Borasio, Gian Domenico

David, M.

Kaufmann, G.

English

Universität München: Elektronischen Publikationen

T4 bacteriophage-coded polynucleotide kinase and RNA ligase are Involved in host tRNA alteration or repair

Open Access LMU ( Ludwig-Maximilians-Univ. München)

Volume 123 1982 EDITORS W. K . Jokl ik, E D I T O R - I N - C H I E F G . E . Bruening P. W. Choppin R. Hase lkorn D . W. Kingsbury A . J . Lev ine R. W . Schlesinger P. K . Vogt ASSOCIATE EDITORS & Adhya E. P, Geiduschek R. B. Luftig 0. P. Sehgal L. A. Ball R. F. Gesteland R. C. Miller, Jr. T. A. Shalla C. Basilico R. M. Goodman T. J. Morris P. A. Sharp T. Ben-Porat A. Granoff B. Moss J. G. Shaw K I. Berns K. A. Harrap F. A. Murphy T. Shenk D. H. L. Bishop R. Hull P. E. Neiman P. E. Spear J. M. Bishop T. Hunter J. F. Obijeski V. Stollar L. W. Black J. N. Ihle P. Palese M. D. Summers M. A. Bratt A. 0. Jackson M. W. Pons M. M. Susskind J. M. Coffin J. E. Johnson F. Rapp R. H. Symons J. S. Colter J. M. Kaper L. B. Rothman-Denes P. Tegtmeyer S. Dales K. S. Kim J. Sambrook H. E. Varmus R, Eisenman R. M. Krug C. E. Samuel I. M. Verma F. A. Eiserling M. Lai A. Scheid E. Wimmer A. J. Faras R. A. Lamb M. J. Schlesinger J. Youngner B. N. Fields R. A. Lazzarini E. M. Scolnick M. Zaitlin S. J. Flint L. Levintaw J. R. Scott N. D. Zinder R. L B. Francki H F. Lodish ACADEMIC PRESS A Subsidiary of Harcourt Brace Jovanovich, Publishers New York London Paris San Diego San Francisco Säo Paulo Sydney Tokyo Toronto Contents of Volume 123 NUMBER 1, NOVEMBER 1982 E. C. HASCOET, G. H. J . PRETORIUS, AND W. F. COETZEE. Proteus mirabilis Phage 5006M: Restriction Maps of Genome in Relation to Headful Packaging 1 K A R E L RASKA, JR. , AND PHILLIP H. GALLIMORE. An Inverse Relation of the Oncogenic Potential of Adenovirus-Transformed Cells and Their Sensitivity to Killing by Syngeneic Natural Killer Cells 8 E L S VAN LEERDAM, CHRISTIAAN KARREMAN, AND P I E T E R VAN DE PUTTE. Ner, a Cro-like Function of Bacteriophage Mu 19 BERNARD R E V E T AND ETIENNE DELAIN. The Drosophila X Virus Contains a 1-^M Double-Stranded RNA Circularized by a 67-kd Terminal Protein: High-Resolution Denaturation Mapping of Its Genome 29 CECILIA CHENG AND JUDYTA PRASZKIER. Regulation of Type 5 Adenovirus Replication in Murine Ter-atocarcinoma Cell Lines 45 D. BROWN, C. L. JONES, B. A. BROWN, AND E . EHRENFELD. Translation of Capped and Uncapped VSV mRNAs in the Presence of Initiation Factors from Poliovirus-Infected Cells 60 DAVID C. JACKSON AND R. G. WEBSTER. A Topographic Map of the Enzyme Active Center and Antigenic Sites on the Neuraminidase of Influenza Virus A/Tokyo/3/67 (H2N2) 69 YAKOV GLUZMAN AND BARBARA AHRENS. SV40 Early Mutants That Are Defective for Viral DNA Syn-thesis but Competent for Transformation of Cultured Rat and Simian Cells 78 ROKUO USHIYAMA AND YUKITAKA NAKAI. Ultrastructural Features of Fungal Virus-like Particles from Lentinus edodes 93 BRIGITTE ROSENWIRTH AND HANS J . E G G E R S . Biochemistry and Pathogenicity of Echovirus 9. I. Char-acterization of the Virus Particles of Strains Barty and Hill 102 E L E N A L. NOTARIANNI AND CHRIS M. PRESTON. Activation of Cellular Stress Protein Genes by Herpes Simplex Virus Temperature-Sensitive Mutants Which Overproduce Immediate Early Polypeptides 113 JORDAN G. SPIVACK, WILLIAM H. PRUSOFF, AND