Regulation Mechanism of Ribonucleases in Escherichia coli

doi:10.13560/j.cnki.biotech.bull.1985.2021-0341

Abstract

Abstract:

Ribonucleases（RNases）involve in almost every aspect of RNA metabolism,and play important regulating role in the physiological functions of bacteria. Bacteria have evolved multiple strategies to regulate RNases to avoid unnecessary RNA degradation. To date,the regulation mechanisms include post-transcriptional regulation,post-translational modification,cellular localization and related trans-acting inhibitors. Here,we systematically describe and explain the classification,function and regulation mechanism of the RNases in E. coli,and summarize the response mechanism of E. coli adaptive regulation to its RNases under different environmental pressures as well as existing issues.

Key words: Escherichia coli, ribonuclease（RNase）, regulation mechanism, RNA metabolism, bacterial stress response

SUN Man-luan, GE Sai, BU Jia, ZHU Zhuang-yan. Regulation Mechanism of Ribonucleases in Escherichia coli[J]. Biotechnology Bulletin, 2022, 38(3): 234-245.

Figures/Tables 6

References 83

[1]	Deutscher MP. Twenty years of bacterial RNases and RNA processing:how we’ve matured[J]. RNA, 2015, 21(4):597-600. doi: 10.1261/rna.049692.115 pmid: 25780155
[2]	de Trinquier A, Durand S, Braun F, et al. Regulation of RNA processing and degradation in bacteria[J]. BBA Gene Regul Mech, 2020, 1863(5):194505.
[3]	Canestrari E, Paroo Z. Ribonucleases as drug targets[J]. Trends Pharmacol Sci, 2018, 39(10):855-866. doi: S0165-6147(18)30121-4 pmid: 30144949
[4]	Vargas-Blanco DA, Shell SS. Regulation of mRNA stability during bacterial stress responses[J]. Front Microbiol, 2020, 11:2111. doi: 10.3389/fmicb.2020.02111 pmid: 33013770
[5]	Barrangou R, Fremaux C, Deveau H, et al. CRISPR provides acquired resistance against viruses in prokaryotes[J]. Science, 2007, 315(5819):1709-1712. doi: 10.1126/science.1138140 pmid: 17379808
[6]	Roux C, Etienne TA, Hajnsdorf E, et al. The essential role of mRNA degradation in understanding and engineering E. coli metabolism[J]. Biotechnol Adv, 2021: 107805.
[7]	Stenum TS, Holmqvist E. CsrA enters Hfq's territory:Regulation of a base-pairing small RNA[J]. Mol Microbiol, 2021:mmi. 14785.
[8]	Bechhofer DH, Deutscher MP. Bacterial ribonucleases and their roles in RNA metabolism[J]. Crit Rev Biochem Mol Biol, 2019, 54(3):242-300. doi: 10.1080/10409238.2019.1651816 URL
[9]	Zhu LQ, Gangopadhyay T, Padmanabha KP, et al. Escherichia coli RNA gene encoding RNase I:cloning, overexpression, subcellular distribution of the enzyme, and use of an RNA deletion to identify additional RNases[J]. J Bacteriol, 1990, 172(6):3146-3151. pmid: 2188952
[10]	Altuvia Y, Bar A, Reiss N, et al. In vivo cleavage rules and target repertoire of RNase III in Escherichia coli[J]. Nucleic Acids Res, 2018, 46(19):10380-10394. doi: 10.1093/nar/gky684 pmid: 30113670
[11]	Lee M, Joo M, Sim M, et al. The coordinated action of RNase III and RNase G controls enolase expression in response to oxygen availability in Escherichia coli[J]. Sci Rep, 2019, 9(1):17257. doi: 10.1038/s41598-019-53883-y URL
[12]	Altuvia S, Storz G, Papenfort K. Cross-regulation between bacteria and phages at a posttranscriptional level[J]. Microbiol Spectr, 2018, 6(4):10. 1128.
