RNA Degradation in Yeast and Human Mitochondria

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1819, Issue 9-10, 2012, Pages 1027-1034

  Szczesny, Roman J ^a,b   Borowski, Lukasz S ^a   Malecki, Michal ^a   Wojcik, Magdalena A ^a   Stepien, Piotr P ^a,b   Golik, Pawel ^a,b  

^a UNIVERSITY OF WARSAW   (Poland)

^b INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

Author keywords

Dss1 ribonuclease; Mitochondrial degradosome; Polynucleotide phosphorylase (PNPase); RNA degradation; Suv3 helicase (SUPV3L1 hSuv3p, hSuv3, Suv3p)

Indexed keywords

DEAD BOX PROTEIN; DOUBLE STRANDED DNA; ENOLASE; MITOCHONDRIAL DNA; MITOCHONDRIAL RNA; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RIBONUCLEASE E; RNA HELICASE;

BINDING SITE; CELL CYCLE REGULATION; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; GENE DELETION; GENE EXPRESSION; HUMAN; HYDROLYSIS; MITOCHONDRIAL GENOME; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; POLYADENYLATION; PRIORITY JOURNAL; REVIEW; RNA BINDING; RNA DEGRADATION; RNA PROCESSING; RNA STABILITY; RNA SYNTHESIS; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; YEAST;

ADENOSINE TRIPHOSPHATE; DEAD-BOX RNA HELICASES; EXORIBONUCLEASES; GENE EXPRESSION REGULATION; HUMANS; MITOCHONDRIA; RNA; RNA STABILITY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84864313560     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2011.11.010     Document Type: Review

References (116)

1. Miczak A., Kaberdin V.R., Wei C.L., Lin-Chao S. Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:3865-3869.
2. Coburn G.A., Miao X., Briant D.J., Mackie G.A. Reconstitution of a minimal RNA degradosome demonstrates functional coordination between a 3' exonuclease and a DEAD-box RNA helicase. Genes Dev. 1999, 13:2594-2603.
3. Kaberdin V.R., Miczak A., Jakobsen J.S., Lin-Chao S., McDowall K.J., von Gabain A. The endoribonucleolytic N-terminal half of Escherichia coli RNase E is evolutionarily conserved in Synechocystis sp. and other bacteria but not the C-terminal half, which is sufficient for degradosome assembly. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:11637-11642.
4. Vanzo N.F., Li Y.S., Py B., Blum E., Higgins C.F., Raynal L.C., Krisch H.M., Carpousis A.J. Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev. 1998, 12:2770-2781.
5. Campos-Guillen J., Bralley P., Jones G.H., Bechhofer D.H., Olmedo-Alvarez G. Addition of poly(A) and heteropolymeric 3' ends in Bacillus subtilis wild-type and polynucleotide phosphorylase-deficient strains. J. Bacteriol. 2005, 187:4698-4706.
6. Mohanty B.K., Kushner S.R. Polynucleotide phosphorylase functions both as a 3' right-arrow 5' exonuclease and a poly(A) polymerase in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11966-11971.
7. Rott R., Zipor G., Portnoy V., Liveanu V., Schuster G. RNA polyadenylation and degradation in cyanobacteria are similar to the chloroplast but different from Escherichia coli. J. Biol. Chem. 2003, 278:15771-15777.
8. Sohlberg B., Huang J., Cohen S.N. The Streptomyces coelicolor polynucleotide phosphorylase homologue, and not the putative poly(A) polymerase, can polyadenylate RNA. J. Bacteriol. 2003, 185:7273-7278.
9. Yehudai-Resheff S., Hirsh M., Schuster G. Polynucleotide phosphorylase functions as both an exonuclease and a poly(A) polymerase in spinach chloroplasts. Mol. Cell. Biol. 2001, 21:5408-5416.
10. Kushner S.R. mRNA decay in Escherichia coli comes of age. J. Bacteriol. 2002, 184:4658-4665.
11. Carpousis A.J. The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu. Rev. Microbiol. 2007, 61:71-87.
12. Hofmann T.J., Min J., Zassenhaus H.P. Formation of the 3' end of yeast mitochondrial mRNAs occurs by site-specific cleavage two bases downstream of a conserved dodecamer sequence. Yeast 1993, 9:1319-1330.
