Transcriptional and cellular responses to defective mitochondrial proteolysis in fission yeast

Journal of Molecular Biology

Volumn 408, Issue 2, 2011, Pages 222-237

  Guha, Suranjana ^a   López Maury, Luis ^b   Shaw, Michael ^c   Bähler, Jürg ^b   Norbury, Chris J ^c   Agashe, Vishwas R ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

iron homeostasis; Lon protease; m AAA protease; Schizosaccharomyces pombe; stress response

Indexed keywords

IRON; PROTEINASE; REACTIVE OXYGEN METABOLITE; SULFUR; TRANSCRIPTOME;

AMINO ACID METABOLISM; ARTICLE; CELL ASSAY; CELL STRESS; CELL SURVIVAL; CELL VIABILITY; CONFOCAL MICROSCOPY; DOWN REGULATION; ELECTRON MICROSCOPY; FUNGAL GENE; FUNGAL GENOME; FUNGAL STRAIN; FUNGUS GROWTH; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENETIC TRANSCRIPTION; LON1 GENE; M AAA GENE; MEMBRANE POTENTIAL; MITOCHONDRIAL GENOME; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; SCHIZOSACCHAROMYCES POMBE; STRESS; ULTRASTRUCTURE; UPREGULATION; YEAST;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 79953676256     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.02.044     Document Type: Article

References (57)

