Bioactive Potential of Turbinaria Conoides (J Agardh) Kuetz: In vitro and In vivo
Ponnan Arumugam1*, Marudhamuthu Murugan2 and Kadarkarai Murugan1
1Department of Zoology, Bharathiar University, India
2Department of Microbial Technology, Madurai Kamaraj University, India
Submission: May 16, 2018; Published: June 14, 2018
*Corresponding author: Ponnan Arumugam, Department of Zoology, School of Life Science, Bharathiar University, Coimbatore, Tamil Nadu, Pin: 641046, India, Mobile No. +91-8939433020 Email: ponnanarumugam@gmail.com
How to cite this article: Ponnan Arumugam, Marudhamuthu Murugan, Kadarkarai Murugan. Bioactive Potential of Turbinaria Conoides (J Agardh) Kuetz: In vitro and In vivo. Mod Appl Bioequiv Availab. 2018; 3(5): 555625.
Abstract
Brown seaweeds including Turbinaria conoides have been used as food since ancient times which are widely consumed in Asian region than that of in Europe and America. Though, the chemical composition varies with species, habitat, maturity and environmental conditions however they are excellent sources for the bioactive phytochemicals with rich dietary fiber, minerals, non-digestible polysaccharides and capacity to absorb inorganic substances from their surroundings. The main bioactive phytochemicals are steroids, phenolics, flavonoids, reducing sugars, fucosterol, sulfated polysaccharides including fucoidan, neutral glucan, guluronic and alginic acid. These phytochemicals are responsible for the following biological properties such as antioxidant, anti-inflammatory, antimicrobial, and anti-cancer. Therefore, in the present work was clearly documented about the bioactive potential of T. conoides with respect to their phytochemicals in both model of in-vitro and in-vivo.
Keywords: Brown algae; Turbinaria conoides; Phytochemicals; Biological activities
Introduction
It is well known that marine algae have budding source because of their numerous health-promoting effects including antioxidant, anti-inflammatory, antimicrobial, and anti-cancer [1,2]. Particularly, brown seaweeds gripped with rich novel antioxidants which are more acceptable than synthetic /chemical components [3]. Henceforth, marine macroalgae are believed to exhibit potent biological impact especially due to phenolic compounds as well as carotenoids, ascorbic acid, glutathione, sulphated polysaccharides, fucoxanthin, astaxanthin, polyphenols, phlorotannins, phospholipids, flavonoids, bromophenols and so on [4,5]. This rich bioactive phytochemicals are also there pretty in Turbinaria. It is brown algae belong to the family of Sargassaceae (brown algae) under the order of Fucales. It is consist of only 22 species so far described in which highest diversity was found in south west Asia akin to India, Srilanka where documented around 14 species. T. turbinate was only present in the Atlantic Ocean where as three species such as T. conoides, T. decurrens and T. ornate found in the South Pacific Ocean [6]. It traditionally been used as a fertilizer, insect repellent, pesticide, anti-bacterialcidal and also antioxidant, anti-inflammatory, and anti-cancer due to bioactive phytochemicals [7,8]. Apart, essential components digestible proteins along with mineral salts (K, Ca, and Fe) and polyunsaturated fatty acids along with wealthy source of dietary fiber and iodine content which play an immense role in enhancing the food quality and biochemical homeostasis [9]. Therefore, in the present review work was aimed to illustrate the potential biological properties of T. conoides with respect to their phytochemicals in both model of in-vitro and in-vivo.
Antioxidant and its phytochemicals
Various methods are essential to give an overall idea about the broad spectrum of antioxidant activity of phyto/chemical components [10]. Radical scavenging is one of the most powerful mechanisms by which antioxidants inhibit oxidation process. Many in-vitro methods has been used to examine scavenging of free radicals in which most often used are ABTS Radical cation, DPPH radical, and reactive oxygen species (ROS), such as superoxide anion, hydrogen peroxide, peroxyl radicals, hydroxyl radical, singlet oxygen and peroxynitrite. ROS are responsible for oxidative damage in the human body as well as in the food samples [11]. ABTS oxidized to give the radical cation (ABTS.+) as blue in colour and decolorized by water-soluble and lipid-soluble food samples/extracts and is expressed as TEAC (Trolox equivalent antioxidant capacity) [12,13]. Using the method, total antioxidant activity (TAA) of T. conoides was documented in the range 46-85% in hexane, dichloromethane, ethyl acetate and aqueous fraction (Table 1). Relative antioxidant activity (RAA) was also found ≥1 in the ethyl acetate fraction than that of other fractions. Apart, the highest superoxide radical scavenging activity was reported in ethyl acetate fraction (77% at the 80μg/ml) and better than ascorbic acid (74% at 30μg/ml) [14].