[13]	Chu LY, Hsieh TJ, Golzarroshan B, et al. Structural insights into RNA unwinding and degradation by RNase R[J]. Nucleic Acids Res, 2017, 45(20):12015-12024. doi: 10.1093/nar/gkx880 URL
[14]	Perwez T, Kushner SR. RNase Z in Escherichia coli plays a significant role in mRNA decay[J]. Mol Microbiol, 2006, 60(3):723-737. pmid: 16629673
[15]	Chen H, Previero A, Deutscher MP. A novel mechanism of ribonuclease regulation:GcvB and Hfq stabilize the mRNA that encodes RNase BN/Z during exponential phase[J]. J Biol Chem, 2019, 294(52):19997-20008. doi: 10.1074/jbc.RA119.011367 pmid: 31744883
[16]	Bandyra KJ, Luisi BF. RNase E and the high-fidelity orchestration of RNA metabolism[J]. Microbiol Spectr, 2018, 6(2). DOI: 10.1128/microbiolspec.rwr-0008-2017. doi: 10.1128/microbiolspec.rwr-0008-2017
[17]	Ali N, Gowrishankar J. Cross-subunit catalysis and a new phenomenon of recessive resurrection in Escherichia coli RNase E[J]. Nucleic Acids Res, 2020, 48(2):847-861. doi: 10.1093/nar/gkz1152 URL
[18]	Hadjeras L, Poljak L, Bouvier M, et al. Detachment of the RNA degradosome from the inner membrane of Escherichia coli results in a global slowdown of mRNA degradation, proteolysis of RNase E and increased turnover of ribosome-free transcripts[J]. Mol Microbiol, 2019, 111(6):1715-1731. doi: 10.1111/mmi.14248 pmid: 30903628
[19]	Mardle CE, Goddard LR, Spelman BC, et al. Identification and analysis of novel small molecule inhibitors of RNase E:Implications for antibacterial targeting and regulation of RNase E[J]. Biochem Biophys Rep, 2020, 23:100773.
[20]	Moore CJ, Go H, Shin E, et al. Substrate-dependent effects of quaternary structure on RNase E activity[J]. Genes Dev, 2021, 35(3/4):286-299. doi: 10.1101/gad.335828.119 URL
[21]	Hamouche L, Poljak L, Carpousis AJ. Ribosomal RNA degradation induced by the bacterial RNA polymerase inhibitor rifampicin[J]. bioRxiv, 2021. DOI: 10.1101/2021.04.24.441238. doi: 10.1101/2021.04.24.441238
[22]	Mohanty BK, Agrawal A, Kushner SR. Generation of pre-tRNAs from polycistronic operons is the essential function of RNase P in Escherichia coli[J]. Nucleic Acids Res, 2020, 48(5):2564-2578. doi: 10.1093/nar/gkz1188 pmid: 31993626
[23]	Kurata T, Nakanishi S, Hashimoto M, et al. Subunit composition of ribosome in the yqgF mutant Is deficient in pre-16S rRNA processing of Escherichia coli[J]. J Mol Microbiol Biotechnol, 2018, 28(4):179-182. doi: 10.1159/000494494 URL
[24]	Kouzminova EA, Kuzminov A. Ultraviolet-induced RNA:DNA hybrids interfere with chromosomal DNA synjournal[J]. Nucleic Acids Res, 2021, 49(7):3888-3906. doi: 10.1093/nar/gkab147 pmid: 33693789
[25]	Prossliner T, Gerdes K, Sørensen MA, et al. Hibernation factors directly block ribonucleases from entering the ribosome in response to starvation[J]. Nucleic Acids Res, 2021, 49(4):2226-2239. doi: 10.1093/nar/gkab017 pmid: 33503254
[26]	Garcia-Rodriguez G, Charlier D, Wilmaerts D, et al. Alternative dimerization is required for activity and inhibition of the HEPN ribonuclease RnlA[J]. Nucleic Acids Res, 2021, 49(12):7164-7178. doi: 10.1093/nar/gkab513 pmid: 34139012
[27]	Dendooven T, Sinha D, Roeselová A, et al. A cooperative PNPase-Hfq-RNA carrier complex facilitates bacterial riboregulation[J]. Mol Cell, 2021, 81(14):2901- 2913. e5.