1. Reinders J., Zahedi R.P., Pfanner N., Meisinger C., and Sickmann A. Toward the complete yeast mitochondrial proteome: multidimensional separation techniques for mitochondrial proteomics J. Proteome Res. 5 2006 1543 1554 (Pubitemid 44036128)
2. Koppen M., and Langer T. Protein degradation within mitochondria: versatile activities of AAA proteases and other peptidases Crit. Rev. Biochem. Mol. Biol. 42 2007 221 242 (Pubitemid 46911963)
3. Wang N., Gottesman S., Willingham M.C., Gottesman M.M., and Maurizi M.R. A human mitochondrial ATP-dependent protease that is highly homologous to bacterial Lon protease Proc. Natl Acad. Sci. USA 90 1993 11247 11251 (Pubitemid 23354406)
4. Tatsuta T., and Langer T. AAA proteases in mitochondria: diverse functions of membrane-bound proteolytic machines Res. Microbiol. 160 2009 711 717
5. Matsuyama A., Arai R., Yashiroda Y., Shirai A., Kamata A., and Sekido S. ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe Nat. Biotechnol. 24 2006 841 847 (Pubitemid 44086626)
6. +: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes Genome Res. 9 1999 27 43 (Pubitemid 29095146)
7. + superfamily of functionally diverse proteins Genome Biol. 9 2008 216
8. Major T., von Janowsky B., Ruppert T., Mogk A., and Voos W. Proteomic analysis of mitochondrial protein turnover: identification of novel substrate proteins of the matrix protease pim1 Mol. Cell. Biol. 26 2006 762 776 (Pubitemid 43146474)
9. Bender T., Leidhold C., Ruppert T., Franken S., and Voos W. The role of protein quality control in mitochondrial protein homeostasis under oxidative stress Proteomics 10 2010 1426 1443
10. Bayot A., Gareil M., Rogowska-Wrzesinska A., Roepstorff P., Friguet B., and Bulteau A.L. Identification of novel oxidized protein substrates and physiological partners of the mitochondrial ATP-dependent Lon-like protease Pim1 J. Biol. Chem. 285 2010 11445 11457
11. Savel'ev A.S., Novikova L.A., Kovaleva I.E., Luzikov V.N., Neupert W., and Langer T. ATP-dependent proteolysis in mitochondria. m-AAA protease and PIM1 protease exert overlapping substrate specificities and cooperate with the mtHsp70 system J. Biol. Chem. 273 1998 20596 20602 (Pubitemid 28377630)
12. Rottgers K., Zufall N., Guiard B., and Voos W. The ClpB homolog Hsp78 is required for the efficient degradation of proteins in the mitochondrial matrix J. Biol. Chem. 277 2002 45829 45837 (Pubitemid 35417561)
13. Suzuki C.K., Suda K., Wang N., and Schatz G. Requirement for the yeast gene LON in intramitochondrial proteolysis and maintenance of respiration Science 264 1994 273 276 (Pubitemid 24189124)
14. Matsushima Y., Goto Y., and Kaguni L.S. Mitochondrial Lon protease regulates mitochondrial DNA copy number and transcription by selective degradation of mitochondrial transcription factor A (TFAM) Proc. Natl Acad. Sci. USA 107 2010 18410 18415
15. Lu B., Yadav S., Shah P.G., Liu T., Tian B., and Pukszta S. Roles for the human ATP-dependent Lon protease in mitochondrial DNA maintenance J. Biol. Chem. 282 2007 17363 17374 (Pubitemid 47100268)
16. Chen X.J., Wang X., and Butow R.A. Yeast aconitase binds and provides metabolically coupled protection to mitochondrial DNA Proc. Natl Acad. Sci. USA 104 2007 13738 13743 (Pubitemid 350003390)
17. Bota D.A., and Davies K.J. Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism Nat. Cell Biol. 4 2002 674 680 (Pubitemid 34993703)
18. Nolden M., Ehses S., Koppen M., Bernacchia A., Rugarli E.I., and Langer T. The m-AAA protease defective in hereditary spastic paraplegia controls ribosome assembly in mitochondria Cell 123 2005 277 289 (Pubitemid 41457217)
19. Tatsuta T., Augustin S., Nolden M., Friedrichs B., and Langer T. m-AAA protease-driven membrane dislocation allows intramembrane cleavage by rhomboid in mitochondria EMBO J. 26 2007 325 335 (Pubitemid 46160934)
20. Casari G., De Fusco M., Ciarmatori S., Zeviani M., Mora M., and Fernandez P. Spastic paraplegia and OXPHOS impairment caused by mutations in paraplegin, a nuclear-encoded mitochondrial metalloprotease Cell 93 1998 973 983 (Pubitemid 28280791)
21. Di Bella D., Lazzaro F., Brusco A., Plumari M., Battaglia G., and Pastore A. Mutations in the mitochondrial protease gene AFG3L2 cause dominant hereditary ataxia SCA28 Nat. Genet. 42 2010 313 321
22. Rep M., van Dijl J.M., Suda K., Schatz G., Grivell L.A., and Suzuki C.K. Promotion of mitochondrial membrane complex assembly by a proteolytically inactive yeast Lon Science 274 1996 103 106 (Pubitemid 26332734)
23. Wagner I., van Dyck L., Savel'ev A.S., Neupert W., and Langer T. Autocatalytic processing of the ATP-dependent PIM1 protease: crucial function of a pro-region for sorting to mitochondria EMBO J. 16 1997 7317 7325 (Pubitemid 28010492)
24. Khalimonchuk O., Ott M., Funes S., Ostermann K., Rodel G., and Herrmann J.M. Sequential processing of a mitochondrial tandem protein: insights into protein import in Schizosaccharomyces pombe Eukaryot. Cell 5 2006 997 1006 (Pubitemid 44100698)
25. Hoog J.L., Schwartz C., Noon A.T., O'Toole E.T., Mastronarde D.N., McIntosh J.R., and Antony C. Organization of interphase microtubules in fission yeast analyzed by electron tomography Dev. Cell 12 2007 349 361
26. Zuin A., Gabrielli N., Calvo I.A., Garcia-Santamarina S., Hoe K.L., and Kim D.U. Mitochondrial dysfunction increases oxidative stress and decreases chronological life span in fission yeast PLoS One 3 2008 e2842
27. Tusher V.G., Tibshirani R., and Chu G. Significance analysis of microarrays applied to the ionizing radiation response Proc. Natl Acad. Sci. USA 98 2001 5116 5121 (Pubitemid 32397092)
