Ribonucleases and their Applications

Authors

  • Shamsher S. Kanwar Department of Biotechnology, Himachal Pradesh University, Summer Hill, Shimla-171 005, India
  • Puranjan Mishra Department of Biotechnology, Himachal Pradesh University, Summer Hill, Shimla-171 005, India
  • Khem Raj Meena Department of Biotechnology, Himachal Pradesh University, Summer Hill, Shimla-171 005, India
  • Shruti Gupta Department of Biotechnology, Himachal Pradesh University, Summer Hill, Shimla-171 005, India
  • Rakesh Kumar Department of Biotechnology, Himachal Pradesh University, Summer Hill, Shimla-171 005, India

DOI:

https://doi.org/10.12970/2311-1755.2016.04.01.3

Keywords:

Microbial ribonucleases, antimicrobial, antiviral, antitumor/ anticancer, apoptosis.

Abstract

Ribonuclease (RNase) is a type of nuclease that catalyzes degradation of RNA into smaller components. RNase can be classified into two broader categories namely endoribonucleases and exoribonucleases on the basis of their site of action. RNases play key roles in the maturation of all RNA molecules; endoribonucleases cleave the RNA molecules from the interior at 5′ end while exoribonucleases degrade RNA molecules in a 3′–5′ direction. With the advent of new frontiers in biotechnology, the applications of ribonucleases besides molecular biology have expended into many other fields like medicinal, clinical, and analytical chemistry. RNase A that belongs to pancreatic ribonucleases super family plays an important key role in structural, biochemical and evolutionary studies. Discovery of eukaryotic orthologues of the bacterial double stranded (ds) RNA-specific ribonuclease III (RNase III) suggests a central role for these enzymes in the regulation of ds-RNA and eukaryotic RNA metabolism. The more recent studies have shown that the mammalian and some fungal RNases are also bestowed with antiproliferative, antiangiogenic and/ or antitumor/ anticancer activities. Some of the members of RNase A superfamily such as RNase 6 and RNase 7 appears to be evolutionary conserved peptides with potent antimicrobial activities for upkeep of sterility in the urinary tract.

References

Sharma R, Chistib Y, Banerjee UC. Production, purification, characterization and applications of lipases. Biotech Adv 2001; 19: 627-662. http://dx.doi.org/10.1016/S0734-9750(01)00086-6

Zhang R, Tian G, Zhao YL, Wang, HGZ, Ng TB. A novel ribonuclease with HIV-1 reverse transcriptase inhibitory activity purified from the fungus Ramaria formosa. J Basic Microbiol 2014; 55: 269-275. http://dx.doi.org/10.1002/jobm.201300876

Deutscher MP, Li Z. Exoribonucleases and their multiple roles in RNA metabolism. Prog Nucleic Acid Res Mol Biol 2001; 66: 67-105. http://dx.doi.org/10.1016/S0079-6603(00)66027-0

Kushner SR. mRNA decay in Escherichia coli comes of age. J Bacteriol 2002; 184: 4658-4665. http://dx.doi.org/10.1128/JB.184.17.4658-4665.2002

Fang EF and Ng TB. Ribonucleases of different origins with wide spectrum of medicinal applications. Biochim Biophy Acta 2011; 1815: 65-74. http://dx.doi.org/10.1016/j.bbcan.2010.09.001

Cobaleda C and Sanchez-Garcia I. In vivo inhibition by a site-specific catalytic RNA subunit of RNase P designated against the BCR-ABL oncogenic products: a novel approach for cancer treatment. Blood 2000; 95: 731-737.

Zhang R, Zhao L, wang H and Ng TB. A novel ribonuclease with antiproliferative activity toward leukemia and lymphoma cells and HIV-1 reverse transcriptase inhibitory activity from the mushroom, Hohenbuehelia serotina. International J Mol Med 2014; 33: 209-214.

