REXO2 Is an Oligoribonuclease Active in Human Mitochondria

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Bruni, Francesco ^a   Gramegna, Pasqua ^a   Oliveira, Jorge M A ^b   Lightowlers, Robert N ^a   Chrzanowska Lightowlers, Zofia M A ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PROTEIN REXO2; RIBONUCLEASE; RNA; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOLIC FRACTION; DNA CONTENT; ENZYME ACTIVITY; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MITOCHONDRION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN DEPLETION; PROTEIN SYNTHESIS; RNA INTERFERENCE;

14-3-3 PROTEINS; ESCHERICHIA COLI; EXORIBONUCLEASES; HELA CELLS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; NUCLEIC ACIDS; PROTEIN BIOSYNTHESIS; RNA, SMALL INTERFERING; TUMOR MARKERS, BIOLOGICAL;

ESCHERICHIA COLI;

EID: 84878568476     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064670     Document Type: Article

References (51)

1. Arraiano C, Andrade JM, Domingues S, Guinote IB, Malecki M, et al. (2010) The critical role of RNA processing and degradation in the control of gene expression. FEMS microbiology reviews 34(5): 883-923.
2. Zuo Y, Deutscher MP, (2001) Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic acids research 29(5): 1017-1026.
3. Steitz TA, Steitz JA, (1993) A general two-metal-ion mechanism for catalytic RNA. Proc Natl Acad Sci U S A 90(14): 6498-6502.
4. Bernad A, Blanco L, Lazaro JM, Martin G, Salas M, (1989) A conserved 3′-5′ exonuclease active site in prokaryotic and eukaryotic DNA polymerases. Cell 59(1): 219-228.
5. Koonin EV, (1997) A conserved ancient domain joins the growing superfamily of 3′-5′ exonucleases. Current biology: CB 7(10): R604-606.
6. Zhang X, Zhu L, Deutscher MP, (1998) Oligoribonuclease is encoded by a highly conserved gene in the 3′-5′ exonuclease superfamily. Journal of bacteriology 180(10): 2779-2781.
7. Ghosh S. Deutscher MP, (1999) Oligoribonuclease is an essential component of the mRNA decay pathway. Proc Natl Acad Sci U S A 96(8): 4372-4377.
8. Goldman SR, Sharp JS, Vvedenskaya IO, Livny J, Dove SL, et al. (2011) NanoRNAs prime transcription initiation in vivo. Molecular cell 42(6): 817-825.
9. Hanekamp T, Thorsness PE, (1999) YNT20, a bypass suppressor of yme1 yme2, encodes a putative 3′-5′ exonuclease localized in mitochondria of Saccharomyces cerevisiae. Current genetics 34(6): 438-448.
10. Leonhard K, Herrmann JM, Stuart RA, Mannhaupt G, Neupert W, et al. (1996) AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria. EMBO Journal 15(16): 4218-4229.
11. van Hoof A, Lennertz P, Parker R, (2000) Three conserved members of the RNase D family have unique and overlapping functions in the processing of 5S, 5.8S, U4, U5, RNase MRP and RNase P RNAs in yeast. The EMBO journal 19(6): 1357-1365.
12. Rorbach J, Minczuk M, (2012) The post-transcriptional life of mammalian mitochondrial RNA. The Biochemical Journal 444(3): 357-373.
13. King MP, Attardi G, (1989) Human Cells Lacking mtDNA: Repopulation with Exogenous Mitochondria by Complementation. Science 246: 500-503.
14. Soleimanpour-Lichaei HR, Kuhl I, Gaisne M, Passos JF, Wydro M, et al. (2007) mtRF1a is a human mitochondrial translation release factor decoding the major termination codons UAA and UAG. Molecular Cell 27(5): 745-757.
15. Ovcharenko D, Jarvis R, Hunicke-Smith S, Kelnar K, Brown D, (2005) High-throughput RNAi screening in vitro: from cell lines to primary cells. RNA 11(6): 985-993.
