Heme biosynthesis and its regulation: Towards understanding and improvement of heme biosynthesis in filamentous fungi

Applied Microbiology and Biotechnology

Volumn 91, Issue 3, 2011, Pages 447-460

  Franken, Angelique C W ^a,d   Lokman, B Christien ^b   Ram, Arthur F J ^a,d   Punt, Peter J ^a,c   Van Den Hondel, Cees A M J J ^a,b,d   De Weert, Sandra ^a,d  

^a KLUYVER CENTRE FOR GENOMICS OF INDUSTRIAL FERMENTATION   (Netherlands)

^b HAN Biocentre   (Netherlands)

^c TNO   (Netherlands)

^d LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Aspergillus; Heme biosynthesis; Heme regulation; Intracellular heme; Peroxidase; Protein production

Indexed keywords

HEME BIOSYNTHESIS; HEME REGULATION; INTRACELLULAR HEME; PEROXIDASE; PROTEIN PRODUCTION;

ASPERGILLUS; BIOCHEMISTRY; BIOSYNTHESIS; PROTEINS;

PORPHYRINS;

5 AMINOLEVULINATE SYNTHASE; COPROPORPHYRINOGEN OXIDASE; FERROCHELATASE; HEME; HYDROLYASE; IRON; OXYGEN; PEROXIDASE; PORPHOBILINOGEN DEAMINASE; PORPHYRIN; PROTOPORPHYRINOGEN OXIDASE; UROPORPHYRINOGEN III SYNTHASE;

ENZYME ACTIVITY; EUKARYOTE; FUNGUS; HYDROPHOBICITY; LIMITING FACTOR; LITERATURE REVIEW; PROTEIN;

ASPERGILLUS; BASIDIOMYCETES; BIOSYNTHESIS; EUKARYOTE; FUNGAL STRAIN; FUNGUS; GENOME; NEGATIVE FEEDBACK; NONHUMAN; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW;

ASPERGILLUS NIGER; COENZYMES; FUNGI; HEME; PEROXIDASES;

ASPERGILLUS; ASPERGILLUS NIGER; ASPERGILLUS SP.; BASIDIOMYCOTA; EUKARYOTA; FUNGI;

EID: 79960715085     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-011-3391-3     Document Type: Review

References (99)

