Recent advances in the biosynthesis of modified tetrapyrroles: the discovery of an alternative pathway for the formation of heme and heme d 1
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  • 作者:Shilpa Bali (2)
    David J. Palmer (1)
    Susanne Schroeder (1)
    Stuart J. Ferguson (2)
    Martin J. Warren (1)
  • 关键词:Heme ; Heme d 1 ; Tetrapyrrole biosynthesis ; Siroheme ; Modified tetrapyrrole ; Alternative heme biosynthesis
  • 刊名:Cellular and Molecular Life Sciences (CMLS)
  • 出版年:2014
  • 出版时间:August 2014
  • 年:2014
  • 卷:71
  • 期:15
  • 页码:2837-2863
  • 全文大小:4,463 KB
  • 参考文献:1. Battersby AR (2000) Tetrapyrroles: the pigments of life. Nat Prod Rep 17(6):507-26. doi:10.1039/b002635m
    2. Rudiger W (1997) Chlorophyll metabolism: from outer space down to the molecular level. Phytochemistry 46(7):1151-167. doi:10.1016/S0031-9422(97)00449-4
    3. Moulin M, Smith AG (2005) Regulation of tetrapyrrole biosynthesis in higher plants. Paper presented at the Conference on coenzymology: biochemistry of vitamin biogenesis and cofactor-containing enzymes. King Coll, Cambridge
    4. Lockhart PJ, Larkum AWD, Steel MA, Waddell PJ, Penny D (1996) Evolution of chlorophyll and bacteriochlorophyll: the problem of invariant sites in sequence analysis. Proc Natl Acad Sci USA 93(5):1930-934. doi:10.1073/pnas.93.5.1930
    5. Blankenship RE, Hartman H (1998) The origin and evolution of oxygenic photosynthesis. Trends Biochem Sci 23(3):94-7. doi:10.1016/S0968-0004(98)01186-4
    6. Friedmann HC, Thauer RK (1992) Macrocyclic tetrapyrrole biosynthesis in bacteria. Encyclopedia of microbiology, vol 1-4. Academic Press, New York, pp 1-9
    7. Thauer RK, Bonacker LG (1994) Biosynthesis of coenzyme F430, a nickel porphinoid involved in methanogenesis. In: Chadwick DJA (ed) Biosynthesis of the tetrapyrrole pigments, vol 180. CIBA Foundation Symposia, John Wiley & Sons Ltd, Chichester, pp 210-22 discussion 222-17
    8. Friedmann HC, Klein A, Thauer RK (1991) Biochemistry of coenzyme F430 a nickel porphinoid involved in methanogenesis. In: Jordan PME (ed) New comprehensive biochemistry, vol 19. Elsevier Science Publishers B.V, New York, pp 139-54
    9. O’Brian MR, Thony-Meyer L (2002) Biochemistry, regulation and genomics of haem biosynthesis in prokaryotes. Adv Microb Physiol 46:257-18. doi:10.1016/S0065-2911(02)46006-7
    10. Layer G, Reichelt J, Jahn D, Heinz DW (2010) Structure and function of enzymes in heme biosynthesis. Protein Sci 19(6):1137-161. doi:10.1002/pro.405
    11. Bernhardt R (2006) Cytochromes P450 as versatile biocatalysts. J Biotechnol 124(1):128-45. doi:10.1016/j.jbiotec.2006.01.026
    12. Sono M, Roach MP, Coulter ED, Dawson JH (1996) Heme-containing oxygenases. Chem Rev 96(7):2841-888. doi:10.1021/cr9500500
    13. Wilks A, Burkhard KA (2007) Heme and virulence: how bacterial pathogens regulate, transport and utilize heme. Nat Prod Rep 24(3):511-22. doi:10.1039/b604193k
    14. Zajicek RS, Bali S, Arnold S, Brindley AA, Warren MJ, Ferguson SJ (2009) / d 1 haem biogenesis: assessing the roles of three / nir gene products. FEBS J 276(21):6399-411. doi:10.1111/j.1742-4658.2009.07354.x
    15. Simon J, Kroneck PM (2013) Microbial sulfite respiration. Adv Microb Physiol 62:45-17. doi:10.1016/B978-0-12-410515-7.00002-0
    16. Wilks A (2002) Analysis of heme and hemoproteins. In: Alison G, Smith MW (eds) Heme, chlorophyll, and bilines. Humana Press, Totova, pp 157-84
    17. Sanders CTS, Onder O, Frawley ER, Kranz RG, Koch HG, Daldal F (2009) Biogenesis of / c-type cytochromes and cytochrome complexes. In: Hunter NCDF, Thurnauer MC, Beatty JT (eds) The purple phototrophic bacteria, vol 28. Springer Science + Business Media B.V, Netherlands, pp 407-23
    18. Kranz RG, Richard-Fogal C, Taylor JS, Frawley ER (2009) Cytochrome / c biogenesis: mechanisms for covalent modifications and trafficking of heme and for heme-iron redox control. Microbiol Mol Biol Rev 73(3):510-28. doi:10.1128/MMBR.00001-09 Table of Contents
    19. Hederstedt L (2012) Heme / a biosynthesis. Biochim Biophys Acta 1817(6):920-27. doi:10.1016/j.bbabio.2012.03.025
    20. Wandersman C, Delepelaire P (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611-47. doi:10.1146/annurev.micro.58.030603.123811
    21. DeRosa MC, Crutchley RJ (2002) Photosensitized singlet oxygen and its applications. Coordin Chem Rev 233:351-71. doi:10.1016/S0010-8545(02)00034-6
    22. Dougherty TJ (1987) Photosensitizers: therapy and detection of malignant tumors. Photochem Photobiol 45(6):879-89. doi:10.1111/j.1751-1097.1987.tb07898.x
    23. Demidova TN, Hamblin MR (2004) Photodynamic therapy targeted to pathogens. Int J Immunopathol Pharmacol 17(3):245-54
    24. Chang CK (1985) On the structure of heme- / d 1: an isobacteriochlorin derivative as the prosthetic group of dissimilatory nitrite reductase. J Biol Chem 260(17):9520-522
    25. Chang CK, Timkovich R, Wu W (1986) Evidence that heme / d 1 is a 1,3-porphyrindione. Biochemistry 25(26):8447-453. doi:10.1021/bi00374a019