13. Osinga K.A., De Vries E., Van der Horst G., Tabak H.F. Processing of yeast mitochondrial messenger RNAs at a conserved dodecamer sequence. EMBO J. 1984, 3:829-834.
14. Conrad-Webb H., Perlman P.S., Zhu H., Butow R.A. The nuclear SUV3-1 mutation affects a variety of post-transcriptional processes in yeast mitochondria. Nucleic Acids Res. 1990, 18:1369-1376.
15. Zhu H., Conrad-Webb H., Liao X.S., Perlman P.S., Butow R.A. Functional expression of a yeast mitochondrial intron-encoded protein requires RNA processing at a conserved dodecamer sequence at the 3' end of the gene. Mol. Cell. Biol. 1989, 9:1507-1512.
16. Stepien P.P., Margossian S.P., Landsman D., Butow R.A. The yeast nuclear gene suv3 affecting mitochondrial post-transcriptional processes encodes a putative ATP-dependent RNA helicase. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:6813-6817.
17. Margossian S.P., Li H., Zassenhaus H.P., Butow R.A. The DExH box protein Suv3p is a component of a yeast mitochondrial 3'-to-5' exoribonuclease that suppresses group I intron toxicity. Cell 1996, 84:199-209.
18. Min J., Heuertz R.M., Zassenhaus H.P. Isolation and characterization of an NTP-dependent 3'-exoribonuclease from mitochondria of Saccharomyces cerevisiae. J. Biol. Chem. 1993, 268:7350-7357.
19. Stepien P.P., Kokot L., Leski T., Bartnik E. 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. 1995, 27:234-238.
20. Golik P., Szczepanek T., Bartnik E., Stepien P.P., Lazowska J. The S. cerevisiae nuclear gene SUV3 encoding a putative RNA helicase is necessary for the stability of mitochondrial transcripts containing multiple introns. Curr. Genet. 1995, 28:217-224.
21. Rogowska A.T., Puchta O., Czarnecka A.M., Kaniak A., Stepien P.P., Golik P. Balance between transcription and RNA degradation is vital for Saccharomyces cerevisiae mitochondria: reduced transcription rescues the phenotype of deficient RNA degradation. Mol. Biol. Cell 2006, 17:1184-1193.
22. Dmochowska A., Golik P., Stepien P.P. The novel nuclear gene DSS-1 of Saccharomyces cerevisiae is necessary for mitochondrial biogenesis. Curr. Genet. 1995, 28:108-112.
23. Dziembowski A., Malewicz M., Minczuk M., Golik P., Dmochowska A., Stepien P.P. 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. 1998, 260:108-114.
24. Dziembowski A., Piwowarski J., Hoser R., Minczuk M., Dmochowska A., Siep M., van der Spek H., Grivell L., Stepien P.P. The yeast mitochondrial degradosome. Its composition, interplay between RNA helicase and RNase activities and the role in mitochondrial RNA metabolism. J. Biol. Chem. 2003, 278:1603-1611.
25. Contamine V., Picard M. Maintenance and integrity of the mitochondrial genome: a plethora of nuclear genes in the budding yeast. Microbiol. Mol. Biol. Rev. 2000, 64:281-315.
26. Lipinski K.A., Kaniak-Golik A., Golik P. Maintenance and expression of the S. cerevisiae mitochondrial genome-from genetics to evolution and systems biology. Biochim. Biophys. Acta 2010, 1797:1086-1098.
27. Myers A.M., Pape L.K., Tzagoloff A. Mitochondrial protein synthesis is required for maintenance of intact mitochondrial genomes in Saccharomyces cerevisiae. EMBO J. 1985, 4:2087-2092.
28. Turk E.M., Caprara M.G. Splicing of yeast aI5beta group I intron requires SUV3 to recycle MRS1 via mitochondrial degradosome-promoted decay of excised intron ribonucleoprotein (RNP). J. Biol. Chem. 2010, 285:8585-8594.
