Investigation of antioxidative and anticancer potentials of Streptomyces sp. MUM256 isolated from Malaysia mangrove soil

Frontiers in Microbiology

Volumn 6, Issue NOV, 2015, Pages

  Tan, Loh Teng Hern ^a   Ser, Hooi Leng ^a   Yin, Wai Fong ^b   Chan, Kok Gan ^b   Lee, Learn Han ^a   Goh, Bey Hing ^a  

^a MONASH UNIVERSITY MALAYSIA   (Malaysia)

^b UNIVERSITY OF MALAYA   (Malaysia)

Author keywords

Anticancer; Antioxidant; Malaysia; Mangrove; Streptomyces sp.

Indexed keywords

BACTERIAL EXTRACT; STREPTOMYCES EXTRACT; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BACTERIAL GROWTH; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DPPH RADICAL SCAVENGING ASSAY; FERMENTATION; GENE SEQUENCE; HUMAN; HUMAN CELL; MASS FRAGMENTOGRAPHY; MTT ASSAY; NONHUMAN; PHYLOGENETIC TREE; SEQUENCE ALIGNMENT;

EID: 84949747825     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.01316     Document Type: Article

References (76)

1. Abdullah, N. S. A., Manaf, S. F. A., Aziz, A., Shahidah, N., Hamzah, F., and Idris, N. (2015). Characterization and identification of isolated microorganism from agricultural soil for degradation of cellulose based waste. Adv. Mat. Res. 1113, 230-235. doi: 10.4028/www.scientific.net/AMR.1113.230
2. Akpuaka, A., Ekwenchi, M., Dashak, D., and Dildar, A. (2012). Gas Chromatography-Mass Spectrometry (GC/MS) analysis of phthalate isolates in n-hexane extract of Azadirachta indica A. Juss (Neem) leaves. J. Am. Sci. 8, 146-155. Available online at: http://www.jofamericanscience.org/journals/am-sci/am0812/022_12494am0812_146_148.pdf
3. Ames, B. N., Shigenaga, M. K., and Hagen, T. M. (1993). Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. U.S.A. 90, 7915-7922. doi: 10.1073/pnas.90.17.7915
4. Atlas, R. M. (2010). Handbook of Microbiological Media, ed L. C. Parks. Boca Raton, FL: CRC Press.
5. Baardseth, P. (1989). Effect of selected antioxidants on the stability of dehydrated mashed potatoes. Food Addit. Contam. 6, 201-207. doi: 10.1080/02652038909373775
6. Bérdy, J. (2005). Bioactive microbial metabolites. J. Antibiot. 58, 1-26. doi: 10.1038/ja.2005.1
7. Brautaset, T., Sekurova, O. N., Sletta, H., Ellingsen, T. E., Strøm, A. R., Valla, S., et al. (2000). Biosynthesis of the polyene antifungal antibiotic nystatin in Streptomyces noursei ATCC 11455: analysis of the gene cluster and deduction of the biosynthetic pathway. Chem. Biol. 7, 395-403. doi: 10.1016/S1074-5521(00)00120-4
8. Carrillo, P. G., Mardaraz, C., Pitta-Alvarez, S. I., and Giulietti, A. M. (1996). Isolation and selection of biosurfactant-producing bacteria. World. J. Microbiol. Biotechnol. 12, 82-84. doi: 10.1007/BF00327807
9. Cerny, G. (1978). Studies on the aminopeptidase test for the distinction of gram-negative from gram-positive bacteria. Eur. J. Appl. Microbiol. 5, 113-122. doi: 10.1007/BF00498805
10. Cruz De Carvalho, M. H. (2008). Drought stress and reactive oxygen species: production, scavenging and signaling. Plant. Signal. Behav. 3, 156-165. doi: 10.4161/psb.3.3.5536
11. Devasagayam, T. P., Tilak, J. C., Boloor, K. K., Sane, K. S., Ghaskadbi, S. S., and Lele, R. D. (2004). Free radicals and antioxidants in human health: current status and future prospects. J. Assoc. Physicians. India. 52, 794-804. Available online at: http://www.japi.org/october2004/R-794.pdf
12. Du, L., Sánchez, C., Chen, M., Edwards, D. J., and Shen, B. (2000). The biosynthetic gene cluster for the antitumor drug bleomycin from Streptomyces verticillus ATCC15003 supporting functional interactions between nonribosomal peptide synthetases and a polyketide synthase. Chem. Biol. 7, 623-642. doi: 10.1016/S1074-5521(00)00011-9
