|
|
|
Ribonucleotide reductase metallocofactor: assembly, maintenance and inhibition |
Caiguo ZHANG,Guoqi LIU,Mingxia HUANG( ) |
| Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, CO 80045, USA |
|
|
|
|
Abstract Ribonucleotide reductase (RNR) supplies cellular deoxyribonucleotide triphosphates (dNTP) pools by converting ribonucleotides to the corresponding deoxy forms using radical-based chemistry. Eukaryotic RNR comprises α and β subunits: α contains the catalytic and allosteric sites; β houses a diferric-tyrosyl radical cofactor (FeIII2-Y•) that is required to initiates nucleotide reduction in α. Cells have evolved multi-layered mechanisms to regulate RNR level and activity in order to maintain the adequate sizes and ratios of their dNTP pools to ensure high-fidelity DNA replication and repair. The central role of RNR in nucleotide metabolism also makes it a proven target of chemotherapeutics. In this review, we discuss recent progress in understanding the function and regulation of eukaryotic RNRs, with a focus on studies revealing the cellular machineries involved in RNR metallocofactor biosynthesis and its implication in RNR-targeting therapeutics.
|
| Keywords
ribonucleotide reductase (RNR)
diferric-tyrosyl radical (FeIII2-Y•)
iron homeostasis
|
|
Corresponding Author(s):
Mingxia HUANG
|
|
Issue Date: 13 May 2014
|
|
| 1 |
AllenJ B, ZhouZ, SiedeW, FriedbergE C, ElledgeS J (1994). The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes Dev, 8(20): 2401–2415
doi: 10.1101/gad.8.20.2401 pmid: 7958905
|
| 2 |
AtkinC L, ThelanderL, ReichardP, LangG (1973). Iron and free radical in ribonucleotide reductase. Exchange of iron and Mössbauer spectroscopy of the protein B2 subunit of the Escherichia coli enzyme. J Biol Chem, 248(21): 7464–7472
pmid: 4355582
|
| 3 |
AyeY, BrignoleE J, LongM J, ChittuluruJ, DrennanC L, AsturiasF J, StubbeJ (2012a). Clofarabine targets the large subunit (α) of human ribonucleotide reductase in live cells by assembly into persistent hexamers. Chem Biol, 19(7): 799–805
doi: 10.1016/j.chembiol.2012.05.015 pmid: 22840768
|
| 4 |
AyeY, LongM J, StubbeJ (2012b). Mechanistic studies of semicarbazone triapine targeting human ribonucleotide reductase in vitro and in mammalian cells: tyrosyl radical quenching not involving reactive oxygen species. J Biol Chem, 287(42): 35768–35778
doi: 10.1074/jbc.M112.396911 pmid: 22915594
|
| 5 |
BarlowT, EliassonR, PlatzA, ReichardP, SjöbergB M (1983). Enzymic modification of a tyrosine residue to a stable free radical in ribonucleotide reductase. Proc Natl Acad Sci USA, 80(6): 1492–1495
doi: 10.1073/pnas.80.6.1492 pmid: 6300856
|
| 6 |
BianchiV, PontisE, ReichardP (1986). Changes of deoxyribonucleoside triphosphate pools induced by hydroxyurea and their relation to DNA synthesis. J Biol Chem, 261(34): 16037–16042
pmid: 3536919
|
| 7 |
BjörklundS, SkogS, TribukaitB, ThelanderL (1990). S-phase-specific expression of mammalian ribonucleotide reductase R1 and R2 subunit mRNAs. Biochemistry, 29(23): 5452–5458
doi: 10.1021/bi00475a007 pmid: 1696835
|
| 8 |
BoehmerP E, LehmanI R (1997). Herpes simplex virus DNA replication. Annu Rev Biochem, 66(1): 347–384
doi: 10.1146/annurev.biochem.66.1.347 pmid: 9242911
|
| 9 |
BollingerJ M Jr, EdmondsonD E, HuynhB H, FilleyJ, NortonJ R, StubbeJ (1991). Mechanism of assembly of the tyrosyl radical-dinuclear iron cluster cofactor of ribonucleotide reductase. Science, 253(5017): 292–298
doi: 10.1126/science. pmid: 1650033
|
| 10 |
BollingerJ M Jr, JiangW, GreenM T, KrebsC (2008). The manganese(IV)/iron(III) cofactor of Chlamydia trachomatis ribonucleotide reductase: structure, assembly, radical initiation, and evolution. Curr Opin Struct Biol, 18(6): 650–657
doi: 10.1016/j.sbi.2008.11.007 pmid: 19046875
|
| 11 |
BollingerJ M Jr, TongW H, RaviN, HuynhB H, EdmondsonD E, StubbeJ A (1995). Use of rapid kinetics methods to study the assembly of the diferric-tyrosyl radical cofactor of E. coli ribonucleotide reductase. Methods Enzymol, 258: 278–303
