In Vitro Cytotoxicity and Antioxidative Potential of Nostoc Microscopicum (Nostocales, Cyanobacteria)
DOI:
https://doi.org/10.17140/TFMOJ-1-102Keywords:
Cyanobacteria, Nostoc microscopicum, Cyanotoxins, Cytotoxicity, Antioxidant activityAbstract
Many cyanobacterial species (cyanoprokaryotes, blue-green algae) are potent producers of various secondary metabolites with low molecular weight and diverse biological activities (anti tumor, antimycotic, antiviral, antimicrobial, immunomodulatory, enzyme inhibition, cytotoxic activity). They have the potential to serve as convenient source of active substances for new medications and other commercial products. Therefore, cyanobacteria have become an object of intense scientific interest. New findings have shown that different cyanoprokaryotic species produce compounds with antioxidant activity. Also, there are reports for successful clinical trials using antitumor agents that contain active substances isolated from these organisms. On the other hand, it is well known that certain cyanobacteria produce toxins that could harm plants, animals and humans. Some cyanotoxins induce severe injuries even by contact with polluted water while washing or swimming. Hence, cyanotoxins production must be analyzed for all widely distributed cyanoprokaryotic species as well as those with potential application in medical practice. Certain species of the genus Nostoc are well known producers of substances with antitumor, enzyme inhibition, immunomodulatory, antioxidant or cytotoxic activities. However, little is known about the species Nostoc microscopicum. Therefore, the aim of the present study was to evaluate the antioxidant activity and potential cytotoxic effects of Nostoc microscopicum using extracts derived with different solvents. We show a moderate antioxidant activity of different Nostoc microscopicum extracts and prominent cytotoxic activity against several human cell lines (HeLa, FL, A549). Our results determine Nostoc microscopicum as interesting source of active compounds for pharmacology and biotechnology. In addition, this report presents for the first time an evidence for saxitoxins and microcystins production by Nostoc microscopicum and highlights the toxicological importance of this cyanobacterial species.
References
Li H, Cheng K, Wong C, Fan K, Chen F, Jiang Y. Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae. Food Chemistry. 2007; 102(3): 771-776. Web site. http://agris.fao.org/agris-search/search. do?recordID=US201300754077. July 13, 2016
Pant G, Kumar G, Karthik L, Gyana Prasuna R, Bhaskara Rao KV. Antioxidant activity of methanolic extract of blue green algae Anabaena sp. (Nostocaceae). J Exp Biol. 2011; 1(1): 156- 162.
Goiris K, Muylaert K, Fraeye I, Foubert I, De Brabanter J, de Cooman L. Antioxidant potential of microalgae in relation to their phenolic and carotenoid content. J Appl Phycol. 2012; 24(6): 1477-1486. doi: 10.1007/s10811-012-9804-6
Shanab SM, Mostafa S, Shalaby EA, Mahmoud G. Aque-ous extracts of microalgae exhibit antioxidant and anticancer activities. Asian Pac J Trop Biomed. 2012; 2(8): 608-615. doi: 10.1016/S2221-1691(12)60106-3
Hajimahmoodi M, Faramarzi MA, Mohammadi N, Soltani N, Oveisi MR, Nafissi-Varcheh N. Evaluation of antioxidant prop-erties and total phenolic contents of some strains of microalgae. J Appl Phycol. 2009; 22: 43-50. doi: 10.1007/s10811-009-9424-y
