Wounding stress causes rapid increase in concentration of the naturally occurring 2′,3′-isomers of cyclic guanosine- and cyclic adenosine monophosphate (cGMP and cAMP) in plant tissues

Damme, Thomas Van; Blancquaert, Dieter; Couturon, Pauline; Straeten, Dominique Van Der; Sandra, Patrick; Lynen, Frédéric

doi:10.1016/j.phytochem.2014.03.013

Cited by 56 publications

(48 citation statements)

References 62 publications

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“…The production of 29,39-cAMP as well as other nucleoside 29,39-cyclic monophosphates by living tissues has been corroborated by multiple independent laboratories. [26][27][28][29][30][31] Our hypothesis that injury increases 29,39-cAMP production also has received confirmation. For example, brain trauma in mice increases brain interstitial levels of 29,39-cAMP, and 29,39-cAMP is elevated in cerebrospinal fluid of humans in the early hours after traumatic brain injury.…”

Section: Discussionmentioning

confidence: 82%

Renal 2′,3′-Cyclic Nucleotide 3′-Phosphodiesterase Is an Important Determinant of AKI Severity after Ischemia-Reperfusion

Jackson

Menshikova

et al. 2015

JASN

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A positional isomer of 39,59-cAMP, 29,39-cAMP, is produced by kidneys in response to energy depletion, and renal 29,39-cyclic nucleotide 39-phosphodiesterase (CNPase) metabolizes 29,39-cAMP to 29-AMP; 29,39-cAMP is a potent opener of mitochondrial permeability transition pores (mPTPs), which can stimulate autophagy. Because autophagy protects against AKI, it is conceivable that inhibition of CNPase protects against ischemia-reperfusion (IR) -induced AKI. Therefore, we investigated renal outcomes, mitochondrial function, number, area, and autophagy in CNPase-knockout (CNPase 2/2 ) versus wild-type (WT) mice using a unique two-kidney, hanging-weight model of renal bilateral IR (20 minutes of ischemia followed by 48 hours of reperfusion). Analysis of urinary purines showed attenuated metabolism of 29,39-cAMP to 29-AMP in CNPase 2/2 mice. Neither genotype nor IR affected BP, heart rate, urine volume, or albumin excretion. In WT mice, renal IR reduced 14 C-inulin clearance (index of GFR) and increased renal vascular resistance (measured by transit time nanoprobes) and urinary excretion of kidney injury molecule-1 and neutrophil gelatinase-associated lipocalin. IR did not affect these parameters in CNPase 2/2 mice. Histologic analysis revealed that IR induced severe damage in kidneys from WT mice, whereas histologic changes were minimal after IR in CNPase 2/2 mice. Measurements of renal cardiolipin levels, citrate synthase activity, rotenone-sensitive NADH oxidase activity, and proximal tubular mitochondrial and autophagosome area and number (by transmission electron microscopy) indicted accelerated autophagy/ mitophagy in injured CNPase 2/2 mice. We conclude that CNPase deletion attenuates IR-induced AKI, in part by accelerating autophagy with targeted removal of damaged mitochondria. In response to energy depletion, rat 1,2 and mouse 3 kidneys produce 29,39-cAMP, a positional isomer of 39,59-cAMP that is generated when mRNA is enzymatically degraded. 2 A study by Azarashvili et al. 4 shows that 29,39-cAMP is a potent opener of mitochondrial permeability transition pores (mPTPs).Opening of mPTPs causes mitochondria damage, 5 and mitochondrial damage is a stimulus for autophagy. [6][7][8] Renal autophagy protects against AKI, [9][10][11][12][13][14][15][16] and insufficient autophagy contributes to organ failure. 17 Therefore, it is conceivable that 29,39-cAMP, by increasing autophagy, protects against AKI. Our recent studies identify 29,39-cyclic nucleotide 39-phosphodiesterase (CNPase) as an important enzyme mediating the renal metabolism of

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Section: Discussionmentioning

confidence: 82%

Renal 2′,3′-Cyclic Nucleotide 3′-Phosphodiesterase Is an Important Determinant of AKI Severity after Ischemia-Reperfusion

Jackson

Menshikova

et al. 2015

JASN

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“…As a consequence of a generally disturbed cell homeostasis, a prompt response to alleviate the impact of stress is necessary. Major players of this early phase of defence response are signalling molecules, including secondary messengers such as calcium ions (Ca 2+ ) or cyclic nucleotides (cNMP; Gao et al ., ; Van Damme et al ., ; Hussain et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Genetic buffering of cyclic AMP in Arabidopsis thaliana compromises the plant immune response triggered by an avirulent strain of Pseudomonas syringae pv. tomato

