Photochemistry and Photobiology of the Spore Photoproduct: A 50-Year Journey

Photochemistry and Photobiology

Volumn 91, Issue 6, 2015, Pages 1263-1290

  Setlow, Peter ^a   Li, Lei ^b,c  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b INDIANA UNIVERSITY   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

THYMINE;

BACTERIAL SPORE; CHEMICAL STRUCTURE; CHEMISTRY; DNA REPAIR; PHOTOBIOLOGY; PHOTOCHEMISTRY; RADIATION RESPONSE; ULTRAVIOLET RADIATION;

DNA REPAIR; MOLECULAR STRUCTURE; PHOTOBIOLOGY; PHOTOCHEMISTRY; SPORES, BACTERIAL; THYMINE; ULTRAVIOLET RAYS;

EID: 84946499080     PISSN: 00318655     EISSN: 17511097     Source Type: Journal    
DOI: 10.1111/php.12506     Document Type: Article

References (203)

1. Donnellan, J. E. Jr, and, R. B. Setlow, (1965) Thymine photoproducts but not thymine dimers found in ultraviolet-irradiated bacterial spores. Science 149, 308-310.
2. Varghese, A. J., and, S. Y. Wang, (1967) Ultraviolet irradiation of DNA in vitro and in vivo produces a third thymine-derived product. Science 156, 955-957.
3. Donnellan, 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.
4. Smith, K. C., and, H. Yoshikawa, (1966) Variation in the photochemical reactivity of thymine in the DNA of B. subtilis spores, vegetative cells and spores germinated in chloramphenicol. Photochem. Photobiol. 5, 777-786.
5. Varghese, A. J., (1971) Photochemistry of thymidine as a thin solid film. Photochem. Photobiol. 13, 357-364.
6. Rahn, R. O., J. K. Setlow, and, J. L. Hosszu, (1969) Ultraviolet inactivation and photoproducts of transforming DNA irradiated at low temperatures. Biophys. J. 9, 510-517.
7. Varghese, A. J., (1970a) 5-Thyminyl-5,6-dihydrothymine from DNA irradiated with ultraviolet light. Biochem. Biophys. Res. Commun. 38, 484-490.
8. Mantel, C., A. Chandor, D. Gasparutto, T. Douki, M. Atta, M. Fontecave, P. A. Bayle, J. M. Mouesca, and, M. Bardet, (2008) Combined NMR and DFT studies for the absolute configuration elucidation of the spore photoproduct, a UV-induced DNA lesion. J. Am. Chem. Soc. 130, 16978-16984.
9. Chandor, A., O. Berteau, T. Douki, D. Gasparutto, Y. Sanakis, S. Ollagnier-De-Choudens, M. Atta, and, M. Fontecave, (2006) Dinucleotide spore photoproduct, a minimal substrate of the DNA repair spore photoproduct lyase enzyme from Bacillus subtilis. J. Biol. Chem. 281, 26922-26931.
10. Munakata, N., (1969) Genetic analysis of a mutant of Bacillus subtilis producing ultraviolet-sensitive spores. Mol. Gen. Genet. 104, 258-263.
11. 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.
12. Munakata, N., and, C. S. Rupert, (1974) Dark repair of DNA containing "spore photoproduct" in Bacillus subtilis. Mol. Gen. Genet. 130, 239-250.
13. Wang, T.-C. V., 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.
14. Sancar, A., (1996) DNA excision repair. Ann. Rev. Biochem. 65, 43-81.
15. Cline, S. D., and, P. C. Hanawalt, (2003) Who's on first in the cellular response to DNA damage? Nat. Rev. Mol. Cell Biol. 4, 361-373.
16. Shah, P., and, Y.-Y. He, (2015) Molecular regulation of UV-induced DNA repair. Photochem. Photobiol. 91, 254-264.
17. Kisker, C., J. Kuper, and, B. Van Houten, (2013) Prokaryotic nucleotide excision repair. Cold Spring Harb. Perspect. Biol. 5, a012591.
18. Pedraza-Reyes, M., F. Gutierrez-Corona, and, W. L. Nicholson, (1997) Spore photoproduct lyase operon (splAB) regulation during Bacillus subtilis sporulation: Modulation of splB-lacZ fusion expression by P1 promoter mutations and by an in-frame deletion of splA. Curr. Microbiol. 34, 133-137.
19. Sofia, H. J., G. Chen, B. G. Hetzler, J. F. Reyes-Spindola, and, N. E. Miller, (2001) Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: Functional characterization using new analysis and information visualization methods. Nucleic Acids Res. 29, 1097-1106.
20. Rebeil, R., Y. Sun, L. Chooback, M. Pedraza-Reyes, C. Kinsland, T. P. Begley, and, W. L. Nicholson, (1998) Spore photoproduct lyase from Bacillus subtilis spores is a novel iron-sulfur DNA repair enzyme which shares features with proteins such as class III anaerobic ribonucleotide reductases and pyruvate-formate lyases. J. Bacteriol. 180, 4879-4885.
21. Mehl, R. A., and, T. P. Begley, (1999) Mechanistic studies on the repair of a novel DNA photolesion: The spore photoproduct. Org. Lett. 1, 1065-1066.
22. 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. 98, 9038-9043.
23. Fajardo-Cavazos, P., R. Rebeil, and, W. Nicholson, (2005) Essential cysteine residues in Bacillus subtilis spore photoproduct lyase identified by alanine scanning mutagenesis. Curr. Microbiol. 51, 331-335.
24. Pieck, J., U. Hennecke, A. Pierik, M. Friedel, and, T. Carell, (2006) Characterization of a new thermophilic spore photoproduct lyase from Geobacillus stearothermophilus (SplG) with defined lesion containing DNA substrates. J. Biol. Chem. 281, 36317-36326.
