Effect of the cyclobutane cytidine dimer on the properties of Escherichia coli DNA photolyase

Anar K. Murphy, Margaret Tammaro, Frank Cortazar, Yvonne Gindt, Johannes Schelvis

Research output: Contribution to journalArticleResearchpeer-review

11 Citations (Scopus)

Abstract

Cyclobutane pyrimidine dimer (CPD) photolyases are structure specific DNA-repair enzymes that specialize in the repair of CPDs, the major photoproducts that are formed upon irradiation of DNA with ultraviolet light. The purified enzyme binds a flavin adenine dinucleotide (FAD), which is in the neutral radical semiquinone (FADḢ) form. The CPDs are repaired by a light-driven, electron transfer from the anionic hydroquinone (FADH -) singlet excited state to the CPD, which is followed by reductive cleavage of the cyclobutane ring and subsequent monomerization of the pyrimidine bases. CPDs formed between two adjacent thymidine bases (T<>T) are repaired with greater efficiency than those formed between two adjacent cytidine bases (C<>C). In this paper, we investigate the changes in Escherichia coli photolyase that are induced upon binding to DNA containing C<>C lesions using resonance Raman, UV-vis absorption, and transient absorption spectroscopies, spectroelectrochemistry, and computational chemistry. The binding of photolyase to a C<>C lesion modifies the energy levels of FADḢ, the rate of charge recombination between FADH and Trp 306 ̇, and protein-FADḢ interactions differently than binding to a T<>T lesion. However, the reduction potential of the FADH-/FADḢ couple is modified in the same way with both substrates. Our calculations show that the permanent electric dipole moment of C<>C is stronger (12.1 D) and oriented differently than that of T<>T (8.7 D). The possible role of the electric dipole moment of the CPD in modifying the physicochemical properties of photolyase as well as in affecting CPD repair will be discussed.

Original languageEnglish
Pages (from-to)15217-15226
Number of pages10
JournalJournal of Physical Chemistry B
Volume112
Issue number47
DOIs
StatePublished - 27 Nov 2008

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Deoxyribodipyrimidine Photo-Lyase
Cyclobutanes
Pyrimidine Dimers
cyclobutane
Cytidine
pyrimidines
Escherichia
Dimers
Escherichia coli
DNA
deoxyribonucleic acid
dimers
Electric dipole moments
lesions
electric moments
Repair
electric dipoles
Spectroelectrochemistry
enzymes
Computational chemistry

Cite this

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title = "Effect of the cyclobutane cytidine dimer on the properties of Escherichia coli DNA photolyase",
abstract = "Cyclobutane pyrimidine dimer (CPD) photolyases are structure specific DNA-repair enzymes that specialize in the repair of CPDs, the major photoproducts that are formed upon irradiation of DNA with ultraviolet light. The purified enzyme binds a flavin adenine dinucleotide (FAD), which is in the neutral radical semiquinone (FADḢ) form. The CPDs are repaired by a light-driven, electron transfer from the anionic hydroquinone (FADH -) singlet excited state to the CPD, which is followed by reductive cleavage of the cyclobutane ring and subsequent monomerization of the pyrimidine bases. CPDs formed between two adjacent thymidine bases (T<>T) are repaired with greater efficiency than those formed between two adjacent cytidine bases (C<>C). In this paper, we investigate the changes in Escherichia coli photolyase that are induced upon binding to DNA containing C<>C lesions using resonance Raman, UV-vis absorption, and transient absorption spectroscopies, spectroelectrochemistry, and computational chemistry. The binding of photolyase to a C<>C lesion modifies the energy levels of FADḢ, the rate of charge recombination between FADH and Trp 306 ̇, and protein-FADḢ interactions differently than binding to a T<>T lesion. However, the reduction potential of the FADH-/FADḢ couple is modified in the same way with both substrates. Our calculations show that the permanent electric dipole moment of C<>C is stronger (12.1 D) and oriented differently than that of T<>T (8.7 D). The possible role of the electric dipole moment of the CPD in modifying the physicochemical properties of photolyase as well as in affecting CPD repair will be discussed.",
author = "Murphy, {Anar K.} and Margaret Tammaro and Frank Cortazar and Yvonne Gindt and Johannes Schelvis",
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Effect of the cyclobutane cytidine dimer on the properties of Escherichia coli DNA photolyase. / Murphy, Anar K.; Tammaro, Margaret; Cortazar, Frank; Gindt, Yvonne; Schelvis, Johannes.

