The effect of ammonium sulfate concentration in protein isolation of lionfish (Pterois volitans) spines venom extract for antitumor test

✅ 全文

硫酸铵浓度对狮子鱼(Pterois volitans)脊刺毒液蛋白提取物用于抗肿瘤试验的影响

作者 Andy Noorsaman Sommeng; Adinda Kemala Eka; Mikael Januardi Ginting; Sonya Pebriani; Muhamad Sahlan; Heri Hermansyah; Anondho Wıjanarko 期刊 AIP conference proceedings 发表日期 2019 ISSN 0094-243X DOI 10.1063/1.5139346 类型 原创研究 (Original Research)

📄 英文摘要 English Abstract

EN

Lionfish (Pterois volitans) is a native species of the Indo-Pacific Ocean. This species is known as destructive invasive species that invade in many areas. The invasion of Lionfish gives negative impacts on the ecology and economic condition of the invaded regions. Therefore, to reduce the number of Lionfish in the ocean and to attract people to exploit Lionfish, the study about Lionfish’s benefit is necessary. The recent study revealed that venom extract from Lionfish spines has a potential cytolytic effect that widely uses for antitumor studies. In this study, to obtain the optimum concentration of the solvent that used for protein isolation and to observe the antitumor properties of Lionfish further, we isolated the protein of Lionfish venom extract with ammonium sulfate and tested it on HeLa cell as the model of tumor cells. The Lowry and BSLT test showed that the highest protein concentration and activity obtained when the highest level of ammonium sulfate isolated crude venom. The highest percentage of inhibition in HeLa cells reach 17-19% at the highest dose of Lionfish protein isolate. Indeed, the inhibition effect on HeLa cells can be enhanced because SDS-PAGE results showed that there are several proteins with different effects on tumor cells contained in the protein isolate of Lionfish venom. Thus, eliminating these proteins might increase the inhibition effects of Lionfish venom protein in tumor cells. These results suggest that Lionfish has an antitumor effect, but need further purification step and more evaluation of the protein in Lionfish venom extract that can enhance the antitumor effect.

📄 中文摘要 Chinese Abstract

中文
狮子鱼(Pterois volitans)是印度洋-太平洋海域的原生物种,已成为许多地区具有破坏性的入侵物种,对生态和经济状况造成负面影响。该入侵导致本地鱼类种群减少、珊瑚礁受损,在美国造成高达1200亿美元的经济损失,在加勒比群岛估计损失达1亿至3亿美元。减少狮子鱼种群的策略之一是开发利用其毒液,该毒液含有具有心血管、神经肌肉和细胞溶解作用的毒素。近期研究表明,狮子鱼毒液的细胞溶解活性可抑制肿瘤细胞(如艾氏腹水癌细胞)的生长,且从粗毒液中分离出的7.6 kDa蛋白质显示出抗肿瘤活性。这些毒素通过激活半胱天冬酶间接破坏肿瘤微环境并诱导细胞凋亡。然而,对抗肿瘤蛋白的分离过程,特别是蛋白质分离过程中硫酸铵浓度的影响,关注甚少。因此,本研究探讨了硫酸铵浓度对狮子鱼毒液提取物蛋白质分离以用于抗肿瘤测试的影响。

📋 英文结构化总结 English Structured Summary

全文整理

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Header:

Background Lionfish (Pterois volitans) is a native species of the Indo-Pacific Ocean that has become a destructive invasive species in many areas, causing negative impacts on ecology and economic conditions. The invasion has reduced local fish populations, damaged coral reefs, and resulted in financial losses of up to 120 billion USD in the US and estimated losses of 100 to 300 million USD in the Caribbean islands. One strategy to reduce the lionfish population is to exploit their venom, which contains toxins with cardiovascular, neuromuscular, and cytolytic effects. Recent studies have shown that the cytolytic activity of lionfish venom can reduce the growth of tumor cells, such as Erlich's Ascites Carcinoma cells, and a 7.6 kDa protein isolated from crude venom demonstrated antitumor activity. The toxins play an indirect role in destroying the tumor microenvironment and inducing apoptosis by activating caspases. However, little attention has been paid to the process of isolating the antitumor protein, specifically the effects of ammonium sulfate concentration during protein isolation. This study therefore examines the effect of ammonium sulfate concentration on protein isolation of lionfish venom extract for antitumor testing.

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Methods The specimens of Pterois volitans were obtained from around the Indonesian oceans. Lionfish were killed by cooling, and the venomous spines were removed and washed with 0.1 M phosphate buffer (pH 7.0) and 0.01 M CaCl₂. HeLa cells, used as the tumor cell model, were obtained from the Indonesia International Institute for Life Sciences (I3L, Indonesia) and harvested for the experiments. The provided text does not detail the protein isolation procedure using ammonium sulfate, the Lowry assay, BSLT test, SDS-PAGE, or the antitumor assay methodology beyond these specimen collection and cell culture steps.

