Bioprocessing of Epothilone B from Aspergillus fumigatus under solid state fermentation: Antiproliferative activity, tubulin polymerization and cell cycle analysis.
Anti-tubulin polymerization
Apoptosis
Aspergillus fumigatus
Epothilone
Solid state fermentation
Journal
BMC microbiology
ISSN: 1471-2180
Titre abrégé: BMC Microbiol
Pays: England
ID NLM: 100966981
Informations de publication
Date de publication:
30 Jan 2024
30 Jan 2024
Historique:
received:
07
10
2023
accepted:
08
01
2024
medline:
31
1
2024
pubmed:
31
1
2024
entrez:
30
1
2024
Statut:
epublish
Résumé
Epothilone derivatives have been recognized as one of the most powerful anticancer drugs towards solid tumors, for their unique affinity to bind with β-tubulin microtubule arrays, stabilizing their disassembly, causing cell death. Sornagium cellulosum is the main source for Epothilone, however, the fermentation bioprocessing of this myxobacteria is the main challenge for commercial production of Epothilone. The metabolic biosynthetic potency of epothilone by Aspergillus fumigatus, an endophyte of Catharanthus roseus, raises the hope for commercial epothilone production, for their fast growth rate and feasibility of manipulating their secondary metabolites. Thus, nutritional optimization of A. fumigatus for maximizing their epothilone productivity under solid state fermentation process is the objective. The highest yield of epothilone was obtained by growing A. fumigatus on orange peels under solid state fermentation (2.2 μg/g), bioprocessed by the Plackett-Burman design. The chemical structure of the extracted epothilone was resolved from the HPLC and LC-MS/MS analysis, with molecular mass 507.2 m/z and identical molecular fragmentation pattern of epothilone B of S. cellulosum. The purified A. fumigatus epothilone had a significant activity towards HepG2 (IC
Identifiants
pubmed: 38291363
doi: 10.1186/s12866-024-03184-w
pii: 10.1186/s12866-024-03184-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
43Informations de copyright
© 2024. The Author(s).
Références
Bollag DM, McQueney PA, Zhu J, Hensens O, Koupal L, Jerrold Liesch MG, et al. Epothilones, a new class of microtubule-stabilizing agents with a taxol-like mechanism of action. Chemtracts. 1998;11:671–7.
Mühlradt PF, Sasse F. Epothilone B stabilizes microtubuli of macrophages like Taxol without showing Taxol-like endotoxin activity. Cancer Res. 1997;57:3344–6.
pubmed: 9269992
Kowalski RJ, Giannakakou P, Hamel E. Activities of the microtubule-stabilizing agents epothilones A and B with purified tubulin and in cells resistant to paclitaxel (Taxol®). J Biol Chem. 1997;272:2534–41.
pubmed: 8999970
doi: 10.1074/jbc.272.4.2534
Reichenbach H, Höfle G. Discovery and development of the epothilones: A novel class of antineoplastic drugs. Drugs in R and D. 2008;9:1–10.
pubmed: 18095749
pmcid: 7044396
doi: 10.2165/00126839-200809010-00001
Cheng KL, Bradley T, Budman DR. Novel microtubule-targeting agents - the epothilones. Biologics. 2008;2:789–811.
pubmed: 19707459
pmcid: 2727900
Villegas C, González-Chavarría I, Burgos V, Iturra-Beiza H, Ulrich H, Paz C. Epothilones as natural compounds for novel anticancer drugs development. Int J Mol Sci. 2023;6063
Lee JJ, Swain SM. The epothilones: translating from the laboratory to the clinic. Clin Cancer Res. 2008;14:1618–24.
pubmed: 18347162
doi: 10.1158/1078-0432.CCR-07-2201
Gerth K, Bedorf N, Höfle G, Irschik H, Reichenbach H. Epothilons A and B: antifungal and cytotoxic compounds from Sorangium cellulosum (Myxobacteria) production, physico-chemical and biological properties. J Antibiot. 1996;49:560–3.
doi: 10.7164/antibiotics.49.560
Puhalla S, Brufsky A. Ixabepilone: a new chemotherapeutic option for refractory metastatic breast cancer. Biologics. 2008;2:505.
