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Fulltext Pyrethroid resistance in the dengue vector Aedes aegypti in Southeast Asia: present situation and prospects for management

Amelia-Yap ZH, Chen CD, Sofian-Azirun M, Low VL

Parasit Vectors, 2018 Jun 04;11(1):332.
PMID: 29866193 DOI: 10.1186/s13071-018-2899-0

Human arboviral diseases transmitted by Aedes aegypti such as dengue, Zika, chikungunya and yellow fever remain global public health threats to date. Of these diseases, dengue fever is particularly prevalent in Southeast Asia. Relentless vector control efforts are performed to curtail disease transmissions through which pyrethroid insecticides are broadly used as the first line of defense to control Ae. aegypti, especially in the course of disease outbreaks. Here, we compile the largest contemporary database for susceptibility profiles and underlying mechanisms involved in Ae. aegypti resistant to pyrethroids in Southeast Asia. The extensive use of pyrethroids inevitably elicit different levels of resistance to numerous populations despite the presence of geographical isolation. The most common mechanisms of pyrethroid resistance that have been identified in Ae. aegypti includes mutations in the voltage sensitive sodium channel gene (Vssc gene) and metabolic-mediated insecticide resistance. Aedes aegypti develops resistance to pyrethroids by acquisition of one or several amino acid substitution(s) in this Vssc gene. Enzymes involved in metabolic-mediated detoxification (i.e. monooxygenases, glutathione-S-transferases and esterases) have been reported to be related to pyrethroid resistance but many specific contributory enzymes are not completely studied. An inadequate amount of data from some countries indicates an urgent need for further study to fill the knowledge gaps. Perspectives and future research needs are also discussed.
Anti-cancer Effects of Epigenetics Drugs Scriptaid and Zebularine in Human Breast Adenocarcinoma Cells

Yap ZH, Kong WY, Azeez AR, Fang CM, Ngai SC

Anticancer Agents Med Chem, 2021 Jun 07.
PMID: 34102995 DOI: 10.2174/1871520621666210608103251

BACKGROUND: High relapse and metastasis progression in breast cancer patients have prompted the need to explore alternative treatments. Epigenetic therapy has emerged as an attractive therapeutic strategy due to the reversibility of epigenome structures.
OBJECTIVE: This study investigated the anti-cancer effects of epigenetic drugs scriptaid and zebularine in human breast adenocarcinoma MDA-MB-231 and MCF-7 cells.
METHODS: First, the half maximal inhibitory concentration (IC50) of scriptaid, zebularine and the combination of both drugs on human breast adenocarcinoma MDA-MB-231 cells was determined. Next, MDA-MB-231 and MCF-7 cells were treated with scriptaid, zebularine and the combination of both. After treatments, the anti-cancer effects were evaluated via cell migration assay, cell cycle analysis and apoptotic studies, which included histochemical staining and reverse-transcriptase polymerase chain reaction (RT-PCR) of the apoptotic genes.
RESULTS: Both epigenetic drugs inhibited cell viability in a dose-dependent manner with 2 nM scriptaid, 8 µM zebularine and combination of 2 nM scriptaid and 2 µM zebularine. Both MDA-MB-231 and MCF-7 cells exhibited a reduction in cell migration after the treatments. In particular, MDA-MB-231 cells exhibited a significant reduction in cell migration (p < 0.05) after the treatments of zebularine and the combination of scriptaid and zebularine. Besides, cell cycle analysis demonstrated that scriptaid and the combination of both drugs could induce cell cycle arrest at the G0/G1 phase in both MDA-MB-231 and MCF-7 cells. Furthermore, histochemical staining allowed the observation of apoptotic features, such as nuclear chromatin condensation, cell shrinkage, membrane blebbing, nuclear chromatin fragmentation and cytoplasmic extension, in both MDA-MB-231 and MCF-7 cells after the treatments. Further apoptotic studies revealed that the upregulation of pro-apoptotic Bax, downregulation of anti-apoptotic Bcl-2 and elevation of Bax/Bcl-2 ratio were found in MDA-MB-231 cells treated with zebularine and MCF-7 cells treated with all drug regimens.
CONCLUSION: Collectively, these findings suggest that scriptaid and zebularine are potential anti-cancer drugs, either single or in combination, for the therapy of breast cancer. Further investigations of the gene regulatory pathways directed by scriptaid and zebularine are definitely warranted in the future.
Fulltext First report of Rdl mutant alleles in Culex quinquefasciatus (Diptera: Culicidae) in Malaysia

Amelia-Yap ZH, Tan TK, Prakash BK, Chen CD, Sofian-Azirun M, Low VL

J Vector Borne Dis, 2020 10 1;57(4):359-361.
PMID: 34856717 DOI: 10.4103/0972-9062.313959
Fulltext Protein Profiling of Aedes aegypti Treated with Streptomyces sp. KSF103 Ethyl Acetate Extract Reveals Potential Insecticidal Targets and Metabolic Pathways

