Genome neighborhood network reveals insights into enediyne biosynthesis and facilitates prediction and prioritization for discovery

Journal of Industrial Microbiology and Biotechnology

Volumn 43, Issue 2-3, 2016, Pages 261-276

  Rudolf, Jeffrey D ^a   Yan, Xiaohui ^a   Shen, Ben ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Biosynthetic gene cluster; Enediyne polyketide synthase; Genome mining; Genome neighborhood network; Natural products

Indexed keywords

ANTIBIOTIC C 1027; CALICHEAMICIN; CYANOSPORASIDE DERIVATIVE; DYNEMICIN; ENEDIYNE; EOCARZINOSTATIN; ESPERAMICIN; FIJIOLIDE DERIVATIVE; KEDARCIDIN; MADUROPEPTIN; N 1999A 2; NAMENAMICIN; SALINISPORA PACIFICA; SHISHIJIMICIN DERIVATIVE; SPOROLIDE DERIVATIVE; UNCIALAMYCIN; UNCLASSIFIED DRUG; BIOLOGICAL PRODUCT; POLYKETIDE SYNTHASE;

ACTINOMADURA MADURAE; ACTINOMADURA VERRUCOSOSPORA; ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BIOSYNTHESIS; CHEMICAL STRUCTURE; DIDEMNUM PROLIFERUM; DNA SEQUENCE; GENE CLUSTER; GENOME NEIGHBORHOOD NETWORK; HIGH THROUGHPUT SEQUENCING; MICROMONOSPORA ECHINOSPORA; NOCARDIOPSIS; NONHUMAN; PHYLOGENY; POLYSYNCRATON LITHOSTROTUM; SALINISPORA TROPICA; STREPTOMYCES; STREPTOMYCES CARZINOSTATICUS; STREPTOMYCES GLOBISPORUS; BACTERIUM; CHEMISTRY; DRUG DEVELOPMENT; ENZYMOLOGY; GENETICS; GENOMICS; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; SECONDARY METABOLISM;

BACTERIA; BIOLOGICAL PRODUCTS; BIOSYNTHETIC PATHWAYS; DRUG DISCOVERY; ENEDIYNES; GENOME, BACTERIAL; GENOMICS; MOLECULAR SEQUENCE ANNOTATION; MULTIGENE FAMILY; POLYKETIDE SYNTHASES; SECONDARY METABOLISM;

EID: 84958119312     PISSN: 13675435     EISSN: 14765535     Source Type: Journal    
DOI: 10.1007/s10295-015-1671-0     Document Type: Article

References (58)