pubmed: 19707381
pmcid: 2721395
Penazzi L, Tackenberg C, Ghori A, Golovyashkina N, Niewidok B, Selle K, et al. Aβ-mediated spine changes in the hippocampus are microtubule-dependent and can be reversed by a subnanomolar concentration of the microtubule-stabilizing agent epothilone D. Neuropharmacol Pergamon. 2016;105:84–95.
doi: 10.1016/j.neuropharm.2016.01.002
Shimkets LJ. Social and developmental biology of the myxobacteria. Microbiol Rev. 1990;54:473–501.
pubmed: 1708086
pmcid: 372790
doi: 10.1128/mr.54.4.473-501.1990
Li PF, Li SG, Li ZF, Zhao L, Wang T, Pan HW, et al. Co-cultivation of Sorangium cellulosum strains affects cellular growth and biosynthesis of secondary metabolite epothilones. FEMS Microbiol Ecol. 2013;85:358–68.
pubmed: 23551077
doi: 10.1111/1574-6941.12125
El-Sayed ASA, Shindia AA, Ali GS, Yassin MA, Hussein H, Awad SA, et al. Production and bioprocess optimization of antitumor Epothilone B analogue from aspergillus fumigatus, endophyte of Catharanthus roseus, with response surface methodology. Enzym Microb Technol. 2021;143:109718.
doi: 10.1016/j.enzmictec.2020.109718
El-Ghareeb DK, Osman GH, El Baz AF. Isolation, cloning, and overexpression of vip3Aa gene isolated from a local Bacillus thuringiensis. Biocontrol Sci Technol. 2012;22(1):11–21.
doi: 10.3390/jof6030137
Singhania RR, Sukumaran RK, Patel AK, Larroche C, Pandey A. Advancement and comparative profiles in the production technologies using solid-state and submerged fermentation for microbial cellulases. Enzym Microb Technol. 2010;46:541–9.
doi: 10.1016/j.enzmictec.2010.03.010
Thomas L, Larroche C, Pandey A. Current developments in solid-state fermentation. Biochem Eng J. 2013;81:146–61.
doi: 10.1016/j.bej.2013.10.013
Ajila CM, Brar SK, Verma M, Tyagi RD, Valéro JR. Solid-state fermentation of apple pomace using Phanerocheate chrysosporium – liberation and extraction of phenolic antioxidants. Food Chem. 2011;126:1071–80.
doi: 10.1016/j.foodchem.2010.11.129
El-Sayed ASA, Shindia AA, Zeid AAA, Yassin AM, Sitohy MZ, Sitohy B. Aspergillus nidulans thermostable arginine deiminase-dextran conjugates with enhanced molecular stability, proteolytic resistance, pharmacokinetic properties and anticancer activity. Enzym Microb Technol. 2019;131:109432.
doi: 10.1016/j.enzmictec.2019.109432
Regentin R, Frykman S, Lau J, Tsuruta H, Licari P. Nutrient regulation of epothilone biosynthesis in heterologous and native production strains. Appl Microbiol Biotechnol. 2003;61:451–5.
pubmed: 12764559
doi: 10.1007/s00253-003-1263-1
Lau J, Frykman S, Regentin R, Ou S, Tsuruta H, Licari P. Optimizing the heterologous production of epothilone D in Myxococcus xanthus. Biotechnol Bioeng. 2002;78:280–8.
pubmed: 11920444
doi: 10.1002/bit.10202
Caputo L, Cornara L, Bazzicalupo M, De Francesco C, De Feo V, Trombetta D, et al. Chemical composition and biological activities of essential oils from peels of three Citrus species. Molecules. 2020:25.
El-Sayed ASA. Purification and characterization of a new L-methioninase from solid cultures of aspergillus flavipes. J Microbiol. 2011;49:130–40.
pubmed: 21369990
doi: 10.1007/s12275-011-0259-2
El-Sayed AS, Khalaf SA, Aziz HA. Characterization of homocysteine γ-lyase from submerged and solid cultures of aspergillus fumigatus ASH (JX006238). J Microbiol Biotechnol. 2013;23:499–510.
pubmed: 23568204
doi: 10.4014/jmb.1208.08070
El-Sayed ASA. L-glutaminase production by Trichoderma koningii under solid-state fermentation. Indian J Microbiol. 2009;49:243–50.
pubmed: 23100777
pmcid: 3450012
doi: 10.1007/s12088-009-0020-2
El-Sayed ASA. L-methioninase production by aspergillus flavipes under solid-state fermentation. J Basic Microbiol. 2009;49:331–41.
pubmed: 19455514
doi: 10.1002/jobm.200800318
Cao W, Gong G, Liu X, Hu W, Li Z, Liu H, et al. Optimization of epothilone B production by Sorangium cellulosum using multiple steps of the response surface methodology. African J Biotechnol. 2014;10(53):11058–70.
