Elsevier

Toxicon

Volume 55, Issue 4, 1 April 2010, Pages 838-845
Toxicon

The lethality of tentacle-only extract from jellyfish Cyanea capillata is primarily attributed to cardiotoxicity in anaesthetized SD rats

https://doi.org/10.1016/j.toxicon.2009.11.022Get rights and content

Abstract

Previous studies in our laboratory have shown that tentacle-only extract (TOE) has similar hypotensive effects with nematocyst venom from jellyfish Cyanea capillata, and the experimental studies on the in vivo cardiovascular effects of TOE were further performed to explore the leading cause of death and analyze the basic physiopathologic change in anaesthztized SD rats. Plots of TOE dose versus time to death showed dose-dependent curvilinear relationship. ECG changed in a dose- and time-dependent manner. Haemodynamic parameters, including the heart rate, mean femoral arterial pressure, left ventricular developed pressure and the first derivative of left ventricular pressures, decreased, but left ventricular end-diastolic pressure did not increase. Arterial partial pressure of oxygen and oxygen saturation did not change. Lactate dehydrogenase, creatine kinase and MB isoenzyme of creatine kinase increased significantly. Histopathological examination showed congestion, haemorrhage, edema and denaturation in the heart; congestion, haemorrhage in the lung and acute congestion in the liver. Transmission electron microscopy examination found that parts of sarcomeric filaments disrupted, dissolved and disappeared, and parts of mitochondria swelled in cardiocytes. Laser scanning confocal microscope examination found that ventricular myocytes from adult rat were deformed and ultimately died within 30 min after TOE treatment. Our results reveal that cardiodepressive effect of C. capillata TOE is the leading cause of death and acute total heart failure is the basic physiopathologic change in anaesthetized SD rats.

Introduction

Cyanea capillata, also called the “Sea Blubber”, the “Hairy Stinger” or the “Snottie”, was described as “a repulsive big slimy jellyfish”, which bears a “general resemblance to a mop hiding under a dinner-plate” by Barnes (1960). C. capillata has a worldwide distribution and is a major kind of jellyfish in southeast Chinese coastal waters. Compared with the fatal jellyfish such as Chironex fleckeri, Carukia barnesi, and Physalia physalis, there are no reported human fatalities caused by C. capillata stings. However, contacting with the tentacles may produce burning feeling, severe pain, swelling, red streak, nausea and abdominal pains. At times, profuse sweating, muscle cramp and respiratory distress are seen (Tibballs, 2006). Recently, the number of C. capillata has increased dramatically in east Chinese coastal waters and patients stung by this kind of jellyfish increased correspondingly. Crude and partially purified C. capillata nematocyst venoms, mainly peptide toxins, have demonstrated a wide spectrum of biological activities, including haemolytic, enzymatic, and cardiovascular activities and so on in a few in vivo and in vitro studies (Rice and Powell, 1972, Walker, 1977a, Walker, 1977b, Walker et al., 1977, Long and Burnett, 1989, Helmholz et al., 2007).

Several studies introduced the differences between the biological activities of nematocyst venom and tentacle-only extract (TOE) from jellyfish tentacles (Endean and Noble, 1971, Ramasamy et al., 2005b, Ramasamy et al., 2005c), indicating the activities found in TOE are independent of nematocyst venom. However, other studies reported similar activities found in both TOE and nematocyst venom, which probably produced by the same proteins or the same gene encoded proteins with different modification and migration (Nagai et al., 2000a, Nagai et al., 2000b). That is to say, the toxic proteins in nematocyst venom should be syntheized and transported from TOE. Studies performed in our laboratory have shown similar hypotensive activity between TOE and nematocyst venom from jellyfish C. capillata (Xiao et al., 2009), so the experimental studies were further performed on the in vivo cardiovascular effects of TOE to explore the leading cause of death and analyze the basic physiopathologic change in anaesthztized SD rats.

Section snippets

Preparation of TOE from jellyfish C. capillata

Specimens of C. capillata were collected in June 2008 on the Sanmenwan coast of the East China Sea in Zhejiang province, China, and identified by Professor Huixin Hong from Fisheries College of Jimei University (Xiamen, China). The removed tentacles were preserved in plastic bags on dry ice and immediately shipped to Shanghai, where the samples were frozen at −70 °C until use. The TOE devoid of nematocysts was prepared following the method described by us before (Xiao et al., 2009). Briefly,

Relationship between TOE dose and time to death in rats

TOE at the doses of 2.5, 5 and 10 mg/kg i.v. all led to rat death within 5 h and the median time of rat death was 160, 80.5 and 20 min, respectively. Plots of TOE dose versus time to death in SD rats showed curvilinear relationship with increasing TOE dose producing corresponding decrease in time to death (Fig. 1).

Effects of TOE on the rat ECG

With the treatment of TOE at the doses of 2.5, 5 and 10 mg/kg i.v., the ECG of rats significantly changed in dose- and time-dependent manners. At the higher dose of 10 mg/kg, bradycardia

Discussion

In recent years, an increasing number of studies have been performed on the cardiovascular effects of jellyfish venoms from C. fleckeri, C. barnesi, Nemopilema nomurai, Chiropsella bronzia and Alatina nr mordens because of the new extraction method of nematocyst venom established by Carrette and Seymour (2004), which allows for rapid, efficient and reliable extraction and is devoid of isolation-related problems such as excessive heat build-up (Ramasamy et al., 2005b, Ramasamy et al., 2005c, Kim

Acknowledgements

This research was funded by the Natural Science Foundation of Shanghai Municipal Government (06ZR14111) and the Foundation of the “Eleventh Five-Year Plan” for Medical Science Development of PLA (06Z020). The authors thank Fang Wei of the Foreign Languages Department of the Second Military Medical University for his careful revision of the English language for this manuscript.

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Co-first authors: Liang Xiao, Guan-sheng Liu and Qian-qian Wang.

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