1. CM Bien PJ Espenshade 2010 Sterol regulatory element binding proteins in fungi: hypoxic transcription factors linked to pathogenesis Eukaryot Cell 9 3 352 359 10.1128/EC.00358-09 1:CAS:528:DC%2BC3cXjs1ersb4%3D
2. M Blanco M Becerra MI González-Siso ME Cerdán 2005 Functional characterization of KlHEM13, a hypoxic gene of Kluyveromyces lactis Can J Microbiol 51 3 241 249 10.1139/w04-133 1:CAS:528:DC%2BD2MXlvFCrsr8%3D (Pubitemid 41039389)
3. Braaksma M, Punt PJ (2008) Aspergillus as a cell factory for protein production: controlling protease activity in fungal production. In: Goldman GH, Osmani SA (eds) The Aspergilli: genomics, medical aspects, biotechnology, and research methods. CRC, Boca Raton, pp 441-455
4. RE Bradshaw SW Dixon DC Raitt TM Pillar 1993 Isolation and nucleotide sequence of the 5-aminolevulinate synthase gene from Aspergillus nidulans Curr Genet 23 5-6 501 507 10.1007/BF00312642 1:CAS:528:DyaK3sXmtFyltLc%3D (Pubitemid 23197035)
5. J-M Camadro P Labbe 1996 Cloning and characterization of the yeast HEM14 gene coding for protoporphyrinogen oxidase, the molecular target of diphenyl ether-type herbicides J Biol Chem 271 15 9120 9128 10.1074/jbc.271.15.9120 1:CAS:528:DyaK28Xitlenur8%3D (Pubitemid 26123346)
6. SR Chandrika G Padmanaban 1980 Purification, properties and synthesis of δ-aminolaevulinate dehydratase from Neurospora crassa Biochem J 191 1 29 36 1:CAS:528:DyaL3MXktlSktg%3D%3D
7. YC Chang CM Bien H Lee PJ Espenshade KJ Kwon-Chung 2007 Sre1p, a regulator of oxygen sensing and sterol homeostasis, is required for virulence in Cryptococcus neoformans Mol Microbiol 64 3 614 629 10.1111/j.1365-2958.2007. 05676.x 1:CAS:528:DC%2BD2sXlsV2kur4%3D (Pubitemid 46653205)
8. YC Chang SS Ingavale C Bien P Espenshade KJ Kwon-Chung 2009 Conservation of the sterol regulatory element-binding protein pathway and its pathobiological importance in Cryptococcus neoformans Eukaryot Cell 8 11 1770 1779 10.1128/EC.00207-09 1:CAS:528:DC%2BD1MXhsFSku73E
9. MG Claros P Vincens 1996 Computational method to predict mitochondrially imported proteins and their targeting sequences Eur J Biochem 241 3 779 786 10.1111/j.1432-1033.1996.00779.x 1:CAS:528:DyaK28XmvFCjurw%3D (Pubitemid 26379380)
10. A Conesa CAMJJ van den Hondel PJ Punt 2000 Studies on the production of fungal peroxidases in Aspergillus niger Appl Environ Microbiol 66 7 3016 3023 10.1128/AEM.66.7.3016-3023.2000 1:CAS:528:DC%2BD3cXkslKlt70%3D (Pubitemid 30497612)
11. HA Dailey 2002 Terminal steps of haem biosynthesis Biochem Soc Trans 30 4 590 595 10.1042/BST0300590 1:CAS:528:DC%2BD38XntVenur0%3D (Pubitemid 35001605)
12. TA Dailey HA Dailey 1998 Identification of an FAD superfamily containing protoporphyrinogen oxidases, monoamine oxidases, and phytoene desaturase. Expression and characterization of phytoene desaturase of Myxococcus xanthus J Biol Chem 273 22 13658 13662 10.1074/jbc.273.22.13658 1:CAS:528: DyaK1cXjvVejtLY%3D (Pubitemid 28268411)
13. TA Dailey HA Dailey 2002 Identification of [2Fe-2S] clusters in microbial ferrochelatases J Bacteriol 184 9 2460 2464 10.1128/JB.184.9.2460-2464.2002 1:CAS:528:DC%2BD38XjvFeis7o%3D (Pubitemid 34311139)
14. TA Dailey HA Dailey P Meissner ARK Prasad 1995 Cloning, sequence, and expression of mouse protoporphyrinogen oxidase Arch Biochem Biophys 324 2 379 384 10.1006/abbi.1995.0051 1:CAS:528:DyaK28Xit1eqtA%3D%3D (Pubitemid 26006421)
