Covid-19 Research

Review Article

OCLC Number/Unique Identifier: 9501836416

Epigenetic Strategies to Discover Novel Fungal Secondary Metabolites

Medicine Group    Start Submission

Komal Anjum* and Ye Xuewei

Volume3-Issue3
Dates: Received: 2022-02-22 | Accepted: 2022-03-08 | Published: 2022-03-11
Pages: 246-263

Abstract

Natural product search is an enduring revitalization upon the exploration of a huge already exotic potential for Secondary Metabolite (SM) production obscure in microbial genomes.

Filamentous fungi genomes have an immense number of “orphan” SM gene clusters. Current evaluation indicates that only 5% of extant fungal species have been explored, thus the apparent for the disclosure of novel metabolites in fungi is extensive. In this situation, fungi burgeoning in severe environments are of special interest since they are distinguished producers of astonishing chemical structures. Genome mining strategies, more specifically epigenetic strategies are playing an important role in natural product discovery. This review has been organized and written to focus on available epigenetic approaches, targeting on DNA methyltransferase and histone deacetylase inhibitors along with reported novel secondary metabolites. To the best of our knowledge, this review article is the first attempt to incorporate the facts regarding DNA methyltransferase inhibitors and histone deacetylase inhibitors along with reported novel secondary metabolites with their recorded bioactivities.

FullText HTML FullText PDF DOI: 10.37871/jbres1430


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© 2022 Anjum K, et al. Distributed under Creative Commons CC-BY 4.0

How to cite this article

Anjum K, Xuewei Y. Epigenetic Strategies to Discover Novel Fungal Secondary Metabolites. J Biomed Res Environ Sci. 2022 Mar 11; 3(3): 246-263. doi: 10.37871/jbres1430, Article ID: JBRES1430, Available at: https://www.jelsciences.com/articles/jbres1430.pdf


