Starvation-induced Mucts62-mediated coding sequence fusion: A role for ClpXP, Lon, RpoS and Crp

Molecular Microbiology

Volumn 32, Issue 2, 1999, Pages 327-343

  Lamranl, Sabah ^a   Ranquet, Caroline ^b   Gama, Marie José ^a   Nakai, Hiroshi ^d   Shapiro, James A ^c   Toussaint, Ariane ^a,b   Maenhaut Michel, Geneviève ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b UNIV GRENOBLE ALPES   (France)

^c UNIVERSITY OF CHICAGO   (United States)

^d GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; PROTEINASE;

AEROBIC METABOLISM; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIOPHAGE MU; CHROMOSOME REARRANGEMENT; CODON; CONTROLLED STUDY; DNA TRANSPOSITION; ESCHERICHIA COLI; GENE FUSION; GENE INDUCTION; GENE MAPPING; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROPHAGE; REPORTER GENE; STARVATION;

EID: 0032948556     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01352.x     Document Type: Article

References (79)

1. Adzuma, K., and Mizuuchi, K. (1989) Interaction of proteins located at a distance along DNA: mechanism of target immunity in the Mu DNA strand-transfer reaction. Cell 57: 41-47.
2. Adzuma, K., and Mizuuchi, K. (1991) Steady-state kinetic analysis of ATP hydrolysis by the B protein of bacteriophage Mu. Involvement of protein oligomerization in the ATPase cycle. J Biol Chem 266: 6159-6167.
3. Alazard, R., Betermier, M., and Chandler, M. (1992) Escherichia coli integration host factor stabilizes bacteriophage Mu repressor interactions with operator DNA in vitro. Mol Microbiol 6: 1707-1714.
4. Arber, W., Enquist, L., Hohn, B., Murray, N., and Murray, K. (1983) Experimental methods for use with lambda. In Lambdall. Hendrix, R.W., Roberts, J.W., Stahl, F.W., and Weisberg, R.A. (eds). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp. 433-466.
5. Atlung, T., and Ingmer, H. (1997) H-NS: a modulator of environmentally regulated gene expression. Mol Microbiol 24: 7-17.
6. Bétermier, M., Poquet, I., Alazard, R., and Chandler, M. (1993) Involvement of Escherichia coli FIS protein in maintenance of bacteriophage Mu lysogeny by the repressor: control of early transcription and inhibition of transposition. J Bacteriol 175: 3798-3811.
7. Bétermier, M., Rousseau, P., Alazard, R., and Chandler, M. (1995) Mutual stabilisation of bacteriophage Mu repressor and histone-like proteins in a nucleoprotein structure. J Mol Biol 249: 332-341.
8. Bourret, R.B., and Fox, M.S. (1988B) Lysogenization of Escherichia coli Him+, himA, and himD hosts by bacteriophage Mu. J Bacteriol 170: 1672-1682.
9. Bukhari, A.I., and Ljungquist, E. (1977) Bacteriophage Mu: methods for cultivation and use. In DNA Insertion Elements, Plasmids and Episomes. Bukhari, A.I., Shapiro J.A., and Adhya, S.L. (eds). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp. 749-756.
10. Casadaban, M. (1976) Transposition and fusion of the lac gene to selected promoters in E. coli using bacteriophage lambda and Mu. J Mol Biol 104: 541-555.
11. Ditto, M.D.M., Roberts, D., and Weisberg, R.A. (1994) Growth phase variation of integration host factor level in Escherichia coli. J Bacteriol 176: 3738-3748.
12. van Drunen, C.M., van Zuylen, C., Mientjes, E.J., Goosen, N., and van de Putte, P. (1993) Inhibition of bacteriophage Mu transposition by Mu repressor and Fis. Mol Microbiol 10: 293-298.
13. Englesberg, E., Irr, J., Power, J., and Lee, N. (1965) Positive control of enzyme synthesis by gene C in the L-arabinose system. J Bacteriol 90: 946-957.
14. Faelen, M., Huisman, O., and Toussaint, A. (1978) Involvement of phage Mu-1 early functions in Mu-mediated chromosomal rearrangements. Nature 271: 580-582.
