Heterotropic Activation of Cytochrome P450 3A4 by Perillyl Alcohol

<b>Background/Objectives</b>: Perillyl alcohol (POH), a monoterpene natural product derived from the essential oils of plants such as perilla (<i>Perilla frutescens</i>), is currently in phase I and II clinical trials as a chemotherapeutic agent. In this study, we investigate...

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Main Authors: Ji Hyeon Ryu, Jieun Yu, Jang Su Jeon, Seongyea Jo, Soo Min Lee, Hyemin Kim, Han-Jin Park, Soo Jin Oh, Sang Kyum Kim
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Pharmaceutics
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Online Access:https://www.mdpi.com/1999-4923/16/12/1581
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author Ji Hyeon Ryu
Jieun Yu
Jang Su Jeon
Seongyea Jo
Soo Min Lee
Hyemin Kim
Han-Jin Park
Soo Jin Oh
Sang Kyum Kim
author_facet Ji Hyeon Ryu
Jieun Yu
Jang Su Jeon
Seongyea Jo
Soo Min Lee
Hyemin Kim
Han-Jin Park
Soo Jin Oh
Sang Kyum Kim
author_sort Ji Hyeon Ryu
collection DOAJ
description <b>Background/Objectives</b>: Perillyl alcohol (POH), a monoterpene natural product derived from the essential oils of plants such as perilla (<i>Perilla frutescens</i>), is currently in phase I and II clinical trials as a chemotherapeutic agent. In this study, we investigated the effect of POH on cytochrome P450 (CYP) activity for evaluating POH–drug interaction potential. <b>Methods</b>: The investigation was conducted using pooled human liver microsomes (HLMs), recombinant CYP3A4 (rCYP3A4) enzymes, and human pluripotent stem cell-derived hepatic organoids (hHOs) employing liquid chromatography-tandem mass spectrometry. <b>Results</b>: POH inhibited the activities of CYP2A6 and CYP2B6 with K<sub>i</sub> of 6.35 and 3.78 μM, respectively, whereas it stimulated CYP3A4 activity in pooled HLMs incubated with midazolam (MDZ). In a direct CYP inhibition assay using HLMs, activities of CYP2C9, CYP2C19, and CYP2E1 were also inhibited by POH, with IC<sub>50</sub> values greater than 50 μM, but those of CYP1A2, CYP2C8, CYP2D6, and CYP3A4 (testosterone) were not significantly inhibited. In pooled HLMs, the V<sub>max</sub>/K<sub>m</sub> value of 1′-hydroxy MDZ, but not that of 4-hydroxy MDZ, was increased 2.7-fold by 100 μM POH compared with that in the absence of POH. Moreover, stimulation of MDZ 1′-hydroxylation by CYP3A4 was observed in hHOs and rCYP3A4 with cytochrome <i>b</i><sub>5</sub> but not rCYP3A4 without cytochrome <i>b</i><sub>5</sub>. Furthermore, activation of CYP3A4-mediated metabolism by POH was observed in HLMs incubated with fimasartan but not atorvastatin, buspirone, donepezil, nifedipine, or tadalafil, suggesting a substrate-dependent activation of CYP3A4 by POH. <b>Conclusions</b>: POH inhibits CYP2A6 and CYP2B6, but it activates CYP3A4. These findings underscore the need for further evaluation of the interactions of clinical drugs with POH.