doi: 10.1016/0076-6879(95)58052-2 pmid: 8524156
|
| 12 |
BrockmanR W, ShaddixS, LasterW R Jr, SchabelF M Jr (1970). Inhibition of ribonucleotide reductase, DNA synthesis, and L1210 leukemia by guanazole. Cancer Res, 30(9): 2358–2368
pmid: 5475481
|
| 13 |
BurrellR A, McClellandS E, EndesfelderD, GrothP, WellerM C, ShaikhN, DomingoE, KanuN, DewhurstS M, GronroosE, ChewS K, RowanA J, SchenkA, ShefferM, HowellM, KschischoM, BehrensA, HelledayT, BartekJ, TomlinsonI P, SwantonC (2013). Replication stress links structural and numerical cancer chromosomal instability. Nature, 494(7438): 492–496
doi: 10.1038/nature11935 pmid: 23446422
|
| 14 |
BussJ L, TortiF M, TortiS V (2003). The role of iron chelation in cancer therapy. Curr Med Chem, 10(12): 1021–1034
doi: 10.2174/0929867033457638 pmid: 12678674
|
| 15 |
CairnsR A, HarrisI S, MakT W (2011). Regulation of cancer cell metabolism. Nat Rev Cancer, 11(2): 85–95
doi: 10.1038/nrc2981 pmid: 21258394
|
| 16 |
CampestreC, AgamennoneM, TortorellaP, PreziusoS, BiasoneA, GavuzzoE, PochettiG, MazzaF, HillerO, TschescheH, ConsalviV, GallinaC (2006). N-Hydroxyurea as zinc binding group in matrix metalloproteinase inhibition: mode of binding in a complex with MMP-8. Bioorg Med Chem Lett, 16(1): 20–24
doi: 10.1016/j.bmcl.2005.09.057 pmid: 16242329
|
| 17 |
CerqueiraN M, FernandesP A, RamosM J (2007). Ribonucleotide reductase: a critical enzyme for cancer chemotherapy and antiviral agents. Recent Patents Anticancer Drug Discov, 2(1): 11–29
doi: 10.2174/157489207779561408 pmid: 18221051
|
| 18 |
ChabesA, GeorgievaB, DomkinV, ZhaoX, RothsteinR, ThelanderL (2003a). Survival of DNA damage in yeast directly depends on increased dNTP levels allowed by relaxed feedback inhibition of ribonucleotide reductase. Cell, 112(3): 391–401
doi: 10.1016/S0092-8674(03)00075-8 pmid: 12581528
|
| 19 |
ChabesA, ThelanderL (2003). DNA building blocks at the foundation of better survival. Cell Cycle, 2(3): 171–173
doi: 10.4161/cc.2.3.354 pmid: 12734415
|
| 20 |
ChabesA L, PflegerC M, KirschnerM W, ThelanderL (2003b). Mouse ribonucleotide reductase R2 protein: a new target for anaphase-promoting complex-Cdh1-mediated proteolysis. Proc Natl Acad Sci USA, 100(7): 3925–3929
doi: 10.1073/pnas.0330774100 pmid: 12655059
|
| 21 |
ChaboutéM E, ClémentB, PhilippsG (2002). S phase and meristem-specific expression of the tobacco RNR1b gene is mediated by an E2F element located in the 5′ leader sequence. J Biol Chem, 277(20): 17845–17851
doi: 10.1074/jbc.M200959200 pmid: 11884409
|
| 22 |
ChaboutéM E, ClémentB, SekineM, PhilippsG, Chaubet-GigotN (2000). Cell cycle regulation of the tobacco ribonucleotide reductase small subunit gene is mediated by E2F-like elements. Plant Cell, 12(10): 1987–2000
pmid: 11041892
|
| 23 |
ChastonT B, LovejoyD B, WattsR N, RichardsonD R (2003). Examination of the antiproliferative activity of iron chelators: multiple cellular targets and the different mechanism of action of triapine compared with desferrioxamine and the potent pyridoxal isonicotinoyl hydrazone analogue 311. Clin Cancer Res, 9(1): 402–414
pmid: 12538494
|
| 24 |
ChastonT B, RichardsonD R (2003). Iron chelators for the treatment of iron overload disease: relationship between structure, redox activity, and toxicity. Am J Hematol, 73(3): 200–210
doi: 10.1002/ajh.10348 pmid: 12827659
|
| 25 |
ClimentI, SjöbergB M, HuangC Y (1991). Carboxyl-terminal peptides as probes for Escherichia coli ribonucleotide reductase subunit interaction: kinetic analysis of inhibition studies. Biochemistry, 30(21): 5164–5171
doi: 10.1021/bi00235a008 pmid: 2036382
|
| 26 |
CotruvoJ A Jr, StubbeJ (2010). An active dimanganese(III)-tyrosyl radical cofactor in Escherichia coli class Ib ribonucleotide reductase. Biochemistry, 49(6): 1297–1309
doi: 10.1021/bi902106n pmid: 20070127
|
| 27 |
CotruvoJ A Jr, StubbeJ (2011). Class I ribonucleotide reductases: metallocofactor assembly and repair in vitro and in vivo. Annu Rev Biochem, 80(1): 733–767
doi: 10.1146/annurev-biochem-061408-095817 pmid: 21456967
|
| 28 |
