Mammalian mitochondrial RNAs are degraded in the mitochondrial intermembrane space by RNASET2
Received date: 30 Jun 2017
Accepted date: 06 Jul 2017
Published date: 06 Nov 2017
Copyright
Mammalian mitochondrial genome encodes a small set of tRNAs, rRNAs, and mRNAs. The RNA synthesis process has been well characterized. How the RNAs are degraded, however, is poorly understood. It was long assumed that the degradation happens in the matrix where transcription and translation machineries reside. Here we show that contrary to the assumption, mammalian mitochondrial RNA degradation occurs in the mitochondrial intermembrane space (IMS) and the IMSlocalized RNASET2 is the enzyme that degrades the RNAs. This provides a new paradigm for understanding mitochondrial RNA metabolism and transport.
Key words: mitochondria; intermembrane space; ribonuclease; mtRNA; RNA degradation; decay; RNASET2; RNase T2; inner membrane; transport; RNA trafficking
Peipei Liu , Jinliang Huang , Qian Zheng , Leiming Xie , Xinping Lu , Jie Jin , Geng Wang . Mammalian mitochondrial RNAs are degraded in the mitochondrial intermembrane space by RNASET2[J]. Protein & Cell, 2017 , 8(10) : 735 -749 . DOI: 10.1007/s13238-017-0448-9
1 |
AcquatiF, BertilaccioS, GrimaldiA, MontiL, CinquettiR, BonettiP, LualdiM, VidalinoL, FabbriM, SaccoMG
|
2 |
AlfonzoJD, ThiemannOH, SimpsonL (1998) Purification and characterization of MAR1. A mitochondrial associated ribonuclease from Leishmania tarentolae.J Biol Chem273:30003–30011
|
3 |
AndersonS, BankierAT, BarrellBG, de BruijnMH, CoulsonAR, DrouinJ, EperonIC, NierlichDP, RoeBA, SangerF
|
4 |
Bienertova-VaskuJ, SanaJ, SlabyO (2013) The role of microRNAs in mitochondria in cancer.Cancer Lett336:1–7
|
5 |
BonawitzND, RodehefferMS, ShadelGS (2006) Defective mitochondrial gene expression results in reactive oxygen speciesmediated inhibition of respiration and reduction of yeast life span.Mol Cell Biol26:4818–4829
|
6 |
BorowskiLS, DziembowskiA, HejnowiczMS, StepienPP, SzczesnyRJ (2013) Human mitochondrial RNA decay mediated by PNPase-hSuv3 complex takes place in distinct foci.Nucleic Acids Res41:1223–1240
|
7 |
BruniF, GramegnaP, OliveiraJM, LightowlersRN, Chrzanowska-LightowlersZM (2013) REXO2 is an oligoribonuclease active in human mitochondria.PLoS ONE8:e64670
|
8 |
ChangDD, ClaytonDA (1989) Mouse RNAase MRP RNA is encoded by a nuclear gene and contains a decamer sequence complementary to a conserved region of mitochondrial RNA substrate.Cell56:131–139
|
9 |
ChenHW, RaineyRN, BalatoniCE, DawsonDW, TrokeJJ, WasiakS, HongJS, McBrideHM, KoehlerCM, TeitellMA
|
10 |
ChujoT, OhiraT, SakaguchiY, GoshimaN, NomuraN, NagaoA, SuzukiT (2012) LRPPRC/SLIRP suppresses PNPase-mediated mRNA decay and promotes polyadenylation in human mitochondria.Nucleic Acids Res40:8033–8047
|
11 |
ClementeP, PajakA, LaineI, WibomR,WedellA,FreyerC,WredenbergA (2015) SUV3 helicase is required for correct processing of mitochondrial transcripts.Nucleic Acids Res43:7398–7413
|
12 |
CoteJ, Ruiz-CarrilloA (1993) Primers for mitochondrial DNA replication generated by endonuclease G.Science261:765–769
