Why is CarH photolytically active in comparison to other B12-dependent enzymes?

doi:10.1016/j.jphotobiol.2020.111919

Journal of Photochemistry and Photobiology B: Biology

Volume 209, August 2020, 111919

https://doi.org/10.1016/j.jphotobiol.2020.111919 Get rights and content

Highlights

•
The Co-C_5' bond of coenzyme-B₁₂ in CarH is cleaved by light.
•
Photo-cleavage of the Co-C_5' bond is a key step in CarH's mechanism of action.
•
The S₁ PES of CarH has similar features to other B₁₂-dependent enzymes.
•
CarH alters the stereochemistry of the Ado ligand to facilitate photoproduct formation.
•
CarH is photolytically active due to the dual role of AdoCbl.

Abstract

The discovery of naturally occurring B₁₂-depedent photoreceptors has allowed for applications of cobalamins (Cbls) in optogenetics and synthetic biology to emerge. However, theoretical investigations of the complex mechanisms of these systems have been lacking. Adenosylcobalamin (AdoCbl)-dependent photoreceptor, CarH, is one example and it relies on daylight to perform its catalytic function. Typically, in enzymes employing AdoCbl as their cofactor, the Co-C_5′ bond activation and cleavage is triggered by substrate binding. The cleavage of the Co-C_5′ bond is homolytic resulting in radical pair formation. However, in CarH, this bond is instead activated by light. To explore this peculiarity, the ground and first excited state potential energy surfaces (PESs) were constructed using the quantum mechanics/molecular mechanics (QM/MM) framework and compared with other AdoCbl-dependent enzymes. QM/MM results indicate that CarH is photolytically active as a result of the AdoCbl dual role, acting as a radical generator and as a substrate. Photo-cleavage of the Co-C_5′ bond and subsequent H-atom abstraction is possible because of the specific orientation of the H-C_4′ bond with respect to the Co(II) center. Comparison with other AdoCbl-dependent enzymes indicate that the protein environment in the CarH active center alters the photochemistry of AdoCbl by controlling the stereochemistry of the ribose moiety.

Graphical abstract

Introduction

While the light sensitivity of the cobalt‑carbon (Co-C_5′) bond in coenzyme B₁₂ (AdoCbl = adenosylcobalamin, Fig. 1) has been known for nearly five decades, only until recently has this been associated with light controlled reactivity, namely optogenetic regulation and light-activated drug delivery [1,2]. In particular, the CarH photoreceptor, uses AdoCbl as a photoactive cofactor capable of inducing significant structural changes of the photoreceptor's protein chains to regulate DNA transcription [[3], [4], [5]]. Coenzyme B₁₂ contains a Co(III) ion that is equatorially coordinated to four nitrogens of a corrin ring and perpendicularly to upper and lower ligands. The upper ligand is variable and used to distinguish Cbls from one another in B₁₂ nomenclature [6]. In CarH, the upper axial ligand is a 5′-deoxy-5'adenosyl (Ado, Fig. 1) and is covalently bound to the Co via the C_5′ of the ribose moiety. The photolytic scission of the Co-C_5′ bond of AdoCbl is a key feature of CarH's mechanism of action [7,8]. In B₁₂-dependent enzymes, the lower ligand is the dimethylbenzimidazole (DBI) base from the nucleotide loop or a histidine (His) residue [6,9,10]. In the CarH photoreceptor, the DBI base is replaced with His177, forming the base-off/His-on conformation of the cofactor [5].

The CarH photoreceptor regulates DNA transcription in bacteria which results in the expression of genes responsible for biosynthesis of carotenoids [[3], [4], [5]]. This involves significant structural changes to the photoreceptor as well as local, molecular level processes in the Cbl binding domain. The overall mode of action for CarH is depicted in Fig. 2. In the dark, CarH-DS (DS = Dark State), forms a tetramer upon AdoCbl binding. Transcription of carotenoid biosynthetic genes is repressed in the absence of daylight, where CarH-DS binds to DNA. In the presence of light, the Co-C_5′ bond is ruptured, and the Ado ligand is converted to the photoproduct, 4′,5′-anhydroadenosine [7]. As a result, His132 will take the place of the Ado ligand, forming a stable adduct with the cofactor [4]. This photoinitiated process induces a large scale structural change in the protein's conformation and the tetramer dissociates into monomers forming CarH-LS (LS = Light State). In CarH-LS, the cofactor retains His132 and His177 as upper and lower axial ligands, respectively, and this is denoted as bis-HisCbl [5]. Ultimately, this cascade of events initiates the transcription of carotenoid biosynthetic genes.