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Results The Lowry and BSLT tests showed that the highest protein concentration and activity were obtained when the highest level of ammonium sulfate was used to isolate crude venom. The highest percentage of inhibition in HeLa cells reached 17–19% at the highest dose of lionfish protein isolate. SDS-PAGE results indicated that several proteins with different effects on tumor cells were present in the protein isolate of lionfish venom, suggesting that eliminating certain proteins might increase the inhibition effect on HeLa cells.

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Data Summary The highest percentage of inhibition in HeLa cells was 17–19% at the highest dose of lionfish protein isolate. The highest protein concentration and activity (as measured by the Lowry and BSLT tests) were obtained when the highest level of ammonium sulfate was used for isolation. No other quantitative values (e.g., exact protein concentrations or statistical measures) are provided in the text.

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Conclusions The results suggest that lionfish has an antitumor effect, but further purification steps and more evaluation of the proteins in lionfish venom extract are needed to enhance the antitumor effect. Eliminating certain proteins identified by SDS-PAGE may increase the inhibition effects of lionfish venom protein on tumor cells.

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Practical Significance Utilizing lionfish venom for antitumor therapy offers both ecological and economic benefits by providing a use for an invasive species, thereby encouraging exploitation to reduce lionfish populations in invaded oceans. This approach can help mitigate the negative impacts of lionfish invasion on marine ecosystems and the tourism industry while contributing to alternative cancer therapy research.

📋 中文结构化总结 Chinese Structured Summary

中文

背景:

狮子鱼(Pterois volitans)是印度洋-太平洋海域的原生物种,已成为许多地区具有破坏性的入侵物种,对生态和经济状况造成负面影响。该入侵导致本地鱼类种群减少、珊瑚礁受损,在美国造成高达1200亿美元的经济损失,在加勒比群岛估计损失达1亿至3亿美元。减少狮子鱼种群的策略之一是开发利用其毒液,该毒液含有具有心血管、神经肌肉和细胞溶解作用的毒素。近期研究表明,狮子鱼毒液的细胞溶解活性可抑制肿瘤细胞(如艾氏腹水癌细胞)的生长,且从粗毒液中分离出的7.6 kDa蛋白质显示出抗肿瘤活性。这些毒素通过激活半胱天冬酶间接破坏肿瘤微环境并诱导细胞凋亡。然而,对抗肿瘤蛋白的分离过程,特别是蛋白质分离过程中硫酸铵浓度的影响,关注甚少。因此,本研究探讨了硫酸铵浓度对狮子鱼毒液提取物蛋白质分离以用于抗肿瘤测试的影响。

方法:

狮子鱼(Pterois volitans)标本采集自印度尼西亚周边海域。通过低温处死狮子鱼,取下毒刺,用0.1 M磷酸缓冲液(pH 7.0)和0.01 M CaCl₂清洗。HeLa细胞作为肿瘤细胞模型,取自印度尼西亚国际生命科学研究所(I3L,印度尼西亚),并培养用于实验。所提供的文本未详细描述使用硫酸铵进行蛋白质分离、Lowry测定、BSLT测试、SDS-PAGE或抗肿瘤测定的具体方法,仅包含上述标本采集和细胞培养步骤。

结果:

Lowry和BSLT测试表明,使用最高浓度硫酸铵分离粗毒液时,蛋白质浓度和活性最高。HeLa细胞的最高抑制率达到17-19%,出现在狮子鱼蛋白质分离物最高剂量组。SDS-PAGE结果显示,狮子鱼毒液蛋白质分离物中存在多种对肿瘤细胞具有不同作用的蛋白质,提示去除某些蛋白质可能增强对HeLa细胞的抑制效果。

数据摘要:

HeLa细胞的最高抑制率为17-19%,出现在狮子鱼蛋白质分离物最高剂量组。使用最高浓度硫酸铵分离时,蛋白质浓度和活性(通过Lowry和BSLT测试测定)最高。文本中未提供其他定量数值(如精确蛋白质浓度或统计学指标)。

结论:

结果表明狮子鱼具有抗肿瘤作用,但需要进一步纯化步骤和对狮子鱼毒液提取物中蛋白质的更多评估,以增强抗肿瘤效果。通过SDS-PAGE鉴定的某些蛋白质的去除可能增强狮子鱼毒液蛋白质对肿瘤细胞的抑制作用。

实际意义:

