Herboxidiene biosynthesis, production, and structural modifications: prospect for hybrids with related polyketide

Applied Microbiology and Biotechnology

Volumn 99, Issue 20, 2015, Pages 8351-8362

  Pokhrel, Anaya Raj ^a   Dhakal, Dipesh ^a   Jha, Amit Kumar ^a   Sohng, Jae Kyung ^a  

^a SunMoon University   (South Korea)

Author keywords

Combinatorial biosynthesis; Enhancement; Herboxidiene; Hybrid polyketide; Polyketide

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; GENE EXPRESSION; IMAGE ENHANCEMENT; METABOLIC ENGINEERING;

COMBINATORIAL BIOSYNTHESIS; GLUCOSYLTRANSFERASES; HERBOXIDIENE; HETEROLOGOUS EXPRESSION; METABOLIC ENGINEERING APPROACH; POLYKETIDE SYNTHASES; POLYKETIDES; STRUCTURAL MODIFICATIONS;

KETONES;

CYTOCHROME P450; GLUCOSYLTRANSFERASE; HERBICIDE; HERBOXIDIENE; POLYKETIDE; POLYKETIDE SYNTHASE; PRE MRNA SPLICING INHIBITOR; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; FATTY ALCOHOL; PYRAN DERIVATIVE;

BIOACTIVITY; BIOTECHNOLOGY; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ENGINEERING; HERBICIDE; SECONDARY METABOLITE;

BACTERIAL STRAIN; COMPARATIVE STUDY; DRUG MANUFACTURE; DRUG POTENCY; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME ENGINEERING; GENE; HETEROLOGOUS EXPRESSION; MODULATION; NONHUMAN; REVIEW; STREPTOMYCES; STREPTOMYCES CHROMOFUSCUS; BIOSYNTHESIS; GENETICS; METABOLISM;

STREPTOMYCES CHROMOFUSCUS;

BIOSYNTHETIC PATHWAYS; CYTOCHROME P-450 ENZYME SYSTEM; FATTY ALCOHOLS; GLUCOSYLTRANSFERASES; POLYKETIDE SYNTHASES; POLYKETIDES; PYRANS; STREPTOMYCES;

EID: 84941994201     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-6860-2     Document Type: Review

References (98)

