|
|
Essential functions of iron-requiring proteins in DNA replication, repair and cell cycle control |
Caiguo Zhang( ) |
Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, CO 80045, USA |
|
|
Abstract Eukaryotic cells contain numerous iron-requiring proteins such as iron-sulfur (Fe-S) cluster proteins, hemoproteins and ribonucleotide reductases (RNRs). These proteins utilize iron as a cofactor and perform key roles in DNA replication, DNA repair, metabolic catalysis, iron regulation and cell cycle progression. Disruption of iron homeostasis always impairs the functions of these ironrequiring proteins and is genetically associated with diseases characterized by DNA repair defects in mammals. Organisms have evolved multi-layered mechanisms to regulate iron balance to ensure genome stability and cell development. This review briefly provides current perspectives on iron homeostasis in yeast and mammals, and mainly summarizes the most recent understandings on iron-requiring protein functions involved in DNA stability maintenance and cell cycle control.
|
Keywords
iron-requiring protein
DNA replication
DNA repair
cell cycle
iron homeostasis
|
Corresponding Author(s):
Caiguo Zhang
|
Issue Date: 24 October 2014
|
|
1 |
Acharya N, Johnson RE, Prakash S, Prakash L (2006) Complex formation with Rev1 enhances the proficiency of Saccharomyces cerevisiae DNA polymerase zeta for mismatch extension and for extension opposite from DNA lesions. Mol Cell Biol26: 9555-9563
https://doi.org/10.1128/MCB.01671-06
|
2 |
Alvaro D, Lisby M, Rothstein R (2007) Genome-wide analysis of Rad52 foci reveals diverse mechanisms impacting recombination. PLoS Genet3: e228
https://doi.org/10.1371/journal.pgen.0030228
|
3 |
Amillet JM, Galiazzo F, Labbe-Bois R (1996) Effect of heme and vacuole deficiency on FRE1 gene expression and ferrireductase activity in Saccharomyces cerevisiae. FEMS Microbiol Lett137: 25-29
https://doi.org/10.1111/j.1574-6968.1996.tb08077.x
|
4 |
Anderson GJ, Vulpe CD (2009) Mammalian iron transport. Cellular Mol Life Sci CMLS66: 3241-3261
https://doi.org/10.1007/s00018-009-0051-1
|
5 |
Andrews NC, Schmidt PJ (2007) Iron homeostasis. Annu Rev Physiol69: 69-85
https://doi.org/10.1146/annurev.physiol.69.031905.164337
|
6 |
Aslan M, Horoz M, Kocyigit A, Ozgonul S, Celik H, Celik M, Erel O (2006) Lymphocyte DNA damage and oxidative stress in patients with iron deficiency anemia. Mutat Res601: 144-149
https://doi.org/10.1016/j.mrfmmm.2006.06.013
|
7 |
Beaumont C (2010) Multiple regulatory mechanisms act in concert to control ferroportin expression and heme iron recycling by macrophages: 1233-1236
https://doi.org/10.3324/haematol.2010.025585
|
8 |
Berthelet S, Usher J, Shulist K, Hamza A, Maltez N, Johnston A, Fong Y, Harris LJ, Baetz K (2010) Functional genomics analysis of the Saccharomyces cerevisiae iron responsive transcription factor Aft1 reveals iron-independent functions. Genetics185: 1111-1128
https://doi.org/10.1534/genetics.110.117531
|
9 |
Bjorklund S, Skog S, Tribukait B, Thelander L (1990) S-phasespecific expression of mammalian ribonucleotide reductase R1 and R2 subunit mRNAs. Biochemistry29: 5452-5458
https://doi.org/10.1021/bi00475a007
|
10 |
Brown KR, Brown BM, Hoagland E, Mayne CL, Hegg EL (2004) Heme A synthase does not incorporate molecular oxygen into the formyl group of heme A. Biochemistry43: 8616-8624
https://doi.org/10.1021/bi049056m
|
11 |
Cendra Mdel M, Juarez A, Madrid C, Torrents E (2013) H-NS is a novel transcriptional modulator of the ribonucleotide reductase genes in Escherichia coli. J Bacteriol195: 4255-4263
https://doi.org/10.1128/JB.00490-13
|
12 |
Chabes AL, Pfleger CM, Kirschner MW, Thelander L (2003) Mouse ribonucleotide reductase R2 protein: a new target for anaphasepromoting complex-Cdh1-mediated proteolysis. Proc Natl Acad Sci USA100: 3925-3929
https://doi.org/10.1073/pnas.0330774100
|
13 |
Chabes AL, Bjorklund S, Thelander L (2004) S Phase-specific transcription of the mouse ribonucleotide reductase R2 gene requires both a proximal repressive E2F-binding site and an upstream promoter activating region. J Biol Chem279: 10796-10807
