Streptomyces zerumbet W14, a novel species of the endophyte genus Streptomyces was isolated from the rhizome tissue of Zingiber zerumbet (L.) Smith. Identification of strain W14 was based on its morphology, chemotaxonomy and phylogenetic analysis using 16S rDNA sequence. It was classified as the secondary meabolites of the culture extract were studied. The major active ingredients from the crude extract were purified by silica gel column chromatography and identified by spectroscopic data. The crude extract and purified compounds were tested for their biological activities on antibacterial and anti-inflammatory properties. The crude extract showed inhibition on the growth of Gram-positive bacteria with the MIC and MBC values of 8 - 32 μg/ml and 32 - 128 μg/ml, respectively. The isolated compounds were identified to be methyl 5-(hydroxymethyl)furan-2-carboxylate (1) and geldanamycin (2). Bioassay studies showed that compound 1 had antibacterial activity against Staphylococus aureus ATCC 25923 and Methicillin Resistant S. aureus strain Sp6 (clinical isolate) with the MIC and MBC values of 1 μg/ml and 16 - 64 μg/ml, respectively, and also showed activity against Bacillus Calmette-Guérin (vaccine strain) with MIC and MBC values of 128.00 μg/ml and 128.00 μg/ml, respectively. The compound 2 at the concentration of 1 - 5 μg/ml had in vitro anti-inflammatory activity on LPS-induced RAW 264.7 cells by inhibition of mRNA expression and production of inducible NO synthase (iNOS), tumor necrosis factor-alpha (TNF-α), interleukin-1β (IL-1β), and interleukin-6 (IL-6). These results suggest that compounds 1 and 2 produced by S. zerumbet W14 (an endophyte of Z. Zerumbet) have antibacterial and anti-inflammatory activities, respectively. Therefore, the future studies on these compounds could be useful for the management of bacterial infections and inflammatory diseases.
References
[1]
Taechowisan, T. and Lumyong, S. (2003) Activity of Endophytic Actinomycetes from Roots of Zingiber officinale and Alpinia galanga against Phytopathogenic Fungi. Annals of Microbiology, 53, 291-298.
[2]
Taechowisan, T., Lu, C.H., Shen, Y.M. and Lumyong, S. (2005) 4-Arylcoumarins from Endophytic Streptomyces aureofaciens CMUAc130 and Their Antigungal Activity. Annals of Microbiology, 55, 63-66.
[3]
Taechowisan, T., Peberdy, J.F. and Lumyong, S. (2003) Isolation of Endophytic Actinomycetes from Selected Plants and Their Antifungal Activity. World Journal of Microbiology and Biotechnology, 19, 381-385. https://doi.org/10.1023/A:1023901107182
[4]
Taechowisan, T., Chaisaeng, S. and Phutdhawong, W.S. (2017) Antibacterial, Antioxidant and Anticancer Activities of Biphenyls from Streptomyces sp. BO-07: An Endophyte in Boesenbergia rotunda (L.) Mansf A. Journal Food and Agricultural Immunology, 28, 1330-1346. https://doi.org/10.1080/09540105.2017.1339669
[5]
National Committee for Clinical Laboratory Standards (1997) Performance Standards for Antimicrobial Disk Susceptibility Tests. Approved Standard M2-A6. Wayne, PA.
[6]
National Committee for Clinical Laboratory Standards (2000) Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically. Approved standard M7-A5. Wayne, PA.