[28]	Dressaire C, Pobre V, Laguerre S, et al. PNPase is involved in the coordination of mRNA degradation and expression in stationary phase cells of Escherichia coli[J]. BMC Genomics, 2018, 19(1):848. doi: 10.1186/s12864-018-5259-8 URL
[29]	Park H, Yakhnin H, Connolly M, et al. CsrA participates in a PNPase autoregulatory mechanism by selectively repressing translation of pnp transcripts that have been previously processed by RNase III and PNPase[J]. J Bacteriol, 2015, 197(24):3751-3759. doi: 10.1128/JB.00721-15 URL
[30]	Fontaine F, Gasiorowski E, Gracia C, et al. The small RNA SraG participates in PNPase homeostasis[J]. RNA, 2016, 22(10):1560-1573. doi: 10.1261/rna.055236.115 pmid: 27495318
[31]	Cairrão F, Chora A, Zilhão R, et al. RNase II levels change according to the growth conditions:characterization of gmr, a new Escherichia coli gene involved in the modulation of RNase II[J]. Mol Microbiol, 2001, 39(6):1550-1561. pmid: 11260472
[32]	Lu F, Taghbalout A. Membrane association via an amino-terminal amphipathic helix is required for the cellular organization and function of RNase II[J]. J Biol Chem, 2013, 288(10):7241-7251. doi: 10.1074/jbc.M112.408674 URL
[33]	Song L, Wang G, Malhotra A, et al. Reversible acetylation on Lys501 regulates the activity of RNase II[J]. Nucleic Acids Res, 2016, 44(5):1979-1988. doi: 10.1093/nar/gkw053 URL
[34]	dos Santos RF, Andrade JM, Pissarra J, et al. Hfq and RNase R mediate rRNA processing and degradation in a novel RNA quality control process[J]. mBio, 2020, 11(5):e02398-20.
[35]	Liang W, Deutscher MP. Ribosomes regulate the stability and action of the exoribonuclease RNase R[J]. J Biol Chem, 2013, 288(48):34791-34798. doi: 10.1074/jbc.M113.519553 URL
[36]	Martínez VP, Dehò G, Simons RW, et al. Ribonuclease PH interacts with an acidic ribonuclease E site through a basic 80-amino acid domain[J]. FEMS Microbiol Lett, 2014, 355(1):51-60. doi: 10.1111/fml.2014.355.issue-1 URL
[37]	Sulthana S, Quesada E, Deutscher MP. RNase II regulates RNase PH and is essential for cell survival during starvation and stationary phase[J]. RNA, 2017, 23(9):1456-1464. doi: 10.1261/rna.060558.116 pmid: 28625967
[38]	Zuo Y, Deutscher MP. The physiological role of RNase T can be explained by its unusual substrate specificity[J]. J Biol Chem, 2002, 277(33):29654-29661. doi: 10.1074/jbc.M204252200 URL
[39]	Jain C. RNase AM, a 5' to 3' exonuclease, matures the 5' end of all three ribosomal RNAs in E. coli[J]. Nucleic Acids Res, 2020, 48(10):5616-5623. doi: 10.1093/nar/gkaa260 URL
[40]	Mackie GA. RNase E:at the interface of bacterial RNA processing and decay[J]. Nat Rev Microbiol, 2013, 11(1):45-57. doi: 10.1038/nrmicro2930 URL