利用狮子鱼毒液进行抗肿瘤治疗具有生态和经济效益,为入侵物种提供利用途径,从而鼓励开发利用以减少入侵海域的狮子鱼种群。该方法有助于减轻狮子鱼入侵对海洋生态系统和旅游业的负面影响,同时为替代癌症治疗研究做出贡献。

📖 英文全文 English Full Text

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The effect of ammonium sulfate concentration in protein isolation of lionfish (Pterois volitans) spines venom extract for antitumor test Cite as: AIP Conference Proceedings 2193, 030009 (2019); https://doi.org/10.1063/1.5139346 Published Online: 10 December 2019 Andy Noorsaman Sommeng, Adinda Kemala Eka, Mikael Januardi Ginting, Sonya Pebriani, Muhamad Sahlan, Heri Hermansyah, and Anondho Wijanarko

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AIP Conference Proceedings 2193, 030009 (2019); https://doi.org/10.1063/1.5139346 © 2019 Author(s). 2193, 030009

The Effect of Ammonium Sulfate Concentration in Protein Isolation of Lionfish (Pterois Volitans) Spines Venom Extract for Antitumor Test Andy Noorsaman Sommeng1, Adinda Kemala Eka1, Mikael Januardi Ginting2, Sonya Pebriani1, Muhamad Sahlan1,3, Heri Hermansyah1, Anondho Wijanarko1a 1

Departement of Chemical Engineering, Faculty of Engineering Universitas Indonesia, Kampus UI Depok, West Java 16424 Indonesia 2

Marine Science Postgraduate Program, Faculty of Mathematics and Natural Science, Universitas Indonesia, Kampus UI Depok, West Java 16424 Indonesia 3

Research Center for Biomedical Engineering, Faculty of Engineering, Universitas Indonesia, Kampus UI Depok, West Java 16424 Indonesia Corresponding author: a)anondho.wijanarko@yahoo.com Abstract. Lionfish (Pterois volitans) is a native species of the Indo-Pacific Ocean. This species is known as destructive invasive species that invade in many areas. The invasion of Lionfish gives negative impacts on the ecology and economic condition of the invaded regions. Therefore, to reduce the number of Lionfish in the ocean and to attract people to exploit Lionfish, the study about Lionfish's benefit is necessary. The recent study revealed that venom extract from Lionfish spines has a potential cytolytic effect that widely uses for antitumor studies. In this study, to obtain the optimum concentration of the solvent that used for protein isolation and to observe the antitumor properties of Lionfish further, we isolated the protein of Lionfish venom extract with ammonium sulfate and tested it on HeLa cell as the model of tumor cells. The Lowry and BSLT test showed that the highest protein concentration and activity obtained when the highest level of ammonium sulfate isolated crude venom. The highest percentage of inhibition in HeLa cells reach 17-19% at the highest dose of Lionfish protein isolate. Indeed, the inhibition effect on HeLa cells can be enhanced because SDS-PAGE results showed that there are several proteins with different effects on tumor cells contained in the protein isolate of Lionfish venom. Thus, eliminating these proteins might increase the inhibition effects of Lionfish venom protein in tumor cells. These results suggest that Lionfish has an antitumor effect, but need further purification step and more evaluation of the protein in Lionfish venom extract that can enhance the antitumor effect. Keywords: Antitumor, Lionfish, Protein isolation

INTRODUCTION The utilization of venom as an alternative therapy has received much attention in recent years due to its therapeutic effects in several chronic diseases like tumors or cancer, which offer some economic and ecological benefits. Lionfish (Pterois volitans) is a native fish species in the Indo-Pacific Ocean. Lionfish (Pterois volitans) is one of the invasive species in the oceans. The high reproduction and distribution rates of Lionfish cause the widespread of Lionfish invasion. Twenty years from the first time the Lionfish was discovered, the Lionfish invasion area has spread to most of western Atlantic, Florida, Bahamas, Cuba, Dominican Republic, Puerto Rico, most of the Lesser Antilles, Cayman Islands, Jamaica, Colombia, Costa Rica, Belize, Venezuela, and Mexico [1]. However, it has been found that the invasion of P. volitans has caused some negative impacts on marine ecosystems. The growth of P. volitans population has reduced the population of local fish species, thus affecting the economic conditions of the invaded area. The invasion of P. volitans in the US has caused financial losses of up to

The 4th Biomedical Engineering’s Recent Progress in Biomaterials, Drugs Development, Health, and Medical Devices AIP Conf. Proc. 2193, 030009-1–030009-8; https://doi.org/10.1063/1.5139346 Published by AIP Publishing. 978-0-7354-1944-5/$30.00