Eller CH, Chao T-Y, Singarapu KK, Ouerfelli o, Yang G, Markley JL, Danishefsky SJ and Raines RT. Human cancer antigen Globo H is a cell-surface ligand for human Ribonuclease 1. ACS Centarl Science 2015; 1: 181-190. http://dx.doi.org/10.1021/acscentsci.5b00164

Even S, Pellegrini O, Zig L, Labas V, Vinh J,BréchemmierBaey D, Putzer H. Ribonucleases J1 and J2: two novel endoribonucleases in Bacillus subtilis with functional homology to E. coli RNase E. Nucleic Acids Res 2005; 33: 2141-2152. http://dx.doi.org/10.1093/nar/gki505

Mäder U, Zig L, Kretschmer J, Homuth G, Putzer H. mRNA processing by RNases J1 and J2 affects Bacillus subtilis gene expression on a global scale. Mol Microbiol 2008; 70: 183-196. http://dx.doi.org/10.1111/j.1365-2958.2008.06400.x

Barnett TC, Bugrysheva JV, and Scott JR. Role of mRNA stability in growth phase regulation of gene expressionin the group A streptococcus. J Bacteriol 2007; 189:1866-1873. http://dx.doi.org/10.1128/JB.01658-06

Domingues S, Matos RG, Reis FP, Fialho AM, Barbas A, Arraiano CM. Biochemical characterization of the RNase II family of exoribonucleases from the human pathogens Salmonella typhimurium and Streptococcus pneumoniae. Biochemistry 2009; 48:11848-11857. http://dx.doi.org/10.1021/bi901105n

Huntzinger E, Boisset S, Saveanu C, Benito Y, Geissmann T, Namane A. Staphylococcus aureus RNAIII and the endo ribonuclease III co-ordinately regulate spa gene expression. EMBO J 2005; 24: 824-835. http://dx.doi.org/10.1038/sj.emboj.7600572

Boisset S, Geissmann T, Huntzinger E, Fechter P, Bendridi N, Possedko M. Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an anti sense mechanism. Genes Dev 2007; 21: 1353-1366. http://dx.doi.org/10.1101/gad.423507

Anderson KL, Dunman PM (2009). Messenger RNA turnover processes in Escherichia coli, Bacillus subtilis and emerging studies in Staphylococcus aureus. Int J Microbiol 2009; 2009: 15. http://dx.doi.org/10.1155/2009/525491

Bugrysheva JV, Scott JR. The ribonucleasesJ1 and J2 are essential for growth and have independent roles in mRNA decay in Streptococcus pyogenes. Mol Microbiol 2010, 75: 731-743. http://dx.doi.org/10.1111/j.1365-2958.2009.07012.x

Ono M, Kuwano M. A conditional lethal mutation in an Escherichia coli strain with a longer chemical life time of messenger RNA. J Mol Biol 1979; 129: 343-357. http://dx.doi.org/10.1016/0022-2836(79)90500-X

Jain C, Belasco JG. RNase E auto regulates its synthesis by controlling the degradation rate of its own mRNA in Escherichia coli: unusual sensitivity of the rne transcript to RNase E activity. Genes Dev 1995; 9: 84-96. http://dx.doi.org/10.1101/gad.9.1.84

Mudd EA, Higgins CF. Escherichia coli endoribonucleases RNase E: Autoregulation of expression and site-specific cleavage of mRNA. Mol Microbiol 1993; 9: 557-568. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01716.x

Sousa S, Marchand I, Dreyfus M. Auto regulation allow Escherichia coli RNase E to adjust continuously its synthesis to that of its substrates. Mol Microbiol 2001; 42:867-878. http://dx.doi.org/10.1046/j.1365-2958.2001.02687.x

Callaghan AJ, Marcaida MJ, Stead JA, McDowall KJ, Scott WG, Luisi BF. Structure of Escherichia coli RNase E catalytic domain and implications for RNA turn over. Nature 2005; 437: 1187-1191. http://dx.doi.org/10.1038/nature04084

Généreux C, Dehareng D, Devreese B, Van BJ, Frère JM and Joris B. Mutational analysis of the catalytic centre of the CitrobacterfreundiiAmpDN-acetyl muramyl-L-alanine amidase. Biochem J 2004; 377: 111-120. http://dx.doi.org/10.1042/bj20030862

Carpousi AJ, Van Houwe G, Ehretsmann C, Krisch HM. Co purification of E. coli RNAase E and PNPase: evidence for a specific association between two enzymes important in RNA processing and degradation. Cell 1994; 76: 889-900. http://dx.doi.org/10.1016/0092-8674(94)90363-8

Khemici V, Carpousis AJ. The RNA degradosome and poly (A) polymerase of Escherichia coli are required in vivo for the degradation of small mRNA decay intermediates containing REP-stabilizers. Mol Microbiol 2004; 51:777-790. http://dx.doi.org/10.1046/j.1365-2958.2003.03862.x

Vanzo NF, Li YS, Py B, Blum E, Higgins CF, Raynal LC (1998). Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev 1998; 12: 2770-2781. http://dx.doi.org/10.1101/gad.12.17.2770