16. Rorbach J, Richter R, Wessels HJ, Wydro M, Pekalski M, et al. (2008) The human mitochondrial ribosome recycling factor is essential for cell viability. Nucleic Acids Research 36(18): 5787-5799.
17. Oliveira JM, (2011) Techniques to investigate neuronal mitochondrial function and its pharmacological modulation. Current Drug Targets 12(6): 762-773.
18. Chrzanowska-Lightowlers ZM, Preiss T, Lightowlers RN, (1994) Inhibition of mitochondrial protein synthesis promotes increased stability of nuclear-encoded respiratory gene transcripts. The Journal of Biological Chemistry 269(44): 27322-27328.
19. Rorbach J, Yusoff AA, Tuppen H, Abg-Kamaludin DP, Chrzanowska-Lightowlers ZM, et al. (2008) Overexpression of human mitochondrial valyl tRNA synthetase can partially restore levels of cognate mt-tRNAVal carrying the pathogenic C25U mutation. Nucleic Acids Research 36(9): 3065-3074.
20. Anderson S, Bankier AT, Barrell BG, De Bruijn MHL, Coulson AR, et al. (1981) Sequence and organization of the human mitochondrial genome. Nature 290(5806): 457-465.
21. Andrews RM, Kubacka I, Chinnery PF, Lightowlers RN, Turnbull DM, et al. (1999) Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nature Genetics 23(2): 147.
22. Nijtmans LGJ, Henderson N, Holt IJ, (2002) Blue Native electrophoresis to study mitochondrial and other protein complexes. Methods 26: 327-334.
23. Nguyen LH, Erzberger JP, Root J, Wilson DM, (2000) The human homolog of Escherichia coli Orn degrades small single-stranded RNA and DNA oligomers. The Journal of Biological Chemistry 275(34): 25900-25906.
24. Chomyn A, (1996) In vivo labeling and analysis of human mitochondrial translation products. Methods Enzymol. 264: 197-211.
25. Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, et al. (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134(1): 112-123.
26. Kozak M, (1989) Context effects and inefficient initiation at non-AUG codons in eucaryotic cell-free translation systems. Molecular and Cellular Biology 9(11): 5073-5080.
27. Niyogi SK, Datta AK, (1975) A novel oligoribonuclease of Escherichia coli. I. Isolation and properties. The Journal of Biological Chemistry 250(18): 7307-7312.
28. Barni S, Sciola L, Spano A, Pippia P, (1996) Static cytofluorometry and fluorescence morphology of mitochondria and DNA in proliferating fibroblasts. Biotechnic & histochemistry: official publication of the Biological Stain Commission 71(2): 66-70.
29. Margineantu DH, Gregory Cox W, Sundell L, Sherwood SW, Beechem JM, et al. (2002) Cell cycle dependent morphology changes and associated mitochondrial DNA redistribution in mitochondria of human cell lines. Mitochondrion 1(5): 425-435.
30. Chen H, Chan DC, (2009) Mitochondrial dynamics-fusion, fission, movement, and mitophagy in neurodegenerative diseases. Human Molecular Genetics 18(R2): R169-176.
31. Liot G, Bossy B, Lubitz S, Kushnareva Y, Sejbuk N, et al. (2009) Complex II inhibition by 3-NP causes mitochondrial fragmentation and neuronal cell death via an NMDA- and ROS-dependent pathway. Cell Death and Differentiation 16(6): 899-909.
32. Chrzanowska-Lightowlers ZMA, Preiss T, Lightowlers RN, (1994) Inhibition of Mitochondrial Protein Synthesis Promotes Increased Stability of Nuclear-encoded Respiratory Gene Transcripts. The Journal of Biological Chemistry 269(44): 27322-27328.
33. Borowski LS, Szczesny RJ, Brzezniak LK, Stepien PP, (2010) RNA turnover in human mitochondria: more questions than answers? Biochimica et Biophysica Acta 1797(6-7): 1066-1070.