25. Kneuttinger, A. C., K. Heil, G. Kashiwazaki, and, T. Carell, (2013) The radical SAM enzyme spore photoproduct lyase employs a tyrosyl radical for DNA repair. Chem. Commun. 49, 722-724.
26. Benjdia, A., K. Heil, A. Winkler, T. Carell, and, I. Schlichting, (2014) Rescuing DNA repair activity by rewiring the H-atom transfer pathway in the radical SAM enzyme, spore photoproduct lyase. Chem. Commun. 50, 14201-14204.
27. Chandor-Proust, A., O. Berteau, T. Douki, D. Gasparutto, S. Ollagnier-De-Choudens, M. Fontecave, and, M. Atta, (2008) DNA repair and free radicals, new insights into the mechanism of spore photoproduct lyase revealed by single amino Acid substitution. J. Biol. Chem. 283, 36361-36368.
28. Cheek, J., and, J. Broderick, (2002) Direct H atom abstraction from spore photoproduct C-6 initiates DNA repair in the reaction catalyzed by spore photoproduct lyase: Evidence for a reversibly generated adenosyl radical intermediate. J. Am. Chem. Soc. 124, 2860-2861.
29. Buis, J., J. Cheek, E. Kalliri, and, J. Broderick, (2006) Characterization of an active spore photoproduct lyase, a DNA repair enzyme in the radical S-adenosylmethionine superfamily. J. Biol. Chem. 281, 25994-26003.
30. Silver, S., T. Chandra, E. Zilinskas, S. Ghose, W. Broderick, and, J. Broderick, (2010) Complete stereospecific repair of a synthetic dinucleotide spore photoproduct by spore photoproduct lyase. J. Biol. Inorg. Chem. 15, 943-955.
31. Yang, L., G. Lin, D. Liu, K. J. Dria, J. Telser, and, L. Li, (2011) Probing the reaction mechanism of spore photoproduct lyase (SPL) via diastereoselectively labeled dinucleotide SP TpT substrates. J. Am. Chem. Soc. 133, 10434-10447.
32. Yang, L., G. Lin, R. S. Nelson, Y. Jian, J. Telser, and, L. Li, (2012) Mechanistic studies of the spore photoproduct lyase via a single cysteine mutation. Biochemistry 51, 7173-7188.
33. Yang, L., R. S. Nelson, A. Benjdia, G. Lin, J. Telser, S. Stoll, I. Schlichting, and, L. Li, (2013) A radical transfer pathway in spore photoproduct lyase. Biochemistry 52, 3041-3050.
34. Benjdia, A., K. Heil, T. R. M. Barends, T. Carell, and, I. Schlichting, (2012) Structural insights into recognition and repair of UV-DNA damage by spore photoproduct lyase, a radical SAM enzyme. Nucleic Acids Res. 40, 9308-9318.
35. Yang, L., and, L. Li, (2013) The enzyme-mediated direct reversal of a dithymine photoproduct in germinating endospores. Int. J. Mol. Sci. 14, 13137-13153.
36. Yang, L., and, L. Li, (2015) Spore photoproduct lyase: The known, the controversial, and the unknown. J. Biol. Chem. 290, 4003-4009.
37. Li, L., (2012) Mechanistic studies of the radical SAM enzyme spore photoproduct lyase (SPL). Biochim. Biophys. Acta Proteins Proteomics 1824, 1264-1277.
38. Kneuttinger, A. C., G. Kashiwazaki, S. Prill, K. Heil, M. Müller, and, T. Carell, (2014) Formation and direct repair of UV-induced dimeric DNA pyrimidine lesions. Photochem. Photobiol. 90, 1-14.
39. Benjdia, A., (2012) DNA photolyases and SP lyase: Structure and mechanism of light-dependent and independent DNA lyases. Curr. Opin. Struct. Biol. 22, 711-720.
40. Desnous, C. L., D. Guillaume, and, P. Clivio, (2010) Spore photoproduct: A key to bacterial eternal life. Chem. Rev. 110, 1213-1232.
41. Yoshimura, Y., and, H. Takahata, (2012) Recent advances in cyclonucleosides: C-cyclonucleosides and spore photoproducts in damaged DNA. Molecules 17, 11630-11654.
42. 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. 43-63. American Society for Microbiology, Washington, DC.
43. Henriques, A. O., and, C. P. Jr Moran, (2007) Structure, assembly, and function of the spore surface layers. Annu. Rev. Microbiol. 61, 555-588.
44. Setlow, P., (2006) Spores of Bacillus subtilis: Their resistance to and killing by radiation, heat and chemicals. J. Appl. Microbiol. 101, 514-525.
45. McKenney, P. T., A. Driks, and, P. Eichenberger, (2013) The Bacillus subtilis endospore: Assembly and functions of the multilayered coat. Nat. Rev. Microbiol. 11, 33-44.
46. Setlow, P., (1995) Mechanisms for the prevention of damage to DNA in spores of Bacillus species. Annu. Rev. Microbiol. 49, 29-54.
47. Duthie, M. S., I. Kimber, and, M. Norval, (1999) The effects of ultraviolet radiation on the human immune system. Br. J. Dermatol. 140, 995-1009.
48. Nicholson, W., A. Schuerger, and, P. Setlow, (2005) The solar UV environment and bacterial spore UV resistance: Considerations for Earth-to-Mars transport by natural processes and human spaceflight. Mutat. Res. 571, 249-264.
49. Slieman, T. A., and, W. L. Nicholson, (2000) Artificial and solar UV radiation induces strand breaks and cyclobutane pyrimidine dimers in Bacillus subtilis spore DNA. Appl. Environ. Microbiol. 66, 199-205.
50. Moeller, R., T. Douki, J. Cadet, E. Stackebrandt, W. L. Nicholson, P. Rettberg, G. Reitz, and, G. Horneck, (2007a) UV-radiation-induced formation of DNA bipyrimidine photoproducts in Bacillus subtilis endospores and their repair during germination. Int. Microbiol. 10, 39-46.