[7]
Grievink, H.W., Luisman, T., Kluft, C., Moerland, M. and Malone, K.E. (2016) Comparison of Three Isolation Techniques for Human Peripheral Blood Mononuclear Cells: Cell Recovery and Viability, Population Composition, and Cell Functionality. Biopreservation and Biobanking, 14, 410-415. https://doi.org/10.1089/bio.2015.0104
[8]
Green, L.C., Wagner, D.A., Glogowski, J., Skipper, P.L., Wishnok, J.S., et al. (1982) Analysis of Nitrate, Nitrite, and [15N]Nitrate in Biological Fluids. Analytical Biochemistry, 126, 131-138. https://doi.org/10.1016/0003-2697(82)90118-X
[9]
Taechowisan, T., Wanbanjob, A., Tuntiwachwuttikul, P. and Liu, J.K. (2009) Anti-Inflammatory Activity of Lansai C from Endophytic Streptomyces sp. SUC1 in LPS-Induced RAW 264.7 Cells. Journal Food and Agricultural Immunology, 20, 67-77. https://doi.org/10.1080/09540100902730064
[10]
Brosius, J., Palmer, M.L., Kennedy, P.J. and Noller, H.F. (1978) Complete Nucleotide Sequence of a 16S Ribosomal RNA Gene from Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 75, 4801-4805. https://doi.org/10.1073/pnas.75.10.4801
[11]
Liu, T., Liu, L.X., Jiang, X., Huang, X.L. and Chen, J. (2009) A New Furanoid Toxin Produced by Curvularia lunata, the Causal Agent of Maize Curvularia Leaf Spot. Journal Canadian Journal of Plant Pathology, 31, 22-27. https://doi.org/10.1080/07060660909507568
[12]
ōmura, S., Nakagawa, A. and Sadakane, N. (1979) Structure of Herbimycin A New Ansamycin Antibiotic. Tetrahedron Letters, 20, 4323-4326. https://doi.org/10.1016/S0040-4039(01)86578-3
[13]
Qin, H.L. and Panek, J.S. (2008) Total Synthesis of the Hsp90 Inhibitor Geldanamycin. Organic Letters, 10, 2477-2479. https://doi.org/10.1021/ol800749w
[14]
Koga, A.Y., Beltrame, F.L. and Pereira, A.V. (2016) Several Aspects of Zingiber zerumbet: A Review. Revista Brasileira de Farmacognosia, 26, 385-391. https://doi.org/10.1016/j.bjp.2016.01.006
[15]
Malladi, S., Nadh, R.V., Babu, K.S. and Babu, P.S. (2017) Synthesis and Antibacterial Activity Studies of 2,4-di Substituted Furan Derivatives. Beni-Suef University Journal of Basic and Applied Sciences, 6, 345-353.
[16]
Zhou, L., Dong, W., Wang, Y., Zhou, K., Ma, H.Y., et al. (2016) A New Furan-2-Carboxylic Acid from Stem Bark of Cassia alata. China Journal of Chinese Materia Medica, 41, 2652-2654.
[17]
Deboer, C., Meulman, P.A., Wnuk, R.J. and Peterson, D.H. (1970) Geldanamycin, a New Antibiotic. Journal of Antibiotics, 23, 442-447. https://doi.org/10.7164/antibiotics.23.442
[18]
Hu, Z., Liu, Y., Tian, Z.Q., Ma, W., Starks, C.M., et al. (2004) Isolation and Characterization of Novel Geldanamycin Analogues. Journal of Antibiotics, 57, 421-428. https://doi.org/10.7164/antibiotics.57.421
[19]
Jongrungruangchok, S., Tanasupawat, S., Kittakoop, P., Bavovada, R., Kobayashi, H., et al. (2006) Identification of Streptomyces and Kitasatospora Strains from Thai Soils with Geldanamycin Production Strain. Actinomycetologica, 20, 10-14. https://doi.org/10.3209/saj.20.10
[20]
Taechowisan, T., Chaisaeng, S., Puckdee, W. and Phutdhawong, W.S. (2019) Anti-Inflammatory Activity of Biphenyls from Streptomyces sp. BO07 in LPS-Induced RAW 264.7 Cells. Asian Journal of Biological Sciences, 12, 148-155.