THOMAS R. TRITTON. A Study of the Antiviral Mechanism of Action of 2-Deoxy-D-glucose: Normally Glycosylated Proteins Are Not Strictly Required for Herpes Simplex Virus Attachment But Increase Viral Penetration and Infectivity 123 ROBERT H. BASSIN, SANDRA RUSCETTI, IQBAL A L I , DANIEL K. HAAPALA, AND ALAN REIN. Normal DBA/ 2 Mouse Cells Synthesize a Glycoprotein Which Interferes with MCF Virus Infection 139 RICHARD K. GAILLARD, JR. , AND WOLFGANG K. JOKLIK. Quantitation of the Relatedness of Reovirus Serotypes 1, 2, and 3 at the Gene Level 1.52 JOSEPH MERREGAERT AND STUART A. AARONSON. Characterization of Inducible Type-C RNA Viruses of Mouse Strains from Different Geographic Areas 165 ERICRASSART AND PAUL JOLICOEUR. Restriction Analysis and Molecular Cloning of Endogenous Murine Leukemia Virus-Specific DNA Sequences of the Mouse Genome 175 HENRY L. NIMAN AND JOHN H. E L D E R . Structural Analysis of Rauscher Virus Gp70 Using Monoclonal Antibodies: Sites of Antigenicity and P15(E) Linkage 187 SHORT COMMUNICATIONS JONATHAN A. ATWATER AND CHARLES E . SAMUEL. Mechanism of Interferon Action: Interferon In-hibits the Synthesis of Viral Proteins and Induces Protein P x Phosphorylation in Both Ade-nylate Cyclase-Deficient and cAMP-Dependent Protein Kinase-Deficient Variants of Mouse Lymphoma Cells 206 WAYNE D. LANCASTER AND JOHN P. SUNDBERG. Characterization of Papillomaviruses Isolated from Cutaneous Fibromas of White-Tailed Deer and Mule Deer 212 CATHARINA PERLMANN, ARI K. SAEMUNDSEN, AND GEORGE K L E I N . A Fraction of Epstein-Barr Virus Virion DNA Is Methylated in and around the EcoRl-J Fragment 217 JUST M. VLAK AND SANDER VAN DER KROL. Transcription of the Autographa califomica Nuclear Polyhedrosis Virus Genome: Location of Late Cytoplasmic mRNA 222 HEINZ-JURGEN T H I E L , FRANK WEILAND, RUDOLF HAFENRICHTER, THOMAS J . MATTHEWS, AND K E N T J . WEINHOLD. Intracellular Cleavage of an SSV Coded gag-Related Protein 229 AUTHOR INDEX FOR VOLUME 123, NUMBER l 235 NUMBER 2, DECEMBER 1982 ROBERT A. LAMB AND CHING-JUH L A I . Spliced and Unspliced Messenger RNAs Synthesized from Cloned Influenza Virus M DNA in an SV40 Vector: Expression of the Influenza Virus Membrane Protein (M,) 237 KONSTANTIN G. KOUSOULAS, STANLEY PERSON, AND THOMAS C. HOLLAND. Herpes Simplex Virus Type 1 Cell Fusion Occurs in the Presence of Ammonium Chloride-Inhibited Glycoproteins 257 E . ANNE DARRAGH AND RICHARD D. MACDONALD. A Host Range Restriction in Infectious Pancreatic Necrosis Virus Maps to the Large RNA Segment and Involves Virus Attachment to the Cell Surface 264 GERD WENGLER, GISELA WENGLER, AND HANS J. GROSS. Terminal Sequences of Sindbis Virus-Specific Nucleic Acids: Identity in Molecules Synthesized in Vertebrate and Insect Cells and Characteristic Properties of the Replicative Form RNA 273 K A R L H. J. GORDON, DALIP S. G I L L , AND ROBERT H. SYMONS. Highly Purified Cucumber Mosaic Virus-Induced RNA-Dependent RNA Polymerase Does Not Contain Any of the Full Length Translation Products of the Genomic RNAs 284 STEVEN PALMIERI, HARTMUT BEUG, AND THOMAS GRAF. Isolation and Characterization of Four New Temperature-Sensitive Mutants of Avian Erythroblastosis Virus (AEV) 296 GRAHAM E. WILCOX AND RICHARD W. COMP ANS. Cell Fusion Induced by Nelson Bay Virus 312 F. F. FANNIN AND J . G. SHAW. Infection of Tobacco Leaf Epidermal Protoplasts with Tobacco Mosaic Virus 323 M. S. GALINSKI, K.