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References


  1. Schulz B, Boyle C, Draeger S, Römmert A. Endophytic fungi: A source of novel biologically active secondary metabolites. Published online by Cambridge University Press. 2002;106:996-1004. doi: 10.1017/S0953756202006342.
  2. Cichewicz R. Epigenetic regulation of secondary metabolite biosynthetic genes in fungi. In: Witzany G. editor. Biocommunication of Fungi. Springer: Dordrecht; 2012. doi:10.1007/978-94-007-4264-2_4.
  3. Cichewicz RH. Epigenome manipulation as a pathway to new natural product scaffolds and their congeners. Nat Prod Rep. 2010 Jan;27(1):11-22. doi: 10.1039/b920860g. Epub 2009 Oct 27. PMID: 20024091; PMCID: PMC2958777.
  4. Williams RB, Henrikson JC, Hoover AR, Lee AE, Cichewicz RH. Epigenetic remodeling of the fungal secondary metabolome. Org Biomol Chem. 2008 Jun 7;6(11):1895-7. doi: 10.1039/b804701d. Epub 2008 Apr 14. PMID: 18480899.
  5. Henrikson JC, Hoover AR, Joyner PM, Cichewicz RH. A chemical epigenetics approach for engineering the in situ biosynthesis of a cryptic natural product from Aspergillus niger. Org Biomol Chem. 2009 Feb 7;7(3):435-8. doi: 10.1039/b819208a. Epub 2008 Dec 11. PMID: 19156306.
  6. Zhang S, Fang H, Yin C, Wei C, Hu J, Zhang Y. Antimicrobial Metabolites Produced by Penicillium mallochii CCH01 Isolated From the Gut of Ectropis oblique, Cultivated in the Presence of a Histone Deacetylase Inhibitor. Front Microbiol. 2019 Oct 2;10:2186. doi: 10.3389/fmicb.2019.02186. PMID: 31632360; PMCID: PMC6783908.
  7. Liu W, Wang L, Wang B, Xu Y, Zhu G, Lan M, Zhu W, Sun K. Diketopiperazine and Diphenylether Derivatives from Marine Algae-Derived Aspergillus versicolor OUCMDZ-2738 by Epigenetic Activation. Mar Drugs. 2018 Dec 22;17(1):6. doi: 10.3390/md17010006. PMID: 30583513; PMCID: PMC6356248.
  8. Zhu JX, Ding L, He S. Discovery of a new biphenyl derivative by epigenetic manipulation of marine-derived fungus Aspergillus versicolor. Nat Prod Res. 2019 Apr;33(8):1191-1195. doi: 10.1080/14786419.2018.1465423. Epub 2018 Apr 23. PMID: 29683350.
  9. Igboeli HA, Marchbank DH, Correa H, Overy D, Kerr RG. Discovery of Primarolides A and B from Marine Fungus Asteromyces cruciatus Using Osmotic Stress and Treatment with Suberoylanilide Hydroxamic Acid. Mar Drugs. 2019 Jul 24;17(8):435. doi: 10.3390/md17080435. PMID: 31344982; PMCID: PMC6723326.
  10. Jasim B, Sahadevan N, Chithra S, Mathew J, Radhakrishnan EK. Epigenetic Modifier Based Enhancement of Piperine Production in Endophytic Diaporthe sp. PF20. Proc Natl Acad Sci India Sect B Biol Sci. 2019;89:671-677. doi: 10.1007/s40011-018-0982-0.
  11. Asai T, Yamamoto T, Shirata N, Taniguchi T, Monde K, Fujii I, Gomi K, Oshima Y. Structurally diverse chaetophenol productions induced by chemically mediated epigenetic manipulation of fungal gene expression. Org Lett. 2013 Jul 5;15(13):3346-9. doi: 10.1021/ol401386w. Epub 2013 Jun 14. PMID: 23767797.
  12. Wang X, Sena Filho JG, Hoover AR, King JB, Ellis TK, Powell DR, Cichewicz RH. Chemical epigenetics alters the secondary metabolite composition of guttate excreted by an atlantic-forest-soil-derived Penicillium citreonigrum. J Nat Prod. 2010 May 28;73(5):942-8. doi: 10.1021/np100142h. PMID: 20450206; PMCID: PMC2878378.
  13. Kudo S, Murakami T, Miyanishi J, Tanaka K, Takada N, Hashimoto M. Isolation and absolute stereochemistry of optically active sydonic acid from Glonium sp. (Hysteriales, Ascomycota). Biosci Biotechnol Biochem. 2009 Jan;73(1):203-4. doi: 10.1271/bbb.80535. Epub 2009 Jan 7. PMID: 19129640.
  14. Serra S. Bisabolane sesquiterpenes: Synthesis of (R)-(+)-sydowic scid and (R)-(+)- curcumene ether. Syn Lett. 2000;6:890. doi: 10.1055/s-2000-6698.
  15. Chung YM, Wei CK, Chuang DW, El-Shazly M, Hsieh CT, Asai T, Oshima Y, Hsieh TJ, Hwang TL, Wu YC, Chang FR. An epigenetic modifier enhances the production of anti-diabetic and anti-inflammatory sesquiterpenoids from Aspergillus sydowii. Bioorg Med Chem. 2013 Jul 1;21(13):3866-72. doi: 10.1016/j.bmc.2013.04.004. Epub 2013 Apr 13. PMID: 23647825.
  16. Lu Z, Zhu H, Fu P, Wang Y, Zhang Z, Lin H, Liu P, Zhuang Y, Hong K, Zhu W. Cytotoxic polyphenols from the marine-derived fungus Penicillium expansum. J Nat Prod. 2010 May 28;73(5):911-4. doi: 10.1021/np100059m. PMID: 20415462.
  17. Hamasaki T, Sato Y, Hatsuda Y, Tanabe M and Cary LW. Sydowic acid, a new metabolite from Aspergillus sydowic. Tetrahedron Lett. 1975;9:659. doi: 10.1016/S0040-4039(00)71947-2.
  18. Asai T, Yamamoto T, Oshima Y. Histone deacetylase inhibitor induced the production of three novel prenylated tryptophan analogs in the entomopathogenic fungus, Torrubiella luteorostrata. Tetrahedron Lett. 2011;52:7042-7045. doi: 10.1016/j.tetlet.2011.10.020.
  19. Zhang W, Shao CL, Chen M, Liu QA, Wang CY. Brominated resorcylic acid lactones from the marine-derived fungus Cochliobolus lunatus induced by histone deacetylase inhibitors. Tetrahedron Lett. 2014;55:4888-4891. doi: 10.1016/j.tetlet.2014.06.096.
