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Variations in neurotoxicity and proteome profile of Malayan krait (Bungarus candidus) venoms


Autoři: Muhamad Rusdi Ahmad Rusmili aff001;  Iekhsan Othman aff002;  Syafiq Asnawi Zainal Abidin aff002;  Fathin Athirah Yusof aff002;  Kavi Ratanabanangkoon aff003;  Lawan Chanhome aff004;  Wayne C. Hodgson aff005;  Janeyuth Chaisakul aff006
Působiště autorů: Kulliyyah of Pharmacy, International Islamic University Malaysia, Kuantan Campus, Bandar Indera Mahkota, Kuantan, Pahang Darul Makmur, Malaysia aff001;  Jeffrey Cheah School of Medicine and Health Sciences, Monash University Sunway Campus, Bandar Sunway, Malaysia aff002;  Department of Microbiology, Faculty of Science, Mahidol University, Bangkok, Thailand aff003;  Snake Farm, Queen Saovabha Memorial Institute, Thai Red Cross Society, Bangkok, Thailand aff004;  Monash Venom Group, Department of Pharmacology, Biomedical Discovery Institute, Monash University, Clayton, VIC, Australia aff005;  Department of Pharmacology, Phramongkutklao College of Medicine, Bangkok, Thailand aff006
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227122

Souhrn

Malayan krait (Bungarus candidus) is a medically important snake species found in Southeast Asia. The neurotoxic effects of envenoming present as flaccid paralysis of skeletal muscles. It is unclear whether geographical variation in venom composition plays a significant role in the degree of clinical neurotoxicity. In this study, the effects of geographical variation on neurotoxicity and venom composition of B. candidus venoms from Indonesia, Malaysia and Thailand were examined. In the chick biventer cervicis nerve-muscle preparation, all venoms abolished indirect twitches and attenuated contractile responses to nicotinic receptor agonists, with venom from Indonesia displaying the most rapid neurotoxicity. A proteomic analysis indicated that three finger toxins (3FTx), phospholipase A2 (PLA2) and Kunitz-type serine protease inhibitors were common toxin groups in the venoms. In addition, venom from Thailand contained L-amino acid oxidase (LAAO), cysteine rich secretory protein (CRISP), thrombin-like enzyme (TLE) and snake venom metalloproteinase (SVMP). Short-chain post-synaptic neurotoxins were not detected in any of the venoms. The largest quantity of long-chain post-synaptic neurotoxins and non-conventional toxins was found in the venom from Thailand. Analysis of PLA2 activity did not show any correlation between the amount of PLA2 and the degree of neurotoxicity of the venoms. Our study shows that variation in venom composition is not limited to the degree of neurotoxicity. This investigation provides additional insights into the geographical differences in venom composition and provides information that could be used to improve the management of Malayan krait envenoming in Southeast Asia.

Klíčová slova:

Asia – Indonesia – Neurotoxins – Snakebite – Snakes – Thailand – Toxins – Venoms


Zdroje

1. Gutierrez JM, Williams D, Fan HW, Warrell DA. Snakebite envenoming from a global perspective: Towards an integrated approach. Toxicon. 2010; 56(7): 1223–1235. doi: 10.1016/j.toxicon.2009.11.020 19951718

2. WHO. Guidelines for the Management of Snake-Bites. Guidelines for the Management of Snake-Bites. 2010

3. Tongpoo A, Sriapha C, Pradoo A, Udomsubpayakul U, Srisuma S, Wananukul W, et al. Krait envenomation in Thailand. Ther Clin Risk Manag. 2018; 14: 1711–1717. doi: 10.2147/TCRM.S169581 30271155

4. WHO. Venomous snakes of the South-East Asia Region, their venoms and pathophysiology of human envenoming. Guidelines for the management of Snake-Bites, 2nd edition. 2016