51. Tyrrell, R. M., (1978) Solar dosimetry with repair deficient bacterial spores: Action spectra, photoproduct measurements and a comparison with other biological systems. Photochem. Photobiol. 27, 571-579.
52. 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.
53. Moeller, R., E. Stackebrandt, G. Reitz, T. Berger, P. Rettberg, A. J. Doherty, G. Horneck, and, W. L. Nicholson, (2007b) Role of DNA repair by nonhomologous-end joining in Bacillus subtilis spore resistance to extreme dryness, mono- and polychromatic UV, and ionizing radiation. J. Bacteriol. 189, 3306-3311.
54. Moeller, R., G. Reitz, Z. Li, S. Klein, and, W. L. Nicholson, (2012) Multifactorial resistance of Bacillus subtilis spores to high-energy proton radiation: Role of spore structural components and the homologous recombination and non-homologous end joining DNA repair pathways. Astrobiology 12, 1069-1077.
55. Wang, S. T., B. Setlow, E. M. Conlon, J. L. Lyon, D. Imamura, T. Sato, P. Setlow, R. Losick, and, P. Eichenberger, (2006) The forespore line of gene expression in Bacillus subtilis. J. Mol. Biol. 358, 16-37.
56. Setlow, P., (2013) When the sleepers wake: The germination of spores of Bacillus species. J. Appl. Microbiol. 115, 1251-1268.
57. Setlow, P., (2014) Germination of spores of Bacillus species: What we know and do not know. J. Bacteriol. 196, 1297-1305.
58. Moir, A., (2006) How do spores germinate? J. Appl. Microbiol. 101, 526-530.
59. 2+-dipicolinic acid in individual Bacillus spores determined using microfluidic Raman tweezers. J. Bacteriol. 189, 4681-4687.
60. 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.
61. Setlow, B., S. Atluri, R. Kitchel, K. Koziol-Dube, and, P. Setlow, (2006) Role of dipicolinic acid in resistance and stability of spores of Bacillus subtilis with or without DNA-protective α/β-type small acid-soluble proteins. J. Bacteriol. 188, 3740-3747.
62. Bender, G. R., and, R. E. Marquis, (1985) Spore heat resistance and specific mineralization. Appl. Environ. Microbiol. 50, 1414-1421.
63. Douki, T., B. Setlow, and, P. Setlow, (2005a) Photosensitization of DNA by dipicolinic acid, a major component of spores of Bacillus species. Photochem. Photobiol. Sci. 4, 591-597.
64. Stafford, R. S., and, J. E. Jr Donnellan, (1968) Photochemical evidence for conformation changes in DNA during germination of bacterial spores. Proc. Natl Acad. Sci. 59, 822-828.
65. Setlow, B., and, P. Setlow, (1988) Absence of transient elevated UV resistance during germination of Bacillus subtilis spores lacking small, acid-soluble spore proteins alpha and beta. J. Bacteriol. 170, 2858-2859.
66. Sanchez-Salas, J. L., M. L. Santiago-Lara, B. Setlow, M. D. Sussman, and, P. Setlow, (1992) Properties of Bacillus megaterium and Bacillus subtilis mutants which lack the protease that degrades small, acid-soluble proteins during spore germination. J. Bacteriol. 174, 807-814.
67. Setlow, P., (2001) Resistance of spores of Bacillus species to ultraviolet light. Environ. Mol. Mutagen. 38, 97-104.
68. Setlow, P., (2003) Spore germination. Curr. Opin. Microbiol. 6, 550-556.
69. Riemann, H., and, Z. J. Ordal, (1961) Germination of bacterial endospores with calcium and dipicolinic acid. Science 133, 1703-1704.
70. Ablett, S., A. H. Darke, P. J. Lillford, and, D. R. Martin, (1999) Glass formation and dormancy in bacterial spores. Int. J. Food Sci. Tech. 34, 59-69.
71. Leuschner, R. G. K., and, P. J. Lillford, (2003) Thermal properties of bacterial spores and biopolymers. Int. J. Food Microbiol. 80, 131-143.
72. Black, S. H., and, P. Gerhardt, (1962) Permeability of bacterial spores IV.: Water content, uptake, and distribution. J. Bacteriol. 83, 960-967.
73. 2H NMR. Biophys. J. 105, 2016-2023.
74. Stecchini, M. L., M. Del Torre, E. Venir, A. Morettin, P. Furlan, and, E. Maltini, (2006) Glassy state in Bacillus subtilis spores analyzed by differential scanning calorimetry. Int. J. Food Microbiol. 106, 286-290.
75. Strahs, G., and, R. E. Dickerson, (1968) The crystal structure of calcium dipicolinate trihydrate (a bacterial spore metabolite). Acta Crystallogr. B 24, 571-578.
76. Friedline, A. W., M. M. Zachariah, K. Johnson, K. J. Thomas, A. N. Middaugh, R. Garimella, D. R. Powell, P. A. Vaishampayan, and, C. V. Rice, (2014) Water behavior in bacterial spores by deuterium NMR spectroscopy. J. Phys. Chem. B 118, 8945-8955.
77. 2+-dipicolinic acid alone and in the bacterial spore core in both aqueous and dehydrated environments. Analyst 137, 3683-3689.
78. Ghiamati, E., R. Manoharan, W. H. Nelson, and, J. F. Sperry, (1992) UV resonance Raman-spectra of Bacillus spores. Appl. Spectrosc. 46, 357-364.
79. Lindsay, J., and, W. Murrell, (1986) Solution spectroscopy of dipicolinic acid interaction with nucleic acids: Role in spore heat resistance. Curr. Microbiol. 13, 255-259.
