Structure of Ribonuclease H Phased at 2 Å Resolution by MAD Analysis of the Selenomethionyl Protein
10.1126/science.2169648
Crossref journal-article
American Association for the Advancement of Science (AAAS)
Science (221)
Abstract

Ribonuclease H digests the RNA strand of duplex RNA⋅DNA hybrids into oligonucleotides. This activity is indispensable for retroviral infection and is involved in bacterial replication. The ribonuclease H from Escherichia coli is homologous with the retroviral proteins. The crystal structure of the E. coli enzyme reveals a distinctive α-β tertiary fold. Analysis of the molecular model implicates a carboxyl triad in the catalytic mechanism and suggests a likely mode for the binding of RNA⋅DNA substrates. The structure was determined by the method of multiwavelength anomalous diffraction (MAD) with the use of synchrotron data from a crystal of the recombinant selenomethionyl protein.

Bibliography

Yang, W., Hendrickson, W. A., Crouch, R. J., & Satow, Y. (1990). Structure of Ribonuclease H Phased at 2 Å Resolution by MAD Analysis of the Selenomethionyl Protein. Science, 249(4975), 1398–1405.

Authors 4
  1. Wei Yang (first)
  2. Wayne A. Hendrickson (additional)
  3. Robert J. Crouch (additional)
  4. Yoshinori Satow (additional)
References 63 Referenced 380
  1. AMEMIYA, Y, DESIGN AND PERFORMANCE OF AN IMAGING PLATE SYSTEM FOR X-RAY-DIFFRACTION STUDY, NUCLEAR INSTRUMENTS & METHODS IN PHYSICS RESEARCH SECTION A-ACCELERATORS SPECTROMETERS DETECTORS AND ASSOCIATED EQUIPMENT 266: 645 (1988). (10.1016/0168-9002(88)90458-5) / NUCLEAR INSTRUMENTS & METHODS IN PHYSICS RESEARCH SECTION A-ACCELERATORS SPECTROMETERS DETECTORS AND ASSOCIATED EQUIPMENT (1988)
  2. Berkower, I., Journal of Biological Chemistry 248: 5914 (1973). (10.1016/S0021-9258(19)43488-1) / Journal of Biological Chemistry (1973)
  3. CARLISLE, C.H., STRUCTURE OF RIBONUCLEASE AT 25 ANGSTROM RESOLUTION, JOURNAL OF MOLECULAR BIOLOGY 85: 1 (1974). (10.1016/0022-2836(74)90125-9) / JOURNAL OF MOLECULAR BIOLOGY (1974)
  4. Crouch, R. J., Nucleases: 211 (1982). / Nucleases (1982)
  5. DASGUPTA, S, MULTIPLE MECHANISMS FOR INITIATION OF COLE1 DNA-REPLICATION - DNA-SYNTHESIS IN THE PRESENCE AND ABSENCE OF RIBONUCLEASE-H, CELL 51: 1113 (1987). (10.1016/0092-8674(87)90597-6) / CELL (1987)
  6. DEMASSY, B, MULTIPLE ORIGIN USAGE FOR DNA-REPLICATION IN SDRA(RNH) MUTANTS OF ESCHERICHIA-COLI K-12 - INITIATION IN THE ABSENCE OF ORIC, JOURNAL OF MOLECULAR BIOLOGY 178: 227 (1984). (10.1016/0022-2836(84)90141-4) / JOURNAL OF MOLECULAR BIOLOGY (1984)
  7. 10.1126/science.2832946
  8. DOOLITTLE, R.F., ORIGINS AND EVOLUTIONARY RELATIONSHIPS OF RETROVIRUSES, QUARTERLY REVIEW OF BIOLOGY 64: 1 (1989). / QUARTERLY REVIEW OF BIOLOGY (1989)
  9. Fanchon , E., Acta Crystallographica Section A 46: 809 (1990). (10.1107/S0108767390005967) / Acta Crystallographica Section A (1990)