  20. Ying YM, Li L, Yu HF, Xu YL, Huang L, Mao W, Tong CP, Zhang ZD, Zhan ZJ, Zhang Y. Induced production of a new polyketide in Penicillium sp. HS-11 by chemical epigenetic manipulation. Nat Prod Res. 2021 Oct;35(20):3446-3451. doi: 10.1080/14786419.2019.1709190. Epub 2020 Jan 3. PMID: 31899961.
  21. Sheng SL, Li YP, Xiang HY, Liu Y, Wang YD, Kong LP, Du G, Hu QF, Chen YJ, Wang WG. Histone deacetylase inhibitor induced lipase inhibitors from Endophytic Phomopsis sp. 0391. Rec Nat Prod. 2020;14:42-47. doi: 10.25135/rnp.134.19.01.1243.
  22. Waddington CH. The epigenotype. 1942. Int J Epidemiol. 2012 Feb;41(1):10-3. doi: 10.1093/ije/dyr184. Epub 2011 Dec 20. PMID: 22186258.
  23. Kritskiĭ MS, Filippovich SIu, Afanas'eva TP, Bachurina GP, Russo VE. Vliianie ingibitorov fermentativnogo metilirovaniia DNK na obrazovanie reproduktivnykh struktur i karotinogenez u Neurospora crassa [Effect of inhibitors of enzymatic DNA methylation on the formation of reproductive structures and carotenoid production in Neurospora crassa]. Prikl Biokhim Mikrobiol. 2001 May-Jun;37(3):279-84. Russian. PMID: 11443894.
  24. Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet. 2009 May;10(5):295-304. doi: 10.1038/nrg2540. PMID: 19308066.
  25. Migliori V, Phalke S, Bezzi M, Guccione E. Arginine/lysine-methyl/methyl switches: biochemical role of histone arginine methylation in transcriptional regulation. Epigenomics. 2010 Feb;2(1):119-37. doi: 10.2217/epi.09.39. PMID: 22122749.
  26. Li Y, He Y, Li X, Fasoyin OE, Hu Y, Liu Y, Yuan J, Zhuang Z, Wang S. Histone Methyltransferase aflrmtA gene is involved in the morphogenesis, mycotoxin biosynthesis, and pathogenicity of Aspergillus flavus. Toxicon. 2017 Mar 1;127:112-121. doi: 10.1016/j.toxicon.2017.01.013. Epub 2017 Jan 19. Erratum in: Toxicon. 2017 Aug;134:64. PMID: 28109854.
  27. Du J, Johnson LM, Jacobsen SE, Patel DJ. DNA methylation pathways and their crosstalk with histone methylation. Nat Rev Mol Cell Biol. 2015 Sep;16(9):519-32. doi: 10.1038/nrm4043. PMID: 26296162; PMCID: PMC4672940.
  28. Tamaru H, Zhang X, McMillen D, Singh PB, Nakayama J, Grewal SI, Allis CD, Cheng X, Selker EU. Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet. 2003 May;34(1):75-9. doi: 10.1038/ng1143. PMID: 12679815.
  29. Jurkowski TP, Jeltsch A. On the evolutionary origin of eukaryotic DNA methyltransferases and Dnmt2. PLoS One. 2011;6(11):e28104. doi: 10.1371/journal.pone.0028104. Epub 2011 Nov 30. PMID: 22140515; PMCID: PMC3227630.
  30. Migliori V, Phalke S, Bezzi M, Guccione E. Arginine/lysine-methyl/methyl switches: biochemical role of histone arginine methylation in transcriptional regulation. Epigenomics. 2010 Feb;2(1):119-37. doi: 10.2217/epi.09.39. PMID: 22122749.
  31. Stroka J. Food Additives & Contaminants: Part A: Chemistry, Analysis, Control, Exposure & Risk Assessment. Foreword. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2011 Mar;28(3):259. doi: 10.1080/19440049.2011.561599. PMID: 21360372.
  32. Moore LD, Le T, Fan G. DNA methylation and its basic function. Neuropsychopharmacology. 2013 Jan;38(1):23-38. doi: 10.1038/npp.2012.112. Epub 2012 Jul 11. PMID: 22781841; PMCID: PMC3521964.
  33. Liu SY, Lin JQ, Wu HL, Wang CC, Huang SJ, Luo YF, Sun JH, Zhou JX, Yan SJ, He JG, Wang J, He ZM. Bisulfite sequencing reveals that Aspergillus flavus holds a hollow in DNA methylation. PLoS One. 2012;7(1):e30349. doi: 10.1371/journal.pone.0030349. Epub 2012 Jan 20. PMID: 22276181; PMCID: PMC3262820.
  34. Storck R, Nobles MK, Alexopou CJ. The nucleotide composition of deoxyribonucleic acid of some species of hymenochaetaceae and polyporaceae. Mycologia. 1971;63:38-49. doi: 10.1080/00275514.1971.12019080
  35. Antequera F, Tamame M, Villanueva JR, Santos T. DNA methylation in the fungi. J Biol Chem. 1984 Jul 10;259(13):8033-6. PMID: 6330093.
  36. Jeon J, Choi J, Lee GW, Park SY, Huh A, Dean RA, Lee YH. Genome-wide profiling of DNA methylation provides insights into epigenetic regulation of fungal development in a plant pathogenic fungus, Magnaporthe oryzae. Sci Rep. 2015 Feb 24;5:8567. doi: 10.1038/srep08567. PMID: 25708804; PMCID: PMC4338423.
  37. Zemach A, McDaniel IE, Silva P, Zilberman D. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science. 2010 May 14;328(5980):916-9. doi: 10.1126/science.1186366. Epub 2010 Apr 15. PMID: 20395474.
  38. Montanini B, Chen PY, Morselli M, Jaroszewicz A, Lopez D, Martin F, Ottonello S, Pellegrini M. Non-exhaustive DNA methylation-mediated transposon silencing in the black truffle genome, a complex fungal genome with massive repeat element content. Genome Biol. 2014 Jul 31;15(7):411. doi: 10.1186/s13059-014-0411-5. PMID: 25091826; PMCID: PMC4165359.
  39. Fernandez-de Gortari E, Medina-Franco JL. Epigenetic relevant chemical space: A chemoinformatic characterization of inhibitors of DNA methyltransferases. RSC Adv. 2015;5:87465-87476. doi: 10.1039/C5RA19611F.
  40. Naveja JJ, Medina-Franco JL. Activity landscape sweeping: Insights into the mechanism of inhibition and optimization of DNMT1 inhibitors. RSC Adv. 2015;5:63882-63895. doi: 10.1039/C5RA12339A.
