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Cooperation of Two mRNA-Binding Proteins Drives Metabolic Adaptation to Iron Deficiency
Open accessAbstract
Iron (Fe) is an essential cofactor for a wide range of cellular processes. We have previously demonstrated in yeast that Cth2 is expressed during Fe deficiency and promotes degradation of a battery of mRNAs leading to reprogramming of Fe-dependent metabolism and Fe storage. We report here that the Cth2-homologous protein Cth1 is transiently expressed during Fe deprivation and participates in the response to Fe deficiency through the degradation of mRNAs primarily involved in mitochondrially localized activities including respiration and amino acid biosynthesis. In parallel, wild-type cells, but not cth1Deltacth2Delta cells, accumulate mRNAs encoding proteins that function in glucose import and storage and store high levels of glycogen. In addition, Fe deficiency leads to phosphorylation of Snf1, an AMP-activated protein kinase family member required for the cellular response to glucose starvation. These studies demonstrate a metabolic reprogramming as a consequence of Fe starvation that is dependent on the coordinated activities of two mRNA-binding proteins.
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“Under iron limitation, yeast cells lacking the iron-regulated RNA-binding protein Cth2 display high mRNA levels of multiple ERG genes including those of the first steps of the late stage of synthesis (ERG1, ERG7, ERG11 and DAP1) [116,118].”
From Regulation of Ergosterol Biosynthesis in Saccharomyces cerevisiae (2020) · cites this paper as [118]
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Metalloproteins and metal sensing
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HapX-Mediated Adaption to Iron Starvation Is Crucial for Virulence of Aspergillus fumigatus
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mTOR regulates cellular iron homeostasis through tristetraprolin
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Outten, C. E., & Albetel, A. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.07.020 · Cited by 129
The Iron Metallome in Eukaryotic Organisms
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“Interestingly, expressing CTH1 from the CTH2 promoter rescues significantly the growth defect of cth1Δcth2Δ [33].”
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“…once cells encounter Fe deficiency, two CCCH Zn finger proteins (Cth1 and Cth2) are expressed to specifically degrade RNA molecules encoding proteins involved in Fe-dependent pathways, but the Cth1/Cth2 mechanism has not been revealed in other pathogenic fungi (Puig et al., 2005; 2008).”
BackgroundIron Regulatory Mechanisms in Saccharomyces cerevisiae
Ramos-Alonso, L., Romero, A. M., Martínez‐Pastor, M. T., & Puig, S. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.582830 · Cited by 95
“Cth2 amino-terminal region is important for both AMD and translation repression, whereas its carboxy-terminal domain is only required to inhibit protein synthesis (Ramos-Alonso et al., 2018a, 2019).”
BackgroundConserved and Divergent Roles of Bcr1 and CFEM Proteins in Candida parapsilosis and Candida albicans
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BackgroundRegulation of Ribonucleotide Reductase in Response to Iron Deficiency
Sanvisens, N., Bañó, M. C., Huang, M., & Puig, S. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.09.021 · Cited by 92
“cerevisiae promotes the replacement of Fe-dependent processes including glutamate synthase, biotin synthesis and respiration with Fe-independent alternatives when Fe becomes scarce (Puig et al., 2008; Shakoury-Elizeh et al., 2004).”
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Iron and Neurodegeneration: From Cellular Homeostasis to Disease
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“Moreover, cells are able to spare Fe through the regulation of Tis11 homologues and Cth1/2-mediated degradation of mRNAs coding for Fe-binding proteins, thereby facilitating the utilization of limited cellular Fe levels [81, 82].”
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Bresson, S. M., Tuck, A., Staneva, D. P., & Tollervey, D. W. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.01.005 · Cited by 69
“Tye7 is a transcription factor for the glycolytic gene ENO1 (Sato et al., 1999), whereas Cth1 is an RNA decay factor that targets genes involved in oxidative phosphorylation (Puig et al., 2008).”
BackgroundDissecting plant iron homeostasis under short and long-term iron fluctuations
Darbani, B., Briat, J., Holm, P. B., Husted, S., Noeparvar, S., & Borg, S. (2013) · Biotechnology Advances · doi:10.1016/j.biotechadv.2013.05.003 · Cited by 68
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“Two of the Aft1 targets code for the RNA-binding proteins Cth1 and Cth2, that posttranscriptionally downregulate many mRNAs involved in Fe-dependent processes [9,12].”