15. TA Dailey JH Woodruff HA Dailey 2005 Examination of mitochondrial protein targeting of haem synthetic enzymes: in vivo identification of three functional haem-responsive motifs in 5-aminolaevulinate synthase Biochem J 386 Pt 2 381 386 1:CAS:528:DC%2BD2MXhsFSmsbc%3D (Pubitemid 40343796)
16. HA Dailey C-K Wu P Horanyi AE Medlock W Najahi-Missaoui AE Burden TA Dailey J Rose 2007 Altered orientation of active site residues in variants of human ferrochelatase. Evidence for a hydrogen bond network involved in catalysis Biochem 46 27 7973 7979 10.1021/bi700151f 1:CAS:528:DC%2BD2sXmtl2lsLs%3D (Pubitemid 47051633)
17. Elrod SL, Cherry JR, Jones A (1997) A method for increasing hemoprotein production in filamentous fungi. US Patent No. 6261827
18. SL Elrod A Jones RM Berka JR Cherry 2000 Cloning of the Aspergillus oryzae 5-aminolevulinate synthase gene and its use as a selectable marker Curr Genet 38 5 291 298 10.1007/s002940000156 1:CAS:528:DC%2BD3cXotlKktLk%3D
19. O Emanuelsson S Brunak G von Heijne H Nielsen 2007 Locating proteins in the cell using TargetP, SignalP and related tools Nat Protoc 2 4 953 971 10.1038/nprot.2007.131 1:CAS:528:DC%2BD2sXhtFGnur%2FF (Pubitemid 46745592)
20. PT Erskine N Senior S Maignan J Cooper R Lambert G Lewis P Spencer S Awan M Warren IJ Tickle P Thomas SP Wood PM Shoolingin-Jordan 1997 Crystallization of 5-aminolaevulinic acid dehydratase from Escherichia coli and Saccharomyces cerevisiae and preliminary X-ray characterization of the crystals Protein Sci 6 8 1774 1776 10.1002/pro.5560060820 1:CAS:528:DyaK2sXltlKksbg%3D (Pubitemid 27333082)
21. PJ Espenshade AL Hughes 2007 Regulation of sterol synthesis in eukaryotes Annu Rev Genet 41 401 427 10.1146/annurev.genet.41.110306.130315 1:CAS:528:DC%2BD1cXns1SisQ%3D%3D
22. GC Ferreira 1999 Ferrochelatase Int J Biochem Cell Biol 31 10 995 1000 10.1016/S1357-2725(99)00066-7 1:CAS:528:DyaK1MXmsVWitrw%3D (Pubitemid 29454539)
23. GC Ferreira J Gong 1995 5-Aminolevulinate synthase and the first step of heme biosynthesis J Bioenerg Biomembr 27 2 151 159 10.1007/BF02110030 1:CAS:528:DyaK2MXntVemuro%3D
24. GC Ferreira PJ Neame HA Dailey 1993 Heme biosynthesis in mammalian systems: evidence of a Schiff base linkage between the pyridoxal 5′-phosphate cofactor and a lysine residue in 5-aminolevulinate synthase Protein Sci 2 11 1959 1965 10.1002/pro.5560021117 1:CAS:528:DyaK2cXhvVKjs78%3D (Pubitemid 23328550)
25. E Fujino T Fujino S Karita T Kimura K Sakka K Ohmiya 1999 Purification and characterization of the Clostridium josui porphobilinogen deaminase encoded by the hemC gene from a recombinant Escherichia coli J Biosci Bioeng 87 4 535 537 10.1016/S1389-1723(99)80106-6 1:CAS:528:DyaK1MXkvFajt7w%3D (Pubitemid 29239019)
26. SL Gibson JJ Havens L Metz R Hilf 2001 Is δ-aminolevulinic acid dehydratase rate limiting in heme biosynthesis following exposure of cells to δ-aminolevulinic acid? Photochem Photobiol 73 3 312 317 10.1562/0031-8655(2001)073<0312:IAADRL>2.0.CO;2 1:CAS:528: DC%2BD3MXisVSrsr0%3D
27. M González-Domínguez C Méndez-Carro ME Cerdán 1997 Isolation and characterization of the KlHEM1 gene in Kluyveromyces lactis Yeast 13 10 961 971 10.1002/(SICI)1097-0061(199708)13:10<961::AID- YEA156>3.0.CO;2-Y (Pubitemid 27333241)
28. M González-Domínguez MA Freire-Picos E Ramil B Guiard ME Cerdán 2000 Heme-mediated transcriptional control in Kluyveromyces lactis Curr Genet 38 4 171 177 10.1007/s002940000146
