Gene cloning and biochemical characterizations of thermostable ribonuclease HIII from Bacillus stearothermophilus

Bioscience, Biotechnology and Biochemistry

Volumn 68, Issue 10, 2004, Pages 2138-2147

  Chon, Hyongi ^a   Nakano, Rikita ^a   Ohtani, Naoto ^a   Haruki, Mitsuru ^a,c   Takano, Kazufumi ^a,b   Morikawa, Masaaki ^a,d   Kanaya, Shigenori ^a  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c NIHON UNIVERSITY   (Japan)

^d HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Bacillus stearothermophilus; DNA RNA hybrid; Metal dependence; Ribonuclease H (RNase H); Stability

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY; CLONING; ENZYMES; ESCHERICHIA COLI; PROTEINS; THERMAL EFFECTS;

BACTERIUM BACILLUS; GENE ENCODING; MONOMERIC PROTEINS;

GENES;

BACTERIAL PROTEIN; RECOMBINANT PROTEIN; RIBONUCLEASE; RIBONUCLEASE HIII;

AMINO ACID SEQUENCE; ARTICLE; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; GEOBACILLUS STEAROTHERMOPHILUS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY;

AMINO ACID SEQUENCE; BACILLUS STEAROTHERMOPHILUS; BACTERIAL PROTEINS; CLONING, MOLECULAR; ENZYME STABILITY; ESCHERICHIA COLI; MOLECULAR SEQUENCE DATA; MUTATION; RECOMBINANT PROTEINS; RIBONUCLEASES; SUBSTRATE SPECIFICITY;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; GEOBACILLUS; GEOBACILLUS STEAROTHERMOPHILUS; PROKARYOTA;

EID: 9244245824     PISSN: 09168451     EISSN: None     Source Type: Journal    
DOI: 10.1271/bbb.68.2138     Document Type: Article

References (45)