|
13 |
DaoudR, ForgetL, LangBF (2012) Yeast mitochondrial RNase P, RNase Z and the RNA degradosome are part of a stable supercomplex.Nucleic Acids Res40:1728–1736
|
14 |
DuarteFV, PalmeiraCM, RoloAP (2015) The emerging role of MitomiRs in the pathophysiology of human disease.Adv Exp Med Biol888:123–154
|
15 |
DucheneAM, PujolC, Marechal-DrouardL (2009) Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria.Curr Genet55:1–18
|
16 |
DziembowskiA, MalewiczM, MinczukM, GolikP, DmochowskaA, StepienPP (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 Genet260:108–114
|
17 |
HallbergBM, LarssonNG (2014) Making proteins in the powerhouse.Cell Metab20:226–240
|
18 |
HanS, UdeshiND, DeerinckTJ, SvinkinaT, EllismanMH, CarrSA, TingAY (2017) Proximity biotinylation as a method for mapping proteins associated with mtDNA in living cells.Cell Chem Biol24:404–414
|
19 |
HennekeM, DiekmannS, OhlenbuschA, KaiserJ, EngelbrechtV, KohlschutterA, KratznerR, Madruga-GarridoM, MayerM, OpitzL
|
20 |
IrieM (1999) Structure-function relationships of acid ribonucleases: lysosomal, vacuolar, and periplasmic enzymes.Pharmacol Ther81:77–89
|
21 |
JanCH, WilliamsCC, WeissmanJS (2014) Principles of ER cotranslational translocation revealed by proximity-specific ribosome profiling.Science346:1257521
|
22 |
KhidrL,WuG,DavilaA, ProcaccioV, WallaceD, LeeWH (2008) Role of SUV3 helicase in maintaining mitochondrial homeostasis in human cells.J Biol Chem283:27064–27073
|
23 |
KimDI, RouxKJ (2016) Filling the void: proximity-based labeling of proteins in living cells.Trends Cell Biol26:804–817
|
24 |
LevyS, AllerstonCK, LiveanuV, HabibMR, GileadiO, SchusterG (2016) Identification of LACTB2, a metallo-beta-lactamase protein, as a human mitochondrial endoribonuclease.Nucleic Acids Res44:1813–1832
|
25 |
LuhtalaN, ParkerR (2010) T2 Family ribonucleases: ancient enzymes with diverse roles.Trends Biochem Sci35:253–259
|
26 |
MaleckiM, StepienPP, GolikP (2010) Assays of the helicase, ATPase, and exoribonuclease activities of the yeast mitochondrial degradosome.Methods Mol Biol587:339–358
|
27 |
MargossianSP, LiH, ZassenhausHP, ButowRA (1996) The DExH box protein Suv3p is a component of a yeast mitochondrial 3’-to-5’ exoribonuclease that suppresses group I intron toxicity.Cell84:199–209
|
28 |
MercerTR, NephS, DingerME, CrawfordJ, SmithMA, ShearwoodAM, HaugenE, BrackenCP, RackhamO, StamatoyannopoulosJA
|
29 |
MiczakA, KaberdinVR, WeiCL, Lin-ChaoS (1996) Proteins associated with RNase E in a multicomponent ribonucleolytic complex.Proc Natl Acad Sci USA93:3865–3869
|
30 |
MishraP, ChanDC (2016) Metabolic regulation of mitochondrial dynamics.J Cell Biol212:379–387
|
31 |
Nesiel-NuttmanL, DoronS, SchwartzB, ShoseyovO (2015) Human RNASET2 derivatives as potential anti-angiogenic agents: actin binding sequence identification and characterization.Oncoscience2:31–43
|
32 |
NohJH, KimKM, AbdelmohsenK, YoonJH, PandaAC, MunkR, KimJ, CurtisJ, MoadCA, WohlerCM
|
33 |
