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LC.MS-based chemical profiling of Aristotle's lantern and viscera of the sea urchin Echinometra mathaei collected from the Red Sea and evaluation of their antiviral activity

Future Journal of Pharmaceutical Sciences volume 10, Article number: 113 (2024) Cite this article

Abstract

Background

Echinometra mathaei (family Echinometridae), is one of the sea urchins widely distributed on the Egyptian coasts in the Red Sea. This organism contains edible and non-edible parts. The present study was carried out to analyze and identify the metabolites present in the non-edible parts (Aristotle's lantern and viscera) using LC/MS. Also, the cytotoxic activity on Vero cell line and antiviral activity against herpes simplex virus type 1 were evaluated using MTT colorimetric assay.

Results

Chemical profiling of the crude extracts of Aristotle's lantern and viscera using LC/MS indicated the presence of 51 and 59 compounds, respectively. The main metabolites present in both non-edible parts were phospholipids, amino acids, peptides, fatty acids and glycerol derivatives. However, the characteristic difference was the presence of carotenoid pigments only in viscera. The crude extract of Aristotle's lantern and viscera showed no cytotoxic activity on Vero cell line and significant antiviral activity against herpes simplex virus with an IC50 value equal to 115.48 ± 1.20 and 122.4 ± 0.50 µg/mL, respectively.

Conclusions

In the present study, the crude extracts of the non-edible parts of E. mathaei were analyzed using LC.MS.MS.QTOF and indicated the existence of 110 chemical compounds, with significant antiviral activity against HSV-1 and no cytotoxic activity. The diversity of the identified compounds with two main categories of compounds, phospholipids and peptides, may contribute to the antiviral activity of Aristotle's lantern and viscera. Additionally, this research focused on clarification of nutritive, pharmaceutical and economic values of these parts. As future prospects, further studies are required to isolate the metabolites and assess the detailed mechanism of antiviral activity via in vitro, in vivo and in silico studies.

Background

Natural products isolated from marine sources were characterized by unique structures and diverse biological activities. Several drugs from marine sources with characteristic nucleus as peptides, nucleosides and alkaloids were approved for treatment of several diseases, mainly cancer and viral infections, with high efficacy and lower side effects in comparison with synthetic drugs [1,2,3]. Sea urchins are marine organisms with characteristic spines, and belong to the phylum Echinodermata and a class of echinoidea. They are widely distributed and survive in shallow water and some types survive in enormous depths of oceans and seas. Also, these organisms can adapt and accommodate stressful conditions like salinity, PH and climate changes. Marine algae are considered as the main source of food and nutrients for them [4,5,6]. Sea urchins are considered as one of the important parts of seafood products. They are collected in coastal areas around the world. The only consumed part of sea urchins is the gonads; however, the other parts are non-edible; Aristotle's lantern, viscera and outer shell [6,7,8].

Several types of sea urchins are distributed across the Red Sea coasts and Echinometra mathaei is one of the most widely distributed sea urchins on the Red Sea coasts. Several metabolites have been isolated from the sea urchins, such as naphthaquinones, nucleosides, fatty acids, glycerol derivatives, diterpens, steroids and alkaloids with diverse biological activities as anticancer, antimicrobial, anti-inflammatory, antioxidant, anticoagulant and antitoxic properties [7,8,9,10,11,12,13,14].

Nowadays, viral disease causes several pandemic infections and leads to several deaths all over the world. Herpes simplex viruses (HSVs) belong to the family Herpesviridae and based on the World Health Organization report, HSVs infect 90% of the human population during their lives and cause a lifelong persistent infection in the host [15, 16].

Herpes simplex viruses type-1 commonly cause Herpetic gingivastomatitis typically affects the tongue, lips, gingival, buccal mucosa and in neuropsychiatric disorder mainly Alzheimer's disease. In severe infections lead to encephalitis and meningitis [15,16,17]. Reactivation of HSV-1 in immune-compromised patients can be fatal and lead to death. Additionally, HSV-1 reactivation is associated with an increased risk of mortality and pneumonia in critically ill COVID-19 patients [17, 18].

The development of viral resistance and limited treatment options in some cases encouraged us for searching on more effective therapy. Nowadays, Researchers are focusing their research projects on sea urchin due to its promising pharmacological applications, with diverse and vast medicinal values. There are few reports on the chemical or biological activity of the sea urchins distributed in the Egyptian coasts [11, 12].

In our on-going project toward discovery of bioactive metabolites from sea urchins collected from the Egyptian coasts in the Red Sea and in order to intensify the pharmacological and economic impacts of these organisms, chemical profiling of the Aristotle's lantern and viscera parts of E. mathaei, were analyzed using LC/MS and antiviral activity against HSV-1 were assessed using MTT colorimetric assay.