In general, metal ions (Fe2+) can also kindle and speed up oxidative damage later on leads to lipid peroxidation which is inhibited by chelators either decreasing metal reactivity or by physically partitioning the metal away from the lipids [15]. It is well know that bioactive compounds like phenolic acids, flavonoid, quercetin, and phenolic glycosides are potentially participate to chelate metal ions which is determine by Spectrophotometry [10]. Iron chelation and uric acid inhibition activities of ethyl acetate fraction of T. conoides were reported in the range of 15-70% [14]. The reducing capacity assay is one of the methods to reduce the oxidative damage by inhibiting the peroxidation process. This process can be done by low molecular weight antioxidants which is able to donate electrons to reactive oxygen species. It can be determined by simple methods:
- a) The FRAP assay, based on the reduction of the Fe3+/ tripyridyltriazine complex [16],
- b) The direct reduction of Fe3+ ferricyanide complexes and
- c) Electrochemical methods [17,18]. Reducing power exhibited by solvent extracts of Turbinaria spp. was comparatively higher than α-tocopherol [19].
Antimicrobial and its phytochemicals
Antimicrobial properties of T. conoides were determined by disc diffusion method which was well documented by many research articles (Table 1). Arumugam P et al. [14] reported that among the four solvent fractions of T. conoides, ethyl acetate fraction exhibited highest antibacterial activity which was comparable to the standard, streptomycin against Bacillus subtilis, Enterococcus faecalis and Pseudomonas aeruginosa. Similarly, out of four solvent fractions, petroleum ether extract reported to be showed effective antibacterial activity [20]. The antimicrobial activity of T. conoides was also reported in dose dependent activity of all four extracts and highest activity exhibited at 500μg/mL [21]. It is mainly due to secondary metabolites like phenolic compounds which may explore inhibiting effect on microbial growth based on their chemical constitutions and concentrations [22]. Consecutive extraction of T. conoides with n-hexane, cyclohexane, methanol and ethanol: water (1:1) was also documented with their antibacterial and antifungal activities by disc diffusion method. In which, cyclohexane extract was possessed a broad array of antibacterial activity and exhibited remarkable antifungal property over the other extracts [23]
Anti-inflammatory, anti-genotoxicity and its phytochemicals
During the oxidative damage of cell or tissue, several inflammatory mediators such as histamine, bradykinin, serotonine, and prostaglandins are released and stimulate the inflammation and nociceptors by the induction of pain [24]. These mediators are occupied in tissues with high content of water and plasma during arachidonic acid metabolism via cyclo-oxygenase and lipo-oxygenase enzyme pathways [25]. The first phase of inflammation begins immediately up to an hour after injection of carrageenan by the release of histamine and serotonin whereas the second phase started after one hour and up to three hours by the release of bradykinin, protease and prostaglandins [26]. Antiinflammatory effect of ethyl acetate fraction of T. conoides were reported to be significantly (P < 0.05) better than that of control and indomethacin (Table 1). The reduction of paw volume was found to be dose dependent. The acetic acid induced abdominal writhes in mice were recovered significantly from all the tested doses of T. conoides. Ethyl acetate fraction of T. conoides might have capable of reduce inflammation through stabilizing the lysosomal membrane. In addition, the analgesic effect of T. conoides on the tail immersion-test in mice was found to be dose dependent and significantly reduce the pain response by the increase of reaction [27]. Recent report on T. ornate extract revealed their better anti-inflammatory and free radical scavenging property due to fucoidan like sulfated polysaccharides [28]. T. conoides reported to have better antipyretic activity by restoring many hematological and biochemical parameters under toxic environment [29]. In general, exposure of any environmental toxin/genotoxin leads to genetic damage which is determined by mouse bone marrow micronucleus assay described by [30]. For each bone marrow/peripheral blood cells (experimental/control), 2,500 polychromatic erythrocytes (with or without micronuclei) and a corresponding number of normal chromatic erythrocytes (NCEs) were scored under a light microscope. Ethyl acetate fraction of T. conoides reported to be 72% anti-genotoxic activity against 4-NQO induced genotoxicity [27]. These biological activities of T. conoides are mainly due to rich source of bioactive compounds such as fucosterol, sulfated polysaccharides fucoidan, neutral glucan, guluronic and alginic acid [28,31].
