Localisation of the human hSuv3p helicase in the mitochondrial matrix and its preferential unwinding of dsDNA

Nucleic Acids Research

Volumn 30, Issue 23, 2002, Pages 5074-5086

  Minczuk, Michal ^a,b   Piwowarski, Jan ^a,b   Papworth, Monika A ^c   Awiszus, Karen ^d   Schalinski, Sarah ^d   Dziembowski, Andrzej ^a,b   Dmochowska, Aleksandra ^a,b   Bartnik, Ewa ^a,b   Tokatlidis, Kostas ^e,f   Stepien, Piotr P ^a,b   Borowski, Peter ^d  

^a UNIVERSITY OF WARSAW   (Poland)

^b INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^d BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

^f UNIVERSITY OF CRETE   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DOUBLE STRANDED DNA; HELICASE; MITOCHONDRIAL RNA; POLYNUCLEOTIDE; RECOMBINANT PROTEIN; RNA;

ANIMAL CELL; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DNA DENATURATION; DNA RNA HYBRIDIZATION; DNA STRUCTURE; ENZYME LOCALIZATION; ENZYME PURIFICATION; GENE EXPRESSION SYSTEM; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; MITOCHONDRION; MOLECULAR EVOLUTION; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; REVIEW; RNA METABOLISM; RNA PROCESSING;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ANIMALS; COS CELLS; DEAD-BOX RNA HELICASES; DNA; DNA HELICASES; ESCHERICHIA COLI; HELA CELLS; HUMANS; MITOCHONDRIA; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN TRANSPORT; RNA HELICASES; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY; YEASTS;

ANIMALIA; BACTERIA (MICROORGANISMS); CAENORHABDITIS; CAENORHABDITIS ELEGANS;

EID: 0036929748     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkf647     Document Type: Review

References (62)