https://doi.org/10.1074/jbc.M312482200
|
14 |
Chaboute ME, Clement B, Philipps G (2002) S phase and meristemspecific expression of the tobacco RNR1b gene is mediated by an E2F element located in the 5’ leader sequence. J Biol Chem277: 17845-17851
https://doi.org/10.1074/jbc.M200959200
|
15 |
Chen KC, Csikasz-Nagy A, Gyorffy B, Val J, Novak B, Tyson JJ (2000) Kinetic analysis of a molecular model of the budding yeast cell cycle. Mol Biol Cell11: 369-391
https://doi.org/10.1091/mbc.11.1.369
|
16 |
Cheng NH, Zhang W, Chen WQ, Jin J, Cui X, Butte NF, Chan L, Hirschi KD (2011) A mammalian monothiol glutaredoxin, Grx3, is critical for cell cycle progression during embryogenesis. FEBS J278: 2525-2539
https://doi.org/10.1111/j.1742-4658.2011.08178.x
|
17 |
Coin F, Oksenych V, Egly JM (2007) Distinct roles for the XPB/p52 and XPD/p44 subcomplexes of TFIIH in damaged DNA opening during nucleotide excision repair. Mol Cell26: 245-256
https://doi.org/10.1016/j.molcel.2007.03.009
|
18 |
Couturier J, Touraine B, Briat JF, Gaymard F, Rouhier N (2013) The iron-sulfur cluster assembly machineries in plants: current knowledge and open questions. Front Plant Sci4: 259
https://doi.org/10.3389/fpls.2013.00259
|
19 |
D’Angiolella V, Donato V, Forrester FM, Jeong YT, Pellacani C, Kudo Y, Saraf A, Florens L, Washburn MP, Pagano M (2012) Cyclin F-mediated degradation of ribonucleotide reductase M2 controls genome integrity and DNA repair. Cell149: 1023-1034
https://doi.org/10.1016/j.cell.2012.03.043
|
20 |
Danilova N, Bibikova E, Covey TM, Nathanson D, Dimitrova E, Konto Y, Lindgren A, Glader B, Radu CG, Sakamoto KM. (2014). The role of DNA damage response in zebrafish and cellular models of Diamond Blackfan Anemia. Disease models & mechanisms
https://doi.org/10.1242/dmm.015495
|
21 |
Deans AJ, West SC (2009) FANCM connects the genome instability disorders Bloom’s syndrome and Fanconi anemia. Mol Cell36: 943-953
https://doi.org/10.1016/j.molcel.2009.12.006
|
22 |
Denic S, Agarwal MM (2007) Nutritional iron deficiency: an evolutionary perspective. Nutrition23: 603-614
https://doi.org/10.1016/j.nut.2007.05.002
|
23 |
Diaz-Castro J, Alferez MJ, Lopez-Aliaga I, Nestares T, Granados S, Barrionuevo M, Campos MS (2008) Influence of nutritional iron deficiency anemia on DNA stability and lipid peroxidation in rats. Nutrition24: 1167-1173
https://doi.org/10.1016/j.nut.2008.05.012
|
24 |
Dlouhy AC, Outten CE (2013) The iron metallome in eukaryotic organisms. Metal Ions Life Sci12: 241-278
https://doi.org/10.1007/978-94-007-5561-1_8
|
25 |
Dunn LL, Suryo Rahmanto Y, Richardson DR (2007) Iron uptake and metabolism in the new millennium. Trends Cell Biol17: 93-100
https://doi.org/10.1016/j.tcb.2006.12.003
|
26 |
Emerson LR, Nau ME, Martin RK, Kyle DE, Vahey M, Wirth DF (2002) Relationship between chloroquine toxicity and iron acquisition in Saccharomyces cerevisiae. Antimicrob Agents Chemother46: 787-796
https://doi.org/10.1128/AAC.46.3.787-796.2002
|
27 |
Fregoso M, Laine JP, Aguilar-Fuentes J, Mocquet V, Reynaud E, Coin F, Egly JM, Zurita M (2007) DNA repair and transcriptional deficiencies caused by mutations in the Drosophila p52 subunit of TFIIH generate developmental defects and chromosome fragility. Mol Cell Biol27: 3640-3650
https://doi.org/10.1128/MCB.00030-07
|
28 |
Fu D, Richardson DR (2007) Iron chelation and regulation of the cell cycle: 2 mechanisms of posttranscriptional regulation of the universal cyclin-dependent kinase inhibitor p21CIP1/WAF1 by iron depletion. Blood110: 752-761
https://doi.org/10.1182/blood-2007-03-076737
|
29 |
Gan L, von Moltke LL, Trepanier LA, Harmatz JS, Greenblatt DJ, Court MH (2009) Role of NADPH-cytochrome P450 reductase and cytochrome-b5/NADH-b5 reductase in variability of CYP3A activity in human liver microsomes. Drug Metab Dispos37: 90-96
https://doi.org/10.1124/dmd.108.023424
|
30 |
Gari K, Leon Ortiz AM, Borel V, Flynn H, Skehel JM, Boulton SJ (2012) MMS19 links cytoplasmic iron-sulfur cluster assembly to DNA metabolism. Science337: 243-245
