Insecticides Pest Engineering Part 10 pdf

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12

Metabolism of Pyrethroids by Mosquito

Cytochrome P450 Enzymes: Impact on Vector Control

Pornpimol Rongnoparut1, Sirikun Pethuan1, Songklod Sarapusit2 and Panida Lertkiatmongkol1

1Department of Biochemistry, Faculty of Science, Mahidol University,

2Department of Biochemistry, Faculty of Science, Burapha University,

Thailand

1 Introduction

Cytochrome P450 enzymes (P450s) are heme-containing monooxygenases that catalyze metabolisms of various endogenous and exogenous compounds These P450s constitute a superfamily of enzymes present in various organisms including mammals, plants, bacteria, and insects P450 enzymes are diverse and metabolize a wide variety of substrates, but their structures are largely conserved A universal nomenclature has been assigned to P450 superfamily based on their amino acid sequence homology (Nelson et al., 1996) In eukaryotes, P450 is membrane-bound and in general functions to insert one molecule of oxygen into its substrate, with its heme prosthetic group playing a role in substrate oxidation This catalytic reaction requires a pair of electrons shuttled from NADPH via the NADPH-cytochrome P450 reductase (CYPOR) enzyme, a P450 redox partner, to target P450s (Ortiz de Montellano, 2005) In contrast in bacteria and mitochondria, ferredoxin reductase and iron-sulfur ferredoxin proteins act as a bridge to transfer reducing equivalent from NAD(P)H to target P450s In insects, P450s are membrane-bound enzymes that play key roles in endogenous metabolisms (i.e metabolisms of steroid molting and juvenile hormones, and pheromones) and xenobiotic metabolisms, as well as detoxification of insecticides (Feyereisen, 1999) It becomes evident that P450s are implicated in pyrethroid resistance in insects

Insecticides form a mainstay for vector control programs of vector-borne diseases However intensive uses of insecticides have led to development of insecticide resistance in many insects thus compromising success of insect vector control In particular pyrethroid resistance has been found widespread in many insects such as house flies, cockroaches, and mosquitoes (Acevedo et al., 2009; Awolola et al., 2002; Cochran, 1989; Hargreaves et al., 2000; Jirakanjanakit et al., 2007) Two major mechanisms have been recorded responsible for insecticide resistance, which are alteration of target sites and metabolic resistance (Hemingway et al., 2004) Metabolic resistance is conferred by increased activities of detoxification enzymes such as P450s, non-specific esterases (Hemingway et al., 2004; Price, 1991) Initial approaches to detect involvement of detoxification mechanisms in metabolic resistance are to compare activities of detoxification enzymes between resistant and

susceptible insect strains, and by identification of corresponding genes that display higher expression level in resistant insects (Bautista et al., 2007; Chareonviriyaphap et al., 2003; Tomita et al., 1995; Yaicharoen et al., 2005) Examinations in various insects such as house fly, cotton ballworm, and mosquito have implicated involvement of up-regulation of different P450 genes in pyrethroid resistance (Liu & Scott, 1998; Müller et al., 2007; Ranasinghe & Hobbs, 1998; Rodpradit et al., 2005; Tomita et al., 1995) Such P450 overexpression has been assumed constituting a defense mechanism against insecticides and responsible for insecticide resistance, presumably by virtue of enhanced insecticide detoxification

Recent advanced methods employing microarray-based approach, when genomic sequence information for insects is available, have identified multiple genes involved in pyrethroid resistance in mosquitoes Genes in CYP6 family, in particular, are reported to have an

implication in insecticide resistance In Anopheles gambiae malaria vector, microarray

analyses reveal that several CYP6 P450 genes could contribute to pyrethroid resistance, these include CYP6M2, CYP6Z2 and CYP6P3 (Djouaka et al., 2008; Müller et al., 2007) These genes were observed up-regulated in pyrethroid resistant mosquitoes (Müller et al., 2008; Stevenson et al., 2011) CYP6M2 and CYP6P3 have shown ability to bind and metabolize pyrethroids, on the other hand CYP6Z2 is able to bind pyrethroids but does not degrade pyrethroids (Mclauglin et al., 2008) Genetic mapping of genes conferring pyrethroid

resistance in An gambiae also supports involvement of CYP6P3 in pyrethroid resistance

