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Downloaded from Ligno Biotech Sdn TOXICOLOGICAL AND BIOPHARMACOLOGICAL INVESTIGATIONS OF TIGER MILK MUSHROOM−Lignosus tigris KONG BOON HONG Malaya of FACULTY OF MEDICINE UniversityUNIVERSITY OF MALAYA KUALA LUMPUR 2018 TOXICOLOGICAL AND BIOPHARMACOLOGICAL INVESTIGATIONS OF TIGER MILK MUSHROOM−Lignosus tigris KONG BOON HONG Malaya of THESIS SUBMITTED IN FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UniversityFACULTY OF MEDICINE UNIVERSITY OF MALAYA KUALA LUMPUR 2018 UNIVERSITY OF MALAYA ORIGINAL LITERARY WORK DECLARATION Name of Candidate: KONG BOON HONG Matric No: MHA140006 Name of Degree: DOCTOR OF PHILOSOPHY Title of Project Paper/Research Report/Dissertation/Thesis (“this Work”): TOXICOLOGICAL AND BIOPHARMACOLOGICAL INVESTIGATIONS OF TIGER MILK MUSHROOM-Lignosus tigris Field of Study: MOLECULAR MEDICINE I do solemnly and sincerely declare that: (1) I am the sole author/writer of this Work; (2) This Work is original; (3) Any use of any work in which copyright exists was done by way of fair dealing and for permitted purposes and any excerpt or extract from, or reference to or reproduction of any copyright work has been disclosed expressly and sufficiently and the title of the Work and its authorship have been acknowledged in this Work; (4) I do not have any actual knowledge nor do IMalaya ought reasonably to know that the making of this work constitutes an infringement of any copyright work; (5) I hereby assign all and every rights in the copyright to this Work to the University of Malaya (“UM”), who henceforth ofshall be owner of the copyright in this Work and that any reproduction or use in any form or by any means whatsoever is prohibited without the written consent of UM having been first had and obtained; (6) I am fully aware that if in the course of making this Work I have infringed any copyright whether intentionally or otherwise, I may be subject to legal action or any other action as may be determined by UM. Candidate’s Signature Date: 11 June 2018 SubscribedUniversity and solemnly declared before, Witness’s Signature Date: 11 June 2018 Name: Designation: ii TOXICOLOGICAL AND BIOPHARMACOLOGICAL INVESTIGATIONS OF TIGER MILK MUSHROOM-Lignosus tigris ABSTRACT The traditional use for the sclerotium of Tiger Milk mushroom (Lignosus spp.) by local Malaysian natives as a cure for a variety of illnesses has been well documented and scientifically validated. Lignosus tigris C.S. Tan, a species of the Tiger Milk mushroom, has been identified recently and successfully cultivated. In the present study, the potential toxicity of the cultivated L. tigris E sclerotia was evaluated using Sprague Dawley (SD) rats in 14-day acute and 28-day sub-acute toxicity studies. Acute toxicity study showed that the sclerotial powder at a single dose of 2000 mg/kgMalaya did not cause adverse effects on growth rate, neither hematological and biochemical parameters, nor pathological changes in vital organ tissues. In addition, daily administrationof of L. tigris E sclerotial powder at three different doses of 250, 500 and 1000 mg/kg for 28 consecutive days did not cause any treatment-related toxicity in the SD rats, as evidenced by the body weight, general behavior, hematological, clinical biochemical, relative organ weights, and histopathological examination on the vital and reproductive organs. Therefore, the no- observed-adverse-effect level (NOAEL) dose for sub-acute toxicity of the L. tigris E sclerotial powder is more than 1000 mg/kg. The nutritional value, chemical composition, antioxidantUniversity and cytotoxic activities of the L. tigris E sclerotium were also investigated. The L. tigris E sclerotium is rich in carbohydrate and protein with moderate amounts of dietary fibers and contains nine essential amino acids. The cold water extract (CWE) of the sclerotial powder showed potent antioxidant activity and cytotoxic selectivity on human breast adenocarcinoma (MCF7) cells. Further fractionation of the CWE using Sephadex G-50 chromatography followed by ammonium sulfate precipitation showed iii that the cytotoxic activity of the mushroom extract against MCF7 cells is contributed mainly by the high molecular weight proteins (HMW-P). HMW-P showed selective cytotoxicity against MCF7 cells (IC50 value = 1.17 ± 0.47 µg/mL) through induction of apoptosis mediated by both intrinsic and extrinsic pathways as indicated by an increase in caspase-8 and -9 activities as well as a decrease of Bcl-2 and increase of Bax expression levels. The intraperitoneal administration of HMW-P (5 µg/g of body weight) to mice bearing MCF7 solid tumor successfully suppressed the tumor growth. HMW-P induced cell death in the tumor via apoptosis as high number of apoptotic cells (stained with TUNEL) was detected in the tumor tissue of the treated mice. Mice