13. Duncan, K., Haltli, B., Gill, K. A., and Kerr, R. G. (2014). Bioprospecting from marine sediments of New Brunswick, Canada: exploring the relationship between total bacterial diversity and actinobacteria diversity. Mar. Drugs. 12, 899-925. doi: 10.3390/md12020899
14. Felsenstein, J. (1981). Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17, 368-376. doi: 10.1007/BF01734359
15. Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783-791. doi: 10.2307/2408678
16. Fu, P., Yang, C., Wang, Y., Liu, P., Ma, Y., Xu, L., et al. (2012). Streptocarbazoles A and B, two novel indolocarbazoles from the marine-derived actinomycete strain Streptomyces sp. FMA. Org. Lett. 14, 2422-2425. doi: 10.1021/ol3008638
17. Goh, B. H., Chan, C. K., Kamarudin, M. N. A., and Kadir, H. A. (2014). Swietenia macrophylla King induces mitochondrial-mediated apoptosis through p53 upregulation in HCT116 colorectal carcinoma cells. J. Ethnopharmacol. 153, 375-385. doi: 10.1016/j.jep.2014.02.036
18. Gopi, M., Dhayanithi, N. B., Devi, K. N., and Kumar, T. T. A. (2014). Marine natural product, Pyrrolo [1,2-a] pyrazine-1,4-dione, hexahydro-(C7H10N2O2) of antioxidant properties from Bacillus species at Lakshadweep archipelago. J. Coast. Life Med. 2, 632-637. doi: 10.12980/jclm.2.201414j40
19. Grimm, A., Madduri, K., Ali, A., and Hutchinson, C. (1994). Characterization of the Streptomyces peucetius ATCC 29050 genes encoding doxorubicin polyketide synthase. Gene 151, 1-10. doi: 10.1016/0378-1119(94)90625-4
20. Hong, K., Gao, A.-H., Xie, Q.-Y., Gao, H., Zhuang, L., Lin, H.-P., et al. (2009). Actinomycetes for marine drug discovery isolated from mangrove soils and plants in China. Mar. Drugs. 7, 24-44. doi: 10.3390/md7010024
21. Hu, H., Lin, H.-P., Xie, Q., Li, L., Xie, X.-Q., and Hong, K. (2012). Streptomyces qinglanensis sp. nov., isolated from mangrove sediment. Int. J. Syst. Evol. Microbiol. 62, 596-600. doi: 10.1099/ijs.0.032201-0
22. Jemal, A., Center, M. M., Desantis, C., and Ward, E. M. (2010). Global patterns of cancer incidence and mortality rates and trends. Cancer. Epidem. Biomar. 19, 1893-1907. doi: 10.1158/1055-9965.EPI-10-0437
23. Jennerjahn, T. C., and Ittekkot, V. (2002). Relevance of mangroves for the production and deposition of organic matter along tropical continental margins. Naturwissenschaften 89, 23-30. doi: 10.1007/s00114-001-0283-x
24. Karthik, L., Kumar, G., and Rao, K. V. B. (2013). Antioxidant activity of newly discovered lineage of marine actinobacteria. Asian. Pac. J. Trop. Med. 6, 325-332. doi: 10.1016/S1995-7645(13)60065-6
25. Kelly, K. L. (1964). Inter-Society Color Council-National Bureau of Standards Color Name Charts Illustrated with Centroid Colors. Washington, DC: U.S. Government Printing Office.
26. Kim, O.-S., Cho, Y.-J., Lee, K., Yoon, S.-H., Kim, M., Na, H., et al. (2012). Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 62, 716-721. doi: 10.1099/ijs.0.038075-0
27. Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111-120. doi: 10.1007/BF01731581
28. Krishnan, K., Mani, A., and Jasmine, S. (2014). Cytotoxic activity of bioactive compound 1, 2-benzene dicarboxylic acid, mono 2-ethylhexyl ester extracted from a marine derived Streptomyces sp. VITSJK8. Int. J. Mol. Cell. Med. 3, 246. Available online at: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4293612/pdf/ijmcm-3-246.pdf