Namdeo AG, Sharma A. HPLC analysis of camptothecin content in various parts of Nothapodytes foetida collected on different periods. Asian Pac J Trop Biomed. 2012;2:389–93.
pubmed: 23569936
pmcid: 3609305
doi: 10.1016/S2221-1691(12)60062-8
El-Sayed ASA, Zayed RA, El-Baz AF, Ismaeil WM. Bioprocesses optimization and anticancer activity of camptothecin from aspergillus flavus, an endophyte of in vitro cultured Astragalus fruticosus. Mol Biol Rep. 2022;49:4349–64.
pubmed: 35312933
doi: 10.1007/s11033-022-07271-x
El-Sayed ASA, Hassan WHB, Sweilam SH, Alqarni MHS, El Sayed ZI, Abdel-Aal MM, et al. Production, bioprocessing and anti-proliferative activity of camptothecin from penicillium chrysogenum, an endozoic of marine sponge, cliona sp., as a metabolically stable camptothecin producing isolate. Molecules. 2022;27:3033.
pubmed: 35566384
pmcid: 9104752
doi: 10.3390/molecules27093033
Jin F. LC–MS for in Vitro Determination of a Novel Epothilone D Derivative (Epo D 7-HD) in Human Plasma. Chromatographia. 2015;71:923–6.
Lu HM, Ye M. LC-MS/MS method for determination of epothilone B in rat plasma and its application in pharmacokinetic study. Arzneimittelforschung/Drug Res. 2012;62:609–13.
doi: 10.1055/s-0032-1327695
Eldeghidy A, Abdel-Fattah G, El-Sayed ASA, Abdel-Fattah GG. Production, bioprocessing and antiproliferative activity of camptothecin from aspergillus terreus, endophyte of Cinnamomum camphora: restoring their biosynthesis by indigenous microbiome of C. Camphora. Microb Cell Factories. 2023;22:143.
doi: 10.1186/s12934-023-02158-3
El-Sayed ASA, Khalaf SA, Azez HA, Hussein HA, El-Moslamy SH, Sitohy B, et al. Production, bioprocess optimization and anticancer activity of Camptothecin from aspergillus terreus and aspergillus flavus, endophytes of Ficus elastica. Process Biochem. 2021;107:59–73.
doi: 10.1016/j.procbio.2021.05.007
El-Sayed ASA, George NM, Abou-Elnour A, El-Mekkawy RM, El-Demerdash MM. Production and bioprocessing of camptothecin from aspergillus terreus, an endophyte of Cestrum parqui, restoring their biosynthetic potency by Citrus limonum peel extracts. Microb Cell Factories. 2023;22:1–14.
doi: 10.1186/s12934-022-02012-y
Zhang Y, Bilbao A, Bruderer T, Luban J, Strambio-De-Castillia C, Lisacek F, et al. The use of variable Q1 isolation windows improves selectivity in LC-SWATH-MS acquisition. J Proteome Res. 2015;14:4359–71.
pubmed: 26302369
doi: 10.1021/acs.jproteome.5b00543
Ahmed EA, El-Derany MO, Anwar AM, Saied EM, Magdeldin S. Metabolomics and Lipidomics screening reveal reprogrammed signaling pathways toward Cancer development in non-alcoholic Steatohepatitis. Int J Mol Sci. 2023;24
Cory AH, Owen TC, Barltrop JA, Cory JG. Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture. Cancer commun. 1991;3:207–12.
pubmed: 1867954
doi: 10.3727/095535491820873191
Bates AD, Maxwell A. DNA topology: topoisomerases keep it simple. Curr Biol. 1997;7(12):R778–81.
pubmed: 9382831
doi: 10.1016/S0960-9822(06)00403-9
El-Sayed ASA, Fathalla M, Yassin MA, Zein N, Morsy S, Sitohy M, Sitohy B. Conjugation of Aspergillus flavipes taxol with porphyrin increases the anticancer activity of taxol and ameliorates its cytotoxic effects. Molecules. 2020;25(2):263.