    26. Chang CK, Wu W (1986) The porphinedione structure of heme- / d 1: synthesis and spectral properties of model compounds of the prosthetic group of dissimilatory nitrite reductase. J Biol Chem 261(19):8593-596
    27. Carlson CA, Ingraham JL (1983) Comparison of denitrification by / Pseudomonas stutzeri, / Pseudomonas / aeruginosa, and / Paracoccus / denitrificans. Appl Environ Microbiol 45(4):1247-253
    28. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61(4):533-16
    29. Jones WL, Schroeder ED, Wilderer PA (1990) Denitrification in a batch waste-water treatment system using sequestered organic-substances. Res J Water Pollut C 62(3):259-67
    30. Tavares P, Pereira AS, Moura JJG, Moura I (2006) Metalloenzymes of the denitrification pathway. J Inorg Biochem 100(12):2087-100. doi:10.1016/j.jinorgbio.2006.09.003
    31. Fulop V, Moir JWB, Ferguson SJ, Hajdu J (1995) The anatomy of a bifunctional enzyme: structural basis for reduction of oxygen to water and synthesis of nitric-oxide by cytochrome / cd 1. Cell 81(3):369-77. doi:10.1016/0092-8674(95)90390-9
    32. Pearson IV, Page MD, van Spanning RJM, Ferguson SJ (2003) A mutant of / Paracoccus denitrificans with disrupted genes coding for cytochrome / c 550 and pseudoazurin establishes these two proteins as the in vivo electron donors to cytochrome / cd 1 nitrite reductase. J Bacteriol 185(21):6308-315. doi:10.1128/jb.185.21.6308-6315.2003
    33. Allen JW, Ferguson SJ, Fül?p V (2011) Cytochrome / cd 1 nitrite reductase. Encyclop Inorgan Bioinorgan Chem. doi:10.1002/9781119951438.eibc0557
    34. Zajicek RS, Cartron ML, Ferguson SJ (2006) Probing the unusual oxidation/reduction behavior of / Paracoccus pantotrophus cytochrome / cd 1 nitrite reductase by replacing a switchable methionine heme iron ligand with histidine. Biochemistry 45(37):11208-1216. doi:10.1021/bi0604983
    35. Radoul M, Bykov D, Rinaldo S, Cutruzzola F, Neese F, Goldfarb D (2011) Dynamic hydrogen-bonding network in the distal pocket of the nitrosyl complex of / P. aeruginosa / cd 1 nitrite reductase. J Am Chem Soc 133(9):3043-055. doi:10.1021/ja109688w
    36. Shemin D, Rittenberg D (1946) The biological utilization of glycine for the synthesis of the protoporphyrin of hemoglobin. J Biol Chem 166(2):621-25
    37. Kikuchi G, Kumar A, Talmage P, Shemin D (1958) The enzymatic synthesis of delta-aminolevulinic acid. J Biol Chem 233(5):1214-219
    38. Beale SI, Castelfranco PA (1973) 14 C incorporation from exogenous compounds into––aminolevulinic acid by greening cucumber cotyledons. Biochem Biophys Res Commun 52(1):143-49. doi:10.1016/0006-291X(73)90966-2
    39. Jahn D, Heinz DW (2009) Biosynthesis of 5-aminolevulinic acid. In: Warren MJ, Smith AG (eds) Tetrapyrroles: birth, life, and death. Landes Bioscience, Austin. doi:10.1007/978-0-387-78518-9_2
    40. Weinstein JD, Beale SI (1983) Separate physiological roles and subcellular compartments for two tetrapyrrole biosynthetic pathways in / Euglena gracilis. J Biol Chem 258(11):6799-807
    41. Iida K, Mimura I, Kajiwara M (2002) Evaluation of two biosynthetic pathways to delta-aminolevulinic acid in / E. gracilis. Eur J Biochem 269(1):291-97. doi:10.1046/j.0014-2956.2001.02651.x
    42. Cavallaro G, Decaria L, Rosato A (2008) Genome-based analysis of heme biosynthesis and uptake in prokaryotic systems. J Proteome Res 7(11):4946-954. doi:10.1021/pr8004309
    43. Ishida T, Yu L, Akutsu H, Ozawa K, Kawanishi S, Seto A, Inubushi T, Sano S (1998) A primitive pathway of porphyrin biosynthesis and enzymology in / D. vulgaris. Proc Natl Acad Sci USA 95(9):4853-858. doi:10.1073/pnas.95.9.4853
    44. Bali S, Lawrence AD, Lobo SA, Saraiva LM, Golding BT, Palmer DJ, Howard MJ, Ferguson SJ, Warren MJ (2011) Molecular hijacking of siroheme for the synthesis of heme and / d 1 heme. Proc Natl Acad Sci USA 108(45):18260-8265. doi:10.1073/pnas.1108228108
    45. Muir HM, Neuberger A (1950) The biogenesis of porphyrins. 2. The origin of the methyne carbon atoms. Biochem J 47(1):97-04
    46. Ferreira GC, Gong J (1995) 5-aminolevulinate synthase and the first step of heme-biosynthesis. J Bioenerg Biomembr 27(2):151-59. doi:10.1007/Bf02110030
    47. Fanica-Gaignier M, Clement-Metral J (1973) 5-aminolevulinic-acid synthetase of / Rhodopseudomonas spheroides Y. kinetic mechanism and inhibition by ATP. Eur J Biochem 40(1):19-4. doi:10.1111/j.1432-1033.1973.tb03164.x
    48. Astner I, Schulze JO, van den Heuvel J, Jahn D, Schubert WD, Heinz DW (2005) Crystal structure of 5-aminolevulinate synthase, the first enzyme of heme biosynthesis, and its link to XLSA in humans. EMBO J 24(18):3166-177. doi:10.1038/sj.emboj.7600792
    49. Beale SI, Gough SP, Granick S (1975) Biosynthesis of delta-aminolevulinic acid from the intact carbon skeleton of glutamic acid in greening barley. Proc Natl Acad Sci USA 72(7):2719-723. doi:10.1073/pnas.72.7.2719
    50. Schon A, Krupp G, Gough S, Berry-Lowe S, Kannangara CG, Soll D (1986) The RNA required in the first step of chlorophyll biosynthesis is a chloroplast glutamate tRNA. Nature 322(6076):281-84. doi:10.1038/322281a0