29. Schafer B. RNA maturation in mitochondria of S. cerevisiae and S. pombe. Gene 2005, 354:80-85.
30. Amiott E.A., Jaehning J.A. Mitochondrial transcription is regulated via an ATP "sensing" mechanism that couples RNA abundance to respiration. Mol. Cell 2006, 22:329-338.
31. Shadel G.S., Clayton D.A. Mitochondrial transcription initiation. Variation and conservation. J. Biol. Chem. 1993, 268:16083-16086.
32. Fekete Z., Ellis T.P., Schonauer M.S., Dieckmann C.L. Pet127 governs a 5' -> 3'-exonuclease important in maturation of apocytochrome b mRNA in Saccharomyces cerevisiae. J. Biol. Chem. 2008, 283:3767-3772.
33. Wiesenberger G., Fox T.D. Pet127p, a membrane-associated protein involved in stability and processing of Saccharomyces cerevisiae mitochondrial RNAs. Mol. Cell. Biol. 1997, 17:2816-2824.
34. Krause K., Dieckmann C.L. Analysis of transcription asymmetries along the tRNAE-COB operon: evidence for transcription attenuation and rapid RNA degradation between coding sequences. Nucleic Acids Res. 2004, 32:6276-6283.
35. Wegierski T., Dmochowska A., Jablonowska A., Dziembowski A., Bartnik E., Stepien P.P. Yeast nuclear PET127 gene can suppress deletions of the SUV3 or DSS1 genes: an indication of a functional interaction between 3' and 5' ends of mitochondrial mRNAs. Acta Biochim. Pol. 1998, 45:935-940.
36. Dake E., Hofmann T.J., McIntire S., Hudson A., Zassenhaus H.P. Purification and properties of the major nuclease from mitochondria of Saccharomyces cerevisiae. J. Biol. Chem. 1988, 263:7691-7702.
37. Vincent R.D., Hofmann T.J., Zassenhaus H.P. Sequence and expression of NUC1, the gene encoding the mitochondrial nuclease in Saccharomyces cerevisiae. Nucleic Acids Res. 1988, 16:3297-3312.
38. Zassenhaus H.P., Hofmann T.J., Uthayashanker R., Vincent R.D., Zona M. Construction of a yeast mutant lacking the mitochondrial nuclease. Nucleic Acids Res. 1988, 16:3283-3296.
39. Burhans W.C., Weinberger M. Yeast endonuclease G: complex matters of death, and of life. Mol. Cell 2007, 25:323-325.
40. Buttner S., Carmona-Gutierrez D., Vitale I., Castedo M., Ruli D., Eisenberg T., Kroemer G., Madeo F. Depletion of endonuclease G selectively kills polyploid cells. Cell Cycle 2007, 6:1072-1076.
41. Buttner S., Eisenberg T., Carmona-Gutierrez D., Ruli D., Knauer H., Ruckenstuhl C., Sigrist C., Wissing S., Kollroser M., Frohlich K.U., Sigrist S., Madeo F. Endonuclease G regulates budding yeast life and death. Mol. Cell 2007, 25:233-246.
42. Zassenhaus H.P., Denniger G. Analysis of the role of the NUC1 endo/exonuclease in yeast mitochondrial DNA recombination. Curr. Genet. 1994, 25:142-149.
43. Huh W.K., Falvo J.V., Gerke L.C., Carroll A.S., Howson R.W., Weissman J.S., O'Shea E.K. Global analysis of protein localization in budding yeast. Nature 2003, 425:686-691.
44. Reinders J., Zahedi R.P., Pfanner N., Meisinger C., Sickmann A. Toward the complete yeast mitochondrial proteome: multidimensional separation techniques for mitochondrial proteomics. J. Proteome Res. 2006, 5:1543-1554.
45. Malecki M., Jedrzejczak R., Puchta O., Stepien P.P., Golik P. In vivo and in vitro approaches for studying the yeast mitochondrial RNA degradosome complex. Methods Enzymol. 2008, 447:463-488.
46. Malecki M., Jedrzejczak R., Stepien P.P., Golik P. In vitro reconstitution and characterization of the yeast mitochondrial degradosome complex unravels tight functional interdependence. J. Mol. Biol. 2007, 372:23-36.
