Multiple degradation pathways of the rpsO mRNA of Escherichia coli. RNase E interacts with the 5' and 3' extremities of the primary transcript

Biochimie

Volumn 78, Issue 6, 1996, Pages 416-424

  Hajnsdorf, E ^a   Braun, F ^a   Haugel Nielsen, J ^a   Le Derout, J ^a   Regnier P ^a  

^a INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

Author keywords

mRNA decay; Poly(A) polymerase I; Polyadenylation; Ribonucleases

Indexed keywords

ENDONUCLEASE; MESSENGER RNA; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; RIBONUCLEASE;

ARTICLE; ESCHERICHIA COLI; MOLECULAR INTERACTION; NONHUMAN; POLYADENYLATION; RNA DEGRADATION; RNA TRANSLATION; TRANSCRIPTION TERMINATION;

ESCHERICHIA COLI;

EID: 0029825005     PISSN: 03009084     EISSN: None     Source Type: Journal    
DOI: 10.1016/0300-9084(96)84748-1     Document Type: Article

References (73)

1. 1 Brawerman G (1993) mRNA degradation in eukaryotic cells: an overview. In: Control of Messenger RNA stability (Belasco JG, Brawerman G, eds) Academic Press, New York, 149-159
2. 2 Belasco JG (1993) mRNA degradation in prokaryotic cells: An overview. In: Control of Messenger RNA stability (Belasco JG, Brawerman G, eds) Academic Press, New York, 3-12
3. 3 Yu D, Deutscher MP (1995) Oligoribonuclease is distinct from the other known exoribonucleases of Escherichia coli J Bacteriol 177, 4137-4139
4. 4 Deutscher MP (1988) The metabolic role of RNases. TIBS 13, 136-139
5. 5 Grunberg-Manago M (1963) Polynucleotide phosphorylase. In: Progress in Nucleic Acids Research (Cohn W, ed) Academic Press, New York, 93-133
6. 6 Spahr PF, Schlessinger D (1964) Breakdown of messenger ribonucleic acid by a potassium-activated phophodiesterase from Escherichia coli. J Biol Chem 238, PC2251-PC2253
7. 7 Hajnsdorf E, Steier O, Coscoy L, Teysset L, Régnier P. (1994) Roles of RNase E, RNase II and PNPase in the degradation of the rpsO transcript of Escherichia coli: Stabilizing function and evidence for efficient degradation in an ams-pnp-rnb mutant. EMBO J 13, 3368-3377
8. 8 Donovan WP, Kushner SR (1986) Polynucleotide phosphorylase and ribonuclease II are required for cell viability and mRNA turnover in Escherichia coli K-12. Proc Natl Acad Sci USA 83, 120-124
9. 9 King CK, Sirdeshmukh R, Schlessinger D (1986) Nucleolytic processing of ribonucleic acid transcripts in prokaryotes. Microbiol Rev 50, 428-451
10. 10 Mudd EA, Prentki P, Belin D, Krisch HM (1988) Processing of unstable bacteriophage T4 gene 32 mRNAs into a stable species requires E coli ribonuclease E. EMBO J 7, 3601-3607
11. 11 Court D (1993) RNA processing and degradation by RNase III In: Control of mRNA stability (Belasco JG, Brawerman G, eds) Academic Press, New York, 71-116
12. 12 Régnier P, Portier C (1986) Initiation, attenuation and RNase III processing of transcripts from the E coli operon encoding ribosomal protein S15 and polynucleotide phosphorylase. J Mol Biol 187, 23-32
13. 13 Régnier P, Grunberg-Manago M (1989) Cleavage by RNase III in the transcripts of the metY-nusA-infB operon of E coli releases the tRNA and initiates the decay of the downstream mRNA. J Mol Biol 210, 293-302
14. 14 Bardwell JCA, Régnier P, Chen S-M, Nakamura Y Grunberg-Manago M, Court D (1989) Autoregulation of RNase III operon by mRNA processing. EMBO J 8, 3401-3407
15. 15 Régnier P, Hajnsdorf E (1991) Decay of mRNA encoding ribosomal protein S15 of Escherichia coli is initiated by an RNase E-dependent endonucleolytic cleavage that removes the 3′ stabilizing stem and loop structure. J Mol Biol 217, 283-292.