    51. Moser J, Lorenz S, Hubschwerlen C, Rompf A, Jahn D (1999) / Methanopyrus kandleri glutamyl-tRNA reductase. J Biol Chem 274(43):30679-0685. doi:10.1074/jbc.274.43.30679
    52. Chen MW, Jahn D, O’Neill GP, Soll D (1990) Purification of the glutamyl-tRNA reductase from / Chlamydomonas reinhardtii involved in delta-aminolevulinic acid formation during chlorophyll biosynthesis. J Biol Chem 265(7):4058-063
    53. Hoober JK, Kahn A, Ash DE, Gough S, Kannangara CG (1988) Biosynthesis of delta-aminolevulinate in greening barley leaves. IX. Structure of the substrate, mode of gabaculine inhibition, and the catalytic mechanism of glutamate 1-semialdehyde aminotransferase. Carlsberg Res Commun 53(1):11-5. doi:10.1007/BF02908411
    54. Hennig M, Grimm B, Contestabile R, John RA, Jansonius JN (1997) Crystal structure of glutamate-1-semialdehyde aminomutase: an alpha2-dimeric vitamin B6-dependent enzyme with asymmetry in structure and active site reactivity. Proc Natl Acad Sci USA 94(10):4866-871. doi:10.1073/pnas.94.10.4866
    55. Moser J, Schubert WD, Beier V, Bringemeier I, Jahn D, Heinz DW (2001) V-shaped structure of glutamyl-tRNA reductase, the first enzyme of tRNA-dependent tetrapyrrole biosynthesis. EMBO J 20(23):6583-590. doi:10.1093/emboj/20.23.6583
    56. Schulze JO, Schubert WD, Moser J, Jahn D, Heinz DW (2006) Evolutionary relationship between initial enzymes of tetrapyrrole biosynthesis. J Mol Biol 358(5):1212-220. doi:10.1016/j.jmb.2006.02.064
    57. Luer C, Schauer S, Mobius K, Schulze J, Schubert WD, Heinz DW, Jahn D, Moser J (2005) Complex formation between glutamyl-tRNA reductase and glutamate-1-semialdehyde 2,1-aminomutase in / E. coli during the initial reactions of porphyrin biosynthesis. J Biol Chem 280(19):18568-8572. doi:10.1074/jbc.M500440200
    58. Nogaj LA, Beale SI (2005) Physical and kinetic interactions between glutamyl-tRNA reductase and glutamate-1-semialdehyde aminotransferase of / Chlamydomonas reinhardtii. J Biol Chem 280(26):24301-4307. doi:10.1074/jbc.M502483200
    59. Deery E, Schroeder S, Lawrence AD, Taylor SL, Seyedarabi A, Waterman J, Wilson KS, Brown D, Geeves MA, Howard MJ, Pickersgill RW, Warren MJ (2012) An enzyme-trap approach allows isolation of intermediates in cobalamin biosynthesis. Nat Chem Biol 8(11):933-40. doi:10.1038/nchembio.1086
    60. Gibson KD, Neuberger A, Scott JJ (1954) The enzymic conversion of delta-aminolaevulic acid to porphobilinogen. Biochem J 58(4):xli–xlii
    61. Bollivar DW, Clauson C, Lighthall R, Forbes S, Kokona B, Fairman R, Kundrat L, Jaffe EK (2004) / Rhodobacter capsulatus porphobilinogen synthase, a high activity metal ion independent hexamer. BMC Biochem 5:17. doi:10.1186/1471-2091-5-17
    62. Senior NM, Brocklehurst K, Cooper JB, Wood SP, Erskine P, Shoolingin-Jordan PM, Thomas PG, Warren MJ (1996) Comparative studies on the 5-aminolaevulinic acid dehydratases from / Pisum sativum, / E. coli and / S. cerevisiae. Biochem J 320(Pt 2):401-12
    63. Jaffe EK (2000) The porphobilinogen synthase family of metalloenzymes. Acta Crystallogr D Biol Crystallogr 56(Pt 2):115-28. doi:10.1107/S0907444999014894
    64. Shoolingin-Jordan PM, Spencer P, Sarwar M, Erskine PE, Cheung KM, Cooper JB, Norton EB (2002) 5-aminolaevulinic acid dehydratase: metals, mutants and mechanism. Paper presented at the Colloquium on Tetrapyrroles: Their Life, Birth and Death Heriot-Watt, Edinburgh
    65. Frankenberg N, Erskine PT, Cooper JB, Shoolingin-Jordan PM, Jahn D, Heinz DW (1999) High-resolution crystal structure of a Mg2+-dependent porphobilinogen synthase. J Mol Biol 289(3):591-02. doi:10.1006/jmbi.1999.2808
    66. Erskine PT, Newbold R, Brindley AA, Wood SP, Shoolingin-Jordan PM, Warren MJ, Cooper JB (2001) The X-ray structure of yeast 5-aminolaevulinic acid dehydratase complexed with substrate and three inhibitors. J Mol Biol 312(1):133-41. doi:10.1006/jmbi2001.4947
    67. Erskine PT, Norton E, Cooper JB, Lambert R, Coker A, Lewis G, Spencer P, Sarwar M, Wood SP, Warren MJ, Shoolingin-Jordan PM (1999) X-ray structure of 5-aminolaevulinic acid dehydratase from / E. coli complexed with the inhibitor levulinic acid at 2.0-A resolution. Biochemistry 38(14):4266-276. doi:10.1021/bi982137w
    68. Warren MJ, Jordan PM (1988) Investigation into the nature of substrate binding to the dipyrromethane cofactor of / E. coli porphobilinogen deaminase. Biochemistry 27(25):9020-030. doi:10.1021/bi00425a021
    69. Awan SJ, Siligardi G, Shoolingin-Jordan PM, Warren MJ (1997) Reconstitution of the holoenzyme form of / E. coli porphobilinogen deaminase from apoenzyme with porphobilinogen and pre-uroporphyrinogen: a study using circular dichroism spectroscopy. Biochemistry 36(30):9273-282. doi:10.1021/bi9702602
    70. Hart GJ, Miller AD, Leeper FJ, Battersby AR (1987) Biosynthesis of the natural porphyrins: proof that hydroxymethylbilane synthase (Porphobilinogen Deaminase) uses a novel binding group in its catalytic action. J Chem Soc Chem Comm 23:1762-764. doi:10.1039/C39870001762