Blum E, Py B, Carpousis AJ, Higgins CF. Polyphosphate kinase is a component of the Escherichia coli RNA degradosome. Mol Microbiol 1997; 26: 387-398. http://dx.doi.org/10.1046/j.1365-2958.1997.5901947.x

Miczak A, Kaberdin VR, Wei CL, Lin-Chao S. Proteins associated with RNase E in a multi component ribonucleolytic complex. Proc Natl Acad Sci USA 1996; 93: 3865-3869. http://dx.doi.org/10.1073/pnas.93.9.3865

Purusharth RI, Klein F, Sulthana S, Jäger S, Jagannadham MV, Evguenieva-Hackenberg E (2005). Exo ribonuclease R interacts with endo ribonuclease E andan RNA helicase in the psychrotrophic bacterium Pseudomonas syringae Lz4W. J Biol Chem 2005; 280:14572-14578. http://dx.doi.org/10.1074/jbc.M413507200

Cheng B, Liping L, Bruce WW. Nickel affects xylem Sap RNase A and converts RNase A to a urease. BMC Plant Biology 2013; 13: 207. http://dx.doi.org/10.1186/1471-2229-13-207

Berkower I, Leis J, Hurwitz J. Isolation and characterization of an endonuclease from Escherichia coli specific for ribonucleic acid in ribonucleic acid-deoxyribonucleic acid hybrid structures. J Biol Chem 1973; 248: 5914-5921.

Scott AJ, Jianming Hu. Hepatitis B virus reverse transcriptase: diverse functions as classical and emerging targets for antiviral intervention. Emerg Microbes Infect. 2013; 2: e56. http://dx.doi.org/10.1038/emi.2013.56

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: 5408-16. http://dx.doi.org/10.1128/MCB.21.16.5408-5416.2001

Ishii I, Nureki O and Yokoyama, S.Crystal structure of the tRNA processing enzyme RNase PH from Aquifexaeolicus. J Biol Chem 2003; 278: 32397-32404. http://dx.doi.org/10.1074/jbc.M300639200

Coburn GA, Mackie GA. Overexpression, purification and properties of Escherichia coli ribonuclease II. J Biol Chem 1996; 271:1048-1053. http://dx.doi.org/10.1074/jbc.271.2.1048

Cheng M, Deutscher MP. An important role for RNase R in mRNA decay. Mol Cell 2005; 17: 313-8. http://dx.doi.org/10.1016/j.molcel.2004.11.048

Zu I, Wang Y, Malhotra A. Crystal structure of Escherichia coli RNase D, an exoribonucleases involved in structured RNA processing. Structure 2005; 13: 973-84. http://dx.doi.org/10.1016/j.str.2005.04.015

Pace CN, Grimsley GR, Thomson JA, Barnett BJ. Conformational stability and activity of ribonuclease T1 with zero, one, and two intact disulfide bonds. J Biol Chem 1998; 263: 11820-11825.

Glitz DG, Dekker CA. Studies on a ribonuclease from Ustilago sphaerogena.Purification and properties of the enzyme. Biochemistry 1964; 3: 1391-1399. http://dx.doi.org/10.1021/bi00898a001

Asha PK, Blouin RT, Zaniewski R, Deutscher MP. Ribonuclease BN: identification and partial characterization of a new tRNA processing enzyme. Proc. Natl Acad. Sci. USA 1983; 80: 3301-3304. http://dx.doi.org/10.1073/pnas.80.11.3301

Raines RT. Metabolism and enzymology of nucleic acids including gene and protein engineering, Slovak Academy of Sciences, Bratislava 191; 47-53.

Court D. RNA processing and degradation by RNase III. In: Control of Messenger RNA Stability. Academic Press, NewYork 1993. http://dx.doi.org/10.1016/b978-0-08-091652-1.50009-8

Mackie GA. Ribonuclease E is a 5'-end-dependent endonuclease. Nature 1998; 395: 720-723. http://dx.doi.org/10.1038/27246

Teppei M, Hiroji A. RNase E action at a distance: degradation of target mRNAs mediated by an Hfq-binding small RNA in bacteria. Genes Dev 2011; 5: 294-298.