1. Aharonowitz Y (1980) Nitrogen metabolite regulation of antibiotic biosynthesis. Annu Rev Microbiol 34:209–233
2. Aharonowitz Y, Demain AL (1978) Carbon catabolite regulation of cephalosporin production in Streptomyces clavuligerus. Antimicrob Agents Chemother 14:159–164
3. Andersen JF, Tatsuta K, Gunji H, Ishiyama T, Hutchinson CR (1993) Substrate specificity of 6-deoxyerythronolide B hydroxylase, a bacterial cytochrome P450 of erythromycin A biosynthesis. Biochemistry 32:1905–1913
4. Baltz RH (1998) Genetic manipulation of antibiotic producing Streptomyces. Trends Microbiol 6:76–83
5. Basnet DB, Park JW, Yoon YJ (2008) Combinatorial biosynthesis of 5-O-desosaminyl erythronolide A as a potent precursor of ketolide antibiotics. J Biotechnol 135:92–96
6. Bierman M, Logan R, O’Brien K, Seno ET, Rao RN, Schoner BE (1992) Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116:43–49
7. Bisang C, Long PF, Cortés J, Westcott J, Crosby J, Matharu AL, Cox RJ, Simpson TJ, Staunton J, Leadlay PF (1999) A chain initiation factor common to both modular and aromatic polyketide synthases. Nature 401:502–505
8. Blakemore P, Kocieński P (1999) A synthesis of herboxidiene. J Chem Soc Perkin 1(8):955–968
9. Blanchard S, Thorson JS (2006) Enzymatic tools for engineering natural product glycosylation. Curr Opin Chem Biol 10:263–271
10. Bonnal S, Vigevani L, Valcarcel J (2012) The spliceosome as a target of novel antitumour drugs. Nat Rev Drug Discov 11:847–859
11. Breitling R, Ceniceros A, Jankevics A, Takano E (2013) Metabolomics for secondary metabolite research. Metabolites 3:1076–1083
12. Brown MS, Goldstein JL (1986) A receptor-mediated pathway for cholesterol homeostasis. Science 232:34–47
13. Byers DM, Gong H (2007) Acyl carrier protein: structure-function relationships in a conserved multifunctional protein family. Biochem Cell Biol 85:649–662
14. Chan YA, Podevels AM, Kevany BM, Thomas MG (2009) Biosynthesis of polyketide synthase extender units. Nat Prod Rep 26:90–114
15. Chaudhary AK, Dhakal D, Sohng JK (2013) An insight into the “-omics” based engineering of streptomycetes for secondary metabolite overproduction. Biomed Res Int 2013:968518
16. Chen XS, Mao ZG (2013) Comparison of glucose and glycerol as carbon sources for ε-poly-l-lysine production by Streptomyces sp. M-Z18. Appl Biochem Biotechnol 170:185–197
17. Chen X, Tang L, Li S, Liao L, Zhang J, Mao Z (2011) Optimization of medium for enhancement of ε-poly-L-lysine production by Streptomyces sp. M-Z18 with glycerol as carbon source. Bioresour Technol 102:1727–1732
18. Chiang PK, Gordon RK, Tal J, Zeng GC, Doctor BP, Pardhasaradhi K, McCann PP (1996) S-Adenosylmethionine and methylation. FASEB J 10:471–480
19. Cobb RE, Wang Y, Zhao H (2014) High-efficiency multiplex genome editing of Streptomyces species using an engineered CRISPR/Cas system. ACS Synth Biol 4:723–728
20. Danielson PB (2002) The cytochrome P450 superfamily: biochemistry, evolution and drug metabolism in humans. Curr Drug Metab 3:561–597
21. Dhakal D, Le TT, Pandey RP, Jha AK, Gurung R, Parajuli P, Pokhrel AR, Yoo JC, Sohng JK (2015) Enhanced production of nargenicin A1 and generation of novel glycosylated derivatives. Appl Biochem Biotechnol 175:2934–2949
22. Edmunds AJF, Trueb W, Oppolzer W, Cowley P (1997) Herboxidiene: determination of absolute configuration by degradation and synthetic studies. Tetrahedron 53:2785–2802
23. Edmunds AJF, Arnold G, Hagmann L, Schaffner R, Furlenmeier H (2000) Synthesis of simplified herboxidiene aromatic hybrids. Bioorg Med Chem Lett 10:1365–1368