CovesJ, ZeghoufM, MacherelD, GuigliarelliB, AssoM, FontecaveM (1997). Flavin mononucleotide-binding domain of the flavoprotein component of the sulfite reductase from Escherichia coli. Biochemistry, 36(19): 5921–5928
doi: 10.1021/bi9623744 pmid: 9153434
|
| 29 |
D’AngiolellaV, DonatoV, ForresterF M, JeongY T, PellacaniC, KudoY, SarafA, FlorensL, WashburnM P, PaganoM (2012). Cyclin F-mediated degradation of ribonucleotide reductase M2 controls genome integrity and DNA repair. Cell, 149(5): 1023–1034
doi: 10.1016/j.cell.2012.03.043 pmid: 22632967
|
| 30 |
DaviesB W, KohanskiM A, SimmonsL A, WinklerJ A, CollinsJ J, WalkerG C (2009). Hydroxyurea induces hydroxyl radical-mediated cell death in Escherichia coli. Mol Cell, 36(5): 845–860
doi: 10.1016/j.molcel.2009.11.024 pmid: 20005847
|
| 31 |
DayaniP N, BishopM C, BlackK, ZeltzerP M (2004). Desferoxamine (DFO)—mediated iron chelation: rationale for a novel approach to therapy for brain cancer. J Neurooncol, 67(3): 367–377
doi: 10.1023/B:NEON.0000024238.21349.37 pmid: 15164994
|
| 32 |
DonehowerR C (1992). An overview of the clinical experience with hydroxyurea. Semin Oncol, 19(3 Suppl 9): 11–19
pmid: 1641651
|
| 33 |
EklundH, UhlinU, FärnegårdhM, LoganD T, NordlundP (2001). Structure and function of the radical enzyme ribonucleotide reductase. Prog Biophys Mol Biol, 77(3): 177–268
doi: 10.1016/S0079-6107(01)00014-1 pmid: 11796141
|
| 34 |
ElledgeS J, ZhouZ, AllenJ B, NavasT A (1993). DNA damage and cell cycle regulation of ribonucleotide reductase. BioEssays, 15: 333–339
|
| 35 |
EnyedyE A, PrimikM F, KowolC R, ArionV B, KissT, KepplerB K (2011). Interaction of Triapine and related thiosemicarbazones with iron(III)/(II) and gallium(III): a comparative solution equilibrium study. Dalton Trans, 40(22): 5895–5905
doi: 10.1039/c0dt01835j pmid: 21523301
|
| 36 |
FanH, VillegasC, HuangA, WrightJ A (1998). The mammalian ribonucleotide reductase R2 component cooperates with a variety of oncogenes in mechanisms of cellular transformation. Cancer Res, 58(8): 1650–1653
pmid: 9563477
|
| 37 |
FinchR A, LiuM C, CoryA H, CoryJ G, SartorelliA C (1999). Triapine (3-aminopyridine-2-carboxaldehyde thiosemicarbazone; 3-AP): an inhibitor of ribonucleotide reductase with antineoplastic activity. Adv Enzyme Regul, 39(1): 3–12
doi: 10.1016/S0065-2571(98)00017-X pmid: 10470363
|
| 38 |
FishbeinW N, CarboneP P (1963). Hydroxyurea: Mechanism of Action. Science, 142(3595): 1069–1070
doi: 10.1126/science.142.3595.1069 pmid: 14068223
|
| 39 |
FontecaveM, EliassonR, ReichardP (1987). NAD(P)H:flavin oxidoreductase of Escherichia coli. A ferric iron reductase participating in the generation of the free radical of ribonucleotide reductase. J Biol Chem, 262(25): 12325–12331
pmid: 3305505
|
| 40 |
FontecaveM, EliassonR, ReichardP (1989). Enzymatic regulation of the radical content of the small subunit of Escherichia coli ribonucleotide reductase involving reduction of its redox centers. J Biol Chem, 264(16): 9164–9170
pmid: 2656697
|
| 41 |
FontecaveM, MulliezE, LoganD T (2002). Deoxyribonucleotide synthesis in anaerobic microorganisms: the class III ribonucleotide reductase. Prog Nucleic Acid Res Mol Biol, 72: 95–127
doi: 10.1016/S0079-6603(02)72068-0 pmid: 12206460
|
| 42 |
GwiltP R, TracewellW G (1998). Pharmacokinetics and pharmacodynamics of hydroxyurea. Clin Pharmacokinet, 34(5): 347–358
doi: 10.2165/00003088-199834050-00002 pmid: 9592619
|
| 43 |
HalimiY, DessauM, PollakS, AstT, ErezT, Livnat-LevanonN, KarniolB, HirschJ A, ChamovitzD A (2011). COP9 signalosome subunit 7 from Arabidopsis interacts with and regulates the small subunit of ribonucleotide reductase (RNR2). Plant Mol Biol, 77(1-2): 77–89
doi: 10.1007/s11103-011-9795-8 pmid: 21614643
|
| 44 |
HanahanD, WeinbergR A (2011). Hallmarks of cancer: the next generation. Cell, 144(5): 646–674
doi: 10.1016/j.cell.2011.02.013 pmid: 21376230
|
| 45 |
HaoZ, QiaoT, JinX, LiX, GaoJ, FanD (2005). Preparation and characterization of a specific monoclonal antibody against CIAPIN1. Hybridoma (Larchmt), 24(3): 141–145