16. 16 Ehretsmann CP, Carpousis AJ, Krisch HM (1992) mRNA degradation in prokaryotes. FASEB J 6, 3186-3192
17. 17 Jain C, Belasco JG (1995) RNase E autoregulates its synthesis by controlling the degradation rate of its own mRNA in Escherichia coli: unusual sensitivity of the rne transcript to RNase E activity. Genes Dev 9, 84-96
18. 18 Apirion D, Lassar AB (1978) A conditional lethal mutant of E coli which affects the processing of ribosomal RNA. J Biol Chem 253, 1738-1742
19. 19 Mudd EA, Krish HM, Higgins CF (1990) RNase E, an endoribonuclease, has a general role in the chemical decay of E coli mRNA: evidence that rne and ams are the same genetic locus. Mol Microbiol 2127-2135
20. 20 Ono M, Kuwano M (1979) A conditional lethal mutation in an E coli strain with longer chemical lifetime of messenger RNA. J Mol Biol 129, 343-357
21. 21 Babitzke P, Kushner SR (1991) The ams (altered mRNA stability) protein and ribonuclease E are encoded by the same structural gene of Escherichia coli. Proc Natl Acad Sci USA 88, 1-5
22. 22 Régnier P, Grunberg-Manago M (1990) RNase III cleavages in non-coding leaders of Escherichia coli transcripts control mRNA stability and genetic expression. Biochimie 72, 825-834
23. 23 Alifano P, Rivellini F, Piscitelli C, Arraiano CM, Bruni CB, Carlomagno MS (1994) Ribonuclease E provides substrates for ribonuclease P-dependent processing of a polycistronic mRNA. Genes Dev 8, 3021-3031
24. 24 Py B, Higgins CF, Krisch HM, Carpousis AJ (1996) A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature 381, 169-172
25. 25 Miczak A, Kaberdin VR, Wei C-W, Lin-Chao S (1996) Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc Natl Acad Sci USA 93, 3865-3869
26. 26 Carpousis AG, Van Houwe G, Ehretsmann C, Krisch HM (1994) Co-purification of E coli RNase E and PNPase: Evidence for a specific association between two enzymes important in RNA processing and degradation. Cell 76, 889-900
27. 27 Bouvet P, Belasco JG (1992) Control of RNase E-mediated RNA degradation by 5′ terminal base pairing in E coli. Nature 360, 488-491
28. 28 Emory SA, Bouvet P, Belasco JG (1992) A 5′-terminal stem-loop structure can stabilize mRNA in Escherichia coli. Genes Dev 6, 135-148
29. 29 Belasco JG, Higgins CF (1988) Mechanism of mRNA decay in bacteria: a perspective. Gene 11, 15-23
30. 30 Higgins CF, Causton HC, Dance GSC, Mudd EA (1993) The role of 3′ end in mRNA stability and decay. In: Control of messenger RNA stability (Belasco JG, Brawerman G, eds) Academic Press. New York, 13-30
31. 31 McLaren RS, Newbury SF, Dance GSC, Causton HC, Higgins CF (1991) mRNA degradation by processive 3′-5′ exonucleases in vitro and the implication for prokaryotic mRNA decay in vivo. J Mol Biol 221, 81-95
32. 32 Causton H, Py B, McLaren RS, Higgins CF (1994) mRNA degradation in Escherichia coli: a novel factor which impedes the exoribonucleolytic activity of PNPase at stem-loop structures. Mol Microbiol 14, 731-741
33. 33 Régnier P, Grunberg-Manago M, Portier C (1987) Nucleotide sequence of the pnp gene of E coli encoding polynucleotide phosphorylase; homology of the primary structure of the protein with the RNA binding domain of ribosomal protein S1. J Biol Chem 262, 63-68