  41. Naveja JJ, Medina-Franco JL. Insights from pharmacological similarity of epigenetic targets in epipolypharmacology. Drug Discov Today. 2018 Jan;23(1):141-150. doi: 10.1016/j.drudis.2017.10.006. Epub 2017 Oct 14. PMID: 29038074.
  42. Medina-Franco JL, Méndez-Lucio O, Dueñas-González A, Yoo J. Discovery and development of DNA methyltransferase inhibitors using in silico approaches. Drug Discov Today. 2015 May;20(5):569-77. doi: 10.1016/j.drudis.2014.12.007. Epub 2014 Dec 16. PMID: 25526932.
  43. Kabro A, Lachance H, Marcoux-Archambault I, Perrier V, Dore V, Gros C, Masson V, Gregoire JM, Ausseil F, Cheishvili D, Laulan NB, St-Pierre Y, Szyf M, Arimondo PB, Gagnon A. Preparation of phenylethylbenzamide derivatives as modulators of DNMT3 activity. Med Chem Comm. 2013;4:1562-1570. doi: 10.1039/C3MD00214D.
  44. Garella D, Atlante S, Borretto E, Cocco M, Giorgis M, Costale A, Stevanato L, Miglio G, Cencioni C, Fernández-de Gortari E, Medina-Franco JL, Spallotta F, Gaetano C, Bertinaria M. Design and synthesis of N-benzoyl amino acid derivatives as DNA methylation inhibitors. Chem Biol Drug Des. 2016 Nov;88(5):664-676. doi: 10.1111/cbdd.12794. Epub 2016 Jun 24. PMID: 27225604.
  45. Zwergel C, Valente S, Mai A. DNA Methyltransferases Inhibitors from Natural Sources. Curr Top Med Chem. 2016;16(7):680-96. doi: 10.2174/1568026615666150825141505. PMID: 26303417.
  46. Watson JD, Baker TA, Gann A, Levine M, Losik R. Molecular biology of the gene 7th Ed. Boston: Pearson/CSH Press; 2014. https://tinyurl.com/99s65uu9
  47. Jeon J, Choi J, Lee GW, Park SY, Huh A, Dean RA, Lee YH. Genome-wide profiling of DNA methylation provides insights into epigenetic regulation of fungal development in a plant pathogenic fungus, Magnaporthe oryzae. Sci Rep. 2015 Feb 24;5:8567. doi: 10.1038/srep08567. PMID: 25708804; PMCID: PMC4338423.
  48. Garnaud C, Champleboux M, Maubon D, Cornet M, Govin J. Histone Deacetylases and Their Inhibition in Candida Species. Front Microbiol. 2016 Aug 5;7:1238. doi: 10.3389/fmicb.2016.01238. PMID: 27547205; PMCID: PMC4974301.
  49. Jasim B, Sahadevan N, Chithra S, Mathew J, Radhakrishnan EK. Epigenetic modifier based enhancement of piperine production in Endophytic Diaporthe sp. PF20. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences. 2019;89:671-677. https://tinyurl.com/2p8vudsy
  50. Li G, Kusari S, Golz C, Laatsch H, Strohmann C, Spiteller M. Epigenetic Modulation of Endophytic Eupenicillium sp. LG41 by a Histone Deacetylase Inhibitor for Production of Decalin-Containing Compounds. J Nat Prod. 2017 Apr 28;80(4):983-988. doi: 10.1021/acs.jnatprod.6b00997. Epub 2017 Mar 23. PMID: 28333449.
  51. Bai J, Mu R, Dou M, Yan D, Liu B, Wei Q, Wan J, Tang Y, Hu Y. Epigenetic modification in histone deacetylase deletion strain of Calcarisporium arbuscula leads to diverse diterpenoids. Acta Pharm Sin B. 2018 Jul;8(4):687-697. doi: 10.1016/j.apsb.2017.12.012. Epub 2018 Feb 21. PMID: 30109192; PMCID: PMC6090014.
  52. Zhang S, Fang H, Yin C, Wei C, Hu J, Zhang Y. Antimicrobial Metabolites Produced by Penicillium mallochii CCH01 Isolated From the Gut of Ectropis oblique, Cultivated in the Presence of a Histone Deacetylase Inhibitor. Front Microbiol. 2019 Oct 2;10:2186. doi: 10.3389/fmicb.2019.02186. PMID: 31632360; PMCID: PMC6783908.
  53. Huang D, Cui L, Sajid A, Zainab F, Wu Q, Wang X, Yuan Z. The epigenetic mechanisms in Fusarium mycotoxins induced toxicities. Food Chem Toxicol. 2019 Jan;123:595-601. doi: 10.1016/j.fct.2018.10.059. Epub 2018 Oct 27. PMID: 30599843.
  54. Henrikson JC, Hoover AR, Joyner PM, Cichewicz RH. A chemical epigenetics approach for engineering the in situ biosynthesis of a cryptic natural product from Aspergillus niger. Org Biomol Chem. 2009 Feb 7;7(3):435-8. doi: 10.1039/b819208a. Epub 2008 Dec 11. PMID: 19156306.
  55. Fisch KM, Gillaspy AF, Gipson M, Henrikson JC, Hoover AR, Jackson L, Najar FZ, Wägele H, Cichewicz RH. Chemical induction of silent biosynthetic pathway transcription in Aspergillus niger. J Ind Microbiol Biotechnol. 2009 Sep;36(9):1199-213. doi: 10.1007/s10295-009-0601-4. Epub 2009 Jun 12. PMID: 19521728.
  56. Mooibroek H, Kuipers AG, Sietsma JH, Punt PJ, Wessels JG. Introduction of hygromycin B resistance into Schizophyllum commune: preferential methylation of donor DNA. Mol Gen Genet. 1990 Jun;222(1):41-8. doi: 10.1007/BF00283021. PMID: 1700269.
  57. Birch PR, Sims PF, Broda P. A reporter system for analysis of regulatable promoter functions in the basidiomycete fungus Phanerochaete chrysosporium. J Appl Microbiol. 1998 Sep;85(3):417-24. doi: 10.1046/j.1365-2672.1998.853468.x. PMID: 9750271.
  58. Cichewicz RH. Epigenome manipulation as a pathway to new natural product scaffolds and their congeners. Nat Prod Rep. 2010 Jan;27(1):11-22. doi: 10.1039/b920860g. Epub 2009 Oct 27. PMID: 20024091; PMCID: PMC2958777.