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Qu, J., Kang, S. G., Wang, W., Musier‐Forsyth, K., & Jang, J.-C. (2014) · The Plant Journal · doi:10.1111/tpj.12485 · Cited by 61
“Therefore, they play significant roles in iron homeostasis by modulating cellular metabolism in response to iron deficiency (Puig et al., 2008).”
InfluentialCellular sensing and transport of metal ions: implications in micronutrient homeostasis
Bird, A. J. (2015) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2015.08.002 · Cited by 60
“Thus, by increasing the expression of CTH1 and CTH2 in low iron, Aft1 is able to indirectly control the levels of a large number of mRNAs that are involved in iron metabolism thereby adjusting iron utilization according to the cells iron status.”
BackgroundInfluentialEndoplasmic reticulum–mitochondria junction is required for iron homeostasis
Xue, Y., Schmollinger, S., Attar, N., Campos, O. A., Vogelauer, M., Carey, M., Merchant, S., & Kurdistani, S. K. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.784249 · Cited by 58
“The transcriptional response to iron deficiency also involves activation of genes such as CTH2, which is involved in mediating the metabolic acclimation to iron deficiency by sparing iron use, and genes involved in iron-independent pathways such as glutamate dehydrogenase GDH3 (30, 32, 33).”
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Puig, S., de Llanos, R., & Sanvisens, N. (2013) · Biomedical Journal · doi:10.4103/2319-4170.110398 · Cited by 54
Hammering out details: regulating metal levels in eukaryotes
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The yeast CLC protein counteracts vesicular acidification during iron starvation
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“Interestingly, iron starvation leads to major remodelling of carbohydrate metabolism, with a shift away from oxidative phosphorylation (Puig et al., 2008).”
BackgroundAdaptation to iron deficiency in human pathogenic fungi
Martínez‐Pastor, M. T., & Puig, S. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2020.118797 · Cited by 47
A novel hybrid iron regulation network combines features from pathogenic and nonpathogenic yeasts
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“Under iron-deprived conditions, the Fe/S protein Ilv3, which is crucial for -IPM production (25), is inactive due to the lack of its cofactor and the ILV3 mRNA is the target of the Cth proteins (38).”
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“In response to iron deficiency, cells activate transcription of CTH1 transiently and of CTH2 persistently, which target specific mRNA degradation leading to metabolic reprogramming of iron utilization and iron storage (39, 40).”
BackgroundYeast Dun1 Kinase Regulates Ribonucleotide Reductase Inhibitor Sml1 in Response to Iron Deficiency
Sanvisens, N., Romero, A. M., An, X., Zhang, C., de Llanos, R., Martínez‐Pastor, M. T., Bañó, M. C., Huang, M., & Puig, S. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.00472-14 · Cited by 40
“Upon Fe limitation, the RNA-binding proteins Cth1 and Cth2 posttranscriptionally activate the downregulation of multiple Fe-dependent processes, including the Wtm1 RNR nuclear anchor (35, 36, 52).”
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“protein was previously observed in wild-type cells during Fe deficiency (20), FLAG-Cth1 protein levels are induced by Fe deficiency and sustained in cells that do not express Cth2 (Fig.”
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“Cth1p/cth2p proteins preferentially bind to AU-rich elements (AREs) and then destabilize the mRNAs of iron-requiring proteins, thus salvaging iron for use in essential functions[34].”
BackgroundWar-Fe-re: iron at the core of fungal virulence and host immunity
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“superfamily (Fig. 2a) ( Philpott and Protchenko 2008 ).”
BackgroundInfluentialRegulatory and pathogenic mechanisms in response to iron deficiency and excess in fungi
Pijuan, J., Moreno, D. F., Yahya, G., Moisa, M., Ul Haq, I., Krukiewicz, K., Mosbah, R., Metwally, K., & Cavalu, S. (2023) · Microbial Biotechnology · doi:10.1111/1751-7915.14346 · Cited by 37
“• Enzymes of the tricarboxylic acid (TCA) cycle and respiratory chain, such as succinate dehydrogenase, aconitase, isocitrate dehydrogenase, and alpha-ketoglutarate dehydrogenase (Puig et al., 2005, 2008).”
BackgroundInfluentialWhen less is more: novel mechanisms of iron conservation
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“In addition, accumulation of protoporphyrin IX (PPIX), an unmetallated precursor of heme, induces significant oxidative damage to the cell [36].”