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spelling doaj-art-9f32b504b16043ab91781ff71746f7452024-12-27T14:46:35ZengMDPI AGPharmaceutics1999-49232024-12-011612158110.3390/pharmaceutics16121581Heterotropic Activation of Cytochrome P450 3A4 by Perillyl AlcoholJi Hyeon Ryu0Jieun Yu1Jang Su Jeon2Seongyea Jo3Soo Min Lee4Hyemin Kim5Han-Jin Park6Soo Jin Oh7Sang Kyum Kim8College of Pharmacy, Chungnam National University, Daejeon 34134, Republic of KoreaCollege of Pharmacy, Chungnam National University, Daejeon 34134, Republic of KoreaCollege of Pharmacy, Chungnam National University, Daejeon 34134, Republic of KoreaCenter for Biomimetic Research, Division of Advanced Predictive Research, Korea Institute of Toxicology, Daejeon 34114, Republic of KoreaDepartment of Medical Science, Asan Medical Institute of Convergence Science and Technology, Asan Medical Center, University of Ulsan College of Medicine, Seoul 05505, Republic of KoreaCenter for Biomimetic Research, Division of Advanced Predictive Research, Korea Institute of Toxicology, Daejeon 34114, Republic of KoreaCenter for Biomimetic Research, Division of Advanced Predictive Research, Korea Institute of Toxicology, Daejeon 34114, Republic of KoreaDepartment of Medical Science, Asan Medical Institute of Convergence Science and Technology, Asan Medical Center, University of Ulsan College of Medicine, Seoul 05505, Republic of KoreaCollege of Pharmacy, Chungnam National University, Daejeon 34134, Republic of Korea<b>Background/Objectives</b>: Perillyl alcohol (POH), a monoterpene natural product derived from the essential oils of plants such as perilla (<i>Perilla frutescens</i>), is currently in phase I and II clinical trials as a chemotherapeutic agent. In this study, we investigated the effect of POH on cytochrome P450 (CYP) activity for evaluating POH–drug interaction potential. <b>Methods</b>: The investigation was conducted using pooled human liver microsomes (HLMs), recombinant CYP3A4 (rCYP3A4) enzymes, and human pluripotent stem cell-derived hepatic organoids (hHOs) employing liquid chromatography-tandem mass spectrometry. <b>Results</b>: POH inhibited the activities of CYP2A6 and CYP2B6 with K<sub>i</sub> of 6.35 and 3.78 μM, respectively, whereas it stimulated CYP3A4 activity in pooled HLMs incubated with midazolam (MDZ). In a direct CYP inhibition assay using HLMs, activities of CYP2C9, CYP2C19, and CYP2E1 were also inhibited by POH, with IC<sub>50</sub> values greater than 50 μM, but those of CYP1A2, CYP2C8, CYP2D6, and CYP3A4 (testosterone) were not significantly inhibited. In pooled HLMs, the V<sub>max</sub>/K<sub>m</sub> value of 1′-hydroxy MDZ, but not that of 4-hydroxy MDZ, was increased 2.7-fold by 100 μM POH compared with that in the absence of POH. Moreover, stimulation of MDZ 1′-hydroxylation by CYP3A4 was observed in hHOs and rCYP3A4 with cytochrome <i>b</i><sub>5</sub> but not rCYP3A4 without cytochrome <i>b</i><sub>5</sub>. Furthermore, activation of CYP3A4-mediated metabolism by POH was observed in HLMs incubated with fimasartan but not atorvastatin, buspirone, donepezil, nifedipine, or tadalafil, suggesting a substrate-dependent activation of CYP3A4 by POH. <b>Conclusions</b>: POH inhibits CYP2A6 and CYP2B6, but it activates CYP3A4. These findings underscore the need for further evaluation of the interactions of clinical drugs with POH.https://www.mdpi.com/1999-4923/16/12/1581heterotropic activationCYP3A4perillyl alcoholhuman hepatic organoidsdrug interaction
spellingShingle Ji Hyeon Ryu
Jieun Yu
Jang Su Jeon
Seongyea Jo
Soo Min Lee
Hyemin Kim
Han-Jin Park
Soo Jin Oh
Sang Kyum Kim
Heterotropic Activation of Cytochrome P450 3A4 by Perillyl Alcohol
Pharmaceutics
heterotropic activation
CYP3A4
perillyl alcohol
human hepatic organoids
drug interaction
title Heterotropic Activation of Cytochrome P450 3A4 by Perillyl Alcohol
title_full Heterotropic Activation of Cytochrome P450 3A4 by Perillyl Alcohol
title_fullStr Heterotropic Activation of Cytochrome P450 3A4 by Perillyl Alcohol
title_full_unstemmed Heterotropic Activation of Cytochrome P450 3A4 by Perillyl Alcohol
title_short Heterotropic Activation of Cytochrome P450 3A4 by Perillyl Alcohol
title_sort heterotropic activation of cytochrome p450 3a4 by perillyl alcohol
topic heterotropic activation
CYP3A4
perillyl alcohol
human hepatic organoids
drug interaction
url https://www.mdpi.com/1999-4923/16/12/1581
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