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Tan Choo Hock Thesis Submitted in Fulfi

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Tan Choo Hock Thesis Submitted in Fulfi TOXINOLOGICAL CHARACTERIZATIONS OF THE VENOM OF HUMP-NOSED PIT VIPER (HYPNALE HYPNALE) TAN CHOO HOCK THESIS SUBMITTED IN FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY FACULTY OF MEDICINE UNIVERSITY OF MALAYA KUALA LUMPUR 2013 Abstract Hump-nosed pit viper (Hypnale hypnale) is a medically important snake in Sri Lanka and Western Ghats of India. Envenomation by this snake still lacks effective antivenom clinically. The species is also often misidentified, resulting in inappropriate treatment. The median lethal dose (LD50) of H. hypnale venom varies from 0.9 µg/g intravenously to 13.7 µg/g intramuscularly in mice. The venom shows procoagulant, hemorrhagic, necrotic, and various enzymatic activities including those of proteases, phospholipases A2 and L-amino acid oxidases which have been partially purified. The monovalent Malayan pit viper antivenom and Hemato polyvalent antivenom (HPA) from Thailand effectively cross-neutralized the venom’s lethality in vitro (median effective dose, ED50 = 0.89 and 1.52 mg venom/mL antivenom, respectively) and in vivo in mice, besides the procoagulant, hemorrhagic and necrotic effects. HPA also prevented acute kidney injury in mice following experimental envenomation. Therefore, HPA may be beneficial in the treatment of H. hypnale envenomation. H. hypnale-specific antiserum and IgG, produced from immunization in rabbits, effectively neutralized the venom’s lethality and various toxicities, indicating the feasibility to produce an effective specific antivenom with a common immunization regime. On indirect ELISA, the IgG cross-reacted extensively with Asiatic crotalid venoms, particularly that of Calloselasma rhodostoma (73.6%), suggesting that the two phylogenically related snakes share similar venoms antigenic properties. Double- sandwich ELISA was specific and able to distinguish and quantify venoms of H. hypnale, Daboia russelii and Echis carinatus sinhaleyus (three common Sri Lankan viperids) in human sera; hence it may be useful in diagnostics and venom level monitoring especially during clinical studies. iv In rabbits, the venom when injected intravenously showed a rapid distribution phase (t1/2α = 0.6 h) and a slow elimination phase (t1/2β = 20 h), consistent with prolonged abnormal hemostasis reported. The intramuscular bioavailability was exceptionally low (Fi.m = 4%), accountable for the highly varied LD50 between intravenous and intramuscular envenomings in animals. HPA infused post-envenomation markedly reduced the serum venom levels and subsequently induced venom redistribution. The redistributed venom was completely neutralized by a second dose of HPA. Proteomic study by shotgun-liquid chromatography-mass spectrometry/mass spectrometry (shotgun-LC-MS/MS) revealed 52 proteins in the venom, 70% of which are toxinologically related. The combined use of reverse-phase high performance liquid chromatography, sodium dodecyl sulfate-polyacrylamide gel electrophoresis, peptide sequencing and mass fingerprinting technologies enabled the identification of the venom major components, i.e. zinc-dependent metalloproteases, phospholipases A2, L- amino acid oxidases, serine proteases and C-type lectins. These toxins correlate with the venom’s principal effects: hematoxicity (hemorrhage, coagulopathy) and tissue destruction (necrosis). Understanding of the venom composition is essential for ascertaining the principal toxins, and for optimizing antivenom formulation. Furthermore, hypnobin, a 37 kDa thrombin-like enzyme was purified. It exhibits arginine esterese and amidase activities, besides distinct specificity towards different mammalian fibrinogens. In fibrinogen coagulation, hypnobin predominantly releases fibrinopeptide A, followed slowly by a small amount of fibrinopeptide B. The findings provide insights into the structures and mechanism of the thrombin-like enzyme, which are important for elucidation of the pathophysiology and for potential drug discovery, e.g. an anticoagulant for thromboembolic disorders. v Abstrak Ular Hypnale hypnale adalah penting dari segi perubatan di Sri Lanka dan Western Ghats, India. Envenomasi (patukan berbisa) ular ini masih tiada penawar bisa yang berkesan. Species ini juga kerap salah dikenalpasti dan ini mengakibatkan rawatan yang tidak sewajar. Dos maut median (LD50) bisa H. hypnale berbeza dari 0.9 µg/g secara intravena ke 13.7 µg/g scara intramuskular pada tikus. Bisa ini menunjukkan kesan-kesan prokoagulan, pendarahan, nekrosis dan aktiviti pelbagai enzim termasuk proteases, phospholipases A2 serta L-amino acid oxidases yang separanya telah diekstrakkan. Monovalent Malayan pit viper antivenom dan Hemato polyvalent antivenom (HPA) dari Thailand meneutralkan kesan