1. Crouch, R. J., and Dirksen, M.-L., Ribonuclease H. In "Nuclease", eds. Linn, S. M., and Roberts, R. J., Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp. 211-241 (1982).
2. Ohtani, N., Haruki, M., Morikawa, M., and Kanaya, S., Molecular diversities of RNases H. J. Biosci. Bioeng., 88, 12-19 (1999).
3. Kogoma, T., and Foster, P. L., Physiological functions of E. coli RNase HI. In "Ribonucleases H", eds. Crouch, R. J., and Toulme, J. J., INSERM, Paris, pp. 39-66 (1998).
4. Murante, R. S., Henricksen, L. A., and Bambara, R. A., Junction ribonuclease: an activity in Okazaki fragment processing. Proc. Natl. Acad. Sci. U.S.A., 95, 2244-2249 (1998).
5. Qiu, J., Qian, Y., Frank, P., Wintersberger, U., and Shen, B., 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 (1999).
6. Arudchandran, A., Cerritelli, S., Narimatsu, S., Itaya, M., Shin, D. Y., Shimada, Y., and Crouch, R. J., 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 (2000).
7. Haruki, M., Tsunaka, Y., Morikawa, M., and Kanaya, S., Cleavage of a DNA-RNA-DNA/DNA chimeric substrate containing a single ribonucleotide at the DNA-RNA junction with prokaryotic RNases HII. FEBS Lett., 531, 204-208 (2002).
8. Sato, A., Kanai, A., Itaya, M., and Tomita, M., Cooperative regulation for Okazaki fragment processing by RNase HII and FEN-1 purified from a hyperthermophilic archaeon, Pyrococcus furiosus. Biochem. Biophys. Res. Commun., 309, 247-252 (2003).
9. Rydberg, B., and Game, J., Excision of misincorporated ribonucleotides in DNA by RNase H (type 2) and FEN-1 in cell-free extracts. Proc. Natl. Acad. Sci. U.S.A., 99, 16654-16659 (2002).
10. Nanni, R. G., Ding, J., Jacobo-Molina, A., Hughes, S. H., and Arnold, E., Review of HIV-1 reverse transcriptase three-dimensional structure: implications for drug design. Perspectives in Drug Discovery and Design, 1, 129-150 (1993).
11. Toulme, J. J., and Tidd, D., Role of ribonuclease H in antisense oligonucleotide-mediated effects. In "Ribonucleases H", eds. Crouch, R. J., and Toulme, J. J., INSERM, Paris, pp. 225-250 (1998).
12. 2+-dependent RNase HIII from Bacillus subtilis: Classification of RNases H into three families. Biochemistry, 38, 605-618 (1999).
13. Katayanagi, K., Miyagawa, M., Matsushima, M., Ishikawa, M., Kanaya, S., Ikehara, M., Matsuzaki, T., and Morikawa, K., Three-dimensional structure of ribonuclease H from E. coli. Nature, 347, 306-309 (1990).
14. Yang, W., Hendrickson, W. A., Crouch, R. J., and Satow, Y., Structure of ribonuclease H phased at 2 Å resolution by MAD analysis of the selenomethionyl protein. Science, 249, 1398-1405 (1990).
15. Ishikawa, K., Okumura, M., Katayanagi, K., Kimura, S., Kanaya, S., Nakamura, H., and Morikawa, K., Crystal structure of ribonuclease HI from Thermus thermophilus HB8 refined at 2.8 Å resolution. J. Mol. Biol., 230, 529-542 (1993).
16. Lai, L., Yokota, H., Hung, L. W., Kim, R., and Kim, S. H., Crystal structure of archaeal RNase HII: a homologue of human major RNase H. Structure, 8, 897-904 (2000).
17. Muroya, A., Tsuchiya, D., Ishikawa, M., Haruki, M., Morikawa, M., Kanaya, S., and Morikawa, K., Catalytic center of an archaeal Type 2 Ribonuclease H as revealed by X-ray crystallographic and mutational analyses. Protein Sci., 10, 707-714 (2001).
18. Chapados, B. R., Chai, Q., Hosfield, D. J., Shen, B., and Tainer, J. A., Structural biochemistry of a type 2 RNase H: RNA primer recognition and removal during DNA replication. J. Mol. Biol., 307, 541-556 (2001).
19. Davies, J. F. D., Hostomska, Z., Hostomsky, Z., Jordan, S. R., and Matthews, D. A., Crystal structure of the ribonuclease H domain of HIV-1 reverse transcriptase. Science, 252, 88-95 (1991).
20. Kohlstaedt, L. A., Wang, J., Friedman, J. M., Rice, P. A., and Steitz, T. A., Crystal structure at 3.5 Å resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science, 256, 1783-1790 (1992).
21. Jacobo-Molina, A., Ding, J., Nanni, R. G., Clark, A. D. Jr., Lu, X., Tantillo, C., Williams, R. L., Kamer, G., Ferris, A. L., Clark, P., Hizi, A., Hughes, S. H., and Arnold, E., Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 Å resolution shows bent DNA. Proc. Natl. Acad. Sci. U.S.A., 90, 6320-6324 (1993).
22. Kanaya, S., Enzymatic activity and protein stability of E. coli ribonuclease HI. In "Ribonucleases H", eds. Crouch, R. J., and Toulme, J. J., INSERM, Paris, pp. 1-38 (1998).
