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 Journal

Volumn 275, Issue 19, 2008, Pages 4836-4849

  Rohman, Muhammad S ^a   Koga, Yuichi ^a   Takano, Kazufumi ^a,b   Chon, Hyongi ^c   Crouch, Robert J ^c   Kanaya, Shigenori ^a  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Heterotrimer; Saccharomyces cerevisiae; Site directed mutagenesis; Thermococcus kodakaraensis; Type 2 RNase H

Indexed keywords

ARCHAEAL RNA; GLYCINE; RIBONUCLEASE H;

AICARDI GOUTIERES SYNDROME; ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PURIFICATION; ESCHERICHIA COLI; GENE EXPRESSION; GENE MUTATION; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN STABILITY; THERMOCOCCUS;

AMINO ACID SEQUENCE; BASAL GANGLIA DISEASES; CIRCULAR DICHROISM; ENZYME STABILITY; GLYCINE; HUMANS; MOLECULAR SEQUENCE DATA; RIBONUCLEASE H; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; THERMOCOCCUS;

ARCHAEA; ESCHERICHIA COLI; EUKARYOTA; SACCHAROMYCES CEREVISIAE; THERMOCOCCUS; THERMOCOCCUS KODAKARENSIS;

EID: 51749083488     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06622.x     Document Type: Article

References (45)

