Human mitochondrial RNA turnover caught in flagranti: Involvement of hSuv3p helicase in RNA surveillance

Nucleic Acids Research

Volumn 38, Issue 1, 2009, Pages 279-298

  Szczesny, Roman J ^a   Borowski, Lukasz S ^a   Brzezniak, Lien K ^a   Dmochowska, Aleksandra ^a   Gewartowski, Kamil ^a   Bartnik, Ewa ^a   Stepien, Piotr P ^a  

^a UNIVERSITY OF WARSAW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 1; MESSENGER RNA; MITOCHONDRIAL RNA; MUTANT PROTEIN; POLYADENYLATED RNA; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; PROTEIN SUV3P; RNA HELICASE; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PURIFICATION; GENE EXPRESSION; GROWTH RATE; HALF LIFE TIME; HUMAN; HUMAN CELL; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA DEGRADATION; RNA METABOLISM; RNA PROCESSING; RNA STABILITY; RNA TRANSCRIPTION;

BASE SEQUENCE; CELL GROWTH PROCESSES; CELL LINE; CELL SHAPE; DEAD-BOX RNA HELICASES; ELECTRON TRANSPORT COMPLEX I; HUMANS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; POLYADENYLATION; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RNA; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, ANTISENSE; RNA, MESSENGER; RNA, TRANSFER; RNA, UNTRANSLATED;

EID: 75649152422     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp903     Document Type: Article

References (51)