23. Keck, J. L., Goedken, E. R., and Marqusee, S., Activation/attenuation model for RNase H. A one-metal mechanism with second-metal inhibition. J. Biol. Chem., 273, 34128-34133 (1998).
24. 2+-dependent activity of E. coli ribonuclease HI. Biochemistry, 42, 3366-3374 (2003).
25. Lai, B., Li, Y., Cao, A., and Lai, L., Metal ion binding and enzymatic mechanism of Methanococcus jannaschii RNase HII. Biochemistry, 42, 785-791 (2003).
26. Nakamura, H., Oda, Y., Iwai, S., Inoue, H., Ohtsuka, E., Kanaya, S., Kimura, S., Katsuda, C., Katayanagi, K., Morikawa, K., Miyashiro, H., and Ikehara, M., How does ribonuclease H recognize a DNA-RNA hybrid? Proc. Natl. Acad. Sci. U.S.A., 88, 11535-11539 (1991).
27. Sarafianos, S. G., Das, K., Tantillo, C., Clark, A. D. Jr., Ding, J., Whitcomb, J. M., Boyer, P. L., Hughes, S. H., and Arnold, E., Crystal structure of HIV-1 reverse transcriptase in complex with a polypurine tract RNA:DNA. EMBO J., 20, 1449-1461 (2001).
28. Imanaka, T., Fujii, M., Aramori, I., and Aiba, S., Transformation of Bacillus stearothermophilus with plasmid DNA and characterization of shuttle vector plasmids between Bacillus stearothermophilus and Bacillus subtilis. J. Bacteriol., 149, 824-830 (1982).
29. Aiba, S., Kitai, K., and Imanaka, T., Cloning and expression of thermostable α-amylase gene from Bacillus stearothermophilus in Bacillus stearothermophilus and Bacillus subtilis. Appl. Environ. Microbiol, 46, 1059-1065 (1983).
30. Fujii, M., Takagi, M., Imanaka, T., and Aiba, S., Molecular cloning of a thermostable neutral protease gene from Bacillus stearothermophilus in a vector plasmid and its expression in Bacillus stearothermophilus and Bacillus subtilis. J. Bacteriol., 154, 831-837 (1983).
31. Itaya, M., and Crouch, R. J., A combination of RNase H (rnh) and recBCD or sbcB mutations in Escherichia coli K12 adversely affects growth. Mol. Gen. Genet., 227, 424-432 (1991).
32. Itaya, M., Omori, A., Kanaya, S., Crouch, R. J., Tanaka, T., and Kondo, K., Isolation of RNase H genes that are essential for growth of Bacillus subtilis 168. J. Bacteriol., 181, 2118-2123 (1999).
33. Ohtani, N., Haruki, M., Muroya, A., Morikawa, M., and Kanaya, S., Characterization of ribonuclease HII from Escherichia coli overproduced in a soluble form. J. Biochem. (Tokyo), 127, 895-899 (2000).
34. Imanaka, T., Tanaka, T., Tsunekawa, H., and Aiba, S., Cloning of the genes for penicillinase, penP and penI, of Bacillus licheniformis in some vector plasmids and their expression in Escherichia coli, Bacillus subtilis, and Bacillus licheniformis. J. Bacteriol., 147, 776-786 (1981).
35. Laemmli, U. K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685 (1970).
36. Goodwin, T. W., and Morton, R. A., The spectrophotometric determination of tyrosine and tryptophan in proteins. Biochem. J., 40, 628-632 (1946).
37. Kanaya, S., Katsuda, C., Kimura, S., Nakai, T., Kitakuni, E., Nakamura, H., Katayanagi, K., Morikawa, K., and Ikehara, M., Stabilization of Escherichia coli ribonuclease H by introduction of an artificial disulfide bond. J. Biol. Chem., 266, 6038-6044 (1991).
38. Jay, E., Bambara, R., Padmanabham, P., and Wu, R., DNA sequence analysis: a general, simple and rapid method for sequencing large oligodeoxyribonucleotide fragments by mapping. Nucleic Acids Res., 1, 331-353 (1974).
39. Haruki, M., Hayashi, K., Kochi, T., Muroya, A., Koga, Y., Morikawa, M., Imanaka, T., and Kanaya, S., Gene cloning and characterization of recombinant ribonuclease HII from a hyperthermophilic archaeon. J. Bacteriol., 180, 6207-6214 (1998).
40. 2+ ions reveals two divalent metals bound in the active site. J. Biol. Chem., 276, 7266-7271 (2001).
41. 2+-binding site. Proteins: Struct. Funct. Genet., 17, 337-346 (1993).
42. Huang, H. W., and Cowan, J. A., Metallobiochemistry of the magnesium ion: Characterization of the essential metal-binding site in Escherichia coli ribonuclease H. Eur. J. Biochem., 219, 253-260 (1994).
43. 48. J. Biol. Chem., 271, 32729-32736 (1996).
44. Chai, Q., Qiu, J., Chapados, B. R., and Shen, B., Archaeoglobus fulgidus RNase HII in DNA replication: enzymological functions and activity regulation via metal cofactors. Biochem. Biophys. Res. Commun., 286, 1073-1081 (2001).
45. Muroya, A., Nakano, R., Ohtani, N., Haruki, M., Morikawa, M., and Kanaya, S., Importance of an N-terminal extension of ribonuclease HII from Bacillus stearothermophilus for substrate binding. J. Biosci. Bioeng., 93, 170-175 (2002).