  59. Costa MA, Silva NC, Castro-Prado MA. Genetic and cytological characterization of a developmental mutant of Aspergillus nidulans induced by 5-azacytidine. Biol Res. 2001;34(2):91-8. doi: 10.4067/s0716-97602001000200012. PMID: 11715212.
  60. Bernstein BE, Tong JK, Schreiber SL. Genomewide studies of histone deacetylase function in yeast. Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13708-13. doi: 10.1073/pnas.250477697. Erratum in: Proc Natl Acad Sci U S A 2001 Apr 24;98(9):5368. PMID: 11095743; PMCID: PMC17640.
  61. Walton JD. HC-toxin. Phytochemistry. 2006 Jul;67(14):1406-13. doi: 10.1016/j.phytochem.2006.05.033. Epub 2006 Jul 12. PMID: 16839576.
  62. Brosch G, Dangl M, Graessle S, Loidl A, Trojer P, Brandtner EM, Mair K, Walton JD, Baidyaroy D, Loidl P. An inhibitor-resistant histone deacetylase in the plant pathogenic fungus Cochliobolus carbonum. Biochemistry. 2001 Oct 30;40(43):12855-63. doi: 10.1021/bi010508u. PMID: 11669622.
  63. Kritskiĭ MS, Filippovich SIu, Afanas'eva TP, Bachurina GP, Russo VE. Vliianie ingibitorov fermentativnogo metilirovaniia DNK na obrazovanie reproduktivnykh struktur i karotinogenez u Neurospora crassa [Effect of inhibitors of enzymatic DNA methylation on the formation of reproductive structures and carotenoid production in Neurospora crassa]. Prikl Biokhim Mikrobiol. 2001 May-Jun;37(3):279-84. Russian. PMID: 11443894.
  64. Shwab EK, Bok JW, Tribus M, Galehr J, Graessle S, Keller NP. Histone deacetylase activity regulates chemical diversity in Aspergillus. Eukaryot Cell. 2007 Sep;6(9):1656-64. doi: 10.1128/EC.00186-07. Epub 2007 Jul 6. PMID: 17616629; PMCID: PMC2043372.
  65. Li G, Kusari S, Golz C, Laatsch H, Strohmann C, Spiteller M. Epigenetic Modulation of Endophytic Eupenicillium sp. LG41 by a Histone Deacetylase Inhibitor for Production of Decalin-Containing Compounds. J Nat Prod. 2017 Apr 28;80(4):983-988. doi: 10.1021/acs.jnatprod.6b00997. Epub 2017 Mar 23. PMID: 28333449.
  66. Bai J, Mu R, Dou M, Yan D, Liu B, Wei Q, Wan J, Tang Y, Hu Y. Epigenetic modification in histone deacetylase deletion strain of Calcarisporium arbuscula leads to diverse diterpenoids. Acta Pharm Sin B. 2018 Jul;8(4):687-697. doi: 10.1016/j.apsb.2017.12.012. Epub 2018 Feb 21. PMID: 30109192; PMCID: PMC6090014.
  67. Sun K, Zhu G, Hao J, Wang Y, Zhu W. Chemical-epigenetic method to enhance the chemodiversity of the marine algicolous fungus, Aspergillus terreus OUCMDZ-2739. Tetrahedron. 2017;74:83-87. doi: 10.1016/j.tet.2017.11.039.
  68. Cihák A. Biological effects of 5-azacytidine in eukaryotes. Oncology. 1974;30(5):405-22. doi: 10.1159/000224981. PMID: 4142650.
  69. "Zolinza (vorinostat) dosing, indications, interactions, adverse effects, and more". Medscape Reference. WebMD. Retrieved. 2014. https://tinyurl.com/2p9f9pdr
  70. Kruh J. Effects of sodium butyrate, a new pharmacological agent, on cells in culture. Mol Cell Biochem. 1982 Feb 5;42(2):65-82. doi: 10.1007/BF00222695. PMID: 6174854.
  71. Candido EP, Reeves R, Davie JR. Sodium butyrate inhibits histone deacetylation in cultured cells. Cell. 1978 May;14(1):105-13. doi: 10.1016/0092-8674(78)90305-7. PMID: 667927.
  72. Davie JR. Inhibition of histone deacetylase activity by butyrate. J Nutr. 2003 Jul;133(7 Suppl):2485S-2493S. doi: 10.1093/jn/133.7.2485S. PMID: 12840228.
  73. Magotra A, Kumar M, Kushwaha M, Awasthi P, Raina C, Gupta AP, Shah BA, Gandhi SG, Chaubey A. Epigenetic modifier induced enhancement of fumiquinazoline C production in Aspergillus fumigatus (GA-L7): an endophytic fungus from Grewia asiatica L. AMB Express. 2017 Dec;7(1):43. doi: 10.1186/s13568-017-0343-z. Epub 2017 Feb 17. PMID: 28213885; PMCID: PMC5315648.
  74. Silva MG, Furtado NA, Pupo MT, Fonseca MJ, Said S, da Silva Filho AA, Bastos JK. Antibacterial activity from Penicillium corylophilum Dierckx. Microbiol Res. 2004;159(4):317-22. doi: 10.1016/j.micres.2004.06.003. PMID: 15646377.
  75. Belofsky GN, Anguera M, Jensen PR, Fenical W, Köck M. Oxepinamides A-C and fumiquinazolines H--I: bioactive metabolites from a marine isolate of a fungus of the genus Acremonium. Chemistry. 2000 Apr 14;6(8):1355-60. doi: 10.1002/(sici)1521-3765(20000417)6:8<1355::aid-chem1355>3.0.co;2-s. PMID: 10840958.
  76. Han XX, Xu XY, Cui CB, Gu QQ. Alkaloidal compounds produced by a marinederived fungus. Aspergillus fumigatus H1-04, and their antitumor activities. Chin J Med Chem. 2007;17:232-237. https://tinyurl.com/4w2emyvs
  77. Chen HJ, Awakawa T, Sun J, Wakimoto T, Abe I. Epigenetic modifier-induced biosynthesis of novel fusaric acid derivatives in endophytic fungi from Datura stramonium L. Nat Prod Bioprospect. 2013;3:20-23. doi: 10.1007/s13659-013-0010-2.
  78. Asai T, Morita S, Taniguchi T, Monde K, Oshima Y. Epigenetic stimulation of polyketide production in Chaetomium cancroideum by an NAD(+)-dependent HDAC inhibitor. Org Biomol Chem. 2016 Jan 14;14(2):646-651. doi: 10.1039/c5ob01595b. PMID: 26549741.
  79. Vervoort HC, Drašković M, Crews P. Histone deacetylase inhibitors as a tool to up-regulate new fungal biosynthetic products: isolation of EGM-556, a cyclodepsipeptide, from Microascus sp. Org Lett. 2011 Feb 4;13(3):410-3. doi: 10.1021/ol1027199. Epub 2010 Dec 21. PMID: 21174394; PMCID: PMC3031758.
