Production, characterization and anticancer activity of Candida bombicola sophorolipids by means of solid state fermentation of sunflower oil cake and soybean oil
DOI:
https://doi.org/10.3989/gya.098413Keywords:
Anticancer activity, Candida bombicola, Solid state fermentation, Sophorolipids, Soybean oil, Sunflower oilcakeAbstract
The production of sophorolipids by Candida bombicola NRRL Y- 17069 grown in a mixture of sunflower oil cake and crude soybean oil as economic substrates with different fermentation techniques was studied. The highest yield (49.5 g·100 g−1 substrates) was obtained from solid state fermentation after employing a new concept for extraction by methanol (E I) followed by ethyl acetate (E II), then partially purified with hexane (E III). The course of time of fermentation was also studied, and E I extracted of the 12th day showed the minimum surface tension (45 mN·m−1) at a critical micelle dilution (CMD) of 10% concentration. The produced sophorolipids were characterized and confirmed by FTIR and 1H NMR spectroscopy. The anticancer activity of the produced compounds was assessed against MCF-7, HepG2, A549, HCT116 cancer cell lines and the results revealed that E III and E IV (a mixture of E I & E III) act as promising anticancer agents in HepG2 and A549 by inhibiting urokinase and histone deacetylase activities.
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Amaral PF, Silva Da, Lehocky JM, Barros-Timmons M, Coelho AV, Marrucho MZ. 2006. Production and characterization of a bioemulsifier from Yarrowia lipolytica. Process Biochem. 41, 1894–1898. http://dx.doi.org/10.1016/j.procbio.2006.03.029
Bajaj V, Tilay A, Annapure U. 2012. Enhanced Production of Bioactive Sophorolipids by Starmerella bombicola NRRL Y-17069 by Design of Experiment Approach with Successive Purification and Characterization. J. Oleo Sci. 61, 377–386. http://dx.doi.org/10.5650/jos.61.377 PMid:22790168
Bdeir K, Kuo A, Sachais BS. 2003.The kringle stabilizes urokinase binding to the urokinase receptor. Blood 102, 3600–3608. http://dx.doi.org/10.1182/blood-2003-03-0949 PMid:12881310
Bi G, Jiang G. 2006. The molecular mechanism of HDAC inhibitors in anticancer effects. Cellular Mol. Immunol. 3, 285–290. PMid:16978537
Cavalero DA, Cooper DG. 2003. The effect of medium composition on the structure and physical state of sophorolipids produced by Candida bombicola ATCC22214. J. Biotech. 103, 31–41. http://dx.doi.org/10.1016/S0168-1656(03)00067-1
Chandran P. and Das N. 2011. Characterization of sophorolipid biosurfactant produced by yeast species grownon diesel oil. Internat. J. Sci. Nature 2, 63–71.
Chen J, Song X, Zhang H, Qu Y, Miao J. 2006a. Sophorolipid produced from the new yeast strain Wickerhamiell adomercqiae induces apoptosis in H7402 human liver cancer cells. Appl. Microbiol. Biotech. 72, 52–59. http://dx.doi.org/10.1007/s00253-005-0243-z PMid:16528516
Chen J, Song X, Zhang H, Qu Y. 2006b. Production, structure elucidation and anticancer properties of sophorolipid from Wickerhamiell adomercqiae. Enzyme Microb. Tech. 39, 501–506. http://dx.doi.org/10.1016/j.enzmictec.2005.12.022
Daniel HJ, Otto RT, Reuss M, Syldatk C. 1998. Sophorolipid production with high yields on whey concentrate and rapeseed oil without consumption of lactose. Biotech. Letter 20, 805–807. http://dx.doi.org/10.1023/B:BILE.0000015927.29348.1a
Daverey A, Pakshirajan K. 2009. Production, characterization, and properties of sophorolipids from the yeast Candida bombicola using a low-cost fermentative medium. Appl Biochem Biotech. 158, 663–674. http://dx.doi.org/10.1007/s12010-008-8449-z PMid:19082764
Daverey A, Pakshirajan K. 2010. Sophorolipids from Candida bombicola using mixed hydrophilic substrates: production, purification and characterization. Colloid Surface B 79, 246–253. http://dx.doi.org/10.1016/j.colsurfb.2010.04.002 PMid:20427162
Duffy MJ, Duggan C. 2004. The urokinase plasminogen activator system: a rich source of tumour markers for the individualised management of patients with cancer. Clin. Biochem. 37, 541–548. http://dx.doi.org/10.1016/j.clinbiochem.2004.05.013 PMid:15234235