1. Houseley, J. and Tollervey, D. (2009) The many pathways of RNA degradation. Cell, 136, 763-776.
2. Carpousis, A.J. (2007) The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu. Rev. Microbiol., 61, 71-87.
3. Parker, R. and Song, H. (2004) The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol., 11, 121-127.
4. Gagliardi, D., Stepien, P.P., Temperley, R.J., Lightowlers, R.N. and Chrzanowska-Lightowlers, Z.M. (2004) Messenger RNA stability in mitochondria: different means to an end. Trends Genet., 20, 260-267.
5. Linder, P. (2006) Dead-box proteins: a family affair-active and passive players in RNP-remodeling. Nucleic Acids Res., 34, 4168-4180.
6. Stepien, P.P., Margossian, S.P., Landsman, D. and Butow, R.A. (1992) The yeast nuclear gene suv3 affecting mitochondrial post-transcriptional processes encodes a putative ATP-dependent RNA helicase. Proc. Natl Acad. Sci. USA, 89, 6813-6817.
7. Dmochowska, A., Golik, P. and Stepien, P.P. (1995) The novel nuclear gene DSS-1 of Saccharomyces cerevisiae is necessary for mitochondrial biogenesis. Curr. Genet., 28, 108-112.
8. Malecki, M., Jedrzejczak, R., Stepien, P.P. and Golik, P. (2007) In vitro reconstitution and characterization of the yeast mitochondrial degradosome complex unravels tight functional interdependence. J. Mol. Biol., 372, 23-36.
9. Rogowska, A.T., Puchta, O., Czarnecka, A.M., Kaniak, A., Stepien, P.P. and Golik, P. (2006) Balance between transcription and RNA degradation is vital for Saccharomyces cerevisiae mitochondria: reduced transcription rescues the phenotype of deficient RNA degradation. Mol. Biol. Cell, 17, 1184-1193.
10. Dziembowski, A., Piwowarski, J., Hoser, R., Minczuk, M., Dmochowska, A., Siep, M., van der Spek, H., Grivell, L. and Stepien, P.P. (2003) The yeast mitochondrial degradosome. Its composition, interplay between RNA helicase and RNase activities and the role in mitochondrial RNA metabolism. J. Biol. Chem., 278, 1603-1611.
11. Dziembowski, A., Malewicz, M., Minczuk, M., Golik, P., Dmochowska, A. and Stepien, P.P. (1998) The yeast nuclear gene DSS1, which codes for a putative RNase II, is necessary for the function of the mitochondrial degradosome in processing and turnover of RNA. Mol. Gen. Genet., 260, 108-114.
12. Margossian, S.P., Li, H., Zassenhaus, H.P. and Butow, R.A. (1996) The DExH box protein Suv3p is a component of a yeast mitochondrial 3′-to-5′ exoribonuclease that suppresses group I intron toxicity. Cell, 84, 199-209.
13. Hoffmann, B., Nickel, J., Speer, F. and Schafer, B. (2008) The 3′ ends of mature transcripts are generated by a processosome complex in fission yeast mitochondria. J. Mol. Biol., 377, 1024-1037.
14. Mattiacio, J.L. and Read, L.K. (2009) Evidence for a degradosome-like complex in the mitochondria of Trypanosoma brucei. FEBS Lett., 583, 2333-2338.
15. Mattiacio, J.L. and Read, L.K. (2008) Roles for TbDSS-1 in RNA surveillance and decay of maturation by-products from the 12S rRNA locus. Nucleic Acids Res., 36, 319-329.
16. Penschow, J.L., Sleve, D.A., Ryan, C.M. and Read, L.K. (2004) TbDSS-1, an essential Trypanosoma brucei exoribonuclease homolog that has pleiotropic effects on mitochondrial RNA metabolism. Eukaryot. Cell, 3, 1206-1216.
17. Bobrowicz, A.J., Lightowlers, R.N. and Chrzanowska-Lightowlers, Z. (2008) Polyadenylation and degradation of mRNA in mammalian mitochondria: a missing link? Biochem. Soc. Trans., 36, 517-519.
18. Falkenberg, M., Larsson, N.G. and Gustafsson, C.M. (2007) DNA replication and transcription in mammalian mitochondria. Annu. Rev. Biochem., 76, 679-699.
19. Fernandez-Silva, P., Enriquez, J.A. and Montoya, J. (2003) Replication and transcription of mammalian mitochondrial DNA. Exp. Physiol., 88, 41-56.
20. Dmochowska, A., Kalita, K., Krawczyk, M., Golik, P., Mroczek, K., Lazowska, J., Stepien, P.P. and Bartnik, E. (1999) A human putative Suv3-like RNA helicase is conserved between Rhodobacter and all eukaryotes. Acta Biochim. Pol., 46, 155-162.
21. Szczesny, R.J., Obriot, H., Paczkowska, A., Jedrzejczak, R., Dmochowska, A., Bartnik, E., Formstecher, P., Polakowska, R. and Stepien, P.P. (2007) Down-regulation of human RNA/DNA helicase SUV3 induces apoptosis by a caspase- and AIF-dependent pathway. Biol. Cell, 99, 323-332.
22. Minczuk, M., Lilpop, J., Boros, J. and Stepien, P.P. (2005) The 5′ region of the human hSUV3 gene encoding mitochondrial DNA and RNA helicase: promoter characterization and alternative pre-mRNA splicing. Biochim. Biophys. Acta, 1729, 81-87.
23. Shu, Z., Vijayakumar, S., Chen, C.F., Chen, P.L. and Lee, W.H. (2004) Purified human SUV3p exhibits multiple-substrate unwinding activity upon conformational change. Biochemistry, 43, 4781-4790.
24. Minczuk, M., Piwowarski, J., Papworth, M.A., Awiszus, K., Schalinski, S., Dziembowski, A., Dmochowska, A., Bartnik, E., Tokatlidis, K., Stepien, P.P. et al. (2002) Localisation of the human hSuv3p helicase in the mitochondrial matrix and its preferential unwinding of dsDNA. Nucleic Acids Res., 30, 5074-5086.
25. Khidr, L., Wu, G., Davila, A., Procaccio, V., Wallace, D. and Lee, W.H. (2008) Role of SUV3 helicase in maintaining mitochondrial homeostasis in human cells. J. Biol. Chem., 283, 27064-27073.
26. Bogenhagen, D.F., Rousseau, D. and Burke, S. (2008) The layered structure of human mitochondrial DNA nucleoids. J. Biol. Chem., 283, 3665-3675.
27. Lin-Chao, S., Chiou, N.T. and Schuster, G. (2007) The PNPase, exosome and RNA helicases as the building components of evolutionarily-conserved RNA degradation machines. J. Biomed. Sci., 14, 523-532.
