Yeast prion [PSI+] lowers the levels of mitochondrial prohibitins

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1793, Issue 11, 2009, Pages 1703-1709

  Sikora, Jacek ^a   Towpik, Joanna ^a   Graczyk, Damian ^a   Kistowski, Michał ^a   Rubel, Tymon ^b   Poznanski, Jaroslaw ^a   Langridge, James ^c   Hughes, Chris ^c   Dadlez, Michał ^a,d   Boguta, Magdalena ^a,b  

^a INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^b WARSAW UNIVERSITY OF TECHNOLOGY   (Poland)

^c WATERS CORPORATION   (United States)

^d UNIVERSITY OF WARSAW   (Poland)

Author keywords

Differential proteomics; Prohibitin; Yeast mitochondria; Yeast prion

Indexed keywords

CELL EXTRACT; CYCLOOXYGENASE 2; CYTOCHROME C OXIDASE; MITOCHONDRIAL PROTEIN; PROHIBITIN; TRANSLATION TERMINATION FACTOR;

ARTICLE; CONTROLLED STUDY; CYTOSOL; ENZYME STABILITY; ENZYME SUBUNIT; FRACTIONATION; IMMUNOBLOTTING; MAMMAL CELL; MITOCHONDRION; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEOMICS; YEAST;

ELECTRON TRANSPORT COMPLEX IV; ENZYME STABILITY; MITOCHONDRIAL PROTEINS; PEPTIDE TERMINATION FACTORS; PROTEIN TRANSPORT; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

MAMMALIA;

EID: 72049114707     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2009.08.003     Document Type: Article

References (62)

