Abstract
Escherichia coli chaperones DnaJ, DnaK and GrpE increase P1 plasmid initiator binding to the origin by promoting initiator folding. The binding allows initiation and also promotes pairing of origins which is believed to control initiation frequency. Chaperone-independent DNA binding mutants are often defective in replication control. We show here that these mutants have increased rates of association for DNA binding and defects in origin pairing. The increases in association rates were found to be due either to increased protein folding into active forms or to increases in the association rate constant, kon. Since the dissociation rate constants for DNA release with these mutants are not changed, it is unlikely that the DNA binding domain is affected. The pairing domain may thus control replication and modulate DNA binding. The role of the pairing domain in DNA binding can be significant in vivo as the selection for chaperone-independent binding favors pairing-defective mutants.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Abeles A. L. P1 plasmid replication. Purification and DNA-binding activity of the replication protein RepA. J Biol Chem. 1986 Mar 15;261(8):3548–3555. [PubMed] [Google Scholar]
- Abeles A. L., Reaves L. D., Austin S. J. A single DnaA box is sufficient for initiation from the P1 plasmid origin. J Bacteriol. 1990 Aug;172(8):4386–4391. doi: 10.1128/jb.172.8.4386-4391.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Abeles A. L., Snyder K. M., Chattoraj D. K. P1 plasmid replication: replicon structure. J Mol Biol. 1984 Mar 5;173(3):307–324. doi: 10.1016/0022-2836(84)90123-2. [DOI] [PubMed] [Google Scholar]
- Alfano C., McMacken R. Heat shock protein-mediated disassembly of nucleoprotein structures is required for the initiation of bacteriophage lambda DNA replication. J Biol Chem. 1989 Jun 25;264(18):10709–10718. [PubMed] [Google Scholar]
- Amster-Choder O., Wright A. Modulation of the dimerization of a transcriptional antiterminator protein by phosphorylation. Science. 1992 Sep 4;257(5075):1395–1398. doi: 10.1126/science.1382312. [DOI] [PubMed] [Google Scholar]
- Beckmann R. P., Mizzen L. E., Welch W. J. Interaction of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly. Science. 1990 May 18;248(4957):850–854. doi: 10.1126/science.2188360. [DOI] [PubMed] [Google Scholar]
- Chattoraj D. K., Mason R. J., Wickner S. H. Mini-P1 plasmid replication: the autoregulation-sequestration paradox. Cell. 1988 Feb 26;52(4):551–557. doi: 10.1016/0092-8674(88)90468-0. [DOI] [PubMed] [Google Scholar]
- Chattoraj D. K., Snyder K. M., Abeles A. L. P1 plasmid replication: multiple functions of RepA protein at the origin. Proc Natl Acad Sci U S A. 1985 May;82(9):2588–2592. doi: 10.1073/pnas.82.9.2588. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chattoraj D., Cordes K., Abeles A. Plasmid P1 replication: negative control by repeated DNA sequences. Proc Natl Acad Sci U S A. 1984 Oct;81(20):6456–6460. doi: 10.1073/pnas.81.20.6456. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DasGupta S., Mukhopadhyay G., Papp P. P., Lewis M. S., Chattoraj D. K. Activation of DNA binding by the monomeric form of the P1 replication initiator RepA by heat shock proteins DnaJ and DnaK. J Mol Biol. 1993 Jul 5;232(1):23–34. doi: 10.1006/jmbi.1993.1367. [DOI] [PubMed] [Google Scholar]
- Fried M. G., Crothers D. M. Kinetics and mechanism in the reaction of gene regulatory proteins with DNA. J Mol Biol. 1984 Jan 25;172(3):263–282. doi: 10.1016/s0022-2836(84)80026-1. [DOI] [PubMed] [Google Scholar]
- Hwang D. S., Crooke E., Kornberg A. Aggregated dnaA protein is dissociated and activated for DNA replication by phospholipase or dnaK protein. J Biol Chem. 1990 Nov 5;265(31):19244–19248. [PubMed] [Google Scholar]
- Kawasaki Y., Wada C., Yura T. Binding of RepE initiator protein to mini-F DNA origin (ori2). Enhancing effects of repE mutations and DnaJ heat shock protein. J Biol Chem. 1992 Jun 5;267(16):11520–11524. [PubMed] [Google Scholar]
- Kawasaki Y., Wada C., Yura T. Mini-F plasmid mutants able to replicate in the absence of sigma 32: mutations in the repE coding region producing hyperactive initiator protein. J Bacteriol. 1991 Feb;173(3):1064–1072. doi: 10.1128/jb.173.3.1064-1072.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kawasaki Y., Wada C., Yura T. Roles of Escherichia coli heat shock proteins DnaK, DnaJ and GrpE in mini-F plasmid replication. Mol Gen Genet. 1990 Jan;220(2):277–282. doi: 10.1007/BF00260494. [DOI] [PubMed] [Google Scholar]
- Kim B., Little J. W. Dimerization of a specific DNA-binding protein on the DNA. Science. 1992 Jan 10;255(5041):203–206. doi: 10.1126/science.1553548. [DOI] [PubMed] [Google Scholar]
- Landry S. J., Gierasch L. M. Recognition of nascent polypeptides for targeting and folding. Trends Biochem Sci. 1991 Apr;16(4):159–163. doi: 10.1016/0968-0004(91)90060-9. [DOI] [PubMed] [Google Scholar]
- Lobell R. B., Schleif R. F. DNA looping and unlooping by AraC protein. Science. 1990 Oct 26;250(4980):528–532. doi: 10.1126/science.2237403. [DOI] [PubMed] [Google Scholar]
