Malaria-induced Alterations of Drug Kinetics and Metabolism in Rodents and Humans

Author(s): Ana C.A.X. De-Oliveira*, Francisco J.R. Paumgartten

Journal Name: Current Drug Metabolism

Volume 22 , Issue 2 , 2021


Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

Background: Infections and inflammation lead to a downregulation of drug metabolism and kinetics in experimental animals. These changes in the expression and activities of drug-metabolizing enzymes may affect the effectiveness and safety of pharmacotherapy of infections and inflammatory conditions.

Objective: In this review, we addressed the available evidence on the effects of malaria on drug metabolism activity and kinetics in rodents and humans.

Results: An extensive literature review indicated that infection by Plasmodium spp consistently decreased the activity of hepatic Cytochrome P450s and phase-2 enzymes as well as the clearance of a variety of drugs in mice (lethal and non-lethal) and rat models of malaria. Malaria-induced CYP2A5 activity in the mouse liver was an exception. Except for paracetamol, pharmacokinetic trials in patients during acute malaria and in convalescence corroborated rodent findings. Trials showed that, in acute malaria, clearance of quinine, primaquine, caffeine, metoprolol, omeprazole, and antipyrine is slower and that AUCs are greater than in convalescent individuals.

Conclusion: Notwithstanding the differences between rodent models and human malaria, studies in P. falciparum and P. vivax patients confirmed rodent data showing that CYP-mediated clearance of antimalarials and other drugs is depressed during the symptomatic disease when rises in levels of acute-phase proteins and inflammatory cytokines occur. Evidence suggests that inflammatory cytokines and the interplay between malaria-activated NF-kB-signaling and cell pathways controlling phase 1/2 enzyme genes transcription mediate drug metabolism changes. The malaria-induced decrease in drug clearance may exacerbate drug-drug interactions, and the occurrence of adverse drug events, particularly when patients are treated with narrow-margin-of-safety medicines.

Keywords: Drug metabolizing enzymes, Plasmodium falciparum, Plasmodium berghei, Plasmodium chabaudi, antimalarial drugs, pharmacokinetic changes, inflammatory stimuli, innate immune responses.

[1]
Renton, K.W. Regulation of drug metabolism and disposition during inflammation and infection. Expert Opin. Drug Metab. Toxicol., 2005, 1(4), 629-640.
[http://dx.doi.org/10.1517/17425255.1.4.629] [PMID: 16863429]
[2]
Aitken, A.E.; Richardson, T.A.; Morgan, E.T. Regulation of drug-metabolizing enzymes and transporters in inflammation. Annu. Rev. Pharmacol. Toxicol., 2006, 46, 123-149.
[http://dx.doi.org/10.1146/annurev.pharmtox.46.120604.141059] [PMID: 16402901]
[3]
Petrovic, V.; Teng, S.; Piquette-Miller, M. Regulation of drug transporters during infection and inflammation. Mol. Interv., 2007, 7(2), 99-111.
[http://dx.doi.org/10.1124/mi.7.2.10] [PMID: 17468390]
[4]
Morgan, E.T. Impact of infectious and inflammatory disease on cytochrome P450-mediated drug metabolism and pharmacokinetics. Clin. Pharmacol. Ther., 2009, 85(4), 434-438.
[http://dx.doi.org/10.1038/clpt.2008.302] [PMID: 19212314]
[5]
Coutant, D.E.; Hall, S.D. Disease-drug interactions in inflammatory states via effects on CYP-mediated drug clearance. J. Clin. Pharmacol., 2018, 58(7), 849-863.
[http://dx.doi.org/10.1002/jcph.1093] [PMID: 29505093]
[6]
De-Oliveira, A.C.A.X.; Da-Matta, A.C.; Paumgartten, F.J.R. Plasmodium berghei (ANKA): infection induces CYP2A5 and 2E1 while depressing other CYP isoforms in the mouse liver. Exp. Parasitol., 2006, 113(4), 256-261.
[http://dx.doi.org/10.1016/j.exppara.2006.01.013] [PMID: 16540109]
[7]
De-Oliveira, A.C.A.X.; Carvalho, R.S.; Paixão, F.H.M.; Tavares, H.S.; Gueiros, L.S.; Siqueira, C.M.; Paumgartten, F.J.R. Up- and down-modulation of liver cytochrome P450 activities and associated events in two murine malaria models. Malar. J., 2010, 9(1), 9-17.
[8]
Alvares, A.P.; Ueng, T-H.; Scheibel, L.W.; Hollingdale, M.R. Impairment of hepatic cytochrome P-450-dependent monooxygenases by the malaria parasite Plasmodium berghei. Mol. Biochem. Parasitol., 1984, 13(3), 277-282.