1. Ahlert J, Shepard E, Lomovskaya N, Zazopoulos E, Staffa A, Bachmann BO, Huang K, Fonstein L, Czisny A, Whitwam RE, Farnet CM, Thorson JS (2002) The calicheamicin gene cluster and its iterative type I enediyne PKS. Science 297:1173–1176. doi:10.1126/science.1072105
2. Belecki K, Crawford JM, Townsend CA (2009) Production of octaketide polyenes by the calicheamicin polyketide synthase CalE8: implications for the biosynthesis of enediyne core structures. J Am Chem Soc 131:12564–12566. doi:10.1021/ja904391r
3. Boghaert ER, Sridharan L, Armellino DC, Khandke KM, DiJoseph JF, Kunz A, Dougher MM, Jiang F, Kalyandrug LB, Hamann PR, Frost P, Damle NK (2004) Antibody-targeted chemotherapy with the calicheamicin conjugate hu3S193-N-acetyl γ calicheamicin dimethyl hydrazide targets Lewisy and eliminates Lewisy-positive human carcinoma cells and xenografts. Clin Cancer Res 10:4538–4549. doi:10.1158/1078-0432.ccr-04-0037
4. Brown SD, Babbitt PC (2012) Inference of functional properties from large-scale analysis of enzyme superfamilies. J Biol Chem 287:35–42. doi:10.1074/jbc.R111.283408
5. Buchanan GO, Williams PG, Feling RH, Kauffman CA, Jensen PR, Fenical W (2005) Sporolides A and B: structurally unprecedented halogenated macrolides from the marine actinomycete Salinisporatropica. Org Lett 7:2731–2734. doi:10.1021/ol050901i
6. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden Thomas L (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421. doi:10.1186/1471-2105-10-421
7. Chari RVJ (2008) Targeted cancer therapy: conferring specificity to cytotoxic drugs. Acc Chem Res 41:98–107. doi:10.1021/ar700108g
8. Chow J-Y, Tian B-X, Ramamoorthy G, Hillerich BS, Seidel RD, Almo SC, Jacobson MP, Poulter CD (2015) Computational-guided discovery and characterization of a sesquiterpene synthase from Streptomycesclavuligerus. Proc Natl Acad Sci USA 112:5661–5666. doi:10.1073/pnas.1505127112
9. Davies J, Wang H, Taylor T, Warabi K, Huang X-H, Andersen RJ (2005) Uncialamycin, a new enediyne antibiotic. Org Lett 7:5233–5236. doi:10.1021/ol052081f
10. Dedon PC, Goldberg IH (1990) Sequence-specific double-strand breakage of DNA by neocarzinostatin involves different chemical mechanisms within a staggered cleavage site. J Biol Chem 265:14713–14716
11. Edo K, Mizugaki M, Koide Y, Seto H, Furihata K, Otake N, Ishida N (1985) The structure of neocarzinostatin chromophore possessing a novel bicyclo[7.3.0]dodecadiyne system. Tetrahedron Lett 26:331–334. doi:10.1016/s0040-4039(01)80810-8
12. Elshahawi SI, Ramelot TA, Seetharaman J, Chen J, Singh S, Yang Y, Pederson K, Kharel MK, Xiao R, Lew S, Yennamalli RM, Miller MD, Wang F, Tong L, Montelione GT, Kennedy MA, Bingman CA, Zhu H, Phillips GN, Thorson JS (2014) Structure-guided functional characterization of enediyne self-sacrifice resistance proteins, CalU16 and CalU19. ACS Chem Biol 9:2347–2358. doi:10.1021/cb500327m
13. Galm U, Hager MH, Van Lanen SG, Ju J, Thorson JS, Shen B (2005) Antitumor antibiotics: bleomycin, enediynes, and mitomycin. Chem Rev 105:739–758. doi:10.1021/cr030117g
14. Gao Q, Thorson JS (2008) The biosynthetic genes encoding for the production of the dynemicin enediyne core in Micromonosporachersina ATCC53710. FEMS Microbiol Lett 282:105–114. doi:10.1111/j.1574-6968.2008.01112.x
15. Golik J, Dubay G, Groenewold G, Kawaguchi H, Konishi M, Krishnan B, Ohkuma H, Saitoh K, Doyle TW (1987) Esperamicins, a novel class of potent antitumor antibiotics. 3. Structures of esperamicins A1, A2, and A1b. J Am Chem Soc 109:3462–3464. doi:10.1021/ja00245a049
16. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98
17. Hirama M, Akiyama K, Tanaka T, Noda T, K-I Iida, Sato I, Hanaishi R, Fukuda-Ishisaka S, Ishiguro M, Otani T, Leet JE (2000) Paramagnetic enediyne antibiotic C-1027: spin identification and characterization of radical species. J Am Chem Soc 122:720–721. doi:10.1021/ja993256h
18. Horsman GP, Chen Y, Thorson JS, Shen B (2010) Polyketide synthase chemistry does not direct biosynthetic divergence between 9- and 10-membered enediynes. Proc Natl Acad Sci USA 107:11331–11335. doi:10.1073/pnas.1003442107
19. Horsman GP, Lechner A, Ohnishi Y, Moore BS, Shen B (2013) Predictive model for epoxide hydrolase-generated stereochemistry in the biosynthesis of nine-membered enediyne antitumor antibiotics. Biochemistry 52:5217–5224. doi:10.1021/bi400572a