5. Chew KS, Khor HW, Ahmad R, Rahman NH. A five-year retrospective review of snakebite patients admitted to a tertiary university hospital in Malaysia. Int J Emerg Med. 2011; 4: 41. doi: 10.1186/1865-1380-4-41 21752254

6. Chaisakul J, Rusmili MR, Hodgson WC, Hatthachote P, Suwan K, Inchan A, et al. A Pharmacological Examination of the Cardiovascular Effects of Malayan Krait (Bungarus candidus) Venoms. Toxins (Basel). 2017; 9. Mar 29;9(4). pii: E122. doi: 10.3390/toxins9040122 28353659

7. Trinh KX, Khac QL, Trinh LX, Warrell DA. Hyponatraemia, rhabdomyolysis, alterations in blood pressure and persistent mydriasis in patients envenomed by Malayan kraits (Bungarus candidus) in southern Viet Nam. Toxicon. 2010; 56(6): 1070–1075. doi: 10.1016/j.toxicon.2010.06.026 20637219

8. Charoenpitakchai M, Wiwatwarayos K, Jaisupa N, Rusmili MRA, Mangmool S, Hodgson WC, et al. Non-neurotoxic activity of Malayan krait (Bungarus candidus) venom from Thailand. J Venom Anim Toxins Incl Trop Dis. 2018; 24: 9. doi: 10.1186/s40409-018-0146-y 29556251

9. Laothong C, Sitprija V. Decreased parasympathetic activities in Malayan krait (Bungarus candidus) envenoming. Toxicon. 2001; 39: 1353–1357. doi: 10.1016/s0041-0101(01)00087-3 11384723

10. Leong PK, Sim SM, Fung SY, Sumana K, Sitprija V, Tan NH. Cross neutralization of Afro-Asian cobra and Asian krait venoms by a Thai polyvalent snake antivenom (Neuro Polyvalent Snake Antivenom). PLoS Negl Trop Dis. 2012; 6: e1672. doi: 10.1371/journal.pntd.0001672 22679522

11. Leeprasert W, Kaojarern S.Specific antivenom for Bungarus candidus. J Med Assoc Thai. 2007; 90: 1467–1476. 17710993

12. Chanhome L, Wongtongkam N, Khow O, Pakmanee N, Omori-Satoh T, Sitprija V. Genus specific neutralization of Bungarus snake venoms by Thai Red Cross banded krait antivenom. J Nat Toxins. 1999; 8: 135–140. 10091133

13. Rusmili MR, Yee TT, Mustafa MR, Othman I, Hodgson WC. In-vitro neurotoxicity of two Malaysian krait species (Bungarus candidus and Bungarus fasciatus) venoms: neutralization by monovalent and polyvalent antivenoms from Thailand. Toxins (Basel). 2014; 6 (3): 1036–1048. doi: 10.3390/toxins6031036 24625762

14. Rusmili MR, Yee TT, Mustafa MR, Hodgson WC, Othman I. Isolation and characterization of a presynaptic neurotoxin, P-elapitoxin-Bf1a from Malaysian Bungarus fasciatus venom. Biochem Pharmacol. 2014; 91(3): 409–416. doi: 10.1016/j.bcp.2014.07.001 25064255

15. Rusmili MR, Tee TY, Mustafa MR, Othman I, Hodgson WC. Isolation and characterization of alpha-elapitoxin-Bf1b, a postsynaptic neurotoxin from Malaysian Bungarus fasciatus venom. Biochem Pharmacol. 2014; 88(2): 229–236. doi: 10.1016/j.bcp.2014.01.004 24440452

16. Rossetto O, Morbiato L, Caccin P, Rigoni M, Montecucco C. Presynaptic enzymatic neurotoxins. J Neurochem. 2006; 97(6): 1534–1545. doi: 10.1111/j.1471-4159.2006.03965.x 16805767

