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Article ; Online: Cholinergic blockade of neuroinflammation: from tissue to RNA regulators.

Zorbaz, Tamara / Madrer, Nimrod / Soreq, Hermona

Neuronal signaling

2022 Volume 6, Issue 1, Page(s) NS20210035

Abstract: Inflammatory stimuli and consequent pro-inflammatory immune responses may facilitate neurodegeneration and threaten survival following pathogen infection or trauma, but potential controllers preventing these risks are incompletely understood. Here, we ... ...

Abstract	Inflammatory stimuli and consequent pro-inflammatory immune responses may facilitate neurodegeneration and threaten survival following pathogen infection or trauma, but potential controllers preventing these risks are incompletely understood. Here, we argue that small RNA regulators of acetylcholine (ACh) signaling, including microRNAs (miRs) and transfer RNA fragments (tRFs) may tilt the balance between innate and adaptive immunity, avoid chronic inflammation and prevent the neuroinflammation-mediated exacerbation of many neurological diseases. While the restrictive permeability of the blood-brain barrier (BBB) protects the brain from peripheral immune events, this barrier can be disrupted by inflammation and is weakened with age. The consequently dysregulated balance between pro- and anti-inflammatory processes may modify the immune activities of brain microglia, astrocytes, perivascular macrophages, oligodendrocytes and dendritic cells, leading to neuronal damage. Notably, the vagus nerve mediates the peripheral cholinergic anti-inflammatory reflex and underlines the consistent control of body-brain inflammation by pro-inflammatory cytokines, which affect cholinergic functions; therefore, the disruption of this reflex can exacerbate cognitive impairments such as attention deficits and delirium. RNA regulators can contribute to re-balancing the cholinergic network and avoiding its chronic deterioration, and their activities may differ between men and women and/or wear off with age. This can lead to hypersensitivity of aged patients to inflammation and higher risks of neuroinflammation-driven cholinergic impairments such as delirium and dementia following COVID-19 infection. The age- and sex-driven differences in post-transcriptional RNA regulators of cholinergic elements may hence indicate new personalized therapeutic options for neuroinflammatory diseases.
Language	English
Publishing date	2022-02-11
Publishing country	England
Document type	Journal Article ; Review
ISSN	2059-6553
ISSN (online)	2059-6553
DOI	10.1042/NS20210035
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Article ; Online: Cytotoxicity-related effects of imidazolium and chlorinated bispyridinium oximes in SH-SY5Y cells.

Zandona, Antonio / Zorbaz, Tamara / Miš, Katarina / Pirkmajer, Sergej / Katalinić, Maja

Arhiv za higijenu rada i toksikologiju

2022 Volume 73, Issue 4, Page(s) 277–284

Abstract: Current research has shown that several imidazolium and chlorinated bispyridinium oximes are cytotoxic and activate different mechanisms or types of cell death. To investigate this further, we analysed interactions between these oximes and acetylcholine ... ...

Abstract	Current research has shown that several imidazolium and chlorinated bispyridinium oximes are cytotoxic and activate different mechanisms or types of cell death. To investigate this further, we analysed interactions between these oximes and acetylcholine receptors (AChRs) and how they affect several signalling pathways to find a relation between the observed toxicities and their effects on these specific targets. Chlorinated bispyridinium oximes caused time-dependent cytotoxicity by inhibiting the phosphorylation of STAT3 and AMPK without decreasing ATP and activated ERK1/2 and p38 MAPK signal cascades. Imidazolium oximes induced a time-independent and significant decrease in ATP and inhibition of the ERK1/2 signalling pathway along with phosphorylation of p38 MAPK, AMPK, and ACC. These pathways are usually triggered by a change in cellular energy status or by external signals, which suggests that oximes interact with some membrane receptors. Interestingly,
MeSH term(s)	Humans ; Oximes/pharmacology ; Antidotes/pharmacology ; AMP-Activated Protein Kinases ; Pyridinium Compounds/toxicity ; Neuroblastoma ; p38 Mitogen-Activated Protein Kinases ; Adenosine Triphosphate ; Cholinesterase Inhibitors/toxicity ; Cholinesterase Reactivators/pharmacology ; Acetylcholinesterase/metabolism
Chemical Substances	Oximes ; Antidotes ; AMP-Activated Protein Kinases (EC 2.7.11.31) ; Pyridinium Compounds ; p38 Mitogen-Activated Protein Kinases (EC 2.7.11.24) ; Adenosine Triphosphate (8L70Q75FXE) ; Cholinesterase Inhibitors ; Cholinesterase Reactivators ; Acetylcholinesterase (EC 3.1.1.7)
Language	English
Publishing date	2022-12-30
Publishing country	Croatia
Document type	Journal Article
ZDB-ID	127289-5
ISSN	1848-6312 ; 0004-1254
ISSN (online)	1848-6312
ISSN	0004-1254
DOI	10.2478/aiht-2022-73-3688
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Article: Altered levels of variant cholinesterase transcripts contribute to the imbalanced cholinergic signaling in Alzheimer's and Parkinson's disease.

