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Salehzadeh, Areaf (2002) Effects of Azadirachtin on Insect and Mammalian Cultured Cells. Phd Thesis

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Salehzadeh, Areaf (2002) Effects of Azadirachtin on Insect and Mammalian Cultured Cells. Phd Thesis Salehzadeh, Areaf (2002) Effects of azadirachtin on insect and mammalian cultured cells. PhD thesis. http://theses.gla.ac.uk/3060/ Copyright and moral rights for this thesis are retained by the author A copy can be downloaded for personal non-commercial research or study, without prior permission or charge This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the Author The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the Author When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given Glasgow Theses Service http://theses.gla.ac.uk/ [email protected] Effects of azadirachtin on insect and mammalian cultured cells By Areaf Salehzadeh (M.Sc. Medical Entomology) (University of Tehran, Tehran, Iran) Thesis submitted for the Degree of Doctor of Philosophy July 2002 UNIVERSITY of GLASGOW Division of Biochemistry and Molecular Biology, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow GI2 8QQ Scotland UK In the name of ALLAH Most gracious Most merciful Thanking Him With a full heart and devoted tongue II era My parents III Acknowledgement I would like to express my sincerest thanks to everyone who assisted me during the course of my work especially: Dr. R. H. C. Strang for his able guidance, unlimited encouragement and constructive criticism. It has been a great privilege to have worked with him. His co­ operation and support is highly appreciated; Prof. R. L. P. Adams for his constructive criticism, and invaluable advice; Prof. G.Milligan for making the facilities of the department available; Prof. J.R. Kusel for his assistance and guidance in fluorescence microscopy; Dr. W. Cushley for his assistance and guidance in cell cytometry; Dr. L. Fixter for his advice and encouragement; Dr. A. Akhakha for his useful criticise, friendship, advice and moral help; Prof. J. G. Lindsay for his encouragement; Mrs Heather for her endless help and technical support; My Iranian colleagues M. Golchin, A. Hosseini and M. J. Namazi for their assistance in SDS-PAGE and Immunoblotting; Finally, I would like to thank my wife for her patience and scientific advice during my research. IV DECLARATION I hereby declare that the thesis which follows is my own composition, that is a record of work done by myself and that has not been presented in any previous application for a Higher Degree. ~2.6106111 Areaf Salehzadeh v Summary: Azadirachtin, a tetranortripenoid from the Neem Tree (Azadirachta indica), has been shown to affect insects in many ways. Antifeedancy, repellency, and profound effects on growth, development and reproduction, are the most important pesticidal properties of this phytochemical. Many experiments with insects have shown that azadirachtin interferes with the functions of the neurosecretory system. In the last ten years, it has been shown that the compound is cytotoxic to cultured insect cells, but there is still uncertainty as to its exact mode of action at the cellular level. The aim of this project was to try to find the mode of action of azadirachtin in cultured cells, and to compare its cytotoxicity with some well-known phytochemical pesticides. The results presented here showed that azadirachtin was toxic to the cultured insect cells used (Sf9 and C6/36, derived respectively from Spodoptera Jrugiperda and Aedes albopictus) even in very low concentrations with an ECso for the Spodoptera cells estimated at 5xlO-9 M, but that the mammalian fibroblast cell line L929 was little affected except at concentrations greater than 10-4 M. The other major neem terpenoids, nimbin and salannin, showed low toxicity towards the cultured cells. The neurotoxic pyrethrum showed little effect against the cultures, except for some slight stimulatory effect on growth at 10-8 M. Rotenone, known to inhibit the electron transport chain, effectively inhibited the growth of both insect and mammalian cells. Nicotine, another neurotoxic phytochemical, had little effect on the growth of the cultured cells. It was concluded that while cell growth assessment is not appropriate for all phytochemical pesticides, it is useful for those, such as azadirachtin and rotenone, whose effect is on the essential mechanisms of insect cells in general. Rotenone was used as a positive control to investigate if azadirachtin had its effect on respiration of the cells. Only at the highest feasible concentration of azadirachtin, was there a slight but significant (15%) reduction