  10. FREEMONT, P.S., COCRYSTAL STRUCTURE OF AN EDITING COMPLEX OF KLENOW FRAGMENT WITH DNA, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 85: 8924 (1988). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1988)
  11. GILSON, M.K., J COMPUT CHEM 9: 327 (1987). / J COMPUT CHEM (1987)
  12. GOFF, S.P., RETROVIRAL REVERSE-TRANSCRIPTASE - SYNTHESIS, STRUCTURE, AND FUNCTION, JOURNAL OF ACQUIRED IMMUNE DEFICIENCY SYNDROMES AND HUMAN RETROVIROLOGY 3: 817 (1990). / JOURNAL OF ACQUIRED IMMUNE DEFICIENCY SYNDROMES AND HUMAN RETROVIROLOGY (1990)
  13. GRAVES, B.J., STRUCTURE OF INTERLEUKIN 1-ALPHA AT 2.7-A RESOLUTION, BIOCHEMISTRY 29: 2679 (1990). (10.1021/bi00463a009) / BIOCHEMISTRY (1990)
  14. GUERRIERTAKADA, C, METAL-ION REQUIREMENTS AND OTHER ASPECTS OF THE REACTION CATALYZED BY M1 RNA, THE RNA SUBUNIT OF RIBONUCLEASE-P FROM ESCHERICHIA-COLI, BIOCHEMISTRY 25: 1509 (1986). (10.1021/bi00355a006) / BIOCHEMISTRY (1986)
  15. 10.1126/science.3406739
  16. HANSEN, J, IDENTIFICATION AND CHARACTERIZATION OF HIV-SPECIFIC RNASE-H BY MONOCLONAL-ANTIBODY, EMBO JOURNAL 7: 239 (1988). (10.1002/j.1460-2075.1988.tb02805.x) / EMBO JOURNAL (1988)
  17. Hendrickson, W. A., Computing in Crystallography: 13.01 (1980). / Computing in Crystallography (1980)
  18. HENDRICKSON, W.A., SELENOMETHIONYL PROTEINS PRODUCED FOR ANALYSIS BY MULTIWAVELENGTH ANOMALOUS DIFFRACTION (MAD) - A VEHICLE FOR DIRECT DETERMINATION OF 3-DIMENSIONAL STRUCTURE, EMBO JOURNAL 9: 1665 (1990). (10.1002/j.1460-2075.1990.tb08287.x) / EMBO JOURNAL (1990)
  19. HENDRICKSON, W.A., CRYSTAL-STRUCTURE OF CORE STREPTAVIDIN DETERMINED FROM MULTIWAVELENGTH ANOMALOUS DIFFRACTION OF SYNCHROTRON RADIATION, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 86: 2190 (1989). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1989)
  20. HENDRICKSON, W.A., CRYSTALLOGRAPHIC STRUCTURE-ANALYSIS OF LAMPREY HEMOGLOBIN FROM ANOMALOUS DISPERSION OF SYNCHROTRON RADIATION, PROTEINS-STRUCTURE FUNCTION AND GENETICS 4: 77 (1988). (10.1002/prot.340040202) / PROTEINS-STRUCTURE FUNCTION AND GENETICS (1988)
  21. HENDRICKSON, W.A., TRANSACTIONS OF THE AMERICAN CRYSTALLOGRAPHIC ASSOCIATION 21: 11 (1985). / TRANSACTIONS OF THE AMERICAN CRYSTALLOGRAPHIC ASSOCIATION (1985)
  22. HILL, C, THE STRUCTURAL AND SEQUENCE HOMOLOGY OF A FAMILY OF MICROBIAL RIBONUCLEASES, TRENDS IN BIOCHEMICAL SCIENCES 8: 364 (1983). (10.1016/0968-0004(83)90363-8) / TRENDS IN BIOCHEMICAL SCIENCES (1983)
  23. HIZI, A, MUTATIONAL ANALYSIS OF THE RIBONUCLEASE-H ACTIVITY OF HUMAN IMMUNODEFICIENCY VIRUS-1 REVERSE-TRANSCRIPTASE, VIROLOGY 175: 575 (1990). (10.1016/0042-6822(90)90444-V) / VIROLOGY (1990)
  24. HORIUCHI, T, RNASE H-DEFECTIVE MUTANTS OF ESCHERICHIA-COLI - A POSSIBLE DISCRIMINATORY ROLE OF RNASE-H IN INITIATION OF DNA-REPLICATION, MOLECULAR & GENERAL GENETICS 195: 17 (1984). (10.1007/BF00332717) / MOLECULAR & GENERAL GENETICS (1984)