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, NY.
2. Kogoma T Foster PL (1998) Physiological functions of E. coli RNase HI. In Ribonucleases 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. Itaya M, Omori A, Kanaya S, Crouch RJ, Tanaka T Kondo K (1999) Isolation of RNase H genes that are essential for growth of Bacillus subtilis 168. J Bacteriol 181, 2118 2123.
5. Arudchandran A, Cerritelli S, Narimatsu S, 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.
6. Haruki M, Tsunaka Y, Morikawa M Kanaya S (2002) Cleavage of a DNA-RNA-DNA/DNA chimeric substrate containing single ribonucleotide at the DNA-RNA junction with prokaryotic RNases HII. FEBS Lett 531, 204 208.
7. 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.
8. 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.
9. 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.
10. 2 + -dependent RNase HIII from Bacillus subtilis: classification of RNases H into three families. Biochemistry 38, 605 618.
11. Ohtani N, Haruki M, Morikawa M Kanaya S (1999) Molecular diversity of RNases H. J Biosci Bioeng 88, 12 19.
12. 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.
13. Katayanagi K, Miyagawa M, Matsushima M, Ishikawa M, Kanaya S, Ikehara M, Matsuzaki T Morikawa K (1990) Three-dimensional structure of ribonuclease H from E. coli. Nature 347, 306 309.
14. Yang W, Hendrickson WA, Crouch RJ Satow Y (1990) Structure of ribonuclease H phased at 2 Å resolution by MAD analysis of the selenomethionyl protein. Science 249, 1398 1405.
15. Davies JF, Hostomska Z, Hostomsky Z, Jordan SR Matthews DA (1991) Crystal structure of the ribonuclease H domain of HIV-1 reverse transcriptase. Science 252, 88 95.
16. Kohlstaedt LA, Wang J, Friedman JM, Rice PA Steitz TA (1992) Crystal structure at 3.5 Å resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256, 1783 1790.
17. Ishikawa K, Okumura M, Katayanagi K, Kimura S, Kanaya S, Nakamura H Morikawa K (1993) Crystal structure of ribonuclease HI from Thermus thermophilus HB8 refined at 2.8 Å resolution. J Mol Biol 230, 529 542.
18. 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.
19. Lim D, Gregorio GG, Bingman C, Martinez-Hackert E, Hendrickson WA Goff SP (2006) Crystal structure of the moloney murine leukemia virus RNase H domain. J Virol 80, 8379 8389.
20. You D-J, Chon H, Koga Y, Takano K Kanaya S (2007) Crystal structure of type 1 RNase H from hyperthermophilic archaeon Sulfolobus tokodaii: role of Arg118 and C-terminal anchoring. Biochemistry 46, 11494 11503.
21. 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.
22. Lai L, Yokota H, Hung L-W, Kim R Kim S-H (2000) Crystal structure of archeal RNase HII: a homologue of human major RNase H. Structure 8, 897 904.
23. Muroya A, Tsuchiya D, Ishikawa M, Haruki M, Morikawa M, Kanaya S Morikawa K (2000) Catalytic center of archaeal type 2 ribonuclease H as revealed by X-ray crystallographic and mutational analyses. Protein Sci 10, 707 714.
24. Chapados BR, Chai Q, Hosfield DJ, Qiu J, Shen B Tainer JA (2001) Structural biochemistry of a type 2 RNase H: RNA primer recognition and removal during DNA replication. J Mol Biol 307, 541 556.
25. Chon H, Matsumura H, Koga Y, Takano K Kanaya S (2005) 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.
26. 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.
27. 2+-ion catalysis and substrate specificity. Mol Cell 22, 5 13.
28. Kanaya S (2001) Prokaryotic type 2 RNases H. Methods Enzymol 341, 377 394.
29. Jeong HS, Backlund PS, Chen H-C, Karavanov AA Crouch RJ (2004) RNase H2 of Saccharomyces cerevisiae is a complex of three proteins. Nucleic Acids Res 32, 407 414.
30. Crow YJ, Leitch A, Hayward BE, Garner A, Parmar R, Griffith E, Ali M, Semple C, Aicardi J, Babul-Hirji R (2006) Mutations in genes encoding ribonuclease H2 subunits cause Aicardi-Goutieres syndrome and mimic congenital viral brain infection. Nat Genet 38, 910 916.
31. Rice G, Patrick T, Parmer R, Taylor CF, Aeby A, Aicardi J, Artuch R, Montalto SA, Bacino CA, Barraso B et al. (2007) Clinical and molecular phenotype of Aicardi-Goutieres syndrome. Am J Hum Genet 81, 713 725.
32. Haruki M, Hayashi K, Kochi T, Muroya A, Koga Y, Morikawa M, Imanaka T Kanaya S (1998) Gene cloning and characterization of recombinant RNase HII from hyperthermophilic archaeon. J Bacteriol 180, 6207 6214.
33. Mukaiyama A, Takano K, Haruki M, Morikawa M Kanaya S (2004) Kinetically robust monomeric protein from hyperthermophile. Biochemistry 43, 13859 13866.
34. Mukaiyama A, Haruki M, Ota M, Koga M, Takano K Kanaya S (2006) A hyperthermophilic protein acquires function at the cost of stability. Biochemistry 45, 12673 12679.
35. Nicholson H, Soderlind E, Tronrud DE Matthews BW (1989) Contributions of left-handed helical residues to the structure and stability of bacteriophage T4 lysozyme. J Mol Biol 210, 181 193.
36. Efimov AV (1986) Standard conformations of a polypeptide chain in irregular protein regions (Russian). Mol Biol (Moskow) 20, 250 260.
37. 95 with Gly or Asn. J Biol Chem 267, 22014 22017.
38. Ishikawa K, Kimura S, Kanaya S, Morikawa K Nakamura H (1993) Structural study of mutants of Escherichia coli ribonuclease HI with enhanced thermostability. Protein Eng 6, 85 91.
39. Takano K, Yamagata Y Yutani K (2001) Role of amino acid residues in left-handed helical conformation for the conformational stability of a protein. Proteins 45, 274 280.
40. Pulido M, Tanaka S, Sringiew C, You D-J, Matsumura H, Koga Y, Takano K Kanaya S (2007) Requirement of left-handed glycine residue for high stability of the Tk-subtilisin propeptide as revealed by mutational and crystallographic analyses. J Mol Biol 374, 1359 1373.
41. Horton RM, Cai ZL, Ho SN Pease LR (1990) Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8, 528 535.
42. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680 685.
43. Goodwin TW Morton RA (1946) The spectrophotometric determination of tyrosine and tryptophan in proteins. Biochem J 40, 628 632.
44. Jay E, Bambara R, Padmanabham P Wu R (1974) DNA sequence analysis: a general, simple and rapid method for sequencing large oligodeoxyribonucleotide fragments by mapping. Nucleic Acids Res 1, 331 353.
45. Becktel WJ Schellman JA (1987) Protein stability curves. Biopolymers 26, 1859 1877.