29. Kumar, S. S., Price, T. J., Mohyieldin, O., Borg, M., Townsend, A., and Hardingham, J. E. (2014). KRAS G13D mutation and sensitivity to cetuximab or panitumumab in a colorectal cancer cell line model. Gastrointest. Cancer. Res. 7, 23. Available online at: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3930148/pdf/gcr23.pdf
30. Küster, E., and Williams, S. (1964). Media for the isolation of streptomycetes: starch casein medium. Nature 202, 928-929. doi: 10.1038/202928a0
31. Lee, D.-R., Lee, S.-K., Choi, B.-K., Cheng, J., Lee, Y.-S., Yang, S. H., et al. (2014a). Antioxidant activity and free radical scavenging activities of Streptomyces sp. strain MJM 10778. Asian. Pac. J. Trop. Med. 7, 962-967. doi: 10.1016/S1995-7645(14)60170-X
32. Lee, L.-H., Cheah, Y.-K., Sidik, S. M., Ab Mutalib, N.-S., Tang, Y.-L., Lin, H.-P., et al. (2012). Molecular characterization of Antarctic actinobacteria and screening for antimicrobial metabolite production. World. J. Microbiol. Biotechnol. 28, 2125-2137. doi: 10.1007/s11274-012-1018-1
33. Lee, L.-H., Zainal, N., Azman, A.-S., Ab Mutalib, N.-S., Hong, K., and Chan, K.-G. (2014b). Mumia flava gen. nov., sp. nov., an actinobacterium of the family Nocardioidaceae. Int. J. Syst. Evol. Microbiol. 64, 1461-1467. doi: 10.1099/ijs.0.058701-0
34. Lee, L.-H., Zainal, N., Azman, A.-S., Eng, S.-K., Ab Mutalib, N.-S., Yin, W.-F., et al. (2014c). Streptomyces pluripotens sp. nov., a bacteriocin-producing streptomycete that inhibits meticillin-resistant Staphylococcus aureus. Int. J. Syst. Evol. Microbiol. 64, 3297-3306. doi: 10.1099/ijs.0.065045-0
35. Lee, L.-H., Zainal, N., Azman, A.-S., Eng, S.-K., Goh, B.-H., Yin, W.-F., et al. (2014d). Diversity and antimicrobial activities of actinobacteria isolated from tropical mangrove sediments in Malaysia. ScientificWorldJournal. 2014:698178. doi: 10.1155/2014/698178
36. Li, X.-L., Xu, M.-J., Zhao, Y.-L., and Xu, J. (2010). A novel benzo [f][1, 7] naphthyridine produced by Streptomyces albogriseolus from mangrove sediments. Molecules 15, 9298-9307. doi: 10.3390/molecules15129298
37. Liu, L., Taverna, P., Whitacre, C. M., Chatterjee, S., and Gerson, S. L. (1999). Pharmacologic disruption of base excision repair sensitizes mismatch repair-deficient and-proficient colon cancer cells to methylating agents. Clin. Cancer. Res. 5, 2908-2917.
38. Mac Faddin, J. F. (1976). Biochemical Tests for Identification of Medical Bacteria. Philadelphia, PA: Lippincott Williams and Wilkins.
39. Manimaran, M., Gopal, J. V., and Kannabiran, K. (2015). Antibacterial activity of Streptomyces sp. VITMK1 isolated from mangrove soil of Pichavaram, Tamil Nadu, India. Proc. Indian. Acad. Sci. Sect. B. 1-8. doi: 10.1007/s40011-015-0619-5
40. Maxwell, S. R. (1995). Prospects for the use of antioxidant therapies. Drugs 49, 345-361. doi: 10.2165/00003495-199549030-00003
41. Meena, B., Rajan, L. A., Vinithkumar, N. V., and Kirubagaran, R. (2013). Novel marine actinobacteria from emerald Andaman & Nicobar Islands: a prospective source for industrial and pharmaceutical byproducts. BMC Microbiol. 13:145. doi: 10.1186/1471-2180-13-145
42. Narasaiah, B. C., Leelavathi, V., Sudhakar, G., Mariyadasu, P., Swapna, G., and Manne, A. K. (2014). Isolation and structural confirmation of bioactive compounds produced by the strain Streptomyces albus CN-4. IOSR. J. Pharm. Biol. Sci. 9, 49-54. doi: 10.9790/3008-09654954
43. Narendhran, S., Rajiv, P., Vanathi, P., and Sivaraj, R. (2014). Spectroscopic analysis of bioactive compounds from Streptomyces cavouresis KUV39: evaluation of antioxidant and cytotoxicity activity. Int. J. Pharm. Pharm. Sci. 6, 319-322. Available online at: http://innovareacademics.in/journals/index.php/ijpps/article/viewFile/2009/9983