29. M González-Domínguez MA Freire-Picos ME Cerdán 2001 Haem regulation of the mitochondrial import of the Kluyveromyces lactis 5-aminolaevulinate synthase: an organelle approach Yeast 18 1 41 48 10.1002/1097-0061(200101)18:1<41::AID-YEA654>3.0.CO;2-E (Pubitemid 32104862)
30. M Góra K Pluta A Chelstowska T Zoła̧dek 2000 Suppressors of translation initiation defect in hem12 locus of Saccharomyces cerevisiae Acta Biochim Pol 47 1 181 190
31. SA Graf SE Haigh ED Corson OS Shirihai 2004 Targeting, import, and dimerization of a mammalian mitochondrial ATP binding cassette (ABC) transporter, ABCB10 (ABC-me) J Biol Chem 279 41 42954 42963 10.1074/jbc. M405040200 1:CAS:528:DC%2BD2cXotVOgt7s%3D (Pubitemid 39372187)
32. N Grünberg-Etkovitz L Greenbaum B Grinblat Z Malik 2006 Proteasomal degradation regulates expression of porphobilinogen deaminase (PBGD) mutants of acute intermittent porphyria Biochim Biophys Acta 1762 9 819 827 (Pubitemid 44403049)
33. T Guillemette NNME van Peij T Goosen K Lanthaler GD Robson CAMJJ van den Hondel H Stam DB Archer 2007 Genomic analysis of the secretion stress response in the enzyme-producing cell factory Aspergillus niger BMC Genomics 8 158 10.1186/1471-2164-8-158 (Pubitemid 46993520)
34. GG Guo M Gu JD Etlinger 1994 240-kDa proteasome inhibitor (CF-2) is identical to delta-aminolevulinic acid dehydratase J Biol Chem 269 17 12399 12402 (Pubitemid 24202014)
35. H Haas M Eisendle BG Turgeon 2008 Siderophores in fungal physiology and virulence Annu Rev Phytopathol 46 149 187 10.1146/annurev.phyto.45.062806.094338 1:CAS:528:DC%2BD1cXhtFCqt7%2FN
36. I Hamza 2006 Intracellular trafficking of porphyrins ACS Chem Biol 1 10 627 629 10.1021/cb600442b 1:CAS:528:DC%2BD28Xht1Wkt7nE
37. M Hoffman M Góra J Rytka 2003 Identification of rate-limiting steps in yeast heme biosynthesis Biochem Biophys Res Commun 310 4 1247 1253 10.1016/j.bbrc.2003.09.151 1:CAS:528:DC%2BD3sXotVCisbk%3D (Pubitemid 37237669)
38. P Horton KJ Park T Obayashi N Fujita H Harada CJ Adams-Collier K Nakai 2007 WoLF PSORT: protein localization predictor Nucleic Acids Res 35 W585 W587 10.1093/nar/gkm259 (Web Server Issue)
39. P Hortschansky M Eisendle Q Al Abdallah AD Schmidt S Bergmann M Thon O Kniemeyer B Abt B Seeber ER Werner M Kato AA Brakhage H Haas 2007 Interaction of HapX with the CCAAT-binding complex-a novel mechanism of gene regulation by iron EMBO J 26 13 3157 3168 10.1038/sj.emboj.7601752 1:CAS:528: DC%2BD2sXnsFejt74%3D (Pubitemid 47057492)
40. S Hou MF Reynolds FT Horrigan SH Heinemann T Hoshi 2006 Reversible binding of heme to proteins in cellular signal transduction Acc Chem Res 39 12 918 924 10.1021/ar040020w 1:CAS:528:DC%2BD28XpsVyktL8%3D
41. AL Hughes BL Todd PJ Espenshade 2005 SREBP pathway responds to sterols and functions as an oxygen sensor in fission yeast Cell 120 6 831 842 10.1016/j.cell.2005.01.012 1:CAS:528:DC%2BD2MXjtVOqtLo%3D (Pubitemid 40568800)
42. Y Jiang MJ Vasconcelles S Wretzel A Light L Gilooly K McDaid C-S Oh CE Martin MA Goldberg 2002 Mga2p processing by hypoxia and unsaturated fatty acids in Saccharomyces cerevisiae: impact on LORE-dependent gene expression Eukaryot Cell 1 3 481 490 10.1128/EC.1.3.481-490.2002 1:CAS:528:DC%2BD38XkvVWls7k%3D (Pubitemid 36557757)
43. PM Jordan A Berry 1980 Preuroporphyrinogen, a universal intermediate in the biosynthesis of uroporphyrinogen III FEBS Lett 112 1 86 88 10.1016/0014-5793(80)80134-7 1:CAS:528:DyaL3cXktVagtbo%3D (Pubitemid 10076186)