47. Malecki M., Stepien P.P., Golik P. Assays of the helicase, ATPase, and exoribonuclease activities of the yeast mitochondrial degradosome. Methods Mol. Biol. 2010, 587:339-358.
48. Cannistraro V.J., Kennell D. The processive reaction mechanism of ribonuclease II. J. Mol. Biol. 1994, 243:930-943.
49. Cannistraro V.J., Kennell D. The reaction mechanism of ribonuclease II and its interaction with nucleic acid secondary structures. Biochim. Biophys. Acta 1999, 1433:170-187.
50. Cheng Z.F., Deutscher M.P. Purification and characterization of the Escherichia coli exoribonuclease RNase R. Comparison with RNase II. J. Biol. Chem. 2002, 277:21624-21629.
51. Dziembowski A., Lorentzen E., Conti E., Seraphin B. A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat. Struct. Mol. Biol. 2007, 14:15-22.
52. Py B., Higgins C.F., Krisch H.M., Carpousis A.J. A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature 1996, 381:169-172.
53. Anderson J.S., Parker R.P. The 3' to 5' degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3' to 5' exonucleases of the exosome complex. EMBO J. 1998, 17:1497-1506.
54. Tran H., Schilling M., Wirbelauer C., Hess D., Nagamine Y. Facilitation of mRNA deadenylation and decay by the exosome-bound, DExH protein RHAU. Mol. Cell 2004, 13:101-111.
55. Dumont S., Cheng W., Serebrov V., Beran R.K., Tinoco I., Pyle A.M., Bustamante C. RNA translocation and unwinding mechanism of HCV NS3 helicase and its coordination by ATP. Nature 2006, 439:105-108.
56. Jankowsky E., Gross C.H., Shuman S., Pyle A.M. The DExH protein NPH-II is a processive and directional motor for unwinding RNA. Nature 2000, 403:447-451.
57. Kim J.L., Morgenstern K.A., Griffith J.P., Dwyer M.D., Thomson J.A., Murcko M.A., Lin C., Caron P.R. Hepatitis C virus NS3 RNA helicase domain with a bound oligonucleotide: the crystal structure provides insights into the mode of unwinding. Structure 1998, 6:89-100.
58. Frazao C., McVey C.E., Amblar M., Barbas A., Vonrhein C., Arraiano C.M., Carrondo M.A. Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 2006, 443:110-114.
59. Lorentzen E., Basquin J., Tomecki R., Dziembowski A., Conti E. Structure of the active subunit of the yeast exosome core, Rrp44: diverse modes of substrate recruitment in the RNase II nuclease family. Mol. Cell 2008, 29:717-728.
60. Minczuk M., Dmochowska A., Palczewska M., Stepien P.P. Overexpressed yeast mitochondrial putative RNA helicase Mss116 partially restores proper mtRNA metabolism in strains lacking the Suv3 mtRNA helicase. Yeast 2002, 19:1285-1293.
61. Mattiacio J.L., Read L.K. Roles for TbDSS-1 in RNA surveillance and decay of maturation by-products from the 12S rRNA locus. Nucleic Acids Res. 2008, 36:319-329.
62. Mattiacio J.L., Read L.K. Evidence for a degradosome-like complex in the mitochondria of Trypanosoma brucei. FEBS Lett. 2009, 583:2333-2338.
63. Golik P., Zwolinska U., Stepien P.P., Lazowska J. The SUV3 gene from Saccharomyces douglasii is a functional equivalent of its Saccharomyces cerevisiae orthologue and is essential for respiratory growth. FEMS Yeast Res. 2004, 4:477-485.
64. Chabrier-Rosello Y., Giesselman B.R., De Jesus-Andino F.J., Foster T.H., Mitra S., Haidaris C.G. Inhibition of electron transport chain assembly and function promotes photodynamic killing of Candida. J. Photochem. Photobiol. B 2010, 99:117-125.
65. Fuchs B.B., Eby J., Nobile C.J., El Khoury J.B., Mitchell A.P., Mylonakis E. Role of filamentation in Galleria mellonella killing by Candida albicans. Microbes Infect. 2010, 12:488-496.