Gok, Muslum / Madrer, Nimrod / Zorbaz, Tamara / Bennett, Estelle R / Greenberg, David / Bennett, David A / Soreq, Hermona

Frontiers in molecular neuroscience

2022 Volume 15, Page(s) 941467

Abstract: Acetylcholinesterase and butyrylcholinesterase (AChE and BChE) are involved in modulating cholinergic signaling, but their roles in Alzheimer's and Parkinson's diseases (AD and PD) remain unclear. We identified a higher frequency of the functionally ... ...

Abstract	Acetylcholinesterase and butyrylcholinesterase (AChE and BChE) are involved in modulating cholinergic signaling, but their roles in Alzheimer's and Parkinson's diseases (AD and PD) remain unclear. We identified a higher frequency of the functionally impaired BCHE-K variant (rs1803274) in AD and PD compared to controls and lower than in the GTEx dataset of healthy individuals (
Language	English
Publishing date	2022-09-02
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452967-9
ISSN	1662-5099
ISSN	1662-5099
DOI	10.3389/fnmol.2022.941467
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Article: Sex-specific declines in cholinergic-targeting tRNA fragments in the nucleus accumbens in Alzheimer's disease.

Shulman, Dana / Dubnov, Serafima / Zorbaz, Tamara / Madrer, Nimrod / Paldor, Iddo / Bennett, David A / Seshadri, Sudha / Mufson, Elliott J / Greenberg, David S / Loewenstein, Yonatan / Soreq, Hermona

bioRxiv : the preprint server for biology

2023

Abstract: Introduction: Females with Alzheimer's disease (AD) suffer accelerated dementia and loss of cholinergic neurons compared to males, but the underlying mechanisms are unknown. Seeking causal contributors to both these phenomena, we pursued changes in tRNA ...

Abstract	Introduction: Females with Alzheimer's disease (AD) suffer accelerated dementia and loss of cholinergic neurons compared to males, but the underlying mechanisms are unknown. Seeking causal contributors to both these phenomena, we pursued changes in tRNA fragments (tRFs) targeting cholinergic transcripts (CholinotRFs). Methods: We analyzed small RNA-sequencing data from the Results: NAc CholinotRFs of mitochondrial genome origin showed reduced levels that correlated with elevations in their predicted cholinergic-associated mRNA targets. Single cell RNA seq from AD temporal cortices showed altered sex-specific levels of cholinergic transcripts in diverse cell types; inversely, human-originated neuroblastoma cells under cholinergic differentiation presented sex-specific CholinotRF elevations. Discussion: Our findings support CholinotRFs contributions to cholinergic regulation, predicting their involvement in AD sex-specific cholinergic loss and dementia.
Language	English
Publishing date	2023-02-20
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.02.08.527612
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Article ; Online: Butyrylcholinesterase inhibited by nerve agents is efficiently reactivated with chlorinated pyridinium oximes.

Zorbaz, Tamara / Malinak, David / Kuca, Kamil / Musilek, Kamil / Kovarik, Zrinka

Chemico-biological interactions

2019 Volume 307, Page(s) 16–20

Abstract: Bispyridinium oximes with one (K865, K866, K867) or two (K868, K869, K870) ortho-positioned chlorine moiety, analogous to previously known K027, K048 and K203 oximes, and potent reactivators of human acetylcholinesterase (AChE) inhibited by nerve agents, ...