https://doi.org/10.1126/science.1219664
|
31 |
Girvan HM, Munro AW (2013) Heme sensor proteins. J Biol Chem288: 13194-13203
https://doi.org/10.1074/jbc.R112.422642
|
32 |
Gkouvatsos K, Papanikolaou G, Pantopoulos K (2012) Regulation of iron transport and the role of transferrin. Biochim Biophys Acta1820: 188-202
https://doi.org/10.1016/j.bbagen.2011.10.013
|
33 |
Hamza A, Baetz K (2012) Iron-responsive transcription factor Aft1 interacts with kinetochore protein Iml3 and promotes pericentromeric cohesin. J Biol Chem287: 4139-4147
https://doi.org/10.1074/jbc.M111.319319
|
34 |
Haro KJ, Sheth A, Scheinberg DA (2012) Dysregulation of IRP1-mediated iron metabolism causes gamma ray-specific radioresistance in leukemia cells. PLoS ONE7: e48841
https://doi.org/10.1371/journal.pone.0048841
|
35 |
Harper JW, Elledge SJ (2007) The DNA damage response: ten years after. Mol Cell28: 739-745
https://doi.org/10.1016/j.molcel.2007.11.015
|
36 |
Haunhorst P, Hanschmann EM, Brautigam L, Stehling O, Hoffmann B, Muhlenhoff U, Lill R, Berndt C, Lillig CH (2013) Crucial function of vertebrate glutaredoxin 3 (PICOT) in iron homeostasis and hemoglobin maturation. Mol Biol Cell24: 1895-1903
https://doi.org/10.1091/mbc.E12-09-0648
|
37 |
He L, Wang H, Jin H, Guo C, Xie H, Yan K, Li X, Shen Q, Qiao T, Chen G (2009) CIAPIN1 inhibits the growth and proliferation of clear cell renal cell carcinoma. Cancer Lett276: 88-94
https://doi.org/10.1016/j.canlet.2008.10.044
|
38 |
Heath JL, Weiss JM, Lavau CP, Wechsler DS (2013) Iron deprivation in cancer—potential therapeutic implications. Nutrients5: 2836-2859
https://doi.org/10.3390/nu5082836
|
39 |
Herbik A, Bolling C, Buckhout TJ (2002) The involvement of a multicopper oxidase in iron uptake by the green algae Chlamydomonas reinhardtii. Plant Physiol130: 2039-2048
https://doi.org/10.1104/pp.013060
|
40 |
Heymann P, Ernst JF, Winkelmann G (2000) Identification and substrate specificity of a ferrichrome-type siderophore transporter (Arn1p) in Saccharomyces cerevisiae. FEMS Microbiol Lett186: 221-227
https://doi.org/10.1111/j.1574-6968.2000.tb09108.x
|
41 |
Holmes-Hampton GP, Jhurry ND, McCormick SP, Lindahl PA (2013) Iron content of Saccharomyces cerevisiae cells grown under irondeficient and iron-overload conditions. Biochemistry52: 105-114
https://doi.org/10.1021/bi3015339
|
42 |
Jiang X, Wang X (2004) Cytochrome C-mediated apoptosis. Annu Rev Biochem73: 87-106
https://doi.org/10.1146/annurev.biochem.73.011303.073706
|
43 |
Kamei A, Watanabe Y, Ishijima T, Uehara M, Arai S, Kato H, Nakai Y, Abe K (2010) Dietary iron-deficient anemia induces a variety of metabolic changes and even apoptosis in rat liver: a DNA microarray study. Physiol Genomics42: 149-156
https://doi.org/10.1152/physiolgenomics.00150.2009
|
44 |
Kaplan CD, Kaplan J (2009) Iron acquisition and transcriptional regulation. Chem Rev109: 4536-4552
https://doi.org/10.1021/cr9001676
|
45 |
Kaplan J, McVey Ward D, Crisp RJ, Philpott CC (2006) Irondependent metabolic remodeling in S. cerevisiae. Biochim Biophys Acta1763: 646-651
https://doi.org/10.1016/j.bbamcr.2006.03.008
|
46 |
Keyes SR, Cinti DL (1980) Biochemical properties of cytochrome b5-dependent microsomal fatty acid elongation and identification of products. J Biol Chem255: 11357-11364
|
47 |
Kilkenny ML, Longo MA, Perera RL, Pellegrini L (2013) Structures of human primase reveal design of nucleotide elongation site and mode of Pol alpha tethering. Proc Natl Acad Sci USA110: 15961-15966
https://doi.org/10.1073/pnas.1311185110
|
48 |
Kumar D, Viberg J, Nilsson AK, Chabes A (2010) Highly mutagenic and severely imbalanced dNTP pools can escape detection by the S-phase checkpoint. Nucleic Acids Res38: 3975-3983
https://doi.org/10.1093/nar/gkq128
|
49 |
Laha S, Das SP, Hajra S, Sanyal K, Sinha P (2011) Functional characterization of the Saccharomyces cerevisiae protein Chl1 reveals the role of sister chromatid cohesion in the maintenance of spindle length during S-phase arrest. BMC Genet12: 83
https://doi.org/10.1186/1471-2156-12-83