- Luisi B. F., Xu W. X., Otwinowski Z., Freedman L. P., Yamamoto K. R., Sigler P. B. Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA. Nature. 1991 Aug 8;352(6335):497–505. doi: 10.1038/352497a0. [DOI] [PubMed] [Google Scholar]
- McEachern M. J., Bott M. A., Tooker P. A., Helinski D. R. Negative control of plasmid R6K replication: possible role of intermolecular coupling of replication origins. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7942–7946. doi: 10.1073/pnas.86.20.7942. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mendel D. B., Khavari P. A., Conley P. B., Graves M. K., Hansen L. P., Admon A., Crabtree G. R. Characterization of a cofactor that regulates dimerization of a mammalian homeodomain protein. Science. 1991 Dec 20;254(5039):1762–1767. doi: 10.1126/science.1763325. [DOI] [PubMed] [Google Scholar]
- Miron A., Mukherjee S., Bastia D. Activation of distant replication origins in vivo by DNA looping as revealed by a novel mutant form of an initiator protein defective in cooperativity at a distance. EMBO J. 1992 Mar;11(3):1205–1216. doi: 10.1002/j.1460-2075.1992.tb05161.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pal S. K., Chattoraj D. K. P1 plasmid replication: initiator sequestration is inadequate to explain control by initiator-binding sites. J Bacteriol. 1988 Aug;170(8):3554–3560. doi: 10.1128/jb.170.8.3554-3560.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pal S. K., Mason R. J., Chattoraj D. K. P1 plasmid replication. Role of initiator titration in copy number control. J Mol Biol. 1986 Nov 20;192(2):275–285. doi: 10.1016/0022-2836(86)90364-5. [DOI] [PubMed] [Google Scholar]
- Papp P. P., Chattoraj D. K., Schneider T. D. Information analysis of sequences that bind the replication initiator RepA. J Mol Biol. 1993 Sep 20;233(2):219–230. doi: 10.1006/jmbi.1993.1501. [DOI] [PubMed] [Google Scholar]
- Riggs A. D., Bourgeois S., Cohn M. The lac repressor-operator interaction. 3. Kinetic studies. J Mol Biol. 1970 Nov 14;53(3):401–417. doi: 10.1016/0022-2836(70)90074-4. [DOI] [PubMed] [Google Scholar]
- Ruusala T., Crothers D. M. Sliding and intermolecular transfer of the lac repressor: kinetic perturbation of a reaction intermediate by a distant DNA sequence. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):4903–4907. doi: 10.1073/pnas.89.11.4903. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sozhamannan S., Chattoraj D. K. Heat shock proteins DnaJ, DnaK, and GrpE stimulate P1 plasmid replication by promoting initiator binding to the origin. J Bacteriol. 1993 Jun;175(11):3546–3555. doi: 10.1128/jb.175.11.3546-3555.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Swack J. A., Pal S. K., Mason R. J., Abeles A. L., Chattoraj D. K. P1 plasmid replication: measurement of initiator protein concentration in vivo. J Bacteriol. 1987 Aug;169(8):3737–3742. doi: 10.1128/jb.169.8.3737-3742.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tilly K., Sozhamannan S., Yarmolinsky M. Participation of the Escherichia coli heat shock proteins DnaJ, DnaK, and GrpE in autorepression of the P1 plasmid repA promoter. New Biol. 1990 Sep;2(9):812–817. [PubMed] [Google Scholar]
- Tilly K., Yarmolinsky M. Participation of Escherichia coli heat shock proteins DnaJ, DnaK, and GrpE in P1 plasmid replication. J Bacteriol. 1989 Nov;171(11):6025–6029. doi: 10.1128/jb.171.11.6025-6029.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wagner S., Green M. R. HTLV-I Tax protein stimulation of DNA binding of bZIP proteins by enhancing dimerization. Science. 1993 Oct 15;262(5132):395–399. doi: 10.1126/science.8211160. [DOI] [PubMed] [Google Scholar]
- Wickner S. H. Three Escherichia coli heat shock proteins are required for P1 plasmid DNA replication: formation of an active complex between E. coli DnaJ protein and the P1 initiator protein. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2690–2694. doi: 10.1073/pnas.87.7.2690. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wickner S., Hoskins J., McKenney K. Function of DnaJ and DnaK as chaperones in origin-specific DNA binding by RepA. Nature. 1991 Mar 14;350(6314):165–167. doi: 10.1038/350165a0. [DOI] [PubMed] [Google Scholar]
- Wickner S., Hoskins J., McKenney K. Monomerization of RepA dimers by heat shock proteins activates binding to DNA replication origin. Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):7903–7907. doi: 10.1073/pnas.88.18.7903. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wickner S., Skowyra D., Hoskins J., McKenney K. DnaJ, DnaK, and GrpE heat shock proteins are required in oriP1 DNA replication solely at the RepA monomerization step. Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10345–10349. doi: 10.1073/pnas.89.21.10345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zylicz M., Ang D., Liberek K., Georgopoulos C. Initiation of lambda DNA replication with purified host- and bacteriophage-encoded proteins: the role of the dnaK, dnaJ and grpE heat shock proteins. EMBO J. 1989 May;8(5):1601–1608. doi: 10.1002/j.1460-2075.1989.tb03544.x. [DOI] [PMC free article] [PubMed] [Google Scholar]