Abstract	Bispyridinium oximes with one (K865, K866, K867) or two (K868, K869, K870) ortho-positioned chlorine moiety, analogous to previously known K027, K048 and K203 oximes, and potent reactivators of human acetylcholinesterase (AChE) inhibited by nerve agents, were tested in the reactivation of human butyrylcholinesterase (BChE) inhibited by sarin, cyclosarin, VX, and tabun. A previously highlighted AChE reactivator, dichlorinated bispyridinium oxime with propyl linker (K868), was tested in more detail for reactivation of four nerve agent-BChE conjugates. Its BChE reactivation potency was showed to be promising when compared to the standard oximes used in medical practice, asoxime (HI-6) and pralidoxime (2-PAM), especially in case of sarin and tabun. This finding could be used in the pseudo-catalytic scavenging of the most nerve agents due to its cumulative capacity to reactivate both AChE and BChE.
MeSH term(s)	Butyrylcholinesterase/chemistry ; Butyrylcholinesterase/metabolism ; Cholinesterase Inhibitors/chemistry ; Cholinesterase Inhibitors/metabolism ; Enzyme Activation/drug effects ; Halogenation ; Humans ; Kinetics ; Nerve Agents/chemistry ; Nerve Agents/metabolism ; Oximes/chemistry ; Oximes/metabolism ; Oximes/pharmacology ; Pyridinium Compounds/chemistry ; Sarin/chemistry ; Sarin/metabolism
Chemical Substances	Cholinesterase Inhibitors ; Nerve Agents ; Oximes ; Pyridinium Compounds ; Sarin (B4XG72QGFM) ; Butyrylcholinesterase (EC 3.1.1.8)
Language	English
Publishing date	2019-04-18
Publishing country	Ireland
Document type	Journal Article
ZDB-ID	218799-1
ISSN	1872-7786 ; 0009-2797
ISSN (online)	1872-7786
ISSN	0009-2797
DOI	10.1016/j.cbi.2019.04.020
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Article ; Online: Sex-specific declines in cholinergic-targeting tRNA fragments in the nucleus accumbens in Alzheimer's disease.

Shulman, Dana / Dubnov, Serafima / Zorbaz, Tamara / Madrer, Nimrod / Paldor, Iddo / Bennett, David A / Seshadri, Sudha / Mufson, Elliott J / Greenberg, David S / Loewenstein, Yonatan / Soreq, Hermona

Alzheimer's & dementia : the journal of the Alzheimer's Association

2023 Volume 19, Issue 11, Page(s) 5159–5172

Abstract	Introduction: Females with Alzheimer's disease (AD) suffer accelerated dementia and loss of cholinergic neurons compared to males, but the underlying mechanisms are unknown. Seeking causal contributors to both these phenomena, we pursued changes in transfer RNS (tRNA) fragments (tRFs) targeting cholinergic transcripts (CholinotRFs). Methods: We analyzed small RNA-sequencing (RNA-Seq) data from the nucleus accumbens (NAc) brain region which is enriched in cholinergic neurons, compared to hypothalamic or cortical tissues from AD brains; and explored small RNA expression in neuronal cell lines undergoing cholinergic differentiation. Results: NAc CholinotRFs of mitochondrial genome origin showed reduced levels that correlated with elevations in their predicted cholinergic-associated mRNA targets. Single-cell RNA seq from AD temporal cortices showed altered sex-specific levels of cholinergic transcripts in diverse cell types; inversely, human-originated neuroblastoma cells under cholinergic differentiation presented sex-specific CholinotRF elevations. Discussion: Our findings support CholinotRFs contributions to cholinergic regulation, predicting their involvement in AD sex-specific cholinergic loss and dementia.
MeSH term(s)	Male ; Female ; Humans ; Alzheimer Disease/genetics ; Alzheimer Disease/metabolism ; Nucleus Accumbens/metabolism ; Cholinergic Neurons/metabolism ; Cholinergic Agents/metabolism ; RNA/metabolism ; RNA, Transfer/metabolism
Chemical Substances	Cholinergic Agents ; RNA (63231-63-0) ; RNA, Transfer (9014-25-9)
Language	English
Publishing date	2023-05-09
Publishing country	United States
Document type	Journal Article
ZDB-ID	2211627-8
ISSN	1552-5279 ; 1552-5260
ISSN (online)	1552-5279
ISSN	1552-5260
DOI	10.1002/alz.13095
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Zs.A 6316: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 2021: Bestellungen von Artikeln über das Online-Bestellformular ab Jg. 2022: Lesesaal (EG)
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Article ; Online: The estimation of oxime efficiency is affected by the experimental design of phosphylated acetylcholinesterase reactivation.

Maček Hrvat, Nikolina / Zorbaz, Tamara / Šinko, Goran / Kovarik, Zrinka

Toxicology letters

2018 Volume 293, Page(s) 222–228

Abstract: Reactivation of acetylcholinesterase (AChE), an essential enzyme in neurotransmission, is a key point in the treatment of acute poisoning by nerve agents and pesticides, which structurally belong to organophosphorus compounds (OP). Due to the high ... ...