doi: 10.1017/S003358350800468X
Tariq A, Green L, Jeynes JCG, Soeller C, Wakefield JG. In vitro reconstitution of branching microtubule nucleation. eLife. 2020;9:e49769.
pubmed: 31933481
pmcid: 6959987
doi: 10.7554/eLife.49769
El-Sayed ASA, Ibrahim H, Sitohy MZ. Co-immobilization of PEGylated Aspergillus flavipes l-methioninase with glutamate dehydrogenase: A novel catalytically stable anticancer consortium. Enzyme Microb Technol. 2014;54(1):59–69.
pubmed: 3972806
doi: 10.1016/S0021-9258(18)89437-6
Skok Ž, Zidar N, Kikelj D, Ilaš J. Dual inhibitors of human DNA topoisomerase II and other Cancer-related targets. J Med Chem. 2020;63:884–904.
pubmed: 31592646
doi: 10.1021/acs.jmedchem.9b00726
Kanaze FI, Termentzi A, Gabrieli C, Niopas I, Georgarakis M, Kokkalou E. The phytochemical analysis and antioxidant activity assessment of orange peel (Citrus sinensis) cultivated in Greece-Crete indicates a new commercial source of hesperidin. Biomed Chromatogr. 2009;23:239–49.
pubmed: 18823075
doi: 10.1002/bmc.1090
Manthey JA, Grohmann K. Phenols in citrus peel byproducts. Concentrations of hydroxycinnamates and polymethoxylated flavones in citrus peel molasses. J Agric Food Chem. 2001;49:3268–73.
pubmed: 11453761
doi: 10.1021/jf010011r
Peterson JJ, Dwyer JT, Beecher GR, Bhagwat SA, Gebhardt SE, Haytowitz DB, et al. Flavanones in oranges, tangerines (mandarins), tangors, and tangelos: a compilation and review of the data from the analytical literature. J Food Compos Anal. 2006;93:S66–73.
doi: 10.1016/j.jfca.2005.12.006
L-Amino acid oxidase from filamentous fungi: Screening and optimization. Ann Microbiol. 2012;62(2):773–84.
Gao J, Weng H, Zhu D, Yuan M, Guan F, Xi Y. Production and characterization of cellulolytic enzymes from the thermoacidophilic fungal aspergillus terreus M11 under solid-state cultivation of corn Stover. Bioresour Technol. 2008;99:7623–9.
pubmed: 18346891
doi: 10.1016/j.biortech.2008.02.005
El-Sayed AS, Khalaf SA, Abdel-Hamid G, El-Batrik MI. Screening, morphological and molecular characterization of fungi producing cystathionine γ-lyase. Acta Biologica Hungarica. 2015;66(1)119–32.
doi: 10.1016/0167-7799(85)90092-7
Mahanta N, Gupta A, Khare SK. Production of protease and lipase by solvent tolerant Pseudomonas aeruginosa PseA in solid-state fermentation using Jatropha curcas seed cake as substrate. Bioresour Technol. 2008;99:1729–35.
pubmed: 17509877
doi: 10.1016/j.biortech.2007.03.046
Abdel-Fatah SS, El-Sherbiny GM, Khalaf M, Baz AFE, ASA E-S, El-Batal AI. Boosting the anticancer activity of aspergillus flavus “endophyte of jojoba” Taxol via conjugation with gold nanoparticles mediated by γ-irradiation. Appl Biochem Biotechnol. 2022;194:3558–81.
pubmed: 35438406
pmcid: 9270289
doi: 10.1007/s12010-022-03906-8
Abdel-Fatah SS, El-Batal AI, El-Sherbiny GM, Khalaf MA, El-Sayed AS. Production, bioprocess optimization and γ-irradiation of Penicillium polonicum, as a new Taxol producing endophyte from Ginko biloba. Biotechnol Rep. 2021;30:e00623.
doi: 10.1016/j.btre.2021.e00623
El-Sayed ASA, Mohamed NZ, Yassin MA, Amer MM, El-Sharkawy R, El-Sayed N, et al. Microbial cytosine deaminase is a programmable anticancer prodrug mediating enzyme: antibody, and gene directed enzyme prodrug therapy. Heliyon. 2022;8:e10660.