    71. Warren MJ, Scott AI (1990) Tetrapyrrole assembly and modification into the ligands of biologically functional cofactors. Trends Biochem Sci 15(12):486-91. doi:10.1016/0968-0004(90)90304-T
    72. Louie GV, Brownlie PD, Lambert R, Cooper JB, Blundell TL, Wood SP, Warren MJ, Woodcock SC, Jordan PM (1992) Structure of porphobilinogen deaminase reveals a flexible multidomain polymerase with a single catalytic site. Nature 359(6390):33-9. doi:10.1038/359033a0
    73. Shoolingin-Jordan PM (1995) Porphobilinogen deaminase and uroporphyrinogen III synthase: structure, molecular biology, and mechanism. J Bioenerg Biomembr 27(2):181-95. doi:10.1007/BF02110033
    74. Burton G, Fagerness PE, Hosozawa S, Jordan PM, Scott AI (1979) 13C NMR evidence for a new intermediate, pre-uroporphyrinogen, in the enzymic transformation of porphobilinogen into uroporphyrinogens I and III. J Chem Soc Chem Comm 5:202. doi:10.1039/c39790000202
    75. Timkovich R, Burkhalter RS, Xavier AV, Chen L, Legall J (1994) Iron uroporphyrin-I and a heme / c-derivative are prosthetic groups in / D. gigas rubredoxin oxidase. Bioorg Chem 22(3):284-93. doi:10.1006/bioo1994.1022
    76. Schubert HL, Raux E, Matthews MAA, Phillips JD, Wilson KS, Hill CP, Warren MJ (2002) Structural diversity in metal ion chelation and the structure of uroporphyrinogen III synthase. In: Colloquium on tetrapyrroles: their life, birth and death, Heriot-Watt, Edinburgh, pp 595-00
    77. Luo J, Lim CK (1993) Order of uroporphyrinogen III decarboxylation on incubation of porphobilinogen and uroporphyrinogen III with erythrocyte uroporphyrinogen decarboxylase. Biochem J 289(Pt 2):529-32
    78. Dailey HA (2002) Terminal steps of haem biosynthesis. Biochem Soc Trans 4:590-95
    79. Whitby FG (1998) Crystal structure of human uroporphyrinogen decarboxylase. EMBO J 17(9):2463-471. doi:10.1093/emboj/17.9.2463
    80. Phillips JD, Warby CA, Whitby FG, Kushner JP, Hill CP (2009) Substrate shuttling between active sites of uroporphyrinogen decarboxylase is not required to generate coproporphyrinogen. J Mol Biol 389(2):306-14. doi:10.1016/j.jmb.2009.04.013
    81. Medlock AE, Dailey HA (1996) Human coproporphyrinogen oxidase is not a metalloprotein. J Biol Chem 271(51):32507-2510
    82. Cavaleiro JA, Kenner GW, Smith KM (1974) Pyrroles and related compounds. XXXII. Biosynthesis of protoporphyrin-IX from coproporphyrinogen-III. J Chem Soc Perkin 110:1188-194. doi:10.1039/P19740001188
    83. Elder GH, Evans JO, Jackson JR, Jackson AH (1978) Factors determining sequence of oxidative decarboxylation of 2-propionate and 4-propionate substituents of coproporphyrinogen-Iii by coproporphyrinogen oxidase in rat-liver. Biochem J 169(1):215-23
    84. Jackson AH, Jones DM, Philip G, Lash TD, Batlle AM, Smith SG (1980) Synthetic and biosynthetic studies of porphyrins, Part IV. Further studies of the conversion of corporporhyrinogen-III to protoporphyrin-IX: mass spectrometric investigations of the incubation of specifically deuteriated corporporhyringen-III with chicken red cell haemolysates. Int J Biochem 12(5-):681-88. doi:10.1016/0020-711X(80)90144-5
    85. Phillips JD, Whitby FG, Warby CA, Labbe P, Yang C, Pflugrath JW, Ferrara JD, Robinson H, Kushner JP, Hill CP (2004) Crystal structure of the oxygen-dependant coproporphyrinogen oxidase (Hem13p) of / S. cerevisiae. J Biol Chem 279(37):38960-8968. doi:10.1074/jbc.M406050200
    86. Lee DS, Flachsova E, Bodnarova M, Demeler B, Martasek P, Raman CS (2005) Structural basis of hereditary coproporphyria. Natl Acad Sci USA 102(40):14232-4237. doi:10.1073/pnas.0506557102
    87. Stephenson JR, Stacey JA, Morgenthaler JB, Friesen JA, Lash TD, Jones MA (2007) Role of aspartate 400, arginine 262, and arginine 401 in the catalytic mechanism of human coproporphyrinogen oxidase. Protein Sci 16(3):401-10. doi:10.1110/ps.062636907
    88. Silva PJ, Ramos MJ (2008) A comparative density-functional study of the reaction mechanism of the O2-dependent coproporphyrinogen III oxidase. Bioorg Med Chem Lett 16(6):2726-733. doi:10.1016/j.bmc.2008.01.008
    89. Lash TD (2005) The enigma of coproporphyrinogen oxidase: how does this unusual enzyme carry out oxidative decarboxylations to afford vinyl groups? Bioorg Med Chem Lett 15(20):4506-509. doi:10.1016/j.bmcl.2005.07.010
    90. Layer G, Grage K, Teschner T, Schunemann V, Breckau D, Masoumi A, Jahn M, Heathcote P, Trautwein AX, Jahn D (2005) Radical / S-adenosylmethionine enzyme coproporphyrinogen III oxidase HemN: functional features of the [4Fe-S] cluster and the two bound / S-adenosyl-l -methionines. J Biol Chem 280(32):29038-9046. doi:10.1074/jbc.M501275200
    91. Atta M, Mulliez E, Arragain S, Forouhar F, Hunt JF, Fontecave M (2010) / S-Adenosylmethionine-dependent radical-based modification of biological macromolecules. Curr Opin Struc Biol 20(6):684-92. doi:10.1016/j.sbi.2010.09.009
    92. Booker SJ (2009) Anaerobic functionalization of unactivated C–H bonds. Curr Opin Chem Biol 13(1):58-3. doi:10.1016/j.cbpa.2009.02.036