80. Lindsay, J., and, W. Murrell, (1985) Changes in density of DNA after interaction with dipicolinic acid and its possible role in spore heat resistance. Curr. Microbiol. 12, 329-333.
81. Setlow, B., and, P. Setlow, (1993) Dipicolinic acid greatly enhances production of spore photoproduct in bacterial spores upon UV irradiation. Appl. Environ. Microbiol. 59, 640-643.
82. Du, Q., H. Zhao, D. Song, K. Liu, and, H. Su, (2012) Consecutive reaction mechanism for the formation of spore photoproduct in DNA photolesion. J. Phys. Chem. B 116, 11117-11123.
83. Lamola, A. A., (1970) Triplet photosensitization and the photobiology of thymine dimers in DNA. Pure Appl. Chem. 24, 599-610.
84. Carstensen, E. L., R. E. Marquis, S. Z. Child, and, G. R. Bender, (1979) Dielectric properties of native and decoated spores of Bacillus megaterium. J. Bacteriol. 140, 917-928.
85. Carstensen, E. L., R. E. Marquis, and, P. Gerhardt, (1971) Dielectric study of the physical state of electrolytes and water within Bacillus cereus spores. J. Bacteriol. 107, 106-113.
86. Cowan, A. E., E. M. Olivastro, D. E. Koppel, C. A. Loshon, B. Setlow, and, P. Setlow, (2004) Lipids in the inner membrane of dormant spores of Bacillus species are largely immobile. Proc. Natl Acad. Sci. 101, 7733-7738.
87. 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: Implications for spore dormancy. Proc. Natl Acad. Sci. 100, 4209-4214.
88. Setlow, P., (2007) I will survive: DNA protection in bacterial spores. Trends Microbiol. 15, 172-180.
89. Mohr, S. C., N. V. Sokolov, C. M. He, and, P. Setlow, (1991) Binding of small acid-soluble spore proteins from Bacillus subtilis changes the conformation of DNA from B to A. Proc. Natl Acad. Sci. 88, 77-81.
90. Griffith, J., A. Makhov, L. Santiagolara, and, P. Setlow, (1994) Electron-microscopic studies of the interaction between a Bacillus-Subtilis 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. 91, 8224-8228.
91. Setlow, P., (1988) Small, acid-soluble spore proteins of Bacillus species: Structure, synthesis, genetics, function, and degradation. Annu. Rev. Microbiol. 42, 319-338.
92. 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. 88, 8288-8292.
93. 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 after UV irradiation. J. Bacteriol. 174, 2874-2880.
94. Douki, T., B. Setlow, and, P. Setlow, (2005b) 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. Photochem. Photobiol. 81, 163-169.
95. Mason, J. M., and, P. Setlow, (1987) Different small, acid-soluble proteins of the α/β type have interchangeable roles in the heat and UV radiation resistance of Bacillus subtilis spores. J. Bacteriol. 169, 3633-3637.
96. Tovar-Rojo, F., and, P. Setlow, (1991) Effects of mutant small, acid-soluble spore proteins from Bacillus subtilis on DNA in vivo and in vitro. J. Bacteriol. 173, 4827-4835.
97. Raju, D., P. Setlow, and, M. R. Sarker, (2007) Antisense-RNA-mediated decreased synthesis of small, acid-soluble spore proteins leads to decreased resistance of Clostridium perfringens spores to moist heat and UV radiation. Appl. Environ. Microbiol. 73, 2048-2053.
98. Raju, D., M. Waters, P. Setlow, and, M. Sarker, (2006) Investigating the role of small, acid-soluble spore proteins (SASPs) in the resistance of Clostridium perfringens spores to heat. BMC Microbiol. 6, 50.
99. Setlow, B., A. R. Hand, and, P. Setlow, (1991) Synthesis of a Bacillus subtilis small, acid-soluble spore protein in Escherichia coli causes cell DNA to assume some characteristics of spore DNA. J. Bacteriol. 173, 1642-1653.
100. Ragkousi, K., A. E. Cowan, M. A. Ross, and, P. Setlow, (2000) Analysis of nucleoid morphology during germination and outgrowth of spores of Bacillus species. J. Bacteriol. 182, 5556-5562.
101. Pogliano, K., E. Harry, and, R. Losick, (1995) Visualization of the subcellular location of sporulation proteins in Bacillus subtilis using immunofluorescence microscopy. Mol. Microbiol. 18, 459-470.
102. Setlow, B., D. Sun, and, P. Setlow, (1992) Interaction between DNA and α/β-type small, acid-soluble spore proteins: A new class of DNA-binding protein. J. Bacteriol. 174, 2312-2322.
103. Frenkiel-Krispin, D., R. Sack, 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 the DNA-SspC complex: Implications for DNA packaging, protection, and repair in bacterial spores. J. Bacteriol. 186, 3525-3530.
104. Hayes, C. S., and, P. Setlow, (2001) An α/β-type, small, acid-soluble spore protein which has very high affinity for DNA prevents outgrowth of Bacillus subtilis spores. J. Bacteriol. 183, 2662-2666.
105. Kosman, J., and, P. Setlow, (2003) Effects of carboxy-terminal modifications and pH on binding of a Bacillus subtilis small, acid-soluble spore protein to DNA. J. Bacteriol. 185, 6095-6103.
106. Lee, K. S., D. Bumbaca, J. Kosman, P. Setlow, and, M. J. Jedrzejas, (2008) Structure of a protein-DNA complex essential for DNA protection in spores of Bacillus species. Proc. Natl Acad. Sci. 105, 2806-2811.
107. Bumbaca, D., J. Kosman, P. Setlow, R. K. Henderson, and, M. J. Jedrzejas, (2007) Crystallization and preliminary X-ray analysis of the complex between a Bacillus subtilis α/β-type small acid-soluble spore protein and DNA. Acta Crystallogr. F 63, 503-506.