24. Fernández-Martínez LT, Bibb MJ (2014) Use of the meganuclease I-SceI of Saccharomyces cerevisiae to select for gene deletions in actinomycetes. Sci Rep 4:7100
25. Floss HG (2006) Combinatorial biosynthesis-potential and problems. J Biotechnol 124:242–257
26. Fontecave M, Atta M, Mulliez E (2004) S-adenosylmethionine: nothing goes to waste. Trends Biochem Sci 29:243–249
27. Gantt RW, Peltier-Pain P, Thorson JS (2011) Enzymatic methods for glyco(diversification/randomization) of drugs and small molecules. Nat Prod Rep 28:1811–1853
28. Gao Y, Vogt A, Forsyth CJ, Koide K (2013) Comparison of splicing factor 3b inhibitors in human cells. Chembiochem 14:49–52
29. Gerth K, Bedorf N, Hofle G, Irschik H, Reichenbach H (1996) Epothilons A and B: antifungal and cytotoxic compounds from Sorangium cellulosum (Myxobacteria). Production, physico-chemical and biological properties. J Antibiot 49:560–563
30. Ghosh AK, Li J (2010) A stereoselective synthesis of (+)-herboxidiene/GEX1A. Org Lett 13:66–69
31. Goodin S, Kane MP, Rubin EH (2004) Epothilones: mechanism of action and biologic activity. J Clin Oncol 22:2015–2025
32. Greasham RL (1983) Media for microbial fermentations. In: Rehm HJ, Read G, Puhler A, Stagler P (eds) Bioprocessing, biotechnology, vol 3. Wiley-VCH Verlag GmbH, Weinheim, Germany, pp 128–139
33. Hasegawa M, Miura T, Kuzuya K, Inoue A, Won Ki S, Horinouchi S, Yoshida T, Kunoh T, Koseki K, Mino K, Sasaki R, Yoshida M, Mizukami T (2011) Identification of SAP155 as the target of GEX1A (herboxidiene), an antitumor natural product. ACS Chem Biol 6:229–233
34. Hasemann CA, Kurumbail RG, Boddupalli SS, Peterson JA, Deisenhofer J (1995) Structure and function of cytochromes P450: a comparative analysis of three crystal structures. Structure 3:41–62
35. Helfrich EJ, Reiter S, Piel J (2014) Recent advances in genome-based polyketide discovery. Curr Opin Biotechnol 29:107–115
36. Horinouchi S, Hara O, Beppu T (1983) Cloning of a pleiotropic gene that positively controls biosynthesis of A-factor, actinorhodin, and prodigiosin in Streptomyces coelicolor A3 (2) and Streptomyces lividans. J Bacteriol 155:1238–1248
37. Huh JH, Kim DJ, Zhao XQ, Li M, Jo YY, Yoon TM, Shin SK, Yong JH, Ryu YW, Yang YY, Suh JW (2004) Widespread activation of antibiotic biosynthesis by S-adenosylmethionine in streptomycetes. FEMS Microbiol Lett 238:439–447
38. Hwang KS, Kim HU, Charusanti P, Palsson BØ, Lee SY (2014) Systems biology and biotechnology of Streptomyces species for the production of secondary metabolites. Biotechnol Adv 32:255–268
39. Isaac BG, Ayer SW, Elliott RC, Stonard RJ (1992) Herboxidiene: a potent phytotoxic polyketide from Streptomyces sp. A7847. J Org Chem 57:7220–7226
40. Jha AK, Lamichhane J, Sohng JK (2014) Enhancement of herboxidiene production in Streptomyces chromofuscus ATCC 49982. J Microbiol Biotechnol 24:52–58
41. Jha AK, Dhakal D, Van PT, Pokhrel AR, Yamaguchi T, Jung HJ, Yoon YJ, Sohng JK (2015) Structural modification of herboxidiene by substrate-flexible cytochrome P450 and glycosyltransferase. Appl Microbiol Biotechnol 99:3421–3431
42. Jnawali HN, Lee HC, Sohng JK (2010) Enhancement of clavulanic acid production by expressing regulatory genes in gap gene deletion mutant of Streptomyces clavuligerus NRRL3585. J Microbiol Biotechnol 20:146–152
43. Keasling JD (2012) Synthetic biology and the development of tools for metabolic engineering. Metab Eng 14:189–195