Felse PA, Shah V, Chan J, Rao KJ, Gross RA. 2007. Sophorolipid biosynthesis by Candida bombicola from industrial fatty acid residues. Enzyme Microb. Tech. 40, 316–323. http://dx.doi.org/10.1016/j.enzmictec.2006.04.013
Fu SL, Wallner SR, Bowne WB, Hagler MD, Zenilman ME, Gross R, Bluth MH. 2008. Sophorolipids and their derivatives are lethal against human pancreatic cancer cells. J. Surg. Res. 148, 77–82. http://dx.doi.org/10.1016/j.jss.2008.03.005 PMid:18570934
Gao W, Hagver R, Shah V, Xie W, Gross RA, Ilker MF, Bell C, Burke KA, Coughlin EB. 2007. Glycolipid polymer synthesized from natural lactonic sophorolipids by ring-opening metathesis polymerization. Macromolecules 40, 145–147. http://dx.doi.org/10.1021/ma0620159
Gorin PAJ, Spencer JFT, Tulloch AP. 1961. Hydroxy fatty acid glycosides of sophorose from Torulopsis magnoliae. Can. J. Chem. 39, 846–855. http://dx.doi.org/10.1139/v61-104
Haba E, Espuny MJ, Busquets M, Manresa A. 2000. Screening and production of rhamnolipids by Pseudomonas aeruginosa 47T2 NCIB 40044 from waste frying oils. J. Appl. Microb. 88, 379–387. http://dx.doi.org/10.1046/j.1365-2672.2000.00961.x PMid:10747218
Hu Y, Ju L K. 2001. Purification of lactonic sophorolipids by crystallization. J. Biotechnol. 87, 263–272. http://dx.doi.org/10.1016/S0168-1656(01)00248-6
Hu E, Chen Z, Fredrickson T, Zhu Y, Kirkpatrick R, Zhang GF, Johanson K, Sung CM, Liu R, Winkler J. 2000. Cloning and characterization of a novel human class I histone deacetylase that functions as a transcription repressor. J. Biol. Chem. 275, 15254–15264. http://dx.doi.org/10.1074/jbc.M908988199 PMid:10748112
Kim HS, Kim YB, Lee BS, Kim EK. 2005. Sophorolipid production by Candida bombicola ATCC 22214 from a corn-oil processing byproduct. J. Microb. Biotech. 15, 55–58.
Kim HS, Yoon BD, Choung DH, Oh HM, Katsuragi T, Tani Y. 1999. Characterization of a biosurfactant, mannosyl erythritol lipid produced from Candida sp. SY16. Appl. Microbiol. Biotechnol. 52, 713–721. http://dx.doi.org/10.1007/s002530051583 PMid:10570818
Komatsu Y, Hayashi H. 1998. Histone deacetylase inhibitors upregulate the expression of cell surface MHC class-I molecules in B16/BL6 cells. J. Antibiot. 51, 89–91. http://dx.doi.org/10.7164/antibiotics.51.89 PMid:9531994
Komatsu Y, Tomizaki K, Tsukamoto M, Kato T, Nishino N, Sato S, Yamori T, Tsuruo T, Furumai R, Yoshida M, Horinouchi S, Hayashi H. 2001. Cyclichydroxamic-acid-containing peptide 31, a potent synthetic histone deacetylase inhibitor with antitumor activity. Cancer Res. 61, 4459–4466. PMid:11389076
Lee YJ, Choi JK, Kim EK, Youn SH, Yang EJ. 2008. Field experiments on mitigation of harmful algal blooms using a sophorolipid–yellow clay mixture and effects on marine plankton. Harmful Algae 7, 154–162. http://dx.doi.org/10.1016/j.hal.2007.06.004
Li H, Ma X, Wang S, Song X. 2013. Production of sophorolipids with eicosapentaenoic acid and docosahexaenoic acid from Wickerhamiella domercqiae var. sophorolipid using fish oil as a hydrophobic carbon source. Biotechnol. Lett. 35, 901–908. http://dx.doi.org/10.1007/s10529-013-1151-4 PMid:23386226
Makkar RS, Cameotra SS. 1997. Utilization of molasses for biosurfactant production by two Bacillus strains at thermophilic conditions. J. Am. Oil Chem. Soc. 74, 887–889. http://dx.doi.org/10.1007/s11746-997-0233-7
McInerney MJ, Youssef N, Fincher T, Maudgalya SK, Folmsbee MJ, Knapp R, Nagle D. 2004. Development of Microorganisms with Improved Transport and Biosurfactant Activity for Enhanced Oil Recovery. Annual Report Department of Botany and Microbiology and Department of Petroleum Engineering University of Oklahoma. http://dx.doi.org/10.2172/834168
Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55–63. http://dx.doi.org/10.1016/0022-1759(83)90303-4
Nampoothiri KM, Ramachandran S, Soccol CR, Pandey A. 2002. Advances in fermentation technology. Int. Sugar J. 104, 493–499.
