Negative feedback regulation of the yeast Cth1 and Cth2 mRNA binding proteins is required for adaptation to iron deficiency and iron supplementation

Molecular and Cellular Biology

Volumn 33, Issue 11, 2013, Pages 2178-2187

  Martínez Pastor, Mar ^a   Vergara, Sandra V ^a,c   Puig, Sergi ^b   Thiele, Dennis J ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CTH1 PROTEIN; CTH2 PROTEIN; IRON; PROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; IRON DEFICIENCY; MUTAGENESIS; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SUPPLEMENTATION; YEAST;

3' UNTRANSLATED REGIONS; ADAPTATION, PHYSIOLOGICAL; AU RICH ELEMENTS; BASE SEQUENCE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; IRON; MOLECULAR SEQUENCE DATA; RNA STABILITY; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; TRISTETRAPROLIN;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84878981799     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01458-12     Document Type: Article

References (39)

1. Lill R. 2009. Function and biogenesis of iron-sulphur proteins. Nature 460:831-838.
2. 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. Acta 1823:1491-1508.
3. Lill R, Muhlenhoff U. 2008. Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu. Rev. Biochem. 77:669-700.
4. Ozer A, Bruick RK. 2007. Non-heme dioxygenases: cellular sensors and regulators jelly rolled into one? Nat. Chem. Biol. 3:144-153.
5. Ganz T, Nemeth E. 2011. The hepcidin-ferroportin system as a therapeutic target in anemias and iron overload disorders. Hematology Am. Soc. Hematol. Educ. Program 2011:538 -542.
6. Hentze MW, Muckenthaler MU, Galy B, Camaschella C. 2010. Two to tango: regulation of mammalian iron metabolism. Cell 142:24-38.
7. Kaplan JC. 2011. The 2012 version of the gene table of monogenic neuromuscular disorders. Neuromuscul. Disord. 21:833-861.
8. Sheftel A, Stehling O, Lill R. 2010. Iron-sulfur proteins in health and disease. Trends Endocrinol. Metab. 21:302-314.
9. Baynes RD, Bothwell TH. 1990. Iron deficiency. Annu. Rev. Nutr. 10: 133-148.
10. Rouault TA. 2006. The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat. Chem. Biol. 2:406-414.
11. Pantopoulos K. 2004. Iron metabolism and the IRE/IRP regulatory system: an update. Ann. N. Y. Acad. Sci. 1012:1-13.
12. Salahudeen AA, Thompson JW, Ruiz JC, Ma HW, Kinch LN, Li Q, Grishin NV, Bruick RK. 2009. An E3 ligase possessing an iron-responsive hemerythrin domain is a regulator of iron homeostasis. Science 326:722-726.
13. Vashisht AA, Zumbrennen KB, Huang X, Powers DN, Durazo A, Sun D, Bhaskaran N, Persson A, Uhlen M, Sangfelt O, Spruck C, Leibold EA, Wohlschlegel JA. 2009. Control of iron homeostasis by an ironregulated ubiquitin ligase. Science 326:718-721.
14. Pimentel C, Vicente C, Menezes RA, Caetano S, Carreto L, Rodrigues-Pousada C. 2012. The role of the Yap5 transcription factor in remodeling gene expression in response to Fe bioavailability. PLoS One 7:e37434. doi: 10.1371/journal.pone.0037434.
15. Kaplan CD, Kaplan J. 2009. Iron acquisition and transcriptional regulation. Chem. Rev. 109:4536-4552.
16. Philpott CC, Protchenko O. 2008. Response to iron deprivation in Saccharomyces cerevisiae. Eukaryot. Cell 7:20-27.
17. Sanvisens N, Puig S. 2011. Causes and consequences of nutritional iron deficiency in living organisms, p 245-276. In Merkin TC (ed), Biology of starvation in humans and other organisms. Nova Science Publishers, Inc., New York, NY.
18. Carballo E, Lai WS, Blackshear PJ. 1998. Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science 281:1001-1005.
19. Puig S, Askeland E, Thiele DJ. 2005. Coordinated remodeling of cellular metabolism during iron deficiency through targeted mRNA degradation. Cell 120:99-110.
20. Puig S, Vergara SV, Thiele DJ. 2008. Cooperation of two mRNA-binding proteins drives metabolic adaptation to iron deficiency. Cell Metab. 7:555-564.