44. Kim DJ, Huh JH, Yang YY, Kang CM, Lee IH, Hyun CG, Hong SK, Suh JW (2003) Accumulation of S-adenosyl-L-methionine enhances production of actinorhodin but inhibits sporulation in Streptomyces lividans TK23. J Bacteriol 185:592–600
45. Koguchi Y, Nishio M, Kotera J, Omori K, Ohnuki T, Komatsubara S (1997) Trichostatin A and herboxidiene up-regulate the gene expression of low density lipoprotein receptor. J Antibiot 50:970–971
46. Koju D, Dhakal D, Sohng JK (2012) Effect of different biosynthetic precursors on the production of nargenicin A1 from metabolically engineered Nocardia sp. CS682. J Microbiol Biotechnol 22:1127–1132
47. Kotake Y, Sagane K, Owa T, Mimori-Kiyosue Y, Shimizu H, Uesugi M, Ishihama Y, Iwata M, Mizui Y (2007) Splicing factor SF3b as a target of the antitumor natural product pladienolide. Nat Chem Biol 3:570–575
48. Kumar VP, Chandrasekhar S (2013) Enantioselective synthesis of pladienolide B and truncated analogues as new anticancer agents. Org Lett 15:3610–3613
49. Kun GD, Bao ZY, Qian YK (2013) Coordination of glycerol utilization and clavulanic acid biosynthesis to improve clavulanic acid production in Streptomyces clavuligerus. Sci China Life Sci 56:591–600
50. Lagisetti C, Yermolina MV, Sharma LK, Palacios G, Prigaro BJ, Webb TR (2013) Pre-mRNA splicing-modulatory pharmacophores: the total synthesis of herboxidiene, a pladienolide–herboxidiene hybrid analog and related derivatives. ACS Chem Biol 9:643–648
51. Le TT, Pandey RP, Gurung RB, Dhakal D, Sohng JK (2014) Efficient enzymatic systems for synthesis of novel α-mangostin glycosides exhibiting antibacterial activity against Gram-positive bacteria. Appl Microbiol Biotechnol 98:8527–8538
52. Lee SK, Basnet DB, Hong JSJ, Jung WS, Choi CY, Lee HC, Sohng JK, Ryu KG, Kim DJ, Ahn JS, Kim BS, Oh HC, Sherman DH, Yoon YJ (2005) Structural diversification of macrolactones by substrate‐flexible cytochrome P450 monooxygenases. Adv Synth Catal 347:1369–1378
53. Lee SK, Park JW, Kim JW, Jung WS, Park SR, Choi CY, Kim ES, Kim BS, Ahn JS, Sherman DH, Yoon YJ (2006) Neopikromycin and novapikromycin from the pikromycin biosynthetic pathway of Streptomyces venezuelae. J Nat Prod 69:847–849
54. Li R, Townsend CA (2006) Rational strain improvement for enhanced clavulanic acid production by genetic engineering of the glycolytic pathway in Streptomyces clavuligerus. Metab Eng 8:240–252
55. Li L, Zhao Y, Ruan L, Yang S, Ge M, Jiang W, Lu Y (2015) A stepwise increase in pristinamycin II biosynthesis by Streptomyces pristinaespiralis through combinatorial metabolic engineering. Metab Eng 29:12–25
56. Liu X, Biswas S, Berg MG, Antapli CM, Xie F, Wang Q, Tang M-C, Tang G-L, Zhang L, Dreyfuss G, Cheng Y-Q (2013) Genomics-guided discovery of thailanstatins A, B, and C as pre-mRNA splicing inhibitors and antiproliferative agents from Burkholderia thailandensis MSMB43. J Nat Prod 76:685–693
57. Machida K, Arisawa A, Takeda S, Tsuchida T, Aritoku Y, Yoshida M, Ikeda H (2008a) Organization of the biosynthetic gene cluster for the polyketide antitumor macrolide, pladienolide, in Streptomyces platensis Mer-11107. Biosci Biotechnol Biochem 72:2946–2952
58. Machida K, Aritoku Y, Nakashima T, Arisawa A, Tsuchida T (2008b) Increase in pladienolide D production rate using a Streptomyces strain overexpressing a cytochrome P450 gene. J Biosci Bioeng 105:649–654
59. Machida K, Aritoku Y, Tsuchida T (2009) One-pot fermentation of pladienolide D by Streptomyces platensis expressing a heterologous cytochrome P450 gene. J Biosci Bioeng 107:596–598
60. Maharjan S, Oh TJ, Lee HC, Sohng JK (2008) Heterologous expression of metK1-sp and afsR-sp in Streptomyces venezuelae for the production of pikromycin. Biotechnol Lett 30:1621–1626