66. Nobile C.J., Bruno V.M., Richard M.L., Davis D.A., Mitchell A.P. Genetic control of chlamydospore formation in Candida albicans. Microbiology 2003, 149:3629-3637.
67. Richard M.L., Nobile C.J., Bruno V.M., Mitchell A.P. Candida albicans biofilm-defective mutants. Eukaryot. Cell 2005, 4:1493-1502.
68. Hoffmann B., Nickel J., Speer F., Schafer B. The 3' ends of mature transcripts are generated by a processosome complex in fission yeast mitochondria. J. Mol. Biol. 2008, 377:1024-1037.
69. Schafer B., Hansen M., Lang B.F. Transcription and RNA-processing in fission yeast mitochondria. RNA 2005, 11:785-795.
70. Wiesenberger G., Speer F., Haller G., Bonnefoy N., Schleiffer A., Schafer B. RNA degradation in fission yeast mitochondria is stimulated by a member of a new family of proteins that are conserved in lower eukaryotes. J. Mol. Biol. 2007, 367:681-691.
71. 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., Schreier P.H., Smith A.J., Staden R., Young I.G. Sequence and organization of the human mitochondrial genome. Nature 1981, 290:457-465.
72. Brzezniak L.K., Bijata M., Szczesny R.J., Stepien P.P. Involvement of human ELAC2 gene product in 3' end processing of mitochondrial tRNAs. RNA Biol. 2011, 8:616-626.
73. Holzmann J., Frank P., Loffler E., Bennett K.L., Gerner C., Rossmanith W. RNase P without RNA: identification and functional reconstitution of the human mitochondrial tRNA processing enzyme. Cell 2008, 135:462-474.
74. Lopez Sanchez M.I., Mercer T.R., Davies S.M., Shearwood A.M., Nygard K.K., Richman T.R., Mattick J.S., Rackham O., Filipovska A. RNA processing in human mitochondria. Cell Cycle 2011, 10:2904-2916.
75. Ojala D., Montoya J., Attardi G. tRNA punctuation model of RNA processing in human mitochondria. Nature 1981, 290:470-474.
76. Tomecki R., Dmochowska A., Gewartowski K., Dziembowski A., Stepien P.P. Identification of a novel human nuclear-encoded mitochondrial poly(A) polymerase. Nucleic Acids Res. 2004, 32:6001-6014.
77. Rorbach J., Nicholls T.J., Minczuk M. PDE12 removes mitochondrial RNA poly(A) tails and controls translation in human mitochondria. Nucleic Acids Res. 2011, 39:7750-7763.
78. Wydro M., Bobrowicz A., Temperley R.J., Lightowlers R.N., Chrzanowska-Lightowlers Z.M. Targeting of the cytosolic poly(A) binding protein PABPC1 to mitochondria causes mitochondrial translation inhibition. Nucleic Acids Res. 2010, 38:3732-3742.
79. Slomovic S., Laufer D., Geiger D., Schuster G. Polyadenylation and degradation of human mitochondrial RNA: the prokaryotic past leaves its mark. Mol. Cell. Biol. 2005, 25:6427-6435.
80. Bobrowicz A.J., Lightowlers R.N., Chrzanowska-Lightowlers Z. Polyadenylation and degradation of mRNA in mammalian mitochondria: a missing link?. Biochem. Soc. Trans. 2008, 36:517-519.
81. Nagaike T., Suzuki T., Ueda T. Polyadenylation in mammalian mitochondria: insights from recent studies. Biochim. Biophys. Acta 2008, 1779:266-269.
82. Schuster G., Stern D. RNA polyadenylation and decay in mitochondria and chloroplasts. Prog. Mol. Biol. Transl. Sci. 2009, 85:393-422.
83. Dmochowska A., Kalita K., Krawczyk M., Golik P., Mroczek K., Lazowska J., Stepien P.P., Bartnik E. A human putative Suv3-like RNA helicase is conserved between Rhodobacter and all eukaryotes. Acta Biochim. Pol. 1999, 46:155-162.