maut bisa ini secara in vitro (dos efektif median, ED50 = 0.89 dan 1.52 mg bisa/mL antivenom, masing-masing) dan in vivo pada tikus, serta kesan-kesan prokoagulan, pendaraha dan nekrosis. HPA selepas envenomasi eksperimen turut mencegah kecederaan akut ginjal pada tikus. Maka, HPA mungkin bermanfaat sebagai rawatan bagi envenomasi H. hypnale. Antiserum dan IgG spesifik kepada H. hypnale yang dihasilkan melalui imunisasi arnab meneutralkan kesan-kesan maut dan toksik bisa itu. Ini menunkjukkan kebolehkaksanaan penghasilan suatu penawar bisa spesifik dengan rejim imunisasi yang am. Kajian ‘indirect ELISA’ menunjukkan IgG itu bereaksi-silang secara ekstensif dengan pelbagai bisa ular jenis ‘crotalid’ di Asia, khususnya Calloselasma rhodostoma (73.6%). Ini menunjukkan kedua-dua ular yang berhubungan filogenetik ini berkongsi antigen-antigen bisa yang sama. ‘Double-sandwich ELISA’ adalah spesifik dan dapat membezakan serta mengukur paras bisa-bisa H. hypnale, Daboia russelii dan Echis carinatus sinhaleyus (tiga ular jenis viperid yang biasa di Sri Lanka) dalam serum vi manusia. Ini mununjukkan potensinya digunakkan untuk diagnostik dan pemantauan paras bisa khasnya semasa kajian klinikal. Bisa ini apabila disuntik secara intravena pada arnab menunjukkan fasa ‘distribution’ yang pantas (t1/2α = 0.6 h) dan fasa ‘elimination’ yang lambat (t1/2β = 20 h), konsisten dengan hemostasis abnormal berpanjangan seperti dilaporkan. ‘Intramuscular bioavailability’ bisa ini adalah amat rendah (Fi.m = 4%), dan menjelaskan perbezaan LD50 yang besar antara cara pemberian intravena dan intramuskular pada haiwan. Infusi HPA selepas envenomasi eksperimental mengurangkan paras bisa dengan banyak dan seterusnya mendorong ‘venom redistribution’. Bisa yang diedarsemula itu dineutralkan oleh dos kedua HPA. Kajian proteomic dengan ‘shotgun-liquid chromatography-mass spectrometry/mass spectrometry (shotgun-LC-MS/MS)’ mengenalpasti 52 protein dalam bisa, di mana 70% berkaitan dengan aktiviti toksin . Penggunaan ‘reverse-phased high performance liquid chromatography’, ‘sodium dodecyl sulfate-polyacrylamide gel electrophoresis’, ‘peptide sequencing’ bersama ‘mass fingerprinting’ membolehkan komponen- komponen utama bisa itu dikenalpastikan, iaitu zinc-dependent metalloproteases, phospholipases A2, L-amino acid oxidases, serine proteases dan C-type lectins. Toksin- toksin ini berkorelasi dengan kesan-kesan utama bisa ini: hematoksik (pendarahan, koagulopati) dan kemusnahan tisu (nekrosis). Pemahaman komposisi bisa adalah penting bagi menentupasti toksin-toksin utama, dan untuk mengoptimumkan formulasi penawar bisa. Tambahan, hypnobin, suatu enzim jenis trombin berjisim 37 kDa telah diekstrakkan. Hypnobin menunjukkan aktiviti-aktiviti arginine ester hydrolase dan amidase, serta spesifikasi yang berbeza terhadap fibrinogen mamalia yang berlainan. Bagi koagulasi fibrinogen, hypnobin membebaskan fibrinopeptide A kebanyakannya, vii diikui amaun kecil fibrinopeptide B yang dibebaskan dengan lambat. Penemuan sedemikian memberi pemahaman terhadap struktur dan mekanisme thrombin-like enzyme ini, penting bagi penerangan patofisiologi dan penemuan ubat-ubatan, contohnya, sebagai antikoagulan bagi rawatan penyakit tromboembolik. viii Acknowledgement I would like to express my gratitude to my supervisors, Professor Sim Si Mui (Department of Pharmacology) and Professor Tan Nget Hong (Department of Molecular Medicine), Faculty of Medicine, University of Malaya for their guidance and efforts in supervising the research. I sincerely thank them for their endless patience and expertise training which are of immense significance to my future academic career. I thank Professor Christeine Ariaranee Gnanathasan (Department of Clinical Medicine, Faculty of Medicine, University of Colombo, Sri Lanka) and the staff at the serpentarium of the university, for their trust, kind assistance and sharing of samples in this collaborative project, from which I have benefited. I also thank Professor Sumana Khomvilai and Professor Visith Sitprija from the Queen Saovabha Memorial Institute of Bangkok, Thailand, for their good will and the supply of antivenoms, without which the project would not be possible to complete. I take this opportunity to express my special thanks to Professor Datin Zahurin Mohamed (Head, Department of Pharmacology) for her continuous support and encouragement extended towards my study and candidature in the Department. My special thanks is also expressed to Doctor Fung Shin Yee (Department of Molecular Medicine) for her advice and sharing of experiences in this project; to Professor Jayalakshmi Pailoor (Department of Pathology) for her assistance and advice in histopathology; and to all staff from the Department of Pharmacology, the Department of Molecular Medicine and the Laboratory Animal Center (Faculty of Medicine,
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