|
50 |
Larade K, Jiang Z, Zhang Y, Wang W, Bonner-Weir S, Zhu H, Bunn HF (2008) Loss of Ncb5or results in impaired fatty acid desaturation, lipoatrophy, and diabetes. J Biol Chem283: 29285-29291
https://doi.org/10.1074/jbc.M804645200
|
51 |
Lee YD, Elledge SJ (2006) Control of ribonucleotide reductase localization through an anchoring mechanism involving Wtm1. Genes Dev20: 334-344
https://doi.org/10.1101/gad.1380506
|
52 |
Lee PJ, Alam J, Wiegand GW, Choi AM (1996) Overexpression of heme oxygenase-1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia. Proc Natl Acad Sci USA93: 10393-10398
https://doi.org/10.1073/pnas.93.19.10393
|
53 |
Lesuisse E, Simon-Casteras M, Labbe P (1998) Siderophoremediated iron uptake in Saccharomyces cerevisiae: the SIT1 gene encodes a ferrioxamine B permease that belongs to the major facilitator superfamily. Microbiology144(Pt 12): 3455-3462
https://doi.org/10.1099/00221287-144-12-3455
|
54 |
Li H, Outten CE (2012) Monothiol CGFS glutaredoxins and BolA-like proteins: [2Fe-2S] binding partners in iron homeostasis. Biochemistry51: 4377-4389
https://doi.org/10.1021/bi300393z
|
55 |
Li L, Chen OS, McVey Ward D, Kaplan J (2001) CCC1 is a transporter that mediates vacuolar iron storage in yeast. J Biol Chem276: 29515-29519
https://doi.org/10.1074/jbc.M103944200
|
56 |
Li L, Bagley D, Ward DM, Kaplan J (2008) Yap5 is an ironresponsive transcriptional activator that regulates vacuolar iron storage in yeast. Mol Cell Biol28: 1326-1337
https://doi.org/10.1128/MCB.01219-07
|
57 |
Li L, Kaplan J (1998) Defects in the yeast high affinity iron transport system result in increased metal sensitivity because of the increased expression of transporters with a broad transition metal specificity. J Biol Chem273: 22181-22187
https://doi.org/10.1074/jbc.273.35.22181
|
58 |
Li H, Mapolelo DT, Dingra NN, Naik SG, Lees NS, Hoffman BM, Riggs-Gelasco PJ, Huynh BH, Johnson MK, Outten CE (2009) The yeast iron regulatory proteins Grx3/4 and Fra2 form heterodimeric complexes containing a [2Fe-2S] cluster with cysteinyl and histidyl ligation. Biochemistry48: 9569-9581
https://doi.org/10.1021/bi901182w
|
59 |
Lill R, Muhlenhoff U (2008) Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases.Annu Rev Biochem77: 669-700
https://doi.org/10.1146/annurev.biochem.76.052705.162653
|
60 |
Lill R, Hoffmann B, Molik S, Pierik AJ, Rietzschel N, Stehling O, Uzarska MA, Webert H, Wilbrecht C, Muhlenhoff U (2012) The role of mitochondria in cellular iron-sulfur protein biogenesis and iron metabolism. Biochim Biophys Acta1823: 1491-1508
https://doi.org/10.1016/j.bbamcr.2012.05.009
|
61 |
Lipinski P, Starzynski RR, Drapier JC, Bouton C, Bartlomiejczyk T, Sochanowicz B, Smuda E, Gajkowska A, Kruszewski M (2005) Induction of iron regulatory protein 1 RNA-binding activity by nitric oxide is associated with a concomitant increase in the labile iron pool: implications for DNA damage. Biochem Biophys Res Commun327: 349-355
https://doi.org/10.1016/j.bbrc.2004.12.012
|
62 |
Lopez-Millan AF, Grusak MA, Abadia A, Abadia J (2013) Iron deficiency in plants: an insight from proteomic approaches. Front Plant Sci4: 254
https://doi.org/10.3389/fpls.2013.00254
|
63 |
Martinez-Pastor MT, de Llanos R, Romero AM, Puig S (2013) Posttranscriptional regulation of iron homeostasis in Saccharomyces cerevisiae. Int J Mol Sci14: 15785-15809
https://doi.org/10.3390/ijms140815785
|
64 |
Mendenhall MD, Hodge AE (1998) Regulation of Cdc28 cyclindependent protein kinase activity during the cell cycle of the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev62: 1191-1243
|
65 |
Miller JL (2013) Iron deficiency anemia: a common and curable disease. Cold Spring Harbor perspectives in medicine 3
|
66 |
Miyabe I, Kunkel TA, Carr AM (2011) The major roles of DNA polymerases epsilon and delta at the eukaryotic replication fork are evolutionarily conserved. PLoS Genet7: e1002407
https://doi.org/10.1371/journal.pgen.1002407
|
67 |
Muckenthaler MU, Galy B, Hentze MW (2008) Systemic iron homeostasis and the iron-responsive element/iron-regulatory protein (IRE/IRP) regulatory network. Annu Rev Nutr28: 197-213