InfluentialThe oxidative stress response in yeast cells involves changes in the stability of Aft1 regulon mRNAs
Castells‐Roca, L., Mühlenhoff, U., Lill, R., Herrero, E., & Bellı́, G. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07689.x · Cited by 37
“In these same conditions, Cth1 preferentially affects the stability of mRNAs for mitochondrial activities involved in respiration and amino acid biosynthesis (Puig et al., 2008).”
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“Previous studies have shown that iron deficiency promotes the phosphorylation of Snf1 [61], but no evidence for changes in Snf1 phosphorylation stage have been reported in excess iron.”
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“We also constructed a second network that excluded molecular interactions derived from genomics data from this and other studies [11,22] [see Additional file 16].”
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Hepatic tristetraprolin promotes insulin resistance through RNA destabilization of FGF21
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Signaling pathways governing iron homeostasis in budding yeast
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Air proteins control differential TRAMP substrate specificity for nuclear RNA surveillance
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“CgYap5 binds and controls the expression of several genes encoding iron-containing proteins (CgRLI1, CgACO1, CgGLT1, CgSDH2, CgTYW1), the vacuolar iron transporter CgCcc1, the Fe-S cluster assembly factor CgIsa1, the rate-limiting enzyme in haem biosynthesis CgHem3 and the glutaredoxin CgGrx4 [113, 171].”
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“Yeast also respond to low iron by reducing the need for iron-requiring proteins (summarized in [28, 29]), a response achieved by targeted decay of mRNAs encoding ironrequiring proteins [31].”
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A genome-wide transcriptional study reveals that iron deficiency inhibits the yeast TORC1 pathway
Romero, A. M., Ramos-Alonso, L., Montellà-Manuel, S., García‐Martínez, J., de la Torre-Ruiz, M. Á., Pérez-Ortín, J. E., Martínez‐Pastor, M. T., & Puig, S. (2019) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2019.194414 · Cited by 29
“Mean values of fold induction in iron scarcity and standard deviations from at least two independent experiments are shown 0 0,5 1 1,5 2 2,5 3 3,5 4 BY4741 cth1Δcth2Δ A 0 0,5 1 1,5 2 2,5 3 3,5 BY4741 rtg1Δ rtg2Δ rtg3Δ 1.0 2.0 3.0 3.5 2.5 1.5 0.0 0.5 PACO1-lacZ B βG al ac to si da se a ct iv ity (fo ld in du ct io n) 1…”
BackgroundInfluentialZim17/Tim15 links mitochondrial iron–sulfur cluster biosynthesis to nuclear genome stability
de la Loza, M. D. C. D., Gallardo, M., García-Rubio, M. L., Izquierdo, A., Herrero, E., Aguilera, A., & Wellinger, R. E. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr193 · Cited by 26
“Cth1 and Cth2 decrease the stability of mRNAs coding for proteins involved in the major iron-consuming processes (mitochondrial electron transport, hemebiosynthesis and ISC biogenesis) and thereby mediate a rapid downregulation of mitochondrial respiration (46,47).”
BackgroundPost‐transcriptional gene regulation in the biology and virulence ofCandida albicans
Verma‐Gaur, J., & Traven, A. (2016) · Cellular Microbiology · doi:10.1111/cmi.12593 · Cited by 26
“cerevisiae Zfs1 orthologues regulate the response to iron deficiency through decay of mRNAs with functions in iron-dependent processes (Puig et al., 2005; Puig et al., 2008).”
BackgroundCentral roles of iron in the regulation of oxidative stress in the yeast Saccharomyces cerevisiae
Matsuo, R., Mizobuchi, S., Nakashima, M., Miki, K., Ayusawa, D., & Fujii, M. (2017) · Current Genetics · doi:10.1007/s00294-017-0689-4 · Cited by 25
“CTH2 has one paralog, CTH1, which down-regulates a relatively small set of mitochondrial proteins such as the proteins involved in respiration and amino acid metabolism (Puig et al. 2008).”
BackgroundResultMetabolic remodeling in frataxin-deficient yeast is mediated by Cth2 and Adr1
Moreno-Cermeño, A., Alsina, D., Cabiscol, E., Tamarit, J., & Ros, J. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.09.019 · Cited by 23
“Cth2 is induced by Aft1 after iron starvation and it binds to AU-rich elements located in the 3′UTR of mRNAs coding for several iron-related proteins promoting its degradation [16].”