    93. Layer G, Heinz DW, Jahn D, Schubert WD (2004) Structure and function of radical SAM enzymes. Curr Opin Chem Biol 8(5):468-76. doi:10.1016/j.cbpa.2004.08.001
    94. Layer G, Pierik AJ, Trost M, Rigby SE, Leech HK, Grage K, Breckau D, Astner I, Jansch L, Heathcote P, Warren MJ, Heinz DW, Jahn D (2006) The substrate radical of / E. coli oxygen-independent coproporphyrinogen III oxidase HemN. J Biol Chem 281(23):15727-5734. doi:10.1074/jbc.M512628200
    95. Abicht HK, Martinez J, Layer G, Jahn D, Solioz M (2012) / Lactococcus lactis HemW (HemN) is a haem-binding protein with a putative role in haem trafficking. Biochem J 442(2):335-43. doi:10.1042/BJ20111618
    96. Dailey HA, Dailey TA (1996) Protoporphyrinogen oxidase of / Myxococcus xanthus. Expression, purification, and characterization of the cloned enzyme. J Biol Chem 271(15):8714-718
    97. Sasarman A, Letowski J, Czaika G, Ramirez V, Nead MA, Jacobs JM, Morais R (1993) Nucleotide-sequence of the / hemG gene involved in the protoporphyrinogen oxidase activity of / E. coli K12. Can J Microbiol 39(12):1155-161
    98. Boynton TO, Gerdes S, Craven SH, Neidle EL, Phillips JD, Dailey HA (2011) Discovery of a gene involved in a third bacterial protoporphyrinogen oxidase activity through comparative genomic analysis and functional complementation. Appl Environ Microbiol 77(14):4795-801. doi:10.1128/AEM.00171-11
    99. Dailey TA, Dailey HA (1997) Expression, purification, and characteristics of mammalian protoporphyrinogen oxidase. In: McCormick D, Suttie J, Wagner C (eds.) Methods in?Enzymology, vol 281. pp 340-49
    100. Hansson M, Hederstedt L (1994) / Bacillus subtilis HemY is a peripheral membrane-protein essential for protoheme-IX synthesis which can oxidize coproporphyrinogen-III and protoporphyrinogen-IX. J Bacteriol 176(19):5962-970
    101. Dailey TA, Meissner P, Dailey HA (1994) Expression of a cloned protoporphyrinogen oxidase. J Biol Chem 269(2):813-15
    102. Koch M, Breithaupt C, Kiefersauer R, Freigang J, Huber R, Messerschmidt A (2004) Crystal structure of protoporphyrinogen IX oxidase: a key enzyme in haem and chlorophyll biosynthesis. EMBO J 23(8):1720-728. doi:10.1038/sj.emboj.7600189
    103. Corradi HR, Corrigall AV, Boix E, Mohan CG, Sturrock ED, Meissner PN, Acharya KR (2006) Crystal structure of protoporphyrinogen oxidase from / Myxococcus xanthus and its complex with the inhibitor acifluorfen. J Biol Chem 281(50):38625-8633. doi:10.1074/jbc.M606640200
    104. Heinemann IU, Diekmann N, Masoumi A, Koch M, Messerschmidt A, Jahn M, Jahn D (2007) Functional definition of the tobacco protoporphyrinogen IX oxidase substrate-binding site. Biochem J 402(3):575-80. doi:10.1042/BJ20061321
    105. Boynton TO, Daugherty LE, Dailey TA, Dailey HA (2009) Identification of / E. coli HemG as a novel, menadione-dependent flavodoxin with protoporphyrinogen oxidase activity. Biochemistry 48(29):6705-711. doi:10.1021/Bi900850y
    106. Mobius K, Arias-Cartin R, Breckau D, Hannig AL, Riedmann K, Biedendieck R, Schroder S, Becher D, Magalon A, Moser J, Jahn M, Jahn D (2010) Heme biosynthesis is coupled to electron transport chains for energy generation. Proc Natl Acad Sci USA 107(23):10436-0441. doi:10.1073/pnas.1000956107
    107. Kato K, Tanaka R, Sano S, Tanaka A, Hosaka H (2010) Identification of a gene essential for protoporphyrinogen IX oxidase activity in the cyanobacterium / Synechocystis sp. PCC6803. Proc Natl Acad Sci USA 107(38):16649-6654. doi:10.1073/pnas.1000771107
    108. Dailey HA, Dailey TA, Wu CK, Medlock AE, Wang KF, Rose JP, Wang BC (2000) Ferrochelatase at the millennium: structures, mechanisms and [2Fe-S] clusters. Cell Mol Life Sci 57(13-4):1909-926. doi:10.1007/PL00000672
    109. Corrigall AV, Siziba KB, Maneli MH, Shephard EG, Ziman M, Dailey TA, Dailey HA, Kirsch RE, Meissner PN (1998) Purification of and kinetic studies on a cloned protoporphyrinogen oxidase from the aerobic bacterium / B. subtilis. Arch Biochem Biophys 358(2):251-56. doi:10.1006/abbi1998.0834
    110. Hansson M, Hederstedt L (1994) Purification and characterisation of a water-soluble ferrochelatase from / B. subtilis. Eur J Biochem 220(1):201-08. doi:10.1111/j.1432-1033.1994.tb18615.x
    111. Romao CV, Ladakis D, Lobo SA, Carrondo MA, Brindley AA, Deery E, Matias PM, Pickersgill RW, Saraiva LM, Warren MJ (2011) Evolution in a family of chelatases facilitated by the introduction of active site asymmetry and protein oligomerization. Proc Natl Acad Sci USA 108(1):97-02. doi:10.1073/pnas.1014298108
    112. Dailey TA, Boynton TO, Albetel AN, Gerdes S, Johnson MK, Dailey HA (2010) Discovery and characterization of HemQ: an essential heme biosynthetic pathway component. J Biol Chem 285(34):25978-5986. doi:10.1074/jbc.M110.142604
    113. Raux E, Leech HK, Beck R, Schubert HL, Santander PJ, Roessner CA, Scott AI, Martens JH, Jahn D, Thermes C, Rambach A, Warren MJ (2003) Identification and functional analysis of enzymes required for precorrin-2 dehydrogenation and metal ion insertion in the biosynthesis of sirohaem and cobalamin in / Bacillus megaterium. Biochem J 370(2):505-16. doi:10.1042/BJ20021443