Although the ‘big picture’ mode of action for CarH seems to be generally understood, there are many issues and questions about the photo-catalytic mechanism that have not been explored to date. One important question has arisen: “how is the Co-C_5′ bond activated and cleaved in CarH-DS?” This seemingly simple question has in fact been quite perplexing because AdoCbl is known for its radical chemistry and, in terms of photochemistry, the cleavage of the Co-C_5′ bond of AdoCbl is homolytic [6,9,[11], [12], [13], [14], [15]]. It came as quite a surprise that a proposed mechanism for CarH, implicated heterolytic cleavage of the Co-C_5′ bond over homolytic cleavage [8].

Even more intriguing is a second question: “what specifically makes CarH photolytically active in comparison to other AdoCbl-dependent enzymes?” Photolytic properties of AdoCbl-dependent enzymes, including glutamate mutase (GLM) and ethanolamine ammonia-lyase (EAL), have been thoroughly investigated both experimentally [[16], [17], [18], [19], [20]] and computationally [[21], [22], [23]]. It was found that photo-cleavage of the Co-C_5′ in GLM and EAL enzymes is suppressed and only a small portion of the Co-C_5′ bonds undergoes photodissociation. In stark contrast to CarH, excited state dynamics and photolytic studies of GLM and EAL have revealed that these enzymes were essentially photostable. Intuitively, it is reasonable to suppose that there must be some aspect at the molecular level that is responsible for the different photo-reactivities of these enzymes especially considering that coenzyme B₁₂ is utilized in each system mentioned above.

The purpose of this study is to answer these two questions. Quantum mechanics/molecular mechanics (QM/MM) calculations were employed to probe the photolytic properties of CarH-DS and to determine what structural features of the AdoCbl cofactor contribute to these properties. When comparing the excited state properties, exemplified by the S₁ state potential energy surface (PES), of CarH to the previously studied GLM and EAL, there are not any major differences. However, based on theoretical insights, it is apparent that the conformation of the Ado group of the cofactor significantly contributes to CarH's efficiency as a photoreceptor. Present calculations do not indicate that the protein environment in the CarH active center alters the photochemistry of AdoCbl, rather it appears that CarH alters the stereochemistry of the ribose moiety to allow for its photolytic activity. This will undoubtedly have implications for elucidating the entire CarH mechanism at the molecular level and in analyses of other similar photoreceptors.

Section snippets

Activation and Photolytic Co-C_5′ Bond Cleavage

To understand how CarH operates at the molecular level it is paramount to analyze the PESs associated with the ground state (S₀) and the lowest electronically excited state (S₁). The S₁ state is particularly important because photocleavage of the Co-C_5′ bond and the subsequent radical pair (RP) formation occurs from here [1]. DFT/MM and TD-DFT/MM were employed for generating the S₀ and S₁ PESs, respectively. The S₀ and S₁ PESs were constructed as a function of axial bond lengths, Co-C_5′ and Co-N

Conclusions

Present QM/MM calculations clearly indicate that role of light in the mechanism of CarH-DS is simply to generate the Co(II)/Ado• RP, in a similar fashion that has been observed for EAL and GLM . This is evident based on the similar topologies of the S₁ PESs of CarH, EAL, and GLM. In addition, unlike some B₁₂-dependent enzymes like MetH, an energetically feasible route for photodissociation can be identified on the S₁ PES of CarH-DS. It is also apparent that AdoCbl plays a unique dual role in

Computational Methods

The CarH model used in the QM/MM calculations was generated from the crystal structure of Thermus thermophilus CarH-DS bound to DNA (PDB ID: 5C8E) [4]. The computational details for GLM and EAL are included in the SI. Additionally, SI Tables S1 and S2 summarize the differences in the crystal structures and model structures of CarH, GLM, and EAL. CarH-DS is a tetramer, more specifically, it is a dimer-of-dimers type tetramer. In this study, the primary focus is the molecular activity in the

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

The authors acknowledge the Cardinal Research Cluster (CRC) at the University of Louisville for providing access to high performance computing facilities.