[http://dx.doi.org/10.1016/0166-6851(84)90119-1] [PMID: 6396516]
[9]
Srivastava, P.; Tripathi, L.M.; Puri, S.K.; Dutta, G.P.; Pandey, V.C. Effect of Plasmodium berghei infection and chloroquine on the hepatic drug metabolizing system of mice. Int. J. Parasitol., 1991, 21(4), 463-466.
[http://dx.doi.org/10.1016/0020-7519(91)90104-F] [PMID: 1917287]
[10]
Poça, K.S.; De-Oliveira, A.C.A.X.; Santos, M.J.; Paumgartten, F.J. Malaria infection modulates effects of genotoxic chemicals in the mouse bone-marrow micronucleus test. Mutat. Res., 2008, 649(1-2), 28-33.
[http://dx.doi.org/10.1016/j.mrgentox.2007.07.006] [PMID: 17851116]
[11]
Carvalho, R.S.; Friedrich, K.; De-Oliveira, A.C.A.X.; Suarez-Kurtz, G.; Paumgartten, F.J.R. Malaria downmodulates mRNA expression and catalytic activities of CYP1A2, 2E1 and 3A11 in mouse liver. Eur. J. Pharmacol., 2009, 616(1-3), 265-269.
[http://dx.doi.org/10.1016/j.ejphar.2009.05.030] [PMID: 19501084]
[12]
Krücken, J.; Delić, D.; Pauen, H.; Wojtalla, A.; El-Khadragy, M.; Dkhil, M.; Mossmann, H.; Wunderlich, F. Augmented particle trapping and attenuated inflammation in the liver by protective vaccination against Plasmodium chabaudi malaria. Mal. J., 2009, 8(1), 8-11.
[13]
Mimche, S.M.; Lee, C.M.; Liu, K.H.; Mimche, P.N.; Harvey, R.D.; Murphy, T.J.; Nyagode, B.A.; Jones, D.P.; Lamb, T.J.; Morgan, E.T. A non-lethal malarial infection results in reduced drug metabolizing enzyme expression and drug clearance in mice. Malar. J., 2019, 18(1), 234.
[http://dx.doi.org/10.1186/s12936-019-2860-5] [PMID: 31299982]
[14]
Cressman, A.M.; McDonald, C.R.; Silver, K.; Kain, K.C.; Piquette-Miller, M. Malaria infection alters the expression of hepatobiliary and placental drug transporters in pregnant mice. Drug Metab. Dispos., 2014, 42(4), 603-610.
[http://dx.doi.org/10.1124/dmd.113.053983] [PMID: 24281836]
[15]
Saxena, N.; Saxena, A.; Dutta, G.P.; Ghatak, S.; Pandey, V.C. Effect of Plasmodium yoelii nigeriensis infection and chloroquine on the hepatic mixed function oxidase system of mice. Mol. Biochem. Parasitol., 1987, 24(3), 283-287.
[http://dx.doi.org/10.1016/0166-6851(87)90160-5] [PMID: 3627173]
[16]
Srivastava, P.; Sharma, S.N.; Shukla, O.P.; Pandey, V.C. Studies of the hepatic mitochondrial and microsomal mixed-function oxidase system during Plasmodium yoelii infection and inducer treatment in Swiss albino mice. Trop. Med. Int. Health, 1997, 2(10), 989-992.
[http://dx.doi.org/10.1046/j.1365-3156.1997.d01-157.x] [PMID: 9357489]
[17]
Srivastava, P.; Pandey, V.C. Studies on hepatic mitochondrial cytochrome P-450 during Plasmodium yoelii infection and pyrimethamine treatment in mice. Ecotoxicol. Environ. Saf., 2000, 46(1), 19-22.
[http://dx.doi.org/10.1006/eesa.1999.1867] [PMID: 10805988]
[18]
Agrawal, A. Studies on drug metabolizing enzymes during arteether treatment of Plasmodium yoelii nigeriensis infected mice cerebral microvessels. J. Commun. Dis., 2005, 37(1), 44-50.
[PMID: 16637400]
[19]
Song, G.H.; Andre, R.G.; Scheibel, L.W.; Wirtz, R.A.; Strickman, D.A.; Cheriathundam, E.; Alvares, A.P. Plasmodium berghei: sensitivity of chloroquine-resistant and chloroquine-sensitive strains to irradiation and the effect of irradiated malaria parasites on cytochrome P450-dependent monooxygenases. Res. Commun. Mol. Pathol. Pharmacol., 1995, 90(1), 75-86.
[PMID: 8581351]
[20]
Pandey, A.V.; Srivastava, P.; Tekwani, B.L.; Pandey, V.C. Effect of Plasmodium yoelii infection on constitutive and phenobarbitone inducible mixed function oxidase system of mice. J. Parasit. Dis., 1996, 20, 141-144.