Material and method

Marine organism’s material

The sea urchin Echinometra mathaei was collected and identified by Dr. Abdallah Alian (Faculty of Science, Al-Azhar University, Assiut branch, Egypt) from the Red Sea in Hurghada, Egypt in a depth (2–6 m). A voucher sample (EM-21) has been deposited at the Pharmacognosy Department, Faculty of Pharmacy, Assiut University, Egypt.

Extraction

Echinometra mathaei (1.2 kg) was first dissected to separate all parts; the weight of Aristotle's lantern and viscera was 76.5 g and 57.4 g, respectively. Aristotle's lantern and viscera were extracted by maceration in 85% methanol under room temperature for 48 h. followed by filtration. This process was repeated till exhaustion. The crude extract of both was evaporated under reduced pressure using a rotary evaporator, resulting in a dry viscous brown residue weighing 3.4 g and 5.0 g for the viscera and Aristotle's lantern, respectively.

LC.MS analysis

LC–MS–MS–Q–TOF was acquired on Agilent (California, USA). The chromatography and mass Spectrometry Conditions, chromatographic column: YMC-Pack ODS-A C18 column (250 × 4.6 mm, 5 μm); mobile phase: water solution(A)/ acetonitrile(B); gradient: 35 min, 90:10(V(A) V(B)); 50:50(V(A) V(B)); 20 min, 25:75(V(A) V(B)); 20 min, 0.0:100 (V(A) V(B)); flow rate: 0.4 mL· min−1; column temperature: 35 °C ± 5 °C; detection wavelength:300 nm and 350 nm. 3.2.2. LC–MS–MS–QTOF mass spectrometry conditions. Mass spectrometry conditions: positive ion modes; tune mass range max: m/z 3200; ESI source spray voltage:1.50 kV; the ionization temperature: 200 °C; fragmentation voltage: 130 detector voltage: 1.65 kV; Separator voltage: 8.5 kV; Pressure in TOF zone: 1.4 × 10–4 Pa; TOF temperature: 40 °C; Ion accumulation time: 10 ms.

Antiviral assay

Cell and virus

Herpes simplex virus -1 (HSV-1) and Vero cell lines were kindly provided by the Microbiology unit Faculty of Medicine. The cells were grown in DMEM supplemented with 10% of FBS, 100 mg/mL of streptomycin, 100 UI/mL of penicillin and 0.25 mg/mL amphotericin B at 37 °C with 5% CO2.HSV-1 virus titter was determined by cytopathic effect (CPE) of in Vero cells.

Cytotoxic assay

The IC50 of crude extract was determined on Vero cell line using MTT (3-(4,5 dimethyl thiazol-2yl) 2,5-diphenyl tetrazolium bromide) colorimetric assay [12, 19, 20].

Briefly, cells were seeded in 96-well plates at densities of 0.5 × 104 cells/well using DMEM medium at a humid atmosphere of 5% (v/v) CO2 and 95% (v/v) air at 37 °C. After 24 h, the cells were treated with crude extracts dissolved in DMSO). After 72 h. Cell viability was determined using MTT reagent as follows: the medium including MTT reagent (5 mg/mL) was added (20 μl) to each well, followed by 4 h incubation at 37 °C, then 100 μl HCl-isopropanol solution was added to each well. After 5 h incubation in a dark place, the absorbance was measured at 560 nm using a Microplate Reader (Bio-Rad, USA).

$$\% \;{\text{Cell}}\;{\text{Viability}}\;\left( {{\text{v}}\% } \right) \, = \frac{{V{ }\;treated{ }}}{{V\;{ }cont.}} \times 100$$

The concentration that reduces viable cells by 50% (CC50) was calculated from the dose response curve using a program based on Microsoft Excel. The procedure was carried out in triplicate.

Antiviral assay

The antiviral activity of the crude extracts of Aristotle's lantern and viscera against HSV-1 were evaluated by testing their virucidal activity using the MTT assay [12, 19, 20].

Briefly, cells were seeded in 96 well plates and incubated for 24 h. The cells were treated with an equal volume (1:1 v/v) of different concentrations of tested sample and the virus suspension for one hour. Add 100 μl from viral/ sample suspension. Place on a shaking table, 150 rpm for 5 min. Incubate (37 °C, 5% CO2) for 24 h. Cell viability was also assessed using MTT assay. The antiviral activity was expressed as % of inhibition using the following formula:

$${\text{Antiviral}}\;{\text{activity}}\left( \% \right) = \left( {{\text{Atv }} - {\text{ Acv}}} \right)/\left( {{\text{Acd }} - {\text{Acv}}} \right) \times 100$$

where Atv, Acv, and Acd represent the absorbance of the test compounds on virus-infected cells, the absorbance of the virus control and the absorbance of the cell control, respectively. The minimum inhibitory concentration IC50 was calculated from the dose response curve using a program based on Microsoft Excel. The procedure was carried out in triplicate.