References (52)

M.J. Toda et al.
Photolytic properties of the biologically active forms of vitamin B₁₂
Coord. Chem. Rev.
(2019)
S. Padmanabhan et al.
B₁₂-based photoreceptors: from structure and function to applications in optogenetics and synthetic biology
Curr. Opin. Struct. Biol.
(2019)
R. Banerjee
The yin-Yang of Cobalamin biochemistry
Chem. Biol.
(1997)
A.A. Mamun et al.
Can photolysis of the Co-C bond in coenzyme B₁₂-dependent enzymes be used to mimic the native reaction?
J. Photochem. Photobiol. B
(2019)
A.P. Ghosh et al.
Mechanism of the photo-induced activation of CoC bond in methylcobalamin-dependent methionine synthase
J. Photochem. Photobiol. B
(2018)
G.H. Reed
Radical mechanisms in Adenosylcobalamin-dependent enzymes
Curr. Opin. Chem. Biol.
(2004)
F. Weigend et al.
RI-MP2: optimized auxiliary basis sets and demonstration of efficiency
Chem. Phys. Lett.
(1998)
H.M. Marques et al.
Parameters for the amber force field for the molecular mechanics modeling of the cobalt corrinoids
J. Mol. Struct.
(2001)
J.M. Ortiz-Guerrero et al.
Light-dependent gene regulation by a coenzyme B₁₂-based photoreceptor
Proc. Natl. Acad. Sci.
(2011)
M. Jost et al.
Structural basis for gene regulation by a B₁₂-dependent photoreceptor
Nature
(2015)

S. Padmanabhan et al.

A new facet of vitamin B₁₂: gene regulation by Cobalamin-based photoreceptors

Annu. Rev. Biochem.

(2017)

D. Dolphin

B₁₂ volume 1: chemistry

(1982)

M. Jost et al.

The transcription factor CarH safeguards use of Adenosylcobalamin as a light sensor by altering the photolysis products

Biochemistry

(2015)

R.J. Kutta et al.

The photochemical mechanism of a B₁₂-dependent photoreceptor protein

Nat. Commun.

(2015)

R. Banerjee

Chemistry and Biochemistry of B₁₂

(1999)

R. Banerjee et al.

The many faces of vitamin B₁₂: catalysis by cobalamin-dependent enzymes

Annu. Rev. Biochem.

(2003)

L.A. Walker et al.

Time-resolved spectroscopic studies of B₁₂ coenzymes: the photolysis and geminate recombination of Adenosylcobalamin

J. Am. Chem. Soc.

(1998)

A.G. Cole et al.

Time-resolved spectroscopic studies of B₁₂ Coenzymes: a comparison of the primary photolysis mechanism in Methyl-,Ethyl-, n-Propyl-, and 5′-Deoxyadenosylcobalamin

J. Am. Chem. Soc.

(2001)

L.M. Yoder et al.

Time-resolved spectroscopic studies of B12 coenzymes: influence of solvent on the photolysis of Adenosylcobalamin

J. Phys.Chem. B

(2001)

E.N. Marsh et al.

Adenosyl radical: reagent and catalyst in enzyme reactions

ChemBiocChem

(2010)

R.J. Sension et al.

Photolysis and recombination of adenosylcobalamin bound to glutamate mutase

J. Am. Chem. Soc.

(2004)

R.J. Sension et al.

Time-resolved measurements of the photolysis and recombination of Adenosylcobalamin bound to glutamate mutase

J. Phys. Chem. B

(2005)

S.C. Ke et al.

Identification of Dimethylbenzimidazole axial coordination and characterization of (14)N Superhyperfine and nuclear Quadrupole coupling in cob(II)alamin bound to ethanolamine deaminase in a catalytically-engaged substrate radical-cobalt(II) Biradical state

Biochemistry

(1999)

W.D. Robertson et al.

Photolysis of Adenosylcobalamin and radical pair recombination in ethanolamine ammonia-lyase probed on the micro- to millisecond time scale by using time-resolved optical absorption spectroscopy

Biochemistry

(2009)

W.D. Robertson et al.

Characterization of protein contributions to cobalt-carbon bond cleavage catalysis in Adenosylcobalamin-dependent ethanolamine ammonia-lyase by using photolysis in the ternary complex

J. Am. Chem. Soc.

(2011)

A.A. Mamun et al.

Mechanism of light induced radical pair formation in coenzyme B12-dependent ethanolamine ammonia-Lyase

ACS Catal.