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120 billion USD [2]. In the Carribean islands, uncontrolled P. volitans population has also created the damage of coral reefs and marine ecosystems. The revenues from the tourism industry in the Carribean islands decreased by up to 2-5% with an estimated loss of 100 to 300 million USD [3]. One way to reduce the P. volitans population level is by using P. volitans to become something that can be useful. P. volitans produce toxins that have the cardiovascular, neuromuscular and cytolytic effect (causing cell death) associated with the presence of some toxic proteins and other active components such as acetylcholine or noradrenaline and toxin pore-forming [3]. Based on recent studies, the cytolytic effects of the cytotoxic activity of Lionfish (Pterois volitans) from Indian waters, were able to reduce the growth of tumor cells (Erlich's Ascites Carcinoma cells). Protein with a molecular weight 7.6 kDa was isolated from crude venom and tested to tumor cells, and the results showed that there is antitumor activity [4]. The reduction of tumor cells was caused by cytotoxic activity found in P. volitans venom. The toxins play an indirect role in destroying the microenvironment where the tumor cells grow and induce an apoptosis mechanism, which is causing DNA fragmentation by activating the caspases enzyme in tumor cells [5]. Apoptosis activity that occurs in cancer cells was created because P. volitans venom activates caspase-8, which can activate procaspase-3 to activate caspase-3 [6]. However, although the effect of P. volitans venom on tumor cells line was demonstrated over twelve years ago, little attention has been paid to the process of isolating the antitumor protein. One of the conventional protein isolation methods is precipitating protein using ammonium sulfate. Lionfish protein isolation using ammonium sulfate has been done before by Savitri, et al. to observe the phospholipase A2 (PLA2) activity on Lionfish venom [7]. However, the effects of ammonium sulfate concentration added for isolating the antitumor protein is never explained. The present paper explains the effects of ammonium sulfate concentration on the protein of P. volitans venom isolation on an antitumor test and evaluates the activity and the content of its antitumor protein.

MATERIAL AND METHODS Pterois volitans The specimens of Pterois volitans were obtained from around the Indonesian oceans. Lionfish was killed (by cooling), and the venomous spines were removed and washed with 0.1 M phosphate buffer (pH 7.0) and 0.01 M CaCl 2. P. volitans was chosen for this experiment because it is one of the most invasive species and its a common in Indonesia.

HeLa Cell Culture The tumor cells line that was chosen for this research is HeLa cells. HeLa cells culture was obtained from Indonesia International Institute for Life Sciences (I3L, Indonesia). HeLa cells that used for this research were harvested when it reached its log phase. Venom isolation on an antitumor test and evaluates the activity and the content of its antitumor protein.

Extracting The Crude Venom P. volitans spines were extracted using the methods described by [7]. Briefly, the spines (taken from upper dorsal, bottom and back fins) were measured and soaked in 0.1 M phosphate buffer pH 7.0 (which have mixed by CaCl 2 solution with the ratio between phosphate buffer and CaCl2 added is 1:10). The ratio between the weight of spines and the phosphate buffer solution added was 1:2. The spines that have soaked in phosphate buffer solution were sonicated for 16 minutes (with frequency 20 kHz). The extract was centrifuged at 4,500 rpm for 30 minutes. The supernatant (crude venom) was obtained from this process.

Isolating Protein Using Ammonium Sulfate Precipitation The ammonium sulfate was added to crude venom that obtained from the extraction process. This process was done to obtain the protein precipitate from crude venom. The crude venom was aliquoted into five individual volumes (5 mL). 20%, 40%, 60%, and 80% saturated ammonium sulfate was added to each 5 mL of crude venom (the amount of ammonium sulfate that should be added was referred to ammonium sulfate saturation table by [8] and then stirred

030009-2 with vortex or stirrer for 30 minutes. The protein precipitate was separated by removing the supernatant after the centrifugation process at 4,500 rpm for 30 minutes. The amount of saturated ammonium sulfate added to obtain protein precipitate become the independent variables of this experiment

Protein Concentration Measurement The protein concentration of each sample was measured by the Lowry test. The measurement of protein concentration was used to make sure the precipitate that obtained in the previous step is protein. The protein concentration was obtained from five samples. These samples were crude venom (CV), protein precipitate from the addition of 20%, 40%, 60% and 80% saturated ammonium sulfate (AS20%, AS40%, AS60% and AS80%). All of five samples were added by 5 mL biuret reagent and incubated for 10 minutes. 0.5 mL of Folin-Ciocalteu reagent was added to the samples that have incubated. The absorbance of the samples was measured with wavelength 750 nm, and then the data were plotted to Lowry’s curves standard to obtain the protein concentration of the samples.