https://doi.org/10.1146/annurev.nutr.28.061807.155521
|
68 |
Muhlenhoff U, Molik S, Godoy JR, Uzarska MA, Richter N, Seubert A, Zhang Y, Stubbe J, Pierrel F, Herrero E (2010) Cytosolic monothiol glutaredoxins function in intracellular iron sensing and trafficking via their bound iron-sulfur cluster. Cell Metab12: 373-385
https://doi.org/10.1016/j.cmet.2010.08.001
|
69 |
Nakano K, Balint E, Ashcroft M, Vousden KH (2000) A ribonucleotide reductase gene is a transcriptional target of p53 and p73. Oncogene19: 4283-4289
https://doi.org/10.1038/sj.onc.1203774
|
70 |
Nasmyth K (1993) Control of the yeast cell cycle by the Cdc28 protein kinase. Curr Opin Cell Biol5: 166-179
https://doi.org/10.1016/0955-0674(93)90099-C
|
71 |
Netz DJ, Stumpfig M, Dore C, Muhlenhoff U, Pierik AJ, Lill R (2010) Tah18 transfers electrons to Dre2 in cytosolic iron-sulfur protein biogenesis. Nat Chem Biol6: 758-765
https://doi.org/10.1038/nchembio.432
|
72 |
Netz DJ, Stith CM, Stumpfig M, Kopf G, Vogel D, Genau HM, Stodola JL, Lill R, Burgers PM, Pierik AJ (2012) Eukaryotic DNA polymerases require an iron-sulfur cluster for the formation of active complexes. Nat Chem Biol8: 125-132
https://doi.org/10.1038/nchembio.721
|
73 |
Ofir A, Kornitzer D (2010) Candida albicans cyclin Clb4 carries S-phase cyclin activity. Eukaryot Cell9: 1311-1319
https://doi.org/10.1128/EC.00038-10
|
74 |
Orrenius S, Nicotera P, Zhivotovsky B (2011) Cell death mechanisms and their implications in toxicology. Toxicol Sci Off J Soc Toxicol119: 3-19
https://doi.org/10.1093/toxsci/kfq268
|
75 |
Pamplona A, Ferreira A, Balla J, Jeney V, Balla G, Epiphanio S, Chora A, Rodrigues CD, Gregoire IP, Cunha-Rodrigues M (2007) Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat Med13: 703-710
https://doi.org/10.1038/nm1586
|
76 |
Pantopoulos K, Porwal SK, Tartakoff A, Devireddy L (2012) Mechanisms of mammalian iron homeostasis. Biochemistry51: 5705-5724
https://doi.org/10.1021/bi300752r
|
77 |
Parish JL, Rosa J, Wang X, Lahti JM, Doxsey SJ, Androphy EJ (2006) The DNA helicase ChlR1 is required for sister chromatid cohesion in mammalian cells. J Cell Sci119: 4857-4865
https://doi.org/10.1242/jcs.03262
|
78 |
Philpott CC (2006) Iron uptake in fungi: a system for every source. Biochim Biophys Acta1763: 636-645
https://doi.org/10.1016/j.bbamcr.2006.05.008
|
79 |
Philpott CC, Rashford J, Yamaguchi-Iwai Y, Rouault TA, Dancis A, Klausner RD (1998) Cell-cycle arrest and inhibition of G1 cyclin translation by iron in AFT1-1(up) yeast. EMBO J17: 5026-5036
https://doi.org/10.1093/emboj/17.17.5026
|
80 |
Philpott CC, Leidgens S, Frey AG (2012) Metabolic remodeling in iron-deficient fungi. Biochim Biophys Acta1823: 1509-1520
https://doi.org/10.1016/j.bbamcr.2012.01.012
|
81 |
Poor CB, Wegner SV, Li H, Dlouhy AC, Schuermann JP, Sanishvili R, Hinshaw JR, Riggs-Gelasco PJ, Outten CE, He C (2014) Molecular mechanism and structure of the Saccharomyces cerevisiae iron regulator Aft2. Proc Natl Acad Sci USA111: 4043-4048
https://doi.org/10.1073/pnas.1318869111
|
82 |
Portnoy ME, Liu XF, Culotta VC (2000) Saccharomyces cerevisiae expresses three functionally distinct homologues of the nramp family of metal transporters. Mol Cell Biol20: 7893-7902
https://doi.org/10.1128/MCB.20.21.7893-7902.2000
|
83 |
Portnoy ME, Jensen LT, Culotta VC (2002) The distinct methods by which manganese and iron regulate the Nramp transporters inyeast. Biochem J362: 119-124
https://doi.org/10.1042/0264-6021:3620119
|
84 |
Prakash S, Prakash L (2002) Translesion DNA synthesis in eukaryotes: a one- or two-polymerase affair. Genes Dev16: 1872-1883
https://doi.org/10.1101/gad.1009802
|
85 |
Pugh RA, Honda M, Leesley H, Thomas A, Lin Y, Nilges MJ, Cann IK, Spies M (2008) The iron-containing domain is essential in Rad3 helicases for coupling of ATP hydrolysis to DNA translocation and for targeting the helicase to the single-stranded DNAdouble-stranded DNA junction. J Biol Chem283: 1732-1743
https://doi.org/10.1074/jbc.M707064200