(Wondji et al., 2007) Up-regulation of CYP6 genes has also been found in other resistant

insects, for instance CYP6BQ9 in pyrethroid resistant Tribolium castaneum (Zhu et al., 2010), CYP6D1 in Musca domestica that is able to metabolize pyrethroids (Zhang & Scott, 1996), and CYP6BG1 in pyrethroid resistant Plutella xylostella (Bautista et al., 2007) In T castaneum

knockdown of CYP6BQ9 by dsRNA resulted in decreased resistance to deltamethrin (Zhu et

al., 2010) Similar finding has been observed for CYP6BG1 in permethrin resistant P xylostella, supporting the role of overexpression of these CYP6 genes in pyrethroid resistance (Bautista et al., 2009) In An minimus mosquito, CYP6AA3 and CYP6P7 are upregulated and

possess activities toward pyrethroid degradation (Duangkaew et al., 2011b; Rongnoparut et al., 2003)

2 Cytochrome P450 monooxygenase (P450) and NADPH-cytochrome P450

reductase (CYPOR) enzymes isolated from An minimus

In this chapter, we focus on investigation of the P450s that have been shown overexpressed

in a laboratory-selected pyrethroid resistant An minimus mosquito We describe

heterologous expression of the overexpressed P450s in baculovirus-mediated insect cell expression system and characterization of their catalytic roles toward pyrethroid

insecticides Tools utilized in functional investigation of An minimus P450s have been developed and described In parallel the An minimus CYPOR has been cloned and protein expressed via bacterial expression system Amino acid sequence of An minimus CYPOR is

intrigue in that several important residues that might play role in its functioning as P450 redox partner are different from those of previously reported enzymes from mammals and

house fly The An minimus CYPOR is different in enzymatic properties and kinetic mechanisms from other CYPORs In this context we speculate that An minimus CYPOR

could influence electron delivery to target mosquito P450 enzymes, and could act as a limiting step in P450-mediated metabolisms These results together could thus gain an

rate-Metabolism of Pyrethroids by Mosquito Cytochrome P450 Enzymes: Impact on Vector Control 267 insight into pyrethroid metabolisms in this mosquito species and knowledge obtained could contribute to strategies in control of mosquito vectors

An minimus is one of malaria vectors in Southeast Asia, including Thailand, Loas,

Cambodia and Vietnam We previously established a deltamethrin-selected mosquito strain

of An minimus species A, by exposure of subsequent mosquito generations to LD50 and LT50 values of deltamethrin (Chareonviriyaphap et al., 2002) Biochemical assays suggested that

deltamethrin-resistant An minimus predominantly employ P450s to detoxify pyrethroids

(Chareonviriyaphap et al., 2003) We next set out on isolation of P450 genes that have a causal linkage in conferring deltamethrin resistance in this mosquito species Using reverse-transcribed-polymerase chain reaction (RT-PCR) in combination with degenerate PCR primers whose sequences were based on CYP6 conserved amino acids, we have isolated

CYP6AA3, CYP6P7, and CYP6P8 complete cDNAs from deltamethrin-resistant An minimus

(Rongnoparut et al., 2003) The three genes showed elevated transcription level in deltamethrin resistant populations compared to the parent susceptible strain We found that fold of mRNA increase of CYP6AA3 and CYP6P7 is correlated with increase of resistance during deltamethrin selection However, this correlation was not observed for CYP6P8 (Rodpradit et al., 2005) The three mosquito P450s could thus be used as model enzymes for characterization of their metabolic activities toward insecticides and possibly for future development of tools for mosquito vector control This can be accomplished by determining whether they possess catalytic activities toward pyrethroid insecticides, thus assuming a causal linkage of overexpression and increased pyrethroid detoxification leading to

pyrethroid resistance Equally important, elucidating properties of the An minimus CYPOR

and its influential role in P450 system is beneficial for understanding of P450 metabolisms of this mosquito species