[21]
Ahmad, R.; Srivastava, A.K. Effect of Plasmodium yoelii nigeriensis infection on hepatic and splenic glutathione-S-transferase(s) in Swiss albino and db/+ mice: efficacy of mefloquine and menadione in antimalarial chemotherapy. Parasitology, 2007, 134(Pt 7), 931-938.
[http://dx.doi.org/10.1017/S003118200700234X] [PMID: 17352848]
[22]
McCarthy, J.S.; Furner, R.L.; Van Dyke, K.; Stitzel, R.E. Effects of malarial infection on host microsomal drug-metabolizing enzymes. Biochem. Pharmacol., 1970, 19(4), 1341-1349.
[http://dx.doi.org/10.1016/0006-2952(70)90049-3] [PMID: 5513924]
[23]
Mihaly, G.W.; Date, N.M.; Veenendaal, J.R.; Newman, K.T.; Smallwood, R.A. Decreased hepatic elimination of pyrimethamine during malaria infection. Studies in the isolated perfused rat liver. Biochem. Pharmacol., 1987, 36(17), 2827-2829.
[http://dx.doi.org/10.1016/0006-2952(87)90272-3] [PMID: 3307789]
[24]
Mihaly, G.W.; Date, N.M.; Ireton, H.J.; Smallwood, R.A. The effect of malaria infection on primaquine elimination in the isolated perfused rat liver. Biochem. Pharmacol., 1987, 36(2), 225-228.
[http://dx.doi.org/10.1016/0006-2952(87)90693-9] [PMID: 3814168]
[25]
Mansor, S.M.; Edwards, G.; Roberts, P.J.; Ward, S.A. The effect of malaria infection on paracetamol disposition in the rat. Biochem. Pharmacol., 1991, 41(11), 1707-1711.
[http://dx.doi.org/10.1016/0006-2952(91)90173-3] [PMID: 2043159]
[26]
Mansor, S.M.; Ward, S.A.; Edwards, G. The effect of malaria infection on antipyrine metabolite formation in the rat. Biochem. Pharmacol., 1991, 41(8), 1264-1266.
[http://dx.doi.org/10.1016/0006-2952(91)90669-V] [PMID: 2009102]
[27]
Ismail, S.; Back, D.J.; Edwards, G. The effect of malaria infection on 3′-azido-3′-deoxythymidine and paracetamol glucuronidation in rat liver microsomes. Biochem. Pharmacol., 1992, 44(9), 1879-1882.
[http://dx.doi.org/10.1016/0006-2952(92)90084-V] [PMID: 1449539]
[28]
Ismail, S.; Kokwaro, G.O.; Back, D.J.; Edwards, G. Effect of malaria infection on the pharmacokinetics of paracetamol in rat. Xenobiotica, 1994, 24(6), 527-533.
[http://dx.doi.org/10.3109/00498259409043255] [PMID: 7975718]
[29]
Murdoch, R.T.; Ghabrial, H.; Smallwood, R.A.; Morgan, D.J. Effect of malaria on phenol conjugation pathways in perfused rat liver. Biochem. Pharmacol., 1992, 43(6), 1229-1234.
[http://dx.doi.org/10.1016/0006-2952(92)90496-6] [PMID: 1562275]
[30]
Kokwaro, G.O.; Glazier, A.P.; Ward, S.A.; Breckenridge, A.M.; Edwards, G. Effect of malaria infection and endotoxin-induced fever on phenacetin O-deethylation by rat liver microsomes. Biochem. Pharmacol., 1993, 45(6), 1235-1241.
[http://dx.doi.org/10.1016/0006-2952(93)90275-2] [PMID: 8466544]
[31]
Kokwaro, G.O.; Ismail, S.; Glazier, A.P.; Ward, S.A.; Edwards, G. Effect of malaria infection and endotoxin-induced fever on the metabolism of antipyrine and metronidazole in the rat. Biochem. Pharmacol., 1993, 45(6), 1243-1249.
[http://dx.doi.org/10.1016/0006-2952(93)90276-3] [PMID: 8466545]
[32]
Kokwaro, G.O.; Szwandt, I.S.; Glazier, A.P.; Ward, S.A.; Edwards, G. Metabolism of caffeine and theophylline in rats with malaria and endotoxin-induced fever. Xenobiotica, 1993, 23(12), 1391-1397.
[http://dx.doi.org/10.3109/00498259309059448] [PMID: 8135041]
[33]
Glazier, A.P.; Kokwaro, G.O.; Edwards, G. Possible isozyme-specific effects of experimental malaria infection with Plasmodium berghei on cytochrome P450 activity in rat liver microsomes. J. Pharm. Pharmacol., 1994, 46(5), 352-355.