    114. Raux E, McVeigh T, Peters SE, Leustek T, Warren MJ (1999) The role of / S. cerevisiae Met1p and Met8p in sirohaem and cobalamin biosynthesis. Biochem J 338:701-08. doi:10.1042/0264-6021:3380701
    115. Warren MJ, Bolt EL, Roessner CA, Scott AI, Spencer JB, Woodcock SC (1994) Gene dissection demonstrates that the / E. coli cysG gene encodes a multifunctional protein. Biochem J 302(Pt 3):837-44
    116. Warren MJ, Raux E, Schubert HL, Escalante-Semerena JC (2002) The biosynthesis of adenosylcobalamin (vitamin B12). Nat Prod Rep 19(4):390-12. doi:10.1069/b108967f
    117. Platt MD, Schurr MJ, Sauer K, Vazquez G, Kukavica-Ibrulj I, Potvin E, Levesque RC, Fedynak A, Brinkman FS, Schurr J, Hwang SH, Lau GW, Limbach PA, Rowe JJ, Lieberman MA, Barraud N, Webb J, Kjelleberg S, Hunt DF, Hassett DJ (2008) Proteomic, microarray, and signature-tagged mutagenesis analyses of anaerobic / P. aeruginosa at pH 6.5, likely representing chronic, late-stage cystic fibrosis airway conditions. J Bacteriol 190(8):2739-758. doi:10.1128/JB.01683-07
    118. Storbeck S, Rolfes S, Raux-Deery E, Warren MJ, Jahn D, Layer G (2010) A novel pathway for the biosynthesis of heme in ?: genome-based bioinformatic predictions and experimental evidence. Archaea 2010:175050. doi:10.1155/2010/175050
    119. Brindley AA, Raux E, Leech HK, Schubert HL, Warren MJ (2003) A story of chelatase evolution: identification and characterization of a small 13-5-kDa “ancestral-cobaltochelatase (CbiXS) in the archaea. J Biol Chem 278(25):22388-2395. doi:10.1074/jbc.M302468200
    120. Lobo SA, Brindley A, Warren MJ, Saraiva LM (2009) Functional characterization of the early steps of tetrapyrrole biosynthesis and modification in / D. vulgaris Hildenborough. Biochem J 420(2):317-25. doi:10.1042/BJ20090151
    121. Lobo SAL, Brindley AA, Romao CV, Leech HK, Warren MJ, Saraiva LM (2008) Two distinct roles for two functional cobaltochelatases (CbiK) in / D. vulgaris Hildenborough. Biochemistry 47(21):5851-857. doi:10.1021/Bi800342c
    122. Lobo SAL, Warren MJ, Saraiva LM (2012) Chapter seven––sulfate-reducing bacteria reveal a new branch of tetrapyrrole metabolism. In: Robert KP (ed) Advance microbiol physiology, vol 61. Amsterdam, Netherlands, pp 267-95. doi:10.1016/B978-0-12-394423-8.00007-X
    123. Tripathy BC, Sherameti I, Oelmuller R (2010) Siroheme: an essential component for life on earth. Plant Sign Behav 5(1):14-0
    124. Yapbondoc F, Bondoc LL, Timkovich R, Baker DC, Hebbler A (1990) C-methylation occurs during the biosynthesis of heme / d 1. J Biol Chem 265(23):13498-3500
    125. Bali S, Warren MJ, Ferguson SJ (2010) NirF is a periplasmic protein that binds / d 1 heme as part of its essential role in / d 1 heme biogenesis. FEBS J 277(23):4944-955. doi:10.1111/j.1742-4658.2010.07899.x
    126. Suzuki M, Hirai T, Arai H, Ishii M, Igarashi Y (2006) Purification, characterization, and gene cloning of thermophilic cytochrome / cd 1 nitrite reductase from / Hydrogenobacter thermophilus TK-6. J Biosci Bioeng 101(5):391-97. doi:10.1263/jbb.101.391
    127. Palmedo G, Seither P, Korner H, Matthews JC, Burkhalter RS, Timkovich R, Zumft WG (1995) Resolution of the / nirD locus for heme / d 1 synthesis of cytochrome / cd 1 (respiratory nitrite reductase) from / Pseudomonas stutzeri. Eur J Biochem 232(3):737-46. doi:10.1111/j.1432-1033.1995.tb20868.x
    128. Glockner AB, Zumft WG (1996) Sequence analysis of an internal 9.72-kb segment from the 30-kb denitrification gene cluster of / Pseudomonas stutzeri. Biochimica Et Biophysica Acta-Bioenergetics 1277((1-2)):6-2. doi:10.1016/s0005-2728(96)00108-9
    129. Kawasaki S, Arai H, Kodama T, Igarashi Y (1997) Gene cluster for dissimilatory nitrite reductase ( / nir) from / P. aeruginosa: sequencing and identification of a locus for heme / d 1 biosynthesis. J Bacteriol 179(1):235-42
    130. Silvestrini MC, Cutruzzola F, D’Alessandro R, Brunori M, Fochesato N, Zennaro E (1992) Expression of / P. aeruginosa nitrite reductase in / P. putida and characterization of the recombinant protein. Biochem J 285(Pt 2):661-66
    131. Deboer APN, Reijnders WNM, Kuenen JG, Stouthamer AH, Vanspanning RJM (1994) Isolation, sequencing and mutational analysis of a gene-cluster involved in nitrite reduction in / Paracoccus denitrificans. Anton Leeuw Int J G 66(1-):111-27
    132. Ohshima T, Sugiyama M, Uozumi N, Iijima S, Kobayashi T (1993) Cloning and sequencing of a gene encoding nitrite reductase from / Paracoccus / denitrificans and expression of the gene in / E. / coli. J Ferment Bioeng 76(2):82-8. doi:10.1016/0922-338x(93)90061-c
    133. Warren MJ, Smith AG, Deery E, Rose RS (2009) Biosynthesis of Siroheme and Coenzyme F430. In: Tetrapyrroles: birth, life and death. Molecular biology intelligence unit. Springer, Berlin Heidelberg New York, pp 344-51, doi: 10.1007/978-0-387-78518-9_22