  25. INOUE, H, SEQUENCE-DEPENDENT HYDROLYSIS OF RNA USING MODIFIED OLIGONUCLEOTIDE SPLINTS AND RNASE H, FEBS LETTERS 215: 327 (1987). (10.1016/0014-5793(87)80171-0) / FEBS LETTERS (1987)
  26. Itaya, M., Molecular Genetics and Genomics 227: 438 (1991). (10.1007/BF00273935) / Molecular Genetics and Genomics (1991)
  27. ITOH, T, FORMATION OF AN RNA PRIMER FOR INITIATION OF REPLICATION OF COLE1 DNA BY RIBONUCLEASE-H, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 77: 2450 (1980). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1980)
  28. JOHNSON, M.S., COMPUTER-ANALYSIS OF RETROVIRAL POL GENES - ASSIGNMENT OF ENZYMATIC FUNCTIONS TO SPECIFIC SEQUENCES AND HOMOLOGIES WITH NONVIRAL ENZYMES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 83: 7648 (1986). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1986)
  29. 10.1107/S0021889878013308
  30. 10.1002/bip.360221211
  31. KAHN, R, CRYSTAL-STRUCTURE STUDY OF OPSANUS-TAU PARVALBUMIN BY MULTIWAVELENGTH ANOMALOUS DIFFRACTION, FEBS LETTERS 179: 133 (1985). (10.1016/0014-5793(85)80207-6) / FEBS LETTERS (1985)
  32. KANAYA, S, DNA-SEQUENCE OF THE GENE CODING FOR ESCHERICHIA-COLI RIBONUCLEASE-H, JOURNAL OF BIOLOGICAL CHEMISTRY 258: 1276 (1983). (10.1016/S0021-9258(18)33189-2) / JOURNAL OF BIOLOGICAL CHEMISTRY (1983)
  33. KANAYA, S, OVERPRODUCTION AND PRELIMINARY CRYSTALLOGRAPHIC STUDY OF RIBONUCLEASE H FROM ESCHERICHIA-COLI, JOURNAL OF BIOLOGICAL CHEMISTRY 264: 11546 (1989). (10.1016/S0021-9258(18)80096-5) / JOURNAL OF BIOLOGICAL CHEMISTRY (1989)
  34. KANAYA, S, IDENTIFICATION OF THE AMINO-ACID-RESIDUES INVOLVED IN AN ACTIVE-SITE OF ESCHERICHIA-COLI RIBONUCLEASE-H BY SITE-DIRECTED MUTAGENESIS, JOURNAL OF BIOLOGICAL CHEMISTRY 265: 4615 (1990). (10.1016/S0021-9258(19)39607-3) / JOURNAL OF BIOLOGICAL CHEMISTRY (1990)
  35. KARLE, J, INTERNATIONAL JOURNAL OF QUANTUM CHEMISTRY SYMPOSIUM 7: 357 (1980). / INTERNATIONAL JOURNAL OF QUANTUM CHEMISTRY SYMPOSIUM (1980)
  36. KARTHA, G, TERTIARY STRUCTURE OF RIBONUCLEASE, NATURE 213: 862 (1967). (10.1038/213862a0) / NATURE (1967)
  37. KELLER, W, DEGRADATION OF DNA RNA HYBRIDS BY RIBONUCLEASE-H AND DNA POLYMERASES OF CELLULAR AND VIRAL ORIGIN, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 69: 3360 (1972). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1972)
  38. KITANI, T, EVIDENCE THAT DISCONTINUOUS DNA-REPLICATION IN ESCHERICHIA-COLI IS PRIMED BY APPROXIMATELY 10 TO 12 RESIDUES OF RNA STARTING WITH A PURINE, JOURNAL OF MOLECULAR BIOLOGY 184: 45 (1985). (10.1016/0022-2836(85)90042-7) / JOURNAL OF MOLECULAR BIOLOGY (1985)
  39. KONNERT, J.H., RESTRAINED-PARAMETER STRUCTURE-FACTOR LEAST-SQUARES REFINEMENT PROCEDURE FOR LARGE ASYMMETRIC UNITS, ACTA CRYSTALLOGRAPHICA SECTION A 32: 614 (1976). / ACTA CRYSTALLOGRAPHICA SECTION A (1976)