84. Minczuk M., Lilpop J., Boros J., Stepien P.P. The 5' region of the human hSUV3 gene encoding mitochondrial DNA and RNA helicase: promoter characterization and alternative pre-mRNA splicing. Biochim. Biophys. Acta 2005, 1729:81-87.
85. Minczuk M., Piwowarski J., Papworth M.A., Awiszus K., Schalinski S., Dziembowski A., Dmochowska A., Bartnik E., Tokatlidis K., Stepien P.P., Borowski P. Localisation of the human hSuv3p helicase in the mitochondrial matrix and its preferential unwinding of dsDNA. Nucleic Acids Res. 2002, 30:5074-5086.
86. Bogenhagen D.F., Rousseau D., Burke S. The layered structure of human mitochondrial DNA nucleoids. J. Biol. Chem. 2008, 283:3665-3675.
87. Wang Y., Bogenhagen D.F. Human mitochondrial DNA nucleoids are linked to protein folding machinery and metabolic enzymes at the mitochondrial inner membrane. J. Biol. Chem. 2006, 281:25791-25802.
88. Szczesny R.J., Obriot H., Paczkowska A., Jedrzejczak R., Dmochowska A., Bartnik E., Formstecher P., Polakowska R., Stepien P.P. Down-regulation of human RNA/DNA helicase SUV3 induces apoptosis by a caspase- and AIF-dependent pathway. Biol. Cell 2007, 99:323-332.
89. Veno S.T., Kulikowicz T., Pestana C., Stepien P.P., Stevnsner T., Bohr V.A. The human Suv3 helicase interacts with replication protein A and flap endonuclease 1 in the nucleus. Biochem. J. 2011, 440:293-300.
90. Shu Z., Vijayakumar S., Chen C.F., Chen P.L., Lee W.H. Purified human SUV3p exhibits multiple-substrate unwinding activity upon conformational change. Biochemistry 2004, 43:4781-4790.
91. Venoe S., Kulikowicz T., Pestana C., Stepien P., Stevnsner T., Bohr V. The Human Suv3 Helicase Interacts with Replication Protein A and Flap Endonuclease 1 in the Nucleus. Biochem. J. 2011, 440:293-300.
92. Wang D.D., Shu Z., Lieser S.A., Chen P.L., Lee W.H. 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. 2009, 284:20812-20821.
93. Khidr L., Wu G., Davila A., Procaccio V., Wallace D., Lee W.H. Role of SUV3 helicase in maintaining mitochondrial homeostasis in human cells. J. Biol. Chem. 2008, 283:27064-27073.
94. Szczesny R.J., Borowski L.S., Brzezniak L.K., Dmochowska A., Gewartowski K., Bartnik E., Stepien P.P. Human mitochondrial RNA turnover caught in flagranti: involvement of hSuv3p helicase in RNA surveillance. Nucleic Acids Res. 2010, 38:279-298.
95. Aloni Y., Attardi G. Symmetrical in vivo transcription of mitochondrial DNA in HeLa cells. Proc. Natl. Acad. Sci. U. S. A. 1971, 68:1757-1761.
96. Taanman J.W. The mitochondrial genome: structure, transcription, translation and replication. Biochim. Biophys. Acta 1999, 1410:103-123.
97. Houseley J., Tollervey D. The many pathways of RNA degradation. Cell 2009, 136:763-776.
98. Mukherjee S., Mahata B., Mahato B., Adhya S. Targeted mRNA degradation by complex-mediated delivery of antisense RNAs to intracellular human mitochondria. Hum. Mol. Genet. 2008, 17:1292-1298.
99. Aphasizheva I., Aphasizhev R. RET1-catalyzed uridylylation shapes the mitochondrial transcriptome in Trypanosoma brucei. Mol. Cell. Biol. 2010, 30:1555-1567.
100. Slomovic S., Schuster G. Stable PNPase RNAi silencing: its effect on the processing and adenylation of human mitochondrial RNA. RNA 2008, 14:310-323.