Matsui K, Nazifi E, Hirai Y, Wada N, Matsugo S, Sakamoto T. The cyanobacterial UV-absorbing pigment scytonemin displays radical-scavenging activity. J Gen Appl Microbiol. 2012; 58: 137-144. doi: 10.2323/jgam.58.137
Suhail S, Biswas D, Farooqui A, Arif JM, Zeeshan M. Antibac-terial and free radical scavenging potential of some cyanobacte-rial strains and their growth characteristics. J Chem Pharm Res. 2011; 3(2): 472-478. Web site. http://jocpr.com/vol3-iss2-2011/ JCPR-2011-3-2-472-478.pdf. July 13, 2016
Babic O, Kovac D, Raseta M, Sibul F, Svircev Z, Simeu-novic J. Evaluation of antioxidant activity and phenolic profile of filamentous terrestrial cyanobacterial strains isolated from forest ecosystem. J Appl Phycol. 2016; 28(4): 2333-2342. doi: 10.1007/s10811-015-0773-4
Shalaby E. Algae as promising organisms for environment and health. Plant Signal Behav. 2014; 6(9): 1338-1350. doi:
4161/psb.6.9.16779 10. Schwartz RE, Hirsch CF, Sesin DF, et al. Pharmaceuticals from cultured algae. J Ind Microbiol. 1990; 5(2-3): 113-123. doi: 10.1007/BF01573860
Golakoti T, Yoshida WY, Chaganty S, Moore RE. Isolation and structure determination of nostocyclopeptides A1 and A2 from the terrestrial cyanobacterium Nostoc sp. ATCC53789. J Nat Prod. 2001; 64(1): 54-59. doi: 10.1021/np000316k
Ploutno A, Carmeli S. Nostocyclyne A, a novel antimicro-bial cyclophane from the cyanobacterium Nostoc sp. J Nat Prod. 2000; 63(11): 1524-1526. doi: 10.1021/np0002334
Mehner C, Muller D, Kehraus S, Hautmann S, Gutschow M, Konig GM. New peptolides from the cyanobacterium Nostoc insulare as selective and potent inhibitors of human leukocyte elastase. Chem Bio Chem. 2008; 9: 2692-2703. doi: 10.1002/ cbic.200800415
Ploutno A, Carmeli S. Modified peptides from a water bloom of the cyanobacterium Nostoc sp. Tetrahedron. 2002; 58: 9949- 9957.
Murakami M, Sun Q, Ishida K, Matsuda H, Okino T, Yama-guchi K. Microviridins, elastase inhibitors from the cyanobac-terium Nostoc minutum (NIES-26). Phytochemistry. 1997; 45: 1197-1202. doi: 10.1016/S0031-9422(97)00131-3
Chlipala GE, Sturdy M, Krunic A, et al. Cylindrocyclo-phanes with proteasome inhibitory activity from the Cyano-bacterium Nostoc sp. J Nat Prod. 2010; 73(9): 1529-1537. doi: 10.1021/np100352e
Kang HS, Santarsiero BD, Kim H, et al. Merocyclophanes A and B, antiproliferative cyclophanes from the cultured terrestrial Cyanobacterium Nostoc sp. Phytochemistry. 2012; 79: 109-115. doi: 10.1016/j.phytochem.2012.03.005
Jokela J, Herfindal L, Wahlsten M, et al. A Novel cyanobac-terial nostocyclopeptide is a potent antitoxin against microcys-tins. Chem Bio Chem. 2010; 11(11): 1594-1599. doi: 10.1002/ cbic.201000179
Muir JC, Pattenden G, Thomas RM. Total synthesis of (-)-muscoride A – a novel bis-oxazole based alkaloid from the cyanobacterium Nostoc-muscorum. Synthesis. 1998: 613-618. doi: 10.1055/s-1998-5934
Nagatsu A, Kajitani H, Sakakibara J. Muscoride A: A new oxazole peptide alkaloid from freshwater cyanobacte-rium Nostoc muscorum. Tetrahedron Lett. 1995; 36: 4097- 4100. Web site. http://agris.fao.org/agris-search/search. do?recordID=US201301505456. Accessed July 13, 2016
Knübel G, Larsen LK, Moore RE, Levine IA, Patterson GM. Cytotoxic, antiviral indolocarbazoles from a blue-green alga be-longing to the Nostocaceae. J Antibiot (Tokyo). 1990; 43(10): 1236-1239. doi: 10.7164/antibiotics.43.1236
Burja AM, Banaigs B, Abou-Mansour E, Burgess JG, Wright PC. Marine cyanobacteria – a prolific source of natural products. Tetrahedron. 2001; 57: 9347-9377.