|
86 |
Pyrih J, Harant K, Martincova E, Sutak R, Lesuisse E, Hrdy I, Tachezy J (2014) Giardia intestinalis incorporates heme into cytosolic cytochrome b(5). Eukaryot Cell13: 231-239
https://doi.org/10.1128/EC.00200-13
|
87 |
Quincozes-Santos A, Bobermin LD, Latini A, Wajner M, Souza DO, Goncalves CA, Gottfried C (2013) Resveratrol protects C6 astrocyte cell line against hydrogen peroxide-induced oxidative stress through heme oxygenase 1. PLoS ONE8: e64372
https://doi.org/10.1371/journal.pone.0064372
|
88 |
Rao VA (2013) Iron chelators with topoisomerase-inhibitory activity and their anticancer applications. Antioxid Redox Signal18: 930-955
https://doi.org/10.1089/ars.2012.4877
|
89 |
Rae TD, Goff HM (1998) The heme prosthetic group of lactoperoxidase. Structural characteristics of heme l and heme l-peptides: 27968-27977
https://doi.org/10.1074/jbc.273.43.27968
|
90 |
Reddy VV, Kupfer D, Caspi E (1977) Mechanism of C-5 double bond introduction in the biosynthesis of cholesterol by rat liver microsomes. J Biol Chem252: 2797-2801
|
91 |
Reid EL, Weynberg KD, Love J, Isupov MN, Littlechild JA, Wilson WH, Kelly SL, Lamb DC, Allen MJ (2013) Functional and structural characterisation of a viral cytochrome b5. FEBS Lett587: 3633-3639
https://doi.org/10.1016/j.febslet.2013.09.035
|
92 |
Renton FJ, Jeitner TM (1996) Cell cycle-dependent inhibition of the proliferation of human neural tumor cell lines by iron chelators. Biochem Pharmacol51: 1553-1561
https://doi.org/10.1016/0006-2952(96)00099-8
|
93 |
Romero A, Ramos E, de Los Rios C, Egea J, Del Pino J, Reiter RJ (2014) A review of metal-catalyzed molecular damage: protection by melatonin. J Pineal Res56: 343
https://doi.org/10.1111/jpi.12132
|
94 |
Rouault TA (2012) Biogenesis of iron-sulfur clusters in mammalian cells: new insights and relevance to human disease. Dis Models Mech5: 155-164
https://doi.org/10.1242/dmm.009019
|
95 |
Rudolf J, Makrantoni V, Ingledew WJ, Stark MJ, White MF (2006) The DNA repair helicases XPD and FancJ have essential iron-sulfur domains. Mol Cell23: 801-808
https://doi.org/10.1016/j.molcel.2006.07.019
|
96 |
Rutherford JC, Jaron S, Ray E, Brown PO, Winge DR (2001) A second iron-regulatory system in yeast independent of Aft1p. Proc Natl Acad Sci USA98: 14322-14327
https://doi.org/10.1073/pnas.261381198
|
97 |
Sanvisens N, Bano MC, Huang M, Puig S (2011) Regulation of ribonucleotide reductase in response to iron deficiency. Mol Cell44: 759-769
https://doi.org/10.1016/j.molcel.2011.09.021
|
98 |
Sanvisens N, de Llanos R, Puig S (2013) Function and regulation of yeast ribonucleotide reductase: cell cycle, genotoxic stress, and iron bioavailability. Biomed J36: 51-58
https://doi.org/10.4103/2319-4170.110398
|
99 |
Sauguet L, Klinge S, Perera RL, Maman JD, Pellegrini L (2010) Shared active site architecture between the large subunit of eukaryotic primase and DNA photolyase. PLoS ONE5: e10083
https://doi.org/10.1371/journal.pone.0010083
|
100 |
Schenkman JB, Jansson I (2003) The many roles of cytochrome b5. Pharmacol Ther97: 139-152
https://doi.org/10.1016/S0163-7258(02)00327-3
|
101 |
Schumacher SB, Stucki M, Hubscher U (2000) The N-terminal region of DNA polymerase delta catalytic subunit is necessary for holoenzyme function. Nucleic Acids Res28: 620-625
https://doi.org/10.1093/nar/28.2.620
|
102 |
Severance S, Hamza I (2009) Trafficking of heme and porphyrins in metazoa. Chem Rev109: 4596-4616
https://doi.org/10.1021/cr9001116
|
103 |
Shah R, Agarwal AK (2013) Anemia associated with chronic heart failure: current concepts. Clin Interv Aging8: 111-122
|
104 |
Shakoury-Elizeh M, Protchenko O, Berger A, Cox J, Gable K, Dunn TM, Prinz WA, Bard M, Philpott CC (2010) Metabolic response to iron deficiency in Saccharomyces cerevisiae. J Biol Chem285: 14823-14833
https://doi.org/10.1074/jbc.M109.091710
|
105 |
Sharp P, Srai SK (2007) Molecular mechanisms involved in intestinal iron absorption. World J Gastroenterol13: 4716-4724
|
106 |
Sipos K, Lange H, Fekete Z, Ullmann P, Lill R, Kispal G (2002) Maturation of cytosolic iron-sulfur proteins requires glutathione. J Biol Chem277: 26944-26949
