Biosynthesis of sphinganine-analog mycotoxins

Journal of Industrial Microbiology and Biotechnology

Volumn 35, Issue 6, 2008, Pages 455-464

  Du, L ^a   Zhu, X ^a   Gerber, R ^a   Huffman, J ^a   Lou, L ^a   Jorgenson, J ^a   Yu, F ^a   Zaleta Rivera, K ^a   Wang, Q ^b  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

AAL toxins; Biosynthesis; Fumonisins; Polyketides; Sphinganine analog mycotoxins

Indexed keywords

CERAMIDE; FUMONISIN; MYCOTOXIN; POLYKETIDE; PYRIDOXAL 5 PHOSPHATE; SPHINGANINE; THIOL ESTER HYDROLASE;

ACTINOBACTERIA; ALTERNARIA ALTERNATA; ASPERGILLUS FLAVUS; ASPERGILLUS FUMIGATUS; ASPERGILLUS PARASITICUS; BIOSYNTHESIS; CATALYSIS; COCHLIOBOLUS HETEROSTROPHUS; COLLETOTRICHUM; ENZYME MECHANISM; GENETIC ANALYSIS; HUMAN; NONHUMAN; PENICILLIUM; PNEUMONIA; REVIEW;

ASCOMYCOTA; MYCOTOXINS; POLYKETIDE SYNTHASES; SPHINGOSINE;

ANIMALIA; BACTERIA (MICROORGANISMS); FUNGI;

EID: 43749091938     PISSN: 13675435     EISSN: 14765535     Source Type: Journal    
DOI: 10.1007/s10295-008-0316-y     Document Type: Review

References (89)