108. Nicholson, W. L., B. Setlow, and, P. Setlow, (1990) Binding of DNA in vitro by a small, acid-soluble spore protein from Bacillus subtilis and the effect of this binding on DNA topology. J. Bacteriol. 172, 6900-6906.
109. Patrick, M. H., and, D. M. Gray, (1976) Independence of photoproduct formation on DNA conformation. Photochem. Photobiol. 24, 507-513.
110. Cadet, J., S. Courdavault, J. L. Ravanat, and, T. Douki, (2005) UVB and UVA radiation-mediated damage to isolated and cellular DNA. Pure Appl. Chem. 77, 947-961.
111. Johns, H. E., M. L. Pearson, C. W. Helleiner, and, J. C. Leblanc, (1964) Ultraviolet photochemistry of thymidylyl-(3′ to 5′) -thymidine. J. Mol. Biol. 9, 503-524.
112. Sztumpf, E., and, D. Shugar, (1962) Photochemistry of model oligo- and polynucleotides 6. Photodimerization and its reversal in thymine dinucleotide analogues. Biochim. Biophys. Acta 61, 555-566.
113. Schreier, W. J., T. E. Schrader, F. O. Koller, P. Gilch, C. E. Crespo-Hernandez, V. N. Swaminathan, T. Carell, W. Zinth, and, B. Kohler, (2007) Thymine dimerization in DNA is an ultrafast photoreaction. Science 315, 625-629.
114. Kwok, W.-M., C. Ma, and, D. L. Phillips, (2008) A doorway state leads to photostability or triplet photodamage in thymine DNA. J. Am. Chem. Soc. 130, 5131-5139.
115. Cuquerella, M. C., V. Lhiaubet-Vallet, F. Bosca, and, M. A. Miranda, (2011) Photosensitised pyrimidine dimerisation in DNA. Chem. Sci. 2, 1219-1232.
116. Schreier, W. J., J. Kubon, N. Regner, K. Haiser, T. E. Schrader, W. Zinth, P. Clivio, and, P. Gilch, (2009) Thymine dimerization in DNA model systems: Cyclobutane photolesion is predominantly formed via the singlet channel. J. Am. Chem. Soc. 131, 5038-5039.
117. Kozak, C. R., K. A. Kistler, Z. Lu, and, S. Matsika, (2010) Excited-state energies and electronic couplings of DNA base dimers. J. Phys. Chem. B 114, 1674-1683.
118. Banyasz, A., T. Douki, R. Improta, T. Gustavsson, D. Onidas, I. Vaya, M. Perron, and, D. Markovitsi, (2012) Electronic excited states responsible for dimer formation upon UV absorption directly by thymine strands: Joint experimental and theoretical study. J. Am. Chem. Soc. 134, 14834-14845.
119. Giussani, A., L. Serrano-Andrés, M. Merchán, D. Roca-Sanjuán, and, M. Garavelli, (2013) Photoinduced formation mechanism of the thymine-thymine (6-4) adduct. J. Phys. Chem. B 117, 1999-2004.
120. Pilles, B. M., D. B. Bucher, L. Liu, P. Clivio, P. Gilch, W. Zinth, and, W. J. Schreier, (2014) Mechanism of the decay of thymine triplets in DNA single strands. J. Phys. Chem. Lett. 5, 1616-1622.
121. Rahn, R. O., and, J. L. Hosszu, (1968) Photochemistry of polynucleotides: A summary of temperature effects. Photochem. Photobiol. 7, 637-642.
122. Eisenstein, M., F. Frolow, Z. Shakked, and, D. Rabinovich, (1990) The structure and hydration of the A-DNA fragment d(GGGTACCC) at room temperature and low temperature. Nucleic Acids Res. 18, 3185-3194.
123. Varghese, A. J., (1970b) Photochemistry of thymidine in ice. Biochemistry 9, 4781-4787.
124. Ames, D. M., G. Lin, Y. Jian, J. Cadet, and, L. Li, (2014) Unusually large deuterium discrimination during spore photoproduct formation. J. Org. Chem. 79, 4843-4851.
125. Friedel, M., O. Berteau, J. Pieck, M. Atta, S. Ollagnier-de-Choudens, M. Fontecave, and, T. Carell, (2006a) The spore photoproduct lyase repairs the 5S- and not the 5R-configured spore photoproduct DNA lesion. Chem. Commun. 28, 445-447.
126. Friedel, M., J. Pieck, J. Klages, C. Dauth, H. Kessler, and, T. Carell, (2006b) Synthesis and stereochemical assignment of DNA spore photoproduct analogues. Chem. Eur. J. 12, 6081-6094.
127. Chandra, T., S. C. Silver, E. Zilinskas, E. M. Shepard, W. E. Broderick, and, J. B. Broderick, (2009) Spore photoproduct lyase catalyzes specific repair of the 5R but not the 5S spore photoproduct. J. Am. Chem. Soc. 131, 2420-2421.
128. Lin, G., C.-H. Chen, M. Pink, J. Pu, and, L. Li, (2011) Chemical synthesis, crystal structure and enzymatic evaluation of a dinucleotide spore photoproduct analogue containing a formacetal linker. Chem. Eur. J. 17, 9658-9668.
129. Heil, K., A. C. Kneuttinger, S. Schneider, U. Lischke, and, T. Carell, (2011a) Crystal structures and repair studies reveal the identity and the base-pairing properties of the UV-induced spore photoproduct DNA lesion. Chem. Eur. J. 17, 9651-9657.
130. Valle-Orero, J., A. Wildes, J.-L. Garden, and, M. Peyrard, (2013) Purification of A-form DNA fiber samples by the removal of B-form DNA residues. J. Phys. Chem. B 117, 1849-1856.
131. Falk, M., K. A. Hartman, and, R. C. Lord, (1963) Hydration of deoxyribonucleic acid. III. A spectroscopic study of the effect of hydration on the structure of deoxyribonucleic acid. J. Am. Chem. Soc. 85, 391-394.