  80. Oku N, Kawabata K, Adachi K, Katsuta A, Shizuri Y. Unnarmicins A and C, new antibacterial depsipeptides produced by marine bacterium Photobacterium sp. MBIC06485. J Antibiot (Tokyo). 2008 Jan;61(1):11-7. doi: 10.1038/ja.2008.103. PMID: 18305354.
  81. Sasakawa Y, Naoe Y, Inoue T, Sasakawa T, Matsuo M, Manda T, Mutoh S. Effects of FK228, a novel histone deacetylase inhibitor, on human lymphoma U-937 cells in vitro and in vivo. Biochem Pharmacol. 2002 Oct 1;64(7):1079-90. doi: 10.1016/s0006-2952(02)01261-3. PMID: 12234611.
  82. Albright JC, Henke MT, Soukup AA, McClure RA, Thomson RJ, Keller NP, Kelleher NL. Large-scale metabolomics reveals a complex response of Aspergillus nidulans to epigenetic perturbation. ACS Chem Biol. 2015 Jun 19;10(6):1535-41. doi: 10.1021/acschembio.5b00025. Epub 2015 Apr 3. PMID: 25815712; PMCID: PMC4475433.
  83. Gubiani JR, Wijeratne EM, Shi T, Araujo AR, Arnold AE, Chapman E, Gunatilaka AA. An epigenetic modifier induces production of (10'S)-verruculide B, an inhibitor of protein tyrosine phosphatases by Phoma sp. nov. LG0217, a fungal endophyte of Parkinsonia microphylla. Bioorg Med Chem. 2017 Mar 15;25(6):1860-1866. doi: 10.1016/j.bmc.2017.01.048. Epub 2017 Feb 3. PMID: 28202316; PMCID: PMC5362119.
  84. Sun J, Awakawa T, Noguchi H, Abe I. Induced production of mycotoxins in an endophytic fungus from the medicinal plant Datura stramonium L. Bioorg Med Chem Lett. 2012 Oct 15;22(20):6397-400. doi: 10.1016/j.bmcl.2012.08.063. Epub 2012 Aug 24. PMID: 22967766.
  85. Vasanthakumari MM, Jadhav SS, Sachin N, Vinod G, Shweta S, Manjunatha BL, Kumara PM, Ravikanth G, Nataraja KN, Uma Shaanker R. Restoration of camptothecine production in attenuated endophytic fungus on re-inoculation into host plant and treatment with DNA methyltransferase inhibitor. World J Microbiol Biotechnol. 2015 Oct;31(10):1629-39. doi: 10.1007/s11274-015-1916-0. Epub 2015 Aug 20. PMID: 26289161.
  86. Yang XL, Huang L, Ruan XL. Epigenetic modifiers alter the secondary metabolite composition of a plant endophytic fungus, Pestalotiopsis crassiuscula obtained from the leaves of Fragaria chiloensis. J Asian Nat Prod Res. 2014;16(4):412-7. doi: 10.1080/10286020.2014.881356. Epub 2014 Feb 5. PMID: 24498889.
  87. Asai T, Chung YM, Sakurai H, Ozeki T, Chang FR, Yamashita K, Oshima Y. Tenuipyrone, a novel skeletal polyketide from the entomopathogenic fungus, Isaria tenuipes, cultivated in the presence of epigenetic modifiers. Org Lett. 2012 Jan 20;14(2):513-5. doi: 10.1021/ol203097b. Epub 2011 Dec 27. PMID: 22201477.
  88. Asai, T, Yamamoto T, Chung YM, Chang FR, Wu YC, Yamashita K, Oshima Y. As Aromatic polyketide glycosides from an entomopathogenic fungus, Cordyceps indigotica. Tetrahedron Lett. 2012;53:277-280. doi: 10.1016/j.tetlet.2011.10.013.
  89. Asai T, Luo D, Obara Y, Taniguchi T, Monde K, Yamashita K, Oshima Y. Dihydrobenzofurans as cannabinoid receptor ligands from Cordyceps annullata, an entomopathogenic fungus cultivated in the presence of an HDAC inhibitor. Tetrahedron Lett. 2012;53:2239-2243. doi: 10.1016/j.tetlet.2012.02.088.
  90. Asai T, Morita S, Shirata N, Taniguchi T, Monde K, Sakurai H, Ozeki T, Oshima Y. Structural diversity of new C13-polyketides produced by Chaetomium mollipilium cultivated in the presence of a NAD(+)-dependent histone deacetylase inhibitor. Org Lett. 2012 Nov 2;14(21):5456-9. doi: 10.1021/ol302539s. Epub 2012 Oct 19. PMID: 23083076.
  91. Asai T, Chung YM, Sakurai H, Ozeki T, Chang FR, Wu YC, Yamashita K, Oshima Y. Highly oxidized ergosterols and isariotin analogs from an entomopathogenic fungus, Gibellula formosana, cultivated in the presence of epigenetic modifyin gagents. Tetrahedron. 2012;68:5817-5823. doi: 10.1016/j.tet.2012.05.020.
  92. Asai T, Otsuki S, Sakurai H, Yamashita K, Ozeki T, Oshima Y. Benzophenones from an endophytic fungus, Graphiopsis chlorocephala, from Paeonia lactiflora cultivated in the presence of an NAD+-dependent HDAC inhibitor. Org Lett. 2013 Apr 19;15(8):2058-61. doi: 10.1021/ol400781b. Epub 2013 Apr 11. PMID: 23578108.
  93. Chung YM, El-Shazly M, Chuang DW, Hwang TL, Asai T, Oshima Y, Ashour ML, Wu YC, Chang FR. Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor, induces the production of anti-inflammatory cyclodepsipeptides from Beauveria felina. J Nat Prod. 2013 Jul 26;76(7):1260-6. doi: 10.1021/np400143j. Epub 2013 Jul 3. PMID: 23822585.
  94. Chen JJ, Han MY, Gong T, Qiao YM, Yang JL, Zhu P. Epigenetic modification enhances ergot alkaloid production of Claviceps purpurea. Biotechnol Lett. 2019 Dec;41(12):1439-1449. doi: 10.1007/s10529-019-02750-x. Epub 2019 Oct 28. PMID: 31659576.
  95. Akone SH, Mandi A, Kurtan T, Hartmann R, Lin W, Daletos G, Proksch P. Inducing secondary metabolite production by the endophytic fungus Chaetomium sp. through fungal bacterial co-culture and epigenetic modification. Tetrahedron. 2016;72:6340-6347. doi: 10.1016/j.tet.2016.08.022.