Napolitano LM. 2006. Sophorolipids in sepsis: Anti-inflammatory or antibacterial? Crit. Care Med. 34, 258–259. http://dx.doi.org/10.1097/01.CCM.0000196082.26483.F0 PMid:16374196
Nitschke M, Pastore GM. 2006. Production and properties of a surfactant obtained from Bacillus subtilis grown on cassava wastewater. Bioresour. Technol. 97, 336–341. http://dx.doi.org/10.1016/j.biortech.2005.02.044 PMid:16171690
Ohno A, Ano T, Shoda N. 1995. Production of a lipopeptide antibiotic, surfactin, by recombinant Bacillus subtilis in solid state fermentation. Biotechnol. Bioeng. 47, 209–214. http://dx.doi.org/10.1002/bit.260470212 PMid:18623394
Pandey A, Selvakumar P, Soccol CR, Nigam P. 1999. Solid state fermentation for the production of industrial enzymes. Curr. Sci. 77, 149–162.
Parekh VJ, Patravale VB, Pandit AB. 2012. Mango kernel fat: A novel lipid source for the fermentative production of sophorolipid biosurfactant using Starmerella Bombicola NRRL-Y 17069. Annals Biol. Res. 3, 1798–1803.
Ramachandran S, Singh SK, Larroche C, Soccol, CR, Pandey A. 2007. Oil cakes and their biotechnological applications. Bioresour Technol. 98, 2000–2009. http://dx.doi.org/10.1016/j.biortech.2006.08.002 PMid:17023161
Rashad MM, Mahmoud AE, Al-Kashef AS, Nooman MU. 2012. Purification and Characterization of Novel Fibrinolytic Enzyme by Candida guilliermondii Grown on Sunflower Oil Cake. J. Appl. Sci. Res. 8, 635–645.
Roongsawang N, Thaniyavarn J, Thaniyavarn S, Kameyama T, Haruki M, Imanaka T, Morikawa M, Kanaya S. 2002. Isolation and characterization of a halotolerant Bacillus subtilis BBK-1 which produces three kinds of lipopeptides: bacillomycin L, plipastatin, and surfactin. Extremophiles 6, 499–506. http://dx.doi.org/10.1007/s00792-002-0287-2 PMid:12486459
Roopesh K, Ramachandran S, Nampoothiri KM, Szakacs G, Pandey A. 2006. Comparison of phytase production on wheat bran and oil cakes in solid-state fermentation by Mucor racemosus. Bioresour Technol. 97, 506–511. http://dx.doi.org/10.1016/j.biortech.2005.02.046 PMid:15979307
Shah V, Doncel GF, Seyoum T, Eaton KM, Zalenskaya I, Hagver R, Azim A, Gross R. 2005. Sophorolipids, microbial glycolipids with anti-human immunodeficiency virus and sperm-immobilizing activities. Antimicrob. Agents Chemother. 49, 4093–4100. http://dx.doi.org/10.1128/AAC.49.10.4093-4100.2005 PMid:16189085 PMCid:PMC1251511
Shao L, Song X, Ma X, Li H, Qu Y. 2012. Bioactivities of Sophorolipid with Different Structures Against Human Esophageal Cancer Cells. J. Surg. Res. 173, 286–291. http://dx.doi.org/10.1016/j.jss.2010.09.013 PMid:21035135
Sitohy MZ, Rashad MM, Sharobeem SF, Abeer EM, Nooman MU, AlKashef AS. 2010. Bioconversion of soy processing waste for production of surfactants. Afr. J. Microbiol. Res. 4, 2811– 2821.
