Effects of the binding of α/β-type small, acid-soluble spore proteins on the photochemistry of DNA in spores of Bacillus subtilis and In Vitro

Photochemistry and Photobiology

Volumn 81, Issue 1, 2005, Pages 163-169

  Douki, Thierry ^a   Setlow, Barbara ^b   Setlow, Peter ^b  

^a CEA GRENOBLE   (France)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 THYMINYL 5,6 DIHYDROTHYMINE; BACTERIAL DNA; BACTERIAL PROTEIN; CYCLOBUTANE DERIVATIVE; CYCLOBUTANE PYRIMIDINE DIMER; DIMER; PYRIMIDINE DERIVATIVE; PYRIMIDINE PYRIMIDONE PHOTOPRODUCT; PYRIMIDINONE DERIVATIVE; THYMINE DERIVATIVE; UNCLASSIFIED DRUG;

AQUEOUS SOLUTION; ARTICLE; BACILLUS SUBTILIS; BACTERIAL SPORE; BINDING ASSAY; BIOSYNTHESIS; CHEMICAL ANALYSIS; CONTROLLED STUDY; DNA DEGRADATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDRATION; IN VITRO STUDY; MASS SPECTROMETRY; NONHUMAN; PHOTOCHEMISTRY; PROTEIN DNA BINDING; TECHNIQUE; ULTRAVIOLET C RADIATION; ULTRAVIOLET IRRADIATION; WILD TYPE;

ACIDS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; DNA, BACTERIAL; PHOTOCHEMISTRY; SPORES, BACTERIAL; ULTRAVIOLET RAYS;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS);

EID: 14644425512     PISSN: 00318655     EISSN: None     Source Type: Journal    
DOI: 10.1562/2004-08-18-RA-278.1     Document Type: Article

References (46)