doi: 10.1089/hyb.2005.24.141 pmid: 15943561
|
| 46 |
HarperJ W, ElledgeS J (2007). The DNA damage response: ten years after. Mol Cell, 28(5): 739–745
doi: 10.1016/j.molcel.2007.11.015 pmid: 18082599
|
| 47 |
HaunhorstP, HanschmannE M, BräutigamL, StehlingO, HoffmannB, MühlenhoffU, LillR, BerndtC, LilligC H (2013). Crucial function of vertebrate glutaredoxin 3 (PICOT) in iron homeostasis and hemoglobin maturation. Mol Biol Cell, 24(12): 1895–1903
doi: 10.1091/mbc.E12-09-0648 pmid: 23615448
|
| 48 |
HoferA, CronaM, LoganD T, SjöbergB M (2012). DNA building blocks: keeping control of manufacture. Crit Rev Biochem Mol Biol, 47(1): 50–63
doi: 10.3109/10409238.2011.630372 pmid: 22050358
|
| 49 |
HristovaD, WuC H, JiangW, KrebsC, StubbeJ (2008). Importance of the maintenance pathway in the regulation of the activity of Escherichia coli ribonucleotide reductase. Biochemistry, 47(13): 3989–3999
doi: 10.1021/bi702408k pmid: 18314964
|
| 50 |
HuC M, YehM T, TsaoN, ChenC W, GaoQ Z, ChangC Y, LeeM H, FangJ M, SheuS Y, LinC J, TsengM C, ChenY J, ChangZ F (2012). Tumor cells require thymidylate kinase to prevent dUTP incorporation during DNA repair. Cancer Cell, 22(1): 36–50
doi: 10.1016/j.ccr.2012.04.038 pmid: 22789537
|
| 51 |
HuangM, ElledgeS J (1997). Identification of RNR4, encoding a second essential small subunit of ribonucleotide reductase in Saccharomyces cerevisiae. Mol Cell Biol, 17(10): 6105–6113
pmid: 9315670
|
| 52 |
JiangW, YunD, SalehL, BarrE W, XingG, HoffartL M, MaslakM A, KrebsC, BollingerJ M Jr (2007). A manganese(IV)/iron(III) cofactor in Chlamydia trachomatis ribonucleotide reductase. Science, 316(5828): 1188–1191
doi: 10.1126/science.1141179 pmid: 17525338
|
| 53 |
JohnsD G, GaoW Y (1998). Selective depletion of DNA precursors: an evolving strategy for potentiation of dideoxynucleoside activity against human immunodeficiency virus. Biochem Pharmacol, 55(10): 1551–1556
pmid: 9633990
|
| 54 |
JordanA, ReichardP (1998). Ribonucleotide reductases. Annu Rev Biochem, 67(1): 71–98
doi: 10.1146/annurev.biochem.67.1.71 pmid: 9759483
|
| 55 |
KaplanJ, McVey WardD, CrispR J, PhilpottC C (2006). Iron-dependent metabolic remodeling in S. cerevisiae. Biochim Biophys Acta, 1763(7): 646–651
doi: 10.1016/j.bbamcr.2006.03.008 pmid: 16697062
|
| 56 |
KashlanO B, CoopermanB S (2003). Comprehensive model for allosteric regulation of mammalian ribonucleotide reductase: refinements and consequences. Biochemistry, 42(6): 1696–1706
doi: 10.1021/bi020634d pmid: 12578384
|
| 57 |
KeP Y, KuoY Y, HuC M, ChangZ F (2005). Control of dTTP pool size by anaphase promoting complex/cyclosome is essential for the maintenance of genetic stability. Genes Dev, 19(16): 1920–1933
doi: 10.1101/gad.1322905 pmid: 16103219
|
| 58 |
KennedyB J (1992). The evolution of hydroxyurea therapy in chronic myelogenous leukemia. Semin Oncol, 19(3 Suppl 9): 21–26
pmid: 1641653
|
| 59 |
KolbergM, StrandK R, GraffP, AnderssonK K (2004). Structure, function, and mechanism of ribonucleotide reductases. Biochim Biophys Acta, 1699(1-2): 1–34
doi: 10.1016/j.bbapap.2004.02.007 pmid: 15158709
|
| 60 |
KumarD, VibergJ, NilssonA K, ChabesA (2010). Highly mutagenic and severely imbalanced dNTP pools can escape detection by the S-phase checkpoint. Nucleic Acids Res, 38(12): 3975–3983
doi: 10.1093/nar/gkq128 pmid: 20215435
|
| 61 |
KunkelT A, SilberJ R, LoebL A (1982). The mutagenic effect of deoxynucleotide substrate imbalances during DNA synthesis with mammalian DNA polymerases. Mutat Res, 94(2): 413–419
doi: 10.1016/0027-5107(82)90304-9 pmid: 6213856
|
| 62 |
KunosC, RadivoyevitchT, Abdul-KarimF W, FanningJ, AbulafiaO, BonebrakeA J, UshaL (2012). Ribonucleotide reductase inhibition restores platinum-sensitivity in platinum-resistant ovarian cancer: a Gynecologic Oncology Group Study. J Transl Med, 10(1): 79
doi: 10.1186/1479-5876-10-79 pmid: 22541066
|
| 63 |
KuritaJ, NakajimaK (2012). Megalocytiviruses. Viruses, 4(4): 521–538
doi: 10.3390/v4040521 pmid: 22590684
|
| 64 |