17. Rusmili MR, Yee TT, Mustafa MR, Hodgson WC, Othman I. Proteomic characterization and comparison of Malaysian Bungarus candidus and Bungarus fasciatus venoms. J Proteomics. 2014; 110: 129–144. doi: 10.1016/j.jprot.2014.08.001 25154052

18. Oh AMF, Tan CH, Tan KY, Quraishi NH, Tan NH. Venom proteome of Bungarus sindanus (Sind krait) from Pakistan and in vivo cross-neutralization of toxicity using an Indian polyvalent antivenom. J Proteomics. 2019; 193: 243–254. doi: 10.1016/j.jprot.2018.10.016 30385415

19. Oh AMF, Tan CH, Ariaranee GC, Quraishi N, Tan NH. Venomics of Bungarus caeruleus (Indian krait): Comparable venom profiles, variable immunoreactivities among specimens from Sri Lanka, India and Pakistan. J Proteomics. 2017; 164: 1–18. doi: 10.1016/j.jprot.2017.04.018 28476572

20. Tan KY, Tan CH, Sim SM, Fung SY, Tan NH. Geographical venom variations of the Southeast Asian monocled cobra (Naja kaouthia): venom-induced neuromuscular depression and antivenom neutralization. Comp Biochem Physiol C Toxicol Pharmacol. 2016; 185–186: 77–86. doi: 10.1016/j.cbpc.2016.03.005 26972756

21. Chanhome L, Khow O, Puempunpanich S, Sitprija V, Chaiyabutr N. Biological characteristics of the Bungarus candidus venom due to geographical variation. J Cell Anim Biol. 2009; 3: 93–100.

22. Skejic J, Hodgson WC. Population divergence in venom bioactivities of elapid snake Pseudonaja textilis: role of procoagulant proteins in rapid rodent prey incapacitation. PLoS One. 2013; 8: e63988. doi: 10.1371/journal.pone.0063988 23691135

23. Fry BG, Wickramaratna JC, Jones A, Alewood PF, Hodgson WC. Species and regional variations in the effectiveness of antivenom against the in vitro neurotoxicity of death adder (Acanthophis) venoms. Toxicol Appl Pharmacol. 2001; 175: 140–148. doi: 10.1006/taap.2001.9233 11543646

24. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227: 680–685. doi: 10.1038/227680a0 5432063

25. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012; 9: 671–675. doi: 10.1038/nmeth.2089 22930834

26. Adiwinata R, Nelwan EJ. Snakebite in Indonesia. Acta Med Indones. 2015; 47: 358–365. 26932707

27. Warrell DA, Looareesuwan S, White NJ, Theakston R, Warrell M, Kosakarn W, et al. Severe neurotoxic envenoming by the Malayan krait Bungarus candidus (Linnaeus): response to antivenom and anticholinesterase. Br Med J (Clin Res Ed). 1983; 286: 678–680. doi: 10.1136/bmj.286.6366.678 6402200

28. Crachi MT, Hammer LW, Hodgson WC. A pharmacological examination of venom from the Papuan taipan (Oxyuranus scutellatus canni). Toxicon. 1999; 37: 1721–1734. doi: 10.1016/s0041-0101(99)00114-2 10519650

29. Barber CM, Isbister GK, Hodgson WC. Solving the 'Brown snake paradox': in vitro characterisation of Australasian snake presynaptic neurotoxin activity. Toxicol Lett. 2012 210(3): 318–323. doi: 10.1016/j.toxlet.2012.02.001 22343038

30. Gutierrez JM, Lomonte B. Phospholipases A2: unveiling the secrets of a functionally versatile group of snake venom toxins. Toxicon. 2013; 62: 27–39. doi: 10.1016/j.toxicon.2012.09.006 23025922

31. Rouault M, Rash LD, Escoubas P, Boilard E, Bollinger J, Lomonte B, et al. Neurotoxicity and other pharmacological activities of the snake venom phospholipase A2 OS2: the N-terminal region is more important than enzymatic activity. Biochemistry. 2006; 45: 5800–5816. doi: 10.1021/bi060217r 16669624