[http://dx.doi.org/10.1111/j.2042-7158.1994.tb03811.x] [PMID: 8083805]
[34]
Glazier, A.P.; Kokwaro, G.O.; Ismail, S.; Edwards, G. Effect of an experimental malaria infection on the metabolism of phenacetin in the rat isolated perfused liver. Xenobiotica, 1994, 24(8), 785-793.
[http://dx.doi.org/10.3109/00498259409043278] [PMID: 7839701]
[35]
Leo, K.U.; Grace, J.M.; Li, Q.; Peggins, J.; Mitchell, A.L.; Aguilar, T.; Brewer, T.G. Effects of Plasmodium berghei infection on arteether metabolism and disposition. Pharmacology, 1997, 54(5), 276-284.
[http://dx.doi.org/10.1159/000139496] [PMID: 9380774]
[36]
Uhl, K.; Grace, J.M.; Kocisko, D.A.; Jennings, B.T.; Mitchell, A.L.; Brewer, T.G. Effects of Plasmodium berghei infection on cytochromes P-450 2E1 and 3A2. Eur. J. Drug Metab. Pharmacokinet., 1999, 24(2), 169-176.
[http://dx.doi.org/10.1007/BF03190365] [PMID: 10510746]
[37]
Nneji, C.M.; Adaramoye, O.A.; Falade, C.O.; Ademowo, O.G. Effect of chloroquine, methylene blue and artemether on red cell and hepatic antioxidant defence system in mice infected with Plasmodium yoelii nigeriensis. Parasitol. Res., 2013, 112(7), 2619-2625.
[http://dx.doi.org/10.1007/s00436-013-3426-z] [PMID: 23604568]
[38]
Pussard, E.; Bernier, A.; Fouquet, E.; Bouree, P. Quinine distribution in mice with Plasmodium berghei malaria. Eur. J. Drug Metab. Pharmacokinet., 2003, 28(1), 11-20.
[http://dx.doi.org/10.1007/BF03190862] [PMID: 14503660]
[39]
Lirussi, F.; Pussard, E. Quinine distribution in pregnant mice with Plasmodium berghei malaria. Eur. J. Pharm. Sci., 2006, 28(4), 284-290.
[http://dx.doi.org/10.1016/j.ejps.2006.03.004] [PMID: 16716571]
[40]
Trenholme, G.M.; Williams, R.L.; Rieckmann, K.H.; Frischer, H.; Carson, P.E. Quinine disposition during malaria and during induced fever. Clin. Pharmacol. Ther., 1976, 19(4), 459-467.
[http://dx.doi.org/10.1002/cpt1976194459] [PMID: 773582]
[41]
White, N.J.; Looareesuwan, S.; Warrell, D.A.; Warrell, M.J.; Bunnag, D.; Harinasuta, T. Quinine pharmacokinetics and toxicity in cerebral and uncomplicated falciparum malaria. Am. J. Med., 1982, 73(4), 564-572.
[http://dx.doi.org/10.1016/0002-9343(82)90337-0] [PMID: 6751085]
[42]
Supanaranond, W.; Davis, T.M.; Pukrittayakamee, S.; Silamut, K.; Karbwang, J.; Molunto, P.; Chanond, L.; White, N.J. Disposition of oral quinine in acute falciparum malaria. Eur. J. Clin. Pharmacol., 1991, 40(1), 49-52.
[http://dx.doi.org/10.1007/BF00315138] [PMID: 2060545]
[43]
Edwards, G.; McGrath, C.S.; Ward, S.A.; Supanaranond, W.; Pukrittayakamee, S.; Davis, T.M.E.; White, N.J. Interactions among primaquine, malaria infection and other antimalarials in Thai subjects. Br. J. Clin. Pharmacol., 1993, 35(2), 193-198.
[http://dx.doi.org/10.1111/j.1365-2125.1993.tb05685.x] [PMID: 8443039]
[44]
Wilairatana, P.; Looareesuwan, S.; Vanijanonta, S.; Charoenlarp, P.; Wittayalertpanya, S. Hepatic metabolism in severe falciparum malaria: caffeine clearance study. Ann. Trop. Med. Parasitol., 1994, 88(1), 13-19.
[http://dx.doi.org/10.1080/00034983.1994.11812829] [PMID: 8192510]
[45]
Ismail, S.; Na Bangchang, K.; Karbwang, J.; Back, D.J.; Edwards, G. Paracetamol disposition in Thai patients during and after treatment of falciparum malaria. Eur. J. Clin. Pharmacol., 1995, 48(1), 65-69.
[http://dx.doi.org/10.1007/BF00202175] [PMID: 7621851]
[46]
Sowunmi, A. Disposition of oral quinine in African patients suffering from acute uncomplicated falciparum malaria. East Afr. Med. J., 1996, 73(8), 519-523.