LassmannG, ThelanderL, GräslundA (1992). EPR stopped-flow studies of the reaction of the tyrosyl radical of protein R2 from ribonucleotide reductase with hydroxyurea. Biochem Biophys Res Commun, 188(2): 879–887
doi: 10.1016/0006-291X(92)91138-G pmid: 1332707
|
| 65 |
LeeY D, WangJ, StubbeJ, ElledgeS J (2008). Dif1 is a DNA-damage-regulated facilitator of nuclear import for ribonucleotide reductase. Mol Cell, 32(1): 70–80
doi: 10.1016/j.molcel.2008.08.018 pmid: 18851834
|
| 66 |
LillR, HoffmannB, MolikS, PierikA J, RietzschelN, StehlingO, UzarskaM A, WebertH, WilbrechtC, MühlenhoffU (2012). The role of mitochondria in cellular iron-sulfur protein biogenesis and iron metabolism. Biochim Biophys Acta, 1823(9): 1491–1508
doi: 10.1016/j.bbamcr.2012.05.009 pmid: 22609301
|
| 67 |
LiuC, PowellK A, MundtK, WuL, CarrA M, CaspariT (2003). Cop9/signalosome subunits and Pcu4 regulate ribonucleotide reductase by both checkpoint-dependent and-independent mechanisms. Genes Dev, 17(9): 1130–1140
doi: 10.1101/gad.1090803 pmid: 12695334
|
| 68 |
LiuX, ZhouB, XueL, YenF, ChuP, UnF, YenY (2007). Ribonucleotide reductase subunits M2 and p53R2 are potential biomarkers for metastasis of colon cancer. Clin Colorectal Cancer, 6(5): 374–381
doi: 10.3816/CCC.2007.n.007 pmid: 17311703
|
| 69 |
LoebL A, KunkelT A (1982). Fidelity of DNA synthesis. Annu Rev Biochem, 51(1): 429–457
doi: 10.1146/annurev.bi.51.070182.002241 pmid: 6214209
|
| 70 |
LoganD T, MulliezE, LarssonK M, BodevinS, AttaM, GarnaudP E, SjobergB M, FontecaveM (2003). A metal-binding site in the catalytic subunit of anaerobic ribonucleotide reductase. Proc Natl Acad Sci USA, 100(7): 3826–3831
doi: 10.1073/pnas.0736456100 pmid: 12655046
|
| 71 |
LovejoyD B, RichardsonD R (2003). Iron chelators as anti-neoplastic agents: current developments and promise of the PIH class of chelators. Curr Med Chem, 10(12): 1035–1049
doi: 10.2174/0929867033457557 pmid: 12678675
|
| 72 |
MadaanK, KaushikD, VermaT (2012). Hydroxyurea: a key player in cancer chemotherapy. Expert Rev Anticancer Ther, 12(1): 19–29
doi: 10.1586/era.11.175 pmid: 22149429
|
| 73 |
MathewsC K (2006). DNA precursor metabolism and genomic stability. FASEB J, 20: 1300–1314
|
| 74 |
MayhewC N, SumpterR, InayatM, CibullM, PhillipsJ D, ElfordH L, GallicchioV S (2005). Combination of inhibitors of lymphocyte activation (hydroxyurea, trimidox, and didox) and reverse transcriptase (didanosine) suppresses development of murine retrovirus-induced lymphoproliferative disease. Antiviral Res, 65(1): 13–22
doi: 10.1016/j.antiviral.2004.09.003 pmid: 15652967
|
| 75 |
MinnihanE C, AndoN, BrignoleE J, OlshanskyL, ChittuluruJ, AsturiasF J, DrennanC L, NoceraD G, StubbeJ (2013a). Generation of a stable, aminotyrosyl radical-induced α2β2 complex of Escherichia coli class Ia ribonucleotide reductase. Proc Natl Acad Sci USA, 110(10): 3835–3840
doi: 10.1073/pnas.1220691110 pmid: 23431160
|
| 76 |
MinnihanE C, NoceraD G, StubbeJ (2013b). Reversible, long-range radical transfer in E. coli class Ia ribonucleotide reductase. Acc Chem Res, 46(11): 2524–2535
doi: 10.1021/ar4000407 pmid: 23730940
|
| 77 |
MiyajimaH, TakahashiY, KamataT, ShimizuH, SakaiN, GitlinJ D (1997). Use of desferrioxamine in the treatment of aceruloplasminemia. Ann Neurol, 41(3): 404–407
doi: 10.1002/ana.410410318 pmid: 9066364
|
| 78 |
MowaM B, WarnerD F, KaplanG, KanaB D, MizrahiV (2009). Function and regulation of class I ribonucleotide reductase-encoding genes in mycobacteria. J Bacteriol, 191(3): 985–995
doi: 10.1128/JB.01409-08 pmid: 19028890
|
| 79 |
MühlenhoffU, MolikS, GodoyJ R, UzarskaM A, RichterN, SeubertA, ZhangY, StubbeJ, PierrelF, HerreroE, LilligC H, LillR (2010). Cytosolic monothiol glutaredoxins function in intracellular iron sensing and trafficking via their bound iron-sulfur cluster. Cell Metab, 12(4): 373–385
doi: 10.1016/j.cmet.2010.08.001 pmid: 20889129
|
| 80 |
NakanoK, BálintE, AshcroftM, VousdenK H (2000). A ribonucleotide reductase gene is a transcriptional target of p53 and p73. Oncogene, 19(37): 4283–4289