44. WH Jung S Saikia G Hu J Wang CK Fung C D'Souza R White JW Kronstad 2010 HapX positively and negatively regulates the transcriptional response to iron deprivation in Cryptococcus neoformans PLoS Pathog 6 11 e1001209 10.1371/journal.ppat.1001209
45. Y Kabe M Ohmori K Shinouchi Y Tsuboi S Hirao M Azuma H Watanabe I Okura H Handa 2006 Porphyrin accumulation in mitochondria is mediated by 2-oxoglutarate carrier J Biol Chem 281 42 31729 31735 10.1074/jbc.M604729200 1:CAS:528:DC%2BD28XhtVOrtrrM (Pubitemid 46041437)
46. T Keng 1992 HAP1 and ROX1 form a regulatory pathway in the repression of HEM13 transcription in Saccharomyces cerevisiae Mol Cell Biol 12 6 2616 2623 1:CAS:528:DyaK38XksVWrsbY%3D
47. T Keng L Guarente 1987 Constitutive expression of the yeast HEM1 gene is actually a composite of activation and repression Proc Natl Acad Sci USA 84 24 9113 9117 10.1073/pnas.84.24.9113 1:CAS:528:DyaL1cXhtVOgsLo%3D
48. T Keng C Richard R Larocque 1992 Structure and regulation of yeast HEM3, the gene for porphobilinogen deaminase Mol Gen Genet 234 2 233 243 10.1007/BF00283844 1:CAS:528:DyaK3sXksVagsrY%3D
49. LG Klinkenberg TA Mennella K Luetkenhaus RS Zitomer 2005 Combinatorial repression of the hypoxic genes of Saccharomyces cerevisiae by DNA binding proteins Rox1 and Mot3 Eukaryot Cell 4 4 649 660 10.1128/EC.4.4.649-660.2005 1:CAS:528:DC%2BD2MXjvVGqsLg%3D (Pubitemid 40600419)
50. PC Krishnamurthy G Du Y Fukuda D Sun J Sampath KE Mercer J Wang B Sosa-Pineda KG Murti JD Schuetz 2006 Identification of a mammalian mitochondrial porphyrin transporter Nature 443 7111 586 589 1:CAS:528:DC%2BD28XhtVCiu7zM (Pubitemid 44527295)
51. P Krishnamurthy T Xie JD Schuetz 2007 The role of transporters in cellular heme and porphyrin homeostasis Pharmacol Ther 114 3 345 358 10.1016/j.pharmthera.2007.02.001 1:CAS:528:DC%2BD2sXmtVant78%3D (Pubitemid 46843250)
52. A Kurlandzka T Zoła̧dek J Rytka R Labbe-Bois D Urban-Grimal 1988 The effects in vivo of mutationally modified uroporphyrinogen decarboxylase in different hem12 mutants of baker's yeast (Saccharomyces cerevisiae) Biochem J 253 1 109 116 1:CAS:528:DyaL1cXksFWmtr8%3D
53. M Lamas-Maceiras L Núñez E Rodríguez-Belmonte MI González-Siso ME Cerdán 2007 Functional characterization of KlHAP1: a model to foresee different mechanisms of transcriptional regulation by Hap1p in yeasts Gene 405 1-2 96 107 10.1016/j.gene.2007.09.012 1:CAS:528:DC%2BD2sXht1GitLbM (Pubitemid 350016665)
54. JT Lathrop MP Timko 1993 Regulation by heme of mitochondrial protein transport through a conserved amino acid motif Science 259 5094 522 525 10.1126/science.8424176 1:CAS:528:DyaK3sXhvVGqsro%3D (Pubitemid 23058711)
55. G Layer J Reichelt D Jahn DW Heinz 2010 Structure and function of enzymes in heme biosynthesis Protein Sci 19 6 1137 1161 10.1002/pro.405 1:CAS:528:DC%2BC3cXmslSrsb4%3D
56. T Leustek M Smith M Murillo DP Singh AG Smith SC Woodcock SJ Awan MJ Warren 1997 Siroheme biosynthesis in higher plants. Analysis of an S-adenosyl-L-methionine-dependent uroporphyrinogen III methyltransferase from Arabidopsis thaliana J Biol Chem 272 5 2744 2752 10.1074/jbc.272.5.2744 1:CAS:528:DyaK2sXpslektg%3D%3D (Pubitemid 27053318)
57. S Masuo Y Terabayashi M Shimizu T Fujii T Kitazume N Takaya 2010 Global gene expression analysis of Aspergillus nidulans reveals metabolic shift and transcription suppression under hypoxia Mol Genet Genomics 284 6 415 424 10.1007/s00438-010-0576-x 1:CAS:528:DC%2BC3cXhsVagsrrI
