The basic leucine zipper stress response regulator Yap5 senses high-iron conditions by coordination of [2Fe-2S] clusters

Molecular and Cellular Biology

Volumn 35, Issue 2, 2015, Pages 370-378

  Rietzschel, Nicole ^a   Pierik, Antonio J ^a,b   Bill, Eckhard ^c   Lill, Roland ^a,d   Mühlenhoff, Ulrich ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

^c MAX PLANCK INSTITUTE FOR CHEMICAL ENERGY CONVERSION   (Germany)

^d Unit of Metabolism   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CYSTEINE; IRON; IRON SULFUR PROTEIN; SULFUR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR YAP5; UNCLASSIFIED DRUG; CATION TRANSPORT PROTEIN; CCC1 PROTEIN, S CEREVISIAE; LEUCINE ZIPPER PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; YAP5 PROTEIN, S CEREVISIAE;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL VIABILITY; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; ELECTRON SPIN RESONANCE; IN VITRO STUDY; IN VIVO STUDY; IRON BINDING CAPACITY; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; STRESS; TRANSCRIPTION INITIATION; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

EUKARYOTA; FUNGI; SACCHAROMYCES CEREVISIAE;

ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CATION TRANSPORT PROTEINS; CYSTEINE; GENE EXPRESSION REGULATION, FUNGAL; IRON; IRON-SULFUR PROTEINS; LEUCINE ZIPPERS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SULFUR;

EID: 84919626418     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01033-14     Document Type: Article

References (43)