61. Maharjan S, Koju D, Lee HC, Yoo JC, Sohng JK (2012) Metabolic engineering of Nocardia sp. CS682 for enhanced production of nargenicin A1. Appl Biochem Biotechnol 166:805–817
62. McDowall KJ, Thamchaipenet A, Hunter IS (1999) Phosphate control of oxytetracycline production by Streptomyces rimosus is at the level of transcription from promoters overlapped by tandem repeats similar to those of the DNA-binding sites of the OmpR family. J Bacteriol 181:3025–3032
63. Medema MH, Breitling R, Bovenberg R, Takano E (2011) Exploiting plug-and-play synthetic biology for drug discovery and production in microorganisms. Nat Rev Microbiol 9:131–137
64. Menzella HG, Reeves CD (2007) Combinatorial biosynthesis for drug development. Curr Opin Microbiol 10:238–245
65. Miller-Wideman M, Makkar N, Tran M, Isaac B, Biest N, Stonard R (1992) Herboxidiene, a new herbicidal substance from Streptomyces chromofuscus A7847. Taxonomy, fermentation, isolation, physico-chemical and biological properties. J Antibiot 45:914–921
66. Nakajima H, Hori Y, Terano H, Okuhara M, Manda T, Matsumoto S, Shimomura K (1996a) New antitumor substances, FR901463, FR901464 and FR901465. II Activities against experimental tumors in mice and mechanism of action. J Antibiot 49:1204–1211
67. Nakajima H, Sato B, Fujita T, Takase S, Terano H, Okuhara M (1996b) New antitumor substances, FR901463, FR901464 and FR901465. I. Taxonomy, fermentation, isolation, physico-chemical properties and biological activities. J Antibiot 49:1196–1203
68. Nett M, Ikeda H, Moore BS (2009) Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat Prod Rep 26:1362–1384
69. Nguyen QT, Merlo ME, Medema MH, Jankevics A, Breitling R, Takano E (2012) Metabolomics methods for the synthetic biology of secondary metabolism. FEBS Lett 586:2177–2183
70. Okamoto S, Lezhava A, Hosaka T, Okamoto-Hosoya Y, Ochi K (2003) Enhanced expression of S-adenosylmethionine synthetase causes overproduction of actinorhodin in Streptomyces coelicolor A3(2). J Bacteriol 185:601–609
71. Olano C, Lombó F, Méndez C, Salas JA (2008) Improving production of bioactive secondary metabolites in actinomycetes by metabolic engineering. Metab Eng 10:281–292
72. Parajuli N, Viet HT, Ishida K, Tong HT, Lee HC, Liou K, Sohng JK (2005) Identification and characterization of the afsR homologue regulatory gene from Streptomyces peucetius ATCC 27952. Res Microbiol 156:707–712
73. Parajuli P, Pandey RP, Pokhrel AR, Ghimire GP, Sohng JK (2014) Enzymatic glycosylation of the topical antibiotic mupirocin. Glycoconj J 31:563–572
74. Park HR, Lee JC, Hwang JH, Park DJ, Kim C (2007) Glycerol affects the acyl moieties of teicoplanin components produced by Actinoplanes teichomyceticus MSl2210. Microbiol Res 164:588–592
75. Patrikainen P, Kallio P, Fan K, Klika KD, Shaaban KA, Mäntsälä P, Rohr J, Yang K, Niemi J, Metsä-Ketelä M (2012) Tailoring enzymes involved in the biosynthesis of angucyclines contain latent context-dependent catalytic activities. Chem Biol 19:647–655
76. Pickens LB, Tang Y, Chooi YH (2011) Metabolic engineering for the production of natural products. Annu Rev Chem Biomol Eng 2:211–236
77. Podust LM, Sherman DH (2012) Diversity of P450 enzymes in the biosynthesis of natural products. Nat Prod Rep 29:1251–1266
78. Poulos TL, Finzel BC, Howard AJ (1987) High-resolution crystal structure of cytochrome P450cam. J Mol Biol 195:687–700
79. Rix U, Fischer C, Remsing LL, Rohr J (2002) Modification of post-PKS tailoring steps through combinatorial biosynthesis. Nat Prod Rep 19:542–580