Tan KS, Azman AS, Hassandarvish P, Amelia-Yap ZH, Tan TK, Low VL

Int J Mol Sci, 2023 Aug 03;24(15).
PMID: 37569772 DOI: 10.3390/ijms241512398

The insecticidal activity of Streptomyces sp. KSF103 ethyl acetate (EA) extract against mosquitoes is known; however, the underlying mechanism behind this activity remains elusive. In this study, liquid chromatography with tandem mass spectrometry (LC-MS/MS) was employed to investigate changes in the protein profile of Aedes aegypti larvae and adults treated with lethal concentrations of 50 (LC50) EA extract. By comparing the treated and untreated mosquitoes, this study aimed to identify proteins or pathways that exhibit alterations, potentially serving as targets for future insecticide development. Treatment with a lethal concentration of EA extract upregulated 15 proteins in larvae, while in adults, 16 proteins were upregulated, and two proteins were downregulated. These proteins were associated with metabolism, protein regulation/degradation, energy production, cellular organization and structure, enzyme activity, and catalysis, as well as calcium ion transport and homeostasis. Notably, ATP synthase, fructose-bisphosphate aldolase (FBA), and ATP citrate synthase were significantly expressed in both groups. Gene ontology analysis indicated a focus on energy metabolic processes. Molecular docking revealed a strong interaction between dodemorph, selagine (compounds from the EA extract), and FBA, suggesting FBA as a potential protein target for insecticide development. Further studies such as Western blot and transcriptomic analyses are warranted to validate the findings.
Adulticide Resistance Status of Aedes albopictus (Diptera: Culicidae) in Sabah, Malaysia: A Statewide Assessment

Elia-Amira NMR, Chen CD, Low VL, Lau KW, Haziqah-Rashid A, Amelia-Yap ZH, et al.

J Med Entomol, 2019 10 28;56(6):1715-1725.
PMID: 31290534 DOI: 10.1093/jme/tjz117

Resistance status of Aedes albopictus (Diptera: Culicidae) collected from Sabah, East Malaysia, was evaluated against four major classes of adulticides, namely pyrethroid, carbamate, organochlorine, and organophosphate. Adult bioassays conforming to WHO standard protocols were conducted to assess knockdown and mortality rates of Ae. albopictus. Among tested pyrethroid adulticides, only cyfluthrin, lambda-cyaholthrin, and deltamethrin were able to inflict total knockdown. The other adulticide classes mostly failed to cause any knockdown; the highest knockdown rate was only 18.33% for propoxur. With regards to mortality rate, Ae. albopictus was unanimously susceptible toward all pyrethroids, dieldrin, and malathion, but exhibited resistance toward bendiocarb, propoxur, dichlorodiphenyltrichloroethane, and fenitrothion. Additionally, correlation analysis demonstrated cross-resistance between bendiocarb and propoxur, and malathion and propoxur. In conclusion, this study has disclosed that pyrethroids are still generally effective for Aedes control in Sabah, Malaysia. The susceptibility status of Ae. albopictus against pyrethroids in descending order was cyfluthrin > lambda-cyhalothrin > deltamethrin > etofenprox > permethrin.
V1016G Point Mutation: The Key Mutation in the Voltage-Gated Sodium Channel (Vgsc) Gene of Pyrethroid-Resistant Aedes aegypti (Diptera: Culicidae) in Indonesia

Amelia-Yap ZH, Sofian-Azirun M, Chen CD, Lau KW, Suana IW, Syahputra E, et al.

J Med Entomol, 2019 06 27;56(4):953-958.
PMID: 30942885 DOI: 10.1093/jme/tjz035

Resistance to pyrethroid insecticides is widespread in Indonesian Aedes aegypti (Linnaeus), the primary vector of dengue viruses. This study aims to investigate the mutations in the voltage-gated sodium channel (Vgsc) conferring pyrethroid resistance against Ae. aegypti populations from Indonesia. Molecular genotyping of mutations using polymerase chain reaction assay and direct DNA sequencing were performed at positions 989 and 1,016 in IIS6 region, and 1,534 in IIIS6 region of the voltage-gated sodium channel (Vgsc) in nine populations of Indonesian Ae. aegypti. The V1016G and S989P genotyping identified the RR genotype to be predominant in six out of nine populations of Ae. aegypti, whereas the SS genotype occurred only in minority. Interestingly, co-occurrence of the V1016G and S989P mutations was detected in the aforementioned six populations with high frequency. Genotyping of F1534C showed all nine populations exhibited the SS genotype, with merely two individuals from a population were heterozygous (RS). Significant correlations were demonstrated between the allele frequencies of the V1016G mutation and the survivability rates as well as resistance ratios in pyrethroid adult bioassays. This signifies the V1016G can contribute more to the insensitivity of Vgsc than the F1534C. Homozygous 1016G mosquitoes were likelier to survive pyrethroid exposure. Identification of underlying mechanisms resulting in insecticide resistance is advantageous in developing effective mosquito control programs in Indonesia.
Efficacy of Mosquito Coils: Cross-resistance to Pyrethroids in Aedes aegypti (Diptera: Culicidae) From Indonesia

Amelia-Yap ZH, Chen CD, Sofian-Azirun M, Lau KW, Suana IW, Harmonis, et al.