101. Le Roy F., Bisbal C., Silhol M., Martinand C., Lebleu B., Salehzada T. The 2-5A/RNase L/RNase L inhibitor (RLI) [correction of (RNI)] pathway regulates mitochondrial mRNAs stability in interferon alpha-treated H9 cells. J. Biol. Chem. 2001, 276:48473-48482.
102. Le Roy F., Silhol M., Salehzada T., Bisbal C. Regulation of mitochondrial mRNA stability by RNase L is translation-dependent and controls IFNalpha-induced apoptosis. Cell Death Differ. 2007, 14:1406-1413.
103. Chandrasekaran K., Mehrabian Z., Li X.L., Hassel B. RNase-L regulates the stability of mitochondrial DNA-encoded mRNAs in mouse embryo fibroblasts. Biochem. Biophys. Res. Commun. 2004, 325:18-23.
104. Chen H.W., Koehler C.M., Teitell M.A. Human polynucleotide phosphorylase: location matters. Trends Cell Biol. 2007, 17:600-608.
105. Leszczyniecka M., Su Z.Z., Kang D.C., Sarkar D., Fisher P.B. Expression regulation and genomic organization of human polynucleotide phosphorylase, hPNPase(old-35), a Type I interferon inducible early response gene. Gene 2003, 316:143-156.
106. Lange H., Sement F.M., Canaday J., Gagliardi D. Polyadenylation-assisted RNA degradation processes in plants. Trends Plant Sci. 2009, 14:497-504.
107. Walter M., Kilian J., Kudla J. PNPase activity determines the efficiency of mRNA 3'-end processing, the degradation of tRNA and the extent of polyadenylation in chloroplasts. EMBO J. 2002, 21:6905-6914.
108. Holec S., Lange H., Kuhn K., Alioua M., Borner T., Gagliardi D. Relaxed transcription in Arabidopsis mitochondria is counterbalanced by RNA stability control mediated by polyadenylation and polynucleotide phosphorylase. Mol. Cell. Biol. 2006, 26:2869-2876.
109. Leszczyniecka M., Kang D.C., Sarkar D., Su Z.Z., Holmes M., Valerie K., Fisher P.B. Identification and cloning of human polynucleotide phosphorylase, hPNPase old-35, in the context of terminal differentiation and cellular senescence. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:16636-16641.
110. Piwowarski J., Grzechnik P., Dziembowski A., Dmochowska A., Minczuk M., Stepien P.P. Human polynucleotide phosphorylase, hPNPase, is localized in mitochondria. J. Mol. Biol. 2003, 329:853-857.
111. Portnoy V., Palnizky G., Yehudai-Resheff S., Glaser F., Schuster G. Analysis of the human polynucleotide phosphorylase (PNPase) reveals differences in RNA binding and response to phosphate compared to its bacterial and chloroplast counterparts. RNA 2008, 14:297-309.
112. 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., French S.W. Mammalian polynucleotide phosphorylase is an intermembrane space RNase that maintains mitochondrial homeostasis. Mol. Cell. Biol. 2006, 26:8475-8487.
113. Nagaike T., Suzuki T., Katoh T., Ueda T. Human mitochondrial mRNAs are stabilized with polyadenylation regulated by mitochondria-specific poly(A) polymerase and polynucleotide phosphorylase. J. Biol. Chem. 2005, 280:19721-19727.
114. Wang G., Chen H.W., Oktay Y., Zhang J., Allen E.L., Smith G.M., Fan K.C., Hong J.S., French S.W., McCaffery J.M., Lightowlers R.N., Morse H.C., Koehler C.M., Teitell M.A. PNPASE regulates RNA import into mitochondria. Cell 2010, 142:456-467.
115. Liou G.G., Jane W.N., Cohen S.N., Lin N.S., Lin-Chao S. RNA degradosomes exist in vivo in Escherichia coli as multicomponent complexes associated with the cytoplasmic membrane via the N-terminal region of ribonuclease E. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:63-68.
116. Liou G.G., Chang H.Y., Lin C.S., Lin-Chao S. DEAD box RhlB RNA helicase physically associates with exoribonuclease PNPase to degrade double-stranded RNA independent of the degradosome-assembling region of RNase E. J. Biol. Chem. 2002, 277:41157-41162.