[21]
Roe, S., Prodromou, C., O’Brien, R., Ladbury, J., Piper, P., et al. (1999) Structural Basis for Inhibition of the Hsp90 Molecular Chaperone by the Antitumor Antibiotics Radicicol and Geldanamycin. Journal of Medicinal Chemistry, 42, 260-266. https://doi.org/10.1021/jm980403y
[22]
Ochel, H.J., Eichhorn, K. and Gademann, G. (2001) Geldanamycin, the Prototype of a Class of Antitumor Drugs Targeting the Heat Shock Protein 90 Family of Molecular Chaperones. Cell Stress Chaperones, 6, 105-112. https://doi.org/10.1379/1466-1268(2001)006<0105:GTPOAC>2.0.CO;2
[23]
Scheufler, C., Brinker, A., Bourenkov, G., Pegoraro, S., Moroder, L., et al. (2000) Structure of TPR Domain-Peptide Complexes, Critical Elements in the Assembly of the Hsp70-Hsp90 Multichaperone Machine. Cell, 101, 199-210. https://doi.org/10.1016/S0092-8674(00)80830-2
[24]
Davis, M. and Carbott, D. (1999) Herbimycin A and Geldanamycin Inhibit Okadaic Acid-Induced Apoptosis and p38 Activation in NRK-52E Renal Epithelial Cells. Toxicology and Applied Pharmacology, 161, 59-74. https://doi.org/10.1006/taap.1999.8765
[25]
Bijlmakers, M.J. and Marsh, M. (2000) Hsp90 Is Essential for the Synthesis and Subsequent Membrane Association, but Not the Maintenance, of the Src-Kinase p56lck. Molecular Biology of the Cell, 11, 1585-1595. https://doi.org/10.1091/mbc.11.5.1585
[26]
Richter, K. and Buchner, J. (2001) Hsp90, Chaperoning Signal Transduction. Journal of Cellular Physiology, 188, 281-290. https://doi.org/10.1002/jcp.1131
[27]
Pritchard, K.A., Ackerman, A.W., Gross, E.R., Stepp, D.W., Shi, Y., et al. (2001) Heat Shock Protein 90 Mediates the Balance of Nitric Oxide and Superoxide Anion from Endothelial Nitric-Oxide Synthase. Journal of Biological Chemistry, 276, 17621-17624. https://doi.org/10.1074/jbc.C100084200
[28]
Schulte, T.W., An, W.G. and Neckers, L.M. (1997) Geldanamycin-Induced Desta-Bilization of Raf-1 Involves the Proteasome. Biochemical and Biophysical Research Communications, 239, 655-659. https://doi.org/10.1006/bbrc.1997.7527
[29]
Pratt, W. (1998) The Hsp90-Based Chaperone System, Involvement in Signal Transduction from a Variety of Hormone and Growth Factor Receptors. Proceedings of the Society for Experimental Biology and Medicine, 217, 420-434. https://doi.org/10.3181/00379727-217-44252
[30]
Sakagami, M., Morrison, P. and Welch, W. (1999) Benzoquinoid Ansamycins (Herbimycin A and Geldanamycin) Interfere with the Maturation of Growth Factor Receptor Tyrosine Kinases. Cell Stress Chaperones, 4, 19-28. https://doi.org/10.1379/1466-1268(1999)004<0019:BAHAAG>2.3.CO;2
[31]
Schnaider, T., Somogyi, J., Csermely, P. and Szamel, M. (2000) The Hsp90-Specific Inhibitor Geldanamycin Selectively Disrupts Kinase-Mediated Signaling Events of T-Lymphocyte Activation. Cell Stress Chaperones, 5, 52-61. https://doi.org/10.1379/1466-1268(2000)005<0052:THSIGS>2.0.CO;2
[32]
Whitesell, L. and Cook, P. (1996) Stable and Specific Binding of Heat Shock Protein 90 by Geldanamycin Disrupts Glucocorticoid Receptor Function in Intact Cells. Molecular Endocrinology, 10, 705-712.