28. van Dyck L., Neupert W., and Langer T. The ATP-dependent PIM1 protease is required for the expression of intron-containing genes in mitochondria Genes Dev. 12 1998 1515 1524 (Pubitemid 28243636)
29. Chen D., Toone W.M., Mata J., Lyne R., Burns G., and Kivinen K. Global transcriptional responses of fission yeast to environmental stress Mol. Biol. Cell 14 2003 214 229 (Pubitemid 36106031)
30. Chen D., Wilkinson C.R., Watt S., Penkett C.J., Toone W.M., Jones N., and Bahler J. Multiple pathways differentially regulate global oxidative stress responses in fission yeast Mol. Biol. Cell 19 2008 308 317 (Pubitemid 351186155)
31. Crabtree H.G. Observations on the carbohydrate metabolism of tumours Biochem. J. 23 1929 536 545
32. Otterstedt K., Larsson C., Bill R.M., Stahlberg A., Boles E., Hohmann S., and Gustafsson L. Switching the mode of metabolism in the yeast Saccharomyces cerevisiae EMBO Rep. 5 2004 532 537 (Pubitemid 38745046)
33. Labbe S., Pelletier B., and Mercier A. Iron homeostasis in the fission yeast Schizosaccharomyces pombe BioMetals 20 2007 523 537 (Pubitemid 46776571)
34. Pelletier B., Beaudoin J., Mukai Y., and Labbe S. Fep1, an iron sensor regulating iron transporter gene expression in Schizosaccharomyces pombe J. Biol. Chem. 277 2002 22950 22958 (Pubitemid 34967279)
35. Chen O.S., Crisp R.J., Valachovic M., Bard M., Winge D.R., and Kaplan J. Transcription of the yeast iron regulon does not respond directly to iron but rather to iron-sulfur cluster biosynthesis J. Biol. Chem. 279 2004 29513 29518 (Pubitemid 38915831)
36. Jensen L.T., and Culotta V.C. Role of Saccharomyces cerevisiae ISA1 and ISA2 in iron homeostasis Mol. Cell. Biol. 20 2000 3918 3927 (Pubitemid 30314491)
37. Kispal G., Csere P., Prohl C., and Lill R. The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins EMBO J. 18 1999 3981 3989 (Pubitemid 29335851)
38. Lill R., and Muhlenhoff U. Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases Annu. Rev. Biochem. 77 2008 669 700
39. Hausmann A., Samans B., Lill R., and Muhlenhoff U. Cellular and mitochondrial remodeling upon defects in iron-sulfur protein biogenesis J. Biol. Chem. 283 2008 8318 8330
40. Lange H., Muhlenhoff U., Denzel M., Kispal G., and Lill R. The heme synthesis defect of mutants impaired in mitochondrial iron-sulfur protein biogenesis is caused by reversible inhibition of ferrochelatase J. Biol. Chem. 279 2004 29101 29108 (Pubitemid 38915781)
41. Wingert R.A., Galloway J.L., Barut B., Foott H., Fraenkel P., and Axe J.L. Deficiency of glutaredoxin 5 reveals Fe-S clusters are required for vertebrate haem synthesis Nature 436 2005 1035 1039 (Pubitemid 41191688)
42. Zhan K., Vattem K.M., Bauer B.N., Dever T.E., Chen J.J., and Wek R.C. Phosphorylation of eukaryotic initiation factor 2 by heme-regulated inhibitor kinase-related protein kinases in Schizosaccharomyces pombe is important for resistance to environmental stresses Mol. Cell. Biol. 22 2002 7134 7146
43. Zhan K., Narasimhan J., and Wek R.C. Differential activation of eIF2 kinases in response to cellular stresses in Schizosaccharomyces pombe Genetics 168 2004 1867 1875 (Pubitemid 40066328)
44. Yoneda T., Benedetti C., Urano F., Clark S.G., Harding H.P., and Ron D. Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones J. Cell Sci. 117 2004 4055 4066 (Pubitemid 39328294)
45. Haynes C.M., Yang Y., Blais S.P., Neubert T.A., and Ron D. The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C. elegans Mol. Cell 37 2010 529 540
46. Zhao Q., Wang J., Levichkin I.V., Stasinopoulos S., Ryan M.T., and Hoogenraad N.J. A mitochondrial specific stress response in mammalian cells EMBO J. 21 2002 4411 4419 (Pubitemid 34984328)
47. Arnold I., Wagner-Ecker M., Ansorge W., and Langer T. Evidence for a novel mitochondria-to-nucleus signalling pathway in respiring cells lacking i-AAA protease and the ABC-transporter Mdl1 Gene 367 2006 74 88 (Pubitemid 43286742)
48. Horowitz M.P., and Greenamyre J.T. Mitochondrial iron metabolism and its role in neurodegeneration J. Alzheimer's Dis. 20 2010 S551 S568
49. Forsburg S.L., and Rhind N. Basic methods for fission yeast Yeast 23 2006 173 183
50. Moreno S., Klar A., and Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe Methods Enzymol. 194 1991 795 823
51. Bahler J., Wu J.Q., Longtine M.S., Shah N.G., McKenzie A. 3rd, and Steever A.B. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe Yeast 14 1998 943 951 (Pubitemid 28328000)
52. Hawes P., Netherton C.L., Mueller M., Wileman T., and Monaghan P. Rapid freeze-substitution preserves membranes in high-pressure frozen tissue culture cells J. Microsc. 226 2007 182 189 (Pubitemid 46625285)
53. Lyne R., Burns G., Mata J., Penkett C.J., Rustici G., and Chen D. Whole-genome microarrays of fission yeast: characteristics, accuracy, reproducibility, and processing of array data BMC Genomics 4 2003 27
54. Chiron S., Gaisne M., Guillou E., Belenguer P., Clark-Walker G.D., and Bonnefoy N. Studying mitochondria in an attractive model: Schizosaccharomyces pombe Methods Mol. Biol. 372 2007 91 105
55. Meisinger C., Sommer T., and Pfanner N. Purification of Saccharomyces cerevisiae mitochondria devoid of microsomal and cytosolic contaminations Anal. Biochem. 287 2000 339 342 (Pubitemid 32006247)
56. Morrison J.F. The activation of aconitase by ferrous ions and reducing agents Biochem. J. 58 1954 685 692
57. Munujos P., Coll-Canti J., Gonzalez-Sastre F., and Gella F.J. Assay of succinate dehydrogenase activity by a colorimetric-continuous method using iodonitrotetrazolium chloride as electron acceptor Anal. Biochem. 212 1993 506 509 (Pubitemid 23245103)