1. Abbas HK, Duke SO, Shier WT, Riley RT, Kraus GA (1996) The chemistry and biological activities of the natural products AAL-toxin and the fumonisins. Adv Exp Med Biol 391:293-308
2. Beck J, Ripka S, Siegner A, Schiltz E, Schweizer E (1990) The multifunctional 6-methylsalicylic acid synthase gene of Penicillium patulum. Its gene structure relative to that of other polyketide synthases. Eur J Biochem 192:487-498
3. Bedford DJ, Schweizer E, Hopwood DA, Khosla C (1995) Expression of a functional fungal polyketide synthase in the bacterium Streptomyces coelicolor A3(2). J Bacteriol 177:4544-4548
4. Bingle LE, Simpson TJ, Lazarus CM (1999) Ketosynthase domain probes identify two subclasses of fungal polyketide synthase genes. Fungal Genet Biol 26:209-223
5. Blackwell BA, Edwards OE, Fruchier A, ApSimon JW, Miller JD (1996) NMR structural studies of fumonisin B1 and related compounds from Fusarium moniliforme. Adv Exp Med Biol 392:75-91
6. Bojja RS, Cerny RL, Proctor RH, Du L (2004) Determining the biosynthetic sequence in the early steps of the fumonisin pathway by use of three gene-disruption mutants of Fusarium verticillioides. J Agric Food Chem 52:2855-2860
7. Bottini AT, Bowen JR, Gilchrist DG (1981) Phytotoxins. II. A characterization of a phytotoxic fraction from Alternaria alternata f. sp. lycopersici. Tetrahedron Lett 22:2723-2726
8. Bottini AT, Gilchrist DG (1981) Phytotoxins. I. A 1- aminodimethylheptadecapentol from Alternaria alternata f. sp. lycopersici. Tetrahedron Lett 22:2719-2722
9. Brandwagt BF, Mesbah LA, Takken FL, Laurent PL, Kneppers TJ, Hille J, Nijkamp HJ (2000) A longevity assurance gene homolog of tomato mediates resistance to Alternaria alternata f. sp. lycopersici toxins and fumonisin B1. Proc Natl Acad Sci USA 97:4961-4966
10. Branham BE, Plattner RD (1993) Alanine is a precursor in the biosynthesis of fumonisin B1 by Fusarium moniliforme. Mycopathologia 124:99-104
11. Brown DW, Yu JH, Kelkar HS, Fernandes M, Nesbitt TC, Keller NP, Adams TH, Leonard TJ (1996) Twenty-five coregulated transcripts define a sterigmatocystin gene cluster in Aspergillus nidulans. Proc Natl Acad Sci USA 93:1418-1422
12. Bruner SD, Weber T, Kohli RM, Schwarzer D, Marahiel MA, Walsh CT, Stubbs MT (2002) Structural basis for the cyclization of the lipopeptide antibiotic surfactin by the thioesterase domain SrfTE. Structure 10:301-310
13. Butchko RA, Plattner RD, Proctor RH (2003) FUM9 is required for C-5 hydroxylation of fumonisins and complements the meitotically defined Fum3 locus in Gibberella moniliformis. Appl Environ Microbiol 69:6935-6937
14. Butchko RA, Plattner RD, Proctor RH (2003) FUM13 encodes a short chain dehydrogenase/reductase required for C-3 carbonyl reduction during fumonisin biosynthesis in Gibberella moniliformis. J Agric Food Chem 51:3000-3006
15. Butchko RA, Plattner RD, Proctor RH (2006) Deletion analysis of FUM genes involved in tricarballylic ester formation during fumonisin biosynthesis. J Agric Food Chem 54:9398-9404
16. Caldas ED, Sadilkova K, Ward BL, Jones AD, Winter CK, Gilchrist DG (1998) Biosynthetic studies of fumonisin B1 and AAL toxins. J Agric Food Chem 46:4734-4743
17. Cane DE, Walsh CT, Khosla C (1998) Harnessing the biosynthetic code: combinations, permutations, and mutations. Science 282:63-68
18. Cheng Q, Xiang L, Izumikawa M, Meluzzi D, Moore BS (2007) Enzymatic total synthesis of enterocin polyketides. Nat Chem Biol 3:557-558
19. Cortes J, Haydock SF, Roberts GA, Bevitt DJ, Leadlay PF (1990) An unusually large multifunctional polypeptide in the erythromycin-producing polyketide synthase of Saccharopolyspora erythraea. Nature 348:176-178
20. Cox RJ (2007) Polyketides, proteins, genes in fungi programmed nano-machines begin to reveal their secrets. Org Biomol Chem 5:2010-2026
21. Cox RJ, Glod F, Hurley D, Lazarus CM, Nicholson TP, Rudd BA, Simpson TJ, Wilkinson B, Zhang Y (2004) Rapid cloning and expression of a fungal polyketide synthase gene involved in squalestatin biosynthesis Chem Commun (Camb) 20:2260-2261
22. Crawford JM, Dancy BC, Hill EA, Udwary DW, Townsend CA (2006) Identification of a starter unit acyl-carrier protein transacylase domain in an iterative type I polyketide synthase. Proc Natl Acad Sci USA 103:16728-16733