-C. CHOW, G. F. ROHRMANN, G. D. PEARSON, AND G. S. BEAUDREAU. Size Determination of Orgyia pseudotsugata Cytoplasmic Polyhedrosis Virus Genomic RNA 328 MARY K. YORK AND MARVIN STODOLSKY. Characterization of PlargF Derivatives from Escherichia coli K12 Transduction. III. PlCml3arörF Derivatives 336 MARK R. H A L L , NIKOU AGHILI, CLAIRE H A L L , J E S S E MARTINEZ, AND STEPHEN ST. JEOR. Chromosomal Organization of the Herpes Simplex Virus Type 2 Genome 344 OSCAR R E Y E S . Characterization of the Recombination Function of Coliphage <j>S0 as Analogous to the recE Recombinative Pathway of Escherichia coli 357 PAUL L. KAPLAN AND BRAD OZANNE. Polyoma Virus-Transformed Cells Produce Transforming Growth Factor(s) and Grow in Serum-Free Medium 372 P. COULON AND D. CONTAMINE. Role of the Drosophila Genome in Sigma Virus Multiplication. II. Host Spectrum Variants among the haP Mutants 381 G A L E E. SMITH AND MAX D. SUMMERS. DNA Homology among Subgroup A, B, and C Baculoviruses 393 VIRGINIA M. H I L L AND DONALD F. SUMMERS. Synthesis of VSV RNPs in Vitro by Cellular VSV RNPs Added to Uninfected HeLa Cell Extracts: VSV Protein Requirements for Replication in Vitro . 407 E . S. ZALMANZON, R. A. V I N K E L E , L. V. GRIGORYEVA, AND R. L. TURETSKAYA. A Study of Rat Embryo Cells Transformed in Vitro by the Bovine Adenovirus Type 3 (BAV-3) DNA before and after a Passage in the Host 420 WERNER STIBBE AND WOLFRAM H. GERLICH. Variable Protein Composition of Hepatitis B Surface An-tigen from Different Donors 436 SHORT COMMUNICATIONS CLAVE L I L I E N . Escherichia coli dnaG Gene Product Is Required for a Normal Rate of Phage T4 DNA Synthesis 443 FAZLUL H. SARKAR AND SOHAN L. GUPTA. On the Inhibition of Interferon Action by Inhibitors of Fatty Acid Cyclooxygenase 448 DAVID P. BOERSMA, FARANGIS S A L E H , KIYOTO NAKAMURA, AND RICHARD W. COMPANS. Structure and Glycosylation of Tacaribe Viral Glycoproteins 452 PAUL ANDERSON AND JAN VILCEK. Synthesis and Biological Characterization of a Covalent Con-jugate between Interferon and Ricin Toxin B Chain 457 B. BLONDEL, R. CRAINIC, 0. AKACEM, P. BRUNEAU, M. GIRARD, AND F. HORODNICEANU. Evidence for Common, Intertypic Antigenic Determinants on Poliovirus Capsid Polypeptides 461 ANNE D. JOHNSON, A L I C E BARKAN, AND JANET E . MERTZ. Nucleotide Sequence Analysis of the Recombinant Joints in 16 Naturally Arising Deletion Mutants of Simian Virus 40 464 DENNIS E . HRUBY, DONNA B. MILLER, AND L. ANDREW BALL. Synthesis of Vaccinia Virus Thymidine Kinase in Microinjected Xenopus Oocytes 470 PHILIP SERWER, G I S E L E A. GREENHAW, AND JERRY L. A L L E N . Concatemers in a Rapidly Sedimenting, Replicating Bacteriophage T7 DNA 474 MICHAEL DAVID, GIAN DOMENICO BORASIO, AND GABRIEL KAUFMANN. T4 Bacteriophage-Coded Poly-nucleotide Kinase and RNA Ligase Are Involved in Host tRNA Alteration or Repair 480 AUTHOR INDEX FOR VOLUME 123 484 CUMULATIVE AUTHOR INDEX FOR VOLUMES 116-123 486 CUMULATIVE SUBJECT INDEX FOR VOLUMES 116-123 493 VIROLOGY 123, 480-483 (1982) T 4 Bacteriophage-Coded Polynucleotide Kinase and R N A Ligase Are Involved in Host tRNA Alteration or Repair M I C H A E L DAVID, GIAN DOMENICO BORASIO, AND G A B R I E L KAUFMANN 1 Biochemistry Department, Weizmann