[41]	Mohanty BK, Petree JR, Kushner SR. Endonucleolytic cleavages by RNase E generate the mature 3' termini of the three proline tRNAs in Escherichia coli[J]. Nucleic Acids Res, 2016, 44(13):6350-6362. doi: 10.1093/nar/gkw517 pmid: 27288443
[42]	Sulthana S, Basturea GN, Deutscher MP. Elucidation of pathways of ribosomal RNA degradation:an essential role for RNase E[J]. RNA, 2016, 22(8):1163-1171. doi: 10.1261/rna.056275.116 pmid: 27298395
[43]	Ow MC, Kushner SR. Initiation of tRNA maturation by RNase E is essential for cell viability in E. coli[J]. Genes Dev, 2002, 16(9):1102-1115. doi: 10.1101/gad.983502 URL
[44]	Sousa S, Marchand I, Dreyfus M. Autoregulation allows Escherichia coli RNase E to adjust continuously its synjournal to that of its substrates[J]. Mol Microbiol, 2001, 42(3):867-878. pmid: 11722748
[45]	Jain C, Deana A, Belasco JG. Consequences of RNase E scarcity in Escherichia coli[J]. Mol Microbiol, 2002, 43(4):1053-1064. doi: 10.1046/j.1365-2958.2002.02808.x URL
[46]	Mohanty BK, Kushner SR. Polyadenylation of Escherichia coli transcripts plays an integral role in regulating intracellular levels of polynucleotide phosphorylase and RNase E[J]. Mol Microbiol, 2002, 45(5):1315-1324. pmid: 12207699
[47]	Jaso-Vera ME, Domínguez-Malfavón L, Curiel-Quesada E, et al. Dynamics of the canonical RNA degradosome components during glucose stress[J]. Biochimie, 2021, 187:67-74. doi: 10.1016/j.biochi.2021.05.006 pmid: 34022290
[48]	McQuail J, Carpousis AJ, Wigneshweraraj S. The association between Hfq and RNase E in long-term nitrogen starved Escherichia coli[J]. bioRxiv, 2021. DOI: 10.1101/2021.04, 19. 440462. doi: 10.1101/2021.04
[49]	Singh D, Murashko ON, Lin-Chao SE. Posttranscriptional regulation of tnaA by protein-RNA interaction mediated by ribosomal protein L4 in Escherichia coli[J]. J Bacteriol, 2020, 202(10):e00799-19. DOI: 10.1128/jb.00799-19. doi: 10.1128/jb.00799-19
[50]	Lee K, Zhan X, Gao J, et al. RraA. a protein inhibitor of RNase E activity that globally modulates RNA abundance in E. coli[J]. Cell, 2003, 114(5):623-634. doi: 10.1016/j.cell.2003.08.003 URL
[51]	Lim B, Sim M, Lee H, et al. Regulation of Escherichia coli RNase III activity[J]. J Microbiol Seoul Korea, 2015, 53(8):487-494.
[52]	Sirdeshmukh R, Schlessinger D. Ordered processing of Escherichia coli 23S rRNA in vitro[J]. Nucleic Acids Res, 1985, 13(14):5041-5054. pmid: 2991850
[53]	King TC, Sirdeshmukh R, Schlessinger D. RNase III cleavage is obligate for maturation but not for function of Escherichia coli pre-23S rRNA[J]. PNAS, 1984, 81(1):185-188. pmid: 6364133
[54]	Stead MB, Marshburn S, Mohanty BK, et al. Analysis of Escherichia coli RNase E and RNase III activity in vivo using tiling microarrays[J]. Nucleic Acids Res, 2011, 39(8):3188-3203. doi: 10.1093/nar/gkq1242 pmid: 21149258