J Econ Entomol, 2018 12 14;111(6):2854-2860.
PMID: 30265353 DOI: 10.1093/jee/toy296

Aedes aegypti (L.) (Diptera: Culicidae) is the primary vector of several arthropod-borne viral infectious diseases globally. Relentless vector control efforts are performed to curtail disease transmissions, insecticides remain as the first line of defense in Indonesia. With a dearth of publication on the efficacy of mosquito coil in Indonesia, this is the first report related to mosquito coil despite its common use in households. Ae. aegypti mosquitoes were sampled from nine regencies in Indonesia and tested using the glass-chamber method against three commercially available local pyrethroid-based mosquito coils containing d-allethrin, transfluthrin, and metofluthrin. The 50% knockdown time of female Ae. aegypti tested with d-allethrin, transfluthrin, and metofluthrin containing coils ranged from 0.65 to 14.32; 0.8 to 16.4; and 0.78 to 20.57 min, respectively. Mortality rates in accordance with WHO resistance indicators showed that strains from Denpasar, Mataram, Kuningan, Padang, Samarinda, and Sumba Timur were resistant (<80% mortality rate), whereas strains from Manggarai Barat, Dompu, and Pontianak were susceptible (>98% mortality rate) to the active ingredients assayed. Moreover, the knockdown rates between d-allethrin and transfluthrin, d-allethrin and metofluthrin, as well as transfluthrin and metofluthrin displayed significant associations, portraying the presence of cross-resistance within pyrethroid insecticides. The minimal insecticidal effect of mosquito coils against some Indonesian Ae. aegypti also pointed out the development of pyrethroid resistance, prompting a revamping of the vector control system.
Assessment of the susceptibility status of Aedes albopictus (Diptera: Culicidae) from Interior, Sandakan and Tawau divisions of Sabah, Malaysia based on WHO diagnostic doses of larvicides

Elia-Amira NMR, Chen CD, Low VL, Lau KW, Haziqah-Rashid A, Amelia-Yap ZH, et al.

Trop Biomed, 2021 Jun 01;38(2):196-204.
PMID: 34172711 DOI: 10.47665/tb.38.2.058

Susceptibility status of Aedes albopictus (Skuse) sampled from residential areas in Interior, Sandakan and Tawau divisions of Sabah, Malaysia, was evaluated based on the WHOrecommended doses of organochlorine and organophosphate larvicides. To determine susceptibility status, larval bioassays were carried out and post 24-hour mortalities based on WHO resistance classifications were adopted. The results demonstrated that Ae. albopictus larvae were resistant toward 5 out of the 8 larvicides tested. Larvae from all populations were resistant against bromophos, fenitrothion, malathion, temephos and dichlorodiphenyltrichloroethane (DDT), with mortalities ranging from 0.00 to 89.33%. Dieldrin, on the other hand, could induce 100.00% mortalities in all populations, followed by fenthion and chlorpyrifos, with mortalities ranging from 97.33 to 100.00% and 81.33 to 100.00% respectively. Despite most populations exhibiting similitude in their resistance status, larvae from Sandakan exhibited the highest resistance level whereas the lowest level was observed in Keningau. In view of the inadequacy of some larvicides in controlling Ae. albopictus in this study, integrated management such as insecticide rotation or combination of interventions is warranted.
Statewide Efficacy Assessment of Insect Growth Regulators Against Aedes albopictus (Diptera: Culicidae) in Sabah, Malaysia: An Alternative Control Strategy?

Elia-Amira NMR, Chen CD, Low VL, Lau KW, Haziqah-Rashid A, Amelia-Yap ZH, et al.

J Med Entomol, 2022 01 12;59(1):301-307.
PMID: 34459477 DOI: 10.1093/jme/tjab146

The efficacy of three groups of insect growth regulators, namely juvenile hormone mimics (methoprene and pyriproxyfen), chitin synthesis inhibitors (diflubenzuron and novaluron), and molting disruptor (cyromazine) was evaluated for the first time, against Aedes albopictus Skuse (Diptera: Culicidae) larvae from 14 districts in Sabah, Malaysia. The results showed that all field populations of Ae. albopictus were susceptible towards methoprene, pyriproxyfen, diflubenzuron, novaluron, and cyromazine, with resistance ratio values ranging from 0.50-0.90, 0.60-1.00, 0.67-1.17, 0.71-1.29, and 0.74-1.07, respectively. Overall, the efficacy assessment of insect growth regulators in this study showed promising outcomes and they could be further explored as an alternative to conventional insecticides.
Insecticidal activities of Streptomyces sp. KSF103 ethyl acetate extract against medically important mosquitoes and non-target organisms

Amelia-Yap ZH, Low VL, Saeung A, Ng FL, Chen CD, Hassandarvish P, et al.