doi: 10.1038/sj.onc.1203774 pmid: 10980602
|
| 81 |
NetzD J, StümpfigM, DoréC, MühlenhoffU, PierikA J, LillR (2010). Tah18 transfers electrons to Dre2 in cytosolic iron-sulfur protein biogenesis. Nat Chem Biol, 6(10): 758–765
doi: 10.1038/nchembio.432 pmid: 20802492
|
| 82 |
NiidaH, KatsunoY, SengokuM, ShimadaM, YukawaM, IkuraM, IkuraT, KohnoK, ShimaH, SuzukiH, TashiroS, NakanishiM (2010). Essential role of Tip60-dependent recruitment of ribonucleotide reductase at DNA damage sites in DNA repair during G1 phase. Genes Dev, 24(4): 333–338
doi: 10.1101/gad.1863810 pmid: 20159953
|
| 83 |
NordlundP, ReichardP (2006). Ribonucleotide reductases. Annu Rev Biochem, 75(1): 681–706
doi: 10.1146/annurev.biochem.75.103004.142443 pmid: 16756507
|
| 84 |
NyholmS, ThelanderL, GräslundA (1993). Reduction and loss of the iron center in the reaction of the small subunit of mouse ribonucleotide reductase with hydroxyurea. Biochemistry, 32(43): 11569–11574
doi: 10.1021/bi00094a013 pmid: 8218224
|
| 85 |
OffenbacherA R, VassilievI R, SeyedsayamdostM R, StubbeJ, BarryB A (2009). Redox-linked structural changes in ribonucleotide reductase. J Am Chem Soc, 131(22): 7496–7497
doi: 10.1021/ja901908j pmid: 19489635
|
| 86 |
OrmöM, deMaréF, RegnströmK, AbergA, SahlinM, LingJ, LoehrT M, Sanders-LoehrJ, SjöbergB M (1992). Engineering of the iron site in ribonucleotide reductase to a self-hydroxylating monooxygenase. J Biol Chem, 267(13): 8711–8714
pmid: 1577712
|
| 87 |
OrtigosaA D, HristovaD, PerlsteinD L, ZhangZ, HuangM, StubbeJ (2006). Determination of the in vivo stoichiometry of tyrosyl radical per betabeta’ in Saccharomyces cerevisiae ribonucleotide reductase. Biochemistry, 45(40): 12282–12294
doi: 10.1021/bi0610404 pmid: 17014081
|
| 88 |
PollycoveM, MaqsoodM (1962). Existence of an erythropoietic labile iron pool in animals. Nature, 194(4824): 152–154
doi: 10.1038/194152a0 pmid: 14487670
|
| 89 |
Pujol-CarrionN, BelliG, HerreroE, NoguesA, de la Torre-RuizM A (2006). Glutaredoxins Grx3 and Grx4 regulate nuclear localisation of Aft1 and the oxidative stress response in Saccharomyces cerevisiae. J Cell Sci, 119(Pt 21): 4554–4564
doi: 10.1242/jcs.03229 pmid: 17074835
|
| 90 |
ReeceS Y, HodgkissJ M, StubbeJ, NoceraD G (2006). Proton-coupled electron transfer: the mechanistic underpinning for radical transport and catalysis in biology. Philos Trans R Soc Lond B Biol Sci, 361(1472): 1351–1364
doi: 10.1098/rstb.2006.1874 pmid: 16873123
|
| 91 |
ReichardP (1988). Interactions between deoxyribonucleotide and DNA synthesis. Annu Rev Biochem, 57(1): 349–374
doi: 10.1146/annurev.bi.57.070188.002025 pmid: 3052277
|
| 92 |
ReichardP (1993). From RNA to DNA, why so many ribonucleotide reductases? Science, 260(5115): 1773–1777
doi: 10.1126/science. pmid: 8511586
|
| 93 |
RenS, WangR, KomatsuK, Bonaz-KrauseP, ZyrianovY, McKennaC E, CsipkeC, TokesZ A, LienE J (2002). Synthesis, biological evaluation, and quantitative structure-activity relationship analysis of new Schiff bases of hydroxysemicarbazide as potential antitumor agents. J Med Chem, 45(2): 410–419
doi: 10.1021/jm010252q pmid: 11784145
|
| 94 |
RichardsonD R, KalinowskiD S, RichardsonV, SharpeP C, LovejoyD B, IslamM, BernhardtP V (2009). 2-Acetylpyridine thiosemicarbazones are potent iron chelators and antiproliferative agents: redox activity, iron complexation and characterization of their antitumor activity. J Med Chem, 52(5): 1459–1470
doi: 10.1021/jm801585u pmid: 19216562
|
| 95 |
RofougaranR, VodnalaM, HoferA (2006). Enzymatically active mammalian ribonucleotide reductase exists primarily as an alpha6beta2 octamer. J Biol Chem, 281(38): 27705–27711
doi: 10.1074/jbc.M605573200 pmid: 16861739
|
| 96 |
RouaultT, KlausnerR (1997). Regulation of iron metabolism in eukaryotes. Curr Top Cell Regul, 35: 1–19
doi: 10.1016/S0070-2137(97)80001-5 pmid: 9192174
|
| 97 |
SaitoY, ShibayamaH, TanakaH, TanimuraA, MatsumuraI, KanakuraY (2011). PICOT is a molecule which binds to anamorsin. Biochem Biophys Res Commun, 408(2): 329–333