34. 34 Sands JF, Régnier P, Cummings HS, Grunberg-Manago M, Hershey JWB (1988) The existence of two genes between infB and rpsO in the E coli genome: DNA sequencing and S1 nuclease mapping. Nucleic Acids Res 22, 10803-10816
35. 35 Robert-Le Meur M, Portier C (1992) E coli polynucleotide phosphorylase expression is autoregulated through an RNase III-dependent mechanism. EMBO J 11, 2633-2641
36. 36 Portier C, Dondon L, Grunberg-Manago M, Régnier P (1987) The first step in the functional inactivation of the E coli polynucleotide phosphorylase messenger is a ribonuclease III processing at the 5′ end. EMBOJ 6, 2165-2170
37. 37 Braun F, Hajnsdorf E, Regnier P (1996) Polynucleotide phosphorylase is required for the rapid degradation of the RNase E processed rpsO mRNA of Escherichia coli devoid of its 3′ hairpin. Mol Microbiol 19, 997-1005
38. 38 Hajnsdorf E, Braun F, Haugel-Nielsen J, Régnier P (1995) Polyadenylylation destabilizes the rpsO mRNA of Escherichia coli. Proc Natl Acad Sci USA 92, 3973-3977
39. 39 Melefors O, Lundberg U, von Gabain A (1993) RNA processing and degradation by RNase K, RNase E. In: Control of mRNA stability (Belasco JG, Brawerman G, eds) Academic Press, New York, 53-70
40. 40 Guarneros G, Portier C (1990) Different specificities of ribonuclease II and polynucleotide phosphorylase in 3′ mRNA decay. Biochimie 72, 771-777
41. 41 Thang MN, Guschlbauer W, Zachau HG, Grunberg-Manago M (1967) Degradation of transfer nucleic acid by polynucleotide phosphorylase. J Mol Biol 26, 403-421
42. 42 Gupta RS, Kasai T, Schlessinger D (1977) Purification and some novel properties of Escherichia coli RNase II. J Biol Chem 252, 8945-8949
43. 43 Petersen C (1993) Translation and mRNA stability in bacteria: A complex relationship. In: In Control of messenger RNA Stability (Belasco J, Brawerman G, eds) Academic Press, New York, 117-147
44. 44 Iost I, Dreyfus M (1994) mRNAs can be stabilized by DEAD-box proteins. Nature 372, 193-196
45. 45 Iost I, Dreyfus M (1995) The stability of Escherichia coli lacZ mRNA depends upon the simultaneity of its synthesis and translation. EMBO J 14, 3252-3261
46. 46 He L, Söderbom F, Wagner EGH, Binnie U, Binns N, Masters M (1993) PcnB is required for the rapid degradation of RNAI, the antisense RNA that controls the copy number of ColE1-related plasmids. Mol Microbiol 9, 1131-1142
47. 47 Xu F, Lin-Chao S, Cohen SN (1993) The Escherichia coli pcnB gene promotes adenylation of antisense RNAI of ColE1-type plasmids in vivo and degradation of RNAI decay intermediate. Proc Natl Acad Sci USA 90, 6756-6760
48. 48 O'Hara EB, Chekanova JA, Ingle CA, Kushner ZR, Peters E, Kushner SR (1995) Polyadenylylation helps regulate mRNA decay in Escherichia coli. Proc Natl Acad Sci USA 92, 1807-1811
49. 49 Cao GJ, Sarkar N (1992a) Poly(A) RNA in Escherichia coli: Nucleotide sequence at the junction of the lpp transcript and the polyadenylate moiety. Proc Natl Acad Sci USA 89, 7546-7550
50. 50 Cao G-J, Sarkar N (1993) Poly(A) RNA in Bacillus subtilis. Identification of the polyadenylation site of flagellin mRNA. FEMS Microbiol Lett 108, 281-286
51. 51 Karnik P, Taljanidisz J, Sasvari-Szekely M, Sarkar N (1987) 3′-terminal polyadenylate sequence of Escherichia coli tryptophan synthetase α-subunit messenger RNA. J Mol Biol 196, 347-354
52. 52 Sarkar N, Langley D, Paulus H (1978) Isolation and characterization of polyadenylate-containing RNA from Bacillus brevis. Biochemistry 17, 3468-3474