23. Desjardins AE, Proctor RH (2007) Molecular biology of Fusarium mycotoxins. Int J Food Microbiol 119(1-2):47-50 (Epub ahead of print, PMID: 17707105)
24. Dimroth P, Ringelmann E, Lynen F (1976) 6-Methylsalicylic acid synthetase from Penicillium patulum. Some catalytic properties of the enzyme and its relation to fatty acid synthetase. Eur J Biochem 68:591-596
25. Ding Y, Bojja RS, Du L (2004) Fum3p, a 2-ketoglutarate-dependent dioxygenase required for C-5 hydroxylation of fumonisins in Fusarium verticillioides. Appl Environ Microbiol 70:1931-1934
26. Donadio S, Katz L (1992) Organization of the enzymatic domains in the multifunctional polyketide synthase involved in erythromycin formation in Saccharopolyspora erythraea. Gene 111:51-60
27. Donadio S, Staver MJ, McAlpine JB, Swanson SJ, Katz L (1991) Modular organization of genes required for complex polyketide biosynthesis. Science 252:675-679
28. Du L, Yu F, Zhu X, Zaleta-Rivera K, Bojja RS, Ding Y, Yi H, Wang Q (2007) Biochemical and molecular analysis of the biosynthesis of fumonisins. In: Baerson SR (ed) Polyketides: biosynthesis, biological activities and genetic engineering, American Chemical Society, Washington, DC, pp 81-96
29. Eley KL, Halo LM, Song Z, Powles H, Cox RJ, Bailey AM, Lazarus CM, Simpson TJ (2007) Biosynthesis of the 2-pyridone tenellin in the insect pathogenic fungus Beauveria bassiana. Chembiochem 8:289-297
30. Feng B, Wang X, Hauser M, Kaufmann S, Jentsch S, Haase G, Becker JM, Szaniszlo PJ (2001) Molecular cloning and characterization of WdPKS1, a gene involved in dihydroxynaphthalene melanin biosynthesis and virulence in Wangiella (Exophiala) dermatitidis. Infect Immun 69:1781-1794
31. Ferreira GC, Vajapey U, Hafez O, Hunter GA, Barber MJ (1995) Aminolevulinate synthase: lysine 313 is not essential for binding the pyridoxal phosphate cofactor but is essential for catalysis. Protein Sci 4:1001-1006
32. Fischbach MA, Walsh CT (2006) Assembly-line enzymology for polyketide and nonribosomal Peptide antibiotics: logic, machinery, and mechanisms. Chem Rev 106:3468-3496
33. Fujii I, Mori Y, Watanabe A, Kubo Y, Tsuji G, Ebizuka Y (1999) Heterologous expression and product identification of Colletotrichum lagenarium polyketide synthase encoded by the PKS1 gene involved in melanin biosynthesis. Biosci Biotechnol Biochem 63:1445-1452
34. Fujii I, Ono Y, Tada H, Gomi K, Ebizuka Y, Sankawa U (1996) Cloning of the polyketide synthase gene atX from Aspergillus terreus and its identification as the 6-methylsalicylic acid synthase gene by heterologous expression. Mol Gen Genet 253:1-10
35. Fujii I, Watanabe A, Sankawa U, Ebizuka Y (2001) Identification of Claisen cyclase domain in fungal polyketide synthase WA, a naphthopyrone synthase of Aspergillus nidulans. Chem Biol 8:189-197
36. Gable K, Han G, Monaghan E, Bacikova D, Natarajan M, Williams R, Dunn TM (2002) Mutations in the yeast LCB1 and LCB2 genes, including those corresponding to the hereditary sensory neuropathy type I mutations, dominantly inactivate serine palmitoyltransferase. J Biol Chem 277:10194-10200
37. Gilchrist DG, Grogan RG (1976) Production and nature of a host-specific toxin from Alternaria alternata f. sp. lycopersici. Phytopathology 66:165-171
38. Hanada K (2003) Serine palmitoyltransferase, a key enzyme of sphingolipid metabolism. Biochim Biophys Acta 1632:16-30
39. Hoffmeister D, Keller NP (2007) Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep 24:393-416
40. Hopwood DA (1997) Genetic contributions to understanding polyketide synthases. Chem Rev 97:2465-2498
41. Kealey JT, Liu L, Santi DV, Betlach MC, Barr PJ (1998) Production of a polyketide natural product in nonpolyketide-producing prokaryotic and eukaryotic hosts. Proc Natl Acad Sci USA 95:505-509
42. Kennedy J, Auclair K, Kendrew SG, Park C, Vederas JC, Hutchinson CR (1999) Modulation of polyketide synthase activity by accessory proteins during lovastatin biosynthesis. Science 284:1368-1372
43. Khosla C, Gokhale RS, Jacobsen JR, Cane DE (1999) Tolerance and specificity of polyketide synthases. Annu Rev Biochem 68:219-253