20. Jones RR, Bergman RG (1972) p-Benzyne. Generation as an intermediate in a thermal isomerization reaction and trapping evidence for the 1,4-benzenediyl structure. J Am Chem Soc 94:660–661. doi:10.1021/ja00757a071
21. Kennedy DR, Ju J, Shen B, Beerman TA (2007) Designer enediynes generate DNA breaks, interstrand cross-links, or both, with concomitant changes in the regulation of DNA damage responses. Proc Natl Acad Sci USA 104:17632–17637. doi:10.1073/pnas.0708274104
22. Kobayashi S, Ashizawa S, Takahashi Y, Sugiura Y, Nagaoka M, Lear MJ, Hirama M (2001) The first total synthesis of N1999-A2: absolute stereochemistry and stereochemical implications into DNA cleavage. J Am Chem Soc 123:11294–11295. doi:10.1021/ja011779v
23. Komano K, Shimamura S, Norizuki Y, Zhao D, Kabuto C, Sato I, Hirama M (2009) Total synthesis and structure revision of the (−)-maduropeptin chromophore. J Am Chem Soc 131:12072–12073. doi:10.1021/ja905397p
24. Kong R, Goh LP, Liew CW, Ho QS, Murugan E, Li B, Tang K, Liang Z-X (2008) Characterization of a carbonyl-conjugated polyene precursor in 10-membered enediyne biosynthesis. J Am Chem Soc 130:8142–8143. doi:10.1021/ja8019643
25. Lane AL, Nam S-J, Fukuda T, Yamanaka K, Kauffman CA, Jensen PR, Fenical W, Moore BS (2013) Structures and comparative characterization of biosynthetic gene clusters for cyanosporasides, enediyne-derived natural products from marine actinomycetes. J Am Chem Soc 135:4171–4174. doi:10.1021/ja311065v
26. Lee MD, Dunne TS, Chang CC, Ellestad GA, Siegel MM, Morton GO, McGahren WJ, Borders DB (1987) Calichemicins, a novel family of antitumor antibiotics. 2. Chemistry and structure of calichemicin γ1I. J Am Chem Soc 109:3466–3468. doi:10.1021/ja00245a051
27. Liang Z-X (2010) Complexity and simplicity in the biosynthesis of enediyne natural products. Nat Prod Rep 27:499–528. doi:10.1039/b908165h
28. Lin S, Horsman GP, Chen Y, Li W, Shen B (2009) Characterization of the SgcF epoxide hydrolase supporting an (R)-vicinal diol intermediate for enediyne antitumor antibiotic C-1027 biosynthesis. J Am Chem Soc 131:16410–16417. doi:10.1021/ja901242s
29. Liu W, Christenson SD, Standage S, Shen B (2002) Biosynthesis of the enediyne antitumor antibiotic C-1027. Science 297:1170–1173. doi:10.1126/science.1072110
30. Liu W, Ahlert J, Gao Q, Wendt-Pienkowski E, Shen B, Thorson JS (2003) Rapid PCR amplification of minimal enediyne polyketide synthase cassettes leads to a predictive familial classification model. Proc Natl Acad Sci USA 100:11959–11963. doi:10.1073/pnas.2034291100
31. Liu W, Nonaka K, Nie L, Zhang J, Christenson SD, Bae J, Van Lanen SG, Zazopoulos E, Farnet CM, Yang CF, Shen B (2005) The neocarzinostatin biosynthetic gene cluster from Streptomycescarzinostaticus ATCC 15944 involving two iterative type I polyketide synthases. Chem Biol 12:293–302. doi:10.1016/j.chembiol.2004.12.013
32. Lohman JR, Huang S-X, Horsman GP, Dilfer PE, Huang T, Chen Y, Wendt-Pienkowski E, Shen B (2013) Cloning and sequencing of the kedarcidin biosynthetic gene cluster from Streptoalloteichus sp. ATCC 53650 revealing new insights into biosynthesis of the enediyne family of antitumor antibiotics. Mol Biosyst 9:478–491. doi:10.1039/c3mb25523a
33. McDonald LA, Capson TL, Krishnamurthy G, Ding W-D, Ellestad GA, Bernan VS, Maiese WM, Lassota P, Discafani C et al (1996) Namenamicin, a new enediyne antitumor antibiotic from the marine ascidian Polysyncratonlithostrotum. J Am Chem Soc 118:10898–10899. doi:10.1021/ja961122n
34. McGlinchey RP, Nett M, Moore BS (2008) Unraveling the biosynthesis of the sporolide cyclohexenone building block. J Am Chem Soc 130:2406–2407. doi:10.1021/ja710488m
35. Myers AG (1987) Proposed structure of the neocarzinostatin chromophore-methyl thioglycolate adduct; a mechanism for the nucleophilic activation of neocarzinostatin. Tetrahedron Lett 28:4493–4496. doi:10.1016/s0040-4039(00)96545-6
36. Myers AG, Fraley ME, Tom NJ, Cohen SB, Madar DJ (1995) Synthesis of (+)-dynemicin A and analogs of wide structural variability: establishment of the absolute configuration of natural dynemicin A. Chem Biol 2:33–43. doi:10.1016/1074-5521(95)90078-0
37. Nam S-J, Gaudencio SP, Kauffman CA, Jensen PR, Kondratyuk TP, Marler LE, Pezzuto JM, Fenical W (2010) Fijiolides A and B, inhibitors of TNF-α-induced NFκB activation, from a marine-derived sediment bacterium of the genus Nocardiopsis. J Nat Prod 73:1080–1086. doi:10.1021/np100087c