1. Wickner R.B., Edskes H.K., Ross E.D., Pierce M.M., Baxa U., Brachmann A., and Shewmaker F. Prion genetics: new rules for a new kind of gene. Annu. Rev. Genet. 38 (2004) 681-707
2. Shorter J., and Lindquist S. Prions as adaptive conduits of memory and inheritance. Nat. Rev. Genet. 6 (2005) 435-450
3. Barnham K.J., Cappai R., Beyreuther K., Masters C.L., and Hill A.F. Delineating common molecular mechanisms in Alzheimer's and prion diseases. Trends Biochem. Sci. 31 (2006) 465-472
4. Glover J.R., Kowal A.S., Schirmer E.C., Patino M.M., Liu J.J., and Lindquist S. Self-seeded fibers formed by Sup35, the protein determinant of [PSI+], a heritable prion-like factor of S. cerevisiae. Cell 89 (1997) 811-819
5. Shewmaker F., Ross E., Tycko R., and Wickner R. Amyloids of shuffled prion domains that form prions have a parallel in-register beta-sheet structure. Biochemistry 47 (2008) 4000-4007
6. Wickner R.B., Dyda F., and Tycko R. Amyloid of Rnq1p, the basis of the [PIN+] prion, has a parallel in-register beta-sheet structure. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 2403-2408
7. Kushnirov V.V., and Ter-Avanesyan M.D. Structure and replication of yeast prions. Cell 94 (1998) 13-16
8. Stansfield I., Jones K.M., Kushnirov V.V., Dagkesamanskaya A.R., Poznyakovski A.I., Paushkin S.V., Nierras C.R., Cox B.S., Ter-Avanesyan M.D., and Tuite M.F. The products of the SUP45 (eRF1) and SUP35 genes interact to mediate translation termination in Saccharomyces cerevisiae. EMBO J. 14 (1995) 4365-4373
9. Zhouravleva G., Frolova L., Le Goff X., Le Guellec R., Inge-Vechtomov S., Kisselev L., and Philippe M. Termination of translation in eukaryotes is governed by two interacting polypeptide chain release factors, eRF1 and eRF3. EMBO J. 14 (1995) 4065-4072
10. True H.L., Berlin I., and Lindquist S.L. Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431 (2004) 184-187
11. Chernoff Y.O., Lindquist S.L., Ono B., Inge-Vechtomov S.G., and Liebman S.W. Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+]. Science 268 (1995) 880-884
12. Kushnirov V.V., Kryndushkin D.S., Boguta M., Smirnov V.N., and Ter-Avanesyan M.D. Chaperones that cure yeast artificial [PSI+] and their prion-specific effects. Curr. Biol. 10 (2000) 1443-1446
13. Chacinska A., Szczesniak B., Kochneva-Pervukhova N.V., Kushnirov V.V., Ter-Avanesyan M.D., and Boguta M. Ssb1 chaperone is a [PSI+] prion-curing factor. Curr. Genet. 39 (2001) 62-67
14. Tutar Y., Song Y., and Masison D.C. Primate chaperones Hsc70 (constitutive) and Hsp70 (induced) differ functionally in supporting growth and prion propagation in Saccharomyces cerevisiae. Genetics 172 (2006) 851-861
15. Aron R., Higurashi T., Sahi C., and Craig E.A. J-protein co-chaperone Sis1 required for generation of [RNQ+] seeds necessary for prion propagation. EMBO J. 26 (2007) 3794-3803
16. Kryndushkin D., and Wickner R.B. Nucleotide exchange factors for Hsp70s are required for [URE3] prion propagation in Saccharomyces cerevisiae. Mol. Biol. Cell 18 (2007) 2149-2154
17. Shorter J., and Lindquist S. Hsp104, Hsp70 and Hsp40 interplay regulates formation, growth and elimination of Sup35 prions. EMBO J. 27 (2008) 2712-2724
18. Bagriantsev S.N., Gracheva E.O., Richmond J.E., and Liebman S.W. Variant-specific [PSI+] infection is transmitted by Sup35 polymers within [PSI+] aggregates with heterogeneous protein composition. Mol. Biol. Cell 19 (2008) 2433-2443
19. Allen K.D., Wegrzyn R.D., Chernova T.A., Muller S., Newnam G.P., Winslett P.A., Wittich K.B., Wilkinson K.D., and Chernoff Y.O. Hsp70 chaperones as modulators of prion life cycle: novel effects of Ssa and Ssb on the Saccharomyces cerevisiae prion [PSI+]. Genetics 169 (2005) 1227-1242
20. Chacinska A., Boguta M., Krzewska J., and Rospert S. Prion-dependent switching between respiratory competence and deficiency in the yeast nam9-1 mutant. Mol. Cell. Biol. 20 (2000) 7220-7229
21. Czaplinski K., Ruiz-Echevarria M.J., Paushkin S.V., Han X., Weng Y., Perlick H.A., Dietz H.C., Ter-Avanesyan M.D., and Peltz S.W. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev. 12 (1998) 1665-1677
22. Pflieger D., Caer J.-P.L., Lemaire C., Bernard B.A., Dujardin G.v., and Rossier J. Systematic identification of mitochondrial proteins by LC-MS/MS. Anal. Chem. 74 (2002) 2400-2406