1. 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.
2. 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.
3. 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.
4. Conrad-Webb,H., Perlman,P.S., Zhu,H. and Butow,R.A. (1990) The nuclear SUV3-1 mutation affects a variety of post-transcriptional processes in yeast mitochondria. Nucleic Acids Res., 18, 1369-1376.
5. Stepien,P.P., Kokot,L., Leski,T. and Bartnik,E. (1995) The suv3 nuclear gene product is required for the in vivo processing of the yeast mitochondrial 21s rRNA transcripts containing the r1 intron. Curr. Genet., 27, 234-238.
6. 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.
7. Dziembowski,A., Piwowarski,J., Hoser,R., Minczuk,M., Dmochowska,A., Siep,M., Van der Speck,H., Grivell,L. and Stepien,P.P. (2002) The yeast mitochondrial degradosome: its composition, interplay between RNA helicase and RNase activities and the role in mitochondrial RNA metabolism. J. Biol. Chem., in press.
8. Gagliardi,D., Kuhn,J., Spadinger,U., Brennicke,A., Leaver,C.J. and Binder,S. (1999) An RNA helicase (AtSUV3) is present in Arabidopsis thaliana mitochondria. FEBS Lett., 458, 337-342.
9. Maeda,I., Kohara,Y., Yamamoto,M. and Sugimoto,A. (2001) Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr. Biol., 11, 171-176.
10. Dmochowska,A., Stankiewicz,P., Golik,P., Stepien,P.P., Bocian,E., Hansmann,I. and Bartnik,E. (1998) Assignment of SUPV3L1 to human chromosome band 10q22.1 by in situ hybridization. Cytogenet. Cell Genet., 83, 84-85.
11. 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.
12. Tokatlidis,K. (2000) Directing proteins to mitochondria by fusion to mitochondrial targeting signals. Methods Enzymol., 327, 305-317.
13. Glick,B.S., Brandt,A., Cunningham,K., Muller,S., Hallberg,R.L. and Schatz,G. (1992) Cytochromes c1 and b2 are sorted to the intermembrane space of yeast mitochondria by a stop-transfer mechanism. Cell, 69, 809-822.
14. Gaines,G.L.,III (1996) In organello RNA synthesis system from HeLa cells. Methods Enzymol., 264, 43-49.
15. Bergmeyer,H.U. and Bernt,E. (1974) In Bergmeyer,H.U. (ed.), Methods of Enzymatic Analysis. Academic Press, New York, NY.
16. Graham,J.M. and Rickwood,D. (1997) Subcellular Fractionation- A Practical Approach. Oxford University Press, Oxford, UK.
17. Ostrowski,J., Wyrwicz,L., Rychlewski,L. and Bomsztyk,K. (2002) Heterogeneous nuclear ribonucleoprotein K protein associates with multiple mitochondrial transcripts within the organelle. J. Biol. Chem., 277, 6303-6310.
18. Borowski,P., Kuehl,R., Mueller,O., Hwang,L.-H., Schulze zur Wiesch,J. and Schmitz,H. (1999) Biochemical properties of a minimal functional domain with ATP-binding activity of the NTPase/helicase of hepatitis C virus. Eur. J. Biochem., 266, 715-723.
19. Borowski,P., Mueller,O., Niebuhr,A., Kalitzky,M., Hwang,L.-H., Schmitz,H., Siwecka,M.A. and Kulikowski,T. (2000) ATP-binding domain of NTPase/helicase as target for hepatitis C antiviral therapy. Acta Biochim. Pol., 47, 173-180.
20. Gallinari,P., Brennan,D., Nardi,C., Brunetti,M., Tomei,L., Steinkühler,C. and De Francesco,R. (1998) Multiple enzymatic activities associated with recombinant NS3 of hepatitis C virus. J. Virol., 72, 6758-6769.
21. Tai,C.-L., Chi,W.-K., Chen,D.-S. and Hwang,L.-H. (1996) The helicase activity associated with hepatitis C virus nonstructural protein 3 (NS3). J. Virol., 70, 8477-8484.
22. Sambrook,J., Fritsch,F. and Maniatis,T. (1989) Molecular Cloning: A Laboratory Manual, 2nd Edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
23. Borowski,P., Niebuhr,A., Mueller,O., Bretner,M., Felczak,K., Kulikowski,T. and Schmitz,H. (2001) Purification and characterization of West Nile virus NTPase/helicase. Evidence for dissociation of the NTPase and helicase activities of the enzyme. J. Virol., 75, 3220-3229.
24. Hames,B.D. and Rickwood,D. (1990) Gel Electrophoresis of Proteins: A Practical Approach, 2nd Edn. Oxford University Press, Oxford, UK.
25. Altschul,S.F., Madden,T.L., Schaffer,A.A., Zhang,J., Zhang,Z., Miller,W. and Lipman,D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
26. Nielsen,H., Engelbrecht,J., Brunak,S. and von Heijne,G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng., 10, 1-6.
27. Bauer,M.F. and Neupert,W. (2001) Import of proteins into mitochondria: a novel pathomechanism for progressive neurodegeneration. J. Inherit. Metab. Dis., 24, 166-180.
28. 0-ATPase subunit 9: export from matrix requires delta pH across inner membrane and matrix ATP. EMBO J., 14, 3445-3451.
29. Pfanner,N. and Neupert,W. (1987) Distinct steps in the import of ADP/ATP carrier into mitochondria. J. Biol. Chem., 262, 7528-7536.
30. Martin,J. (1997) Molecular chaperones and mitochondrial protein folding. J. Bioenerg. Biomembr., 29, 35-43
31. Gonzales,D.H. and Neupert,W. (1990) Biogenesis of mitochondrial c-type cytochromes. J. Bioenerg. Biomembr., 22, 753-768.
32. Walker,J.E., Saraste,M., Runswick,M.J. and Gay,N.J. (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J., 1, 945-951.
33. Schmid,S.R. and Linder,P. (1991) Translation initiation factor 4A from Saccharomyces cerevisiae. Analysis of residues conserved in the D-E-A-D family of RNA helicases. Mol. Cell. Biol., 11, 3463-3471.