[55]	Conrad C, Rauhut R. Ribonuclease III:new sense from nuisance[J]. Int J Biochem Cell Biol, 2002, 34(2):116-129. doi: 10.1016/S1357-2725(01)00112-1 URL
[56]	Deutscher MP. Regulation of bacterial ribonucleases[J]. Annu Rev Microbiol, 2021, 75(1). DOI: 10.1146/annurev-micro-020121-011201. doi: 10.1146/annurev-micro-020121-011201
[57]	Lee J, Lee M, Lee K. Trans-acting regulators of ribonuclease activity[J]. J Microbiol, 2021, 59(4):341-359. doi: 10.1007/s12275-021-0650-6 URL
[58]	Paudyal S, Alfonso-Prieto M, Carnevale V, et al. Combined computational and experimental analysis of a complex of ribonuclease III and the regulatory macrodomain protein, YmdB[J]. Proteins, 2015, 83(3):459-472. doi: 10.1002/prot.v83.3 URL
[59]	Kavalchuk K, Madhusudan S, Schnetz K. RNase III initiates rapid degradation of proU mRNA upon hypo-osmotic stress in Escherichia coli[J]. RNA Biol, 2012, 9(1):98-109. doi: 10.4161/rna.9.1.18228 URL
[60]	Song W, Kim YH, Sim SH, et al. Antibiotic stress-induced modulation of the endoribonucleolytic activity of RNase III and RNase G confers resistance to aminoglycoside antibiotics in Escherichia coli[J]. Nucleic Acids Res, 2014, 42(7):4669-4681. doi: 10.1093/nar/gku093 URL
[61]	Li de la Sierra-Gallay I, Pellegrini O, Condon C. Structural basis for substrate binding, cleavage and allostery in the tRNA maturase RNase Z[J]. Nature, 2005, 433(7026):657-661. doi: 10.1038/nature03284 URL
[62]	Chen H, Dutta T, Deutscher MP. Growth phase-dependent variation of RNase BN/Z affects small RNAs[J]. J Biol Chem, 2016, 291(51):26435-26442. pmid: 27875308
[63]	Gupta AK, Siddiqui N, Dutta T. A novel mechanism of RyeA/SraC induction under acid stress[J]. Biochem Biophys Res Commun, 2020, 525(2):298-302. doi: 10.1016/j.bbrc.2020.02.085 URL
[64]	Grünberg S, Coxam B, Chen TH, et al. E. coli RNase I exhibits a strong Ca²⁺-dependent inherent double-stranded RNase activity[J]. Nucleic Acids Res, 2021, 49(9):5265-5277. doi: 10.1093/nar/gkab284 URL
[65]	Fontaine BM, Martin KS, Garcia-Rodriguez JM, et al. RNase I regulates Escherichia coli 2', 3'-cyclic nucleotide monophosphate levels and biofilm formation[J]. Biochem J, 2018, 475(8):1491-1506. doi: 10.1042/BCJ20170906 URL
[66]	Hossain ST, Malhotra A, Deutscher MP. How RNase R degrades structured rna:role of the helicase activity and the S1 domain[J]. J Biol Chem, 2016, 291(15):7877-7887. doi: 10.1074/jbc.M116.717991 URL
[67]	Cheng ZF, Deutscher MP. Purification and characterization of the Escherichia coli exoribonuclease RNase R. Comparison with RNase II[J]. J Biol Chem, 2002, 277(24):21624-21629. doi: 10.1074/jbc.M202942200 URL
[68]	Chen C, Deutscher MP. Elevation of RNase R in response to multiple stress conditions[J]. J Biol Chem, 2005, 280(41):34393-34396. doi: 10.1074/jbc.C500333200 URL