BackgroundA comprehensive mechanistic model of iron metabolism in Saccharomyces cerevisiae
Lindahl, P. A. (2019) · Metallomics · doi:10.1039/c9mt00199a · Cited by 28
Post-Transcriptional Regulation of Iron Homeostasis in Saccharomyces cerevisiae
Martínez‐Pastor, M. T., de Llanos, R., Romero, A. M., & Puig, S. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms140815785 · Cited by 24
“Fe-deficient conditions, Cth2 is responsible for the down-regulation of more that 200 mRNAs, whereas Cth1 contributes to the decrease approximately 60 transcripts [31,36].”
InfluentialSilva, N. C. E., Gonçalves, I., Lemaire, M., Lesuisse, E., Camadro, J., & Blaiseau, P. L. (2009) · Genetics · doi:10.1534/genetics.109.104364 · Cited by 25
“Aft2 controls the transcription of some of the Aft1 target genes (e.g., FTR1, CTH1, and CTH2) (Courel et al. 2005; Puig et al. 2005, 2008) but it also activates the transcription of genes that are not Aft1 target genes, including SMF3 and MRS4, involved in vacuolar and mitochondrial iron transport,…”
BackgroundRepression of the Low Affinity Iron Transporter Gene FET4
Caetano, S. M., Menezes, R., Amaral, C., Rodrigues‐Pousada, C., & Pimentel, C. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.600742 · Cited by 23
“7, B and C), suggesting that Aft1 was more active in this strain.”
MethodInfluentialFoster, A. W., Dainty, S. J., Patterson, C. J., Pohl, E., Blackburn, H., Wilson, C. A., Hess, C. R., Rutherford, J. C., Quaranta, L., Corran, A., et al. (2014) · Molecular Microbiology · doi:10.1111/mmi.12661 · Cited by 23
“…less demanding of iron (Yamaguchi-Iwai et al., 1995; 1996; Martins et al., 1998; Foury and Talibi, 2000; Yun et al., 2000; Protchenko et al., 2001; Rutherford et al., 2001; 2003; Portnoy et al., 2002; Stadler and Schweyen, 2002; Shakoury-Elizeh et al., 2004; Courel et al., 2005; Puig et al., 2008).”
BackgroundInfluentialCankorur‐Cetinkaya, A., Eraslan, S., & Kırdar, B. (2013) · Molecular BioSystems · doi:10.1039/c3mb70276f · Cited by 22
Proteomic Profiling of the Influence of Iron Availability onCryptococcus gattii
Crestani, J., Carvalho, P. C., Han, X., Seixas, A., Broetto, L., Fischer, J. D. S. D. G., Staats, C. C., Schrank, A., Yates, J. R., & Vainstein, M. H. (2011) · Journal of Proteome Research · doi:10.1021/pr2005296 · Cited by 20
Batista-Nascimento, L. S., Tolédano, M. B., Thiele, D. J., & Rodrigues‐Pousada, C. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.12.018 · Cited by 20
“WT cells and the isogenic aft1 mutant were transformed with a β-galactosidase reporter plasmid containing the promoter sequence of CTH2 previously described [9], pCM64-CTH2-FeRE-CYC1-LacZ.”
MethodIron in Translation: From the Beginning to the End
Romero, A. M., Martínez‐Pastor, M. T., & Puig, S. (2021) · Microorganisms · doi:10.3390/microorganisms9051058 · Cited by 20
“cerevisiae, one of these additional mechanisms is mediated by the post-transcriptional factor Cth2, a protein highly expressed under iron deficiency and almost nondetectable in other growth conditions [10,11].”
BackgroundA pathogenic role for histone H3 copper reductase activity in a yeast model of Friedreich’s ataxia
Campos, O. A., Attar, N., Cheng, C., Vogelauer, M., Mallipeddi, N. V., Schmollinger, S., Matulionis, N., Christofk, H. R., Merchant, S., & Kurdistani, S. K. (2021) · Science Advances · doi:10.1126/sciadv.abj9889 · Cited by 19
“This finding is also consistent with previous investigations demonstrating that mRNA abundances of Fe-S cluster genes are generally diminished in concurrence with decreases in cellular iron abundance (43, 44).”