2.1 In vitro insecticide metabolisms

We have heterologously expressed CYP6AA3, CYP6P7, and CYP6P8 in Spodoptera frugiperda (Sf9) insect cells via baculovirus-mediated expression system The expression procedure

employed full-length CYP6AA3, CYP6P7, and CYP6P8 cDNAs as templates to produce

recombinant baculoviruses, and subsequently infected Sf9 cells for production of P450

proteins RT-PCR amplification and sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) analysis were performed to verify expression of P450 mRNAs

and proteins in the infected Sf9 cells Expression of CYP6AA3, CYP6P7, and CYP6P8, each is

predominantly detected in membrane fractions of infected cells after 72 hours of infection, with expected molecular size of approximately 59 kDa detected on SDS-PAGE (Kaewpa et al., 2007; Duangkaew et al., 2011b) The expressed proteins display CO-reduced difference spectrum of a characteristic peak at 450 nm (Omura & Sato, 1964) Total P450 content obtained from baculovirus-mediated expression of CYP6AA3, CYP6P7, and CYP6P8 ranges from 200 to 360 pmol/mg membrane protein The expressed CYP6AA3, CYP6P7, and CYP6P8 proteins were used in enzymatic reaction assays testing against pyrethroids and other insecticide groups Knowledge of the metabolic profile of these P450s could give us insight into functioning of these P450s within mosquitoes towards insecticide metabolisms, i.e how mosquitoes detoxify against a spectrum of insecticide classes through P450-mediated metabolisms

In enzymatic assay, each P450 in the reaction was performed in the presence of

NADPH-regenerating system and was reconstituted with An.minimus CYPOR (Kaewpa et al., 2007),

as CYPOR is required to supply electrons to P450 in the reaction cycle Insecticide

metabolism was determined by detection of disappearance of insecticide substrate at

different times compared with that present at time zero as previously described

(Booseupsakul et al., 2008) This time course degradation was detected through HPLC

analysis Table 1 summarizes enzyme activities of CYP6AA3 and CYP6P7 toward

insecticides and metabolites detected Insecticides that were tested by enzyme assays were

type I pyrethroids (permethrin and bioallethrin), type II pyrethroids (deltamethrin,

cypermethrin, and λ-cyhalothrin), organophosphate (chlorpyrifos), and carbamate

(propoxur) Additional insecticides (bifenthrin, dichlorvos, fenitrothion, temephos, and

thiodicarb) belonging to these four insecticide classes were tested by cytotoxicity assays (see

Section 2.3) Chemical structures of these insecticides are shown in Fig 1

Table 1 Presence (+) and absence (-) of P450 activities in insecticide degradation and

metabolites obtained.ND, products not determined

The results shown in Table 1 demonstrate that CYP6AA3 and CYP6P7 share overlapping

metabolic profile against both type I and II pyrethroids, while no detectable activity was

observed toward chlorpyrifos and propoxur (Duangkaew et al., 2011b), nor in the presence

of piperonyl butoxide (a P450 inhibitor) Differences in activities of both enzymes could be

noted, for CPY6AA3 could metabolize λ-cyhalothrin while CYP6P7 did not display activity

against λ-cyhalothrin For CYP6P8 we initially detected absence of pyrethroid degradation

activity, further tests using cytotoxicity assays described in Section 2.3 suggest that CYP6P8

is not capable of degradation of pyrethroids, organophosphates and carbamates

Determination of products obtained from CYP6AA3-mediated pyrethroid degradations

using GC-MS analysis reveal multiple products for type II pyrethroid cypermethrin

degradation and for earlier described deltamethrin metabolism (Boonseupsakul et al., 2008)

These products were 3-phenoxybenzyaldehyde and two unknown products with chloride

and bromide isotope distribution derived from cypermethrin and deltamethrin

metabolisms, respectively In contrast there was only one unknown product that was

predominantly detected from CYP6AA3-mediated permethrin (type I pyrethroid)

degradation, with mass spectrum profile showing characteristic chloride isotope

distribution of permethrin-derived compound Unlike cypermethrin and deltamethrin

metabolisms, we did not obtain 3-phenoxybenzaldehyde from permethrin degradation

(Boonseupsakul, 2008)

Metabolism of Pyrethroids by Mosquito Cytochrome P450 Enzymes: Impact on Vector Control 269