(2018)

Cited by (18)

Photoproduct formation in coenzyme B<inf>12</inf>-dependent CarH photoreceptor via a triplet pathway
2023, Journal of Photochemistry and Photobiology B: Biology
CarH is a cobalamin-based photoreceptor which has attracted significant interest due to its complex mechanism involving its organometallic coenzyme-B₁₂ chromophore. While several experimental and computational studies have sought to understand CarH's mechanism of action, there are still many aspects of the mechanism which remain unclear. While light is needed to activate the Co-C_5′ bond, it is not entirely clear whether reaction pathway involves singlet or triplet diradical states. A recent experimental study implicated triplet pathway and importance of intersystem crossing (ISC) as a viable mechanistic route for photoproduct formation in CarH. Herein, a combined quantum mechanics/molecular mechanics approach (QM/MM) was used to explore the involvement of triplet states in CarH. Two possibilities were explored. The first possibility involved photo-induced homolytic cleavage of the Co-C_5′ where the radical pair (RP) would deactivate to a triplet state (T₀) on the ground state potential energy surface (PES). However, a pathway for the formation of the photoproduct, 4′,5′-anhydroadenosine (anhAdo), on the triplet ground state PES was not energetically feasible. The second possibility involved exploring a manifold of low-lying triplet excited states computed using TD-DFT within the QM/MM framework. Viable crossings of triplet excited states with singlet excited states were identified using semiclassical Landau-Zener theory and the effectiveness of spin-orbit coupling by El-Sayed rules. Several candidates along both the Co-N_Im potential energy curve (PEC) and Co-C_5′/Co-N_Im PES were identified, which appear to corroborate experimental findings and implicate the possible role of triplet states in CarH.
Cobalt enzymes
2023, Comprehensive Inorganic Chemistry III, Third Edition
Cobalt enzymes come in two major categories: widespread B₁₂-dependent enzymes and lesser known non-corrin cobalt enzymes. We focus here on B₁₂-enzymes, which are grouped further in three classes according to the nature of their stable B₁₂-cofactor forms. Hence, these enzymes either use organometallic B₁₂-cofactors, adenosylcobamides (AdoCbas) or methylcobamides (MeCbas), or primarily redox-active cobamides, such as Co(II)cobamides (Cbas(II)). The AdoCbas catalyze enzymatic radical reactions with “difficult chemistry,” initiated by the reactive 5′-deoxy-5′-adenosyl radical from homolysis of their CoC bond; MeCbas help catalyze enzymatic methyl group transfer reactions, involving either nucleophilic or radical type reaction partners; “non-ligated” Cbas(II) are the typical redox-cofactor forms observed in enzymes dealing with dehalogenation and related reduction reactions. Additional “borderline” cobalt-enzymes are involved in AdoCba-dependent photo-regulatory processes, in B₁₂-processing and B₁₂-biosynthesis. The natural Cbas have evolved a rich spectrum of biological catalysis and regulation as the result of the special interplay of their helical, ring-contracted corrin ligand and the tightly bound cobalt-center. Clearly, enzyme catalysis with cobalt-corrins and other cobalt-centers has become indispensable in the evolved world, where cobalt-corrins play essential roles in most spheres of Life.
Photoproduct formation in coenzyme B<inf>12</inf>-dependent CarH via a singlet pathway
2022, Journal of Photochemistry and Photobiology B: Biology
Citation Excerpt :
Also, previous TD-DFT calculations revealed that RP generation occurs from the ligand field (LF) region of the S1 PES. Thus, in the case of CarH photoreceptor, the S1 PES can also be used as a tool to understand the mechanism of photodissociation and it is reasonable to expect that the S1 state of CarH-DS may play similar role in the photolytic processes as in other coenzyme B12-dependent enzymes [12,38,40–42]. The S1 state of CarH was previously explored based on QM/MM calculations and compared with the S1 states of other B12-dependent enzymes such as ethanolamine ammonia lyase (EAL), glutamate mutase (GLM), and methionine synthase (MetH) [12].
The CarH photoreceptor exploits of the light-sensing ability of coenzyme B₁₂ ( adenosylcobalamin = AdoCbl) to perform its catalytic function, which includes large-scale structural changes to regulate transcription. In daylight, transcription is activated in CarH via the photo-cleavage of the Co-C_5′ bond of coenzyme B₁₂. Subsequently, the photoproduct, 4′,5′-anhydroadenosine (anhAdo) is formed inducing dissociation of the CarH tetramer from DNA. Several experimental studies have proposed that hydridocoblamin (HCbl) may be formed in process with anhAdo. The photolytic cleavage of the Co-C_5′ bond of AdoCbl was previously investigated using photochemical techniques and the involvement of both singlet and triplet excited states were explored. Herein, QM/MM calculations were employed to probe (1) the photolytic processes which may involve singlet excited states, (2) the mechanism of anhAdo formation, and (3) whether HCbl is a