[PMID: 8898467]
[47]
Pukrittayakamee, S.; Looareesuwan, S.; Keeratithakul, D.; Davis, T.M.; Teja-Isavadharm, P.; Nagachinta, B.; Weber, A.; Smith, A.L.; Kyle, D.; White, N.J. A study of the factors affecting the metabolic clearance of quinine in malaria. Eur. J. Clin. Pharmacol., 1997, 52(6), 487-493.
[http://dx.doi.org/10.1007/s002280050323] [PMID: 9342585]
[48]
Babalola, C.P.; Bolaji, O.O.; Ogunbona, F.A.; Sowunmi, A.; Walker, O. Pharmacokinetics of quinine in African patients with acute falciparum malaria. Pharm. World Sci., 1998, 20(3), 118-122.
[http://dx.doi.org/10.1023/A:1008699022244] [PMID: 9618735]
[49]
Akinyinka, O.O.; Sowunmi, A.; Honeywell, R.; Renwick, A.G. The pharmacokinetics of caffeine in Nigerian children suffering from malaria and kwashiorkor. Eur. J. Clin. Pharmacol., 2000, 56(2), 153-158.
[http://dx.doi.org/10.1007/s002280050734] [PMID: 10877010]
[50]
Akinyinka, O.O.; Sowunmi, A.; Honeywell, R.; Renwick, A.G. The effects of acute falciparum malaria on the disposition of caffeine and the comparison of saliva and plasma-derived pharmacokinetic parameters in adult Nigerians. Eur. J. Clin. Pharmacol., 2000, 56(2), 159-165.
[http://dx.doi.org/10.1007/s002280050735] [PMID: 10877011]
[51]
Kloprogge, F.; Jullien, V.; Piola, P.; Dhorda, M.; Muwanga, S.; Nosten, F.; Day, N.P.; White, N.J.; Guerin, P.J.; Tarning, J. Population pharmacokinetics of quinine in pregnant women with uncomplicated Plasmodium falciparum malaria in Uganda. J. Antimicrob. Chemother., 2014, 69(11), 3033-3040.
[http://dx.doi.org/10.1093/jac/dku228] [PMID: 24970740]
[52]
Huang, B.W.; Pearman, E.; Kim, C.C. Mouse models of uncomplicated and fatal malaria. Bio Protoc., 2015, 5(13), e1514.
[http://dx.doi.org/10.21769/BioProtoc.1514] [PMID: 26236758]
[53]
Craig, A.G.; Grau, G.E.; Janse, C.; Kazura, J.W.; Milner, D.; Barnwell, J.W.; Turner, G.; Langhorne, J. participants of the Hinxton Retreat meeting on Animal Models for Research on Severe Malaria. The role of animal models for research on severe malaria. PLoS Pathog., 2012, 8(2), e1002401.
[http://dx.doi.org/10.1371/journal.ppat.1002401] [PMID: 22319438]
[54]
Vaughan, A.M.; Aly, A.S.; Kappe, S.H. Malaria parasite pre-erythrocytic stage infection: gliding and hiding. Cell Host Microbe, 2008, 4(3), 209-218.
[http://dx.doi.org/10.1016/j.chom.2008.08.010] [PMID: 18779047]
[55]
Stephens, R.; Culleton, R.L.; Lamb, T.J. The contribution of Plasmodium chabaudi to our understanding of malaria. Trends Parasitol., 2012, 28(2), 73-82.
[http://dx.doi.org/10.1016/j.pt.2011.10.006] [PMID: 22100995]
[56]
Spence, P.J.; Jarra, W.; Lévy, P.; Nahrendorf, W.; Langhorne, J. Mosquito transmission of the rodent malaria parasite Plasmodium chabaudi. Malar. J., 2012, 11, 407.
[http://dx.doi.org/10.1186/1475-2875-11-407] [PMID: 23217144]
[57]
Huang, H.M.; McMorran, B.J.; Foote, S.J.; Burgio, G. Host genetics in malaria: lessons from mouse studies. Mamm. Genome, 2018, 29(7-8), 507-522.
[http://dx.doi.org/10.1007/s00335-018-9744-9] [PMID: 29594458]
[58]
Greischar, M.A.; Reece, S.E.; Savill, N.J.; Mideo, N. The challenge of quantifying synchrony in malaria parasites. Trends Parasitol., 2019, 35(5), 341-355.
[http://dx.doi.org/10.1016/j.pt.2019.03.002] [PMID: 30952484]
[59]
Niwa, T.; Yamazaki, H. Comparison of cytochrome P450 2C subfamily members in terms of drug oxidation rates and substrate inhibition. Curr. Drug Metab., 2012, 13(8), 1145-1159.
[http://dx.doi.org/10.2174/138920012802850092] [PMID: 22571484]
[60]
Quinn, T.C.; Wyler, D.J. Intravascular clearance of parasitized erythrocytes in rodent malaria. J. Clin. Invest., 1979, 63(6), 1187-1194.