Ku CS, Pham TX, Park Y, et al. Edible blue-green algae re-duce the production of pro-inflammatory cytokines by inhibit-ing NF-kB pathway in macrophages and splenocytes. Biochim Biophys Acta. 2013; 1830(4): 2981-2988. doi: 10.1016/j.bba-gen.2013.01.018
Shanab SM, Shalaby EA, El-Fayoumy EA. Enteromorpha compressa exhibits potent antioxidant activity. J Biomed Bio-technol. 2011; 2011: 726405. doi: 10.1155/2011/726405
Falconer IR. An overview of problems caused by toxic blue-green algae (Cyanobacteria) in drinking and recreational water. Environ Toxicol. 1999; 14(1): 5-12. doi: 10.1002/(SICI)1522- 7278(199902)14:1<5::AID-TOX3>3.0.CO;2-0
Chorus I, Bartram J. Toxic cyanobacteria in water. A guide to their public health consequences, monitoring and management. WHO, E & FN Spon; London. 1999. Web site. http://www.who. int/water_sanitation_health/resourcesquality/toxcyanbegin.pdf. Accessed July 13, 2016
Mohamed ZA, El-Sharouny HM, Ali WSM. Microcystin production in benthic mats of cyanobacteria in the Nile River and irrigation canals, Egypt. Toxicon. 2006; 47: 584-590. Web site. http://www.ncbi.nlm.nih.gov/pubmed/16564062. Accessed July 13, 2016
Genuario DB, Silva-Stenico ME, Welker M, Moraes LAB, Fiore MF. Characterization of a microcystin and detection of mi-crocystin synthetase genes from a Brazilian isolate of Nostoc. Toxicon. 2010; 55: 846-854. doi: 10.1016/j.toxicon.2009.12.001
Bajpai R, Sharma NK, Lawton LA, Edwards C, Rai AK. Mi-crocystin producing cyanobacterium Nostoc sp BHU001 from a pond in India. Toxicon. 2009; 53: 587-590. doi: 10.1016/j.toxi-con.2009.01.023
Oudra B, Andaloussi MDE, Vasconcelos VM. Identification and quantification of microcystins from a Nostoc muscorum bloom occurring in Ouka Meden River (High-Atlas Mountains of Marrakech, Morocco). Environ Monit Assess. 2009; 149: 437- 444. doi: 10.1007/s10661-008-0220-y
Izaguirre G, Jungblut AD, Neilan BA. Benthic cyanobacte-ria (oscillatoriaceae) that produce microcystin-LR, isolated from four reservoirs in Southern California. Wat Res. 2007; 41: 492- 498. Web site. http://www.ncbi.nlm.nih.gov/pubmed/17126876. Accessed July 13, 2016
Oksanen I, Jokela J, Fewer DP, Wahlsten M, Rikkinen J, Sivonen K. Discovery of rare and highly toxic microcystins from lichen-associated cyanobacterium Nostoc sp strain IO-102-I. Appl Environ Microbiol. 2004; 70: 5756-5763. doi: 10.1128/ AEM.70.10.5756-5763.2004
Murch SJ, Cox P, Banack SA. A mechanism for slow release of biomagnified cyanobacterial neurotoxins and neurodegenera-tive disease in Guam. Proc Natl Acad. Sci USA. 2004; 101(33): 12228-12231. doi: 10.1073/pnas.0404926101
Halimoon N, Ali R. Evaluation of antioxidative activity of phenolics in methanolic extracts of blue green algae. Catrina. 2010; 5(1): 9-13. Web site. http://www.catrinajournal.com/pa-per_info/id/128. Accessed July 13, 2016
Singleton VL, Rossi JA. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture. 1965; 16: 144-153. Web site. http://www.ajevonline.org/content/16/3/144. Accessed July 13,