https://doi.org/10.1074/jbc.M200677200
|
107 |
Siriwardana G, Seligman PA (2013) Two cell cycle blocks caused by iron chelation of neuroblastoma cells: separating cell cycle events associated with each block. Physiol Rep1: e00176
https://doi.org/10.1002/phy2.176
|
108 |
Soe-Lin S, Apte SS, Andriopoulos B Jr, Andrews MC, Schranzhofer M, Kahawita T, Garcia-Santos D, Ponka P (2009) Nramp1 promotes efficient macrophage recycling of iron following erythrophagocytosis in vivo. Proc Natl Acad Sci USA106: 5960-5965
https://doi.org/10.1073/pnas.0900808106
|
109 |
Solti A, Gaspar L, Meszaros I, Szigeti Z, Levai L, Sarvari E (2008) Impact of iron supply on the kinetics of recovery of photosynthesis in Cd-stressed poplar (Populus glauca). Ann Bot102: 771-782
https://doi.org/10.1093/aob/mcn160
|
110 |
Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, Brown PO, Botstein D, Futcher B (1998) Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell9: 3273-3297
https://doi.org/10.1091/mbc.9.12.3273
|
111 |
Stehling O, Vashisht AA, Mascarenhas J, Jonsson ZO, Sharma T, Netz DJ, Pierik AJ, Wohlschlegel JA, Lill R (2012) MMS19 assembles iron-sulfur proteins required for DNA metabolism and genomic integrity.Science337: 195-199
https://doi.org/10.1126/science.1219723
|
112 |
Stehling O, Mascarenhas J, Vashisht AA, Sheftel AD, Niggemeyer B, Rosser R, Pierik AJ, Wohlschlegel JA, Lill R (2013) Human CIA2A-FAM96A and CIA2B-FAM96B integrate iron homeostasis and maturation of different subsets of cytosolic-nuclear iron-sulfur proteins. Cell Metab18: 187-198
https://doi.org/10.1016/j.cmet.2013.06.015
|
113 |
Sung P, Guzder SN, Prakash L, Prakash S (1996) Reconstitution of TFIIH and requirement of its DNA helicase subunits, Rad3 and Rad25, in the incision step of nucleotide excision repair. J Biol Chem271: 10821-10826
https://doi.org/10.1074/jbc.271.18.10821
|
114 |
Tanaka H, Arakawa H, Yamaguchi T, Shiraishi K, Fukuda S, Matsui K, Takei Y, Nakamura Y (2000) A ribonucleotide reductase gene involved in a p53-dependent cell-cycle checkpoint for DNA damage. Nature404: 42-49
https://doi.org/10.1038/35003506
|
115 |
Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol552: 335-344
https://doi.org/10.1113/jphysiol.2003.049478
|
116 |
Ueta R, Fujiwara N, Iwai K, Yamaguchi-Iwai Y (2007) Mechanism underlying the iron-dependent nuclear export of the iron-responsive transcription factor Aft1p in Saccharomyces cerevisiae. Mol Biol Cell18: 2980-2990
https://doi.org/10.1091/mbc.E06-11-1054
|
117 |
Ueta R, Fujiwara N, Iwai K, Yamaguchi-Iwai Y (2012) Iron-induced dissociation of the Aft1p transcriptional regulator from target gene promoters is an initial event in iron-dependent gene suppression. Mol Cell Biol32: 4998-5008
https://doi.org/10.1128/MCB.00726-12
|
118 |
Urbanowski JL, Piper RC (1999) The iron transporter Fth1p forms a complex with the Fet5 iron oxidase and resides on the vacuolar membrane. J Biol Chem274: 38061-38070
https://doi.org/10.1074/jbc.274.53.38061
|
119 |
Vergeres G, Waskell L (1995) Cytochrome b5, its functions, structure and membrane topology. Biochimie77: 604-620
https://doi.org/10.1016/0300-9084(96)88176-4
|
120 |
Vohradsky J (2012) Stochastic simulation for the inference of transcriptional control network of yeast cyclins genes. Nucleic Acids Res40: 7096-7103
https://doi.org/10.1093/nar/gks440
|
121 |
Wagener FA, van Beurden HE, von den Hoff JW, Adema GJ, Figdor CG (2003) The heme-heme oxygenase system: a molecular switch in wound healing. Blood102: 521-528
https://doi.org/10.1182/blood-2002-07-2248
|
122 |
Wang X, Ira G, Tercero JA, Holmes AM, Diffley JF, Haber JE (2004) Role of DNA replication proteins in double-strand break-induced recombination in Saccharomyces cerevisiae. Mol Cell Biol24: 6891-6899
https://doi.org/10.1128/MCB.24.16.6891-6899.2004
|
123 |
White MF, Dillingham MS (2012) Iron-sulphur clusters in nucleic acid processing enzymes. Curr Opin Struct Biol22: 94-100
https://doi.org/10.1016/j.sbi.2011.11.004
|