doi: 10.1016/j.bbrc.2011.04.033 pmid: 21513700
|
| 98 |
SaldivarJ C, MiumaS, BeneJ, HosseiniS A, ShibataH, SunJ, WheelerL J, MathewsC K, HuebnerK (2012). Initiation of genome instability and preneoplastic processes through loss of Fhit expression. PLoS Genet, 8(11): e1003077
doi: 10.1371/journal.pgen.1003077 pmid: 23209436
|
| 99 |
SaloweS, BollingerJ M Jr, AtorM, StubbeJ, McCrakenJ, PeisachJ, SamanoM C, RobinsM J (1993). Alternative model for mechanism-based inhibition of Escherichia coli ribonucleotide reductase by 2′-azido-2′-deoxyuridine 5′-diphosphate. Biochemistry, 32(47): 12749–12760
doi: 10.1021/bi00210a026 pmid: 8251496
|
| 100 |
SanvisensN, de LlanosR, PuigS (2013). Function and regulation of yeast ribonucleotide reductase: cell cycle, genotoxic stress, and iron bioavailability. Biomed J, 36: 51–58
|
| 101 |
ScozzafavaA, SupuranC T (2003). Hydroxyurea is a carbonic anhydrase inhibitor. Bioorg Med Chem, 11(10): 2241–2246
doi: 10.1016/S0968-0896(03)00112-3 pmid: 12713833
|
| 102 |
ShaoJ, LiuX, ZhuL, YenY (2013). Targeting ribonucleotide reductase for cancer therapy. Expert Opin Ther Targets, 17(12): 1423–1437
doi: 10.1517/14728222.2013.840293 pmid: 24083455
|
| 103 |
ShaoJ, ZhouB, Di BilioA J, ZhuL, WangT, QiC, ShihJ, YenY (2006). A Ferrous-Triapine complex mediates formation of reactive oxygen species that inactivate human ribonucleotide reductase. Mol Cancer Ther, 5(3): 586–592
doi: 10.1158/1535-7163.MCT-05-0384 pmid: 16546972
|
| 104 |
ShaoJ, ZhouB, ZhuL, QiuW, YuanY C, XiB, YenY (2004). In vitro characterization of enzymatic properties and inhibition of the p53R2 subunit of human ribonucleotide reductase. Cancer Res, 64(1): 1–6
doi: 10.1158/0008-5472.CAN-03-3048 pmid: 14729598
|
| 105 |
ShibayamaH, TakaiE, MatsumuraI, KounoM, MoriiE, KitamuraY, TakedaJ, KanakuraY (2004). Identification of a cytokine-induced antiapoptotic molecule anamorsin essential for definitive hematopoiesis. J Exp Med, 199(4): 581–592
doi: 10.1084/jem.20031858 pmid: 14970183
|
| 106 |
SjöbergB M, ReichardP (1977). Nature of the free radical in ribonucleotide reductase from Escherichia coli. J Biol Chem, 252(2): 536–541
pmid: 188819
|
| 107 |
SongS, PursellZ F, CopelandW C, LongleyM J, KunkelT A, MathewsC K (2005). DNA precursor asymmetries in mammalian tissue mitochondria and possible contribution to mutagenesis through reduced replication fidelity. Proc Natl Acad Sci USA, 102(14): 4990–4995
doi: 10.1073/pnas.0500253102 pmid: 15784738
|
| 108 |
SouglakosJ, BoukovinasI, TaronM, MendezP, MavroudisD, TripakiM, HatzidakiD, KoutsopoulosA, StathopoulosE, GeorgouliasV, RosellR (2008). Ribonucleotide reductase subunits M1 and M2 mRNA expression levels and clinical outcome of lung adenocarcinoma patients treated with docetaxel/gemcitabine. Br J Cancer, 98(10): 1710–1715
doi: 10.1038/sj.bjc.6604344 pmid: 18414411
|
| 109 |
StubbeJ (2003). Di-iron-tyrosyl radical ribonucleotide reductases. Curr Opin Chem Biol, 7(2): 183–188
doi: 10.1016/S1367-5931(03)00025-5 pmid: 12714050
|
| 110 |
StubbeJ, CotruvoJ A Jr (2011). Control of metallation and active cofactor assembly in the class Ia and Ib ribonucleotide reductases: diiron or dimanganese? Curr Opin Chem Biol, 15(2): 284–290
doi: 10.1016/j.cbpa.2010.12.001 pmid: 21216656
|
| 111 |
StubbeJ, GeJ, YeeC S (2001). The evolution of ribonucleotide reduction revisited. Trends Biochem Sci, 26(2): 93–99
doi: 10.1016/S0968-0004(00)01764-3 pmid: 11166566
|
| 112 |
StubbeJ, van Der DonkW A (1998). Protein Radicals in Enzyme Catalysis. Chem Rev, 98(2): 705–762
doi: 10.1021/cr9400875 pmid: 11848913
|
| 113 |
TanakaH, ArakawaH, YamaguchiT, ShiraishiK, FukudaS, MatsuiK, TakeiY, NakamuraY (2000). A ribonucleotide reductase gene involved in a p53-dependent cell-cycle checkpoint for DNA damage. Nature, 404(6773): 42–49
doi: 10.1038/35003506 pmid: 10716435
|
| 114 |
ThelanderL, GräslundA, ThelanderM (1983). Continual presence of oxygen and iron required for mammalian ribonucleotide reduction: possible regulation mechanism. Biochem Biophys Res Commun, 110(3): 859–865