[69]	Liang WX, Malhotra A, Deutscher MP. Acetylation regulates the stability of a bacterial protein:growth stage-dependent modification of RNase R[J]. Mol Cell, 2011, 44(1):160-166. doi: 10.1016/j.molcel.2011.06.037 URL
[70]	Mohanty BK, Kushner SR. Polynucleotide phosphorylase functions both as a 3' right-arrow 5' exonuclease and a poly(A)polymerase in Escherichiacoli[J]. PNAS, 2000, 97(22):11966-11971. pmid: 11035800
[71]	Briani F, Carzaniga T, Dehò G. Regulation and functions of bacterial PNPase[J]. Wiley Interdiscip Rev RNA, 2016, 7(2):241-258. doi: 10.1002/wrna.2016.7.issue-2 URL
[72]	Cameron TA, de Lay NR. The phosphorolytic exoribonucleases polynucleotide phosphorylase and RNase PH stabilize sRNAs and facilitate regulation of their mRNA targets[J]. J Bacteriol, 2016, 198(24):3309-3317. pmid: 27698082
[73]	Saramago M, Bárria C, dos Santos RF, et al. The role of RNases in the regulation of small RNAs[J]. Curr Opin Microbiol, 2014, 18:105-115. doi: 10.1016/j.mib.2014.02.009 URL
[74]	Pobre V, Arraiano CM. Next generation sequencing analysis reveals that the ribonucleases RNase II, RNase R and PNPase affect bacterial motility and biofilm formation in E. coli[J]. BMC Genomics, 2015, 16:72. doi: 10.1186/s12864-015-1237-6 URL
[75]	Wu J, Jiang Z, Liu M, et al. Polynucleotide phosphorylase protects Escherichia coli against oxidative stress[J]. Biochemistry, 2009, 48(9):2012-2020. doi: 10.1021/bi801752p URL
[76]	Hör J, Matera G, Vogel J, et al. Trans-acting small RNAs and their effects on gene expression in Escherichia coli and Salmonella enterica[J]. Ecosal Plus, 2020,9:ecosalplus. ESP-30. DOI: 10.1128/ecosalplus.esp-0030-2019. doi: 10.1128/ecosalplus.esp-0030-2019
[77]	Nurmohamed S, Vincent HA, Titman CM, et al. Polynucleotide phosphorylase activity may be modulated by metabolites in Escherichia coli[J]. J Biol Chem, 2011, 286(16):14315-14323. doi: 10.1074/jbc.M110.200741 pmid: 21324911
[78]	Arraiano CM, Mauxion F, Viegas SC, et al. Intracellular ribonucleases involved in transcript processing and decay:Precision tools for RNA[J]. Biochim et Biophys Acta BBA Gene Regul Mech, 2013, 1829(6/7):491-513.
[79]	Mohanty BK, Maples VF, Kushner SR. Polyadenylation helps regulate functional tRNA levels in Escherichia coli[J]. Nucleic Acids Res, 2012, 40(10):4589-4603. doi: 10.1093/nar/gks006 pmid: 22287637
[80]	Garza-Sánchez F, Shoji S, Fredrick K, et al. RNase II is important for A-site mRNA cleavage during ribosome pausing[J]. Mol Microbiol, 2009, 73(5):882-897. doi: 10.1111/j.1365-2958.2009.06813.x pmid: 19627501
[81]	Pobre V, Barahona S, Dobrzanski T, et al. Defining the impact of exoribonucleases in the shift between exponential and stationary phases[J]. Sci Rep, 2019, 9(1):16271. doi: 10.1038/s41598-019-52453-6 URL