  96. Fisch KM, Gillaspy AF, Gipson M, Henrikson JC, Hoover AR, Jackson L, Najar FZ, Wägele H, Cichewicz RH. Chemical induction of silent biosynthetic pathway transcription in Aspergillus niger. J Ind Microbiol Biotechnol. 2009 Sep;36(9):1199-213. doi: 10.1007/s10295-009-0601-4. Epub 2009 Jun 12. PMID: 19521728.
  97. Beau J, Mahid N, Burda WN, Harrington L, Shaw LN, Mutka T, Kyle DE, Barisic B, van Olphen A, Baker BJ. Epigenetic tailoring for the production of anti-infective cytosporones from the marine fungus Leucostoma persoonii. Mar Drugs. 2012 Apr;10(4):762-74. doi: 10.3390/md10040762. Epub 2012 Mar 28. PMID: 22690142; PMCID: PMC3366674.
  98. Xiao L, Yin Y, Sun W, Zhang F, Li Z. Enhanced production of (+)-terrein by Aspergillus terreus strain PF26 with epigenetic modifier suberoylanilide hydroxamic acid. Process biochem. 2013;48:1635-1639. doi: 10.1016/j.procbio.2013.08.007.
  99. Park SH, Kim DS, Kim WG, Ryoo IJ, Lee DH, Huh CH, Youn SW, Yoo ID, Park KC. Terrein: a new melanogenesis inhibitor and its mechanism. Cell Mol Life Sci. 2004 Nov;61(22):2878-85. doi: 10.1007/s00018-004-4341-3. PMID: 15558216.
  100. Park SH, Kim DS, Lee HK, Kwon SB, Lee S, Ryoo IJ, Kim WG, Yoo ID, Park KC. Long-term suppression of tyrosinase by terrein via tyrosinase degradation and its decreased expression. Exp Dermatol. 2009 Jun;18(6):562-6. doi: 10.1111/j.1600-0625.2009.00847.x. PMID: 19493001.
  101. Lee JC, Yu MK, Lee R, Lee YH, Jeon JG, Lee MH, Jhee EC, Yoo ID, Yi HK. Terrein reduces pulpal inflammation in human dental pulp cells. J Endod. 2008 Apr;34(4):433-7. doi: 10.1016/j.joen.2008.01.015. PMID: 18358890.
  102. Lee YH, Lee NH, Bhattarai G, Oh YT, Yu MK, Yoo ID, Jhee EC, Yi HK. Enhancement of osteoblast biocompatibility on titanium surface with Terrein treatment. Cell Biochem Funct. 2010 Dec 2;28(8):678-85. doi: 10.1002/cbf.1708. Epub 2010 Oct 29. PMID: 21104936.
  103. Malmstrøm J, Christophersen C, Barrero AF, Oltra JE, Justicia J, Rosales A. Bioactive metabolites from a marine-derived strain of the fungus Emericella variecolor. J Nat Prod. 2002 Mar;65(3):364-7. doi: 10.1021/np0103214. PMID: 11908979.
  104. Ghisalberti E, Narbey M, Rowland C. Metabolites of Aspergillus terreus antagonistic towards the take-all fungus. J Nat Prod. 1990;53:520-522. doi: 10.1021/np50068a043.
  105. Phattanawasin P, Pojchanakom K, Sotanaphun U, Piyapolrungroj N, Zungsontiporn S. Weed growth inhibitors from Aspergillus fischeri TISTR 3272. Nat Prod Res. 2007 Dec;21(14):1286-91. doi: 10.1080/14786410701766364. Erratum in: Nat Prod Res. 2008 Feb 15;22(3):285. PMID: 18075891.
  106. Arakawa M, Someno T, Kawada M, Ikeda D. A new terrein glucoside, a novel inhibitor of angiogenin secretion in tumor angiogenesis. J Antibiot (Tokyo). 2008 Jul;61(7):442-8. doi: 10.1038/ja.2008.60. PMID: 18776656.
  107. Liao WY, Shen CN, Lin LH, Yang YL, Han HY, Chen JW, Kuo SC, Wu SH, Liaw CC. Asperjinone, a nor-neolignan, and terrein, a suppressor of ABCG2-expressing breast cancer cells, from thermophilic Aspergillus terreus. J Nat Prod. 2012 Apr 27;75(4):630-5. doi: 10.1021/np200866z. Epub 2012 Feb 23. PMID: 22360613.
  108. Brosch G, Loidl P, Graessle S. Histone modifications and chromatin dynamics: a focus on filamentous fungi. FEMS Microbiol Rev. 2008 May;32(3):409-39. doi: 10.1111/j.1574-6976.2007.00100.x. Epub 2008 Jan 23. PMID: 18221488; PMCID: PMC2442719.
  109. Fang MZ, Chen D, Sun Y, Jin Z, Christman JK, Yang CS. Reversal of hypermethylation and reactivation of p16INK4a, RARbeta, and MGMT genes by genistein and other isoflavones from soy. Clin Cancer Res. 2005 Oct 1;11(19 Pt 1):7033-41. doi: 10.1158/1078-0432.CCR-05-0406. PMID: 16203797.
  110. Majid S, Kikuno N, Nelles J, Noonan E, Tanaka Y, Kawamoto K, Hirata H, Li LC, Zhao H, Okino ST, Place RF, Pookot D, Dahiya R. Genistein induces the p21WAF1/CIP1 and p16INK4a tumor suppressor genes in prostate cancer cells by epigenetic mechanisms involving active chromatin modification. Cancer Res. 2008 Apr 15;68(8):2736-44. doi: 10.1158/0008-5472.CAN-07-2290. PMID: 18413741.
  111. Nijveldt RJ, van Nood E, van Hoorn DE, Boelens PG, van Norren K, van Leeuwen PA. Flavonoids: a review of probable mechanisms of action and potential applications. Am J Clin Nutr. 2001 Oct;74(4):418-25. doi: 10.1093/ajcn/74.4.418. PMID: 11566638.
  112. Priyadarsini RV, Vinothini G, Murugan RS, Manikandan P, Nagini S. The flavonoid quercetin modulates the hallmark capabilities of hamster buccal pouch tumors. Nutr Cancer. 2011;63(2):218-26. doi: 10.1080/01635581.2011.523503. PMID: 21294050.
  113. Seelinger G, Merfort I, Wölfle U, Schempp CM. Anti-carcinogenic effects of the flavonoid luteolin. Molecules. 2008 Oct 22;13(10):2628-51. doi: 10.3390/molecules13102628. PMID: 18946424; PMCID: PMC6245397.
  114. Krifa M, Leloup L, Ghedira K, Mousli M, Chekir-Ghedira L. Luteolin induces apoptosis in BE colorectal cancer cells by downregulating calpain, UHRF1, and DNMT1 expressions. Nutr Cancer. 2014;66(7):1220-7. doi: 10.1080/01635581.2014.951729. Epub 2014 Sep 10. PMID: 25207720.