23. Ohlmeier S., Kastaniotis A.J., Hiltunen J.K., and Bergmann U. The yeast mitochondrial proteome, a study of fermentative and respiratory growth. J. Biol. Chem. 279 (2004) 3956-3979
24. Prokisch H., Scharfe C., Camp D.G., Xiao W., David L., Andreoli C., Monroe M.E., Moore R.J., Gritsenko M.A., Kozany C., Hixson K.K., Mottaz H.M., Zischka H., Ueffing M., Herman Z.S., Davis R.W., Meitinger T., Oefner P.J., Smith R.D., and Steinmetz L.M. Integrative analysis of the mitochondrial proteome in yeast. PLoS Biol. 2 (2004) e160
25. Sickmann A., Reinders J., Wagner Y., Joppich C., Zahedi R., Meyer H.E., Schonfisch B., Perschil I., Chacinska A., Guiard B., Rehling P., Pfanner N., and Meisinger C. The proteome of Saccharomyces cerevisiae mitochondria. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 13207-13212
26. Zahedi R.P., Sickmann A., Boehm A.M., Winkler C., Zufall N., Schonfisch B., Guiard B., Pfanner N., and Meisinger C. Proteomic analysis of the yeast mitochondrial outer membrane reveals accumulation of a subclass of preproteins. Mol. Biol. Cell 17 (2006) 1436-1450
27. 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
28. Reinders J., Wagner K., Zahedi R.P., Stojanovski D., Eyrich B., van der Laan M., Rehling P., Sickmann A., Pfanner N., and Meisinger C. Profiling phosphoproteins of yeast mitochondria reveals a role of phosphorylation in assembly of the ATP synthase. Mol. Cell Proteomics 6 (2007) 1896-1906
29. Gaucher S.P., Taylor S.W., Fahy E., Zhang B., Warnock D.E., Ghosh S.S., and Gibson B.W. Expanded coverage of the human heart mitochondrial proteome using multidimensional liquid chromatography coupled with tandem mass spectrometry. J. Proteome Res. 3 (2004) 495-505
30. Taylor S.W., Fahy E., Zhang B., Glenn G.M., Warnock D.E., Wiley S., Murphy A.N., Gaucher S.P., Capaldi R.A., Gibson B.W., and Ghosh S.S. Characterization of the human heart mitochondrial proteome. Nat. Biotechnol. 21 (2003) 281-286
31. Lescuyer P., Strub J.M., Luche S., Diemer H., Martinez P., Van Dorsselaer A., Lunardi J., and Rabilloud T. Progress in the definition of a reference human mitochondrial proteome. Proteomics 3 (2003) 157-167
32. Xie X., Wilkinson H.H., Correa A., Lewis Z.A., Bell-Pedersen D., and Ebbole D.J. Transcriptional response to glucose starvation and functional analysis of a glucose transporter of Neurospora crassa. Fungal Genet. Biol. 41 (2004) 1104-1119
33. Fountoulakis M., and Schlaeger E.J. The mitochondrial proteins of the neuroblastoma cell line IMR-32. Electrophoresis 24 (2003) 260-275
34. Mootha V.K., Bunkenborg J., Olsen J.V., Hjerrild M., Wisniewski J.R., Stahl E., Bolouri M.S., Ray H.N., Sihag S., Kamal M., Patterson N., Lander E.S., and Mann M. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115 (2003) 629-640
35. Cruz S.D., Xenarios I., Langridge J., Vilbois F., Parone P.A., and Martinou J.-C. Proteomic analysis of the mouse liver mitochondrial inner membrane. J. Biol. Chem. 278 (2003) 41566-41571
36. Perocchi F., Jensen L.J., Gagneur J., Ahting U., von Mering C., Bork P., Prokisch H., and Steinmetz L.M. Assessing systems properties of yeast mitochondria through an interaction map of the organelle. PLoS Genet. 2 (2006) e170
37. Chernoff Y.O., Newnam G.P., Kumar J., Allen K., and Zink A.D. Evidence for a protein mutator in yeast: role of the Hsp70-related chaperone ssb in formation, stability, and toxicity of the [PSI] prion. Mol. Cell. Biol. 19 (1999) 8103-8112
38. Westermann B., and Neupert W. Mitochondria-targeted green fluorescent proteins: convenient tools for the study of organelle biogenesis in Saccharomyces cerevisiae. Yeast 16 (2000) 1421-1427
39. Meisinger C., Sommer T., and Pfanner N. Purification of Saccharomcyes cerevisiae mitochondria devoid of microsomal and cytosolic contaminations. Anal. Biochem. 287 (2000) 339-342
40. Cargile B.J., Sevinsky J.R., Essader A.S., Stephenson J.L., and Bundy J.L. Immobilized pH gradient isoelectric focusing as a first-dimension separation in shotgun proteomics. J. Biomol. Tech. 16 (2005) 181-189
41. Yaffe M.P., and Schatz G. Two nuclear mutations that block mitochondrial protein import in yeast. Proc. Natl. Acad. Sci. U. S. A. 81 (1984) 4819-4823