of respiration which was the same in both insect and mammalian cells. As expected, rotenone inhibited both insect and mammalian cells even at concentrations as low as 10-11 M. When the effects of azadirachtin on the cell cycle were examined by means of cell cytometry, it was shown that the compound arrested the cell-cycle in G21M phase, and that the effect was related to the concentration. Microscopy confirmed that there was a three-fold increase in the mitotic index after 2 hours of exposure to 2xlO-6 M azadirachtin. The similarity of the of the nuclear profiles and cell-cycle distribution to Sf9 cells treated with colchicine, a well-known antimitotic phytochemical, suggested there was a similarity of action between the two compounds. This was confirmed by the fact that both were apparently able to antagonise the effects of taxol, and by displacement experiments with a fluorescent derivative of colchicine. Azadirachtin was shown to inhibit in vitro the polymerisation of purified pig-brain tubulin, suggesting that this was how it prevented cell division. Although azadirachtin only affected L929 cells at 10-4 M, at this concentration the cell cytometry showed an increase in the proportion of cells in S-phase, which could be due to an effect on DNA synthesis. An adverse effect on structure or functions of DNA might also account for the rapid decrease in mitotic index in Sf9 cells after 2 hours in 10-6 M azadirachtin. The cumulative results from this and previous work suggest that azadirachtin in low (nanomolar) concentrations has its effect on insect cells by interfering with the polymerisation VI of tubulin, which in tum prevents many cellular functions, including cell division. There may, however, be other sites of action found in mammalian as well as insect cells. VII CONTENTS Page No Dedication III Acknow ledgement IV Declaration V Summary VI Contents VIII List of illustrations XVII List of tables XXII List of abbreviations XXIII Chapter 1 Introduction 1.1 The phylum Arthropoda and its impact on man 1 1.1.1. Arthropod pests of plants 1 1.1.2. Arthropod Pests of animals and humans 2 1.2. Chemical control of pests 7 1.3. Insect nervous system 8 1.4. Synthetc pesticides 10 1.4.1. Organochlorines 10 1.4.1.1. Dichlorodiphenylene derivatives 10 1.4.1.2. Lindane 12 1.4.1.3. Cyclodienes 13 1.4.1.4. Polychloroterpenes 15 1.4.2. Organophosphorus esters 16 1.4.2.1. Classification of Ops 18 1.4.2.2. Aliphatics 18 1.4.2.3. Phenyl derivatives 19 1.4.2.4. Heterocyclic derivatives 19 1.4.3. Organosulfurs 20 1.4.4. Carbamates 21 VIII 1.4.5. Formamidines 22 1.4.6. Dinitrophenols 23 1.4.7. Organotins 24 1.4.8. Pyrethroids 25 1.4.9. Nicotinoids 26 1.4.10. Spinosyns 27 1.4.11. Phenylpyrazoles 28 1.4.12. Pyrroles 29 1.4.13. Pyrazoles 30 1.4.14. Quinazolines 31 1.4.15. Synergists or activators 32 1.5. Insect growth regulator (lGRs) 33 1.5.1. Juvenile hormone agonists 35 1.5.2. Anti-juvenile hormones 36 1.5.3. Ecdysteroid agonists 36 1.6. Insecticides that inhibit cuticle production 37 17. Insecticides affecting water balance 37 1.8. Fumigants 38 1.9. Insect repellents 39 1.10. Inorganics 40 1.11. Problem with synthetic neurotoxic pesticides 41 1.11.1. Resistance to pesticides 41 1.11.2. The problem of selectivity 42 1.11.3. Pesticides and the environment 43 1.11.4. Pesticides in soils 43 1.11.5. The effect of pesticides on non target animals 44 1.11.6. Genotoxic effect of pesticides 45 1.11.6.1. Carbamates 45 1.11.6.2. Organophosphates 46 1.11.6.3. Pyrethroides 47 IX 1.12. Bacterial Pesticides 47 1.12.1. Bacillus thuringiensis 48 1.13. Botanical pesticides 49 1.13.1. Pyrethrins 50 1.13.2. Nicotine 52 1.13.3. Rotenone 54 1.13.4. Neem 55 1.13.5. Botanical properties of neem 56 1.13.6. Insecticidal properties of neem 60 1.13.7. Medical uses of neem 60 1.13.8. Antimicrobial effects of neem extracts 61 1.13.9. Commercial formulations of neem 62 1.13.10. Active ingredients of neem 63 1.13.11. Azadirachtin as the main biologically active component 65 1.13.11.1. The stability of azadirachtin 66 1.13 .11.2.Effect of azadirachtin on pestiferous insects 66 1.13.11.3.Antifeedancy 67 1.13.11.4.Effect of neem azadirachtin on human and other 71 mammals 1.13.11.5.Mode of action of azadirachtin 72 Aim of the project 73 Chapter 2 A comparison of the effects of botanical pesticides on growth of cultured cells 2.1. Introduction 75 2.1.1. History of animal cell culture 75 2.1.2. Drug development and using cultured cells in toxicological 75 assays 2.1.3. Effect of pesticides on proliferation of cultured cells 77 2.1.4. Effect of azadirachtin on cell growth 79 2.1.5. Effect of azadirachtin on total protein 80 2.1.6.
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