  40. KRUG, M.S., RIBONUCLEASE-H ACTIVITIES ASSOCIATED WITH VIRAL REVERSE TRANSCRIPTASES ARE ENDONUCLEASES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 86: 3539 (1989). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1989)
  41. LEVIN, J.G., FUNCTIONAL-ORGANIZATION OF THE MURINE LEUKEMIA-VIRUS REVERSE-TRANSCRIPTASE - CHARACTERIZATION OF A BACTERIALLY EXPRESSED AKR DNA-POLYMERASE DEFICIENT IN RNASE-H ACTIVITY, JOURNAL OF VIROLOGY 62: 4376 (1988). (10.1128/jvi.62.11.4376-4380.1988) / JOURNAL OF VIROLOGY (1988)
  42. LUO, G.X., SPECIFICITIES INVOLVED IN THE INITIATION OF RETROVIRAL PLUS-STRAND DNA, JOURNAL OF VIROLOGY 64: 592 (1990). (10.1128/jvi.64.2.592-597.1990) / JOURNAL OF VIROLOGY (1990)
  43. 10.1126/science.2470150
  44. MILLER, H.I., RIBONUCLEASE-H (HYBRID) IN ESCHERICHIA-COLI - IDENTIFICATION AND CHARACTERIZATION, JOURNAL OF BIOLOGICAL CHEMISTRY 248: 2621 (1973). (10.1016/S0021-9258(19)44152-5) / JOURNAL OF BIOLOGICAL CHEMISTRY (1973)
  45. MIYAHARA, J, A NEW TYPE OF X-RAY AREA DETECTOR UTILIZING LASER STIMULATED LUMINESCENCE, NUCLEAR INSTRUMENTS & METHODS IN PHYSICS RESEARCH SECTION A-ACCELERATORS SPECTROMETERS DETECTORS AND ASSOCIATED EQUIPMENT 246: 572 (1986). (10.1016/0168-9002(86)90156-7) / NUCLEAR INSTRUMENTS & METHODS IN PHYSICS RESEARCH SECTION A-ACCELERATORS SPECTROMETERS DETECTORS AND ASSOCIATED EQUIPMENT (1986)
  46. MOELLING, K, NATURE 234: 240 (1971). (10.1038/234240a0) / NATURE (1971)
  47. MURTHY, HMK, CRYSTAL-STRUCTURE OF CLOSTRIDIUM-ACIDI-URICI FERREDOXIN AT 5-A RESOLUTION BASED ON MEASUREMENTS OF ANOMALOUS X-RAY-SCATTERING AT MULTIPLE WAVELENGTHS, JOURNAL OF BIOLOGICAL CHEMISTRY 263: 18430 (1988). (10.1016/S0021-9258(19)81376-5) / JOURNAL OF BIOLOGICAL CHEMISTRY (1988)
  48. OGATA C.M. unpublished data.
  49. OYAMA, F, INTRINSIC-PROPERTIES OF REVERSE-TRANSCRIPTASE IN REVERSE TRANSCRIPTION - ASSOCIATED RNASE H IS ESSENTIALLY REGARDED AS AN ENDONUCLEASE, JOURNAL OF BIOLOGICAL CHEMISTRY 264: 18808 (1989). (10.1016/S0021-9258(18)51539-8) / JOURNAL OF BIOLOGICAL CHEMISTRY (1989)
  50. PRASAD, V.R., LINKER INSERTION MUTAGENESIS OF THE HUMAN IMMUNODEFICIENCY VIRUS REVERSE-TRANSCRIPTASE EXPRESSED IN BACTERIA - DEFINITION OF THE MINIMAL POLYMERASE DOMAIN, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 86: 3104 (1989). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1989)
  51. 10.1038/313277a0
  52. READY, M.P., RIBOSOME-INHIBITING PROTEINS, RETROVIRAL REVERSE TRANSCRIPTASES, AND RNASE-H SHARE COMMON STRUCTURAL ELEMENTS, PROTEINS-STRUCTURE FUNCTION AND GENETICS 3: 53 (1988). (10.1002/prot.340030105) / PROTEINS-STRUCTURE FUNCTION AND GENETICS (1988)
  53. REPASKE, R, INHIBITION OF RNASE-H ACTIVITY AND VIRAL REPLICATION BY SINGLE MUTATIONS IN THE 3' REGION OF MOLONEY MURINE LEUKEMIA-VIRUS REVERSE-TRANSCRIPTASE, JOURNAL OF VIROLOGY 63: 1460 (1989). (10.1128/jvi.63.3.1460-1464.1989) / JOURNAL OF VIROLOGY (1989)