124 |
Wu Y, Brosh RM Jr (2012) DNA helicase and helicase-nuclease enzymes with a conserved iron-sulfur cluster. Nucleic Acids Res40: 4247-4260
https://doi.org/10.1093/nar/gks039
|
125 |
Wu H, Li L, Du J, Yuan Y, Cheng X, Ling HQ (2005) Molecular and biochemical characterization of the Fe(III) chelate reductase gene family in Arabidopsis thaliana. Plant Cell Physiol46: 1505-1514
https://doi.org/10.1093/pcp/pci163
|
126 |
Wu Y, Suhasini AN, Brosh RM Jr (2009) Welcome the family of FANCJ-like helicases to the block of genome stability maintenance proteins. Cell Mol Life Sci66: 1209-1222
https://doi.org/10.1007/s00018-008-8580-6
|
127 |
Yamaguchi-Iwai Y, Ueta R, Fukunaka A, Sasaki R (2002) Subcellular localization of Aft1 transcription factor responds to iron status in Saccharomyces cerevisiae. J Biol Chem277: 18914-18918
https://doi.org/10.1074/jbc.M200949200
|
128 |
Yang J, Kim KD, Lucas A, Drahos KE, Santos CS, Mury SP, Capelluto DG, Finkielstein CV (2008) A novel heme-regulatory motif mediates heme-dependent degradation of the circadian factor period 2. Mol Cell Biol28: 4697-4711
https://doi.org/10.1128/MCB.00236-08
|
129 |
Ye H, Rouault TA (2010) Human iron-sulfur cluster assembly, cellular iron homeostasis, and disease. Biochemistry49: 4945-4956
https://doi.org/10.1021/bi1004798
|
130 |
Ye W, Zhang L (2004) Heme controls the expression of cell cycle regulators and cell growth in HeLa cells. Biochem Biophys Res Commun315: 546-554
https://doi.org/10.1016/j.bbrc.2004.01.092
|
131 |
Yu B, Lane ME, Pestell RG, Albanese C, Wadler S (2000) Downregulation of cyclin D1 alters cdk 4- and cdk 2-specific phosphorylation of retinoblastoma protein. Mol Cell Biol Res Commun3: 352-359
https://doi.org/10.1006/mcbr.2000.0238
|
132 |
Yu Y, Kovacevic Z, Richardson DR (2007) Tuning cell cycle regulation with an iron key. Cell Cycle6: 1982-1994
https://doi.org/10.4161/cc.6.16.4603
|
133 |
Yun CW, Ferea T, Rashford J, Ardon O, Brown PO, Botstein D, Kaplan J, Philpott CC (2000a) Desferrioxamine-mediated iron uptake in Saccharomyces cerevisiae. Evidence for two pathways of iron uptake. J Biol Chem275: 10709-10715
https://doi.org/10.1074/jbc.275.14.10709
|
134 |
Yun CW, Tiedeman JS, Moore RE, Philpott CC (2000b) Siderophore-iron uptake in Saccharomyces cerevisiae. Identification of ferrichrome and fusarinine transporters. J Biol Chem275: 16354-16359
https://doi.org/10.1074/jbc.M001456200
|
135 |
Yun CW, Bauler M, Moore RE, Klebba PE, Philpott CC (2001) The role of the FRE family of plasma membrane reductases in the uptake of siderophore-iron in Saccharomyces cerevisiae. J Biol Chem276: 10218-10223
https://doi.org/10.1074/jbc.M010065200
|
136 |
Zhang AS (2010) Control of systemic iron homeostasis by the hemojuvelin-hepcidin axis. Adv Nutr1: 38-45
https://doi.org/10.3945/an.110.1009
|
137 |
Zhang Y, Lyver ER, Nakamaru-Ogiso E, Yoon H, Amutha B, Lee DW, Bi E, Ohnishi T, Daldal F, Pain D (2008) Dre2, a conserved eukaryotic Fe/S cluster protein, functions in cytosolic Fe/S protein biogenesis. Mol Cell Biol28: 5569-5582
https://doi.org/10.1128/MCB.00642-08
|
138 |
Zhang F, Tao Y, Zhang Z, Guo X, An P, Shen Y, Wu Q, Yu Y, Wang F (2012) Metalloreductase Steap3 coordinates the regulation of iron homeostasis and inflammatory responses. Haematologica97: 1826-1835
https://doi.org/10.3324/haematol.2012.063974
|
139 |
Zhang C, Liu G, Huang M (2014a) Ribonucleotide reductase metallocofactor: assembly, maintenance and inhibition. Front Biol9: 104-113
https://doi.org/10.1007/s11515-014-1302-6
|
140 |
Zhang Y, Li H, Zhang C, An X, Liu L, Stubbe J, Huang M (2014) Conserved electron donor complex Dre2-Tah18 is required for ribonucleotide reductase metallocofactor assembly and DNA synthesis. Proceedings of the National Academy of Sciences of the United States of America
|
141 |
Zhao N, Gao J, Enns CA, Knutson MD (2010) ZRT/IRT-like protein 14 (ZIP14) promotes the cellular assimilation of iron from transferrin. J Biol Chem285: 32141-32150
https://doi.org/10.1074/jbc.M110.143248
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|