32. Kini RM. Excitement ahead: structure, function and mechanism of snake venom phospholipase A2 enzymes. Toxicon. 2003; 42: 827–840. doi: 10.1016/j.toxicon.2003.11.002 15019485

33. Chaisakul J, Parkington HC, Isbister GK, Konstantakopoulos N, Hodgson WC. Differential myotoxic and cytotoxic activities of pre-synaptic neurotoxins from Papuan taipan (Oxyuranus scutellatus) and Irian Jayan death adder (Acanthophis rugosus) venoms. Basic Clin Pharmacol Toxicol. 2013; 112(5): 325–334. doi: 10.1111/bcpt.12048 23311944

34. Tan CH, Liew JL, Tan KY, Tan NH. Assessing SABU (Serum Anti Bisa Ular), the sole Indonesian antivenom: A proteomic analysis and neutralization efficacy study. Sci Rep. 2016; 6: 37299. doi: 10.1038/srep37299 27869134

35. Chaisakul J, Alsolaiss J, Charoenpitakchai M, Wiwatwarayos K, Sookprasert N, Harrison RA, et al. Evaluation of the geographical utility of Eastern Russell's viper (Daboia siamensis) antivenom from Thailand and an assessment of its protective effects against venom-induced nephrotoxicity. PLoS Negl Trop Dis. 2019; 13: e0007338. doi: 10.1371/journal.pntd.0007338 31644526

36. Prasarnpun S, Walsh J, Awad SS, Harris JB. Envenoming bites by kraits: the biological basis of treatment-resistant neuromuscular paralysis. Brain. 2005; 128: 2987–2996. doi: 10.1093/brain/awh642 16195243

37. Chippaux JP, Williams V, White J. Snake venom variability: methods of study, results and interpretation. Toxicon. 1991; 29(11): 1279–1303. doi: 10.1016/0041-0101(91)90116-9 1814005

38. Wickramaratna JC, Fry BG, Hodgson WC. Species-dependent variations in the in vitro myotoxicity of death adder (Acanthophis) venoms. Toxicol Sci. 2003; 74: 352–360. doi: 10.1093/toxsci/kfg144 12773755

39. Winter KL, Isbister GK, McGowan S, Konstantakopoulos N, Seymour JE, Hodgson WC. A pharmacological and biochemical examination of the geographical variation of Chironex fleckeri venom. Toxicol Lett. 2010; 192: 419–424. doi: 10.1016/j.toxlet.2009.11.019 19945518

40. Kunalan S, Othman I, Syed Hassan S, Hodgson WC. Proteomic Characterization of Two Medically Important Malaysian Snake Venoms, Calloselasma rhodostoma (Malayan Pit Viper) and Ophiophagus hannah (King Cobra). Toxins (Basel). 2018; 10(11). doi: 10.3390/toxins10110434 30373186

41. Oh AMF, Tan CH, Tan KY, Quraishi NH, Tan NH. Venom proteome of Bungarus sindanus (Sind krait) from Pakistan and in vivo cross-neutralization of toxicity using an Indian polyvalent antivenom. J Proteomics. 2019; 193: 243–254. doi: 10.1016/j.jprot.2018.10.016 30385415

42. Patra A, Chanda A, Mukherjee AK. Quantitative proteomic analysis of venom from Southern India common krait (Bungarus caeruleus) and identification of poorly immunogenic toxins by immune-profiling against commercial antivenom. Expert Rev Proteomics. 2019; 16: 457–469. doi: 10.1080/14789450.2019.1609945 31002271

43. Chapeaurouge A, Silva A, Carvalho P, McCleary R, Modahl C, Perales J, et al. Proteomic Deep Mining the Venom of the Red-Headed Krait, Bungarus flaviceps. Toxins. 2018; 10: 373. doi: 10.3390/toxins10090373 30217057

