Abstract
Two species of jellyfish, Cyanea nozakii Kishinouye and Nemopilema nomurai Kishinouye, have occurred offcoastal areas of the northeastern China Sea, Yellow Sea, and Bohai Sea in recent years. They influence marine ecosystem safety and fishery production, and also pose a risk to human health. The current study examined the hemolytic and cytotoxic activities of crude venoms extracted from the nematocysts of C. nozakii and N. nomurai. The results showed that there were more nematocysts on tentacles from C. nozakii than on tentacles of the same length from N. nomurai. The protein concentration per nematocyst extracted from N. nomurai was higher than that from C. nozakii. Both nematocyst venoms showed dose- and timedependent hemolytic activity on erythrocytes from chicken, pigeon, and sheep, with sheep erythrocytes being the most sensitive, with EC50 values of 69.69 and 63.62 μg/mL over a 30-min exposure with N. nomurai and C. nozakii nematocyst venoms, respectively. A cytotoxic assay of both jellyfish venoms on A431 human epidermal carcinoma cells resulted in IC50 values of 68.6 and 40.9 μg/mL after 24-h incubation, respectively, with venom from C. nozakii showing stronger cytotoxic activity than that from N. nomurai. The results of current study indicate that nematocyst venom from C. nozakii had stronger hemolytic and cytotoxic activities than that from N. nomurai and, thus, C. nozakii might be more harmful to the health of humans and other species than are N. nomurai when they appear in coastal waters.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bailey P M, Bakker A J, Seymour J E, Wilce J A. 2005. A functional comparison of the venom of three Australian jellyfish-Chironex fleckeri, Chiropsalmus sp., and Carybdea xaymacana-on cytosolic Ca2+, haemolysis and Artemia sp. lethality. Toxicon, 45 (2): 233–242, https://doi.org/10.1016/j.toxicon.2004.10.013.
Bhakdi S, Tranum-Jensen J. 1988. Damage to cell membranes by pore-forming bacterial cytolysins. Prog. Allergy, 40: 1–43. https://doi.org/10.1159/000414943.
Bloom D A, Burnett J W, Alderslade P. 1998. Partial purification of box jellyfish (Chironex fleckeri) nematocyst venom isolated at the beachside. Toxicon, 36 (8): 1 075–1 085, https://doi.org/10.1016/S0041-0101(98)00096-8.
Bloom D A, Radwan F F Y, Burnett J W. 2001. Toxinological and immunological studies of capillary electrophoresis fractionated Chrysaora quinquecirrha (Desor) fishing tentacle and Chironex fleckeri Southcott nematocyst venoms. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 128 (1): 75–90, https://doi.org/10.1016/S1532-0456(00)00180-0.
Bradford M M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72 (1–2): 248–254, https://doi.org/10.1016/0003-2697(76)90527-3.
Brinkman D, Burnell J. 2007. Identification, cloning and sequencing of two major venom proteins from the box jellyfish, Chironex fleckeri. Toxicon, 50 (6): 850–860, https://doi.org/10.1016/j.toxicon.2007.06.016.
Burnett J W, Calton G J. 1987. Venomous pelagic coelenterates: chemistry, toxicology, immunology and treatment of their stings. Toxicon, 25 (6): 581–602, https://doi.org/10.1016/0041-0101(87)90105-X.
Carrette T, Seymour J. 2004. A rapid and repeatable method for venom extraction from Cubozoan nematocysts. Toxicon, 44 (2): 135–139, https://doi.org/10.1016/j.toxicon.2004.04.008.
Cheng J H, Li S F, Ding F Y, Yan L P. 2004. Primary analysis on the jellyfish blooms and its cause in the East China Sea and the Yellow Sea. Mod. Fish. Inf., 19 (5): 10–12. (in Chinese)
Ding F Y, Cheng J H. 2005. The analysis on fish stock characteristics in the distribution areas of large jellyfish during summer and autumn in the East China Sea region. Mar. Fish., 27 (2): 120–128. (in Chinese with English abstract)
Dong J, Liu C Y, Wang Y Q, Wang B. 2006. Laboratory observations on the life cycle of Cyanea nozakii (Semeostomida, Scyphozoa). Acta Zool. Sinica, 52 (2): 389–395.