pubmed: 36164544
pmcid: 9508425
doi: 10.1016/j.heliyon.2022.e10660
Mandenius CF, Brundin A. Bioprocess optimization using design-of-experiments methodology. Biotechnol Prog. 2008;24:1191–203.
pubmed: 19194932
doi: 10.1002/btpr.67
DeJong JHM, Liu Y, Bollon AP, Long RM, Jennewein S, Williams D, et al. Genetic engineering of taxol biosynthetic genes in Saccharomyces cerevisiae. Biotechnol Bioeng. 2006;93:212–24.
pubmed: 16161138
doi: 10.1002/bit.20694
Fumoleau P, Coudert B, Isambert N, Ferrant E. Novel tubulin-targeting agents: anticancer activity and pharmacologic profile of epothilones and related analogues. Ann Oncol. 2007;18:v9–15.
pubmed: 17656562
doi: 10.1093/annonc/mdm173
Kline-Smith SL, Walczak CE. Mitotic spindle assembly and chromosome segregation: refocusing on microtubule dynamics. Mol Cell. 2004;15(3):317–27.
pubmed: 15304213
doi: 10.1016/j.molcel.2004.07.012
Dumontet C, Jordan MA. Microtubule-binding agents: A dynamic field of cancer therapeutics [internet]. Nature reviews drug discovery. Nat Rev Drug Discov. 2010:790–803.
Jordan MA, Toso RJ, Thrower D, Wilson L. Mechanism of mitotic block and inhibition of cell proliferation by taxol at low concentrations. Proc Natl Acad Sci U S A. 1993;90:9552–6.
pubmed: 8105478
pmcid: 47607
doi: 10.1073/pnas.90.20.9552
Andreu JM, Barasoain I. The-interaction of baccatin III with the Taxol binding site of microtubules determined by a homogeneous assay with fluorescent taxoid. Biochemistry. 2001;40:11975–84.
pubmed: 11580273
doi: 10.1021/bi010869+
Orr GA, Verdier-Pinard P, McDaid H, Horwitz SB. Mechanisms of Taxol resistance related to microtubules. Oncogene. 2003;22(47):7280–95.
pubmed: 14576838
pmcid: 4039039
doi: 10.1038/sj.onc.1206934
Rai SS, Wolff J. Dissociation of tubulin assembly-inhibiting and aggregation-promoting activities by a vinblastine derivative. FEBS Lett. 1997;416:251–3.
pubmed: 9373163
doi: 10.1016/S0014-5793(97)01211-8
Arita K, Hashimoto H, Shimizu T, Nakashima K, Yamada M, Sato M. Structural basis for Ca2+−induced activation of human PAD4. Nat Struct Mol Biol. 2004;11:777–83.
pubmed: 15247907
doi: 10.1038/nsmb799
Ruschel J, Hellal F, Flynn KC, Dupraz S, Elliott DA, Tedeschi A, et al. Systemic Administration of Epothilone B Promotes Axon Regeneration and Functional Recovery after spinal cord injury. Science. 2015;348:347.
pubmed: 25765066
pmcid: 4445125
doi: 10.1126/science.aaa2958
Rogalska A, Marczak A, Gajek A, Szwed M, Śliwińska A, Drzewoski J, et al. Induction of apoptosis in human ovarian cancer cells by new anticancer compounds, epothilone A and B. Toxicology in vitro : an international journal published in association with BIBRA. Toxicol Vitro. 2013;27:239–49.
doi: 10.1016/j.tiv.2012.09.006
Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science. 1995;267:1456–62.
pubmed: 7878464
doi: 10.1126/science.7878464
Martin TA, Jiang WG. Loss of tight junction barrier function and its role in cancer metastasis. Biochim Biophys Acta – Bioenerg. 2009;1788(4):872–91.
doi: 10.1016/j.bbamem.2008.11.005
Chen P, Kuang P, Wang L, Li W, Chen B, Liu Y, et al. Mechanisms of drugs-resistance in small cell lung cancer: DNA-related, RNA-related, apoptosis-related, drug accumulation and metabolism procedure. Transl Lung Cancer Res. 2020;9(3):768–86.
pubmed: 32676338
pmcid: 7354133
doi: 10.21037/tlcr-19-547