viable intermediate in CarH. Time-dependent density functional theory (TD-DFT) calculations indicate that the mechanism of photodissociation of the Ado ligand involves the ligand field (LF) portion of the lowest singlet excited state (S₁) potential energy surface (PES). This is followed by deactivation to a point on the S₀ PES where the Co-C_5′ bond remains broken. This species corresponds to a singlet diradical intermediate. From this point, the PES for anhAdo formation was explored, using the Co-C_5′ and Co-C_4′ bond distances as active coordinates, and a local minimum representing anhAdo and HCbl formation was found. The transition state (TS) for the formation of the Co-H bond of HCbl was located and its identity was confirmed by a single imaginary frequency of i1592 cm⁻¹. Comparisons to experimental studies and the potential role of rotation around the N-glycosidic bond of the Ado ligand were discussed.
Bioorganometallic Chemistry of Vitamin B<inf>12</inf>-Derivatives
2022, Comprehensive Organometallic Chemistry IV: Volume 1-15
Vitamin B₁₂ is a complex cobalt-corrin whose organometallic chemistry and biological roles continue to pose remarkable puzzles. The discovery of coenzyme B₁₂ revealed organometallic processes to be metabolically relevant. Indeed, the biological roles the B₁₂-cofactor in humans and animals, as well as in many other forms of life are largely based on their organometallic chemistry. As only some microorganisms have the capacity to biosynthesize B₁₂-derivatives, the other B₁₂-dependent organisms need to acquire natural corrinoids and transform them into organometallic B₁₂-cofactors. This review delineates (i) the structural features of natural organometallic B₁₂-derivatives, (ii) their exceptional reactivity, (iii) their enzyme biochemistry, (iv) their gene regulatory roles and (v) structural B₁₂-mimics classified as antivitamins B₁₂, which are useful in the quest for a deeper understanding and the control of B₁₂-metabolism.
Vitamin B<inf>12</inf> photoreceptors
2022, Vitamins and Hormones
Photoreceptor proteins enable living organisms to sense light and transduce this signal into biochemical outputs to elicit appropriate cellular responses. Their light sensing is typically mediated by covalently or noncovalently bound molecules called chromophores, which absorb light of specific wavelengths and modulate protein structure and biological activity. Known photoreceptors have been classified into about ten families based on the chromophore and its associated photosensory domain in the protein. One widespread photoreceptor family uses coenzyme B₁₂ or 5′-deoxyadenosylcobalamin, a biological form of vitamin B₁₂, to sense ultraviolet, blue, or green light, and its discovery revealed both a new type of photoreceptor and a novel functional facet of this vitamin, best known as an enzyme cofactor. Large strides have been made in our understanding of how these B₁₂-based photoreceptors function, high-resolution structural descriptions of their functional states are available, as are details of their unusual photochemistry. Additionally, they have inspired notable applications in optogenetics/optobiochemistry and synthetic biology. Here, we provide an overview of what is currently known about these B₁₂-based photoreceptors, their discovery, distribution, molecular mechanism of action, and the structural and photochemical basis of how they orchestrate signal transduction and gene regulation, and how they have been used to engineer optogenetic control of protein activities in living cells.
Photolytic properties of B<inf>12</inf>-dependent enzymes: A theoretical perspective
2022, Vitamins and Hormones
The biologically active vitamin B₁₂ derivates, methylcobalamin (MeCbl) and adenosylcobalamin (AdoCbl), are ubiquitous organometallic cofactors. In addition to their key roles in enzymatic catalysis, B₁₂ cofactors have complex photolytic properties which have been the target of experimental and theoretical studies. With the recent discovery of B₁₂-dependent photoreceptors, there is an increased need to elucidate the underlying photochemical mechanisms of these systems. This book chapter summarizes the photolytic properties of MeCbl- and AdoCbl-dependent enzymes with particular emphasis on the effect of the environment of the cofactor on the excited state processes. These systems include isolated MeCbl and AdoCbl as well as the enzymes, ethanolamine ammonia-lyase (EAL), glutamate mutase (GLM), methionine synthase (MetH), and photoreceptor CarH. Central to determining the photodissociation mechanism of each system is the analysis of the lowest singlet excited state (S₁) potential energy surface (PES). Time-dependent density functional theory (TD-DFT), employing BP86/TZVPP, is widely used to construct such PESs. Regardless of the environment, the topology of the S₁ PES of AdoCbl or MeCbl is marked by characteristic features, namely the metal-to-ligand charge transfer (MLCT) and ligand field (LF) regions. Conversely, the relative energetics of these electronic states are affected by the environment. Applications and outlooks for Cbl photochemistry are also discussed.