21. Pedro-Segura E, Vergara SV, Rodriguez-Navarro S, Parker R, Thiele DJ, Puig S. 2008. The Cth2 ARE-binding protein recruits the Dhh1 helicase to promote the decay of succinate dehydrogenase SDH4 mRNA in response to iron deficiency. J. Biol. Chem. 283:28527-28535.
22. Ciais D, Bohnsack MT, Tollervey D. 2008. The mRNA encoding the yeast ARE-binding protein Cth2 is generated by a novel 3= processing pathway. Nucleic Acids Res. 36:3075-3084.
23. Prouteau M, Daugeron MC, Seraphin B. 2008. Regulation of ARE transcript 3= end processing by the yeast Cth2 mRNA decay factor. EMBO J. 27:2966-2976.
24. Sanvisens N, Bano MC, Huang M, Puig S. 2011. Regulation of ribonucleotide reductase in response to iron deficiency. Mol. Cell 44:759 -769.
25. SenGupta DJ, Zhang B, Kraemer B, Pochart P, Fields S, Wickens M. 1996. A three-hybrid system to detect RNA-protein interactions in vivo. Proc. Natl. Acad. Sci. U. S. A. 93:8496-8501.
26. Warringer J, Blomberg A. 2003. Automated screening in environmental arrays allows analysis of quantitative phenotypic profiles in Saccharomyces cerevisiae. Yeast 20:53-67.
27. Puig S, Lee J, Lau M, Thiele DJ. 2002. Biochemical and genetic analyses of yeast and human high affinity copper transporters suggest a conserved mechanism for copper uptake. J. Biol. Chem. 277:26021-26030.
28. Rossignol T, Ding C, Guida A, d'Enfert C, Higgins DG, Butler G. 2009. Correlation between biofilm formation and the hypoxic response in Candida parapsilosis. Eukaryot. Cell 8:550-559.
29. Pastor MM, Proft M, Pascual-Ahuir A. 2009. Mitochondrial function is an inducible determinant of osmotic stress adaptation in yeast. J. Biol. Chem. 284:30307-30317.
30. Vergara SV, Puig S, Thiele DJ. 2011. Early recruitment of AU-rich element-containing mRNAs determines their cytosolic fate during iron deficiency. Mol. Cell. Biol. 31:417-429.
31. Thompson MJ, Lai WS, Taylor GA, Blackshear PJ. 1996. Cloning and characterization of two yeast genes encoding members of the CCCH class of zinc finger proteins: zinc finger-mediated impairment of cell growth. Gene 174:225-233.
32. Li L, Bagley D, Ward DM, Kaplan J. 2008. Yap5 is an iron-responsive transcriptional activator that regulates vacuolar iron storage in yeast. Mol. Cell. Biol. 28:1326-1337.
33. Ihrig J, Hausmann A, Hain A, Richter N, Hamza I, Lill R, Muhlenhoff U. 2010. Iron regulation through the back door: iron-dependent metabolite levels contribute to transcriptional adaptation to iron deprivation in Saccharomyces cerevisiae. Eukaryot. Cell 9:460-471.
34. Perez-Ortin JE, Alepuz PM, Moreno J. 2007. Genomics and gene transcription kinetics in yeast. Trends Genet. 23:250-257.
35. Shalem O, Dahan O, Levo M, Martinez MR, Furman I, Segal E, Pilpel Y. 2008. Transient transcriptional responses to stress are generated by opposing effects of mRNA production and degradation. Mol. Syst. Biol. 4:223.
36. Carballo E, Lai WS, Blackshear PJ. 2000. Evidence that tristetraprolin is a physiological regulator of granulocyte-macrophage colony-stimulating factor messenger RNA deadenylation and stability. Blood 95:1891-1899.
37. Rounbehler RJ, Fallahi M, Yang C, Steeves MA, Li W, Doherty JR, Schaub FX, Sanduja S, Dixon DA, Blackshear PJ, Cleveland JL. 2012. Tristetraprolin impairs myc-induced lymphoma and abolishes the malignant state. Cell 150:563-574.
38. Brooks SA, Connolly JE, Rigby WF. 2004. The role of mRNA turnover in the regulation of tristetraprolin expression: evidence for an extracellular signal-regulated kinase-specific, AU-rich element-dependent, autoregulatory pathway. J. Immunol. 172:7263-7271.
39. Tchen CR, Brook M, Saklatvala J, Clark AR. 2004. The stability of tristetraprolin mRNA is regulated by mitogen-activated protein kinase p38 and by tristetraprolin itself. J. Biol. Chem. 279:32393-32400.