Institute of Science, Rehovot 76100, Israel Received August 10, 1982; accepted September 7, 1982 T4-induced polynucleotide kinase, RNA ligase, and a tRNA-specific endonuclease were previously implicated in host tRNA breakage and reunion. To examine this hypothesis we followed the fate of host tRNAs in T4-infected Escherichia coli CTröx, a strain re-stricting phage mutants lacking polynucleotide kinase (pnk~) or RNA ligase (rli~). Two host tRNA species which were cleaved in the anticodon loops were further processed in the wild type but not in the mutant infections, indicating that polynucleotide kinase and RNA ligase are involved in the alteration or repair of these E. coli CTr5X tRNA species. T4-coded polynucleotide kinase (1) and R N A ligase (2) have been thoroughly char-acterized in vitro (3-5) but their roles in phage physiology sti l l need to be deter-mined. W e have previously proposed that both enzymes participate in reactions of host t R N A breakage and reunion, required for phage development in certain host s trains (6, 7). B y following the fate of host t R N A molecules in Escherichia coli C T r 5 X (8), a host strain restrictive to T 4 mutants deficient in 3'-phosphatase- polynucleotide kinase (8-10) or R N A ligase (11), we dem-onstrate here the involvement of these T 4 functions in the alteration or repair of host t R N A species. W e have recently shown that E. coli C T r 5 X differs from other E. coli s trains wh ich are permissive to T 4 polynucleotide kinase (pnk~) or R N A ligase deficient (rli~) mutants in the cleavage pattern of host t R N A s following infection (12). T h u s , while only leucine t R N A : is cleaved in T 4 -infected E. coli B (13, 14) and in other permissive hosts, two additional t R N A species are cleaved during infection of E. coli C T r 5 X . Contrary to leucine t R N A , wh ich is cleaved in the extra-arm (14), the C T r 5 X - s p e c i f i c cleavages occur next to the 1 To whom all correspondence should be addressed: c/o Dr. R. G. Martin, NIAMDD, Bldg. 2, Rm. 214, Bethesda, Md. 20205. anticodon and are mediated by a separate T4- induced t R N A - s p e c i f i c endonuclease (12). I n the present experiment we com-pared host t R N A cleavage patterns during infection of E. coli C T r 5 X wi th either wild-type, prcfe" (8, 9), or rli~ (15) s trains of T 4 . Figure 1 depicts the kinet ics of host t R N A fragment appearance a n d disappearance during these infections. B o t h the wildtype and the mutant infections gave rise to six t R N A fragment bands. B a n d s I a n d I V originated from leucine t R N A ! and are common to all T4- infec ted E. coli s trains tested (12-14). Fragments ( I I and V I ) and ( I I I and V ) correspond, respectively, to the 3' and 5' fragments of two C T r 5 X - s p e c i f i c t R N A species which are cleaved in their anticodon loop (12). I n a l l these infections, leucine t R N A x fragments appeared and disappeared with a s imi lar t ime course. However, a difference was noted between the wild-type and the mutant infections with respect to the behavior of the C T r 5 X -specific fragments. T h u s , during wild-type infection the C T r 5 X - s p e c i f i c fragment bands reached m a x i m a l intensity between 4 and 6 min postinfection and then began to fade, having almost completely disap-peared at 22 min postinfection. B y con-trast, in the pnk~ a n d rli~ infections these fragments appeared somewhat later than in the wild-type infection and persisted (II + V I ) or seemed to have been only 0042-6822/82/160480-04$02.00/0 Copyright © 1982 by Academic Press, Inc. All rights of reproduction in any form reserved. 