Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Apr 25;92(9):3958–3962. doi: 10.1073/pnas.92.9.3958

Increased sensitivity to gamma irradiation in bacteria lacking protein HU.

F Boubrik 1, J Rouviere-Yaniv 1
PMCID: PMC42081  PMID: 7732012

Abstract

The heterodimeric HU protein, isolated from Escherichia coli, is associated with the bacterial nucleoid and shares some properties with both histones and HMG proteins. It is the prototype of small bacterial DNA binding proteins with a pleiotropic role in the cell. HU participates in several biological processes like cell division, initiation of DNA replication, transposition, and other biochemical functions. We show here that bacteria lacking HU are extremely sensitive to gamma irradiation. Expression of either one of the subunits of HU in the hupAB double mutant nearly restores the normal survival rate. This shows that the sensitivity is due to the absence of HU rather than being the result of a secondary mutation occurring in the hupAB cells or a modification of the SOS repair system, since SOS genes are induced normally in the absence of HU. Finally, in vitro studies give an indication of its potential role: HU protects DNA against cleavage by gamma-rays.

Full text

PDF
3961

Images in this article

3961Fig. 5
on p.3961

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bonnefoy E., Almeida A., Rouviere-Yaniv J. Lon-dependent regulation of the DNA binding protein HU in Escherichia coli. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7691–7695. doi: 10.1073/pnas.86.20.7691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bonnefoy E., Rouvière-Yaniv J. HU, the major histone-like protein of E. coli, modulates the binding of IHF to oriC. EMBO J. 1992 Dec;11(12):4489–4496. doi: 10.1002/j.1460-2075.1992.tb05550.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bonnefoy E., Takahashi M., Yaniv J. R. DNA-binding parameters of the HU protein of Escherichia coli to cruciform DNA. J Mol Biol. 1994 Sep 16;242(2):116–129. doi: 10.1006/jmbi.1994.1563. [DOI] [PubMed] [Google Scholar]
  4. Caron F., Jacq C., Rouvière-Yaniv J. Characterization of a histone-like protein extracted from yeast mitochondria. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4265–4269. doi: 10.1073/pnas.76.9.4265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Drlica K., Rouviere-Yaniv J. Histonelike proteins of bacteria. Microbiol Rev. 1987 Sep;51(3):301–319. doi: 10.1128/mr.51.3.301-319.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Flashner Y., Gralla J. D. DNA dynamic flexibility and protein recognition: differential stimulation by bacterial histone-like protein HU. Cell. 1988 Aug 26;54(5):713–721. doi: 10.1016/s0092-8674(88)80016-3. [DOI] [PubMed] [Google Scholar]
  7. Huisman O., D'Ari R. Effect of suppressors of SOS-mediated filamentation on sfiA operon expression in Escherichia coli. J Bacteriol. 1983 Jan;153(1):169–175. doi: 10.1128/jb.153.1.169-175.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Huisman O., Faelen M., Girard D., Jaffé A., Toussaint A., Rouvière-Yaniv J. Multiple defects in Escherichia coli mutants lacking HU protein. J Bacteriol. 1989 Jul;171(7):3704–3712. doi: 10.1128/jb.171.7.3704-3712.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kano Y., Wada M., Nagase T., Imamoto F. Genetic characterization of the gene hupB encoding the HU-1 protein of Escherichia coli. Gene. 1986;45(1):37–44. doi: 10.1016/0378-1119(86)90129-0. [DOI] [PubMed] [Google Scholar]
  10. Krasin F., Hutchinson F. Repair of DNA double-strand breaks in Escherichia coli cells requires synthesis of proteins that can be induced by UV light. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3450–3453. doi: 10.1073/pnas.78.6.3450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Megraw T. L., Chae C. B. Functional complementarity between the HMG1-like yeast mitochondrial histone HM and the bacterial histone-like protein HU. J Biol Chem. 1993 Jun 15;268(17):12758–12763. [PubMed] [Google Scholar]
  12. Paull T. T., Haykinson M. J., Johnson R. C. The nonspecific DNA-binding and -bending proteins HMG1 and HMG2 promote the assembly of complex nucleoprotein structures. Genes Dev. 1993 Aug;7(8):1521–1534. doi: 10.1101/gad.7.8.1521. [DOI] [PubMed] [Google Scholar]
  13. Pontiggia A., Negri A., Beltrame M., Bianchi M. E. Protein HU binds specifically to kinked DNA. Mol Microbiol. 1993 Feb;7(3):343–350. doi: 10.1111/j.1365-2958.1993.tb01126.x. [DOI] [PubMed] [Google Scholar]
  14. Preobrajenskaya O., Boullard A., Boubrik F., Schnarr M., Rouvière-Yaniv J. The protein HU can displace the LexA repressor from its DNA-binding sites. Mol Microbiol. 1994 Aug;13(3):459–467. doi: 10.1111/j.1365-2958.1994.tb00440.x. [DOI] [PubMed] [Google Scholar]
  15. Rouvière-Yaniv J., Gros F. Characterization of a novel, low-molecular-weight DNA-binding protein from Escherichia coli. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3428–3432. doi: 10.1073/pnas.72.9.3428. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Rouvière-Yaniv J., Kjeldgaard N. O. Native Escherichia coli HU protein is a heterotypic dimer. FEBS Lett. 1979 Oct 15;106(2):297–300. doi: 10.1016/0014-5793(79)80518-9. [DOI] [PubMed] [Google Scholar]
  17. Rouvière-Yaniv J. Localization of the HU protein on the Escherichia coli nucleoid. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 1):439–447. doi: 10.1101/sqb.1978.042.01.047. [DOI] [PubMed] [Google Scholar]
  18. Rouvière-Yaniv J., Yaniv M., Germond J. E. E. coli DNA binding protein HU forms nucleosomelike structure with circular double-stranded DNA. Cell. 1979 Jun;17(2):265–274. doi: 10.1016/0092-8674(79)90152-1. [DOI] [PubMed] [Google Scholar]
  19. Segall A. M., Goodman S. D., Nash H. A. Architectural elements in nucleoprotein complexes: interchangeability of specific and non-specific DNA binding proteins. EMBO J. 1994 Oct 3;13(19):4536–4548. doi: 10.1002/j.1460-2075.1994.tb06775.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Setlow P. I will survive: protecting and repairing spore DNA. J Bacteriol. 1992 May;174(9):2737–2741. doi: 10.1128/jb.174.9.2737-2741.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Smith K. C., Wang T. C. recA-dependent DNA repair processes. Bioessays. 1989 Jan;10(1):12–16. doi: 10.1002/bies.950100104. [DOI] [PubMed] [Google Scholar]
  22. Téoule R. Radiation-induced DNA damage and its repair. Int J Radiat Biol Relat Stud Phys Chem Med. 1987 Apr;51(4):573–589. doi: 10.1080/09553008414552111. [DOI] [PubMed] [Google Scholar]
  23. Ward J. F. The yield of DNA double-strand breaks produced intracellularly by ionizing radiation: a review. Int J Radiat Biol. 1990 Jun;57(6):1141–1150. doi: 10.1080/09553009014551251. [DOI] [PubMed] [Google Scholar]
  24. Weisemann J. M., Funk C., Weinstock G. M. Measurement of in vivo expression of the recA gene of Escherichia coli by using lacZ gene fusions. J Bacteriol. 1984 Oct;160(1):112–121. doi: 10.1128/jb.160.1.112-121.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES