The N-terminal hybrid binding domain of RNase HI from Thermotoga maritima is important for substrate binding and Mg2+-dependent activity

FEBS Journal

Volumn 277, Issue 21, 2010, Pages 4474-4489

  Jongruja, Nujarin ^a   You, Dong Ju ^a   Kanaya, Eiko ^a   Koga, Yuichi ^a   Takano, Kazufumi ^a,b   Kanaya, Shigenori ^a  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Cleavage site specificity; Hybrid binding domain; Metal preference; RNase H; Substrate binding affinity; Thermotoga maritima

Indexed keywords

MAGNESIUM CHLORIDE; MAGNESIUM ION; MANGANESE; MANGANESE CHLORIDE; RIBONUCLEASE H; BACTERIAL PROTEIN; MAGNESIUM; RIBONUCLEASE HI; SODIUM CHLORIDE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL MUTATION; BINDING AFFINITY; CIRCULAR DICHROISM; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; ENZYME STABILITY; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; GENETIC COMPLEMENTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA CLEAVAGE; SURFACE PLASMON RESONANCE; THERMOTOGA MARITIMA; AMINO ACID SUBSTITUTION; BINDING SITE; CHEMISTRY; DRUG EFFECT; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; HYDROLYSIS; KINETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN BINDING; PROTEIN DENATURATION; SEQUENCE HOMOLOGY; TEMPERATURE;

ESCHERICHIA COLI; THERMOTOGA MARITIMA;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BINDING SITES; CIRCULAR DICHROISM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME STABILITY; GENETIC COMPLEMENTATION TEST; HYDROLYSIS; KINETICS; MAGNESIUM; MANGANESE; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN DENATURATION; RIBONUCLEASE H; SEQUENCE HOMOLOGY, AMINO ACID; SODIUM CHLORIDE; SUBSTRATE SPECIFICITY; TEMPERATURE; THERMOTOGA MARITIMA;

EID: 79952110542     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07834.x     Document Type: Article

References (47)

1. Crouch RJ & Dirksen ML (1982) Ribonuclease H. In Nuclease (Linn SM & Roberts RJ eds), pp. 211-241. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
2. Kogoma T & Foster PL (1998) Physiological functions of E. coli RNase HI. In Ribonuclease H (Crouch RJ & Toulme JJ eds), pp. 39-66. INSERM, Paris.
3. Qiu J, Qian Y, Frank P, Wintersberger U & Shen B (1999) Saccharomyces cerevisiae RNase H(35) functions in RNA primer removal during lagging-strand DNA synthesis, most efficiently in cooperation with Rad27 nuclease. Mol Cell Biol 19, 8361-8371.
4. Arudchandran A, Cerritelli SM, Narimatsu SK, Itaya M, Shin DY, Shimada Y & Crouch RJ (2000) The absence of ribonuclease H1 or H2 alters the sensitivity of Saccharomyces cerevisiae to hydroxyurea, caffeine and ethyl methanesulphonate: implications for roles of RNases H in DNA replication and repair. Genes Cells 5, 789-802.
5. Rydberg B & Game J (2002) Excision of misincorporated ribonucleotides in DNA by RNase H (Type 2) and FEN-1 in cell-free extracts. Proc Natl Acad Sci USA 99, 16654-16659. (Pubitemid 36034028)
6. Cerritelli SM, Frolova EG, Feng C, Grinberg A, Love PE & Crouch RJ (2003) Failure to produce mitochondrial DNA results in embryonic lethality in Rnaseh1 null mice. Mol Cell 11, 807-815. (Pubitemid 36385132)
7. Dean NM & Bennett CF (2003) Antisense oligonucleotide-based therapeutics for cancer. Oncogene 22, 9087-9096.
8. Chon H, Vassilev A, DePamphilis ML, Zhao Y, Zhang J, Burgers PM, Crouch RJ & Cerritelli SM (2009) Contributions of the two accessory subunits, RNASEH2B and RNASEH2C, to the activity and properties of the human RNase H2 complex. Nucleic Acids Res 37, 96-110.
9. Crow YJ, Leitch A, Hayward BE, Garner A, Parmar R, Griffith E, Ali M, Semple C, Aicardi J, Babul-Hirji R et al. (2006) Mutations in genes encoding ribonuclease H2 subunits cause Aicardi-Goutieres syndrome and mimic congenital viral brain infection. Nat Genet 38, 910-916. (Pubitemid 44141659)
10. Hughes SH, Arnold E & Hostomsky Z (1998) RNase H of retroviral reverse transcriptases. In Ribonucleases H (Crouch RJ & Toulme JJ eds), pp 195-224. Inserm, Paris.
11. Ohtani N, Haruki M, Morikawa M & Kanaya S (1999) Molecular diversities of RNases H. J Biosci Bioeng 88, 12-19. (Pubitemid 29394993)
12. Kanaya E, Sakabe T, Nguyen NT, Koikeda S, Koga Y, Takano K & Kanaya S(2010) Cloning of the RNase H genes from a metagenomic DNA library: identification of a new type 1 RNase H without a typical active-site motif. J Appl Microbiol 109, 974-983.
13. Tadokoro T & Kanaya S (2009) Ribonuclease H: molecular diversities, substrate binding domains, and catalytic mechanism of the prokaryotic enzymes. FEBS J 276, 1482-1493.
14. Nowotny M, Gaidamakov SA, Crouch RJ & Yang W (2005) Crystal structures of RNase H bound to an RNA/DNA hybrid: substrate specificity and metal-dependent catalysis. Cell 121, 1005-1016. (Pubitemid 40884393)
15. Nowotny M, Gaidamakov SA, Ghirlando R, Cerritelli SM, Crouch RJ & Yang W (2007) Structure of human RNase H1 complexed with an RNA/DNA hybrid: insight into HIV reverse transcription. Mol Cell 28, 264-276. (Pubitemid 47599996)
16. Nowotny M & Yang W. (2006) Stepwise analyses of metal ions in RNase H catalysis from substrate destabilization to product release. EMBO J 25, 1924-1933.
17. 2+-ion catalysis and substrate specificity. Mol Cell 22, 5-13.
18. Huber R, Langworthy TA, König H, Thomm M, Woese CR, Sleytr UB & Stetter KO (1986) Thermotoga maritima sp. nov. represents a new genus of unique extremely thermophilic eubacteria growing up to 90°C. Arch Microbiol 144, 324-333. (Pubitemid 16074944)
19. Kyrpides NC, Ouzounis CA, Iliopoulos I, Vonstein V & Overbeek R (2000) Analysis of the Thermotoga maritima genome combining a variety of sequence similarity and genome context tools. Nucleic Acids Res 28, 4573-4576.
20. Cerritelli SM, Fedoroff OY, Reid BR & Crouch RJ (1998) A common 40 amino acid motif in eukaryotic RNase H1 and caulimovirus ORF VI proteins binds to duplex RNAs. Nucleic Acids Res 26, 1834-1840. (Pubitemid 28291824)
21. Cerritelli SM & Crouch RJ (2009) Ribonuclase H: the enzymes in eukaryotes. FEBS J 276, 1494-1505.
22. Nowotny M, Cerritelli SM, Ghirlando R, Gaidamakov SA, Crouch RJ & Yang W (2008) Specific recognition of RNA/DNA hybrid and enhancement of human RNase H1 activity by HBD. EMBO J 27, 1172-1181. (Pubitemid 351508154)
23. Cerritelli SM & Crouch RJ (1995) The non-RNase H domain of Saccharomyces cerevisiae RNase H1 binds double-stranded RNA: magnesium modulates the switch between double-stranded RNA binding and RNase H activity. RNA 1, 246-259.
24. Gaidamakov SA, Gorshkova II, Schuck P, Steinbach PJ, Yamada H, Crouch RJ & Cerritelli SM (2005) Eukaryotic RNases H1 act processively by interactions through the duplex RNA-binding domain. Nucleic Acids Res 33, 2166-2175. (Pubitemid 41439884)
25. Wu H, Lima WF & Crooke ST (2001) Investigating the structure of human RNase H1 by site-directed mutagenesis. J Biol Chem 276, 23547-23553.
26. Lima WF, Wu H, Nichols JG, Prakash TP, Ravikumer V & Crooke ST (2003) Human RNase H1 uses one tryptophan and two lysines to position the enzyme at the 3′-DNA/5′-RNA terminus of the heteroduplex substrate. J Biol Chem 278, 49860-49867. (Pubitemid 37548820)
27. Tadokoro T, Chon H, Koga Y, Takano K & Kanaya S (2007) Identification of the gene encoding a Type 1 RNase H with an N-terminal double-stranded RNA binding domain from a psychrotrophic bacterium. FEBS J 274, 3715-3727. (Pubitemid 47052408)
28. Itaya M & Crouch RJ (1991) A combination of RNase H (rnh) and recBCD or sbcB mutations in Escherichia coli K12 adversely affects growth. Mol Gen Genet 227, 424-432.
29. You DJ, Chon H, Koga Y, Takano K & Kanaya S (2007) Crystal structure of Type 1 ribonuclease H from hyperthermophilic archaeon Sulfolobus tokodaii: role of arginine 118 and C-terminal anchoring. Biochemistry 46, 11494-11503. (Pubitemid 47585495)
30. Haruki M, Hayashi K, Kochi T, Muroya A, Koga Y, Morikawa M, Imanaka T & Kanaya S (1998) Gene cloning and characterization of recombinant ribonuclease HII from a hyperthermophilic archaeon. J Bacteriol 180, 6207-6214. (Pubitemid 28544251)
31. Kanaya S (2001) Prokaryotic type 2 RNases H. Methods Enzymol 341, 377-394.
32. Rohman MS, Koga Y, Takano K, Chon H, Crouch RJ & Kanaya S (2008) Effect of the disease-causing mutations identified in human ribonuclease (RNase) H2 on the activities and stabilities of yeast RNase H2 and archaeal RNase HII. FEBS J 275, 4836-4849.
33. Ohtani N, Yanagawa H, Tomita M & Itaya M (2004) Cleavage of double-stranded RNA by RNase HI from a thermoacidophilic archaeon, Sulfolobus tokodaii 7. Nucleic Acids Res 32, 5809-5819. (Pubitemid 39619163)
34. Keck JL & Marqusee S (1996) The putative substrate recognition loop of Escherichia coli ribonuclease H is not essential for activity. J Biol Chem 271, 19883-19887. (Pubitemid 26281731)
35. 2+. J Biol Chem 271, 1448-1454.
36. Chon H, Matsumura H, Koga Y, Takano K & Kanaya S (2006) Crystal structure and structure-based mutational analyses of RNase HIII from Bacillus stearothermophilus: a new Type 2 RNase H with TBP-like substrate-binding domain at the N-terminus. J Mol Biol 356, 165-178. (Pubitemid 43069735)
37. 2+-dependent activity of E. coli ribonuclease HI. Biochemistry 42, 3366-3374.
38. Cirino NM, Cameron CE, Smith JS, Rausch JW, Roth MJ, Benkovic SJ & Le Grice SF (1995) Divalent cation modulation of the ribonuclease functions of human immunodeficiency virus reverse transcriptase. Biochemistry 34, 9936-9943.
39. Goedken ER, Raschke TM & Marqusee S (1997) Importance of the C-terminal helix to the stability and enzymatic activity of Escherichia coli ribonuclease H. Biochemistry 36, 7256-7263. (Pubitemid 27258142)
40. Itaya M (1990) Isolation and characterization of a second RNase H (RNase HII) of Escherichia coli K-12 encoded by the rnhB gene. Proc Natl Acad Sci USA 87, 8587-8591.
41. 2+-dependent RNase HIII from Bacillus subtilis: classification of RNases H into three families. Biochemistry 38, 605-618.
42. Kanaya S, Oobatake M, Nakamura H & Ikehara M (1993) pH-dependent thermostabilization of Escherichia coli ribonuclease HI by histidine to alanine substitutions. J Biotech 28, 117-136.
43. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T. Nature 227, 680-685.
44. Goodwin TW & Morton RA (1946) The spectrophotometric determination of tyrosine and tryptophan in proteins. Biochem J 40, 628-632.
45. Kanaya S, Katsuda C, Kimura S, Nakai T, Kitakuni E, Nakamura H, Katayanagi K, Morikawa K & Ikehara M (1991) Stabilization of Escherichia coli ribonuclease H by introduction of an artificial disulfide bond. J Biol Chem 266, 6038-6044. (Pubitemid 21906180)
46. Ohtani N, Haruki M, Morikawa M & Kanaya S (2001) Heat labile ribonuclease HI from a psychrotrophic bacterium: gene cloning, characterization, and site-directed mutagenesis. Protein Eng 14, 975-982. (Pubitemid 34137238)
47. Haruki M, Noguchi E, Kanaya S & Crouch RJ (1997) Kinetic and stoichiometric analysis for the binding of Escherichia coli ribonuclease HI to RNA-DNA hybrids using surface plasmon resonance. J Biol Chem 272, 22015-22022. (Pubitemid 27382825)