44. Khosla C, Tang Y, Chen AY, Schnarr NA, Cane DE (2007) Structure and mechanism of the 6-deoxyerythronolide B synthase. Annu Rev Biochem 76:195-221
45. Kittendorf JD, Sherman DH (2006) Developing tools for engineering hybrid polyketide synthetic pathways. Curr Opin Biotechnol 17:597-605
46. Kongsaeree P, Prabpai S, Sriubolmas N, Vongvein C, Wiyakrutta S (2003) Antimalarial dihydroisocoumarins produced by Geotrichum sp., an endophytic fungus of Crassocephalum crepidioides. J Nat Prod 66:709-711
47. Kono Y, Daly JM (1979) Characterization of the host-specific pathotoxin produced by Helminthosporium maydis race T affecting corn with Texas male sterile cytoplasm. Bioorg Chem 8:391-397
48. Kroken S, Glass NL, Taylor JW, Yoder OC, Turgeon BG (2003) Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Natl Acad Sci USA 100:15670-15675
49. Lambalot RH, Gehring AM, Flugel RS, Zuber P, LaCelle M, Marahiel MA, Reid R, Khosla C, Walsh CT (1996) A new enzyme superfamily-the phosphopantetheinyl transferases. Chem Biol 3:923-936
50. Marasas WF, Riley RT, Hendricks KA, Stevens VL, Sadler TW, Gelineau-van Waes J, Missmer SA, Cabrera J, Torres O, Gelderblom WC, Allegood J, Martinez C, Maddox J, Miller JD, Starr L, Sullards MC, Roman AV, Voss KA, Wang E, Merrill AH Jr (2004) Fumonisins disrupt sphingolipid metabolism, folate transport, and neural tube development in embryo culture and in vivo: a potential risk factor for human neural tube defects among populations consuming fumonisin-contaminated maize. J Nutr 134:711-716
51. Menzella HG, Reeves CD (2007) Combinatorial biosynthesis for drug development. Curr Opin Microbiol 10:238-245
52. Merrill AH Jr, van Echten G, Wang E, Sandhoff K (1993) Fumonisin B1 inhibits sphingosine (sphinganine) N-acyltransferase and de novo sphingolipid biosynthesis in cultured neurons in situ. J Biol Chem 268:27299-27306
53. Minto RE, Townsend CA (1997) Enzymology and molecular biology of aflatoxin biosynthesis. Chem Rev 97:2537-2556
54. Moore BS, Hertweck C (2002) Biosynthesis and attachment of novel bacterial polyketide synthase starter units. Nat Prod Rep 19:70-99
55. Moriguchi T, Ebizuka Y, Fujii I (2006) Analysis of subunit interactions in the iterative type I polyketide synthase ATX from Aspergillus terreus. Chembiochem 7:1869-1874
56. Nelson PE, Desjardins AE, Plattner RD (1993) Fumonisins, mycotoxins produced by Fusarium species: biology, chemistry, and significance. Annu Rev Phytopathol 31:233-252
57. Nesbitt BF, O'Kelly J, Sargeant K, Sheridan A (1962) Aspergillus flavus and turkey X disease. Toxic metabolites of Aspergillus flavus. Nature 195:1062-1063
58. Nicholson TP, Rudd BA, Dawson M, Lazarus CM, Simpson TJ, Cox RJ (2001) Design and utility of oligonucleotide gene probes for fungal polyketide synthases. Chem Biol 8:157-178
59. Plattner RD, Shackelford DD (1992) Biosynthesis of labeled fumonisins in liquid cultures of Fusarium moniliforme. Mycopathologia 117:17-22
60. Price WD, Lovell RA, McChesney DG (1993) Naturally occurring toxins in feedstuffs: Center for Veterinary Medicine Perspective. J Anim Sci 71:2556-2562
61. Proctor RH, Brown DW, Plattner RD, Desjardins AE (2003) Co-expression of 15 contiguous genes delineates a fumonisin biosynthetic gene cluster in Gibberella moniliformis. Fungal Genet Biol 38:237-249
62. Proctor RH, Desjardins AE, Plattner RD, Hohn TM (1999) A polyketide synthase gene required for biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal Genet Biol 27:100-112
63. Proctor RH, Plattner RD, Desjardins AE, Busman M, Butchko RA (2006) Fumonisin production in the maize pathogen Fusarium verticillioides: genetic basis of naturally occurring chemical variation. J Agric Food Chem 54:2424-2430
64. Richardson MT, Pohl NL, Kealey JT, Khosla C (1999) Tolerance and specificity of recombinant 6-methylsalicyclic acid synthase. Metab Eng 1:180-187
65. Riley RT, Wang E, Schroeder JJ, Smith ER, Plattner RD, Abbas H, Yoo HS, Merrill AH Jr (1996) Evidence for disruption of sphingolipid metabolism as a contributing factor in the toxicity and carcinogenicity of fumonisins. Nat Toxins 4:3-15