58. MA Mathews HL Schubert FG Whitby KJ Alexander K Schadick HA Bergonia JD Phillips CP Hill 2001 Crystal structure of human uroporphyrinogen III synthase EMBO J 20 21 5832 5839 10.1093/emboj/20.21.5832 1:CAS:528:DC%2BD3MXovVSitro%3D (Pubitemid 33049259)
59. PM McNicholas G Javor S Darie RP Gunsalus 1997 Expression of the heme biosynthetic pathway genes hemCD, hemH, hemM, and hemA of Escherichia coli FEMS Microbiol Lett 146 1 143 148 10.1111/j.1574-6968.1997.tb10184.x 1:CAS:528:DyaK28XnsFSmtbY%3D (Pubitemid 27041755)
60. A Mercier S Watt J Bähler S Labbé 2008 Key function for the CCAAT-binding factor Php4 to regulate gene expression in response to iron deficiency in fission yeast Eukaryot Cell 7 3 493 508 10.1128/EC.00446-07 1:CAS:528:DC%2BD1cXkvVGhsbY%3D (Pubitemid 351959677)
61. MB Moretti SC Garcia A Batlle 2000 Porphyrin biosynthesis intermediates are not regulating δ-aminolevulinic acid transport in Saccharomyces cerevisiae Biochem Biophys Res Commun 272 3 946 950 10.1006/bbrc.2000.2874 1:CAS:528:DC%2BD3cXktVKrs78%3D (Pubitemid 30420739)
62. S Muthukrishnan G Padmanaban PS Sarma 1969 Regulation of heme biosynthesis in Neurspora crassa J Biol Chem 244 15 4241 4246 1:CAS:528:DyaF1MXksFOqtrw%3D
63. S Muthukrishnan K Malathi G Padmanaban 1972 δ-Aminolaevulinate dehydratase, the regulatory enzyme of the haem-biosynthetic pathway in Neurospora crassa Biochem J 129 1 31 37 1:CAS:528:DyaE38Xls1Wmsrk%3D
64. L Núñez I González-Siso M Becerra ME Cerdán 2004 Functional characterisation and transcriptional regulation of the KlHEM12 gene from Kluyveromyces lactis Curr Genet 46 3 147 157 10.1007/s00294-004-0517-5 (Pubitemid 39307203)
65. L Núñez A Rodríguez-Torres ME Cerdán 2008 Regulatory elements in the KlHEM1 promoter Biochim Biophys Acta 1779 2 128 133
66. H Panek MR O'Brian 2002 A whole genome view of prokaryotic haem biosynthesis Microbiol 148 Pt 8 2273 2282 1:CAS:528:DC%2BD38XmslSqs7w%3D
67. T Parish M Schaeffer G Roberts K Duncan 2005 HemZ is essential for heme biosynthesis in Mycobacterium tuberculosis Tuberculosis (Edinb) 85 3 197 204 10.1016/j.tube.2005.01.002 1:CAS:528:DC%2BD2MXltFGls78%3D (Pubitemid 40585808)
68. JK Paterson S Shukla CM Black T Tachiwada S Garfield S Wincovitch DN Ernst A Agadir X Li SV Ambudkar G Szakacs S-i Akiyama MM Gottesman 2007 Human ABCB6 localizes to both the outer mitochondrial membrane and the plasma membrane Biochem 46 33 9443 9452 10.1021/bi700015m 1:CAS:528:DC%2BD2sXot1Glurc%3D (Pubitemid 47291951)
69. JD Phillips FG Whitby CA Warby P Labbe C Yang JW Pflugrath JD Ferrara H Robinson JP Kushner CP Hill 2004 Crystal structure of the oxygen-dependant coproporphyrinogen oxidase (Hem13p) of Saccharomyces cerevisiae J Biol Chem 279 37 38960 38968 10.1074/jbc.M406050200 1:CAS:528:DC%2BD2cXnt1yjsLg%3D (Pubitemid 39296057)
70. CF Polo AL Frisardi ER Resnik AE Schoua AM Batlle 1988 Factors influencing fluorescence spectra of free porphyrins Clin Chem 34 4 757 760 1:CAS:528:DyaL1cXitFynu70%3D
71. ARK Prasad HA Dailey 1995 Effect of cellular location on the function of ferrochelatase J Biol Chem 270 31 18198 18200 10.1074/jbc.270.31.18198 1:CAS:528:DyaK2MXntlCqsbg%3D
72. O Protchenko R Rodriguez-Suarez R Androphy H Bussey CC Philpott 2006 A screen for genes of heme uptake identifies the FLC family required for import of FAD into the endoplasmic reticulum J Biol Chem 281 30 21445 21457 10.1074/jbc.M512812200 1:CAS:528:DC%2BD28Xnt1KjsL0%3D (Pubitemid 44115483)
73. O Protchenko M Shakoury-Elizeh P Keane J Storey R Androphy CC Philpott 2008 Role of PUG1 in inducible porphyrin and heme transport in Saccharomyces cerevisiae Eukaryot Cell 7 5 859 871 10.1128/EC.00414-07 1:CAS:528: DC%2BD1cXmvVSrs7o%3D (Pubitemid 351968829)
