Fumarase: A mitochondrial metabolic enzyme and a cytosolic/nuclear component of the dna damage response

PLoS Biology

Volumn 8, Issue 3, 2010, Pages

  Yogev, Ohad ^a   Yogev, Orli ^a   Singer, Esti ^a   Shaulian, Eitan ^a   Goldberg, Michal ^b   Fox, Thomas D ^b   Pines, Ophry ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

FUMARATE HYDRATASE; FUMARIC ACID; HYPOXIA INDUCIBLE FACTOR; FUMARIC ACID DERIVATIVE; HISTONE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; ISOENZYME; SACCHAROMYCES CEREVISIAE PROTEIN; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CELL PROTECTION; CONTROLLED STUDY; CYTOSOL; DNA METABOLISM; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; FUNGAL STRAIN; GENE CONSTRUCT; GENE FUNCTION; GENE LOCATION; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; MITOCHONDRION; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; TUMOR SUPPRESSOR GENE; YEAST; CELL NUCLEUS; DNA DAMAGE; ENZYMOLOGY; GENE SILENCING; GENETICS; HELA CELL; KIDNEY TUMOR; LEIOMYOMATOSIS; METABOLISM; SACCHAROMYCES CEREVISIAE;

EUKARYOTA;

CELL NUCLEUS; CYTOSOL; DNA DAMAGE; FUMARATE HYDRATASE; FUMARATES; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HISTONES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; ISOENZYMES; KIDNEY NEOPLASMS; LEIOMYOMATOSIS; MITOCHONDRIA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TUMOR SUPPRESSOR PROTEINS;

EID: 77950553262     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000328     Document Type: Article

References (36)