[http://dx.doi.org/10.1172/JCI109413] [PMID: 376554]
[61]
Quinn, T.C.; Wyler, D.J. Resolution of acute malaria (Plasmodium berghei in the rat): reversibility and spleen dependence. Am. J. Trop. Med. Hyg., 1980, 29(1), 1-4.
[http://dx.doi.org/10.4269/ajtmh.1980.29.1] [PMID: 6986095]
[62]
Keita Alassane, S.; Nicolau-Travers, M-L.; Menard, S.; Andreoletti, O.; Cambus, J-P.; Gaudre, N.; Wlodarczyk, M.; Blanchard, N.; Berry, A.; Abbes, S.; Colongo, D.; Faye, B.; Augereau, J-M.; Lacroux, C.; Iriart, X.; Benoit-Vical, F. Young Sprague Dawley rats infected by Plasmodium berghei: a relevant experimental model to study cerebral malaria. PLoS One, 2017, 12(7), e0181300.
[http://dx.doi.org/10.1371/journal.pone.0181300] [PMID: 28742109]
[63]
Marcsisin, S.R.; Jin, X.; Bettger, T.; McCulley, N.; Sousa, J.C.; Shanks, G.D.; Tekwani, B.L.; Sahu, R.; Reichard, G.A.; Sciotti, R.J.; Melendez, V.; Pybus, B.S. CYP450 phenotyping and metabolite identification of quinine by accurate mass UPLC-MS analysis: a possible metabolic link to blackwater fever. Malar. J., 2013, 12, 214.
[http://dx.doi.org/10.1186/1475-2875-12-214] [PMID: 23800033]
[64]
Almeida, A.C.; Elias, A.B.R.; Marques, M.P.; de Melo, G.C.; da Costa, A.G.; Figueiredo, E.F.G.; Brasil, L.W.; Rodrigues-Soares, F.; Monteiro, W.M.; de Lacerda, M.V.G.; Lanchote, V.L.; Suarez-Kurtz, G. Impact of Plasmodium vivax malaria and antimalarial treatment on cytochrome P450 activity in Brazilian patients. Br. J. Clin. Pharmacol., 2020, Epub ahead of print.
[http://dx.doi.org/10.1111/bcp.14574] [PMID: 32997351]
[65]
Luzzi, G.A.; Peto, T.E. Adverse effects of antimalarials. An update. Drug Saf., 1993, 8(4), 295-311.
[http://dx.doi.org/10.2165/00002018-199308040-00004] [PMID: 8481216]
[66]
Zanger, U.M.; Schwab, M. Cytochrome P450 enzymes in drug metabolism: regulation of gene expression, enzyme activities, and impact of genetic variation. Pharmacol. Ther., 2013, 138(1), 103-141.
[http://dx.doi.org/10.1016/j.pharmthera.2012.12.007] [PMID: 23333322]
[67]
Marcsisin, S.R.; Reichard, G.; Pybus, B.S. Primaquine pharmacology in the context of CYP 2D6 pharmacogenomics: current state of the art. Pharmacol. Ther., 2016, 161, 1-10.
[http://dx.doi.org/10.1016/j.pharmthera.2016.03.011] [PMID: 27016470]
[68]
Clark, I.A.; Budd, A.C.; Alleva, L.M.; Cowden, W.B. Human malarial disease: a consequence of inflammatory cytokine release. Malar. J., 2006, 5, 85.
[http://dx.doi.org/10.1186/1475-2875-5-85] [PMID: 17029647]
[69]
Antonelli, L.R.; Junqueira, C.; Vinetz, J.M.; Golenbock, D.T.; Ferreira, M.U.; Gazzinelli, R.T. The immunology of Plasmodium vivax malaria. Immunol. Rev., 2020, 293(1), 163-189.
[http://dx.doi.org/10.1111/imr.12816] [PMID: 31642531]
[70]
Siewert, E.; Bort, R.; Kluge, R.; Heinrich, P.C.; Castell, J.; Jover, R. Hepatic cytochrome P450 down-regulation during aseptic inflammation in the mouse is interleukin 6 dependent. Hepatology, 2000, 32(1), 49-55.
[http://dx.doi.org/10.1053/jhep.2000.8532] [PMID: 10869288]
[71]
Aitken, A.E.; Lee, C.M.; Morgan, E.T. Roles of nitric oxide in inflammatory downregulation of human cytochromes P450. Free Radic. Biol. Med., 2008, 44(6), 1161-1168.
[http://dx.doi.org/10.1016/j.freeradbiomed.2007.12.010] [PMID: 18206661]
[72]
Khatsenko, O.G.; Gross, S.S.; Rifkind, A.B.; Vane, J.R. Nitric oxide is a mediator of the decrease in cytochrome P450-dependent metabolism caused by immunostimulants. Proc. Natl. Acad. Sci. USA, 1993, 90(23), 11147-11151.