[82]	Gutgsell NS, Jain C. Role of precursor sequences in the ordered maturation of E. coli 23S ribosomal RNA[J]. RNA, 2012, 18(2):345-353. doi: 10.1261/rna.027854.111 pmid: 22190745
[83]	Li Z, Pandit S, Deutscher MP. 3' exoribonucleolytic trimming is a common feature of the maturation of small, stable RNAs in Escherichia coli[J]. PNAS, 1998, 95(6):2856-2861. pmid: 9501180

名称 Name		编码基因 Gene	酶活特异性 Enzyme activity	主要生理功能 Physiological functions	已知主要调控方式 Regulation known	主要参考文献 Reference
核糖核酸内切酶	RNAse I	rna	内切酶活性,Ca²⁺依赖的双链mRNA活性	尚不明确	可能与周质空间及胞内定位调节有关	[8-9]
	RNAse III	rnc	双链特异性内切酶活性	rRNA的成熟	转录后自我调控;酶蛋白磷酸化修饰;反式作用因子调控	[10-13]
	RNase BN	rbn	内切酶/外切酶活性	sRNA的降解,mRNA降解	自身mRNA稳定性调节	[14-15]
	RNase E	rne	内切酶活性	mRNA的降解;rRNA及tRNA的成熟	转录后自我调控;酶蛋白磷酸化修饰;反式作用因子调控;sRNA;小分子结合及胞内定位	[16-21]
	RNase P	rnpA/rnpB	内切酶活性	5' tRNA的成熟	未知	[22]
	RNase G	rng	内切酶活性	rRNA的成熟	未知	[23]
	RNase H家族	rnhA/rnhB	RNA/DNA杂交体中RNA的切割与修饰	参与DNA复制过程中RNA的调整	未知	[24]
	YbeY	ybeY	内切酶活性	rRNA成熟与质控,16S rRNA3'末端的加工	未知	[25]
	RNase LS	rnlA/rnlB	内切酶活性	降解T4噬菌体编码的mRNA	未知	[26]
核糖核酸外切酶	PNPase	pnp	磷酸盐依赖的3'-5'外切酶活性	mRNA的降解;rRNA及tRNA的成熟;sRNAs调控伴侣	自我调控;反式作用因子调控;sRNA的调控	[27-30]
	RNAse II	rnb	3'-5'外切酶活性	mRNA的降解;rRNA及tRNA的成熟	酶蛋白的乙酰化修饰	[31-33]
	RNase R	rnr	3'-5'外切酶活性	mRNA的降解;rRNA的成熟与质控;tRNA的成熟	酶蛋白的乙酰化修饰	[13,34-35]
	RNase PH	rph	磷酸盐依赖的3'-5'外切酶活性	tRNA与rRNA的成熟;rRNA的降解	蛋白稳定性调节;RNase II调节（待发表资料）	[36-37]
	RNase T	rnt	3'-5'外切酶活性	tRNA与rRNA的成熟	未知	[38]
	RNase D	rnd	3'-5'外切酶活性	tRNA的成熟	未知	[22]
	Oligo RNase	orn	3'-5'外切酶活性	短链核苷酸的去除	未知	[2]
	RNase AM	trpH/yciV	5'-3'外切酶活性	5S、23S 及16S rRNA的5'末端成熟	未知	[39]

名称 Name		编码基因 Gene	酶活特异性 Enzyme activity	主要生理功能 Physiological functions	已知主要调控方式 Regulation known	主要参考文献 Reference
核糖核酸内切酶	RNAse I	rna	内切酶活性,Ca²⁺依赖的双链mRNA活性	尚不明确	可能与周质空间及胞内定位调节有关	[8-9]
	RNAse III	rnc	双链特异性内切酶活性	rRNA的成熟	转录后自我调控;酶蛋白磷酸化修饰;反式作用因子调控	[10-13]
	RNase BN	rbn	内切酶/外切酶活性	sRNA的降解,mRNA降解	自身mRNA稳定性调节	[14-15]
	RNase E	rne	内切酶活性	mRNA的降解;rRNA及tRNA的成熟	转录后自我调控;酶蛋白磷酸化修饰;反式作用因子调控;sRNA;小分子结合及胞内定位	[16-21]
	RNase P	rnpA/rnpB	内切酶活性	5' tRNA的成熟	未知	[22]
	RNase G	rng	内切酶活性	rRNA的成熟	未知	[23]
	RNase H家族	rnhA/rnhB	RNA/DNA杂交体中RNA的切割与修饰	参与DNA复制过程中RNA的调整	未知	[24]
	YbeY	ybeY	内切酶活性	rRNA成熟与质控,16S rRNA3'末端的加工	未知	[25]
	RNase LS	rnlA/rnlB	内切酶活性	降解T4噬菌体编码的mRNA	未知	[26]
核糖核酸外切酶	PNPase	pnp	磷酸盐依赖的3'-5'外切酶活性	mRNA的降解;rRNA及tRNA的成熟;sRNAs调控伴侣	自我调控;反式作用因子调控;sRNA的调控	[27-30]
	RNAse II	rnb	3'-5'外切酶活性	mRNA的降解;rRNA及tRNA的成熟	酶蛋白的乙酰化修饰	[31-33]
	RNase R	rnr	3'-5'外切酶活性	mRNA的降解;rRNA的成熟与质控;tRNA的成熟	酶蛋白的乙酰化修饰	[13,34-35]
	RNase PH	rph	磷酸盐依赖的3'-5'外切酶活性	tRNA与rRNA的成熟;rRNA的降解	蛋白稳定性调节;RNase II调节（待发表资料）	[36-37]
	RNase T	rnt	3'-5'外切酶活性	tRNA与rRNA的成熟	未知	[38]
	RNase D	rnd	3'-5'外切酶活性	tRNA的成熟	未知	[22]
	Oligo RNase	orn	3'-5'外切酶活性	短链核苷酸的去除	未知	[2]
	RNase AM	trpH/yciV	5'-3'外切酶活性	5S、23S 及16S rRNA的5'末端成熟	未知	[39]