In: Journal of Physical Chemistry B, Vol. 112, No. 47, 27.11.2008, p. 15217-15226.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Effect of the cyclobutane cytidine dimer on the properties of Escherichia coli DNA photolyase

AU - Murphy, Anar K.

AU - Tammaro, Margaret

AU - Cortazar, Frank

AU - Gindt, Yvonne

AU - Schelvis, Johannes

PY - 2008/11/27

Y1 - 2008/11/27

N2 - Cyclobutane pyrimidine dimer (CPD) photolyases are structure specific DNA-repair enzymes that specialize in the repair of CPDs, the major photoproducts that are formed upon irradiation of DNA with ultraviolet light. The purified enzyme binds a flavin adenine dinucleotide (FAD), which is in the neutral radical semiquinone (FADḢ) form. The CPDs are repaired by a light-driven, electron transfer from the anionic hydroquinone (FADH -) singlet excited state to the CPD, which is followed by reductive cleavage of the cyclobutane ring and subsequent monomerization of the pyrimidine bases. CPDs formed between two adjacent thymidine bases (T<>T) are repaired with greater efficiency than those formed between two adjacent cytidine bases (C<>C). In this paper, we investigate the changes in Escherichia coli photolyase that are induced upon binding to DNA containing C<>C lesions using resonance Raman, UV-vis absorption, and transient absorption spectroscopies, spectroelectrochemistry, and computational chemistry. The binding of photolyase to a C<>C lesion modifies the energy levels of FADḢ, the rate of charge recombination between FADH and Trp 306 ̇, and protein-FADḢ interactions differently than binding to a T<>T lesion. However, the reduction potential of the FADH-/FADḢ couple is modified in the same way with both substrates. Our calculations show that the permanent electric dipole moment of C<>C is stronger (12.1 D) and oriented differently than that of T<>T (8.7 D). The possible role of the electric dipole moment of the CPD in modifying the physicochemical properties of photolyase as well as in affecting CPD repair will be discussed.

AB - Cyclobutane pyrimidine dimer (CPD) photolyases are structure specific DNA-repair enzymes that specialize in the repair of CPDs, the major photoproducts that are formed upon irradiation of DNA with ultraviolet light. The purified enzyme binds a flavin adenine dinucleotide (FAD), which is in the neutral radical semiquinone (FADḢ) form. The CPDs are repaired by a light-driven, electron transfer from the anionic hydroquinone (FADH -) singlet excited state to the CPD, which is followed by reductive cleavage of the cyclobutane ring and subsequent monomerization of the pyrimidine bases. CPDs formed between two adjacent thymidine bases (T<>T) are repaired with greater efficiency than those formed between two adjacent cytidine bases (C<>C). In this paper, we investigate the changes in Escherichia coli photolyase that are induced upon binding to DNA containing C<>C lesions using resonance Raman, UV-vis absorption, and transient absorption spectroscopies, spectroelectrochemistry, and computational chemistry. The binding of photolyase to a C<>C lesion modifies the energy levels of FADḢ, the rate of charge recombination between FADH and Trp 306 ̇, and protein-FADḢ interactions differently than binding to a T<>T lesion. However, the reduction potential of the FADH-/FADḢ couple is modified in the same way with both substrates. Our calculations show that the permanent electric dipole moment of C<>C is stronger (12.1 D) and oriented differently than that of T<>T (8.7 D). The possible role of the electric dipole moment of the CPD in modifying the physicochemical properties of photolyase as well as in affecting CPD repair will be discussed.

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U2 - 10.1021/jp806526y

DO - 10.1021/jp806526y

M3 - Article

VL - 112

SP - 15217

EP - 15226

JO - Journal of Physical Chemistry B

JF - Journal of Physical Chemistry B

SN - 1520-6106

IS - 47

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