132. Rahn, R. O., and, H. L. Hosszu, (1969) Influence of relative humidity on the photochemistry of DNA films. Biochim. Biophys. Acta 190, 126-131.
133. Slieman, T. A., R. Rebeil, and, W. L. Nicholson, (2000) Spore photoproduct (SP) lyase from Bacillus subtilis specifically binds to and cleaves SP (5-thyminyl-5,6-dihydrothymine) but not cyclobutane pyrimidine dimers in UV-irradiated DNA. J. Bacteriol. 182, 6412-6417.
134. 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.
135. Douki, T., G. Laporte, and, J. Cadet, (2003) Inter-strand photoproducts are produced in high yield within A-DNA exposed to UVC radiation. Nucleic Acids Res. 31, 3134-3142.
136. Gray, D. M., and, R. L. Ratliff, (1975) Circular-dichroism spectra of poly[d(AC)-d(GT)], poly[r(AC)-r(GU)], and hybrids poly[d(AC)-r(GU)] and poly[r(AC)-d(GT)] in presence of ethanol. Biopolymers 14, 487-498.
137. Ivanov, V. I., L. E. Minchenk, E. E. Minyat, M. D. Frankkam, and, A. K. Schyolki, (1974) B to A transition of DNA in solution. J. Mol. Biol. 87, 817-833.
138. Cadet, J., and, P. Vigny, (1990) Photochemistry and the nucleic acids. In Bioorganic Photochemistry v. 1, Vol. 1. (Edited by, H. Morrison,), pp. 1-272. Wiley, New York.
139. Lin, G., and, L. Li, (2010) Elucidation of spore-photoproduct formation by isotope labeling. Angew. Chem. Int. Ed. 49, 9926-9929.
140. Krishtalik, L. I., (2000) The mechanism of the proton transfer: An outline. Biochim. Biophys. Acta Bioenergetics 1458, 6-27.
141. Ostrowski, T., J.-C. Maurizot, M.-T. Adeline, J.-L. Fourrey, and, P. Clivio, (2003) Sugar conformational effects on the photochemistry of thymidylyl(3′-5′)thymidine. J. Org. Chem. 68, 6502-6510.
142. Moriou, C., M. Thomas, M.-T. Adeline, M.-T. Martin, A. Chiaroni, S. Pochet, J.-L. Fourrey, A. Favre, and, P. Clivio, (2007) Crystal structure and photochemical behavior in solution of the 3′-N-sulfamate analogue of thymidylyl(3′-5′)thymidine. J. Org. Chem. 72, 43-50.
143. Desnous, C., B. R. Babu, C. Moriou, J. U. O. Mayo, A. Favre, J. Wengel, and, P. Clivio, (2008) The sugar conformation governs (6-4) photoproduct formation at the dinucleotide level. J. Am. Chem. Soc. 130, 30-31.
144. Jian, Y., D. M. Ames, H. Ouyang, and, L. Li, (2015) Photochemical reactions of microcrystalline thymidine. Org. Lett. 17, 824-827.
145. Young, D. W., P. Tollin, and, H. R. Wilson, (1969) The crystal and molecular structure of thymidine. Acta Crystallogr. B 25, 1423-1432.
146. Moysan, A., A. Viari, P. Vigny, L. Voituriez, J. Cadet, E. Moustacchi, and, E. Sage, (1991) Formation of cyclobutane thymine dimers photosensitized by pyridopsoralens: Quantitative and qualitative distribution within DNA. Biochemistry 30, 7080-7088.
147. Bergstrom, D. E., and, K. F. Rash, (1979) Synthesis of 5,6-dihydro-5-(alpha-thyminyl)thymine. J. Org. Chem. 44, 1414-1417.
148. Nicewonger, R., and, T. P. Begley, (1997) Synthesis of the spore photoproduct. Tetrahedron Lett. 38, 935-936.
149. Jian, Y., and, L. Li, (2013) Chemical syntheses of oligodeoxyribonucleotides containing spore photoproduct. J. Org. Chem. 78, 3021-3029.
150. Kim, S. J., C. Lester, and, T. P. Begley, (1995) Synthesis of the dinucleotide spore photoproduct. J. Org. Chem. 60, 6256-6257.
151. Matteucci, M., (1990) Deoxyoligonucleotide analogs based on formacetal linkages. Tetrahedron Lett. 31, 2385-2388.
152. Gao, X., F. K. Brown, P. Jeffs, N. Bischofberger, K. Y. Lin, A. J. Pipe, and, S. A. Noble, (1992) Probing structural factors stabilizing antisense oligonucleotide duplexes: NMR studies of a DNA•DNA duplex containing a formacetal linkage. Biochemistry 31, 6228-6236.
153. Jones, R. J., K. Y. Lin, J. F. Milligan, S. Wadwani, and, M. D. Matteucci, (1993) Synthesis and binding properties of pyrimidine oligodeoxynucleoside analogs containing neutral phosphodiester replacements: The formacetal and 3′-thioformacetal internucleoside linkages. J. Org. Chem. 58, 2983-2991.
154. Rozners, E., and, R. Strömberg, (1997) Synthesis and properties of oligoribonucleotide analogs having formacetal internucleoside linkages. J. Org. Chem. 62, 1846-1850.
155. Butenandt, J., A. P. M. Eker, and, T. Carell, (1998) Synthesis, crystal structure, and enzymatic evaluation of a DNA-photolesion isostere. Chem. Eur. J. 4, 642-654.
156. Varma, R. S., (1993) Synthesis of oligonucleotide analogs with modified backbones. Synlett, 4, 621-637.
157. Heil, K., D. Pearson, and, T. Carell, (2011b) Chemical investigation of light induced DNA bipyrimidine damage and repair. Chem. Soc. Rev. 40, 4271-4278.