  54. RICHARDS, F.M., PROTEIN STRUCTURE, RIBONUCLEASE-S AND NUCLEOTIDE INTERACTIONS, COLD SPRING HARBOR SYMPOSIA ON QUANTITATIVE BIOLOGY 36: 35 (1971). / COLD SPRING HARBOR SYMPOSIA ON QUANTITATIVE BIOLOGY (1971)
  55. SATOW, Y, HORIZONTAL-TYPE 4-CIRCLE DIFFRACTOMETER STATION OF THE VERTICAL WIGGLER BEAMLINE AT THE PHOTON FACTORY, REVIEW OF SCIENTIFIC INSTRUMENTS 60: 2390 (1989). (10.1063/1.1140728) / REVIEW OF SCIENTIFIC INSTRUMENTS (1989)
  56. SHERIFF, S, STRUCTURE OF MYOHEMERYTHRIN IN THE AZIDOMET STATE AT 1.7/1.3-A RESOLUTION, JOURNAL OF MOLECULAR BIOLOGY 197: 273 (1987). (10.1016/0022-2836(87)90124-0) / JOURNAL OF MOLECULAR BIOLOGY (1987)
  57. SHINNICK, T.M., NUCLEOTIDE-SEQUENCE OF MOLONEY MURINE LEUKEMIA-VIRUS, NATURE 293: 543 (1981). (10.1038/293543a0) / NATURE (1981)
  58. TANESE, N, DOMAIN-STRUCTURE OF THE MOLONEY MURINE LEUKEMIA-VIRUS REVERSE-TRANSCRIPTASE - MUTATIONAL ANALYSIS AND SEPARATE EXPRESSION OF THE DNA-POLYMERASE AND RNASE-H ACTIVITIES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 85: 1777 (1988). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1988)
  59. TOMIZAWA, J, CONTROL OF COLE1 PLASMID REPLICATION - THE PROCESS OF BINDING OF RNA-I TO THE PRIMER TRANSCRIPT, CELL 38: 861 (1984). (10.1016/0092-8674(84)90281-2) / CELL (1984)
  60. TORREY, T.A., DNAA SUPPRESSOR (DASF) MUTANTS OF ESCHERICHIA-COLI ARE STABLE DNA-REPLICATION (SDRA RNH) MUTANTS, MOLECULAR & GENERAL GENETICS 196: 350 (1984). (10.1007/BF00328070) / MOLECULAR & GENERAL GENETICS (1984)
  61. WANG, AHJ, MOLECULAR-STRUCTURE OF R(GCG)D(TATACGC) - A DNA RNA HYBRID HELIX JOINED TO DOUBLE HELICAL DNA, NATURE 299: 601 (1982). (10.1038/299601a0) / NATURE (1982)
  62. WLODAWER, A, THE REFINED CRYSTAL-STRUCTURE OF RIBONUCLEASE A AT 2.0 A RESOLUTION, JOURNAL OF BIOLOGICAL CHEMISTRY 257: 1325 (1982). (10.1016/S0021-9258(19)68195-0) / JOURNAL OF BIOLOGICAL CHEMISTRY (1982)
  63. YANG, W, J BIOL CHEM 265: 13533 (1990). (10.1016/S0021-9258(18)77380-8) / J BIOL CHEM (1990)
Dates
Type When
Created 18 years, 10 months ago (Oct. 5, 2006, 6:10 p.m.)
Deposited 1 year, 7 months ago (Jan. 12, 2024, 5:21 a.m.)
Indexed 1 month ago (July 25, 2025, 6:07 a.m.)
Issued 34 years, 11 months ago (Sept. 21, 1990)
Published 34 years, 11 months ago (Sept. 21, 1990)
Published Print 34 years, 11 months ago (Sept. 21, 1990)
Funders 0

None

@article{Yang_1990, title={Structure of Ribonuclease H Phased at 2 Å Resolution by MAD Analysis of the Selenomethionyl Protein}, volume={249}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.2169648}, DOI={10.1126/science.2169648}, number={4975}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Yang, Wei and Hendrickson, Wayne A. and Crouch, Robert J. and Satow, Yoshinori}, year={1990}, month=sep, pages={1398–1405} }