Edmondson JM, Armstrong LS, Martinez AO. A rapid and simple MTT-based spectrophotometric assay for determining drug sensitivity in monolayer cultures. J Tissue Cult Meth. 1988; 11: 15-17. doi: 10.1007/BF01404408
Goiris K, De Vreese P, De Cooman L, Muylaert K. Rapid screening and guided extraction of antioxidants from microalgae using voltammetric methods. J Agric Food Chem. 2012; 60(30): 7359-7366. doi: 10.1021/jf302345j
van Apeldoorn ME, van Egmond HP, Speijers GJ, Bakker GJ. Toxins of cyanobacteria. Mol Nutr Food Res. 2007; 51: 7-60. doi: 10.1002/mnfr.200600185
Kahl R, Kappus H. Toxicology of the synthetic antioxidants BHA and BHT in comparison with the natural antioxidant vita-min E. Z Lebensm Unters Forsch. 1993; 196(4): 329-338. doi: 10.1007/BF01197931
Teneva I, Stoyanov P, Belkinova D, Dimitrova-Dyulgerova I, Mladenov R, Dzhambazov B. Production of cyanobacterial toxins from two Nostoc species (Nostocales) and evaluation of their cytotoxicity in vitro. J Bio Sci Biotechnol. 2012; 1(1): 33- 43. Web site. http://www.oalib.com/paper/2762845#.V6BZ5v-l97cs. Accessed July 13, 2016
IvanovaE,StaykovaT,DhzambazovB.Cytotoxicityandgeno-toxicity of the cyanoprokaryote Nostoc microscopicum. Genetics and Breeding. 2009; 38(1): 13-19. Web site. http://procedures. uni-plovdiv.bg/docs/procedure/213/9209199361127217577. pdf. Accessed July 13, 2016
Hrouzek P, Tomek P, Lukesova A, et al. Cytotoxicity and secondary metabolites production in terrestrial Nostoc strains, originating from different climatic/geographic regions and habi-tats: Is their cytotoxicity environmentally dependent? Environ-mental Toxicology. 2010: 1-14. doi: 10.1002/tox.20561
Lowery TH, Richardson KS. Mechanism and Theory in Or-ganic Chemistry. NY, USA: Springer; 1987.
Kovacik J, Klejdus B, Backor M. Physiological responses of scenedesmus quadricauda (Chlorophyceae) to UV-A and UV-C light. Photochem Photobiol. 2010; 86: 612-616. doi: 10.1111/j.1751-1097.2010.00708.x
Custodio L, Justo T, Silvestre L, et al. Microalgae of different phyla display antioxidant, metal chelating and acetylcholinester-ase inhibitory activities. Food Chem 2011; 59(13): 7005-7012.
Duval B, Shetty K, Thomas WH. Phenolic compounds and antioxidant properties in the snow alga chlamydomonas nivalis after exposure to UV light. J Appl Phycol. 2000; 11: 559-566. doi: 10.1023/A:1008178208949
Chen F, Li HB, Wong RNS, Ji B, Jiang Y. Isolation and purification of the bioactive carotenoid zeaxanthin from the microalga Microcystis aeruginosa by high-speed counter-current chromatography. J Chromatogr. A. 2005; 1064(2): 183-186. Web site. http://agris.fao.org/agris-search/search. do?recordID=US201301016794. Accessed July 13, 2016
Sivonen K, Namikoshi M, Evans WR, Färdig M, Carmichael WW, Rinehart KL. Three new microcystins, cyclic heptapeptide hepatotoxins, from Nostoc sp. strain 152. Chem Res Toxicol. 1992; 6: 464-469. doi: 10.1021/tx00028a003
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