15. Faelen, M., Résibois, A., and Toussaint, A. (1979) Mini-Mu. An insertion element derived from temperate phage Mu-1. Cold Spring Harbor Symp Quant Biol 43: 1169-1177.
16. Falconi, M., Odle, J., Hillyard, D., Gualerzi, C., and Higgins, N.P. (1991) Mutations altering chromosomal protein H-NS activate phage Mu transposition. New Biologist 3: 615-625.
17. Finkel, S.E., and Johnson, R.C. (1992) The Fis protein: it's not just for DNA inversion anymore. Mol Microbiol 6: 3257-3260.
18. Foster, P.L. (1993) Adaptive mutation: the uses of adversity. Annu Rev Microbiol 47: 467-504.
19. Frank, E.G., Ennis, D.G., Gonzales, M., Levine, A.S., and Woodgate, R. (1996) Regulation of SOS mutagenesis by proteolysis. Proc Natl Acad Sci USA 93: 10291-10296.
20. Gama, M.J., Toussaint, A., and Higgins, N.P. (1992) Stabilization of bacteriophage Mu repressor-operator complexes by the Escherichia coli integration host factor protein. Mol Microbiol 6: 1715-1722.
21. Geuskens, V., Vogel, J.L., Grimaud, R., Desmet, L., Higgins, N.P., and Toussaint, A. (1991) Frameshift mutations in bacteriophage Mu repressor can confer a trans-dominant virulent phenotype to the phage. J Bacteriol 173: 6578- 6585.
22. Geuskens, V., Mhammedi-Alaoui, A., Desmet, L., and Toussaint, A. (1992) Virulence in bacteriophage Mu: a case of trans-dominant proteolysis by the E. coli Clp serine- protease. EMBO J 11: 5121-5127.
23. Glansdorff, N. (1965) Topography of cotransducible arginine mutations in E. coli K12. Genetics 51: 167-179.
24. Gómez-Gómez, J.M., Blásquez, J., Baquero, F., and Martínez, J.L. (1997) H-NS and RpoS regulate emergence of Lac Ara+ mutants of Escherichia coli MCS2. J Bacteriol 179: 4620-4622.
25. Goosen, N., and van de Putte, P. (1987) Regulation of transcription. In Phage Mu. Symonds, N., Toussaint, A., van de Putte, P., and Howe, M.M. (eds). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp. 41-52.
26. Gottesman, S. (1996) Proteases and their targets in Escherichia coil. Annu Rev Genet 30: 465-506.
27. Gottesman, S., and Zipser, D. (1978) Deg phenotype of Escherichia coli lon mutants. J Bacteriol 133: 844-851.
28. Gottesman, S., Clark, W.P., de Crecy-Lagard, V., and Maurizi, M.R. (1993) ClpX, an alternative subunit for the ATP- dependent Clp protease of Escherichia coli. J Biol Chem 268: 22618-22626.
29. Heffernan, L., Bass, R., and Englesberg, E. (1976) Mutations affecting catabolite repression of the L-arabinose regulon in Escherichia coli B/r. J Bacteriol 126: 1119-1131.
30. Hengge-Aronis, R. (1996) Regulation of gene expression during entry into stationary phase. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. Neidhardt, F.C., et al. (eds). Washington, DC: American Society for Microbiology Press, pp. 1497-1512.
31. Howe, M.M. (1973) Prophage deletion mapping of bacteriophage Mu-1. Virology 54: 93-101.
32. Huisman, G.W., and Kolter, R. (1994) Sensing starvation: a homoserine lactone-dependent signaling pathway in Escherichia coli. Science 265: 537-539.
33. Kaiser, A.D. (1955) A genetic study of the temperate coliphage. Virology 1: 424-443.
34. Krause, H.M., and Higgins, N.P. (1986) Positive and negative regulation of the Mu operator by Mu represser and E. coli integration host factor. J Biol Chem 261: 3744- 3752.
35. Kruklitis, R., Welty, D.J., and Nakai, H. (1996) ClpX protein of Escherichia coli activates bacteriophage Mu transposase in the strand transfer complex for initiation of Mu DNA synthesis. EMBO J 15: 935-944.
36. Laachouch, J., Desmet, L., Geuskens, V., Grimaud, R., and Toussaint, A. (1996) Bacteriophage Mu repressor as a target for the Escherichia coli ATP-dependent Clp protease. EMBO J 15: 437-444.