1. Karniely S, Pines O (2005) Single translation-dual destination: mechanisms of dual protein targeting in eukaryotes. EMBO Rep 6: 420-425.
2. Akiba T, Hiraga K, Tuboi S (1984) Intracellular distribution of fumarase in various animals. J Biochem 96: 189-195.
3. Tuboi S, Suzuki T, Sato M, Yoshida T (1990) Rat liver mitochondrial and cytosolic fumarases with identical amino acid sequences are encoded from a single mRNA with two alternative in-phase AUG initiation sites. Adv Enzyme Regul 30:289-304.
4. Ratner S, Anslow WP Jr., Petrack B (1953) Biosynthesis of urea. VI. Enzymatic cleavage of argininosuccinic acid to arginine and fumaric acid. J Biol Chem 204:115-125.
5. Ravdin RG, Crandall DI (1951) The enzymatic conversion of homogentisic acid to 4-fumarylacetoacetic acid. J Biol Chem 189: 137-149.
6. Stein I, Peleg Y, Even-Ram S, Pines O (1994) The single translation product of the FUM1 gene (fumarase) is processed in mitochondria before being distributed between the cytosol and mitochondria in Saccharomyces cerevisiae. Mol Cell Biol 14: 4770-4778.
7. Knox C, Sass E, Neupert W, Pines O (1998) Import into mitochondria, folding and retrograde movement of fumarase in yeast. J Biol Chem 273: 25587-25593.
8. Sass E, Blachinsky E, Karniely S, Pines O (2001) Mitochondrial and cytosolic isoforms of yeast fumarase are derivatives of a single translation product and have identical amino termini. J Biol Chem 276: 46111-46117.
9. Sass E, Karniely S, Pines O (2003) Folding of fumarase during mitochondrial import determines its dual targeting in yeast. J Biol Chem 278: 45109-45116.
10. Regev-Rudzki N, Karniely S, Ben-Haim NN, Pines O (2005) Yeast aconitase in two locations and two metabolic pathways: seeing small amounts is believing. Mol Biol Cell 16: 4163-4171.
11. Karniely S, Rayzner A, Sass E, Pines O (2006) Alpha-complementation as a probe for dual localization of mitochondrial proteins. Exp Cell Res 312: 3835-3846.
12. Karniely S, Regev-Rudzki N, Pines O (2006) The presequence of fumarase is exposed to the cytosol during import into mitochondria. J Mol Biol 358: 396-405.
13. Launonen V, Vierimaa O, Kiuru M, Isola J, Roth S, et al. (2001) Inherited susceptibility to uterine leiomyomas and renal cell cancer. Proc Natl Acad Sci U S A 98: 3387-3392.
14. Tomlinson IP, Alam NA, Rowan AJ, Barclay E, Jaeger EE, et al. (2002) Germline mutations in FH predispose to dominantly inherited uterine fibroids, skin leiomyomata and papillary renal cell cancer. Nat Genet 30: 406-410.
15. Gottlieb E, Tomlinson IP (2005) Mitochondrial tumour suppressors: a genetic and biochemical update. Nat Rev Cancer 5: 857-866.
16. Isaacs JS, Jung YJ, Mole DR, Lee S, Torres-Cabala C, et al. (2005) HIF overexpression correlates with biallelic loss of fumarate hydratase in renal cancer: novel role of fumarate in regulation of HIF stability. Cancer Cell 8: 143-153.
17. Pollard PJ, Briere JJ, Alam NA, Barwell J, Barclay E, et al. (2005) Accumulation of Krebs cycle intermediates and over-expression of HIF1alpha in tumours which result from germline FH and SDH mutations. Hum Mol Genet 14: 2231-2239.
18. Sudarshan S, Linehan WM, Neckers L (2007) HIF and fumarate hydratase in renal cancer. Br J Cancer 96: 403-407.
19. Young L, Dong Q (2004) Two-step total gene synthesis method. Nucleic Acids Res 32: e59.
20. Mireau H, Arnal N, Fox TD (2003) Expression of Barstar as a selectable marker in yeast mitochondria. Mol Genet Genomics 270: 1-8.
21. Thorsness PE, Fox TD (1993) Nuclear mutations in Saccharomyces cerevisiae that affect the escape of DNA from mitochondria to the nucleus. Genetics 134: 21-28.
22. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73: 39-85.
23. Hurley PJ, Bunz F (2007) ATM and ATR: components of an integrated circuit. Cell Cycle 6: 414-417.
24. Dotiwala F, Haase J, Arbel-Eden A, Bloom K, Haber JE (2007) The yeast DNA damage checkpoint proteins control a cytoplasmic response to DNA damage. Proc Natl Acad Sci U S A 104: 11358-11363.
25. Rudin N, Haber JE (1988) Efficient repair of HO-induced chromosomal breaks in Saccharomyces cerevisiae by recombination between flanking homologous sequences. Mol Cell Biol 8: 3918-3928.
26. Alam NA, Olpin S, Rowan A, Kelsell D, Leigh IM, et al. (2005) Missense mutations in fumarate hydratase in multiple cutaneous and uterine leiomyomatosis and renal cell cancer. J Mol Diagn 7: 437-443.
27. Kokko A, Ylisaukko-Oja SS, Kiuru M, Takatalo MS, Salmikangas P, et al. (2006) Modeling tumor predisposing FH mutations in yeast: effects on fumarase activity, growth phenotype and gene expression profile. Int J Cancer 118: 1340-1345.
28. MacKenzie ED, Selak MA, Tennant DA, Payne LJ, Crosby S, et al. (2007) Cellpermeating alpha-ketoglutarate derivatives alleviate pseudohypoxia in succinate dehydrogenase-deficient cells. Mol Cell Biol 27: 3282-3289.
29. Fillingham J, Keogh MC, Krogan NJ (2006) GammaH2AX and its role in DNA double-strand break repair. Biochem Cell Biol 84: 568-577.
30. Buscemi G, Carlessi L, Zannini L, Lisanti S, Fontanella E, et al. (2006) DNA damage-induced cell cycle regulation and function of novel Chk2 phosphoresidues. Mol Cell Biol 26: 7832-7845.
31. Lavin MF (2008) Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat Rev Mol Cell Biol 9: 759-769.
32. Halazonetis TD, Gorgoulis VG, Bartek J (2008) An oncogene-induced DNA damage model for cancer development. Science 319: 1352-1355.
33. Raimundo N, Ahtinen J, Fumic K, Baric I, Remes AM, et al. (2008) Differential metabolic consequences of fumarate hydratase and respiratory chain defects. Biochim Biophys Acta 1782: 287-294.
34. Chen XJ, Wang X, Kaufman BA, Butow RA (2005) Aconitase couples metabolic regulation to mitochondrial DNA maintenance. Science 307: 714-717.
35. Rouault TA, Stout CD, Kaptain S, Harford JB, Klausner RD (1991) Structural relationship between an iron-regulated RNA-binding protein (IRE-BP) and aconitase: functional implications. Cell 64: 881-883.
36. Christofk HR, Vander Heiden MG, Wu N, Asara JM, Cantley LC (2008) Pyruvate kinase M2 is a phosphotyrosine-binding protein. Nature 452: 181-186.