28. Marcaida, M.J., DePristo, M.A., Chandran, V., Carpousis, A.J. and Luisi, B.F. (2006) The RNA degradosome: life in the fast lane of adaptive molecular evolution. Trends Biochem. Sci., 31, 359-365.
29. Portnoy, V., Palnizky, G., Yehudai-Resheff, S., Glaser, F. and Schuster, G. (2008) Analysis of the human polynucleotide phosphorylase (PNPase) reveals differences in RNA binding and response to phosphate compared to its bacterial and chloroplast counterparts. RNA, 14, 297-309.
30. Holec, S., Lange, H., Kuhn, K., Alioua, M., Borner, T. and Gagliardi, D. (2006) Relaxed transcription in Arabidopsis mitochondria is counterbalanced by RNA stability control mediated by polyadenylation and polynucleotide phosphorylase. Mol. Cell Biol., 26, 2869-2876.
31. Perrin, R., Lange, H., Grienenberger, J.M. and Gagliardi, D. (2004) AtmtPNPase is required for multiple aspects of the 18S rRNA metabolism in Arabidopsis thaliana mitochondria. Nucleic Acids Res., 32, 5174-5182.
32. Leszczyniecka, M., Kang, D.C., Sarkar, D., Su, Z.Z., Holmes, M., Valerie, K. and Fisher, P.B. (2002) Identification and cloning of human polynucleotide phosphorylase, hPNPase old-35, in the context of terminal differentiation and cellular senescence. Proc. Natl Acad. Sci. USA, 99, 16636-16641.
33. Sarkar, D., Park, E.S., Emdad, L., Randolph, A., Valerie, K. and Fisher, P.B. (2005) Defining the domains of human polynucleotide phosphorylase (hPNPaseOLD-35) mediating cellular senescence. Mol. Cell Biol., 25, 7333-7343.
34. Piwowarski, J., Grzechnik, P., Dziembowski, A., Dmochowska, A., Minczuk, M. and Stepien, P.P. (2003) Human polynucleotide phosphorylase, hPNPase, is localized in mitochondria. J. Mol. Biol., 329, 853-857.
35. Chen, H.W., Rainey, R.N., Balatoni, C.E., Dawson, D.W., Troke, J.J., Wasiak, S., Hong, J.S., McBride, H.M., Koehler, C.M., Teitell, M.A. et al. (2006) Mammalian polynucleotide phosphorylase is an intermembrane space RNase that maintains mitochondrial homeostasis. Mol. Cell Biol., 26, 8475-8487.
36. Sarkar, D. and Fisher, P.B. (2006) Polynucleotide phosphorylase: an evolutionary conserved gene with an expanding repertoire of functions. Pharmacol. Ther., 112, 243-263.
37. Rainey, R.N., Glavin, J.D., Chen, H.W., French, S.W., Teitell, M.A. and Koehler, C.M. (2006) A new function in translocation for the mitochondrial i-AAA protease Yme1: import of polynucleotide phosphorylase into the intermembrane space. Mol. Cell Biol., 26, 8488-8497.
38. Slomovic, S. and Schuster, G. (2008) Stable PNPase RNAi silencing: its effect on the processing and adenylation of human mitochondrial RNA. RNA, 14, 310-323.
39. Nagaike, T., Suzuki, T., Katoh, T. and Ueda, T. (2005) Human mitochondrial mRNAs are stabilized with polyadenylation regulated by mitochondria-specific poly(A) polymerase and polynucleotide phosphorylase. J. Biol. Chem., 280, 19721-19727.
40. Wang, D.D., Shu, Z., Lieser, S.A., Chen, P.L. and Lee, W.H. (2009) Human mitochondrial SUV3 and polynucleotide phosphorylase form a 330-kDa heteropentamer to cooperatively degrade double-stranded RNA with a 3'-to-5' directionality. J. Biol. Chem., 284, 20812-20821.
41. Preker, P., Nielsen, J., Kammler, S., Lykke-Andersen, S., Christensen, M.S., Mapendano, C.K., Schierup, M.H. and Jensen, T.H. (2008) RNA exosome depletion reveals transcription upstream of active human promoters. Science, 322, 1851-1854.
42. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M. and Seraphin, B. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol., 17, 1030-1032.
43. Tomecki, R., Dmochowska, A., Gewartowski, K., Dziembowski, A. and Stepien, P.P. (2004) Identification of a novel human nuclear-encoded mitochondrial poly(A) polymerase. Nucleic Acids Res., 32, 6001-6014.
44. Sambrook, J. and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
45. Piechota, J., Szczesny, R., Wolanin, K., Chlebowski, A. and Bartnik, E. (2006) Nuclear and mitochondrial genome responses in HeLa cells treated with inhibitors of mitochondrial DNA expression. Acta Biochim. Pol., 53, 485-495.
46. Spelbrink, J.N., Toivonen, J.M., Hakkaart, G.A., Kurkela, J.M., Cooper, H.M., Lehtinen, S.K., Lecrenier, N., Back, J.W., Speijer, D., Foury, F. et al. (2000) In vivo functional analysis of the human mitochondrial DNA polymerase POLG expressed in cultured human cells. J. Biol. Chem., 275, 24818-24828.
47. Jazayeri, M., Andreyev, A., Will, Y., Ward, M., Anderson, C.M. and Clevenger, W. (2003) Inducible expression of a dominant negative DNA polymerase-gamma depletes mitochondrial DNA and produces a rho0 phenotype. J. Biol. Chem., 278, 9823-9830.
48. Piechota, J., Tomecki, R., Gewartowski, K., Szczesny, R., Dmochowska, A., Kudla, M., Dybczynska, L., Stepien, P.P. and Bartnik, E. (2006) Differential stability of mitochondrial mRNA in HeLa cells. Acta Biochim. Pol., 53, 157-168.
49. Cannone, J.J., Subramanian, S., Schnare, M.N., Collett, J.R., D'Souza, L.M., Du, Y., Feng, B., Lin, N., Madabusi, L.V., Muller, K.M. et al. (2002) The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics, 3, 2.
50. Anderson, S., Bankier, A.T., Barrell, B.G., de Bruijn, M.H., Coulson, A.R., Drouin, J., Eperon, I.C., Nierlich, D.P., Roe, B.A., Sanger, F. et al. (1981) Sequence and organization of the human mitochondrial genome. Nature, 290, 457-465.
51. Slomovic, S., Laufer, D., Geiger, D. and Schuster, G. (2005) Polyadenylation and degradation of human mitochondrial RNA: the prokaryotic past leaves its mark. Mol. Cell Biol., 25, 6427-6435.