    134. Storbeck S, Walther J, Mueller J, Parmar V, Schiebel HM, Kemken D, Duelcks T, Warren MJ, Layer G (2009) The / P. aeruginosa nirE gene encodes the / S-adenosyl-l -methionine-dependent uroporphyrinogen III methyltransferase required for heme / d 1 biosynthesis. FEBS J 276(20):5973-982. doi:10.1111/j.1742-4658.2009.07306.x
    135. Stroupe ME, Leech HK, Daniels DS, Warren MJ, Getzoff ED (2003) CysG structure reveals tetrapyrrole-binding features and novel regulation of siroheme biosynthesis. Nat Struct Biol 10(12):1064-073. doi:10.1038/nsb1007
    136. Hasegawa N, Arai H, Igarashi Y (2001) Two / c-type cytochromes, NirM and NirC, encoded in the / nir gene cluster of / P. aeruginosa act as electron donors for nitrite reductase. Biochem Biophys Res Commun 288(5):1223-230. doi:10.1006/bbrc2001.5919
    137. Nicke T, Schnitzer T, Munch K, Adamczack J, Haufschildt K, Buchmeier S, Kucklick M, Felgentrager U, Jansch L, Riedel K, Layer G (2013) Maturation of the cytochrome / cd 1 nitrite reductase NirS from / P. aeruginosa requires transient interactions between the three proteins NirS. Biosci Rep NirN NirF. doi:10.1042/BSR20130043
    138. Rossmann MG, Moras D, Olsen KW (1974) Chemical and biological evolution of a nucleotide-binding protein. Nature 250(5463):194-99. doi:10.1038/250194a0
    139. Bali S, Ferguson SJ (2011) Assembly of respiratory proteins of the nitrogen cycle In: Moir JWB (ed) Nitrogen cycling in bacteria: molecular analysis, pp 163-75
    140. Heikkila MP, Honisch U, Wunsch P, Zumft WG (2001) Role of the tat transport system in nitrous oxide reductase translocation and cytochrome / cd 1 biosynthesis in / Pseudomonas stutzeri. J Bacteriol 183(5):1663-671. doi:10.1128/jb.183.5.1663-1671.2001
    141. Brinkman AB, Ettema TJ, de Vos WM, van der Oost J (2003) The Lrp family of transcriptional regulators. Mol Microbiol 48(2):287-94. doi:10.1046/j.1365-2958.2003.03442.x
    142. Xiong J, Bauer CE, Pancholy A (2007) Insight into the haem / d 1 biosynthesis pathway in heliobacteria through bioinformatics analysis. Microbiol Sgm 153:3548-562. doi:10.1099/mic.0.2007/007930-0
    143. Sofia HJ, Chen G, Hetzler BG, Reyes-Spindola JF, Miller NE (2001) Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucl Acids Res 29(5):1097-106. doi:10.1093/nar/29.5.1097
    144. Frey PA, Hegeman AD, Ruzicka FJ (2008) The radical SAM superfamily. Crit Rev Biochem Mol 43(1):63-8. doi:10.1080/10409230701829169
    145. Brindley AA, Zajicek R, Warren MJ, Ferguson SJ, Rigby SE (2010) NirJ, a radical SAM family member of the / d 1 heme biogenesis cluster. FEBS Lett 584(11):2461-466. doi:10.1016/j.febslet.2010.04.053
    146. Hanzelmann P, Schindelin H (2004) Crystal structure of the / S-adenosylmethionine-dependent enzyme MoaA and its implications for molybdenum cofactor deficiency in humans. Proc Natl Acad Sci USA 101(35):12870-2875. doi:10.1073/pnas.0404624101
    147. Hanzelmann P, Hernandez HL, Menzel C, Garcia-Serres R, Huynh BH, Johnson MK, Mendel RR, Schindelin H (2004) Characterization of MOCS1A, an oxygen-sensitive iron–sulfur protein involved in human molybdenum cofactor biosynthesis. J Biol Chem 279(33):34721-4732. doi:10.1074/jbc.M313398200
    148. Fluhe L, Knappe TA, Gattner MJ, Schafer A, Burghaus O, Linne U, Marahiel MA (2012) The radical SAM enzyme AlbA catalyzes thioether bond formation in subtilosin A. Nat Chem Biol 8(4):350-57. doi:10.1038/nchembio.798
    149. Yokoyama K, Numakura M, Kudo F, Ohmori D, Eguchi T (2007) Characterization and mechanistic study of a radical SAM dehydrogenase in the biosynthesis of butirosin. J Am Chem Soc 129(49):15147-5155. doi:10.1021/ja072481t
    150. Benjdia A, Subramanian S, Leprince J, Vaudry H, Johnson MK, Berteau O (2008) Anaerobic sulfatase-maturating enzymes, first dual substrate radical / S-adenosylmethionine enzymes. J Biol Chem 283(26):17815-7826. doi:10.1074/jbc.M710074200
    151. Grove TL, Ahlum JH, Sharma P, Krebs C, Booker SJ (2010) A consensus mechanism for radical SAM-dependent dehydrogenation? BtrN contains two 4Fe-S clusters. Biochemistry 49(18):3783-785. doi:10.1021/bi9022126
    152. Grove TL, Lee K-H, St. Clair J, Krebs C, Booker C (2008) In vitro characterization of AtsB, a radical SAM formylglycine-generating enzyme that contains three 4Fe-4S clusters. Biochemistry 47(28):7523-538. doi:10.1021/bi8004297
    153. Akutsu H, Park JS, Sano S (1993) l -methionine methyl is specifically incorporated into the C-2 and C-7 positions of the porphyrin of cytochrome- / c3 in a strictly anaerobic bacterium, / D. vulgaris. J Am Chem Soc 115(25):12185-2186. doi:10.1021/Ja00078a075
    154. Scott AI (1990) Mechanistic and evolutionary aspects of vitamin-B12 biosynthesis. Acc Chem Res 23(9):308-17. doi:10.1021/Ar00177a007
    155. Panek H, O’Brian MR (2002) A whole genome view of prokaryotic haem biosynthesis. Microbiol Sgm 148:2273-282
    156. Buchenau B, Kahnt J, Heinemann IU, Jahn D, Thauer RK (2006) Heme biosynthesis in / Methanosarcina barkeri via a pathway involving two methylation reactions. J Biol Chem 188(24):8666-668. doi:10.1128/Jb.01349-06