44. Rao, K. V. R., and Rao, T. R. (2013). Molecular characterization and its antioxidant activity of a newly isolated Streptomyces coelicoflavus BC 01 from mangrove soil. J. Young. Pharm. 5, 121-126. doi: 10.1016/j.jyp.2013.10.002
45. Reddy, N. S., Navanesan, S., Sinniah, S. K., Wahab, N. A., and Sim, K. S. (2012). Phenolic content, antioxidant effect and cytotoxic activity of Leea indica leaves. BMC Complement. Altern. Med. 12:128. doi: 10.1186/1472-6882-12-128
46. Riganti, C., Mini, E., and Nobili, S. (2015). Editorial: multidrug resistance in cancer: pharmacological strategies from basic research to clinical issues. Front. Oncol. 5:105. doi: 10.3389/fonc.2015.00105
47. Saitou, N., and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
48. Schatz, A., Bugle, E., and Waksman, S. A. (1944). Streptomycin, a substance exhibiting antibiotic activity against gram-positive and gram-negative bacteria.* Adv. Exp. Med. Biol. 55, 66-69. doi: 10.3181/00379727-55-14461
49. Ser, H.-L., Palanisamy, U. D., Yin, W.-F., Abd Malek, S. N., Nurestri, S., Chan, K.-G., et al. (2015a). Presence of antioxidative agent, Pyrrolo [1, 2-a] pyrazine-1, 4-dione, hexahydro-in newly isolated Streptomyces mangrovisoli sp. nov. Front. Microbiol. 6:854. doi: 10.3389/fmicb.2015.00854
50. Ser, H.-L., Zainal, N., Palanisamy, U. D., Goh, B.-H., Yin, W.-F., Chan, K.-G., et al. (2015b). Streptomyces gilvigriseus sp. nov., a novel actinobacterium isolated from mangrove forest soil. Antonie van Leeuwenhoek 107, 1369-1378. doi: 10.1007/s10482-015-0431-5
51. Shieh, W. Y., Chen, Y.-W., Chaw, S.-M., and Chiu, H.-H. (2003). Vibrio ruber sp. nov., a red, facultatively anaerobic, marine bacterium isolated from sea water. Int. J. Syst. Evol. Microbiol. 53, 479-484. doi: 10.1099/ijs.0.02307-0
52. Shirling, E. B., and Gottlieb, D. (1966). Methods for characterization of Streptomyces species. Intl. J. Syst. Evol. Microbiol. 16, 313-340. doi: 10.1099/00207713-16-3-313
53. Siegel, R. L., Miller, K. D., and Jemal, A. (2015). Cancer statistics, 2015. CA 65, 5-29. doi: 10.3322/caac.21254
54. Sivasubramanian, R., and Brindha, P. (2013). In-vitro cytotoxic, antioxidant and GC-MS studies on Centratherum punctatum Cass. Int. J. Pharm. Pharm. Sci. 4, e8. Available online at: http://www.ijppsjournal.com/Vol5Issue3/6947.pdf
55. Stadtman, E. R., and Berlett, B. S. (1997). Reactive oxygen-mediated protein oxidation in aging and disease. Chem. Res. Toxicol. 10, 485-494. doi: 10.1021/tx960133r
56. Sui, J.-L., Xu, X.-X., Qu, Z., Wang, H.-L., Lin, H.-P., Xie, Q.-Y., et al. (2011). Streptomyces sanyensis sp. nov., isolated from mangrove sediment. Int. J. Syst. Evol. Microbiol. 61, 1632-1637. doi: 10.1099/ijs.0.023515-0
57. Sulaiman, S. F., Yusoff, N. A. M., Eldeen, I. M., Seow, E. M., Sajak, A. A. B., and Ooi, K. L. (2011). Correlation between total phenolic and mineral contents with antioxidant activity of eight Malaysian bananas (Musa sp.). J. Food. Compost. Anal. 24, 1-10. doi: 10.1016/j.jfca.2010.04.005
58. Supriady, H., Kamarudin, M. N. A., Chan, C. K., Goh, B. H., and Kadir, H. A. (2015). SMEAF attenuates the production of pro-inflammatory mediators through the inactivation of Akt-dependent NF-κB, p38 and ERK1/2 pathways in LPS-stimulated BV-2 microglial cells. J. Funct. Foods. 17, 434-448. doi: 10.1016/j.jff.2015.05.042
59. Takahashi, Y., Matsumoto, A., Seino, A., Iwai, Y., and Omura, S. (1996). Rare actinomycetes isolated from desert soils. Actinomycetologica 10, 91-97. doi: 10.3209/saj.10_91
60. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197