480 SHORT COMMUNICATIONS 481 0 2 4 6 9 15 22 o 2 4 6 9 15 22 0 2 4 6 9 15 22 C FIG. 1. E. coli CTr5X tRNA cleavage patterns during infection with T4 wild type (a), pnk" (b), or rli~ (c) phage strains. E. coli CTröX cells were pulse labeled with 3 2 P, chased with unlabeled Pi and then infected with the indicated phage strain. Culture aliquots were withdrawn before infection or at the indicated infection times, and RNA was extracted from them and separated by denaturing gel electrophoresis as previously described (12). The mutant strains employed were: pseT2 (polynucleotide kinase deficient, Ref. (9)) and am M69 (RNA ligase deficient, Refs. {15, 16). 482 SHORT COMMUNICATIONS slightly modified ( I I I + V ) at later infec-tion times. Fragments I I and V I remained virtual ly unchanged, both in quantity and electrophoretic mobility unt i l 22 m i n in the pnk~ and rli~ infections. F r a g m e n t I I I did not change in the pnk~ infection while in the rli~ system it appeared to have been part ial ly converted into a slightly faster migrating species designated I I I * (15- and 22-min lanes) which at 22 m i n constituted about one-half of the original b a n d I I I . W i t h both mutants , B a n d V completely disappeared wi th in 15 m i n postinfection with a parallel appearance of a new band migrating somewhat faster than band V I and designated V * . T h e failure of pnk~ and rli~ mutants to process further the C T r 5 X - s p e c i f i c t R N A fragments which disappeared late in the wild-type infection indicates that polynu-cleotide kinase and R N A ligase are nor-mally involved in the alteration or repair of the corresponding t R N A species. A l -though the reactions which cause the "dis-appearance" of the C T r 5 X - s p e c i f i c t R N A fragments are not known presently , it seems reasonable to assume, based on the in vitro properties of polynucleotide k inase (3) and R N A ligase (1, 5), that these frag-ments undergo phosphoryl rearrangement and perhaps additional modifications prior to their ligation. T h e slight changes w h i c h seemed to occur wi th fragments I I I a n d V during the mutant infections (Fig . 1) may reflect such additional steps, presumably leading to an altered t R N A structure fol-lowing the ligation. Alternatively, these changes could be due to abnormal degra-dation of the fragments whose processing was arrested by the mutation. T h e results also indicate that polynucleotide kinase a n d R N A ligase are not related to the re-moval of the leucine t R N A i fragments since this process was not affected by pnk~ a n d rli~ mutations. G i v e n the existence of a pathway which includes the T4- induced anticodon nu-clease (12), polynucleotide kinase, R N A ligase, and perhaps additional processing enzymes, what do these host t R N A alter-ations, or breakage and subsequent repair, contribute to phage development a n d why are they needed in E. coli C T r 5 X a n d not in other host strains permissive to pnk~ and