Molecular basis for <scp>GTP</scp> recognition by light‐activated guanylate cyclase Rh<scp>GC</scp>

Butryn, A.; Raza, Hadeeqa; Rada, Heather; Moraes, Isabel; Owens, Raymond J.; Orville, Allen M.

doi:10.1111/febs.15167

Cited by 11 publications

(15 citation statements)

References 56 publications

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“…Previous studies demonstrated that the N-terminus plays a crucial role for the catalytic activity of RGCs, and both C-terminal and N-terminal GC interactions have been proposed ( Scheib et al, 2018 ; Butryn et al, 2020 ). Therefore, we analyzed different truncations to elucidate potential structure rearrangements in the linker and N-terminal region during photoactivation.…”

Section: Resultsmentioning

confidence: 99%

“…In vitro studies confirmed its function as a photoactivated guanylyl cyclase that is inactive in the dark and fully active when illuminated with green light ( Scheib et al, 2015 ). More functional details are available from the orthologous protein of the related fungus Catenaria anguillulae ( Ca RGC) including the crystal structure of the constitutively active isolated cyclase domain ( Scheib et al, 2018 ; Butryn et al, 2020 ). The results show the photoreceptor to assemble as a homodimer, with the rhodopsin modules responsible to silence the cyclase activity in darkness.…”

Section: Introductionmentioning

confidence: 99%

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The inner mechanics of rhodopsin guanylyl cyclase during cGMP-formation revealed by real-time FTIR spectroscopy

Fischer

Mukherjee

Peter

et al. 2021

eLife

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Enzymerhodopsins represent a recently discovered class of rhodopsins which includes histidine kinase rhodopsin, rhodopsin phosphodiesterases and rhodopsin guanylyl cyclases (RGCs). The regulatory influence of the rhodopsin domain on the enzyme activity is only partially understood and holds the key for a deeper understanding of intra-molecular signaling pathways. Here we present a UV-Vis and FTIR study about the light-induced dynamics of a RGC from the fungus Catenaria anguillulae, which provides insights into the catalytic process. After the spectroscopic characterization of the late rhodopsin photoproducts, we analyzed truncated variants and revealed the involvement of the cytosolic N-terminus in the structural rearrangements upon photo-activation of the protein. We tracked the catalytic reaction of RGC and the free GC domain independently by UV-light induced release of GTP from the photolabile NPE-GTP substrate. Our results show substrate binding to the dark-adapted RGC and GC alike and reveal differences between the constructs attributable to the regulatory influence of the rhodopsin on the conformation of the binding pocket. By monitoring the phosphate rearrangement during cGMP and pyrophosphate formation in light-activated RGC, we were able to confirm the M state as the active state of the protein. The described setup and experimental design enable real-time monitoring of substrate turnover in light-activated enzymes on a molecular scale, thus opening the pathway to a deeper understanding of enzyme activity and protein-protein interactions.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The inner mechanics of rhodopsin guanylyl cyclase during cGMP-formation revealed by real-time FTIR spectroscopy

Fischer

Mukherjee

Peter

et al. 2021

eLife

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“…The rhodopsins consisting of seven transmembrane α-helices belong to the vast family of G protein-coupled receptors [ 324 , 368 ]. The light-induced isomerisation of the 11-cis-retinal is coupled to a cascade of events that relay the signal to guanylate kinases [ 369 , 370 ] or phosphodiesterase [ 371 ] that trigger various intracellular responses. The PYP adopt the fold of the Per-ARNT-Sim (PAS) domain [ 372 , 373 ] that senses a vast range of stimuli, from photon to ligand [ 374 ].…”