158. Taylor, J.-S., and, I. R. Brockie, (1988) Synthesis of a trans-syn thymine dimer building block. Solid phase synthesis of CGTAT[t, s]TATGC. Nucleic Acids Res. 16, 5123-5136.
159. Taylor, J. S., I. R. Brockie, and, C. L. O'Day, (1987) A building block for the sequence-specific introduction of cis-syn thymine dimers into oligonucleotides. Solid-phase synthesis of TpT[c, s]pTpT. J. Am. Chem. Soc. 109, 6735-6742.
160. Ortiz Mayo, J. U., M. Thomas, C. Saintomé, and, P. Clivio, (2003) Facile synthesis of a cis-syn thymine dimer building block and its incorporation into oligodeoxynucleotides. Tetrahedron 59, 7377-7383.
161. Friedel, M. G., J. Gierlich, and, T. Carell, (2006c) Cyclobutane pyrimidine dimers as UV-induced DNA lesions. In The Chemistry of Cyclobutanes, pp. 1031-1059. John Wiley & Sons, Ltd., Hoboken, NJ.
162. Murata, T., S. Iwai, and, E. Ohtsuka, (1990) Synthesis and characterization of a substrate for T4 endonuclease V containing a phosphorodithioate linkage at the thymine dimer site. Nucleic Acids Res. 18, 7279-7286.
163. Tommasi, S., P. M. Swiderski, Y. Tu, B. E. Kaplan, and, G. P. Pfeifer, (1996) Inhibition of transcription factor binding by ultraviolet-induced pyrimidine dimers. Biochemistry 35, 15693-15703.
164. Kosmoski, J. V., and, M. J. Smerdon, (1999) Synthesis and nucleosome structure of DNA containing a UV photoproduct at a specific site. Biochemistry 38, 9485-9494.
165. Butenandt, J., L. T. Burgdorf, and, T. Carell, (1999) Synthesis of DNA lesions and DNA-lesion-containing oligonucleotides for DNA-repair studies. Synthesis, 31, 1085-1105.
166. Iwai, S., M. Shimizu, H. Kamiya, and, E. Ohtsuka, (1996) Synthesis of a phosphoramidite coupling unit of the pyrimidine (6-4) pyrimidone photoproduct and its incorporation into oligodeoxynucleotides. J. Am. Chem. Soc. 118, 7642-7643.
167. Cadet, J., L. Voituriez, F. E. Hruska, and, A. Grand, (1985) Crystal structure of the cis-syn photodimer of thymidylyl (3′-5′) thymidine cyanoethyl ester. Biopolymers 24, 897-903.
168. Zheng, G., X.-J. Lu, and, W. K. Olson, (2009) Web 3DNA-a web server for the analysis, reconstruction, and visualization of three-dimensional nucleic-acid structures. Nucleic Acids Res. 37, W240-W246.
169. Lu, X.-J., and, W. K. Olson, (2008) 3DNA: A versatile, integrated software system for the analysis, rebuilding and visualization of three-dimensional nucleic-acid structures. Nat. Protoc. 3, 1213-1227.
170. Singh, I., Y. Jian, L. Li, and, M. M. Georgiadis, (2014) The structure of an authentic spore photoproduct lesion in DNA suggests a basis for recognition. Acta Crystallogr. D 70, 752-759.
171. Goodwin, K. D., E. C. Long, and, M. M. Georgiadis, (2005) A host-guest approach for determining drug-DNA interactions: An example using netropsin. Nucleic Acids Res. 33, 4106-4116.
172. Park, H., K. Zhang, Y. Ren, S. Nadji, N. Sinha, J.-S. Taylor, and, C. Kang, (2002) Crystal structure of a DNA decamer containing a cis-syn thymine dimer. Proc. Natl Acad. Sci. 99, 15965-15970.
173. Taylor, J. S., D. S. Garrett, I. R. Brockie, D. L. Svoboda, and, J. Telser, (1990) Proton NMR assignment and melting temperature study of cis-syn and trans-syn thymine dimer containing duplexes of d(CGTATTATGC)•d(GCATAATACG). Biochemistry 29, 8858-8866.
174. McAteer, K., Y. Ji ng, J. Kao, J. S. Taylor, and, M. A. Kennedy, (1998) Solution-state structure of a DNA dodecamer duplex containing a cis-syn thymine cyclobutane dimer, the major UV photoproduct of DNA. J. Mol. Biol. 282, 1013-1032.
175. Yokoyama, H., R. Mizutani, and, Y. Satow, (2013) Structure of a double-stranded DNA (6-4) photoproduct in complex with the 64M-5 antibody Fab. Acta Crystallogr. D 69, 504-512.
176. Maul, M., T. M. Barends, A. F. Glas, M. Cryle, T. Domratcheva, S. Schneider, I. Schlichting, and, T. Carell, (2008) Crystal structure and mechanism of a DNA (6-4) photolyase. Angew. Chem. Int. Ed. 47, 10076-10080.
177. Scrima, A., R. Konickova, B. K. Czyzewski, Y. Kawasaki, P. D. Jeffrey, R. Groisman, Y. Nakatani, S. Iwai, N. P. Pavletich, and, N. H. Thoma, (2008) Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 135, 1213-1223.
178. Jong-Ki Kim, R., and, C. Byong-Seok, (1995) The solution structure of DNA duplex-decamer containing the (6-4) photoproduct of thymidylyl (3′→5′)thymidine by NMR and relaxation matrix refinement. Eur. J. Biochem. 228, 849-854.
179. Lee, J.-H., G.-S. Hwang, and, B.-S. Choi, (1999) Solution structure of a DNA decamer duplex containing the stable 3′ T•G base pair of the pyrimidine(6-4)pyrimidone photoproduct [(6-4) adduct]: Implications for the highly specific 3′ T → C transition of the (6-4) adduct. Proc. Natl Acad. Sci. 96, 6632-6636.