61. Tan, L. T. H., Lee, L. H., Yin, W. F., Chan, C. K., Abdul Kadir, H., Chan, K. G., et al. (2015). Traditional uses, phytochemistry, and bioactivities of Cananga odorata (Ylang-Ylang). J. Evid. Based. Complementary. Alternat. Med. 2015:896314. doi: 10.1155/2015/896314
62. Tepe, B., Sokmen, M., Akpulat, H. A., and Sokmen, A. (2005). In vitro antioxidant activities of the methanol extracts of four Helichrysum species from Turkey. Food. Chem. 90, 685-689. doi: 10.1016/j.foodchem.2004.04.030
63. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic. Acids. Res. 25, 4876-4882. doi: 10.1093/nar/25.24.4876
64. Twentyman, P. R., and Luscombe, M. (1987). A study of some variables in a tetrazolium dye (MTT) based assay for cell growth and chemosensitivity. Br. J. Cancer. 56, 279. doi: 10.1038/bjc.1987.190
65. Valko, M., Rhodes, C. J., Moncol, J., Izakovic, M., and Mazur, M. (2006). Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 160, 1-40. doi: 10.1016/j.cbi.2005.12.009
66. Verma, A., Johri, B., and Prakash, A. (2014). Antagonistic evaluation of bioactive metabolite from endophytic fungus, Aspergillus flavipes KF671231. J. Mycol. 2014:371218. doi: 10.1155/2014/371218
67. Waksman, S. A., and Henrici, A. T. (1943). The nomenclature and classification of the actinomycetes. J. Bacteriol. 46, 337.
68. Wang, H., Khor, T. O., Shu, L., Su, Z., Fuentes, F., Lee, J.-H., et al. (2012). Plants against cancer: a review on natural phytochemicals in preventing and treating cancers and their druggability. Anticancer. Agents. Med. Chem. 12, 1281. doi: 10.2174/187152012803833026
69. Weber, J. M., Wierman, C. K., and Hutchinson, C. R. (1985). Genetic analysis of erythromycin production in Streptomyces erythreus. J. Bacteriol. 164, 425-433.
70. Williams, S. T., Goodfellow, M., and Alderson, G. (1989). "Genus streptomyces waksman and henrici 1943, 339AL". in Bergey's Manual of Systematic Bacteriology, eds S. T. Williams, M. E. Sharpe, and J. G., Holt (Baltimore: Williams & Wilkins), 2452-2492.
71. Wong, D. Z. H., Kadir, H. A., Lee, C. L., and Goh, B. H. (2012). Neuroprotective properties of Loranthus parasiticus aqueous fraction against oxidative stress-induced damage in NG108-15 cells. J. Nat. Med. 66, 544-551. doi: 10.1007/s11418-011-0622-y
72. Xiao, J., Wang, Y., Luo, Y., Xie, S.-J., Ruan, J.-S., and Xu, J. (2009). Streptomyces avicenniae sp. nov., a novel actinomycete isolated from the rhizosphere of the mangrove plant Avicennia mariana. Int. J. Syst. Evol. Microbiol. 59, 2624-2628. doi: 10.1099/ijs.0.009357-0
73. Xu, J., Wang, Y., Xie, S.-J., Xu, J., Xiao, J., and Ruan, J.-S. (2009). Streptomyces xiamenensis sp. nov., isolated from mangrove sediment. Int. J. Syst. Evol. Microbiol. 59, 472-476. doi: 10.1099/ijs.0.000497-0
74. Yogeswari, S., Ramalakshmi, S., Neelavathy, R., and Muthumary, J. (2012). Identification and comparative studies of different volatile fractions from Monochaetia kansensis by GCMS. Glob. J. Pharmacol. 6, 65-71. Available online at: http://www.idosi.org/gjp/6(2)12/3.pdf
75. Yuan, G., Hong, K., Lin, H., She, Z., and Li, J. (2013). New azalomycin F analogs from mangrove Streptomyces sp. 211726 with activity against microbes and cancer cells. Mar. Drugs 11, 817-829. doi: 10.3390/md11030817
76. Zheng, L., Yan, X., Han, X., Chen, H., Lin, W., and Lee, F. S. C. (2006). Identification of norharman as the cytotoxic compound produced by the sponge (Hymeniacidon perleve)-associated marine bacterium Pseudoalteromonas piscida and its apoptotic effect on cancer cells. Biotechnol. Appl. Biochem. 44, 135-142. doi: 10.1042/BA20050176