.2012.08.012
doi: 10.1016/j.aquaculture.2012.08.012
Miller DS, Graeff C, Droulle L et al (2002) Xenobiotic efflux pumps in isolated fish brain capillaries. Am J Physiol-Regul Integr Comp Physiol 282:R191–R198. https://doi.org/10.1152/ajpregu.00305.2001
doi: 10.1152/ajpregu.00305.2001 pubmed: 11742838
Nichols J, Rheingans P, Lothenbach D et al (1994) Three-dimensional visualization of physiologically based kinetic model outputs. Environ Health Perspect 102:952–956. https://doi.org/10.1289/ehp.94102952
doi: 10.1289/ehp.94102952 pubmed: 9738209 pmcid: 1567460
Okour M, Brundage RC (2017) Modeling Enterohepatic Circulation. Curr Pharmacol Rep 3:301–313. https://doi.org/10.1007/s40495-017-0096-z
doi: 10.1007/s40495-017-0096-z
PerkinElmer (2008) LSC in practice: LSC sample preparation by solubilization. PerkinElmer, Waltham
Qadir M, O’Loughlin KL, Fricke SM et al (2005) Cyclosporin A Is a Broad-Spectrum Multidrug Resistance Modulator. Clin Cancer Res 11:2320–2326. https://doi.org/10.1158/1078-0432.CCR-04-1725
doi: 10.1158/1078-0432.CCR-04-1725 pubmed: 15788683
Rowland M, Tozer TN (2011) Clinical pharmacokinetics and pharmacodynamics: concepts and applications, 4th edn. Wolters Kluwer Health/Lippincott William & Wilkins, Philadelphia
Scott EW, McKellar QA (1992) The distribution and some pharmacokinetic parameters of ivermectin in pigs. Vet Res Commun 16:139–146. https://doi.org/10.1007/BF01839011
doi: 10.1007/BF01839011 pubmed: 1496816
Shaikh B, Rummel N, Gieseker C et al (2007) Residue depletion of tritium-labeled ivermectin in rainbow trout following oral administration. Aquaculture 272:192–198. https://doi.org/10.1016/j.aquaculture.2007.08.050
doi: 10.1016/j.aquaculture.2007.08.050
Silva R, Vilas-Boas V, Carmo H et al (2015) Modulation of P-glycoprotein efflux pump: induction and activation as a therapeutic strategy. Pharmacol Ther 149:1–123. https://doi.org/10.1016/j.pharmthera.2014.11.013
doi: 10.1016/j.pharmthera.2014.11.013 pubmed: 25435018
Smital T, Kurelec B (1998) The chemosensitizers of multixenobiotic resistance mechanism in aquatic invertebrates: a new class of pollutants. Mutat Res Mol Mech Mutagen 399:43–53. https://doi.org/10.1016/S0027-5107(97)00265-0
doi: 10.1016/S0027-5107(97)00265-0
Smital T, Luckenbach T, Sauerborn R et al (2004) Emerging contaminants—pesticides, PPCPs, microbial degradation products and natural substances as inhibitors of multixenobiotic defense in aquatic organisms. Mutat Res Mol Mech Mutagen 552:101–117. https://doi.org/10.1016/j.mrfmmm.2004.06.006
doi: 10.1016/j.mrfmmm.2004.06.006
Stoknes IS, Økland HMW, Falch E, Synnes M (2004) Fatty acid and lipid class composition in eyes and brain from teleosts and elasmobranchs. Comp Biochem Physiol B Biochem Mol Biol 138:183–191. https://doi.org/10.1016/j.cbpc.2004.03.009
doi: 10.1016/j.cbpc.2004.03.009 pubmed: 15193274
Su L, Cheng CY, Mruk DD (2009) Drug transporter, P-glycoprotein (MDR1), is an integrated component of the mammalian blood–testis barrier. Int J Biochem Cell Biol 41:2578–2587. https://doi.org/10.1016/j.biocel.2009.08.015
doi: 10.1016/j.biocel.2009.08.015 pubmed: 19720156 pmcid: 2783494
Waser WP, Heisler N (2004) Oxygen delivery to the fish eye: blood flow in the pseudobranchial arteryof rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 30:77–85. https://doi.org/10.1007/s10695-005-0268-3
doi: 10.1007/s10695-005-0268-3
Whyte SK, Poley JD, Mueller A et al (2019) Avermectin treatment for Lepeophtheirus salmonis: Impacts on host (Salmo salar) and parasite immunophysiology. Aquaculture 501:488–501. https://doi.org/10.1016/j.aquaculture.2018.10.036
doi: 10.1016/j.aquaculture.2018.10.036
Wolfsegger MJ, Jaki T (2009) Non-compartmental estimation of pharmacokinetic parameters in serial sampling designs. J Pharmacokinet Pharmacodyn 36:479. https://doi.org/10.1007/s10928-009-9133-9
doi: 10.1007/s10928-009-9133-9 pubmed: 19847629
Wu X, Whitfield LR, Stewart BH (2000) Atorvastatin Transport in the Caco-2 Cell Model: Contributions of P-Glycoprotein and the Proton-Monocarboxylic Acid Co-Transporter. Pharm Res 17:209–215. https://doi.org/10.1023/A:1007525616017
doi: 10.1023/A:1007525616017 pubmed: 10751037
Zaja R, Klobučar RS, Smital T (2007) Detection and functional characterization of Pgp1 (ABCB1) and MRP3 (ABCC3) efflux transporters in the PLHC-1 fish hepatoma cell line. Aquat Toxicol 81:365–376. https://doi.org/10.1016/j.aquatox.2006.12.015
doi: 10.1016/j.aquatox.2006.12.015 pubmed: 17313982
Zaja R, Lončar J, Popovic M, Smital T (2011) First characterization of fish P-glycoprotein (abcb1) substrate specificity using determinations of its ATPase activity and calcein-AM assay with PLHC-1/dox cell line. Aquat Toxicol 103:53–62. https://doi.org/10.1016/j.aquatox.2011.02.005
doi: 10.1016/j.aquatox.2011.02.005 pubmed: 21392495

Auteurs

Christina U Johnston (CU)

Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia, Canada.

Vinicius Cavicchioli Azevedo (VC)

Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia, Canada.

Christopher J Kennedy (CJ)

Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia, Canada. ckennedy@sfu.ca.

Classifications MeSH