34. Pause,A. and Sonenberg,N. (1992) Mutational analysis of a DEAD box RNA helicase: the mammalian translation initiation factor eIF-4A. EMBO J., 11, 2643-2654.
35. Kadare,G. and Haenni,A. (1997) Virus-encoded RNA helicases. J. Virol., 71, 2583-2590.
36. Lüking,A., Stahl,U. and Schmidt,U. (1998) The protein family of RNA helicases. Crit. Rev. Biochem. Mol. Biol., 33, 259-296.
37. Dixon,M. (1952) The determination of enzyme inhibitor constants. Biochem. J., 55, 170-171.
38. Borowski,P., Lang,M., Niebuhr,A., Haag,A., Schmitz,H., Schulze zur Wiesch,J., Choe,J., Siwecka,M.A. and Kulikowski,T. (2001) Inhibition of the helicase activity of HCV NTPase/helicase by 1-β-D-ribofuranosyl-1,2,4-triazole-3 carboxamide-5′ triphosphate (ribavirin-TP). Acta Biochim. Pol., 48, 739-744.
39. Dziembowski,A. and Stepien,P.P. (2001) Genetic and biochemical approaches for analysis of mitochondrial degradosome from Saccharomyces cerevisiae. Methods Enzymol., 342, 367-378.
40. Deloukas,P., French,L., Meitinger,T. and Moschonas,N.K. (2000) Report of the third international workshop on human chromosome 10 mapping and sequencing 1999. Cytogenet. Cell Genet., 90, 1-12.
41. Pfanner,N. and Geissler,A. (2001) Versatility of the mitochondrial protein import machinery. Nature Rev. Mol. Cell Biol., 2, 339-349.
42. Renold,A., Koehler,C.M. and Murphy,M.P. (2000) Mitochondrial import of the long and short isoforms of human uncoupling protein 3. FEBS Lett., 465, 135-140.
43. Seki,N., Moczko,M., Nagase,T., Zufall,N., Ehmann,B., Dietmeier,K., Schafer,E., Nomura,N. and Pfanner,N. (1995) A human homolog of the mitochondrial protein import receptor Mom19 can assemble with the yeast mitochondrial receptor complex. FEBS Lett., 375, 307-310.
44. Foury,F. and Kucej,M. (2002) Yeast mitochondrial biogenesis: a model system for humans? Curr. Opin. Chem. Biol., 6, 106-111.
45. Lecrenier,N. and Foury,F. (2000) New features of mitochondrial DNA replication system in yeast and man. Gene, 246, 37-48.
46. Spelbrink,J.N., Li,F.Y., Tiranti,V., Nikali,K., Yuan,Q.P., Tariq,M., Wanrooij,S., Garrido,N., Comi,G., Morandi,L. et al. (2001) Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria. Nature Genet., 28, 223-231.
47. Fox,T.D. (1996) Translational control of endogenous and recoded nuclear genes in yeast mitochondria: regulation and membrane targeting. Experientia, 52, 1130-1135.
48. Gorbalenya,A.E., Koonin,E.V., Donchenko,A.P. and Blinov,V.M. (1989) Two related superfamilies of putative helicases involved in replication, recombination, repair, and expression of DNA and RNA genomes. Nucleic Acids Res., 17, 4713-4730.
49. Gorbalenya,A.E. and Koonin,E.V. (1993) Helicases: amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol., 3, 419-429.
50. Yao,N., Hesson,T., Cable,M., Hong,Z., Kwong,A., Le,H. and Weber,P. (1997) Structure of the hepatitis C virus RNA helicase domain. Nature Struct. Biol., 4, 463-467.
51. Kim,J.L., Morgenstern,K., Griffith,J., Dwyer,M., Thomson,J., Murcko,M., Lin,C. and Caron,P. (1998) Hepatitis C virus NS3 RNA helicase domain with a bound oligonucleotide: the crystal structure provides insights into the mode of unwinding. Structure, 6, 89-100.
52. Theis,K., Chen,P.J., Skorvaga,M., Van Houten,B. and Kisker,C. (1999) Crystal structure of UvrB, a DNA helicase adapted for nucleotide excision repair. EMBO J., 18, 6899-6907.
53. Huang,Y. and Liu,Z.-R. (2002) The ATPase, RNA unwinding, and RNA binding activities of recombinant p68 RNA helicase. J. Biol. Chem., 277, 12810-12815.
54. Gorbalenya,A.E., Koonin,E.V. Donchenko,A.P. and Blinov,V.M. (1988) A novel superfamily of nucleoside triphosphate-binding motif containing proteins which are probably involved in duplex unwinding in DNA and RNA replication and recombination. FEBS Lett., 235, 16-24.
55. Gorbalenya,A.E. and Koonin,E.V. (1989) Viral proteins containing the purine NTP-binding sequence pattern. Nucleic Acids Res., 17, 8413-8440.
56. Porter,D. (1998) A kinetic analysis of the oligonucleotide-modulated ATPase activity of the helicase domain of the NS3 protein from hepatitis C virus. J. Biol. Chem., 273, 14247-14253.
57. Wong,I., Moore,K., Bjornson,K.P., Hsieh,J. and Lohman,T.M. (1996) ATPase activity of Escherichia coli Rep helicase is dramatically dependent on DNA ligation and protein oligomeric states. Biochemistry, 35, 5726-5734.
58. Morgenstern,K.A., Landro,J.A., Hsiao,K., Lin,C., Gu,Y., Su,M.S. and Thomson,J.A. (1997) Polynucleotide modulation of the protease, nucleoside triphosphatase, and helicase activities of a hepatitis C virus NS3-NS4A complex isolated from transfected COS cells. J. Virol., 71, 3767-3775.
59. Jin,L. and Peterson,D.L. (1995) Expression, isolation, and characterization of the hepatitis C virus ATPase/RNA helicase. Arch. Biochem. Biophys., 323, 47-53.
60. Suzich,J., Tamura,J., Palmer-Hill,F., Warrener,P., Grakoui,A., Rice,C., Feinstone,S. and Collett,M. (1993) Hepatitis C virus NS3 protein polynucleotide-stimulated nucleoside triphosphatase and comparison with the related Pestivirus and Flavivirus enzymes. J. Virol., 67, 6152-6158.
61. Xu,D., Nouraini,S., Field,D., Tang,S.J. and Friesen,J.D. (1996) An RNA-dependent ATPase associated with U2/U6 snRNAs in pre-mRNA splicing. Nature, 381, 709-713.
62. 2, and poly(rU). J. Biol. Chem., 273, 7390-7396.