Sci Rep, 2023 Jan 02;13(1):4.
PMID: 36593229 DOI: 10.1038/s41598-022-25387-9

A potentially novel actinobacterium isolated from forest soil, Streptomyces sp. KSF103 was evaluated for its insecticidal effect against several mosquito species namely Aedes aegypti, Aedes albopictus, Anopheles cracens and Culex quinquefasciatus. Mosquito larvae and adults were exposed to various concentrations of the ethyl acetate (EA) extract for 24 h. Considerable mortality was evident after the EA extract treatment for all four important vector mosquitoes. Larvicidal activity of the EA extract resulted in LC50 at 0.045 mg/mL and LC90 at 0.080 mg/mL for Ae. aegypti; LC50 at 0.060 mg/mL and LC90 at 0.247 mg/mL for Ae. albopictus; LC50 at 2.141 mg/mL and LC90 at 6.345 mg/mL for An. cracens; and LC50 at 0.272 mg/mL and LC90 at 0.980 mg/mL for Cx. quinquefasciatus. In adulticidal tests, the EA extract was the most toxic to Ae. albopictus adults (LD50 = 2.445 mg/mL; LD90 = 20.004 mg/mL), followed by An. cracens (LD50 = 5.121 mg/mL; LD90 = 147.854 mg/mL) and then Ae. aegypti (LD50 = 28.873 mg/mL; LD90 = 274.823 mg/mL). Additionally, the EA extract exhibited ovicidal activity against Ae. aegypti (LC50 = 0.715 mg/mL; LC90 = 6.956 mg/mL), Ae. albopictus (LC50 = 0.715 mg/mL; LC90 = 6.956 mg/mL), and An. cracens (LC50 = 0.715 mg/mL; LC90 = 6.956 mg/mL), evaluated up to 168 h post-treatment. It displayed no toxicity on the freshwater microalga Chlorella sp. Beijerinck UMACC 313, marine microalga Chlorella sp. Beijerinck UMACC 258 and the ant Odontoponera denticulata. In conclusion, the EA extract showed promising larvicidal, adulticidal and ovicidal activity against Ae. aegypti, Ae. albopictus, An. cracens, and Cx. quinquefasciatus (larvae only). The results suggest that the EA extract of Streptomyces sp. KSF103 has the potential to be used as an environmental-friendly approach in mosquito control. The current study would serve as an initial step toward complementing microbe-based bioinsecticides for synthetic insecticides against medically important mosquitoes.
Pyrethroids Use: Threats on Metabolic-Mediated Resistance Mechanisms in the Primary Dengue Vector Aedes aegypti (Diptera: Culicidae)

Amelia-Yap ZH, Sofian-Azirun M, Chen CD, Suana IW, Lau KW, Elia-Amira NMR, et al.

J Med Entomol, 2019 04 16;56(3):811-816.
PMID: 30715464 DOI: 10.1093/jme/tjz007

The emergence of pyrethroid resistance in Aedes aegypti (L.) has limited the success of vector control. Early detection of resistance could assist authorities in deciding well-suited control strategies to minimize operational failures of Ae. aegypti control. Herein, biochemical analysis was performed to investigate the mechanisms involved in pyrethroid resistance in nine populations of Indonesian Ae. aegypti. Enzymes of adult Ae. aegypti such as esterases (ESTs), glutathione-S-transferases (GSTs), and mixed-function oxidases (MFOs) were characterized. Elevated MFO activity was correlated with resistance phenotype, indicating the role of this enzyme in contributing to pyrethroid resistance. No significant correlations were shown between pyrethroid resistance phenotype and α-ESTs, suggesting that marginally exceeded enzyme levels relative to the reference strain in some pyrethroid-susceptible populations were causative factor for insecticide resistance in other groups of insecticides. However, significant correlation was demonstrated between β-ESTs and pyrethroid resistance phenotype. The lowest enzyme levels in GSTs indicated that this enzyme was not predominant in causing pyrethroid resistance, despite the presence of significant correlations. Because metabolic detoxification fails to comprehensively explain the pyrethroid resistance in some Indonesian Ae. aegypti, additional mechanisms such as altered target sites in voltage-gated sodium channel may also contribute to the high pyrethroid resistance in Ae. aegypti.

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