Dong Z J, Liu D Y, Keesing J K. 2010. Jellyfish blooms in China: dominant species, causes and consequences. Mar. Pollut. Bull., 60 (7): 954–963, https://doi.org/10.1016/j.marpolbul.2010.04.022.
Edwards L P, Whitter E, Hessinger D A. 2002. Apparent membrane pore-formation by Portuguese Man-of-war (Physalia physalis) venom in intact cultured cells. Toxicon, 40 (9): 1 299–1 305, https://doi.org/10.1016/S0041-0101(02)00138-1.
Feng J H, Yu H H, Xing R E, Liu S, Wang L, Cai S B, Li P C. 2010. Partial characterization of the hemolytic activity of the nematocyst venom from the jellyfish Cyanea nozakii Kishinouye. Toxicol. In Vitro, 24 (6): 1 750–1 756.
Helmholz H, Ruhnau C, Schütt C, Prange A. 2007. Comparative study on the cell toxicity and enzymatic activity of two northern scyphozoan species Cyanea capillata (L.) and Cyanea lamarckii (Péron & Léslieur). Toxicon, 50 (1): 53–64, https://doi.org/10.1016/j.toxicon.2007.02.014.
Huang Z, Lin M. 2012. The Living Species and Their Illustrations in China's Seas (Part I). The Living Species in China's Seas. Ocean Press, Beijing, China, p.317–318. (in Chinese)
Jiang Z G, Liu W B, Yue X A. 2008. Three cases of jellyfishsting induced death. Chin. J. Dermatol., 41 (10): 707. (in Chinese)
Kang C, Munawir A, Cha M, Sohn E T, Lee H, Kim J S, Yoon W D, Lim D, Kim E. 2009. Cytotoxicity and hemolytic activity of jellyfish Nemopilema nomurai (Scyphozoa: Rhizostomeae) venom. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 150 (1): 85–90, https://doi.org/10.1016/j.cbpc.2009.03.003.
Kawahara M, Uye S, Burnett J, Mianzan H. 2006. Stings of edible jellyfish (Rhopilema hispidum, Rhopilema esculentum and Nemopilema nomurai) in Japanese waters. Toxicon, 48 (6): 713–716, https://doi.org/10.1016/j.toxicon.2006.06.015.
Lee H, Jung E S, Kang C, Yoon W D, Kim J S, Kim E. 2011. Scyphozoan jellyfish venom metalloproteinases and their role in the cytotoxicity. Toxicon, 58 (3): 277–284, https://doi.org/10.1016/j.toxicon.2011.06.007.
Li C P, Li P C, Feng J H, Li R F, Yu H H. 2012. Cytotoxicity of the venom from the nematocysts of jellyfish Cyanea nozakii Kishinouye. Toxicol. Ind. Health, 28 (2): 186–192, https://doi.org/10.1177/0748233711410910.
Li R F, Yu H H, Xing R E, Liu S, Qing Y K, Li K C, Li B, Meng X T, Cui J H, Li P C. 2013. Isolation and in vitro partial characterization of hemolytic proteins from the nematocyst venom of the jellyfish Stomolophus meleagris. Toxicol. in Vitro, 27 (6): 1 620–1 625, https://doi.org/10.1016/j.tiv.2013.04.004.
Li R F, Yu H H, Yue Y, Liu S, Xing R E, Chen X L, Wang X Q, Li P C. 2014. In depth analysis of the in vivo toxicity of venom from the jellyfish Stomolophus meleagris. Toxicon, 92: 60–65. https://doi.org/10.1016/j.toxicon.2014.10.002.
Marino A, Morabito R, La Spada G. 2009. Factors altering the haemolytic power of crude venom from Aiptasia mutabilis (Anthozoa) nematocysts. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 152 (3): 418–422, https://doi.org/10.1016/j.cbpa.2008.11.016.
Marino A, Morabito R, Pizzata T, La Spada G. 2008. Effect of various factors on Pelagia noctiluca (Cnidaria, Scyphozoa) crude venom-induced haemolysis. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 151 (1): 144–149, https://doi.org/10.1016/j.cbpa.2008.06.013.
Nagai H, Takuwa K, Nakao M, Ito E, Miyake M, Noda M, Nakajima T. 2000a. Novel proteinaceous toxins from the box jellyfish (sea wasp) Carybdea rastoni. Biochem. Biophys. Res. Commun., 275 (2): 582–588, https://doi.org/10.1006/bbrc.2000.3353.