34. Gagliardi D, Stepien PP, Temperley RJ, Lightowlers RN, Chrzanowska-Lightowlers ZM, (2004) Messenger RNA stability in mitochondria: different means to an end. Trends in Genetics 20(6): 260-267.
35. Temperley RJ, Wydro M, Lightowlers RN, Chrzanowska-Lightowlers ZM, (2010) Human mitochondrial mRNAs: like members of all families, similar but different. Biochimica et Biophysica Acta 1797(6-7): 1081-1085.
36. Szczesny RJ, Borowski LS, Malecki M, Wojcik MA, Stepien PP, et al. (2012) RNA degradation in yeast and human mitochondria. Biochimica et Biophysica Acta 1819(9-10): 1027-1034.
37. Szczesny RJ, Borowski LS, Brzezniak LK, Dmochowska A, Gewartowski K, et al. (2010) Human mitochondrial RNA turnover caught in flagranti: involvement of hSuv3p helicase in RNA surveillance. Nucleic Acids Research 38(1): 279-298.
38. Bruni F, Gramegna P, Lightowlers RN, Chrzanowska-Lightowlers ZM, (2012) The mystery of mitochondrial RNases. Biochemical Society Transactions 40(4): 865-869.
39. Karniely S, Pines O (2005) Single translation-dual destination: mechanisms of dual protein targeting in eukaryotes. EMBO reports 6(5): p.420-425.
40. Yogev O, Pines O, (2011) Dual targeting of mitochondrial proteins: mechanism, regulation and function. Biochimica et Biophysica Acta 1808(3): 1012-1020.
41. Rossmanith W, (2011) Localization of human RNase Z isoforms: dual nuclear/mitochondrial targeting of the ELAC2 gene product by alternative translation initiation. PloS One 6(4): e19152.
42. Suzuki Y, Holmes JB, Cerritelli SM, Sakhuja K, Minczuk M, et al. (2010) An upstream open reading frame and the context of the two AUG codons affect the abundance of mitochondrial and nuclear RNase H1. Molecular and Cellular Biology 30(21): 5123-5134.
43. Spelbrink JN, (2010) Functional organization of mammalian mitochondrial DNA in nucleoids: history, recent developments, and future challenges. IUBMB life 62(1): 19-32.
44. Borowski LS, Dziembowski A, Hejnowicz MS, Stepien PP, Szczesny RJ, (2013) Human mitochondrial RNA decay mediated by PNPase-hSuv3 complex takes place in distinct foci. Nucleic Acids Research 41(2): 1223-1240.
45. Chen HW, Rainey RN, Balatoni CE, Dawson DW, Troke JJ, et al. (2006) Mammalian polynucleotide phosphorylase is an intermembrane space RNase that maintains mitochondrial homeostasis. Molecular and Cellular Biology 26(22): 8475-8487.
46. Wang G, Chen HW, Oktay Y, Zhang J, Allen EL, et al. (2010) PNPASE regulates RNA import into mitochondria. Cell 142(3): 456-467.
47. Khidr L, Wu G, Davila A, Procaccio V, Wallace D, et al. (2008) Role of SUV3 helicase in maintaining mitochondrial homeostasis in human cells. The Journal of Biological Chemistry 283(40): 27064-27073.
48. Wang DD, Shu Z, Lieser SA, Chen PL, Lee WH, (2009) Human mitochondrial SUV3 and polynucleotide phosphorylase form a 330-kDa heteropentamer to cooperatively degrade double-stranded RNA with a 3′-to-5′ directionality. The Journal of Biological Chemistry 284(31): 20812-20821.
49. Lin CL, Wang YT, Yang WZ, Hsiao YY, Yuan HS, (2012) Crystal structure of human polynucleotide phosphorylase: insights into its domain function in RNA binding and degradation. Nucleic Acids Research 40(9): 4146-4157.
50. Di Re M, Sembongi H, He J, Reyes A, Yasukawa T, et al. (2009) The accessory subunit of mitochondrial DNA polymerase gamma determines the DNA content of mitochondrial nucleoids in human cultured cells. Nucleic Acids Research 37(17): 5701-5713.
51. Holt IJ, He J, Mao CC, Boyd-Kirkup JD, Martinsson P, et al. (2007) Mammalian mitochondrial nucleoids: organizing an independently minded genome. Mitochondrion 7(5): 311-321.