Results

Accordingly, several chemical compounds were tentatively identified based on the exact HR-ESIMS with error difference in (0.0 to 10 ppm) and compared with previously published literature. The identified metabolites from both parts were 110 compounds, 51 from Aristotle lantern and 59 from viscera.

Chemical profiling of Aristotle's lantern

The compounds identified from LC/MS analysis of the crude extract of Aristotle's lantern was fifty one and listed in (Tables 1, 2, 3, 4 and Fig. 1). The identified compounds were mainly belonged to lipid derivatives, peptides, amino acids and some miscellaneous compounds. The most intense peaks were recorded for N-(2-hydroxyethyl) icosanamide (100%), followed by benzoic acid derivatives methyl orsellinate (97.3%), eicsoatetraenoyl-2-hydroxy-sn-glycero-3-phosphoethanolamine (65.9%) and tetrapeptide ser. (52.5%), respectively.

Table 1 Phospholipids and sphingolipids identified from the Aristotle's lantern of Echinometra mathaei using LC/MS
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Table 2 Glycerol and fatty acid derivatives identified from the Aristotle's lantern of Echinometra mathaei using LC/MS
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Table 3 Peptides, amino acids and their derivatives identified from the Aristotle's lantern of Echinometra mathaei using LC/MS
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Table 4 Miscellaneous compounds identified from the Aristotle's lantern of Echinometra mathaei using LC/MS
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Fig. 1
figure 1

Total compound chromatogram (TCC) of crude extract of Aristotle's lantern of Sea urchin Echinometra mathaei using positive ion mode

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Chemical profiling of viscera

Fifty nine compounds were identified from the crude extract of viscera of E. mathaei as showed in (Tables 5, 6, 7, 8 and Fig. 2) using LC/MS. the identified compounds were mainly lipid derivatives as phospholipids, glycerol (mono, di, tri), fatty acid derivatives, amino acids, peptides and miscellaneous compounds with characteristic existence of three carotenoid pigment in the viscera. The most intense peak was identified as polyhydroxy unsaturated fatty acid named (8Z,12E)-13-(3,5-dihydroxy-2-pentylcyclopentyl)-11-hydroxytrideca-8,12-dienoic acid (100%), followed by 1-(5Z,8Z,11Z,14Z,17Z) eicosapentaenoy-Sn-glycero-3-phosphocholine (80.1%) and 1-O-palmitoyl-2-O-acetyl-sn-glycero-3-phosphorylcholine (48.59%), respectively.

Table 5 Phospholipids and sphingolipids identified from the viscera of Echinometra mathaei using LC/MS
Full size table
Table 6 Glycerol, Fatty acids (FFA) and their derivatives identified from viscera of Echinometra mathaei using LC/MS
Full size table
Table 7 Peptides, amino acids and their derivatives identified from viscera of Echinometra mathaei using LC/MS
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Table 8 Miscellaneous compounds identified from viscera of Echinometra mathaei using LC/MS
Full size table
Fig. 2
figure 2

Total compound chromatogram (TCC) of crude extract of viscera of Echinometra mathaei using positive ion mode

Full size image

Antiviral activity

Cytotoxic activity

Aristotle's lantern and viscera of the sea urchin E. mathaei, showed no cytotoxic activity (Fig. 3 and Table 9) on Vero cell line with IC50 value equal to 407.4 ± 7.08 and 295.3 ± 2.87 μg/mL, respectively, using MTT colorimetric assay.

Fig. 3
figure 3

Cytotoxic activity of the crude extracts of Aristotle lantern (a) and viscera (b) of the sea urchin Echinometra mathaei on Vero cell line

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Table 9 Cytotoxic and antiviral activities of Aristotle's lantern and viscera of Echinometra mathaei on Vero cell line against HSV-1 using MTT assay
Full size table

Antiviral activity against HSV-1

The antiviral activity of the crude extracts of non-edible parts (Aristotle's lantern and viscera) of the sea urchins E. mathaei against HSV-1 was evaluated using MTT colorimetric assay. The Aristotle's lantern and viscera showed promising antiviral activity with an IC50 equal to 115.48 ± 1.20 and 122.4 ± 0.5 μg/mL and selectivity index equal to 3.5 and 2.4, respectively (Table 9).

Discussion

E. mathaei is one of the sea urchins, widely distributed in the Egyptian coasts of the Red Sea, with edible gonads and the non-edible parts. Aristotle's lantern and viscera were subjected for the first time of any sea urchin in the Red Sea to chemical profiling using LC.MS.MS-QTOF.