1. Nicholson, W. L., N. Munakata, G. Homeck, H. J. Melosh and P. Setlow (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64, 548-572.
2. Setlow, P. (1994) Mechanisms which contribute to the long-term survival of spores of Bacillus species. J. Appl. Bacterial. 76, 129S-134S.
3. Setlow, P. (2000) Resistance of bacterial spores. In Bacterial Stress Responses (Edited by G. Storz and R. Hengge-Aronis), pp. 217-230. American Society for Microbiology, Washington, DC.
4. Setlow, P. (1988) Resistance of bacterial spores to ultraviolet light. Comments Mol. Cell. Biophys. 5, 253-264.
5. Setlow, P. (2001) Resistance of spores of Bacillus species to ultraviolet light. Environ. Mol. Mutagen. 38, 97-104.
6. Donnellan Jr., J. E. and R. B. Setlow (1965) Thymine photoproducts but not thymine dimers are found in ultraviolet-irradiated bacterial spores. Science 149, 308-310.
7. Donnellan Jr., J. E. and R. S. Stafford (1968) The ultraviolet photochemistry and photobiology of vegetative cells and spores of Bacillus megaterium. Biophys. J. 8, 17-28.
8. Varghese, A. J. (1970) 5-Thyminyl-5,6-dihydrothymine from DNA irradiated with ultraviolet light. Biochem. Biophys. Res. Commun. 38, 484-490.
9. Lindsay, J. A. and W. G. Murrell (1983) A comparison of UV induced DNA photoproducts from isolated and non-isolated developing bacterial forespores. Biochem. Biophys. Res. Commun. 113, 618-625.
10. Munakata, N. and C. S. Rupert (1972) Genetically controlled removal of "spore photoproduct" from deoxyribonucleic acid of ultraviolet-irradiated Bacillus subtilis spores. J. Bacteriol. 111, 192-198.
11. Rebeil, R. and W. L. Nicholson (2001) The subunit structure and catalytic mechanism of the Bacillus subtilis DNA repair enzyme spore photoproduct lyase. Proc. Natl. Acad. Sci. USA 98, 9038-9043.
12. Van Wang, T. S. and C. S. Rupert (1977) Evidence for the monomerization of spore photoproduct to two thymines by the light independent "spore repair" process in Bacillus subtilis. Photochem. Photobiol. 25, 123-127.
13. Xue, Y. and W. L. Nicholson (1996) The two major spore DNA repair pathways, nucleotide excision repair and spore photoproduct lyase, are sufficient for the resistance of Bacillus subtilis spores to artificial UV-C and UV-B but not to solar radiation. Appl. Environ. Microbiol. 62, 2221-2227.
14. Gerhardt, P. and R. E. Marquis (1989) Spore thermoresistance mechanisms. In Regulation of Prokaryotic Development (Edited by I. Smith, R. A. Slepecky and P. Setlow), pp. 43-64. American Society for Microbiology, Washington, DC.
15. Patrick, M. H. and D. M. Gray (1976) Independence of photoproduct formation on DNA conformation. Photochem. Photobiol. 24, 507-513.
16. Rahn, R. O. and J. L. Hosszu (1969) Influence of relative humidity on the photochemistry of DNA films. Biochim. Biophys. Acta 190, 126-131.
17. Cowan, A. E., D. E. Koppel, B. Setlow and P. Setlow (2003) A soluble protein is immobile in dormant spores of Bacillus subtilis but is mobile in germinated spores. Proc. Natl. Acad. Sci. USA 100, 4209-4214.
18. Driks, A. and P. Setlow (1999) Morphogenesis and properties of the bacterial spore. In Prokaryotic Development (Edited by Y. V. Brun and L. J. Shimkets), pp. 191-218. American Society for Microbiology, Washington, DC.
19. Setlow, P. (1995) Mechanisms for the prevention of damage to the DNA in spores of Bacillus species. Ann. Rev. Microbiol. 49, 29-54.
20. Setlow, B. and P. Setlow (1987) Thymine containing dimers as well as spore photoproducts are found in ultraviolet-irradiated Bacillus subtilis spores that lack small acid-soluble proteins. Proc. Natl. Acad. Sci. USA 84, 421-423.
21. Griffith, J., A. Makhov, L. Santiago-Lara and P. Setlow (1994) Electron microscopic studies of the interaction between a Bacillus α/β-type small, acid-soluble spore protein with DNA: protein binding is cooperative, stiffens the DNA and induces negative supercoiling. Proc. Natl. Acad. Sci. USA 91, 8224-8228.
22. Frenkiel-Krispin, D., J. Englander, E. Shimoni, M. Eisenstein, E. Bullitt, R. Horowitz-Scherer, C. S. Hayes, P. Setlow, A. Minsky and S. G. Wolf (2004) Structure of DNA-SspC complex: implications for DNA packaging, protection and repair in bacterial spores. J. Bacteriol. 186, 3525-3530.
23. Fairhead, H. and P. Setlow (1992) Binding of DNA to α/β-type small, acid-soluble proteins from spores of Bacillus or Clostridium species prevents formation of cytosine dimers, cytosine-thymine dimers and bipyrimidine photoadducts upon ultraviolet irradiation. J. Bacteriol. 174, 2874-2880.