Ten Asbroek AL, van Groenigen M, Jakobs ME, Koevoets C, Janssen B , Baas F. ribonuclease H1 maps to chromosome 2 and has at least three pseudogene loci in the human genome. Genomics 2002; 79: 818-23. http://dx.doi.org/10.1006/geno.2002.6776

Suhadolnik RJ. Biochemical evidence for a novel low molecular weight 2-5A-dependent RNase L in chronic fatigue syndrome. J Interferon Cytokine Res 1997; 17: 377-85. http://dx.doi.org/10.1089/jir.1997.17.377

Rudolph B, Podschun R, Sahly H, Schubert S, Schro¨der JM and Harder J. Identification of RNase 8 as a novel human antimicrobial protein. Antimicrob Agents Chemother 2006; 50: 3194-3196. http://dx.doi.org/10.1128/AAC.00246-06

Jester BC, Romby P and Lioliou E. When ribonucleases come into play in pathogens: A survey of Gram-Positive bacteria. Int J Microbiol 2012; 2012:18.

Schuster C, Glaser R, Fiala C, Eppel W, Harder J, Schro ¨der J and Elbe-Burger A. Prenatal human skin expresses the antimicrobial peptide RNase 7. Arch Dermatol Res 2013; 305:545-549. http://dx.doi.org/10.1007/s00403-013-1340-y

Torrent M, Badia M, Moussaoui M, Sanchez D, Nogue ´s MV, Boix E. Comparison of human RNase 3 and RNase 7 bactericidal action at the Gram-negative and Gram-positive bacterial cell wall. FEBS Journal 2010; 277: 1713-1725. http://dx.doi.org/10.1111/j.1742-4658.2010.07595.x

Manasherob R, Miller C, Kim KS and Cohen SN. Ribonuclease E modulation of the bacterial SOS response. PLoS ONE 2012; 7: e38426. http://dx.doi.org/10.1371/journal.pone.0038426

Tavis JE, Cheng X, Hu Y, Totten M, Cao F,Michailidis E, Aurora R, Meyers MJ, Jacobsen EJ,Parniak MA and Sarafianos SG. The Hepatitis B virus ribonuclease H is sensitive to inhibitors of the Human Immunodeficiency Virus ribonuclease H and integrase enzymes.PLOS Pathogens 2013; 9: e1003125. http://dx.doi.org/10.1371/journal.ppat.1003125

Cho S, Beintema JJ and Zhang J. The ribonucleases A superfamily of mammals and birds: identifying new members and tracing evolutionary histories.Genomics 2005; 85-208- 220.

Goo SM, Cho S. The expansion and functional diversification of the mammalian ribonucleaseA superfamily epitomizes the efficiency of multi-gene families at generating biological novelty.Genome Biol Evol 2013; 5: 2124-2140. http://dx.doi.org/10.1093/gbe/evt161

Nicholson AW. Function, mechanism and regulation of bacterial ribonucleases. FEMS Microbiol Rev 1999; 23: 371- 390. http://dx.doi.org/10.1111/j.1574-6976.1999.tb00405.x

Reiter NJ, Osterman A, Torres-Larios A, Swinger KK, PanMA. Structure of a bacterial ribonuclease P holoenzyme in complex with t-RNA. Nature 2010; 468: 784-789. http://dx.doi.org/10.1038/nature09516

MacRae IJ, Doudna JA. Ribonuclease revisited: structural insights into ribonuclease III family enzymes. Current Opinion Structural Biology 2007; 17: 1-8. http://dx.doi.org/10.1016/j.sbi.2006.12.002

Mondragón A. Structural Studies of RNase P. Annual Review of Biophysic 2013; 42: 537-557. http://dx.doi.org/10.1146/annurev-biophys-083012-130406

Lamontagne B, Larose S, Boulanger J, and Elela SA. The RNase III Family: A conserved structure and expanding functions in eukaryotic dsRNA metabolism.Curr.Issues Mol Biol 2001; 3: 71-78.

Kawamoto SA, Sudhahar CG,Hatfield CL, Sun J, Behrman EJ and Gopalan V. Studies on the mechanism of inhibition of bacterial ribonuclease P by aminoglycoside derivatives Nucleic Acids Res 2008; 36: 697-704. http://dx.doi.org/10.1093/nar/gkm1088

Durand S, Gilet L, Condon mail C.The essential function of B. subtilis RNase III is to silence foreign toxin genes. PLOS 2012. http://dx.doi.org/10.1371/journal.pgen.1003181

Cerritelli SM, Crouch RJ. Ribonuclease H: the enzymes in eukaryotes. FEBS J 2010; 276: 1494-1505. http://dx.doi.org/10.1111/j.1742-4658.2009.06908.x