OhsatoT, IshiharaN, MutaT, UmedaS, IkedaS, MiharaK, HamasakiN, KangD (2002) Mammalian mitochondrial endonuclease G. Digestion of R-loops and localization in intermembrane space.Eur J Biochem FEBS269:5765–5770
|
34 |
PortnoyV, PalnizkyG, Yehudai-ResheffS, GlaserF, SchusterG (2008) Analysis of the human polynucleotide phosphorylase (PNPase) reveals differences in RNA binding and response to phosphate compared to its bacterial and chloroplast counterparts.RNA14:297–309
|
35 |
RouxKJ, KimDI, RaidaM, BurkeB (2012) A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells.J Cell Biol196:801–810
|
36 |
RubioMA, RinehartJJ, KrettB, Duvezin-CaubetS, ReichertAS, SollD, AlfonzoJD (2008) Mammalian mitochondria have the innate ability to import tRNAs by a mechanism distinct from protein import.Proc Natl Acad Sci USA105:9186–9191
|
37 |
SanchezMI, MercerTR, DaviesSM, ShearwoodAM, NygardKK, RichmanTR, MattickJS, RackhamO, FilipovskaA (2011) RNA processing in human mitochondria.Cell Cycle10:2904–2916
|
38 |
SarkarD, ParkES, EmdadL, RandolphA, ValerieK, FisherPB (2005) Defining the domains of human polynucleotide phosphorylase (hPNPaseOLD-35) mediating cellular senescence.Mol Cell Biol25:7333–7343
|
39 |
SatoR, Arai-IchinoiN, KikuchiA, MatsuhashiT, Numata-UematsuY, UematsuM, FujiiY, MurayamaK, OhtakeA, AbeT
|
40 |
SchaferB, HansenM, LangBF (2005) Transcription and RNAprocessing in fission yeast mitochondria.RNA11:785–795
|
41 |
SimpsonAM, BakalaraN, SimpsonL (1992) A ribonuclease activity is activated by heparin or by digestion with proteinase K in mitochondrial extracts of Leishmania tarentolae.J Biol Chem267:6782–6788
|
42 |
SlomovicS, PortnoyV, Yehudai-ResheffS, BronshteinE, SchusterG (2008) Polynucleotide phosphorylase and the archaeal exosome as poly(A)-polymerases.Biochim et Biophys Acta1779:247–255
|
43 |
SlomovicS, SchusterG (2008) Stable PNPase RNAi silencing: its effect on the processing and adenylation of human mitochondrial RNA.RNA14:310–323
|
44 |
SmirnovA, EntelisN, MartinRP, TarassovI (2011) Biological significance of 5S rRNA import into human mitochondria: role of ribosomal protein MRP-L18.Genes Dev25:1289–1305
|
45 |
SzczesnyRJ, BorowskiLS, MaleckiM, WojcikMA, StepienPP, GolikP (2012) RNA degradation in yeast and human mitochondria.Biochim et Biophys Acta1819:1027–1034
|
46 |
SzczesnyRJ, WojcikMA, BorowskiLS, SzewczykMJ, SkrokMM, GolikP, StepienPP (2013) Yeast and human mitochondrial helicases.Biochim et Biophys Acta1829:842–853
|
47 |
VedrenneV, GowherA, De LonlayP, NitschkeP, SerreV, BoddaertN, AltuzarraC, Mager-HeckelAM, ChretienF, EntelisN
|
48 |
von AmelnS, WangG, BoulouizR, RutherfordMA, SmithGM, LiY, PogodaHM, NurnbergG, StillerB, VolkAE
|
49 |
WangG, ChenHW, OktayY, ZhangJ, AllenEL, SmithGM, FanKC, HongJS, FrenchSW, McCafferyJM
|
50 |
WilliamsCC, JanCH, WeissmanJS (2014) Targeting and plasticity of mitochondrial proteins revealed by proximity-specific ribosome profiling.Science346:748–751
|
51 |
ZhangX, ZuoX, YangB, LiZ, XueY, ZhouY, HuangJ, ZhaoX, ZhouJ, YanY
|
52 |
ZhouQ, LiH, LiH, NakagawaA, LinJL, LeeES, HarryBL, Skeen-GaarRR, SuehiroY, WilliamD
|
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