1. Lyons TJ, Eide DJ. 2007. Transport and storage of metal ions in biology, p 57-77. In Bertini I, Gray HB, Stiefel EI, Valentine JS (ed), Biological inorganic chemistry. University Science Books, Sausalito, CA.
2. Gitlin JD, Lill R. 2012. Special issue: cell biology of metals. Biochim Biophys Acta 1823:1405. http://dx.doi.org/10.1016/j.bbamcr.2012.07.008.
3. Weinberg ED. 2009. Iron availability and infection. Biochim Biophys Acta 1790:600-605. http://dx.doi.org/10.1016/j.bbagen.2008.07.002.
4. Schrettl M, Haas H. 2011. Iron homeostasis: Achilles' heel of Aspergillus fumigatus? Curr Opin Microbiol 14:400-405. http://dx.doi.org/10.1016/j.mib.2011.06.002.
5. Anderson GJ, Vulpe CD. 2009. Mammalian iron transport. Cell Mol Life Sci 66:3241-3261. http://dx.doi.org/10.1007/s00018-009-0051-1.
6. Hentze MW, Muckenthaler MU, Galy B, Camaschella C. 2010. Two to tango: regulation of mammalian iron metabolism. Cell 142:24-38. http://dx.doi.org/10.1016/j.cell.2010.06.028.
7. Dlouhy AC, Outten CE. 2013. The iron metallome in eukaryotic organisms. Metal Ions Life Sci 12:241-278. http://dx.doi.org/10.1007/978-94-007-5561-1_8.
8. Labbe S, Khan MG, Jacques JF. 2013. Iron uptake and regulation in Schizosaccharomyces pombe. Curr Opin Microbiol 16:669-676. http://dx.doi.org/10.1016/j.mib.2013.07.007.
9. Outten CE, Albetel AN. 2013. Iron sensing and regulation in Saccharomyces cerevisiae: ironing out the mechanistic details. Curr Opin Microbiol 16:662-668. http://dx.doi.org/10.1016/j.mib.2013.07.020.
10. Philpott CC, Leidgens S, Frey AG. 2012. Metabolic remodeling in irondeficient fungi. Biochim Biophys Acta 1823:1509-1520. http://dx.doi.org/10.1016/j.bbamcr.2012.01.012.
11. 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. http://dx.doi.org/10.1128/MCB.01219-07.
12. Li L, Jia X, Ward DM, Kaplan J. 2011. Yap5 protein-regulated transcription of the TYW1 gene protects yeast from high iron toxicity. J Biol Chem 286:38488-38497. http://dx.doi.org/10.1074/jbc.M111.286666.
13. Rodrigues-Pousada CA, Nevitt T, Menezes R, Azevedo D, Pereira J, Amaral C. 2004. Yeast activator proteins and stress response: an overview. FEBS Lett 567:80-85. http://dx.doi.org/10.1016/j.febslet.2004.03.119.
14. Herrero E, Ros J, Belli G, Cabiscol E. 2008. Redox control and oxidative stress in yeast cells. Biochim Biophys Acta 1780:1217-1235. http://dx.doi.org/10.1016/j.bbagen.2007.12.004.
15. Rodrigues-Pousada C, Menezes RA, Pimentel C. 2010. The Yap family and its role in stress response. Yeast 27:245-258. http://dx.doi.org/10.1002/yea.1752.
16. Hurst HC. 1995. Transcription factors 1: bZIP proteins. Protein Profile 2:101-168.
17. Reinke AW, Baek J, Ashenberg O, Keating AE. 2013. Networks of bZIP protein-protein interactions diversified over a billion years of evolution. Science 340:730-734. http://dx.doi.org/10.1126/science.1233465.
18. Fernandes L, Rodrigues-Pousada C, Struhl K. 1997. Yap, a novel family of eight bZIP proteins in Saccharomyces cerevisiae with distinct biological functions. Mol Cell Biol 17:6982-6993.
19. Li L, Miao R, Bertram S, Jia X, Ward DM, Kaplan J. 2012. A role for iron-sulfur clusters in the regulation of transcription factor Yap5-dependent high iron transcriptional responses in yeast. J Biol Chem 287:35709-35721. http://dx.doi.org/10.1074/jbc.M112.395533.
20. 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. http://dx.doi.org/10.1016/j.bbamcr.2012.05.009.
21. Muhlenhoff U, Molik S, Godoy JR, Uzarska MA, Richter N, Seubert A, Zhang Y, Stubbe J, Pierrel F, Herrero E, Lillig CH, Lill R. 2010. Cytosolic monothiol glutaredoxins function in intracellular iron sensing and trafficking via their bound iron-sulfur cluster. Cell Metab 12:373-385. http://dx.doi.org/10.1016/j.cmet.2010.08.001.
22. 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 U S A 111:4043-4048. http://dx.doi.org/10.1073/pnas.1318869111.
23. Sherman F. 2002. Getting started with yeast. Methods Enzymol 350:3-41. http://dx.doi.org/10.1016/S0076-6879(02)50954-X.
24. Studier FW, Rosenberg AH, Dunn JJ, Dubendorff JW. 1990. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 185:60-89. http://dx.doi.org/10.1016/0076-6879(90)85008-C.
25. Sambrook J, Russel DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
26. Gietz RD, Woods RA. 2002. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350:87-96. http://dx.doi.org/10.1016/S0076-6879(02)50957-5.
27. Harlow E, Lane D. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
28. Molik S, Lill R, Muhlenhoff U. 2007. Methods for studying iron metabolism in yeast mitochondria. Methods Cell Biol 80:261-280. http://dx.doi.org/10.1016/S0091-679X(06)80013-0.
29. Balk J, Pierik AJ, Netz DJ, Muhlenhoff U, Lill R. 2004. The hydrogenaselike Nar1p is essential for maturation of cytosolic and nuclear ironsulphur proteins. EMBO J 23:2105-2115. http://dx.doi.org/10.1038/sj.emboj.7600216.
30. Netz DJ, Mascarenhas J, Stehling O, Pierik AJ, Lill R. 2014. Maturation of cytosolic and nuclear iron-sulfur proteins. Trends Cell Biol 24:303-312. http://dx.doi.org/10.1016/j.tcb.2013.11.005.
31. Li H, Mapolelo DT, Randeniya S, Johnson MK, Outten CE. 2012. Human glutaredoxin 3 forms [2Fe-2S]-bridged complexes with human BolA2. Biochemistry 51:1687-1696. http://dx.doi.org/10.1021/bi2019089.
32. 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. http://dx.doi.org/10.1371/journal.pone.0037434.
33. Dunham WR, Bearden AJ, Salmeen IT, Palmer G, Sands RH, Orme-Johnson WH, Beinert H. 1971. The two-iron ferredoxins in spinach, parsley, pig adrenal cortex, Azotobacter vinelandii, and Clostridium pasteurianum: studies by magnetic field Mössbauer spectroscopy. Biochim Biophys Acta 253:134-152. http://dx.doi.org/10.1016/0005-2728(71)90240-4.
34. Beinert H, Holm RH, Munck E. 1997. Iron-sulfur clusters: nature's modular, multipurpose structures. Science 277:653-659. http://dx.doi.org/10.1126/science.277.5326.653.
35. Schünemann V, Winkler H. 2000. Structure and dynamics of biomolecules studied by Mössbauer spectroscopy. Rep Prog Phys 63:263-353. http://dx.doi.org/10.1088/0034-4885/63/3/202.
36. Harrison KA, Marzluf GA. 2002. Characterization of DNA binding and the cysteine rich region of SRE, a GATA factor in Neurospora crassa involved in siderophore synthesis. Biochemistry 41:15288-15295. http://dx.doi.org/10.1021/bi0204995.
37. Chao LY, Marletta MA, Rine J. 2008. Sre1, an iron-modulated GATA DNA-binding protein of iron-uptake genes in the fungal pathogen Histoplasma capsulatum. Biochemistry 47:7274-7283. http://dx.doi.org/10.1021/bi800066s.
38. Crack JC, Green J, Hutchings MI, Thomson AJ, Le Brun NE. 2012. Bacterial iron-sulfur regulatory proteins as biological sensor-switches. Antioxid Redox Signal 17:1215-1231. http://dx.doi.org/10.1089/ars.2012.4511.
39. Rouhier N. 2010. Plant glutaredoxins: pivotal players in redox biology and iron-sulphur centre assembly. New Phytol 186:365-372. http://dx.doi.org/10.1111/j.1469-8137.2009.03146.x.
40. Molina L, Kahmann R. 2007. An Ustilago maydis gene involved in H2O2 detoxification is required for virulence. Plant Cell 19:2293-2309. http://dx.doi.org/10.1105/tpc.107.052332.
41. Gsaller F, Hortschansky P, Beattie SR, Klammer V, Tuppatsch K, Lechner BE, Rietzschel N, Werner ER, Vogan AA, Chung D, Muhlenhoff U, Kato M, Cramer RA, Brakhage AA, Haas H. 2014. The Janus transcription factor HapX controls fungal adaptation to both iron starvation and iron excess. EMBO J pii:e201489468.
42. Mathews R, Charlton S, Sands RH, Palmer G. 1974. On the nature of the spin coupling between the iron-sulfur clusters in the eight-iron ferredoxins. J Biol Chem 249:4326-4328.
43. 2 sensing through oxidation of the Yap1 transcription factor. EMBO J 19:5157-5166. http://dx.doi.org/10.1093/emboj/19.19.5157.