Measurement of LC50 using Brine Shrimp Lethality Test The procedures of LC50 measurement were referred to [9]. The measurement of LC50 was done to check the activity of a bioactive compound that contains protein precipitate. Briefly, each of the samples (AS20%, AS40%, AS60%, and AS80%) were diluted into several concentrations (10, 100, 500, and 1000 ppm) by using seawater. Samples that have been diluted into several concentrations were tested to ten A. salina larvas which have hatched for 2x24 h. A. salina larvas were obtained and hatched by Biofarmaka Laboratory, Institut Pertanian Bogor (West Java, Indonesia). The data of the amount of death larva collected after the samples incubate for 24 hours. To obtain the value of LC50, the amount of death larva was calculated using probit analysis regression methods [10], and the activity of the bioactive compound was evaluated using Clarkson’s toxicity index [11].

Identification of Protein Molecular Weight using SDS-PAGE Five samples (CV, AS20%, AS40%, AS60%, and AS80%) were tested using SDS-PAGE to identify the molecular weight of protein precipitate samples. Each of the samples was heated at 100°C for 45 seconds to break the protein binding. 4μL phosphate-buffered saline and 5μL sample buffer was added to 5μL samples (CV, AS20%, AS40%, AS60%, and AS80%) that have heated first. The samples were run into the SDS-PAGE with power 150 V for 1 hour. Running buffer was released, and the gel was taken away from the SDS-PAGE set. Then, the staining process using the coomassie blue and the destaining process using methanol were done. The molecular weight of the protein was determined by comparing the sample gel and the marker protein.

Microculture Tetrazolium Salt Assay (MTT Assay) MTT assay used for evaluating the antitumor effect of samples. The procedures used for this experiment were referred to as CellTiter 96° Nonradioactive Cell Proliferation Assay Instruction. Promega G400 used as a reagent in this assay. Each of samples (CV, AS20%, AS40%, AS60%, and AS80%) was diluted into several concentrations (2, 250, 500 and 2500 ppm) using DMEM, PenStrep and FBS 0.5% solution. 2 x 10 4 of log-phase HeLa cells were seeded into each well and incubated a day prior to treatment with lionfish venom samples. After the cells were treated with different concentrations of the samples, they were incubated for another 20 hours. MTT dye solution was then added into each well and incubated for 4 hours before the stop solution was added. One hour later, the absorbance values at 570nm of each well were then recorded. All treatments were done in duplicate wells. Cell viability was calculated by dividing the absorbance value of each sample concentrations with the absorbance value of untreated HeLa cells.

RESULTS Protein Concentration The protein concentration raised along with the increase of the amount of saturated ammonium sulfate added. The protein precipitate sample obtained from protein isolation using 80% saturated ammonium sulfate (AS80%) resulted in the highest protein concentration.

FIGURE 1. The graphic showed the effects of protein concentration obtained vs. the variation of the amount of saturated ammonium sulfate added. The values attached to the graph were the protein concentration value obtained.

However, the lowest protein concentration was obtained by the protein precipitate sample that was isolated using 20% saturated ammonium sulfate (AS20%). The higher addition of saturated ammonium sulfate added caused the increase of protein concentration slightly. Compared to crude venom sample, samples that isolated using high amount of ammonium sulfate gave a higher result of protein concentration (Figure 1), it’s because the crude venom samples have not gone through the purification process before, so there are still many impurities that inhibit the reaction between the Lowry reagent and protein in crude venom sample.

Lethal Concentration 50 (LC50) LC50 values obtained from Brine Shrimp Lethality Test (BSLT) data. All of the samples (AS20%, AS40%, AS60%, and AS80% that tested to a salina larvas showed the toxicity activity. The toxicity activity indicated that the bioactive compound in the sample was active and the protein isolation process using ammonium sulfate precipitation succeed in precipitate protein, which there was a bioactive compound. TABLE 1. The LC50 value and toxicity level of P. volitans protein venom sample Protein Sample LC50 (ppm) Toxicity Level AS20% 796.66 Less Toxic AS40% 300.01 Moderate Toxic AS60% 196.28 Moderate Toxic AS80% 101.93 Moderate Toxic

The LC50 value that showed on the Table 1 was calculated using probit analysis regression method. The toxicity level of the sample was evaluated using the Clarkson toxicity index [11]. Based on LC50 results, all of the samples

030009-4 categorized as toxic by Clarkson toxicity index. The toxicity rate increased moderately along with the rise of the amount of saturated ammonium sulfate added to crude venom. The lower LC50 value indicated the higher level of toxicity and the higher activity of the bioactive compound. AS80% sample resulted in the highest toxicity level, which categorizes ad moderate toxic. On the other hand, the AS20% sample was the sample with the lowest toxicity level.