ResultPatnaik, P. K., Beaupère, C., Barlit, H., Romero, A. M., Tsuchiya, M., Muir, M., Martínez‐Pastor, M. T., Puig, S., Kaeberlein, M. R., & Labunskyy, V. M. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111113 · Cited by 17
“…Fe-demanding pathways, including mitochondrial oxidative phosphorylation and tricarboxylic acid (TCA) cycle and promotes their degradation to prioritize Fe use to indispensable processes such as DNA synthesis and repair (Puig et al., 2005; Puig et al., 2008; Ramos-Alonso et al., 2018a, 2020).”
Mitochondria function in cytoplasmic FeS protein biogenesis
Dancis, A., Pandey, A. K., & Pain, D. (2024) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2024.119733 · Cited by 17
Nitric oxide prevents Aft1 activation and metabolic remodeling in frataxin-deficient yeast
Alsina, D., Ros, J., & Tamarit, J. (2017) · Redox Biology · doi:10.1016/j.redox.2017.09.001 · Cited by 14
“These were three Adr1 targets (Adh2, Gut2 and Lsc2) [33], two iron-sulfur containing enzymes which are Cth2 targets (Aco1 and Sdh2) and a Cth2 target not containing an iron-sulfur (Sdh1) [25].”
BackgroundRomero, A. M., Martínez-Pastor, M., Du, G., Solé, C., Carlos, M., Vergara, S. V., Sanvisens, N., Wohlschlegel, J. A., Toczyski, D. P., Posas, F., et al. (2018) · mBio · doi:10.1128/mbio.01694-18 · Cited by 17
“…iron deficiency, the budding yeast Saccharomyces cerevisiae activates the expression of Cth2, an mRNA-binding protein that, in coordination with its partially redundant homolog Cth1, plays a pivotal role in the adaptation to iron limitation by posttranscriptionally remodeling iron metabolism (3, 4).”
Molecular strategies to increase yeast iron accumulation and resistance
Ramos-Alonso, L., Wittmaack, N., Mulet, I., Martínez-Garay, C. A., Fita‐Torró, J., Lozano, M. J., Romero, A. M., García‐Ferris, C., Martínez‐Pastor, M. T., & Puig, S. (2018) · Metallomics · doi:10.1039/c8mt00124c · Cited by 16
Barba‐Aliaga, M., Villarroel-Vicente, C., Stanciu, A., Corman, A., Martínez‐Pastor, M. T., & Alepuz, P. M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010219 · Cited by 14
Pujol‐Carrion, N., Pavón‐Vergés, M., Arroyo, J., & de la Torre-Ruiz, M. Á. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2021.118974 · Cited by 14
Sanvisens, N., Romero, A. M., Zhang, C., Wu, X., An, X., Huang, M., & Puig, S. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.720862 · Cited by 13
Dissecting mRNA decay and translation inhibition during iron deficiency
Ramos-Alonso, L., Romero, A. M., Polaina, J., Puig, S., & Martínez‐Pastor, M. T. (2018) · Current Genetics · doi:10.1007/s00294-018-0880-2 · Cited by 13
Mukherjee, K., Gardin, J., Futcher, B., & Leatherwood, J. (2016) · RNA · doi:10.1261/rna.051490.115 · Cited by 13
“Cth2 recognizes AU-rich elements in the 3′ UTR of iron starvation mRNAs and targets them for degradation (Puig et al. 2005, 2008).”
BackgroundIron-mediated post-transcriptional regulation in Toxoplasma gondii
Sloan, M. A., Scott, A., Aghabi, D., Mrvova, L., & Harding, C. R. (2025) · PLoS Pathogens · doi:10.1371/journal.ppat.1012857 · Cited by 15
Yang, Z. R., Wei, Y., Fu, Y., Wang, X., Shen, W., Shi, A., Zhang, H., Li, H., Song, X., Wang, J., et al. (2024) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2024.107605 · Cited by 11
The late‐annotated small ORF LSO 1 is a target gene of the iron regulon of Saccharomyces cerevisiae
An, X., Zhang, C., Sclafani, R. A., Seligman, P. A., & Huang, M. (2015) · MicrobiologyOpen · doi:10.1002/mbo3.303 · Cited by 11
Patial, S., Stumpo, D. J., Young, W. S., Ward, J. M., Flake, G. P., & Blackshear, P. J. (2016) · Molecular and Cellular Biology · doi:10.1128/mcb.01068-15 · Cited by 11
“A link between the two TTP family members expressed in Saccharomyces cerevisiae, CTH1p and CTH2p, and the regulation of cellular iron homeostasis also has been demonstrated previously (42, 43).”