66. Seo JA, Proctor RH, Plattner RD (2001) Characterization of four clustered and coregulated genes associated with fumonisin biosynthesis in Fusarium verticillioides. Fungal Genet Biol 34:155-165
67. Shen B (2000) Biosynthesis of aromatic polyketides. Top Curr Chem 209:1-51
68. Shiao MS, Don HS (1987) Biosynthesis of mevinolin, a hypocholesterolemic fungal metabolite, in Aspergillus terreus. Proc Natl Sci Counc Repub China B 11:223-231
69. Sims JW, Fillmore JP, Warner DD, Schmidt EW (2005) Equisetin biosynthesis in Fusarium heterosporum. Chem Commun (Camb) 2:186-188
70. Song Z, Cox RJ, Lazarus CM, Simpson TT (2004) Fusarin C biosynthesis in Fusarium moniliforme and Fusarium venenatum. Chembiochem 5:1196-1203
71. 2H]malonates. Biochem 31:9107-9116
72. Staunton J, Weissman KJ (2001) Polyketide biosynthesis: a millennium review. Nat Prod Rep 18:380-416
73. Sweeney MJ, Dobson AD (1999) Molecular biology of mycotoxin biosynthesis. FEMS Microbiol Lett 175:149-163
74. Tang Y, Kim CY, Mathews II, Cane DE, Khosla C (2006) The 2.7-Angstrom crystal structure of a 194-kDa homodimeric fragment of the 6-deoxyerythronolide B synthase. Proc Natl Acad Sci USA 103:11124-11129
75. Tsai HF, Fujii I, Watanabe A, Wheeler MH, Chang YC, Yasuoka Y, Ebizuka Y, Kwon-Chung KJ (2001) Pentaketide melanin biosynthesis in Aspergillus fumigatus requires chain-length shortening of a heptaketide precursor. J Biol Chem 276:29292-29298
76. Walsh CT, Gehring AM, Weinreb PH, Quadri LE, Flugel RS (1997) Post-translational modification of polyketide and nonribosomal peptide synthases. Curr Opin Chem Biol 1:309-315
77. Wang Q, Wang J, Yu F, Zhu X, Zaleta-Rivera K, Du L (2006) Mycotoxin fumonisins: health impacts and biosynthetic mechanism. Prog Nat Sci 16:7-15
78. Wang W, Jones C, Ciacci-Zanella J, Holt T, Gilchrist DG, Dickman MB (1996) Fumonisins and Alternaria alternata lycopersici toxins: sphinganine analog mycotoxins induce apoptosis in monkey kidney cells. Proc Natl Acad Sci USA 93:3461-3465
79. Watanabe A, Ebizuka Y (2004) Unprecedented mechanism of chain length determination in fungal aromatic polyketide synthases. Chem Biol 11:1101-1106
80. Watanabe A, Fujii I, Tsai H, Chang YC, Kwon-Chung KJ, Ebizuka Y (2000) Aspergillus fumigatus alb1 encodes naphthopyrone synthase when expressed in Aspergillus oryzae. FEMS Microbiol Lett 192:39-44
81. Webster SP, Alexeev D, Campopiano DJ, Watt RM, Alexeeva M, Sawyer L, Baxter RL (2000) Mechanism of 8-amino-7-oxononanoate synthase: spectroscopic, kinetic, and crystallographic studies. Biochem 39:516-528
82. Winter CK, Gilchrist DG, Dickman MB, Jones C (1996) Chemistry and biological activity of AAL toxins. Adv Exp Med Biol 392:307-316
83. 13C in biosynthetic studies. The labelling pattern in tenellin enriched from isotope-labelled acetate, methionine, and phenylalanine. Can J Biochem 55:678-685
84. Yang G, Rose MS, Turgeon BG, Yoder OC (1996) A polyketide synthase is required for fungal virulence and production of the polyketide T-toxin. Plant Cell 8:2139-2150
85. Yi H, Bojja RS, Fu J, Du L (2005) Direct evidence for the function of FUM13 in 3-ketoreduction of mycotoxin fumonisins in Fusarium verticillioides. J Agric Food Chem 53:5456-5460
86. Yu F, Zhu X, Du L (2005) Developing a genetic system for functional manipulations of FUM1, a polyketide synthase gene for the biosynthesis of fumonisins in Fusarium verticillioides. FEMS Microbiol Lett 248:257-264
87. Zaleta-Rivera K, Xu C, Yu F, Butchko RA, Proctor RH, Hidalgo-Lara ME, Raza A, Dussault PH, Du L (2006) A bidomain nonribosomal peptide synthetase encoded by FUM14 catalyzes the formation of tricarballylic esters in the biosynthesis of fumonisins. Biochem 45:2561-2569
88. Zhu X, Yu F, Bojja RS, Zaleta-Rivera K, Du L (2006) Functional replacement of the ketosynthase domain of FUM1 for the biosynthesis of fumonisins, a group of fungal reduced polyketides. J Ind Microbiol Biotechnol 33:859-868
89. Zhu X, Yu F, Li XC, Du L (2007) Production of dihydroisocoumarins in Fusarium verticillioides by swapping ketosynthase domain of the fungal iterative polyketide synthase Fum1p with that of lovastatin diketide synthase. J Am Chem Soc 129:36-37