74. PJ Punt N van Biezen A Conesa A Albers J Mangnus CAMJJ van den Hondel 2002 Filamentous fungi as cell factories for heterologous protein production Trends Biotechnol 20 5 200 206 10.1016/S0167-7799(02)01933-9 1:CAS:528:DC%2BD38Xis1egs70%3D (Pubitemid 34270781)
75. E Raux T McVeigh SE Peters T Leustek MJ Warren 1999 The role of Saccharomyces cerevisiae Met1p and Met8p in sirohaem and cobalamin biosynthesis Biochem J 338 Pt 3 701 708 10.1042/0264-6021:3380701 1:CAS:528: DyaK1MXit1Ogtrk%3D (Pubitemid 29140076)
76. E Raux HK Leech R Beck HL Schubert PJ Santander CA Roessner AI Scott JH Martens D Jahn C Thermes A Rambach MJ Warren 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 Pt 2 505 516 10.1042/BJ20021443 1:CAS:528:DC%2BD3sXhsVWjtbg%3D (Pubitemid 36315139)
77. IR Schlaepfer JR Mattoon G Bajszar 1994 The sequence and potential regulatory elements of the Hem2 promoter of Saccharomyces cerevisiae Yeast 10 2 227 229 10.1002/yea.320100209 1:CAS:528:DyaK2cXivFWitrw%3D (Pubitemid 24099036)
78. M Schrettl HS Kim M Eisendle C Kragl WC Nierman T Heinekamp ER Werner I Jacobsen P Illmer H Yi AA Brakhage H Haas 2008 SreA-mediated iron regulation in Aspergillus fumigatus Mol Microbiol 70 1 27 43 10.1111/j.1365-2958.2008.06376.x 1:CAS:528:DC%2BD1cXht1ams7fF
79. Schrettl M, Beckmann N, Varga J, Heinekamp T, Jacobsen ID, Jochl C, Moussa TA, Wang S, Gsaller F, Blatzer M, Werner ER, Niermann WC, Brakhage AA, Haas H (2010) HapX-mediated adaption to iron starvation is crucial for virulence of Aspergillus fumigatus. PLoS Pathog 6(9)
80. HL Schubert E Raux AA Brindley HK Leech KS Wilson CP Hill MJ Warren 2002 The structure of Saccharomyces cerevisiae Met8p, a bifunctional dehydrogenase and ferrochelatase EMBO J 21 9 2068 2075 10.1093/emboj/21.9.2068 1:CAS:528:DC%2BD38XktFWjtLk%3D (Pubitemid 34516765)
81. HL Schubert E Raux MA Matthews JD Phillips KS Wilson CP Hill MJ Warren 2002 Structural diversity in metal ion chelation and the structure of uroporphyrinogen III synthase Biochem Soc Trans 30 4 595 600 10.1042/BST0300595 1:CAS:528:DC%2BD38XntVenurs%3D (Pubitemid 35001606)
82. NM Senior K Brocklehurst JB Cooper SP Wood P Erskine PM Shoolingin-Jordan PG Thomas MJ Warren 1996 Comparative studies on the 5-aminolaevulinic acid dehydratases from Pisum sativum, Escherichia coli and Saccharomyces cerevisiae Biochem J 320 Pt 2 401 412 1:CAS:528:DyaK2sXis1Kl (Pubitemid 26417759)
83. OS Shirihai T Gregory C Yu SH Orkin MJ Weiss 2000 ABC-me: a novel mitochondrial transporter induced by GATA-1 during erythroid differentiation EMBO J 19 11 2492 2502 10.1093/emboj/19.11.2492 1:CAS:528:DC%2BD3cXkslansb0%3D (Pubitemid 30323539)
84. S Susa M Daimon H Ono S Li T Yoshida T Kato 2002 Heme inhibits the mitochondrial import of coproporphyrinogen oxidase Blood 100 13 4678 4679 10.1182/blood-2002-08-2621 1:CAS:528:DC%2BD38XpsFCqtLw%3D (Pubitemid 35429716)
85. N Takaya 2009 Response to hypoxia, reduction of electron acceptors, and subsequent survival by filamentous fungi Biosci Biotechnol Biochem 73 1 1 8 10.1271/bbb.80487 1:CAS:528:DC%2BD1MXhs1Khs7Y%3D
86. S Taketani Y Adachi Y Nakahashi 2000 Regulation of the expression of human ferrochelatase by intracellular iron levels Eur J Biochem 267 15 4685 4692 10.1046/j.1432-1327.2000.01519.x 1:CAS:528:DC%2BD3cXlslyksLg%3D (Pubitemid 30619458)