    157. Susanti D, Mukhopadhyay B (2012) An intertwined evolutionary history of methanogenic archaea and sulfate reduction. Plos One. doi:10.1371/journal.pone.0045313
    158. Layer G, Moser J, Heinz DW, Jahn D, Schubert WD (2003) Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of Radical SAM enzymes. EMBO J 22(23):6214-224. doi:10.1093/emboj/cdg598
    159. Romao CV, Louro R, Timkovich R, Lubben M, Liu MY, LeGall J, Xavier AV, Teixeira M (2000) Iron-coproporphyrin III is a natural cofactor in bacterioferritin from the anaerobic bacterium / Desulfovibrio desulfuricans. FEBS Lett 480(2-):213-16. doi:10.1016/S0014-5793(00)01939-6
    160. Oglesby-Sherrouse AG, Vasil ML (2010) Characterization of a heme-regulated non-coding RNA encoded by the / prrF locus of / P. aeruginosa. PLoS ONE 5(4):e9930. doi:10.1371/journal.pone.0009930
    161. Benner SA, Ellington AD, Tauer A (1989) Modern metabolism as a palimpsest of the RNA world. Proc Natl Acad Sci USA 86(18):7054-058. doi:10.1073/pnas.86.18.7054
    162. Dickman SR (1977) Ribonucleotide reduction and possible role of cobalamin in evolution. J Mol Evol 10(3):251-60. doi:10.1007/bf01764600
    163. Banerjee R, Ragsdale SW (2003) The many faces of vitamin B12: catalysis by cobalamin-dependent enzymes. Annu Rev Biochem 72:209-47. doi:10.1146/annurev.biochem.72.121801.161828
    164. Frey PA, Magnusson OT (2003) / S-Adenosylmethionine: a wolf in sheep’s clothing, or a rich man’s adenosylcobalamin? Chem Rev 103(6):2129-148. doi:10.1021/cr020422m
    165. Nicolet Y, Drennan CL (2004) AdoMet radical proteins: from structure to evolution––alignment of divergent protein sequences reveals strong secondary structure element conservation. Nucl Acids Res 32(13):4015-025. doi:10.1093/nar/gkh728
    166. Gough SP, Petersen BO, Duus JO (2000) Anaerobic chlorophyll isocyclic ring formation in / Rhodobacter capsulatus requires a cobalamin cofactor. Proc Natl Acad Sci USA 97(12):6908-913. doi:10.1073/pnas.97.12.6908
    167. Holliday GL, Thornton JM, Marquet A, Smith AG, Rebeille F, Mendel R, Schubert HL, Lawrence AD, Warren MJ (2007) Evolution of enzymes and pathways for the biosynthesis of cofactors. Nat Prod Rep 24(5):972-87. doi:10.1039/b703107f
    168. Ferguson SJ (2011) Remarkable diversity in biosynthesis of / c-type cytochromes in eukaryotes and prokaryotes. FEBS J 278(22):4169. doi:10.1111/j.1742-4658.2011.08378.x
    169. Ducluzeau AL, van Lis R, Duval S, Schoepp-Cothenet B, Russell MJ, Nitschke W (2009) Was nitric oxide the first deep electron sink? Trends Biochem Sci 34(1):9-5. doi:10.1016/j.tibs.2008.10.005
    170. Crane BR, Getzoff ED (1996) The relationship between structure and function for the sulfite reductases. Curr Opin Struc Biol 6(6):744-56. doi:10.1016/s0959-440x(96)80003-0
    171. Lubben M, Morand K (1994) Novel prenylated hemes as cofactors of cytochrome oxidases: archaea have modified heme / a and heme / o. J Biol Chem 269(34):21473-1479
  • 作者单位:Shilpa Bali (2)
    David J. Palmer (1)
    Susanne Schroeder (1)
    Stuart J. Ferguson (2)
    Martin J. Warren (1)

    2. Department of Biochemistry, University of Oxford, South Parks Road, Oxford, OX1 3QU, UK
    1. School of Biosciences, University of Kent, Kent, Canterbury, CT2 7NZ, UK
  • ISSN:1420-9071
文摘
Hemes (a, b, c, and o) and heme d 1 belong to the group of modified tetrapyrroles, which also includes chlorophylls, cobalamins, coenzyme F430, and siroheme. These compounds are found throughout all domains of life and are involved in a variety of essential biological processes ranging from photosynthesis to methanogenesis. The biosynthesis of heme b has been well studied in many organisms, but in sulfate-reducing bacteria and archaea, the pathway has remained a mystery, as many of the enzymes involved in these characterized steps are absent. The heme pathway in most organisms proceeds from the cyclic precursor of all modified tetrapyrroles uroporphyrinogen III, to coproporphyrinogen III, which is followed by oxidation of the ring and finally iron insertion. Sulfate-reducing bacteria and some archaea lack the genetic information necessary to convert uroporphyrinogen III to heme along the “classical-route and instead use an “alternative-pathway. Biosynthesis of the isobacteriochlorin heme d 1, a cofactor of the dissimilatory nitrite reductase cytochrome cd 1, has also been a subject of much research, although the biosynthetic pathway and its intermediates have evaded discovery for quite some time. This review focuses on the recent advances in the understanding of these two pathways and their surprisingly close relationship via the unlikely intermediate siroheme, which is also a cofactor of sulfite and nitrite reductases in many organisms. The evolutionary questions raised by this discovery will also be discussed along with the potential regulation required by organisms with overlapping tetrapyrrole biosynthesis pathways.

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