  115. Chi P, Allis CD, Wang GG. Covalent histone modifications--miswritten, misinterpreted and mis-erased in human cancers. Nat Rev Cancer. 2010 Jul;10(7):457-69. doi: 10.1038/nrc2876. PMID: 20574448; PMCID: PMC3262678.
  116. Kauntz H, Bousserouel S, Gossé F, Raul F. Epigenetic effects of the natural flavonolignan silibinin on colon adenocarcinoma cells and their derived metastatic cells. Oncol Lett. 2013 Apr;5(4):1273-1277. doi: 10.3892/ol.2013.1190. Epub 2013 Feb12.PMID:23599778;PMCID:PMC3629096.
  117. Ko HH, Yen MH, Wu RR, Won SJ, Lin CN. Cytotoxic isoprenylated flavans of Broussonetia kazinoki. J Nat Prod. 1999 Jan;62(1):164-6. doi: 10.1021/np980281c.PMID:9917310.
  118. Nass SJ, Herman JG, Gabrielson E, Iversen PW, Parl FF, Davidson NE, Graff JR. Aberrant methylation of the estrogen receptor and E-cadherin 5' CpG islands increases with malignant progression in human breast cancer. Cancer Res. 2000 Aug 15;60(16):4346-8. PMID: 10969774.
  119. Tanaka H, Marumo H, Nagai T, Okada M, Taniguchi K. Nanaomycins, new antibiotics produced by a strain of Streptomyces. III. A new component, nanaomycin C, and biological activities of nanaomycin derivatives. J Antibiot (Tokyo). 1975 Dec;28(12):925-30. doi: 10.7164/antibiotics.28.925. PMID: 1206004.
  120. Kuck D, Singh N, Lyko F, Medina-Franco JL. Novel and selective DNA methyltransferase inhibitors: Docking-based virtual screening and experimental evaluation. Bioorg Med Chem. 2010 Jan 15;18(2):822-9. doi: 10.1016/j.bmc.2009.11.050. Epub 2009 Nov 27. PMID: 20006515.
  121. Burwood R, Read G, Schofield K, Wright DE. 1133. The pigments of stick lac. Part I. Isolation and preliminary examination. J Chem Soc. 1965;6067-6073. doi: 10.1039/JR9650006067.
  122. Yoder JA, Soman NS, Verdine GL, Bestor TH. DNA (cytosine-5)-methyltransferases in mouse cells and tissues. Studies with a mechanism-based probe. J Mol Biol. 1997 Jul 18;270(3):385-95. doi: 10.1006/jmbi.1997.1125. PMID: 9237905.
  123. Blank M, Mandel M, Keisari Y, Meruelo D, Lavie G. Enhanced ubiquitinylation of heat shock protein 90 as a potential mechanism for mitotic cell death in cancer cells induced with hypericin. Cancer Res. 2003 Dec 1;63(23):8241-7. PMID: 14678981.
  124. Dror N, Mandel M, Lavie G. Unique anti-glioblastoma activities of hypericin are at the crossroad of biochemical and epigenetic events and culminate in tumor cell differentiation. PLoS One. 2013 Sep 16;8(9):e73625. doi:10.1371/journal.pone.0073625. PMID: 24066060; PMCID: PMC3774735.
  125. Fang MZ, Wang Y, Ai N, Hou Z, Sun Y, Lu H, Welsh W, Yang CS. Tea polyphenol (-)-epigallocatechin-3-gallate inhibits DNA methyltransferase and reactivates methylation-silenced genes in cancer cell lines. Cancer Res. 2003 Nov 15;63(22):7563-70. PMID: 14633667.
  126. Liu Z, Xie Z, Jones W, Pavlovicz RE, Liu S, Yu J, Li PK, Lin J, Fuchs JR, Marcucci G, Li C, Chan KK. Curcumin is a potent DNA hypomethylation agent. Bioorg Med Chem Lett. 2009 Feb 1;19(3):706-9. doi:10.1016/j.bmcl.2008.12.041. Epub 2008 Dec 14. PMID: 19112019.
  127. Lee WJ, Zhu BT. Inhibition of DNA methylation by caffeic acid and chlorogenic acid, two common catechol-containing coffee polyphenols. Carcinogenesis. 2006 Feb;27(2):269-77. doi: 10.1093/carcin/bgi206. Epub 2005 Aug 4. PMID: 16081510.
  128. Bhattacharya K, Samanta SK, Tripathi R, Mallick A, Chandra S, Pal BC, Shaha C, Mandal C. Apoptotic effects of mahanine on human leukemic cells are mediated through crosstalk between Apo-1/Fas signaling and the Bid protein and via mitochondrial pathways. Biochem Pharmacol. 2010 Feb 1;79(3):361-72. doi: 10.1016/j.bcp.2009.09.007. Epub 2009 Sep 12. PMID: 19751707.
  129. Shah BA, Qazi GN, Taneja SC. Boswellic acids: a group of medicinally important compounds. Nat Prod Rep. 2009 Jan;26(1):72-89. doi: 10.1039/b809437n. PMID: 19374123.
  130. Sun W, Iijima T, Kano J, Kobayashi H, Li D, Morishita Y, Okubo C, Anami Y, Noguchi M. Frequent aberrant methylation of the promoter region of sterile alpha motif domain 14 in pulmonary adenocarcinoma. Cancer Sci. 2008 Nov;99(11):2177-84. doi: 10.1111/j.1349-7006.2008.00965.x. Epub 2008 Sep 22. PMID: 18823374.
  131. Davis CD, Uthus EO. Dietary selenite and azadeoxycytidine treatments affect dimethylhydrazine-induced aberrant crypt formation in rat colon and DNA methylation in HT-29 cells. J Nutr. 2002 Feb;132(2):292-7. doi: 10.1093/jn/132.2.292. PMID: 11823593.
  132. Uthus EO, Ross SA. Dietary selenium affects homocysteine metabolism differently in Fisher-344 rats and CD-1 mice. J Nutr. 2007 May;137(5):1132-6. doi: 10.1093/jn/137.5.1132. PMID: 17449570.
  133. Fu LJ, Ding YB, Wu LX, Wen CJ, Qu Q, Zhang X, Zhou HH. The Effects of Lycopene on the Methylation of the GSTP1 Promoter and Global Methylation in Prostatic Cancer Cell Lines PC3 and LNCaP. Int J Endocrinol. 2014;2014:620165. doi: 10.1155/2014/620165. Epub 2014 Oct 20. PMID: 25389438; PMCID: PMC4217342.


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