87. A Tanaka M Kato T Nagase T Kobayashi N Tsukagoshi 2002 Isolation of genes encoding novel transcription factors which interact with the Hap complex from Aspergillus species Biochim Biophys Acta 1576 1-2 176 182 1:CAS:528: DC%2BD38XjvVejsL0%3D (Pubitemid 34597099)
88. R te Biesebeke A Boussier N van Biezen M Braaksma CA van den Hondel WM de Vos PJ Punt 2006 Expression of Aspergillus hemoglobin domain activities in Aspergillus oryzae grown on solid substrates improves growth rate and enzyme production Biotechnol J 1 7-8 822 827 10.1002/biot.200600036
89. BL Todd EV Stewart JS Burg AL Hughes PJ Espenshade 2006 Sterol regulatory element binding protein is a principal regulator of anaerobic gene expression in fission yeast Mol Cell Biol 26 7 2817 2831 10.1128/MCB.26.7.2817-2831.2006 1:CAS:528:DC%2BD28XivFSrt7s%3D
90. M Tsuchida Y Emi Y Kida M Sakaguchi 2008 Human ABC transporter isoform B6 (ABCB6) localizes primarily in the Golgi apparatus Biochem Biophys Res Commun 369 2 369 375 10.1016/j.bbrc.2008.02.027 1:CAS:528:DC%2BD1cXjs12gt7s%3D
91. PD Vargas K Furuyama S Sassa S Shibahara 2008 Hypoxia decreases the expression of the two enzymes responsible for producing linear and cyclic tetrapyrroles in the heme biosynthetic pathway FEBS J 275 23 5947 5959 10.1111/j.1742-4658.2008.06723.x 1:CAS:528:DC%2BD1cXhsV2murrF
92. MJ Vasconcelles Y Jiang K McDaid L Gilooly S Wretzel DL Porter CE Martin MA Goldberg 2001 Identification and characterization of a low oxygen response element involved in the hypoxic induction of a family of Saccharomyces cerevisiae genes. Implications for the conservation of oxygen sensing in eukaryotes J Biol Chem 276 17 14374 14384 1:CAS:528:DC%2BD3MXjt12rt7k%3D
93. Vödisch M, Scherlach K, Winkler R, Hertweck C, Braun HP, Roth M, Haas H, Werner ER, Brakhage AA, Kniemeyer O (2011) Analysis of the Aspergillus fumigatus proteome reveals metabolic changes and the activation of the pseurotin A biosynthesis gene cluster in response to hypoxia. J Proteome Res [Epub ahead of print]
94. SD Willger S Puttikamonkul KH Kim JB Burritt N Grahl LJ Metzler R Barbuch M Bard CB Lawrence RA Cramer Jr 2008 A sterol-regulatory element binding protein is required for cell polarity, hypoxia adaptation, azole drug resistance, and virulence in Aspergillus fumigatus PLoS Pathog 4 11 e1000200 10.1371/journal.ppat.1000200
95. M Zagorec J-M Buhler I Treich T Keng L Guarente R Labbe-Bois 1988 Isolation, sequence, and regulation by oxygen of the yeast HEM13 gene coding for coproporphyrinogen oxidase J Biol Chem 263 20 9718 9724 1:CAS:528: DyaL1cXltVGkt70%3D
96. S Zhou S Fushinobu Y Nakanishi SW Kim T Wakagi H Shoun 2009 Cloning and characterization of two flavohemoglobins from Aspergillus oryzae Biochem Biophys Res Commun 381 1 7 11 10.1016/j.bbrc.2009.01.112 1:CAS:528:DC%2BD1MXjt1KmtLs%3D
97. S Zhou S Fushinobu SW Kim Y Nakanishi T Wakagi H Shoun 2010 Aspergillus oryzae flavohemoglobins promote oxidative damage by hydrogen peroxide Biochem Biophys Res Commun 394 3 558 561 10.1016/j.bbrc.2010.03.018 1:CAS:528: DC%2BC3cXks1Kisrg%3D
98. S Zhou S Fushinobu SW Kim Y Nakanishi J Maruyama K Kitamoto T Wakagi H Shoun 2011 Functional analysis and subcellular location of two flavohemoglobins from Aspergillus oryzae Fungal Genet Biol 48 2 200 207 10.1016/j.fgb.2010.08.011 1:CAS:528:DC%2BC3cXhsFCqsbrF
99. RS Zitomer CV Lowry 1992 Regulation of gene expression by oxygen in Saccharomyces cerevisiae Microbiol Rev 56 1 1 11 1:CAS:528:DyaK38XitlWgt7s%3D