37. Leach, D., and Symonds, N. (1979) The isolation and characterization of a plaque-forming derivative of bacteriophage Mu carrying a fragment of Tn3 conferring ampicillin resistance. Mol Gen Genet 172: 179-184.
38. Leathers, T.D., Noti, J., and Umbarger, H.E. (1979) Physical characterization of ilv-lac fusions. J Bacteriol 140: 251-260.
39. van Leerdam, E., Karreman, C., and van de Putte, P. (1982) Ner, a Cro-like function of bacteriophage Mu. Virology 123: 19-28.
40. Lennox, E.S. (1955) Transduction of linked genetic characters of the host bacteriophage P1. Virology 1: 190-206.
41. Levchenko, I., Luo, L., and Baker, T. (1995) Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev 9: 2399-2409.
42. Levchenko, I., Yamauchi, M., and Baker, T. (1997) ClpX and MuB interact with overlapping regions of Mu transposase: implications for control of the transposition pathway. Genes Dev 11: 1561-1572.
43. Maenhaut-Michel, G., and Shapiro, J.A. (1994) The roles of starvation and selective substrates in the emergence of araB-lacZ fusion clones. EMBO J 13: 5229-5239.
44. Maenhaut-Michel, G., Blake, C.E., Leach, D.R., and Shapiro, J.A. (1997) Different structures of selected and unselected araB-lacZ fusions. Mol Microbiol 23: 1133-1145.
45. Manna, D., and Higgins, N.P. (1999) Phage Mu transposition immunity reflects supercoil domain structure of the chromosome. Mol Microbiol (in press).
46. Maxwell, A., Craigie, R., and Mizuuchi, K. (1987) B protein of bacteriophage Mu is an ATPase that preferentially stimulates intermolecular DNA strand transfer. Proc Natl Acad Sci USA 84: 699-703.
47. Mhammedi-Alaoui, A., Pato, M., Gama, M.J., and Toussaint, A. (1994) A new component of bacteriophage Mu replicative transposition machinery: the E.coli ClpX protein. Mol Microbiol 11: 1109-1116.
48. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
49. Mittler, J., and Lenski, R.E. (1990) Further experiments on excisions of Mu from Escherichia coli MCS2 cast doubt on directed mutation hypothesis. Nature 344: 173-175.
50. Naigamwalla, D.Z., and Chaconas, G. (1997) A new set of transposition intermediates: alternate pathways of target capture preceding strand transfer. EMBO J 16: 5227-5234.
51. O'Day, K., Schultz, D., Ericsen, W., Reawluk, L., and Howe, M. (1979) Correction and refinement of the genetic map of bacteriophage Mu. Virology 93: 320-328.
52. Pato, M.L., Karlok, M., Wall, C., and Higgins, N.P. (1995) Characterization of Mu prophage lacking the central strong gyrase binding site: localization of the block in replication. J Bacteriol 177: 5937-5942.
53. Priess, H., Bräuer, B., Schmidt, C., and Kamp, D. (1987) Sequence of the left end of Mu. In Phage Mu. Symonds, N., Toussaint, A. van de Putte, P., and Howe, M. (eds). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp. 277-296.
54. Résibois, A., Toussaint, A., van Gijsegem, F., and Faelen, M. (1981) Physical characterization of mini-Mu and mini-D108. Gene 14: 103-113.
55. van Rijn, P.A., Goosen, N., and van de Putte, P. (1988) Integration host factor of Escherichia coli regulates early and repressor transcription of bacteriophage Mu by two different mechanisms. Nucleic Acids Res 16: 4595-45605.
56. van Rijn, P.A., Goosen, N., Turk, S.C.H., and van de Putte, P. (1989) Regulation of Mu repressor transcription by IHF depends on the level of the early transcription. Nucleic Acids Res 17: 10203-10211.
57. Ross, W., Shore, S.H., and Howe, M. (1986) Mutants of Escherichia coli defective for replicative transposition of bacteriophage Mu. J Bacteriol 167: 905-919.
58. Saier, Jr, M.H., Ramseier, T.M., Reizer, J. (1996) Regulation of carbon utilization. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. Neidhardt, F.C., et al. (eds). Washington, DC: American Society for Microbiology Press, pp. 1325-1343.
59. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning, a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp. 1847-1873.
60. Schweder, T., Lee, K.H., Lomovskaya, O., and Matin, A. (1996) Regulation of Escherichia coli starvation sigma factor (sigma s) by ClpXP protease. J Bacteriol 178: 470-476.
61. Shapiro, J.A. (1984a) Observations on the formation of clones containing araB - lacZ cistron fusions. Mol Gen Genet 194: 79-90.
62. Shapiro, J.A. (1984b) The use of Mudlac transposons as tools for vital staining to visualize clonal and non-clonal patterns of organization in bacterial growth an agar and non-agar surface. J Gen Microbiol 130: 1169-1181.
63. Shapiro, J.A. (1993) A role for the Clp protease in activating Mu-mediated DNA rearrangements. J Bacteriol 175: 2625- 2631.
64. Shapiro, J.A., and Higgins, N.P. (1989) Differential activity of a transposable element in Escherichia coli colonies. J Bacteriol 171: 5975-5986.
65. Shapiro, J.A., and Leach, D. (1990) Action of a transposable element in coding sequence fusions. Genetics 126: 293- 299.
66. Simons, R.W., Houman, F., and Kleckner, N. (1987) Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53: 85-96.
67. Symonds, N., Toussaint, A., van de Putte, P., and Howe, M.M. (1987) Phage Mu. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
68. Toussaint, A., and Résibois, A. (1983) Phage Mu: Transposition as a life-style. In Mobile Genetic Elements. Shapiro, J.A. (ed.). New York: Academic Press, pp. 105-158.
69. Toussaint, A., Desmet, L., Faelen, M., Alazard, R., Chandler, M., and Pato, M. (1987) In vivo mutagenesis of bacteriophage Mu transposase. J Bacteriol 169: 5700-5707.
70. van Ulsen, P., Hillebrand, M., Zulianello, L., van de Putte, P., and Goosen, N. (1996) Integration host factor alleviates the H-NS-mediated repression of the early promoter of bacteriophage Mu. Mol Microbiol 21: 567-578.
71. van de Putte, P., Westmaas, G.C., and Wijffelman, C. (1977) On the kil gene of bacteriophage Mu. In DNA Insertion Elements, Plasmids and Episomes. Bukhari, A.I., Shapiro, J.A., and Adhya, S.L. (eds). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp. 287-294.
72. Van Melderen, L., Bernard, P., and Couturier, M. (1994) Lon- dependent proteolysis of CcdA is the key control for activation of CcdB in plasmid-free segregant bacteria. Mol Microbiol 11: 1151-1157.
73. van Vliet, F., Couturier, M., Desmet, L., Faelen, M., and Toussaint, A. (1978) Virulent mutants of temperate phage Mu-1. Mol Gen Genet 160: 195-202.
74. Vogel, J.L., Zhu Juan, L., Howe, M.M., Toussaint, A., and Higgins, N.P. (1991) Temperature sensitive mutations in bacteriophage Mu c repressor define a DNA binding site. J Bacteriol 173: 6568-6577.
75. Vogel, J.L., Geuskens, V., Desmet, L., Higgins, N.P., and Toussaint, A. (1996) C-terminal deletions can suppress temperature-sensitive mutations and change dominance in the phage Mu repressor. Genetics 142: 661-672.
76. Waggoner, B.T., Marrs, C.F., Howe, M.M., and Pato, M.L. (1984) Multiple factors and processes involved in host cell killing by bacteriophage Mu: characterization and mapping. Virology 136: 168-185.
77. Welty, D.J., Jones, J.M., and Nakai, H. (1997) Communication of ClpXP protease hypersensitivity to bacteriophage Mu repressor isoforms. J Mol Biol 272: 31-41.
78. Wojtkowiak, D., Georgopoulos, C., and Zylicz, M. (1993) Isolation and characterization of ClpX, a new ATP-dependent specificity component of the Clp protease of Escherichia coli. J Biol Chem 268: 22609-22617.
79. Zipser, D., Moses, P., Kahmann, R., and Kamp, D. (1977) The molecular cloning of the immunity gene of phage Mu. Gene 2: 263-271.