View all citing articles on Scopus

View full text

Why is CarH photolytically active in comparison to other B12-dependent enzymes?

Highlights

Abstract

Graphical abstract

Introduction

Section snippets

Activation and Photolytic Co-C5′ Bond Cleavage

Conclusions

Computational Methods

Declaration of Competing Interest

Acknowledgements

Coord. Chem. Rev.

Curr. Opin. Struct. Biol.

Chem. Biol.

J. Photochem. Photobiol. B

J. Photochem. Photobiol. B

Curr. Opin. Chem. Biol.

Chem. Phys. Lett.

J. Mol. Struct.

Light-dependent gene regulation by a coenzyme B12-based photoreceptor

Proc. Natl. Acad. Sci.

Structural basis for gene regulation by a B12-dependent photoreceptor

Nature

A new facet of vitamin B12: gene regulation by Cobalamin-based photoreceptors

Annu. Rev. Biochem.

B12 volume 1: chemistry

The transcription factor CarH safeguards use of Adenosylcobalamin as a light sensor by altering the photolysis products

Biochemistry

The photochemical mechanism of a B12-dependent photoreceptor protein

Nat. Commun.

Chemistry and Biochemistry of B12

The many faces of vitamin B12: catalysis by cobalamin-dependent enzymes

Annu. Rev. Biochem.

Time-resolved spectroscopic studies of B12 coenzymes: the photolysis and geminate recombination of Adenosylcobalamin

J. Am. Chem. Soc.

Time-resolved spectroscopic studies of B12 Coenzymes: a comparison of the primary photolysis mechanism in Methyl-,Ethyl-, n-Propyl-, and 5′-Deoxyadenosylcobalamin

J. Am. Chem. Soc.

Time-resolved spectroscopic studies of B12 coenzymes: influence of solvent on the photolysis of Adenosylcobalamin

J. Phys.Chem. B

Adenosyl radical: reagent and catalyst in enzyme reactions

ChemBiocChem

Photolysis and recombination of adenosylcobalamin bound to glutamate mutase

J. Am. Chem. Soc.

Time-resolved measurements of the photolysis and recombination of Adenosylcobalamin bound to glutamate mutase

J. Phys. Chem. B

Identification of Dimethylbenzimidazole axial coordination and characterization of (14)N Superhyperfine and nuclear Quadrupole coupling in cob(II)alamin bound to ethanolamine deaminase in a catalytically-engaged substrate radical-cobalt(II) Biradical state

Biochemistry

Photolysis of Adenosylcobalamin and radical pair recombination in ethanolamine ammonia-lyase probed on the micro- to millisecond time scale by using time-resolved optical absorption spectroscopy

Biochemistry

Characterization of protein contributions to cobalt-carbon bond cleavage catalysis in Adenosylcobalamin-dependent ethanolamine ammonia-lyase by using photolysis in the ternary complex

J. Am. Chem. Soc.

Mechanism of light induced radical pair formation in coenzyme B12-dependent ethanolamine ammonia-Lyase

ACS Catal.

Why is CarH photolytically active in comparison to other B₁₂-dependent enzymes?

Activation and Photolytic Co-C_5′ Bond Cleavage

Light-dependent gene regulation by a coenzyme B₁₂-based photoreceptor

Structural basis for gene regulation by a B₁₂-dependent photoreceptor

A new facet of vitamin B₁₂: gene regulation by Cobalamin-based photoreceptors

B₁₂ volume 1: chemistry

The photochemical mechanism of a B₁₂-dependent photoreceptor protein

Chemistry and Biochemistry of B₁₂

The many faces of vitamin B₁₂: catalysis by cobalamin-dependent enzymes

Time-resolved spectroscopic studies of B₁₂ coenzymes: the photolysis and geminate recombination of Adenosylcobalamin

Time-resolved spectroscopic studies of B₁₂ Coenzymes: a comparison of the primary photolysis mechanism in Methyl-,Ethyl-, n-Propyl-, and 5′-Deoxyadenosylcobalamin