24. Nicholson, W. L., B. Setlow and P. Setlow (1991) Ultraviolet irradiation of DNA complexed with α/β-type small, acid-soluble proteins from spores of Bacillus or Clostridium species makes spore photoproduct but not thymine dimers. Proc. Natl. Acad. Sci. USA 88, 8288-8292.
25. Douki, T. and J. Cadet (2003) Formation of the spore photoproduct and other dimeric lesions between adjacent pyrimidines in UVC-irradiated dry DNA. Photochem. Photobiol. Sci. 2, 433-436.
26. Douki, T., G. Laporte and J. Cadet (2003) Inter-strand photoproducts are produced in high yield within A-DNA exposed to UVC radiation. Nucleic Adds Res. 31, 3134-3142.
27. Nguyen, H. T. and K. W. Minton (1988) Ultraviolet-induced dimerization of non-adjacent pyrimidines. A potential mechanism for the targeted -1 frameshift mutation. J. Mol. Biol. 200, 681-693.
28. Nguyen, H. T. and K. W. Minton (1989) Extensive photodimerization of non-adjacent pyrimidines. J. Mol. Biol. 210, 869-874.
29. Todd, P. A. and B. W. Glickman (1982) Mutational specificity of UV light in Escherichia coli: indications for a role of DNA secondary structure. Proc. Natl. Acad. Sci. USA 79, 4123-4127.
30. Mason, J. M. and P. Setlow (1986) Evidence for an essential role for small, acid-soluble spore proteins in the resistance of Bacillus subtilis spores to ultraviolet light. J. Bacteriol. 167, 174-178.
31. Nicholson, W. L. and P. Setlow (1990) Sporulation, germination and outgrowth. In Molecular Biological Methods for Bacillus (Edited by C. R. Harwood and S. M. Cutting), pp. 391-450. John Wiley and Sons, Chichester, UK.
32. Paidhungat, M., B. Setlow, A. Driks and P. Setlow (2000) Characterization of spores of Bacillus subtilis which lack dipicolinic acid. J. Bacteriol. 182, 5505-5512.
33. Kosman, J. and P. Setlow (2003) Effects of carboxyl-terminal modifications and pH on the binding of a Bacillus subtilis small, acid-soluble spore protein to DNA. J. Bacteriol. 185, 6095-6103.
34. Douki, T. and J. Cadet (2001) Individual determination of the yield of the main-UV induced dimeric pyrimidine photoproducts in DNA suggests a high mutagenicity of CC photo lesions. Biochemistry 40, 2495-2501.
35. Douki, T., A. Reynaud-Angelin, J. Cadet and E. Sage (2003) Bipyrimidine photoproducts rather than oxidative lesions are the main type of DNA damage involved in the genotoxic effect of solar UVA radiation. Biochemistry 42, 9221-9226.
36. Courdavault, S., C. Baudouin, S. Sauvaigo, S. Mouret, S. Candéias, M. Charveron, A. Favier, J. Cadet and T. Douki (2004) Unrepaired cyclobutane pyrimidine dimers do not prevent proliferation of UVB-irradiated cultured human fibroblasts. Photochem. Photobiol. 79, 145-151.
37. Douki, T., D. Angelov and J. Cadet (2001) UV laser photolysis of DNA: effect of duplex stability on charge-transfer efficiency. J. Am. Chem. Soc. 123, 11360-11366.
38. Lindsay, S. M., S. A. Lee, J. W. Powell, T. Weidlich, C. DeMarco, G. D. Lewen and N. J. Tao (1988) The origin of the A to B transition in DNA fibers and films. Biopolymers 27, 1015-1043.
39. Cooper, P. J. and L. D. Hamiton (1966) The A-B conformational change in the sodium salt of DNA. J. Mol. Biol. 16, 562-563.
40. Cabrera-Juarez, E. and J. K. Setlow (1980) Different chromatographic behavior of a thymine containing new ultraviolet photoproduct and spore photoproduct. Photochem. Photobiol. 31, 603-606.
41. Lindberg, C. and G. Horneck (1991) Action spectra for survival and spore photoproduct formation of Bacillus subtilis irradiated with short-wavelength (200-300 nm) UV at atmospheric pressure. J. Photochem. Photobiol. B: Biol. 11, 69-80.
42. Lindberg, C. and G. Horneck (1992) Thymine photoproduct formation and inactivation of intact spores of Bacillus subtilis irradiated with short wavelength UV (200-300 nm) at atmospheric pressure in vacuo. Adv. Space Res. 12, 275-279.
43. Dronkert, M. L. G. and R. Kanaar (2001) Repair of DNA interstrand cross-links. Mutation Res. 486, 217-247.
44. Popham, D. L., S. Sengupta and P. Setlow (1995) Heat, hydrogen peroxide, and UV resistance of Bacillus subtilis spores with increased core water content and with or without major DNA-binding proteins. Appl. Environ. Microbiol. 61, 3633-3638.
45. Girod, J. C., W. C. Johnson, S. K. Hunnington and M. F. Maestre (1973) Conformation of deoxyribonucleic acid in alcohol solutions. Biochemistry 12, 5092-5096.
46. Mohr, S. C., N. V. H. A. Sokolov, C. He and P. Setlow (1991) Binding of small acid-soluble proteins from Bacillus subtilis changes the conformation of DNA from B to A. Proc. Natl. Acad. Sci. USA 88, 77-81.