Protein molecular weight P. volitans protein venom sample that was tested (CV, AS20%, AS40%, AS60%, and AS80%) produced protein bands on an SDS-PAGE gel. The thickest protein band generated by AS40%, AS60%, and AS80% sample. The thickest protein band obtained showed the more protein contained in the sample. A protein band of AS20% and CV samples were not clear because the protein content in the sample was low (not as high as AS40%, AS60%, and AS80% sample). Therefore the molecular protein weight could not be determined.

FIGURE 2. SDS-PAGE gel result contained protein bands that were separated based on its molecular weight. (A) is CV sample, (B) AS20%, (C) AS40%, (D) AS60% and (E) AS80%. Protein molecular weight was determined by comparing the protein band that was formed with a protein marker. TABLE 2. Protein identification results based on its molecular weight Protein Molecular Weight Name, function

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# 硫酸铵浓度对狮子鱼(Pterois volitates)棘刺毒液提取物蛋白质分离用于抗肿瘤测试的影响

引用格式:AIP Conference Proceedings 2193, 030009 (2019); https://doi.org/10.1063/1.5139346 在线发表日期:2019年12月10日

Andy Noorsaman Sommeng, Adinda Kemala Eka, Mikael Januardi Ginting, Sonya Pebriani, Muhamad Sahlan, Heri Hermansyah, Anondho Wijanarko

**摘要.** 狮子鱼(*Pterois volitans*)是印度洋-太平洋海域的本土物种。该物种被视为入侵性极强的破坏性物种,已入侵多个区域。狮子鱼的入侵对入侵地区的生态环境和经济状况造成了负面影响。因此,为减少海洋中狮子鱼的数量并鼓励人们开发利用狮子鱼,研究狮子鱼的利用价值十分必要。近期研究表明,狮子鱼棘刺中的毒液提取物具有潜在的溶细胞效应,广泛应用于抗肿瘤研究。在本研究中,为获得蛋白质分离所用溶剂的最佳浓度,并进一步观察狮子鱼的抗肿瘤特性,我们采用硫酸铵对狮子鱼毒液提取物中的蛋白质进行分离,并以HeLa细胞作为肿瘤细胞模型进行测试。Lowry法和BSLT(卤虫致死试验)结果表明,当使用最高浓度的硫酸铵分离粗毒液时,蛋白质浓度和活性均达到最高值。在最高剂量下,狮子鱼蛋白质分离物对HeLa细胞的抑制率达到17-19%。事实上,由于SDS-PAGE结果显示狮子鱼毒液蛋白质分离物中含有多种对肿瘤细胞具有不同效应的蛋白质,因此消除这些蛋白质可能会增强狮子鱼毒液蛋白质对肿瘤细胞的抑制效果。上述结果表明,狮子鱼具有抗肿瘤效应,但需要进一步的纯化步骤,并对狮子鱼毒液提取物中能够增强抗肿瘤效应的蛋白质进行更多评估。

**关键词:** 抗肿瘤;狮子鱼;蛋白质分离

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## 引言

近年来,毒液作为一种替代疗法因其在肿瘤或癌症等多种慢性疾病中的治疗作用而受到广泛关注,具有一定的经济和生态效益。狮子鱼(*Pterois volitans*)是印度洋-太平洋海域的本土鱼类物种,也是海洋中的入侵物种之一。狮子鱼的高繁殖率和广泛分布导致其入侵范围不断扩大。自首次发现狮子鱼以来,二十年间其入侵区域已扩展至大西洋西部大部分地区,包括佛罗里达、巴哈马、古巴、多米尼加共和国、波多黎各、大部分小安的列斯群岛、开曼群岛、牙买加、哥伦比亚、哥斯达黎加、伯利兹、委内瑞拉和墨西哥[1]。

然而,已发现*P. volitans*的入侵对海洋生态系统造成了一些负面影响。*P. volitans*种群的增长减少了本地鱼类的种群数量,从而影响了入侵地区的经济状况。*P. volitans*在美国的入侵已造成高达1200亿美元的经济损失[2]。在加勒比群岛,*P. volitans*种群失控也对珊瑚礁和海洋生态系统造成了破坏。加勒比群岛旅游业的收入下降了2-5%,估计损失达1亿至3亿美元[3]。

降低*P. volitans*种群数量的方法之一是将其转化为有用的资源。*P. volitans*产生的毒素具有心血管、神经肌肉和溶细胞效应(导致细胞死亡),这些效应与某些毒性蛋白质及其他活性成分(如乙酰胆碱、去甲肾上腺素和毒素成孔蛋白)的存在有关[3]。根据近期研究,来自印度海域狮子鱼(*Pterois volitans*)的细胞毒性活性能够抑制肿瘤细胞(艾氏腹水癌细胞)的生长。从粗毒液中分离出分子量为7.6 kDa的蛋白质并测试其对肿瘤细胞的作用,结果显示其具有抗肿瘤活性[4]。