Anticancer and its phytochemicals
Cytotoxicity assay has been considered as the cell killing property of a chemical compound which is independent mechanism from the programmed cell death pathway [32]. Cytotoxicity of ethyl acetate fraction of T. conoides was reported to be significant and comparable to the standard of quercetin (Table1). Hence, cytotoxicity and antioxidant of T. conoides were well correlated and concentration dependent. The anticancer analysis exhibited that the number of accumulated cancer cells was significantly (p < 0.05) higher in the proliferative G0/ G1 phase and a significant decrease in the S phase, after 48h of treatment with ethyl acetate fraction of T. conoides. Similarly, T. conoides showed (43%) statistically (p < 0.05) significant increase of apoptotic cells than that of quercetin standard (32%, 80 μg/ml) [15]. Other reports revealed that cell cycle arrest leads to increase in sub-G0/G1 cell population after treatment with increasing doses of linalool terpenoid [33]. Cyclohexane extracts of T. conoides exhibited effective cytotoxicity in human embryonic lung cells [24]. Anticancer activity of fucosterols obtained from T. conoides was explored in various cancer cell lines [8]. Steroid from ethyl acetate extract of T. conoides reported to be effective cytotoxic in HeLa cells [34]. Various extract obtained from a variety algae collectively demonstrated that the brown algae have a potential source of phytochemicals exhibiting biological activities on tumor cells [35].
Conclusion
It is well know that T. conoides possess large content of dietary fiber, minerals, steroids, phenolics, flavonoids, reducing sugars, fucosterol, sulfated polysaccharides including fucoidan, neutral glucan, guluronic and alginic acid. As results, it exhibited different biological properties such as antioxidant, antimicrobial, anti-inflammatory and anti-cancer. Many articles revealed that cyclohexane and ethyl acetate extracts/fraction of T. conoides have potential bioactive phytochemicals with different biological properties.
References
- Gupta S, Abu Ghannam N (2011) Recent developments in the application of seaweeds or seaweed extracts as a means for enhancing the safety and quality attributes of foods. Innov Food Sci Emerg Technol 12(4): 600-609.
- Gupta S, Abu Ghannam N (2011) Bioactive potential and possible health effects of edible brown seaweeds. Trends Food Sci Technol 22(6): 315-326.
- Liu L, Heinrich M, Myers S, Dworjanyn SA (2012) Towards a better understanding of medicinal uses of the brown seaweed Sargassum in Traditional Chinese Medicine: a phytochemical and pharmacological review. J Ethnopharmacol 142: 591-619.
- Lee JC, Hou MF, Huang HW, Chang FR, Yeh CC, et al. (2013) Marine algal natural products with anti oxidative anti-inflammatory and anti cancer properties. Cancer Cell Int 13: 55-60.
- Gamze Y, Serap C, Ozgur V, Sukran D (2011) Determination of the antioxidative capacity and bioactive compounds in green seaweed Ulva rigida C. Agardh. Int J Food Prop 11: 44-52.
- Le Lann K, Kraffe E, Kervarec N, Cerantola S, Payri CE, et al. (2014) Isolation of turbinaric acid as a chemomarker of Turbinaria conoides (J. Agardh) Kutzing from south pacific islands. J Phycol 50(6): 1048- 1057.
- Sheu JH, Wang GH, Sung PJ, Duh CY (1999) New cytotoxic oxygenated fucosterols from the brown alga Turbinaria conoides. J Nat Prod 62(2): 224-227.
- Chattopadhyay N, Ghosh T, Sinha S, Kausik C, Karmakar P, et al. (2010) Polysaccharides from Turbinaria conoides: structural features and antioxidant capacity. Food Chem 118(3): 823-829.
- Rajeshkumar S, Malarkodi C, Gnanajobitha G, Paulkumar K, Vanaja M, et al. (2013) Seaweed mediated synthesis of gold nanoparticles using Turbinaria conoides and its characterization. J Nanostructure Chem 3: 44-50.
- Chakraborty K, Praveen NK, Vijayan KK, Syda Rao G (2013) Evaluation of phenolic contents and antioxidant activities of brown seaweeds belonging to Turbinaria spp (Phaeophyta, Sargassaceae) collected from Gulf of Mannar. Asian Paci J Trop Biomed 3(1): 8-16.
- Craft BD, Kerrihard AL, Amarowicz R, Pegg RB (2012) Phenol based antioxidants and the in vitro methods used for their assessment. Comprehen Revi Food Sci Food Safety 11(2): 148-173.
- Cofrades S, López Lopez I, Bravo L, Ruiz Capillas C, Bastida S, et al. (2010) Nutritional and antioxidant properties of different brown and red spanish edible seaweeds. Food Sci Technol Int 16(5): 361-370.
- Elena DRM, Pérez JJ, Saura CF (2009) Dietary fiber and antioxidant capacity in Fucus vesiculosus products. J Int J Food Sci Nutri 60 Suppl 2: 23-34.
- Arumugam P, Kavipriya R, Murugan M, Ramar M, Kamalakannan S, et al. (2017) Antibacterial antioxidant and anticancer properties of Turbinaria conoides (J Agardh) Kuetz. Clin Phytosci 3(5): 1-10.