rli~ mutants? One explanation is that this putative pathway provides a suppres-sor t R N A species required later in T 4 gene expression. Such a suppressor t R N A spe-cies may already exist in most T 4 host strains but probably not in E. coli C T r 5 X (7, 9, 10) in which this function could be provided by the putative T4- induced a l -teration pathway. Supporting this view is the fact that E. coli C T r 5 X can be con-verted into a host permissive to a pnk~ deletion mutant by transformation with an amber suppressor function (10, 11). Al ter-natively, polynucleotide kinase and R N A ligase may restore the t R N A s cleaved ear-lier by the anticodon nuclease without fur-ther change. W e have recently isolated, among pseudorevertants of pnkT mutants able to grow on E. coli C T r 5 X , a phage lacking the anticodon nuclease activity. T h i s double mutant forms smal l plaques on E. coli C T r 5 X but wild-type sized plaques on E. coli B , providing further ev-idence for a functional connection between the anticodon nuclease, polynucleotide k i -nase, and R N A ligase and suggesting that the alteration of host t R N A s , if it occurs, is not an "essential" function for T 4 . ACKNOWLEDGMENTS We thank L . Snyder for phage and bacterial strains. G. K. was an incumbent of the Alan Dixon Career Development Chair. R E F E R E N C E S /. RICHARDSON, C. C , Proc. Nat. Acad. Sei. USA 54, 158-165 (1965). 2. S ILBER, R., MALATHI, V. G., and HURWITZ, J . , Proc. Nat. Acad. Sei. USA 69, 3009-3013 (1972). 3. K L E P P E , K., and L l L L E H A U G , J . R., Advan. En-zymol. 63, 245-275 (1977). 4. H l G G I N S , N. P., and COZZARELLI , N. R., In "Methods in Enzymology" (R. Wu, ed.), Vol. 68, pp. 50-71. Academic Press, New York, 1979. 5. GUMPORT, R. I., and U H L E N B E C K , O. C , In "Gene Amplification and Analysis" (J. G . Chi-rikjian and T. S. Papas, eds.), Vol. 2, pp. 1-44. Elsevier North-Holland, New York, 1981. 6. KAUFMANN, G. , and KALLENBACH, N. R., Nature (London) 254, 452-454 (1975). 7. DAVID, M., V E K S T E I N , R., and KAUFMANN, G. , S H O R T C O M M U N I C A T I O N S 483 Proc. Nat. Acad. Sei. USA 76, 5430-5434 (1979). 8. D E P E W , R . E . , and C O Z Z A R E L L I , N . R . , J. Viroi 13, 888-897 (1974). 9. C A M E R O N , V . , and U H L E N B E K , O. C , Biochem-istry 16, 5120-5126 (1977). 10. S l R O T K I N , K . , C O O L E Y , W. , R U N N E L S , J . , and S N Y D E R , L . R . , J. Mol. Biol. 123, 221-233 (1978). 11. RUNNELS, J . M. , SOLTIS, D. , H E Y , T . , and SNY-DER, L . , J. Mol. Biol. 154, 273-286 (1982). 12. DAVID, M., BORASIO, G . D., and KAUFMANN, G . Proc. Nat. Acad. Sei. USA, in press. 13. KANO-SUEOKA, T . , and S u E O K A , N., J. Mol. Biol 37, 475-491 (1968). 14. Y U D E L E V I C H , A . , J. Mol. Biol. 60, 21-29 (1972). 15. SNOPEK, T . J . , WOOD, W . B. , C O N L E Y , M . E . , C H E N , P., and C O Z Z A R E L L I , N . R., Proc. Nat. Acad. Sei. USA 74, 3355-3359 (1978). 16. WOOD, W . B . , and HENNINGER, M. , J. Mol. Biol. 39, 603-618 (1969). 

Gene Amplification and Analysis&quot;

In &quot;Methods in Enzymology&quot;

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T4 bacteriophage-coded polynucleotide kinase and RNA ligase are Involved in host tRNA alteration or repair

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