Nagai H, Takuwa, K, Nakao M, Sakamoto B, Crow G L, Nakajima T. 2000b. Isolation and characterization of a novel protein toxin from the Hawaiian box jellyfish (Sea Wasp) Carybdea alata. Biochem. Biophys. Res. Commun., 275 (2): 589–594, https://doi.org/10.1006/bbrc.2000.3352.
Nagai H, Takuwa-Kuroda K. Nakao M, Oshiro N, Iwanaga S, Nakajima T. 2002. A novel protein toxin from the deadly box jellyfish (Sea Wasp, Habu-kurage) Chiropsalmus quadrigatus. Biosci. Biotech nol. Bioch em., 66 (1): 97–102, https://doi.org/10.1271/bbb.66.97.
Peng L S, Zhang X Q. 1999. Cyanea sp. endanger marine fishery resources. Mar. Inf., 8: 25. (in Chinese)
Rottini G, Gusmani L, Parovel E, Avian M, Patriarca P. 1995. Purification and properties of a cytolytic toxin in venom of the jellyfish Carybdea marsupialis. Toxicon, 33 (3): 315–326, https://doi.org/10.1016/0041-0101(94)00174-7.
Tibballs J. 2006. Australian venomous jellyfish, envenomation syndromes, toxins and therapy. Toxicon, 48 (7): 830–859, https://doi.org/10.1016/j.toxicon.2006.07.020.
Torres M, Aguilar M B, Falcón A, Sánchez L, Radwan F F Y, Burnett J W, Heimer-De La Cotera E P, Arellano R O. 2001. Electrophysiological and hemolytic activity elicited by the venom of the jellyfish Cassiopea xamachana. Toxicon, 39 (9): 1 297–1 307, https://doi.org/10.1016/S0041-0101(01)00081-2.
Xu J T, Zhang X L, Pang M. 2014. Comparative study on cytotoxicity of Nemopilema nomurai and Cyanea nozakii nematocyst venoms. Adv. Mar. Sci., 32 (4): 543–550. (in Chinese with English abstract)
Xu Y, Li H H, Li Z Z. 2007. Clinical analysis and treatment experience of 530 cases of jellyfish dermatitis. J. Clin. Dermatol., 36 (5): 294–295. (in Chinese)
Yu H H, Liu X G, Dong X L, Li C P, Xing R E, Liu S, Li P C. 2005. Insecticidal activity of proteinous venom from tentacle of jellyfish Rhopilema esculent um Kishinouye. Bioorg. Med. Chem. Lett., 15 (22): 4 949–4 952, https://doi.org/10.1016/j.bmcl.2005.08.015.
Yu H H, Xing R E, Liu S, Li C P, Guo Z Y, Li P C. 2007. Studies on the hemolytic activity of tentacle extracts of jellyfish Rhopilema esculentum Kishinouye: application of orthogonal test. Int. J. Biol. Macromol., 40 (3): 276–280, https://doi.org/10.1016/j.ijbiomac.2006.06.020.
Zhang M L, Qin S D, Li M, Chen G Z. 1993. Investigation of coelenterare stings in North China Sea. Acta Acad. Med. Qingdao, 29 (4): 263–268. (in Chinese with English abstract)
Zhong X M, Tang J H, Liu P T. 2004. A study on the relationship between Cyanea nozakii Kisninouye breaking out and ocean ecosystem. Mod. Fish. Inf., 19 (3): 15–17. (in Chinese with English abstract)
Author information
Authors and Affiliations
Corresponding author
Additional information
Supported by the NSFC-Shandong Joint Funds Project (No. U1606404), the National Natural Science Foundation of China (No. 41606140), and the National Special Research Fund for Non-Profit Marine Sector (No. 201005018)
Rights and permissions
About this article
Cite this article
Pang, M., Xu, J., Liu, Y. et al. Comparative study of the hemolytic and cytotoxic activities of nematocyst venoms from the jellyfish Cyanea nozakii Kishinouye and Nemopilema nomurai Kishinouye. J. Ocean. Limnol. 36, 1255–1265 (2018). https://doi.org/10.1007/s00343-018-7104-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00343-018-7104-y