doi: 10.1016/0006-291X(83)91040-9 pmid: 6340669
|
| 115 |
WangJ, LohmanG J, StubbeJ (2007). Enhanced subunit interactions with gemcitabine-5′-diphosphate inhibit ribonucleotide reductases. Proc Natl Acad Sci USA, 104(36): 14324–14329
doi: 10.1073/pnas.0706803104 pmid: 17726094
|
| 116 |
WhiteM F, DillinghamM S (2012). Iron-sulphur clusters in nucleic acid processing enzymes. Curr Opin Struct Biol, 22(1): 94–100
doi: 10.1016/j.sbi.2011.11.004 pmid: 22169085
|
| 117 |
WillingA, FollmannH, AulingG (1988). Ribonucleotide reductase of Brevibacterium ammoniagenes is a manganese enzyme. Eur J Bio, 170: 603–611
|
| 118 |
WuC H, JiangW, KrebsC, StubbeJ (2007). YfaE, a ferredoxin involved in diferric-tyrosyl radical maintenance in Escherichia coli ribonucleotide reductase. Biochemistry, 46(41): 11577–11588
doi: 10.1021/bi7012454 pmid: 17880186
|
| 119 |
WuX, HuangM (2008). Dif1 controls subcellular localization of ribonucleotide reductase by mediating nuclear import of the R2 subunit. Mol Cell Biol, 28(23): 7156–7167
doi: 10.1128/MCB.01388-08 pmid: 18838542
|
| 120 |
XueL, ZhouB, LiuX, QiuW, JinZ, YenY (2003). Wild-type p53 regulates human ribonucleotide reductase by protein-protein interaction with p53R2 as well as hRRM2 subunits. Cancer Res, 63(5): 980–986
pmid: 12615712
|
| 121 |
YangF D, SpanevelloR A, CelikerI, HirschmannR, RubinH, CoopermanB S (1990). The carboxyl terminus heptapeptide of the R2 subunit of mammalian ribonucleotide reductase inhibits enzyme activity and can be used to purify the R1 subunit. FEBS Lett, 272(1-2): 61–64
doi: 10.1016/0014-5793(90)80449-S pmid: 2226836
|
| 122 |
YaoR, ZhangZ, AnX, BucciB, PerlsteinD L, StubbeJ, HuangM (2003). Subcellular localization of yeast ribonucleotide reductase regulated by the DNA replication and damage checkpoint pathways. Proc Natl Acad Sci USA, 100(11): 6628–6633
doi: 10.1073/pnas.1131932100 pmid: 12732713
|
| 123 |
YeH, RouaultT A (2010). Human iron-sulfur cluster assembly, cellular iron homeostasis, and disease. Biochemistry, 49(24): 4945–4956
doi: 10.1021/bi1004798 pmid: 20481466
|
| 124 |
YenY, GrillS P, DutschmanG E, ChangC N, ZhouB S, ChengY C (1994). Characterization of a hydroxyurea-resistant human KB cell line with supersensitivity to 6-thioguanine. Cancer Res, 54(14): 3686–3691
pmid: 7518343
|
| 125 |
YuY, WongJ, LovejoyD B, KalinowskiD S, RichardsonD R (2006). Chelators at the cancer coalface: desferrioxamine to Triapine and beyond. Clin Cancer Res, 12(23): 6876–6883
doi: 10.1158/1078-0432.CCR-06-1954 pmid: 17145804
|
| 126 |
ZeidnerJ F, KarpJ E, BlackfordA L, SmithB D, GojoI, GoreS D, LevisM J, CarrawayH E, GreerJ M, IvyS P, PratzK W, McDevittM A (2013). Phase II trial of sequential ribonucleotide reductase inhibition in aggressive myeloproliferative neoplasms. Haematologica,
doi: 10.3324/haematol.2013.097246 pmid: 24362550
|
| 127 |
ZhangY, LiuL, WuX, AnX, StubbeJ, HuangM (2011). Investigation of in vivo diferric tyrosyl radical formation in Saccharomyces cerevisiae Rnr2 protein: requirement of Rnr4 and contribution of Grx3/4 AND Dre2 proteins. J Biol Chem, 286(48): 41499–41509
doi: 10.1074/jbc.M111.294074 pmid: 21931161
|
| 128 |
ZhangY, LyverE R, Nakamaru-OgisoE, YoonH, AmuthaB, LeeD W, BiE, OhnishiT, DaldalF, PainD, DancisA (2008). Dre2, a conserved eukaryotic Fe/S cluster protein, functions in cytosolic Fe/S protein biogenesis. Mol Cell Biol, 28(18): 5569–5582
doi: 10.1128/MCB.00642-08 pmid: 18625724
|
| 129 |
ZhaoX, ChabesA, DomkinV, ThelanderL, RothsteinR (2001). The ribonucleotide reductase inhibitor Sml1 is a new target of the Mec1/Rad53 kinase cascade during growth and in response to DNA damage. EMBO J, 20(13): 3544–3553
doi: 10.1093/emboj/20.13.3544 pmid: 11432841
|
| 130 |
ZuckermanJ E, HsuehT, KoyaR C, DavisM E, RibasA (2011). siRNA knockdown of ribonucleotide reductase inhibits melanoma cell line proliferation alone or synergistically with temozolomide. J Invest Dermatol, 131(2): 453–460
doi: 10.1038/jid.2010.310 pmid: 20944646
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