44. Wong KY, Tan CH, Tan KY, Quraishi NH, Tan NH. Elucidating the biogeographical variation of the venom of Naja naja (spectacled cobra) from Pakistan through a venom-decomplexing proteomic study. J Proteomics. 2018; 175: 156–173. doi: 10.1016/j.jprot.2017.12.012 29278784

45. Khow O, Chanhome L, Omori-Satoh T, Ogawa Y, Yanoshita R, Samejima Y, et al. Isolation, toxicity and amino terminal sequences of three major neurotoxins in the venom of Malayan krait (Bungarus candidus) from Thailand. J Biochem. 2003; 134: 799–804. doi: 10.1093/jb/mvg187 14769867

46. Kessler P, Marchot P, Silva M, Servent D. The three‐finger toxin fold: a multifunctional structural scaffold able to modulate cholinergic functions. J Neurochem. 2017;142: 7–18. doi: 10.1111/jnc.13975 28326549

47. Kini RM, Doley R. Structure, function and evolution of three-finger toxins: mini proteins with multiple targets. Toxicon. 2010; 56: 855–867. doi: 10.1016/j.toxicon.2010.07.010 20670641

48. Kini RM. Molecular moulds with multiple missions: functional sites in three‐finger toxins. Clin Exp Pharmacol Physiol. 2002; 29: 815–822. doi: 10.1046/j.1440-1681.2002.03725.x 12165048

49. Kuhn P, Deacon AM, Comoso S, Rajaseger G, Kini RM, Uson I, et al. The atomic resolution structure of bucandin, a novel toxin isolated from the Malayan krait, determined by direct methods. Acta Cryst. 2000; 56: 1401–1407. doi: 10.1107/S0907444900011501 11053837

50. Nirthanan S, Charpantier E, Gopalakrishnakone P, Gwee MC, Khoo HE, Cheah LS, et al. Candoxin, a novel toxin from Bungarus candidus, is a reversible antagonist of muscle (alphabetagammadelta) but a poorly reversible antagonist of neuronal alpha 7 nicotinic acetylcholine receptors. J Biol Chem. 2002; 277: 17811–17820. doi: 10.1074/jbc.M111152200 11884390

51. Karsani SA, Othman I. Isolation, complete amino acid sequence and characterization of a previously unreported post-synaptic neurotoxin–AlphaN3, from the venom of Bungarus candidus. Biochem Biophys Res Commun. 2009;389: 343–348. doi: 10.1016/j.bbrc.2009.08.145 19728988

52. Shan LL, Gao JF, Zhang YX, Shen SS, He Y, Wang J, et al. Proteomic characterization and comparison of venoms from two elapid snakes (Bungarus multicinctus and Naja atra) from China. J Proteomics. 2016; 138: 83–94. doi: 10.1016/j.jprot.2016.02.028 26924299

53. Utkin YN, Kuch U, Kasheverov IE, Lebedev DS, Cederlund E, Molles BE, et al. Novel long- chain neurotoxins from Bungarus candidus distinguish the two binding sites in muscle-type nicotinic acetylcholine receptors. Biochem J. 2019; 476: 1285–1302. doi: 10.1042/BCJ20180909 30944155

54. Chang CC. Neurotoxins with phospholipase A2 activity in snake venoms. Proc Natl Sci Counc Repub China B. 1985; 9: 126–142. 2996044

55. Tsai IH, Tsai HY, Saha A, Gomes A. Sequences, geographic variations and molecular phylogeny of venom phospholipases and threefinger toxins of eastern India Bungarus fasciatus and kinetic analyses of its Pro31 phospholipases A2. FEBS J. 2007;l 274: 512–525. doi: 10.1111/j.1742-4658.2006.05598.x 17166178

56. Slowinski JB. A phylogenetic analysis of Bungarus (Elapidae) based on morphological characters. J Herpetol. 1994; 440–446.


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