Fig 1 Chemical structures of insecticides used in the study

Type I and type II pyrethroids are different by the presence of cyano group (see Fig 1) Thus our results implicate that presence of cyano group may play role in CYP6AA3-mediated pyrethroid degradations resulting in detection of 3-phenoxybenzaldehyde, possibly through

oxidative cleavage reaction In An gambiae CYP6M2-mediated deltamethrin metabolism and

house fly CYP6D1-mediated cypermethrin metabolism, 4’-hydroxylation of deltamethrin and cypermethrin is the major route of their metabolisms since 4’-hydroxylation products were predominantly detected (Stevenson et al., 2011; Zhang & Scott, 1996) The 4’-

hydroxylation and 3-phenoxybenzaldehyde products have been observed in in vitro

pyrethroid metabolisms mediated by mammalian microsomal enzymes (Shono et al., 1979) The absence of detection of 3-phenoxybenzaldehyde in CYP6AA3-mediated permethrin degradation could be predicted that the reaction underwent monooxygenation of permethrin

2.2 Characterization of CYP6AA3 and CYP6P7 enzymes

As described, both CYP6AA3 and CYP6P7 enzymes have enzymatic activities against

pyrethroid insecticides and their metabolic profiles are different Kinetics and inhibition

studies further support their abilities to metabolize pyrethroids, however with different enzyme and kinetic properties that influence substrate and inhibitor selectivity Such

knowledge could have an implication in pyrethroid detoxification in An minimus mosquito,

for example how the two P450s redundantly metabolize overlapping sets of pyrethroids Alongside investigation of pyrethroid metabolisms, we examined their activities toward fluorescent compounds for development of rapid enzymatic assays Finally we performed cell-based MTT (3-[4,5-dimethylthiazol-2-yl]-2,5-diphenyltetrazolium bromide) cytotoxicity assays for further determination of substrates and inhibitors of both P450 enzymes as

reported herein

2.2.1 Determination of enzyme kinetics of CYP6AA3 and CYP6P7 enzymes

We recently reported kenetic paremeters for CYP6AA3 and CYP6P7 enzymes (Duangkaew

et al., 2011b) Kinetic results reveal that CYP6AA3 has preference in binding to and has

higher rate in degradation of permethrin type I pyrethroid than type II pyrethroids (Kmvalues toward permethrin, cypermethrin, deltamethrin, and λ-cyhalothrin of 41.0 ± 8.5,

70.0 ± 7.1, 80.2 ± 2.0, and 78.3 ± 7.0 µM, respectively and Vmax values of 124.2 ± 1.2, 40.0 ± 7.1, 60.2 ± 3.6, and 60.7 ± 1.1 pmol/min/pmol P450, respectively) In contradictory CYP6P7 does

not have preference for type of pyrethroids (Km values toward permethrin, cypermethrin,

and deltamethrin of 69.7 ± 10.5 , 97.3 ± 6.4, and 73.3 ± 2.9, respectively and Vmax values of 65.7 ± 1.6, 83.3 ± 7.6, and 55.3 ± 5.7 pmol/min/pmol P450, respectively) and does not metabolize λ-cyhalothrin Thus although both enzymes are comparable in terms of

capability to metabolize pyrethroids in vitro, their kinetic values are different Enzyme

structure could account for their differences in kinetic properties and substrate preference Since there has been no known crystal structure available for insect P450s, we initially constructed homology models for CYP6AA3, CYP6P7, and CYP6P8 in an attempt to increase our understanding of molecular mechanisms underlying their binding sites toward insecticide substrates and inhibitors The three enzyme models are different in geometry of their active-site cavities and substrate access channels Upon docking with various insecticide groups, results of its active site could predict and explain metabolic behavior toward pyrethroid, organophosphate, and carbamate insecticides (Lertkiatmongkol et al., 2011) These results suggest that differences in metabolic activities among P450 enzymes in

Metabolism of Pyrethroids by Mosquito Cytochrome P450 Enzymes: Impact on Vector Control 271

insects could be attributed to structural differences resulting in selectivity and different

enzymatic activities against insecticides

In human, CYP2C8, CYP2C9, CYP2C19, and CYP3A4 have been reported abilities to

metabolize both type I and II pyrethroids (Godin et al., 2007; Scollon et al., 2009) The

preference for type I pyrethroid in CYP6AA3 is similar to human CYP2C9 and CYP2C19,

while similar metabolic activity toward both types of pyrethroids found for CYP6P7 is

similar to that of human CYP2C8 enzyme (Scollon et al., 2009) Nevertheless efficiency of

CYP6AA3 and CYP6P7 in deltamethrin degradation is 5- to 10-fold less effective than

human CYP2C8 and CYP2C19 It is noteworthy that more than one P450s residing within

an organism can metabolize pyrethroids as described for human and mosquito, multiple rat