Zuo Y, Deutscher MP. The DNase activity of RNase T and its application to DNA cloning. Nucl Acids Res 1999; 27: 4077- 4082. http://dx.doi.org/10.1093/nar/27.20.4077

Leszczyniecka M, Su ZZ, Kang DC, Sarkar D, Fisher PB. Expression regulation and genomicorganization of human polynucleotide phosphorylase, hPNPase (old-35), a Type I interferon inducible earlyresponse gene. Gene 2003; 316: 143-156. http://dx.doi.org/10.1016/S0378-1119(03)00752-2

Köten B, Simanski M, Gläser R, Podschun R, Schröder JM, Harder J. RNase 7 contributes to thecutaneous defense against Enterococcus faecium. PLoS ONE 2009, 4: e6424. http://dx.doi.org/10.1371/journal.pone.0006424

Lewsey MG, Carr JP. Effects of DICER-like proteins 2, 3 and 4 on cucumber mosaic virus and tobaccomosaic virus infections in salicylic acid-treated plants. J Gen Virol 2009; 90: 3010-3014. http://dx.doi.org/10.1099/vir.0.014555-0

Patrick KL, Shi H, Kolev NG, Ersfeld K, Tschudi C, Ullu E. Distinct and overlapping roles for twoDicer-like proteins in the RNA interference pathways of the ancient eukaryote Trypanosoma brucei. Proc Natl Acad Sci USA 2009; 106: 17933-17938. http://dx.doi.org/10.1073/pnas.0907766106

Sun Q, Choi GH, Nuss DL (2009). A single Argonautegene is required for induction of RNA silencing antiviraldefense and promotes viral RNA recombination. Proc Natl Acad Sci USA 2009; 106: 17927-17932. http://dx.doi.org/10.1073/pnas.0907552106

Hongyu C, Wenxuan Z, Jie Z. Ribonuclease J is required for chloroplast and embryo development in Arabidopsis. J Exp Bot 2015. http://dx.doi.org/10.1093/jxb/erv010

Becknell B, Eichler TE, Beceiro S, Li B, Easterling RS, Carpenter AR, James CL, McHugh KM, Hains DS, Partidasanchez S and Spencer JD. Ribonucleases 6 and 7 have antimicrobial function in the human and murine urinary tract. Kidney International 2014; 78: 151-161.

Eller CH, Chao T-Y, Singarapu KK, Ouerfelli O, Yang G, Markley JL, Danishefsky SJ, Raines RT. Human cancer antigen Globo H is a cell-surface ligand for human Ribonuclease 1. ACS Cent Sci 2015; 1: 181-190. http://dx.doi.org/10.1021/acscentsci.5b00164

Cobaleda C, Sanchez-Garcia I. In vivo inhibition by a sitespecific catalytic RNA subunit of RNase P designated against the BCR-ABL oncogenic products: a novel approach for cancer treatment. Blood 2000; 95: 731-737.

Nesiel-Nuttman L, Doron S, Schwartz B and Shoseyov O. Human RNASET2 derivatives as potential anti-angiogenic agents: actin binding sequence identification and characterization. Oncoscience 2015; 2: 31-43. http://dx.doi.org/10.18632/oncoscience.100

Thorn A, Steinfeld R, Ziegenbein M, grapp m, Hsiao H-H, Urlaub H, Sheldrick GM, Gartner J and Kratzner R. structure and activity of the only human RNase T2. Nucleic Acids Res 2012; 40: 8733-8742. http://dx.doi.org/10.1093/nar/gks614

Dube DH and Bertozzi CR. Glycans in cancer and inflammation - potential for therapeutics and diagnostics. Nat Rev Drug Discovery 2005; 4: 477-488. http://dx.doi.org/10.1038/nrd1751

Chao T-Y, Lavis LD, Raines RT. Cellular uptake of ribonuclease A relies on anionic glycans. Biochem 2010; 49: 10666-10673.

Folkman J. Biology of endothelial cells. Vol. 27. Boston, MA: Springer US 1984; 412-428.

Cobaleda C, Perez-Losada J, sanchez-garcia I. Chromosomal abnormalities and tumor development: from genes to therapeutic mechanisms. Bioessays 1998; 20: 922. http://dx.doi.org/10.1002/(SICI)1521- 1878(199811)20:113.0.CO;2-O

Downloads

Published

2016-03-06

Issue

Section

Articles