42. Prokisch H., Andreoli C., Ahting U., Heiss K., Ruepp A., Scharfe C., and Meitinger T. MitoP2: the mitochondrial proteome database-now including mouse data. Nucleic Acids Res. 34 (2006) D705-D711
43. Langer T., Kaser M., Klanner C., and Leonhard K. AAA proteases of mitochondria: quality control of membrane proteins and regulatory functions during mitochondrial biogenesis. Biochem. Soc. Trans. 29 (2001) 431-436
44. Nijtmans L.G., de Jong L., Sanz M.A., Coates P.J., Berden J.A., Back J.W., Muijsers A.O., van der Spek H., and Grivell L.A. Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J. 19 (2000) 2444-2451
45. Nijtmans L.G.J., Artal S.M., Grivell L.A., and Coates P.J. The mitochondrial PHB complex: roles in mitochondrial respiratory complex assembly, ageing and degenerative disease. Cell. Mol. Life Sci. 59 (2002) 143-155
46. Kiemer L., Costa S., Ueffing M., and Cesareni G. WI-PHI: a weighted yeast interactome enriched for direct physical interactions. Proteomics 7 (2007) 932-943
47. Paushkin S.V., Kushnirov V.V., Smirnov V.N., and Ter-Avanesyan M.D. Propagation of the yeast prion-like [psi+] determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor. EMBO J. 15 (1996) 3127-3134
48. Piper P.W., Jones G.W., Bringloe D., Harris N., MacLean M., and Mollapour M. The shortened replicative life span of prohibitin mutants of yeast appears to be due to defective mitochondrial segregation in old mother cells. Aging Cell 1 (2002) 149-157
49. Merkwirth C., Dargazanli S., Tatsuta T., Geimer S., Lower B., Wunderlich F.T., von Kleist-Retzow J.C., Waisman A., Westermann B., and Langer T. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev. 22 (2008) 476-488
50. Steglich G., Neupert W., and Langer T. Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria. Mol. Cell Biol. 19 (1999) 3435-3442
51. Osman C., Wilmes C., Tatsuta T., and Langer T. Prohibitins interact genetically with Atp23, a novel processing peptidase and chaperone for the F1Fo-ATP synthase. Mol. Biol. Cell 18 (2007) 627-635
52. Back J.W., Sanz M.A., Jong L.D., Koning L.J.D., Nijtmans L.G.J., Koster C.G.D., Grivell L.A., Spek H.V.D., and Muijsers A.O. A structure for the yeast prohibitin complex: Structure prediction and evidence from chemical crosslinking and mass spectrometry. Protein Sci. 11 (2002) 2471-2478
53. Tatsuta T., Model K., and Langer T. Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol. Biol. Cell 16 (2005) 248-259
54. Meeusen S., DeVay R., Block J., Cassidy-Stone A., Wayson S., McCaffery J.M., and Nunnari J. Mitochondrial inner-membrane fusion and crista maintenance requires the dynamin-related GTPase Mgm1. Cell 127 (2006) 383-395
55. Ishihara N., Fujita Y., Oka T., and Mihara K. Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J. 25 (2006) 2966-2977
56. Cerveny K.L., Tamura Y., Zhang Z., Jensen R.E., and Sesaki H. Regulation of mitochondrial fusion and division. Trends Cell Biol. 17 (2007) 563-569
57. Merkwirth C., Dargazanli S., Tatsuta T., Geimer S., Merkwirth C., and Langer T. Prohibitin function within mitochondria: Essential roles for cell proliferation and cristae morphogenesis. Biochim. Biophys. Acta 1793 (2009) 27-32
58. Sesaki H., Southard S.M., Hobbs A.E.A., and Jensen R.E. Cells lacking Pcp1p/Ugo2p, a rhomboid-like protease required for Mgm1p processing, lose mtDNA and mitochondrial structure in a Dnm1p-dependent manner, but remain competent for mitochondrial fusion. Biochem. Biophys. Res. Commun. 308 (2003) 276-283
59. Herlan M., Vogel F., Bornhovd C., Neupert W., and Reichert A.S. Processing of Mgm1 by the rhomboid-type protease Pcp1 is required for maintenance of mitochondrial morphology and of mitochondrial DNA. J. Biol. Chem. 278 (2003) 27781-27788
60. Lewandowska A., Gierszewska M., Marszalek J., and Liberek K. Hsp78 chaperone functions in restoration of mitochondrial network following heat stress. Biochim. Biophys. Acta 1763 (2006) 141-151
61. Paushkin S.V., Kushnirov V.V., Smirnov V.N., and Ter-Avanesyan M.D. Interaction between yeast Sup45p (eRF1) and Sup35p (eRF3) polypeptide chain release factors: implications for prion-dependent regulation. Mol. Cell. Biol. 17 (1997) 2798-2805
62. Patino M.M., Liu J.J., Glover J.R., and Lindquist S. Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science 273 (1996) 622-626