80. Roybal GA, Jurica MS (2010) Spliceostatin A inhibits spliceosome assembly subsequent to prespliceosome formation. Nucleic Acids Res 38:6664–6672
81. Ryu YG, Butler MJ, Chater KF, Lee KJ (2006) Engineering of primary carbohydrate metabolism for increased production of actinorhodin in Streptomyces coelicolor. Appl Environ Microbiol 72:7132–7139
82. Sakai Y, Tsujita T, Akiyama T, Yoshida T, Mizukami T, Akinaga S, Horinouchi S, Yoshida M, Yoshida T (2002a) GEX1 compounds, novel antitumor antibiotics related to herboxidiene, produced by Streptomyces sp. II The effects on cell cycle progression and gene expression. J Antibiot 55:863–872
83. Sakai Y, Tsujita T, Akiyama T, Yoshida T, Mizukami T, Akinaga S, Horinouchi S, Yoshida M, Yoshida T (2002b) GEX1 compounds, novel antitumor antibiotics related to herboxidiene, produced by Streptomyces sp. I. Taxonomy, production, isolation, physicochemical properties and biological activities. J Antibiot 55:855–862
84. Shafiee A, Hutchinson CR (1988) Purification and reconstitution of the electron transport components for 6-deoxyerythronolide B hydroxylase, a cytochrome P-450 enzyme of macrolide antibiotic (erythromycin) biosynthesis. J Bacteriol 170:1548–1553
85. Shao L, Zi J, Zeng J, Zhan J (2012) Identification of the herboxidiene biosynthetic gene cluster in Streptomyces chromofuscus ATCC 49982. Appl Microbiol Biotechnol 78:2034–2038
86. Shen B (2003) Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms. Curr Opin Chem Biol 7:285–295
87. Siegl T, Luzhetskyy A (2012) Actinomycetes genome engineering approaches. Antonie Van Leeuwenhoek 102:503–516
88. Staunton J, Weissman KJ (2001) Polyketide biosynthesis: a millennium review. Nat Prod Rep 18:380–416
89. Tsai SC, Lu H, Cane DE, Khosla C, Stroud RM (2002) Insights into channel architecture and substrate specificity from crystal structures of two macrocycle-forming thioesterases of modular polyketide synthases. Biochemistry 41:12598–12606
90. Weber T, Charusanti P, Musiol-Kroll EM, Jiang X, Tong Y, Kim HU, Lee SY (2015) Metabolic engineering of antibiotic factories: new tools for antibiotic production in actinomycetes. Trends Biotechnol 33:15–26
91. Wietzorrek A, Bibb M (1997) A novel family of proteins that regulates antibiotic production in streptomycetes appears to contain an OmpR-like DNA-binding fold. Mol Microbiol 25:1181–1184
92. Wong FT, Khosla C (2012) Combinatorial biosynthesis of polyketides-a perspective. J Bacteriol 16:117–123
93. Yoon YJ, Beck BJ, Kim BS, Kang HY, Reynolds KA, Sherman DH (2002) Generation of multiple bioactive macrolides by hybrid modular polyketide synthases in Streptomyces venezuelae. Chem Biol 9:203–214
94. Yu D, Xu F, Zhang S, Shao L, Wang S, Zhan J (2013) Characterization of a methyltransferase involved in herboxidiene biosynthesis. Bioorg Med Chem Lett 23:5667–5670
95. Yu D, Xu F, Shao L, Zhan J (2014) A specific cytochrome P450 hydroxylase in herboxidiene biosynthesis. Bioorg Med Chem Lett 24:4511–4514
96. Zhang Y, Panek JS (2007) Total synthesis of herboxidiene/GEX 1A. Org Lett 9:3141–3143
97. Zhang Q, Sherman DH (2001) Isolation and structure determination of novamethymycin, a new bioactive metabolite of the methymycin biosynthetic pathway in Streptomyces venezuelae. J Nat Prod 64:1447–1450
98. Zhao XQ, Jin YY, Kwon HJ, Yang YY, Suh JW (2006) S-Adenosylmethionine (SAM) regulates antibiotic biosynthesis in Streptomyces spp. in a mode independent of its role as a methyl donor. J Microbiol Biotechnol 16:927–932