38. Oh D-C, Williams PG, Kauffman CA, Jensen PR, Fenical W (2006) Cyanosporasides A and B, chloro- and cyano-cyclopenta[a]indene glycosides from the marine actinomycete “Salinisporapacifica”. Org Lett 8:1021–1024. doi:10.1021/ol052686b
39. Oku N, Matsunaga S, Fusetani N (2003) Shishijimicins A–C, novel enediyne antitumor antibiotics from the ascidian Didemnumproliferum. J Am Chem Soc 125:2044–2045. doi:10.1021/ja0296780
40. Otani T, Yoshida K-I, Sasaki T, Minami Y (1999) C-1027 enediyne chromophore: presence of another active form and its chemical structure. J Antibiot 52:415–421. doi:10.7164/antibiotics.52.415
41. Ren F, Hogan PC, Anderson AJ, Myers AG (2007) Kedarcidin chromophore: synthesis of its proposed structure and evidence for a stereochemical revision. J Am Chem Soc 129:5381–5383. doi:10.1021/ja071205b
42. Rudolf JD, Dong L-B, Huang T, Shen B (2015) A genetically amenable platensimycin- and platencin-overproducer as a platform for biosynthetic explorations: a showcase of PtmO4, a long-chain acyl-CoA dehydrogenase. Mol Biosyst. doi:10.1039/C5MB00302D
43. Senter PD (2009) Potent antibody drug conjugates for cancer therapy. Curr Opin Chem Biol 13:235–244. doi:10.1016/j.cbpa.2009.03.023
44. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. doi:10.1101/gr.1239303
45. Shen B, Hindra Yan X, Huang T, Ge H, Yang D, Teng Q, Rudolf JD, Lohman JR (2015) Enediynes: exploration of microbial genomics to discover new anticancer drug leads. Bioorg Med Chem Lett 25:9–15. doi:10.1016/j.bmcl.2014.11.019
46. Sievers EL, Appelbaum FR, Spielberger RT, Forman SJ, Flowers D, Smith FO, Shannon-Dorcy K, Berger MS, Bernstein ID (1999) Selective ablation of acute myeloid leukemia using antibody-targeted chemotherapy: a phase I study of an anti-CD33 calicheamicin immunoconjugate. Blood 93:3678–3684
47. Sugimoto Y, Otani T, Oie S, Wierzba K, Yamada Y (1990) Mechanism of action of a new macromolecular antitumor antibiotic, C-1027. J Antibiot 43:417–421. doi:10.7164/antibiotics.43.417
48. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197
49. Thompson JD, Higgins DG, Gibson TJ (1994) Improved sensitivity of profile searches through the use of sequence weights and gap excision. CABIOS Comput Appl Biosci 10:19–29
50. Thorson JS, Sievers EL, Ahlert J, Shepard E, Whitwam RE, Onwueme KC, Ruppen M (2000) Understanding and exploiting nature’s chemical arsenal: the past, present and future of calicheamicin research. Curr Pharm Des 6:1841–1879. doi:10.2174/1381612003398564
51. Van Lanen SG, Shen B (2008) Biosynthesis of enediyne antitumor antibiotics. Curr Top Med Chem 8:448–459. doi:10.2174/156802608783955656
52. Van Lanen SG, T-j Oh, Liu W, Wendt-Pienkowski E, Shen B (2007) Characterization of the maduropeptin biosynthetic gene cluster from Actinomaduramadurae ATCC 39144 supporting a unifying paradigm for enediyne biosynthesis. J Am Chem Soc 129:13082–13094. doi:10.1021/ja073275o
53. Van Lanen SG, Lin S, Horsman GP, Shen B (2009) Characterization of SgcE6, the flavin reductase component supporting FAD-dependent halogenation and hydroxylation in the biosynthesis of the enediyne antitumor antibiotic C-1027. FEMS Microbiol Lett 300:237–241. doi:10.1111/j.1574-6968.2009.01802.x
54. Zazopoulos E, Huang K, Staffa A, Liu W, Bachmann BO, Nonaka K, Ahlert J, Thorson JS, Shen B, Farnet CM (2003) A genomics-guided approach for discovering and expressing cryptic metabolic pathways. Nat Biotechnol 21:187–190. doi:10.1038/nbt784
55. Zhang J, Van Lanen SG, Ju J, Liu W, Dorrestein PC, Li W, Kelleher NL, Shen B (2008) A phosphopantetheinylating polyketide synthase producing a linear polyene to initiate enediyne antitumor antibiotic biosynthesis. Proc Natl Acad Sci USA 105:1460–1465. doi:10.1073/pnas.0711625105
56. Zhang X, Kumar R, Vetting MW, Zhao S, Jacobson MP, Almo SC, Gerlt JA (2015) A unique cis-3-hydroxy-l-proline dehydratase in the enolase superfamily. J Am Chem Soc 137:1388–1391. doi:10.1021/ja5103986
57. Zhao S, Jacobson Matthew P, Sakai A, Zhang X, Kumar R, San Francisco B, Solbiati J, Gerlt John A, Vetting Matthew W, Hillerich B, Seidel Ronald D, Almo Steven C, Steves A, Brown S, Akiva E, Barber A, Babbitt Patricia C (2014) Prediction and characterization of enzymatic activities guided by sequence similarity and genome neighborhood networks. eLife 3:e03275. doi:10.7554/eLife.03275
58. Zhen Y, Ming X, Yu B, Otani T, Saito H, Yamada Y (1989) A new macromolecular antitumor antibiotic, C-1027. III. Antitumor activity. J Antibiot 42:1294–1298. doi:10.7164/antibiotics.42.1294