Section: Cell Signalling and Sensory Motricitymentioning

confidence: 99%

Towards the Idea of Molecular Brains

Timsit

Sergeant-Perthuis

2021

IJMS

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How can single cells without nervous systems perform complex behaviours such as habituation, associative learning and decision making, which are considered the hallmark of animals with a brain? Are there molecular systems that underlie cognitive properties equivalent to those of the brain? This review follows the development of the idea of molecular brains from Darwin’s “root brain hypothesis”, through bacterial chemotaxis, to the recent discovery of neuron-like r-protein networks in the ribosome. By combining a structural biology view with a Bayesian brain approach, this review explores the evolutionary labyrinth of information processing systems across scales. Ribosomal protein networks open a window into what were probably the earliest signalling systems to emerge before the radiation of the three kingdoms. While ribosomal networks are characterised by long-lasting interactions between their protein nodes, cell signalling networks are essentially based on transient interactions. As a corollary, while signals propagated in persistent networks may be ephemeral, networks whose interactions are transient constrain signals diffusing into the cytoplasm to be durable in time, such as post-translational modifications of proteins or second messenger synthesis. The duration and nature of the signals, in turn, implies different mechanisms for the integration of multiple signals and decision making. Evolution then reinvented networks with persistent interactions with the development of nervous systems in metazoans. Ribosomal protein networks and simple nervous systems display architectural and functional analogies whose comparison could suggest scale invariance in information processing. At the molecular level, the significant complexification of eukaryotic ribosomal protein networks is associated with a burst in the acquisition of new conserved aromatic amino acids. Knowing that aromatic residues play a critical role in allosteric receptors and channels, this observation suggests a general role of π systems and their interactions with charged amino acids in multiple signal integration and information processing. We think that these findings may provide the molecular basis for designing future computers with organic processors.

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“…Rhodopsin consisting of seven trans-membrane α-helices belongs to the vast family of G-protein-coupled receptors [ 99 , 100 , 101 , 102 , 103 , 104 , 105 ]. The light inducing isomerization of the 11-cis-retinal is coupled to a cascade of events that ultimately acts as a switch to relay the signal to G-proteins [ 106 , 107 ], guanylate kinases [ 101 , 108 ] or phosphodiesterase [ 102 ] that triggers various intracellular responses. Sensory rhodopsins that are responsible for light signalling and photo-behaviours have been found in archaea and bacteria [ 109 , 110 , 111 , 112 ].…”

Section: Introductionmentioning

confidence: 99%

Bioluminescence and Photoreception in Unicellular Organisms: Light-Signalling in a Bio-Communication Perspective

Timsit

Lescot

Valiadi

et al. 2021

IJMS

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Bioluminescence, the emission of light catalysed by luciferases, has evolved in many taxa from bacteria to vertebrates and is predominant in the marine environment. It is now well established that in animals possessing a nervous system capable of integrating light stimuli, bioluminescence triggers various behavioural responses and plays a role in intra- or interspecific visual communication. The function of light emission in unicellular organisms is less clear and it is currently thought that it has evolved in an ecological framework, to be perceived by visual animals. For example, while it is thought that bioluminescence allows bacteria to be ingested by zooplankton or fish, providing them with favourable conditions for growth and dispersal, the luminous flashes emitted by dinoflagellates may have evolved as an anti-predation system against copepods. In this short review, we re-examine this paradigm in light of recent findings in microorganism photoreception, signal integration and complex behaviours. Numerous studies show that on the one hand, bacteria and protists, whether autotrophs or heterotrophs, possess a variety of photoreceptors capable of perceiving and integrating light stimuli of different wavelengths. Single-cell light-perception produces responses ranging from phototaxis to more complex behaviours. On the other hand, there is growing evidence that unicellular prokaryotes and eukaryotes can perform complex tasks ranging from habituation and decision-making to associative learning, despite lacking a nervous system. Here, we focus our analysis on two taxa, bacteria and dinoflagellates, whose bioluminescence is well studied. We propose the hypothesis that similar to visual animals, the interplay between light-emission and reception could play multiple roles in intra- and interspecific communication and participate in complex behaviour in the unicellular world.

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Molecular basis for GTP recognition by light‐activated guanylate cyclase RhGC

Cited by 11 publications

References 56 publications

The inner mechanics of rhodopsin guanylyl cyclase during cGMP-formation revealed by real-time FTIR spectroscopy

The inner mechanics of rhodopsin guanylyl cyclase during cGMP-formation revealed by real-time FTIR spectroscopy

Towards the Idea of Molecular Brains

Bioluminescence and Photoreception in Unicellular Organisms: Light-Signalling in a Bio-Communication Perspective

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