肿瘤细胞的减少是由*P. volitans*毒液中的细胞毒性活性引起的。毒素通过间接破坏肿瘤细胞生长的微环境并诱导凋亡机制发挥作用,即通过激活肿瘤细胞中的半胱天冬酶(caspase)引起DNA片段化[5]。癌细胞中发生的凋亡活性是由于*P. volitans*毒液激活了caspase-8,后者可激活procaspase-3进而激活caspase-3[6]。

然而,尽管*P. volitans*毒液对肿瘤细胞系的作用在十多年前已被证实,但对抗肿瘤蛋白质的分离过程关注甚少。传统的蛋白质分离方法之一是使用硫酸铵沉淀法。Savitri等人此前已采用硫酸铵对狮子鱼蛋白质进行分离,以观察狮子鱼毒液中磷脂酶A2(PLA2)的活性[7]。然而,用于分离抗肿瘤蛋白质的硫酸铵浓度的影响从未被阐明。本文阐述了硫酸铵浓度对*P. volitans*毒液蛋白质分离在抗肿瘤测试中的影响,并评估了其抗肿瘤蛋白质的活性和含量。

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## 材料与方法

### 狮子鱼(*Pterois volitans*)

*Pterois volitans*样本采集自印度尼西亚周边海域。狮子鱼通过冷却方式处死后,取下毒棘并用0.1 M磷酸盐缓冲液(pH 7.0)和0.01 M CaCl₂清洗。选择*P. volitans*作为实验对象是因为它是最具入侵性的物种之一,且在印度尼西亚较为常见。

### HeLa细胞培养

本研究选用的肿瘤细胞系为HeLa细胞。HeLa细胞培养物取自印度尼西亚国际生命科学研究所(I3L, Indonesia)。当HeLa细胞达到对数生长期时进行收获,用于毒液分离的抗肿瘤测试及其抗肿瘤蛋白质活性和含量的评估。

### 粗毒液的提取

*P. volitans*棘刺的提取方法参照文献[7]。简言之,取棘刺(来自背鳍上部、底部和背部鳍),测量后浸泡于0.1 M磷酸盐缓冲液(pH 7.0)中(该缓冲液已按磷酸盐缓冲液与CaCl₂溶液1:10的比例混合)。棘刺重量与磷酸盐缓冲液体积之比为1:2。浸泡于磷酸盐缓冲液中的棘刺超声处理16分钟(频率20 kHz)。提取液在4,500 rpm下离心30分钟。上清液即为粗毒液。

### 硫酸铵沉淀法分离蛋白质

向提取过程中获得的粗毒液中加入硫酸铵,以从粗毒液中获得蛋白质沉淀。将粗毒液分装为五份等体积样品(各5 mL),分别向每份5 mL粗毒液中加入20%、40%、60%和80%饱和度的硫酸铵(硫酸铵加入量参照文献[8]的硫酸铵饱和表),然后用涡旋振荡器或搅拌器搅拌30分钟。在4,500 rpm下离心30分钟后,去除上清液,分离得到蛋白质沉淀。加入的饱和硫酸铵量作为本实验的自变量。

### 蛋白质浓度测定

各样品的蛋白质浓度通过Lowry法测定。蛋白质浓度测定用于确认上一步获得的沉淀为蛋白质。共测定五个样品的蛋白质浓度:粗毒液(CV),以及分别加入20%、40%、60%和80%饱和硫酸铵获得的蛋白质沉淀(AS20%、AS40%、AS60%和AS80%)。向所有五个样品中加入5 mL双缩脲试剂,孵育10分钟。然后向已孵育的样品中加入0.5 mL Folin-Ciocalteu试剂。在750 nm波长下测定样品的吸光度,将数据绘制至Lowry标准曲线以获得各样品的蛋白质浓度。

### 半数致死浓度(LC₅₀)测定——卤虫致死试验(BSLT)

LC₅₀测定方法参照文献[9]。LC₅₀的测定用于检测含蛋白质沉淀的生物活性化合物的活性。简言之,将各样品(AS20%、AS40%、AS60%和AS80%)用海水稀释为不同浓度(10、100、500和1000 ppm)。将稀释后的样品分别加入已孵化2×24小时的10只卤虫(*A. salina*)幼虫中进行测试。*A. salina*幼虫由茂物农业大学(西爪哇,印度尼西亚)生物农药实验室提供并孵化。在样品孵育24小时后收集死亡幼虫数量数据。采用概率单位分析回归法[10]计算死亡幼虫数量以获得LC₅₀值,并采用Clarkson毒性指数[11]评估生物活性化合物的活性。