[33]
Bamberger, C., Wald, M., Bamberger, A. and Schulte, H. (1997) Inhibition of Mineralocorticoid and Glucocorticoid Receptor Function by the Heat Shock Protein 90-Binding Agent Geldanamycin. Molecular and Cellular Endocrinology, 131, 233-240. https://doi.org/10.1016/S0303-7207(97)00115-9
[34]
Fliss, A., Benzeno, S., Rao, J. and Caplan, A. (2000) Control of Estrogen Receptor Ligand Binding by Hsp90. Journal of Steroid Biochemistry and Molecular Biology, 72, 223-230. https://doi.org/10.1016/S0960-0760(00)00037-6
[35]
Neckers, L., Schulte, T. and Mimnaugh, E. (1999) Geldanamycin as a Potential Anticancer Agent, Its Molecular Target and Biochemical Activity. Investigational New Drugs, 17, 361-373. https://doi.org/10.1023/A:1006382320697
[36]
Sugita, T., Tanaka, S., Murakami, T., Miyoshi, H. and Ohnuki, T. (1999) Immuno-Suppressive Effects of the Heat Shock Protein 90-Binding Antibiotic Geldanamycin. Biochemistry and Molecular Biology International, 47, 587-595.
[37]
Bucci, M., Roviezzo, F., Cicala, C., Sessa, W. and Cirino, G. (2000) Geldanamycin: an Inhibitor of Heat Shock Protein 90 (Hsp90) Mediated Signal Transduction Has Anti-Inflammatory Effects and Interacts with Glucocorticoid Receptor in Vivo. British Journal of Pharmacology, 131, 13-16. https://doi.org/10.1038/sj.bjp.0703549
[38]
Grenert, J., Sullivan, W., Fadden, P., Haystead, T., Clark, J., et al. (1997) The Amino-Terminal Domain of Heat Shock Protein 90 (hsp90) That Binds Geldanamycin Is an ATP/ADP Switch Domain That Regulates hsp90 Conformation. Journal of Biological Chemistry, 272, 23843-23850. https://doi.org/10.1074/jbc.272.38.23843
[39]
Mandler, R., Wu, C., Sausville, E., Roettinger, A., Newman, D., et al. (2000) Immunoconjugates of Geldanamycin and Anti-HER2 Monoclonal Antibodies, Antiproliferative Activity on Human Breast Carcinoma Cell Lines. Journal of the National Cancer Institute, 92, 1573-1581. https://doi.org/10.1093/jnci/92.19.1573
[40]
Nimmanapalli, R., O’Bryan, E. and Bhalla, K. (2001) Geldanamycin and Its Analogue 17-Allylamino-17-Demethoxygeldanamycin Lowers Bcr-Abl Levels and Induces Apoptosis and Differentiation of Bcr-Abl-Positive Human Leukemic Blasts. Cancer Research, 61, 1799-1804.
[41]
Yang, J., Yang, J.M., Iannone, M., Shih, W., Lin Y., et al. (2001) Disruption of the EF-2 Kinase/Hsp90 Protein Complex: A Possible Mechanism to Inhibit Glioblastoma by Geldanamycin. Cancer Research, 61, 4010-1016.