180. Lukin, M., and, C. de los Santos, (2006) NMR structures of damaged DNA. Chem. Rev. 106, 607-686.
181. Young, A. R., C. A. Chadwick, G. I. Harrison, J. L. M. Hawk, O. Nikaido, and, C. S. Potten, (1996) The in situ repair kinetics of epidermal thymine dimers and 6-4 photoproducts in human skin types I and II. J. Investig. Dermatol. 106, 1307-1313.
182. de Laat, W. L., N. G. J. Jaspers, and, J. H. J. Hoeijmakers, (1999) Molecular mechanism of nucleotide excision repair. Genes Dev. 13, 768-785.
183. de Boer, J., and, J. H. J. Hoeijmakers, (2000) Nucleotide excision repair and human syndromes. Carcinogenesis 21, 453-460.
184. Jans, J., W. Schul, Y.-G. Sert, Y. Rijksen, H. Rebel, A. P. M. Eker, S. Nakajima, H. van Steeg, F. R. de Gruijl, A. Yasui, J. H. J. Hoeijmakers, and, G. T. J. van der Horst, (2005) Powerful skin cancer protection by a CPD-photolyase transgene. Curr. Biol. 15, 105-115.
185. Yoon, J.-H., L. Prakash, and, S. Prakash, (2009) Highly error-free role of DNA polymerase η in the replicative bypass of UV-induced pyrimidine dimers in mouse and human cells. Proc. Natl Acad. Sci. 106, 18219-18224.
186. Taggart, D. J., T. L. Camerlengo, J. K. Harrison, S. M. Sherrer, A. K. Kshetry, J.-S. Taylor, K. Huang, and, Z. Suo, (2013) A high-throughput and quantitative method to assess the mutagenic potential of translesion DNA synthesis. Nucleic Acids Res. 41, e96.
187. Johnson, R. E., L. Haracska, S. Prakash, and, L. Prakash, (2001) Role of DNA polymerase η in the bypass of a (6-4) TT photoproduct. Mol. Cell. Biol. 21, 3558-3563.
188. Muñoz-Sánchez, J., and, E. Cabrera-Juárez, (1991) In vitro mutation of Haemophilus influenzae transforming deoxyribonucleic acid by ultraviolet radiation at -70C. Mutat. Res.-Fund. Mol. M. 251, 21-29.
189. Lin, G., Y. Jian, K. J. Dria, E. C. Long, and, L. Li, (2014) Reactivity of damaged pyrimidines: DNA cleavage via hemiaminal formation at the C4 positions of the saturated thymine of spore photoproduct and dihydrouridine. J. Am. Chem. Soc. 136, 12938-12946.
190. Cano, R. J., and, M. K. Borucki, (1995) Revival and identification of bacterial spores in 25- to 40-million-year-old Dominican amber. Science 268, 1060-1064.
191. Vreeland, R. H., W. D. Rosenzweig, and, D. W. Powers, (2000) Isolation of a 250 million-year-old halotolerant bacterium from a primary salt crystal. Nature 407, 897-900.
192. Kennedy, M. J., S. L. Reader, and, L. M. Swierczynski, (1994) Preservation records of micro-organisms: Evidence of the tenacity of life. Microbiology 140 (Pt 10), 2513-2529.
193. Cadet, J., A. Grand, and, T. Douki, (2015) Solar UV radiation-induced DNA bipyrimidine photoproducts: Formation and mechanistic insights. In Photoinduced Phenomena in Nucleic Acids II, Vol. 356. (Edited by, M. Barbatti, A. C. Borin, and, S. Ullrich,), pp. 249-275. Springer International Publishing, Switzerland.
194. Hieda, K., (1971) Effects of dehydration on the sensitivity of yeast to ultraviolet light. Mutat. Res.-Fund. Mol. M. 12, 365-380.
195. Hieda, K., (1981) Induction of genetic changes in Saccharomyces cerevisiae by partial drying in air of constant relative humidity and by UV. Mutat. Res. 84, 17-27.
196. Ashwood-Smith, M. J., B. A. Bridges, and, R. J. Munson, (1965) Ultraviolet damage to bacteria and bacteriophage at low temperatures. Science 149, 1103-1105.
197. Hieda, K., and, T. Ito, (1968) The enhancement of UV sensitivity of yeast in frozen state. Mutat. Res. 6, 325-327.
198. DiMaio, F., X. Yu, E. Rensen, M. Krupovic, D. Prangishvili, and, E. H. Egelman, (2015) A virus that infects a hyperthermophile encapsidates A-form DNA. Science 348, 914-917.
199. Mori, T., T. Matsunaga, T. Hirose, and, O. Nikaido, (1988) Establishment of a monoclonal antibody recognizing ultraviolet light-induced (6-4) photoproducts. Mutat. Res. 194, 263-270.
200. Mori, T., M. Nakane, T. Hattori, T. Matsunaga, M. Ihara, and, O. Nikaido, (1991) Simultaneous establishment of monoclonal antibodies specific for either cyclobutane pyrimidine dimer or (6-4) photoproduct from the same mouse immunized with ultraviolet-irradiated DNA. Photochem. Photobiol. 54, 225-232.
201. Strickland, P. T., and, J. M. Boyle, (1981) Characterisation of two monoclonal antibodies specific for dimerised and non-dimerised adjacent thymidines in single stranded DNA. Photochem. Photobiol. 34, 595-601.
202. Strickland, P. T., O. Nikaido, T. Matsunaga, and, J. M. Boyle, (1992) Further characterization of monoclonal antibody indicates specificity for (6-4)-dipyrimidine photoproducts. Photochem. Photobiol. 55, 723-727.
203. Prescott, L. M., J. P. Harley, and, D. A. Klein, (2005) Microbiology. McGraw-Hill Higher Education, Dubuque, IA.