[http://dx.doi.org/10.1073/pnas.90.23.11147] [PMID: 7504296]
[73]
Ke, S.; Rabson, A.B.; Germino, J.F.; Gallo, M.A.; Tian, Y. Mechanism of suppression of cytochrome P-450 1A1 expression by tumor necrosis factor-alpha and lipopolysaccharide. J. Biol. Chem., 2001, 276(43), 39638-39644.
[http://dx.doi.org/10.1074/jbc.M106286200] [PMID: 11470802]
[74]
Gu, X.; Ke, S.; Liu, D.; Sheng, T.; Thomas, P.E.; Rabson, A.B.; Gallo, M.A.; Xie, W.; Tian, Y. Role of NF-kB in regulation of PXR-mediated gene expression. J. Biol. Chem., 2006, 281(26), 17882-17889.
[http://dx.doi.org/10.1074/jbc.M601302200] [PMID: 16608838]
[75]
Punsawad, C.; Krudsood, S.; Maneerat, Y.; Chaisri, U.; Tangpukdee, N.; Pongponratn, E.; Nantavisai, K.; Udomsangpetch, R.; Viriyavejakul, P. Activation of nuclear factor kappa B in peripheral blood mononuclear cells from malaria patients. Malar. J., 2012, 11, 191.
[http://dx.doi.org/10.1186/1475-2875-11-191] [PMID: 22682094]
[76]
Viriyavejakul, P.; Khachonsaksumet, V.; Punsawad, C. Liver changes in severe Plasmodium falciparum malaria: histopathology, apoptosis and nuclear factor kappa B expression. Malar. J., 2014, 13, 106.
[http://dx.doi.org/10.1186/1475-2875-13-106] [PMID: 24636003]
[77]
Navarro-Mabarak, C.; Mitre-Aguilar, I.B.; Camacho-Carranza, R.; Arias, C.; Zentella-Dehesa, A.; Espinosa-Aguirre, J.J. Role of NF-κB in cytochrome P450 epoxygenases down-regulation during an inflammatory process in astrocytes. Neurochem. Int., 2019, 129, 104499.
[http://dx.doi.org/10.1016/j.neuint.2019.104499] [PMID: 31271766]
[78]
Zhou, C.; Tabb, M.M.; Nelson, E.L.; Grün, F.; Verma, S.; Sadatrafiei, A.; Lin, M.; Mallick, S.; Forman, B.M.; Thummel, K.E.; Blumberg, B. Mutual repression between steroid and xenobiotic receptor and NF-kappaB signaling pathways links xenobiotic metabolism and inflammation. J. Clin. Invest., 2006, 116(8), 2280-2289.
[http://dx.doi.org/10.1172/JCI26283] [PMID: 16841097]
[79]
Kusunoki, Y.; Ikarashi, N.; Hayakawa, Y.; Ishii, M.; Kon, R.; Ochiai, W.; Machida, Y.; Sugiyama, K. Hepatic early inflammation induces downregulation of hepatic cytochrome P450 expression and metabolic activity in the dextran sulfate sodium-induced murine colitis. Eur. J. Pharm. Sci., 2014, 54, 17-27.
[http://dx.doi.org/10.1016/j.ejps.2013.12.019] [PMID: 24413062]
[80]
Abualsunun, W.A.; Piquette-Miller, M. Involvement of Nuclear Factor κB, not Pregnane X Receptor, in Inflammation-Mediated Regulation of Hepatic Transporters. Drug Metab. Dispos., 2017, 45(10), 1077-1083.
[http://dx.doi.org/10.1124/dmd.117.076927] [PMID: 28778997]
[81]
Zhou, M.; Maitra, S.R.; Wang, P. The potential role of transcription factor aryl hydrocarbon receptor in downregulation of hepatic cytochrome P-450 during sepsis. Int. J. Mol. Med., 2008, 21(4), 423-8.
[http://dx.doi.org/10.3892/ijmm.21.4.423]
[82]
Wu, R.; Cui, X.; Dong, W.; Zhou, M.; Simms, H.H.; Wang, P. Suppression of hepatocyte CYP1A2 expression by Kupffer cells via AhR pathway: the central role of proinflammatory cytokines. Int. J. Mol. Med., 2006, 18(2), 339-346.
[http://dx.doi.org/10.3892/ijmm.18.2.339] [PMID: 16820944]
[83]
Assenat, E.; Gerbal-Chaloin, S.; Larrey, D.; Saric, J.; Fabre, J.M.; Maurel, P.; Vilarem, M.J.; Pascussi, J.M. Interleukin 1beta inhibits CAR-induced expression of hepatic genes involved in drug and bilirubin clearance. Hepatology, 2004, 40(4), 951-960.
[http://dx.doi.org/10.1002/hep.20387] [PMID: 15382119]
[84]
Pascussi, J.M.; Gerbal-Chaloin, S.; Pichard-Garcia, L.; Daujat, M.; Fabre, J.M.; Maurel, P.; Vilarem, M.J. Interleukin-6 negatively regulates the expression of pregnane X receptor and constitutively activated receptor in primary human hepatocytes. Biochem. Biophys. Res. Commun., 2000, 274(3), 707-713.
[http://dx.doi.org/10.1006/bbrc.2000.3219] [PMID: 10924340]
[85]
Chen, Y-H.; Wang, J-P.; Wang, H.; Sun, M-F.; Wei, L-Z.; Wei, W.; Xu, D.X. Lipopolysaccharide treatment downregulates the expression of the pregnane X receptor, cyp3a11 and mdr1a genes in mouse placenta. Toxicology, 2005, 211(3), 242-252.
[http://dx.doi.org/10.1016/j.tox.2005.03.011] [PMID: 15869837]
[86]
Xu, D-X.; Wei, W.; Sun, M-F.; Wu, C-Y.; Wang, J-P.; Wei, L-Z.; Zhou, C.F. Kupffer cells and reactive oxygen species partially mediate lipopolysaccharide-induced downregulation of nuclear receptor pregnane x receptor and its target gene CYP3a in mouse liver. Free Radic. Biol. Med., 2004, 37(1), 10-22.
[http://dx.doi.org/10.1016/j.freeradbiomed.2004.03.021] [PMID: 15183191]
[87]
Satarug, S.; Lang, M.A.; Yongvanit, P.; Sithithaworn, P.; Mairiang, E.; Mairiang, P.; Pelkonen, P.; Bartsch, H.; Haswell-Elkins, M.R. Induction of cytochrome P450 2A6 expression in humans by the carcinogenic parasite infection, opisthorchiasis viverrini. Cancer Epidemiol. Biomarkers Prev., 1996, 5(10), 795-800.
[PMID: 8896890]
[88]
Kobliakov, V.; Kulikova, L.; Samoilov, D.; Lang, M.A. High expression of cytochrome P450 2a-5 (coumarin 7-hydroxylase) in mouse hepatomas. Mol. Carcinog., 1993, 7(4), 276-280.
[http://dx.doi.org/10.1002/mc.2940070411] [PMID: 8352886]
[89]
Sipowicz, M.A.; Chomarat, P.; Diwan, B.A.; Anver, M.A.; Awasthi, Y.C.; Ward, J.M.; Rice, J.M.; Kasprzak, K.S.; Wild, C.P.; Anderson, L.M. Increased oxidative DNA damage and hepatocyte overexpression of specific cytochrome P450 isoforms in hepatitis of mice infected with Helicobacter hepaticus. Am. J. Pathol., 1997, 151(4), 933-941.
[PMID: 9327726]
[90]
Kirby, G.M.; Nichols, K.D.; Antenos, M. CYP2A5 induction and hepatocellular stress: an adaptive response to perturbations of heme homeostasis. Curr. Drug Metab., 2011, 12(2), 186-197.
[http://dx.doi.org/10.2174/138920011795016845] [PMID: 21395539]
[91]
Deroost, K.; Lays, N.; Pham, T-T.; Baci, D.; Van den Eynde, K.; Komuta, M.; Prato, M.; Roskams, T.; Schwarzer, E.; Opdenakker, G.; Van den Steen, P.E. Hemozoin induces hepatic inflammation in mice and is differentially associated with liver pathology depending on the Plasmodium strain. PLoS One, 2014, 9(11), e113519.
[http://dx.doi.org/10.1371/journal.pone.0113519] [PMID: 25419977]
[92]
Pereira, M.L.M.; Marinho, C.R.F.; Epiphanio, S. Could heme oxygenase-1 be a new target for therapeutic intervention in malaria-associated acute lung injury/acute respiratory distress syndrome? Front. Cell. Infect. Microbiol., 2018, 8, 161.
[http://dx.doi.org/10.3389/fcimb.2018.00161] [PMID: 29868517]
[93]
Lämsä, V.; Levonen, A.L.; Sormunen, R.; Yamamoto, M.; Hakkola, J. Heme and heme biosynthesis intermediates induce heme oxygenase-1 and cytochrome P450 2A5, enzymes with putative sequential roles in heme and bilirubin metabolism: different requirement for transcription factor nuclear factor erythroid- derived 2-like 2. Toxicol. Sci., 2012, 130(1), 132-144.
[http://dx.doi.org/10.1093/toxsci/kfs237] [PMID: 22859313]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 22
ISSUE: 2
Year: 2021
Published on: 01 January, 2021
Page: [127 - 138]
Pages: 12
DOI: 10.2174/1389200221999210101232057
Price: $65

Article Metrics

PDF: 35
HTML: 1