### SDS-PAGE蛋白质分子量鉴定

对五个样品(CV、AS20%、AS40%、AS60%和AS80%)进行SDS-PAGE测试,以鉴定蛋白质沉淀样品的分子量。将各样品在100°C下加热45秒以破坏蛋白质结合。向5 μL已加热的样品(CV、AS20%、AS40%、AS60%和AS80%)中加入4 μL磷酸盐缓冲液和5 μL样品缓冲液。在150 V电压下进行SDS-PAGE电泳1小时。释放电泳缓冲液,从SDS-PAGE装置中取出凝胶。随后进行考马斯蓝染色和甲醇脱色处理。通过与蛋白质标记物对比凝胶条带确定蛋白质分子量。

### 微培养四唑盐测定法(MTT法)

MTT法用于评估样品的抗肿瘤效应。实验步骤参照CellTiter 96®非放射性细胞增殖测定说明书。本实验使用Promega G400作为试剂。将各样品(CV、AS20%、AS40%、AS60%和AS80%)用DMEM、PenStrep和0.5% FBS溶液稀释为不同浓度(2、250、500和2500 ppm)。将2×10⁴个对数生长期的HeLa细胞接种于各孔中,在用狮子鱼毒液样品处理前一天进行孵育。细胞经不同浓度样品处理后,继续孵育20小时。然后向各孔中加入MTT染料溶液,孵育4小时后加入终止溶液。1小时后记录各孔在570 nm处的吸光度值。所有处理均设双复孔。细胞活力通过将各浓度样品的吸光度值除以未处理HeLa细胞的吸光度值计算得出。

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## 结果

### 蛋白质浓度

蛋白质浓度随加入的饱和硫酸铵量的增加而升高。使用80%饱和硫酸铵(AS80%)进行蛋白质分离获得的蛋白质沉淀样品具有最高的蛋白质浓度。

**图1.** 蛋白质浓度随加入的饱和硫酸铵量变化的关系图。图中附值为所获得的蛋白质浓度值。

然而,使用20%饱和硫酸铵(AS20%)分离的蛋白质沉淀样品蛋白质浓度最低。饱和硫酸铵加入量的增加使蛋白质浓度略有升高。与粗毒液样品相比,使用高浓度硫酸铵分离的样品蛋白质浓度更高(图1),这是因为粗毒液样品此前未经过纯化过程,仍存在许多杂质,抑制了Lowry试剂与粗毒液中蛋白质之间的反应。

### 半数致死浓度(LC₅₀)

LC₅₀值由卤虫致死试验(BSLT)数据获得。所有样品(AS20%、AS40%、AS60%和AS80%)在卤虫幼虫测试中均显示出毒性活性。毒性活性表明样品中的生物活性化合物具有活性,且使用硫酸铵沉淀法进行蛋白质分离的过程成功沉淀了含有生物活性化合物的蛋白质。

**表1.** *P. volitans*毒液蛋白质样品的LC₅₀值和毒性水平

| 蛋白质样品 | LC₅₀ (ppm) | 毒性水平 | |---|---|---| | AS20% | 796.66 | 低毒 | | AS40% | 300.01 | 中等毒性 | | AS60% | 196.28 | 中等毒性 | | AS80% | 101.93 | 中等毒性 |

表1中显示的LC₅₀值采用概率单位分析回归法计算。样品的毒性水平采用Clarkson毒性指数[11]评估。根据LC₅₀结果,所有样品按Clarkson毒性指数均归类为有毒。毒性水平随加入粗毒液中的饱和硫酸铵量的增加而适度升高。LC₅₀值越低,表明毒性水平越高,生物活性化合物的活性越强。AS80%样品的毒性水平最高,归类为中等毒性。而AS20%样品的毒性水平最低。

### 蛋白质分子量

经测试的*P. volitans*毒液蛋白质样品(CV、AS20%、AS40%、AS60%和AS80%)在SDS-PAGE凝胶上产生了蛋白质条带。AS40%、AS60%和AS80%样品产生的蛋白质条带最浓。蛋白质条带越浓,表明样品中蛋白质含量越高。AS20%和CV样品的蛋白质条带不清晰,因为样品中蛋白质含量较低(不如AS40%、AS60%和AS80%样品高),因此无法确定蛋白质分子量。

**图2.** SDS-PAGE凝胶结果,显示按分子量分离的蛋白质条带。(A)为CV样品,(B)为AS20%,(C)为AS40%,(D)为AS60%,(E)为AS80%。蛋白质分子量通过与蛋白质标记物对比所形成的蛋白质条带确定。

**表2.** 基于分子量的蛋白质鉴定结果

| 蛋白质分子量 | 名称、功能 | |---|---|