Sobrinho HBS, Rufino RD, Luna JM, Salgueiro AA, Campos-Takaki GM, Leite LFC, Sarubbo LA. 2008. Utilization of two agroindustrial by products for the production of a surfactant by Candida sphaerica UCP0995. Process Biochem. 43, 912–917. http://dx.doi.org/10.1016/j.procbio.2008.04.013
Soccol CR, Brand D, Mohan R, Rodriguez JAL, Pandey A. 2005. Coffee husk: a potential alternative material for bioprocesses. Metals Mater Process 17, 195–206.
Solaiman DKY, Ashby RD, Nunez A, Foglia TA. 2004. Production of sophorolipids by Candida bombicola grown on soy molasses as substrate. Biotechnol. Lett. 26, 1241–1245. http://dx.doi.org/10.1023/B:BILE.0000036605.80577.30 PMid:15289681
Spencer JFT, Gorin PAJ, Tulloch AP. 1970. Torulopsis bombicola sp. n. Antonie Leeuwenhoek 36, 129–133. http://dx.doi.org/10.1007/BF02069014 PMid:5310304
Sudha S, KumananR, Vijayashree P, Muthusamy K. 2010. Comparative study for the production, characterization and antimicrobial studies of sophorolipids using candida Tropicalis. Asian J. Pharm. Clin. Res. 3, 69–72.
Thaniyavarn J, Chianguthai T, Sangvanich P, Roongsawang N, Washio K, Morikawa M, Thaniyavarn S. 2008. Production of sophorolipid biosurfactant by Pichia anomala. Biosci. Biotech. Bioch. 72, 2061–2068. http://dx.doi.org/10.1271/bbb.80166 PMid:18685212
Thavasi R, jayalakshmi S, Balasubramanian T, Banat IM. 2008. Production and characterization of a glycolipid biosurfactant from Bacillus megaterium using economically cheaper sources. World J. Microbiol. Biotechnol. 24, 917–925. http://dx.doi.org/10.1007/s11274-007-9609-y
Tulloch AP, Spencer JFT, Deinema MH. 1968. A new hydroxy fatty acid sophoroside from Candida bogoriensis. Can. J. Chem. 46, 345–348. http://dx.doi.org/10.1139/v68-057
Üstun GL, Kent NC, Civelekoglu H. 1990. Investigation of the technological properties of Nigella sativa (Black cumin) seed oil. J. Am. Oil Chem. Soc. 67, 958–960. http://dx.doi.org/10.1007/BF02541857
Vandenberghe LPS, Soccol CR, Pandey A, Lebeault JM. 2000. Solid-state fermentation for the synthesis of citric acid by Aspergillus niger. Bioresour Technol. 74, 175–178. http://dx.doi.org/10.1016/S0960-8524(99)00107-8
Walkinshaw DR, Yang XJ. 2008. Histone deacetylase inhibitors as novel anticancer therapeutics. Current Oncolog. 15, 237–243. PMid:19008999 PMCid:PMC2582508
Wei YH, Chou CL, Chang JS. 2005. Rhamnolipid production by indigenous Pseudomonas aeruginosa J4 originating from petrochemical wastewater. Biochem. Eng. J. 27, 146–154. http://dx.doi.org/10.1016/j.bej.2005.08.028
Wickerman LJ. 1951. "Taxonomy of yeasts", US Department of Agriculture Technical Bulletin, No. 1029, Washington, pp. 1–56.
Yongmei H and Lu-Kwang J. 2001.Sophorolipid production from different lipid precursors observed with LC-MS. Enzyme Microb. Tech. 29, 593–601. http://dx.doi.org/10.1016/S0141-0229(01)00439-2
Yoo DS, Lee BS, Kim EK. 2005. Characteristics of microbial biosurfactant as an antifungal agent against plant pathogenic fungus. J. Microbiol. Biotechnol. 15, 1164–1169.
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