treated with HMW- P, however, showed a significant reduction in body weight but no pathological changes were observed in the vital organs. Separation of proteins of HMW-P on SDS-PAGE followed by LC-MS/MS analysis identified several potentialMalaya cytotoxic proteins including lectins, serine proteases and a deoxyribonuclease-like protein. L. tigris E deoxyribonuclease-like protein (LTED) wasof purified from HMW-P using an affinity chromatography and it exhibited selective cytotoxicity against MCF7 cells (IC50 value = 6.57 ± 0.61 µg/mL) through induction of apoptosis. LTED-induced apoptosis occurs probably via the activation of caspase-dependent and caspase-independent pathways as evidenced by an increase in the activities of caspase 3/7, -8 and -9, a decrease of Bcl-2 protein expression and increases in Bax, AIF and endoG protein expressions. These results showed that there is a great potential to develop L. tigris E sclerotia into functional foodUniversity and as a nutraceutical, as well as a source of novel proteins with therapeutic applications. Keywords: Lignosus tigris E, sclerotium, toxicity assessment, nutritional composition, antioxidant activity, cytotoxicity, antitumor activity iv KAJIAN TOKSIKOLOGI DAN BIOPHARMAKOLOGI CENDAWAN SUSU HARIMAU-Lignosus tigris ABSTRAK Penggunaan tradisional ubi (juga dikenali sebagai sklerotium) cendawan susu harimau (Lignosus spp.) oleh penduduk tempatan di Malaysia sebagai ubat untuk pelbagai jenis penyakit telah didokumentasikan dan terbukti secara saintifik. Lignosus tigris C.S. Tan, spesies cendawan susu harimau yang baru dikenalpasti telah berjaya dikulturkan. Dalam kajian ini, ketoksikan sklerotium cendawan L. tigris yang dikultur telah dikaji dengan menggunakan tikus Sprague Dawley (SD) dalam ujian ketoksikan akut (14-hari) dan sub- akut (28-hari). Kajian ketoksikan akut menunjukkanMalaya bahawa serbuk sklerotium L. tigris E pada dos tunggal 2000 mg/kg tidak menyebabkan sebarang kesan mudarat ke atas kadar pertumbuhan, parameter hematologi atauof biokimia serta tidak membawa apa-apa perubahan patologi tisu-tisu organ penting. Di samping itu, rawatan selama 28 hari berturutan dengan serbuk sklerotium L. tigris E menggunakan tiga dos yang berbeza (250, 500 dan 1000 mg/kg) tidak menyebabkan sebarang ketoksikan pada tikus SD dan ini terbukti melalui data yang terkumpul. Data terkumpul merangkumi perubahan berat badan, tingkah laku umum, parameter hematologi dan biokimia klinikal, perbezaan berat organ relatif, dan pemeriksaan histopatologi pada organ utama dan organ pembiakan. OlehUniversity demikian, dos tiada-kesan-mudarat (no-observed-adverse-effect level (NOAEL)) untuk ketoksikan sub-akut serbuk sklerotium L. tigris E adalah melebihi 1000 mg/kg. Nilai pemakanan, komposisi kimia, antioksidan dan aktiviti sitotoksik sklerotium L. tigris E juga telah diselidik. Sklerotium L. tigris E kaya dengan karbohidrat dan protein serta mempunyai serat makanan dalam jumlah yang sederhana di samping mengandungi sembilan asid amino perlu. Ekstrak air sejuk (CWE) daripada serbuk sklerotium L. tigris v E menunjukkan aktiviti antioksidan yang kuat dan aktiviti sitotoksik terpilih pada sel adenokarsinoma payudara manusia (MCF7). Penulenan lanjut CWE dengan menggunakan kaedah penurasan jisim Sephadex G-50 diikuti dengan pemendakan ammonium sulfat menunjukkan bahawa aktiviti sitotoksik ekstrak cendawan ini terhadap sel MCF7 disumbangkan terutamanya oleh protein yang mempunyai berat molekul tinggi (HMW-P). HMW-P menunjukkan sitotoksisiti terpilih terhadap sel-sel MCF7 (nilai IC50 = 1.17 ± 0.47 μg/mL) melalui induksi apoptosis yang melibatkan kedua-dua laluan intrinsik dan ekstrinsik. Ini terbukti melalui peningkatan aktiviti caspase-8 dan -9 serta pengurangan Bcl- 2 dan peningkatan tahap ekspresi Bax. Rawatan intraperitoneum dengan HMW-P pada dos 5 μg/g telah berjaya menindas pertumbuhan tumor MCF7 dalam tikus. HMW-P menginduksikan kematian sel dalam tumor melalui kaedah apoptosis. Ini ditunjukkan oleh jumlah sel apoptosisMalaya yang tinggi (ditandawarnakan melalui kaedah TUNEL) dalam tisu tumor tikus yang dirawat dengan HMW-P. Walau bagaimanapun, tikus yang dirawat dengan HMWof-P menunjukkan penurunan dalam berat badan tetapi tiada perubahan patologi yang dikesan dalam organ-organ penting. Pengasingan protein HMW-P menggunakan SDS-PAGE diikuti dengan analisis LC- MS/MS telah mengenalpastikan beberapa protein yang berpotensi termasuk lektin, serina protease dan protein yang menyerupai deoksiribonuklease. Protein menyerupai deoksiribonuklease (LTED) daripada L. tigris E telah diasingkan daripada HMW-P dengan menggunakan kaedah kromatografi afiniti. LTED menunjukkan sitotoksisiti terpilihUniversity terhadap sel MCF7 (nilai IC50 = 6.57 ± 0.61 μg/mL) melalui penginduksian apoptosis. Apoptosis yang disebabkan
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