BackgroundCth2 Protein Mediates Early Adaptation of Yeast Cells to Oxidative Stress Conditions
Castells‐Roca, L., Pijuan, J., Ferrezuelo, F., Bellı́, G., & Herrero, E. (2016) · PLoS ONE · doi:10.1371/journal.pone.0148204 · Cited by 11
“CTH1 and CTH2mRNAs are as well targeted by both Cth1 and Cth2 proteins, resulting in an auto- and cross-regulatory loop that limits expression of the Cth1 and Cth2 proteins and causes their time-regulated expression [20].”
BackgroundInfluentialModulation of yeast Erg1 expression and terbinafine susceptibility by iron bioavailability
Jordá, T., Martínez-Martín, A., Martínez‐Pastor, M. T., & Puig, S. (2022) · Microbial Biotechnology · doi:10.1111/1751-7915.14102 · Cited by 10
“In Figure 5, BY4741 cth1Δcth2Δ cells transformed with the centromeric plasmids pRS416- CTH2 (CTH2) or p416TEFCTH2 (PTEF- CTH2) (Puig et al., 2005; Puig et al., 2008) were grown overnight, reinoculated at an OD600 of 0.2 and then incubated for 6 h to exponential phase in SC- ura or SC- ura with 100…”
BackgroundMethodInfluentialDu, Y., Wang, C., & Li, W. (2012) · Molecules and Cells · doi:10.1007/s10059-012-2242-0 · Cited by 10
“Almost all studies on iron metabolism have used an iron con- centration of 1 mM or lower (Kumanovics et al., 2008; Puig et al., 2008), while the yeast response to 1 mM or higher iron, designated an iron-surplus condition, has not yet been extensively studied.”
BackgroundGaspar‐Cordeiro, A., Caetano, S. M., Amaral, C., Rodrigues‐Pousada, C., & Pimentel, C. (2018) · FEBS Journal · doi:10.1111/febs.14450 · Cited by 10
Barlit, H., Romero, A. M., Gülhan, A., Patnaik, P. K., Tyshkovskiy, A., Martínez‐Pastor, M. T., Gladyshev, V. N., Puig, S., & Labunskyy, V. M. (2024) · iScience · doi:10.1016/j.isci.2024.109868 · Cited by 9
Metadata
- Authors
- Puig, S., Vergara, S. V., & Thiele, D. J.
- Affiliations
- Universitat de València (ES)
- Duke Medical Center (US)
- Corresponding author
- Puig, Sergi
- Thiele, Dennis J.
- Venue
- Cell Metabolism
- Publisher
- Elsevier BV
- Published
- 2008-06
- Volume
- 7
- Issue
- 6
- Pages
- 555-564
- ISSN
- 1550-4131 (ISSN-L)
- PMC
- PMC2459314
- OpenAlex
- W2041968919
- Cited by
- 135
- References
- 38
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 8 · 2023: 4 · 2022: 7 · 2021: 8 · 2020: 6 · 2019: 3 · 2018: 11 · 2017: 8 · 2016: 8 · 2015: 4 · 2014: 7 · 2013: 12 · 2012: 13
- FWCI
- 5.84
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- University of Pittsburgh
- National Institutes of Health
- U.S. Public Health Service (FDK081304A)
- National Institute of General Medical Sciences (GM 41840, R01GM041840)
- National Institute of Diabetes and Digestive and Kidney Diseases (F31DK081304)
- Topics
- Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Keywords
- iron deficiency, mRNA-binding proteins, mRNA degradation, metabolic reprogramming, Snf1, AMPK, glycogen storage, mitochondrial respiration, amino acid biosynthesis, Saccharomyces cerevisiae, iron starvation response
- MeSH terms
- Iron Deficiencies, Adaptation, Physiological, DNA-Binding Proteins, Metabolism, Phosphorylation, RNA, Messenger, Saccharomyces cerevisiae, Transcription Factors, RNA-Binding Proteins, Protein Serine-Threonine Kinases, Saccharomyces cerevisiae Proteins, Tristetraprolin
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