53. 53 Haugel-Nielsen J, Hajnsdorf E, Régnier P (1996) The rpsO mRNA of Escherichia coli is polyadenylated at multiple sites resulting from endonucleolytic processing and exonucleolytic degradation. EMBO J 15, 3144-3152
54. 54 Kalapos MP, Cao G-J, Kushner SR, Sarkar N (1994) Identification of a second poly(A) polymerase in Escherichia coli. Biochem Biophys Res Commun 198, 459-465
55. 55 Keller W (1995) No end yet to messenger RNA 3′ processing. Cell 81, 829-832.
56. 56 Xu F, Cohen S (1995) RNA degradation in Escherichia coli regulated by 3′ adenylation and 5′ phosphorylation. Nature 374, 180-183
57. 57 Cohen SN (1995) Surprises at the 3′ end of prokaryotic RNA. Cell 80, 829-832
58. 58 Pepe CM, Maslesa-Galic S, Simons RW (1994) Decay of the IS10 antisense RNA by 3′ exonucleases: evidence that RNase II stabilizes RNA-OUT against PNPase attack. Mot Microbiol 13, 1133-1142
59. 59 Coburn GA, Mackie GA (1996) Differential sensitivities of portions of the mRNA for ribosomal protein S20 to 3′-exonucleases dependent on oligoadenylation and RNA secondary structure. J Biol Chem 271, 15776-15781
60. 60 Coburn GA, Mackie GA (1996) Overexpression, purification and properties of Escherichia coli ribonuclease II. J Biol Chem 271, 1048-1053
61. 61 Deutscher M (1990) Ribonucleases, tRNA nucleotidyltransferase and the 3′ processing of tRNA. Prog Nucleic Acid Res Mol Biol 39, 209-240
62. 62 Deutscher MP (1993) Promiscuous exoribonucleases of Escherichia coli. J Bacteriol 175, 4577-4583
63. 63 Bilge SS, Apostol J JM, Aldape MA, Moseley SL (1993) mRNA processing independent of RNase III and RNase E in the expression of the F1845 fimbrial adhesin of Escherichia coli. Proc Natl Acad Sci USA 90, 1455-1459
64. 64 Emory SA, Belasco JG (1990) The ompA 5′ untranslated RNA segment functions in E coli as a growth-rate-regulated mRNA stabilizer whose activity is unrelated to transcriptional efficiency. J Bacteriol 172, 4472-4481
65. 65 Hajnsdorf E, Carpousis AJ, Régnier P (1994) Nucleolytic inactivation and degradation of the RNase III processed pnp message encoding polynucleotide phosphorylase of Escherichia coli. J Mol Biol 239, 439-454
66. 66 Philippe C, Eyermann F, Benard L, Portier C, Ehresmann B, Ehresmann C (1993) Ribosomal protein S15 from Escherichia coli modulates its own translation by trapping the ribosome on the mRNA initiation loading site. Proc Natl Acad Sci USA 90, 4394-4398
67. 67 Zhang A, Derbyshire V, Galloway-Salvo JL, Belfort M (1995) Escherichia coli protein StpA stimulates self-spicing by promoting RNA assembly in vitro. RNA 1, 783-793
68. 68 Jones P, Mitta M, Kim Y, Jiang W, Inouye M (1996) Cold shock induces a major ribosomal-associated protein that unwinds double-stranded RNA in Escherichia coli. Proc Natl Acad Sci USA 93, 76-80
69. 69 Coetzee T, Herschlag D (1994) Escherichia coli proteins, including ribosomal protein S12, facilitate in vitro splicing of phage T4 introns by acting as RNA chaperones. Genes Dev 8, 1575-1588
70. 70 Georgellis D, Sohlberg B, Hartl U, von Gabain A (1995) Identification of GroEL as a constituent of an mRNA-protection complex in Escherichia coli. Mol Microbiol 16, 1259-1268
71. 71 Keller KC, Waller PRH, Sauer RT (1996) Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271, 990-993
72. 72 Jackson RJ, Standart N (1990) Do the poly(A) tail and 3′ untranslated region control mRNA stability? Cell 62, 15-24
73. 73 Danchin A (1996) mRNA turn over and DNA synthesis: a lesson from bacterial genome comparisons. Mol Microbiol 4, 893-895