- Cardenia V, Waraho T, Rodriguez Estrada MR, Julian McClements D,Decker EA (2011) Antioxidant and prooxidant activity behavior of phospholipids in stripped soybean oil-in-water emulsions. J Ameri Oil Chem’ Soci 88(9): 1409-1416.
- Benzie IFF, Szeto YT (1999) Total antioxidant capacity of teas by the ferric reducing / antioxidant power assay J Agri Food Chem 47(2): 633- 636.
- Ragubeer N, Beukes DR, Limson JL (2010) Critical assessment of voltammetry for rapid screening of antioxidants in marine algae. Food Chem 121(1): 227-232.
- https://www.sciencedirect.com/science/article/pii/S0308814609013867
- Kumar CS, Ganesan P, Bhaskar N (2008) In vitro antioxidant activities of three selected brown seaweeds of India. Food Chem 107(2): 707- 713.
- Sridharan MC, Dhamotharan R (2012) Antibacterial activity of marine brown alga Turbinaria conoides. J Chem Pharmaceut Res 4(4): 2292- 2294.
- Senthilkumar P, Sudha S (2012) Antibacterial properties of Turbinaria conoides from Gulf of Mannar Coast. Int J Pharm Sci Rev Res 17(1): 74-76.
- Vijayabaskar P, Shiyamala V (2011) Antibacterial activities of brown marine algae (Sargassum wightii and Turbinaria ornata) from the Gulf of Mannar. Biosphere Reserv Adv Bio Res 5(2): 99-102.
- Shanmugam SK, Kumar Y, Sardar Yar KM, Gupta De, Clercq E (2010) Antimicrobial and cytotoxic activities of Turbinaria conoides (J Agardh) Kuetz. Iran J Pharmaceut Res 9(4): 411-416.
- Hajhashemi V, Ghannadi A, Hajiloo M (2010) Analgesic and anti inflammatory effects of Rosa damascena hydro alcoholic extract and its essential oil in animal models. Iran J Pharmaceut Res 9(2): 163-168.
- Moura ACA, Silva ELF, Fraga MCA, Wanderley AG, Afiatpour P (2005) Antiinflammatory and chronic toxicity study of the leaves of Ageratum conyzoides L in rats. Phytomedicine 12(1-2): 138-142.
- Gupta V, Kumar P, Bansal P, Singh R (2009) Anti-inflammatory and antinociceptive activity of Mitragyna parvifolia. Asian J Med Sci 1(3): 97-99.
- Arumugam P, Murugan M, Ramar M, Murugan K (2016) In-vivo evaluation of antigenotoxic and anti-inflammatory potential of Turbinaria conoides (J. Agardh) Kuetz. Int J Drug Develop Res 8(4): 10-13.
- Ananthi S, Gayathri V, Chandronitha C, Lakshmisundaram R, Hannah R, et al. (2011) Fee radical scancenging and anti-inflammatory potential of a mairne borwn alga Turbinaria ornate (Turner) J Agardh. IJMS 40(5): 664-670.
- Sadish KS, Kumar Y, Khan MS, Anbu J, Sam KG (2009) Acute toxicity study and antipyretic effect of the brown alga Turbinaria Conoides (004A Agardh) Kuetz. Afr J Tradit Complement Altern Med 6(3): 233- 240.
- Schmid W (1975) The micronucleus tests. Mutat Res 31(1): 9-15.
- Ananthi S, Gayathri V, Veeresh Kumar S, Meenakshi B, Vasanthi HR (2016) Attenuation of inflammation by marine algae Turbinaria ornata in cotton pellet induced Granuloma mediated by fucoidan like sulphated polysaccharide. Carbohydrate Polymers 151: 1261-1268.
- Jin X, Chen Q, Tang SS, Zou JJ, Chen KP, et al. (2009) Investigation of quinocetone-induced genotoxicity in HepG2 cells using the comet assay, cytokinesis-block micronucleus test and RAPD analysis. Toxicol In Vitro 23(7): 1209-1214.
- Sun XB, Wang SM, Li T, Yang YQ (2015) Anticancer activity of linalool terpenoid: apoptosis induction and cell cycle arrest in prostate cancer cells. Tropic J Pharmaceut Res 14(4): 619-625.
- Sadish KS, Jayendra (2012) Cytotoxity of marine algal steroids in hela cells - 2D & 3D QSAR approach. Int J Pharm Bio Sci 3(2): 204-212.
- Gambato G, Caroline OS, Frozza ÉG, Baroni MS (2014) Brown algae Himantothallus grandifolius (Desmarestiales, Phaeophyceae) suppresses proliferation and promotes apoptosis-mediated cell death in tumor cells. Adv Bio Chem 14(4): 98-108.