Several compounds were identified in the crude extract of Aristotle's lantern and viscera of the sea urchin E. mathaei. The main metabolites existed in both non-edible parts were lipid derivatives, mainly phospholipids as phosphocholine, phosphoethanolamine and sphingosine derivatives, fatty acids and glycerol derivatives, followed by peptides, amino acids and miscellaneous compounds [20,21,22]. The unique and significant difference between Aristotle lantern and viscera was the presence of three kind of carotenoid pigments, (3'RS,3'SR)-Astaxanthin, Uriolide and (3S,3'S,5R,5'R,6R)-6,7-Didehydro-5,6-dihydro-3,3',5,8'-tetrahydroxy beta, kappa-caroten-6'-one in viscera only, which illustrate the feeding habits of E. mathaei on the marine algae on the Red Sea. Additionally, the crude extracts of viscera contain three kinds of glycerol derivatives; mono, di and tri, while Aristotle's lantern contains only mono-acyl derivatives. Both parts contain saturated and polyunsaturated fatty acids in their crude extract. Phenyl alanine, leucine rich peptide was common in viscera and serine rich peptide was common in Aristotle's lantern. Also, the antioxidant amino acid glutathione in Aristotle's lantern and methionine in viscera [23, 24].

The promising antiviral activity of the crude extracts of Aristotle's lantern and viscera with no cytotoxic activity with an IC50 equal to 115.48 ± 1.20 and 122.4 ± 0.5 µg/mL, and SI equal to 3.53, 2.41, respectively. This activity may be attributed to the presence of phospholipids and peptides, which constitute the main compositions of Aristotle's lantern and viscera and these results, are consistent with the previous reports [24,25,26,27]. The suggested mechanism of action of peptides and phospholipids may be attributed to inhibiting the viral particle; or attachment to the host cell membrane, interfering in their interaction. Additionally, they exerted their effects via inhibition of gene expression. In conclusion, lipid and peptide derivatives exert their antiviral activity through prevention of entry of enveloped virus as HSV to the cell [28,29,30].

Conclusions

According to the study findings, several metabolites were identified in the crude extract of Aristotle's lantern and viscera using LC/MS. Both extract showing promising antiviral activity against HSV-1. Phospholipids and peptides were the main constituents identified and may participate in the bioactivities. Further isolation of these metabolites, in vivo, in vitro and in silico studies are also needed to clarify the mechanism of action.

Availability of data and materials

The datasets analyzed during the current study will be available from the corresponding author on reasonable request.

Abbreviations

LC.MS.MS.QTOF:

Liquid chromatography. Mass spectrometry. Mass spectrometry. Quadrupole time-of-flight

DMEM:

Dulbecco's Modified Eagle Medium

FBS:

Fetal bovine serum

HSV-1:

Herpes simplex virus type 1.

MTT:

3-(4, 5-Dimethylthiazol-2-yl)-2, 5-diphenyltetrazolium bromide

CC50 :

The concentration of test compounds required to reduce cell viability by 50%

IC50 :

The concentration of antiviral that lowers 50% of the virus-induced cytopathic effect (CPE)

SI:

The ratio of the 50% cytotoxic concentration (CC50) to the inhibitory concentration of 50% (IC50)

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Authors and Affiliations

  1. Department of Pharmacognosy, Faculty of Pharmacy, Assiut University, Assiut, 71526, Egypt

    Yousra A. Abdelaziz, Ahmed A. A. Ibrahim & Ezz-Eldin K. Desoky

  2. Pharmacognosy and Natural Products Department, Faculty of Pharmacy, Menoufia University, Shibin-Elkom, 32512, Egypt

    Iman S. A. Khallaf

  3. Zoology Department, Faculty of Science, Al-Azhar University, Assiut, 71524, Egypt

    Abdallah Alian

  4. Department of Pharmacognosy, Faculty of Pharmacy, Al-Azhar University, Assiut, 71524, Egypt

    Fahd M. Abdelkarem

  5. Department of Agro-Environmental Sciences, Graduate School of Bioresources and Bioenvironmental Sciences, Kyushu University, Fukuoka, 819-0395, Japan

    Fahd M. Abdelkarem

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Contributions

All the authors contributed in the design of the study. Yousra A Abdelaziz contributed to the literature search, data interpretation, data analysis, and writing. Iman S.A. Khallaf contributed to the data analysis and data interpretation. Fahd M. Abdelkarem contributed to the data analysis and data interpretation and writing. Abdallah Alian collected, identified the sea urchin E. mathaei and writing. Ahmed A A Ibrahim and Ezz-Eldin K. Desoky contributed to revising the work and approved its submission. All authors read and approved the final manuscript.

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Abdelaziz, Y.A., Khallaf, I.S.A., Alian, A. et al. LC.MS-based chemical profiling of Aristotle's lantern and viscera of the sea urchin Echinometra mathaei collected from the Red Sea and evaluation of their antiviral activity. Futur J Pharm Sci 10, 113 (2024). https://doi.org/10.1186/s43094-024-00687-1

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