[42]
Murphy, P., Sharp, A., Shin, J., Gavrilyuk, V., Dello, C., et al. (2002) Suppressive Effects of Ansamycins on Inducible Nitric Oxide Synthase Expression and the Development of Experimental Autoimmune Encephalomyelitis. Journal of Neuroscience Research, 67, 461-470. https://doi.org/10.1002/jnr.10139
[43]
Byrd, C., Bornmann, W., Erdjument-Bromage, H., Tempst, P. and Pavle-Tich, N. (1999) Heat Shock Protein 90 mediates Macrophage Activation by Taxol and Bacterial Lipopolysaccharide. Proceedings of the National Academy of Sciences of the United States of America, 96, 5645-5650. https://doi.org/10.1073/pnas.96.10.5645
[44]
Zhu, F.G. and Pisetsky, D.S. (2001) Role of the Heat Shock Protein 90 in Immune Response Stimulation by Bacterial DNA and Synthetic Oligonucleotides. Infection and Immunity, 69, 5546-5552. https://doi.org/10.1128/IAI.69.9.5546-5552.2001
[45]
Kastelic, T., Schnyder, J., Leutwiler, A., Traber, R., Streit, B., et al. (1996) Induction of Rapid IL-1 Beta mRNA Degradation in THP-1 Cells Mediated through the AU-Rich Region in the 3UTR by a Radicicol Analogue. Cytokine, 8, 751-761. https://doi.org/10.1006/cyto.1996.0100
[46]
Wax, S., Piecyk, M., Maritim, B. and Anderson, P. (2003) Geldanamycin Inhibits the Production of Inflammatory Cytokines in activated Macrophages by Reducing the Stability and Translation of Cytokine Transcripts. Arthritis & Rheumatology, 48, 541-550. https://doi.org/10.1002/art.10780
[47]
Igarashi, Y., Ohnishi, K., Irie, K. and Murakami, A. (2016) Possible Contribution of Zerumbone-Induced Proteo-Stress to Its Anti-Inflammatory Functions via the Activation of Heat Shock Factor 1. PLoS ONE, 11, e0161282. https://doi.org/10.1371/journal.pone.0161282
[48]
Puri, S.C., Verma, V., Amna, T., Qazi, G.N. and Spiteller, M. (2005) An Endophytic Fungus from Nothapodytes foetida That Produces Camptothecin. Journal of Natural Products, 68, 1717-1719. https://doi.org/10.1021/np0502802
[49]
Kusari, S., Zühlke, S. and Spiteller, M. (2009) An Endophytic Fungus from Camptotheca acuminata That Produces Camptothecin and Analogues. Journal of Natural Products, 72, 2-7. https://doi.org/10.1021/np800455b
[50]
Kusari, S., Zühlke, S. and Spiteller, M. (2011) Effect of Artificial Reconstitution of the Interaction between the Plant Camptotheca acuminata and the Fungal Endophyte Fusarium solani on Camptothecin Biosynthesis. Journal of Natural Products, 74, 764-775. https://doi.org/10.1021/np1008398
[51]
Shweta, S., Zuehlke, S., Ramesha, B.T., Priti, V., Kumar, P.M., et al. (2010) Endophytic Fungal Strains of Fusarium solani, from Apodytes dimidiata E. Mey. ex Arn (Lcacinaceae) Produce Camptothecin, 10-Hydroxycamptothecin and 9-Methoxycamptothecin. Phytochemistry, 71, 117-122. https://doi.org/10.1016/j.phytochem.2009.09.030
[52]
Jia, M., Chen, L., Xin, H.L., Zheng, C.J., Rahman, K., et al. (2016) A Friendly Relationship between Endophytic Fungi and Medicinal Plants: A Systematic Review. Frontiers in Microbiology, 7, 906. https://doi.org/10.3389/fmicb.2016.00906
[53]
Al-Tai, A., Kim, B., Kim, S.B., Manfio, G.P. and Goodfellow, M. (1999) Streptomyces malaysiensis sp. nov., a New Streptomycete Species with Rugose, Ornamented Spores. International Journal of Systematic Bacteriology, 49, 1395-1402. https://doi.org/10.1099/00207713-49-4-1395
[54]
Sazak, A., Şahin, N., Güven, K., Işık, K. and Goodfellow, M. (2011) Streptomyces samsunensis sp. nov., a Member of the Streptomyces violaceusniger Clade Isolated from the Rhizosphere of Robinia pseudoacacia. International Journal of Systematic Bacteriology, 61, 1309-1314. https://doi.org/10.1099/ijs.0.021329-0