P450s are also found capable of pyrethroid metabolisms (Scollon et al., 2009) When

comparing to An gambiae CYP6P3, both CYP6AA3 and CYP6P7 possess at least 10 fold

higher Km than CYP6P3, but Vmax values of both An minimus CYP6AA3 and CYP6P7 are at

least 20 fold higher (Müller et al., 2008) Higher values of Km and Vmax of CYP6AA3 and

CYP6P7 than those values of An gambiae CYP6M2 (Stevenson et al., 2011) are also observed

2.2.2 CYP6AA3 and CYP6P7 are inhibited differently by different compounds

To obtain a potential fluorogenic substrate probe for fluorescent-based assays of CYP6AA3

and CYP6P7, we previously screened four resorufin fluorogenic substrates containing

different alkyl groups (Duangkaew et al., 2011b) and results in Table 2 suggest that among

test compounds, benzyloxyresorufin could be used as a fluorescent substrate probe since

both CYP6P7 and CYP6AA3 could bind and metabolize benzyloxyresorufin with lowest Km

(values of 1.92 for CYP6AA3 and 0.49 for CYP6P7) and with highest specific activities

(Duangkaew et al., 2011b) The assays of benzyloxyresorufin-O-debenzylation activity were

further used for inhibition studies of both mosquito enzymes

Specific activity (pmole resorufin/min/pmole P450)

Benzyloxyresorufin 6.81 ± 0.65 4.99 ± 0.74

Ethyloxyresorufin 2.88 ± 0.21 3.61 ± 0.17

Table 2 Specific activities of CYP6AA3 and CYP6P7 toward resorufin derivatives

Using fluorescence-based assays, we could initially determine what compound types that

give mechanism-based inhibition pattern by pre-incubation of enzyme with various

concentrations of test inhibitors in the presence or absence of NADPH for 30 min before

addition of substrates and IC50 values have been determined as described (Duangkaew et

al., 2011b) As known, mechanism-based inactivation inhibits enzyme irreversibly,

rendering this mechanism of inhibition more efficient than reversible inhibition

Nevertheless information on mode of inhibition for inhibitors is potential for understanding

of catalytic nature of enzymes We thus determined mode of inhibition for all compounds

tested As shown in Table 2, the compounds we have tested are phenolic compounds and

their chemical structures are shown in Fig 2

It is apparent that none of test flavonoids and furanocoumarins shows mechanism-based

inhibition pattern, but piperonyl butoxide (PBO) and piperine that are methylenedioxyphenyl

compounds show NADPH-dependent mechanism-based inhibition activities against both

enzymes Piperine has been commonly found in Piper sp plant extracts, it possesses acute

toxicity to mammals (Daware et al., 2000) Inhibition results shown in Table 3 also elucidate that -naphthoflavone displayed strongest inhibitory effect Its inhibition pattern suggests that -naphthoflavone uncompetitively inhibit both enzymes by binding to CYP6AA3– and CYP6P7-benzyloxyresorufin complex Moreover, a difference was noted for xanthotoxin as

it uncompetitively inhibits CYP6AA3 but mixed-type inhibited CYP6P7 Thus inhibition results together with different metabolic profiles thus confirm that CYP6AA3 and CYP6P7

have different enzyme properties We thus also tested crude extracts of two plants (Citrus reticulate and Stemona spp.) that were reported containing phenolic compounds (Kaltenegger

et al., 2003; Jayaprakasha et al., 1997) and are found in Thailand Initial results suggest that compounds within both plants may not possess mechanism-based activities against CYP6AA3 and CYP6P7, and both extracts did not inhibit both enzymes as efficient as flavonoids and methylenedioxyphenyl compounds

Fig 2 Chemical structures of different compound types used for inhibition assays of

mosquito P450s

Metabolism of Pyrethroids by Mosquito Cytochrome P450 Enzymes: Impact on Vector Control 273

Table 3 Mode of inhibition and inhibition constants of CYP6P7- or CYP6AA3-

benzyloxyresorufin-O-debenzylation activities of flavonoids, furanocoumarins, and MDP

compounds (Duangkaew et al., 2011b) Crude plant extracts reported herein are ethanolic extracts Values marked with ’a’ are significantly different between reactions with (w/) and without (w/o) NADPH ND, not determined