et al. 2019

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Cyclic AMP plays important roles in different physiological processes, including plant defence responses. However, as little information is known on plant enzymes responsible for cAMP production/degradation, studies of cAMP functions have relied, to date, on non-specific pharmacological approaches. We therefore developed a more reliable approach, producing transgenic Arabidopsis thaliana lines overexpressing the 'cAMP-sponge' (cAS), a genetic tool that specifically buffers cAMP levels. In response to an avirulent strain of Pseudomonas syringae pv. tomato (PstAvrB), cAS plants showed a higher bacterial growth and a reduced hypersensitive cell death in comparison with wild-type (WT) plants. The low cAMP availability after pathogen infection delayed cytosolic calcium elevation, as well as hydrogen peroxide increase and induction of redox systems. The proteomic analysis, performed 24 h post-infection, indicated that a core of 49 proteins was modulated in both genotypes, while 16 and 42 proteins were uniquely modulated in WT and cAS lines, respectively. The involvement of these proteins in the impairment of defence response in cAS plants is discussed in this paper. Moreover, in silico analysis revealed that the promoter regions of the genes coding for proteins uniquely accumulating in WT plants shared the CGCG motif, a target of the calcium-calmodulinbinding transcription factor AtSR1 (Arabidopsis thaliana signal responsive1). Therefore, following pathogen perception, the low free cAMP content, altering timing and levels of defence signals, and likely acting in part through the mis-regulation of AtSR1 activity, affected the speed and strength of the immune response. Role of cAMP in plant immune response 597Generation of Arabidopsis cAS-mCherry plants expressing the NES-YC3.6 probeThe Arabidopsis Col-0 cAS-transgenic lines were crossed with the Col-0 pUBQ10-NES-YC3.6 line reported in Krebs et al. (2012). Seeds from cross-pollinated flowers were surface sterilized by vapour-

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“…1 B ). Two forms of cAMP have been detected in cells, 3′,5′-cAMP, the classic signaling nucleotide, and 2′,3′-cAMP, suggested to be a nucleotide intermediate formed during the RNA degradation process (22, 23). As revealed by competitive binding assays, only the classic signaling molecule 3′,5′-cAMP but not 2′,3′-cAMP could prevent the binding of radiolabeled 3′,5′-cAMP to TrmD SA (Fig.…”

Section: Resultsmentioning

confidence: 99%

Evolutionary Adaptation of the Essential tRNA Methyltransferase TrmD to the Signaling Molecule 3′,5′-cAMP in Bacteria

Zhang

Agrebi

Bellows

et al. 2017

Journal of Biological Chemistry

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The nucleotide signaling molecule 3′,5′-cyclic adenosine monophosphate (3′,5′-cAMP) plays important physiological roles, ranging from carbon catabolite repression in bacteria to mediating the action of hormones in higher eukaryotes, including human. However, it remains unclear whether 3′,5′-cAMP is universally present in the Firmicutes group of bacteria. We hypothesized that searching for proteins that bind 3′,5′-cAMP might provide new insight into this question. Accordingly, we performed a genome-wide screen and identified the essential Staphylococcus aureus tRNA m1G37 methyltransferase enzyme TrmD, which is conserved in all three domains of life as a tight 3′,5′-cAMP-binding protein. TrmD enzymes are known to use S-adenosyl-l-methionine (AdoMet) as substrate; we have shown that 3′,5′-cAMP binds competitively with AdoMet to the S. aureus TrmD protein, indicating an overlapping binding site. However, the physiological relevance of this discovery remained unclear, as we were unable to identify a functional adenylate cyclase in S. aureus and only detected 2′,3′-cAMP but not 3′,5′-cAMP in cellular extracts. Interestingly, TrmD proteins from Escherichia coli and Mycobacterium tuberculosis, organisms known to synthesize 3′,5′-cAMP, did not bind this signaling nucleotide. Comparative bioinformatics, mutagenesis, and biochemical analyses revealed that the highly conserved Tyr-86 residue in E. coli TrmD is essential to discriminate between 3′,5′-cAMP and the native substrate AdoMet. Combined with a phylogenetic analysis, these results suggest that amino acids in the substrate binding pocket of TrmD underwent an adaptive evolution to accommodate the emergence of adenylate cyclases and thus the signaling molecule 3′,5′-cAMP. Altogether this further indicates that S. aureus does not produce 3′,5′-cAMP, which would otherwise competitively inhibit an essential enzyme.

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Wounding stress causes rapid increase in concentration of the naturally occurring 2′,3′-isomers of cyclic guanosine- and cyclic adenosine monophosphate (cGMP and cAMP) in plant tissues

Cited by 56 publications

References 62 publications

Renal 2′,3′-Cyclic Nucleotide 3′-Phosphodiesterase Is an Important Determinant of AKI Severity after Ischemia-Reperfusion

Renal 2′,3′-Cyclic Nucleotide 3′-Phosphodiesterase Is an Important Determinant of AKI Severity after Ischemia-Reperfusion

Genetic buffering of cyclic AMP in Arabidopsis thaliana compromises the plant immune response triggered by an avirulent strain of Pseudomonas syringae pv. tomato

Evolutionary Adaptation of the Essential tRNA Methyltransferase TrmD to the Signaling Molecule 3′,5′-cAMP in Bacteria

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