Abstract	Reactivation of acetylcholinesterase (AChE), an essential enzyme in neurotransmission, is a key point in the treatment of acute poisoning by nerve agents and pesticides, which structurally belong to organophosphorus compounds (OP). Due to the high diversity of substituents on the phosphorous atom, there is a variety of OP-AChE conjugates deriving from AChE inhibition, and therefore not only is there no universal reactivator efficient enough for the most toxic OPs, but for some nerve agents there is still a lack of any reactivator at all. The endeavor of many chemists to find more efficient reactivators resulted in thousands of newly-designed and synthesized oximes-potential reactivators of AChE. For an evaluation of the oximés reactivation efficiency, many research groups employ a simple spectrophotometric Ellman method. Since parameters that describe reactivator efficiency are often incomparable among laboratories, we tried to emphasize the critical steps in the determination of reactivation parameters as well as in the experimental design of a reactivation assay. We highlighted the important points in evaluation of reactivation kinetic parameters with an aim to achieve better agreement and comparability between the results obtained by different laboratories and overall, a more efficient evaluation of in vitro reactivation potency.
MeSH term(s)	Acetylcholinesterase/chemistry ; Acetylcholinesterase/metabolism ; Algorithms ; Animals ; Antidotes/chemistry ; Antidotes/pharmacology ; Biological Assay ; Chemical Warfare Agents ; Cholinesterase Reactivators/chemistry ; Cholinesterase Reactivators/pharmacology ; Drug Design ; Guinea Pigs ; Humans ; Kinetics ; Nerve Agents/toxicity ; Oximes/chemistry ; Oximes/pharmacology ; Phosphorylation ; Rabbits ; Sarin/antagonists & inhibitors ; Thermodynamics
Chemical Substances	Antidotes ; Chemical Warfare Agents ; Cholinesterase Reactivators ; Nerve Agents ; Oximes ; Sarin (B4XG72QGFM) ; Acetylcholinesterase (EC 3.1.1.7)
Language	English
Publishing date	2018-09-01
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	433788-8
ISSN	1879-3169 ; 0378-4274
ISSN (online)	1879-3169
ISSN	0378-4274
DOI	10.1016/j.toxlet.2017.11.022
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Article ; Online: Halogen substituents enhance oxime nucleophilicity for reactivation of cholinesterases inhibited by nerve agents.

Zorbaz, Tamara / Malinak, David / Hofmanova, Tereza / Maraković, Nikola / Žunec, Suzana / Hrvat, Nikolina Maček / Andrys, Rudolf / Psotka, Miroslav / Zandona, Antonio / Svobodova, Jana / Prchal, Lukas / Fingler, Sanja / Katalinić, Maja / Kovarik, Zrinka / Musilek, Kamil

European journal of medicinal chemistry

2022 Volume 238, Page(s) 114377

Abstract: The fluorinated bis-pyridinium oximes were designed and synthesized with the aim of increasing their nucleophilicity and potential to reactivate phosphorylated human recombinant acetylcholinesterase (AChE) and human purified plasmatic ... ...

Abstract	The fluorinated bis-pyridinium oximes were designed and synthesized with the aim of increasing their nucleophilicity and potential to reactivate phosphorylated human recombinant acetylcholinesterase (AChE) and human purified plasmatic butyrylcholinesterase (BChE) in relation to chlorinated and non-halogenated oxime analogues. Compared to non-halogenated oximes, halogenated oximes showed lower pK
MeSH term(s)	Acetylcholinesterase/metabolism ; Animals ; Butyrylcholinesterase/metabolism ; Cholinesterase Inhibitors/chemistry ; Cholinesterase Reactivators/chemistry ; Halogens ; Mice ; Nerve Agents/pharmacology ; Organophosphorus Compounds ; Oximes/chemistry ; Sarin/chemistry
Chemical Substances	Cholinesterase Inhibitors ; Cholinesterase Reactivators ; Halogens ; Nerve Agents ; Organophosphorus Compounds ; Oximes ; Sarin (B4XG72QGFM) ; Acetylcholinesterase (EC 3.1.1.7) ; Butyrylcholinesterase (EC 3.1.1.8)
Language	English
Publishing date	2022-04-27
Publishing country	France
Document type	Journal Article
ZDB-ID	188597-2
ISSN	1768-3254 ; 0009-4374 ; 0223-5234
ISSN (online)	1768-3254
ISSN	0009-4374 ; 0223-5234
DOI	10.1016/j.ejmech.2022.114377
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Article ; Online: High-throughput morphometric and transcriptomic profiling uncovers composition of naïve and sensory-deprived cortical cholinergic VIP/CHAT neurons.

Yayon, Nadav / Amsalem, Oren / Zorbaz, Tamara / Yakov, Or / Dubnov, Serafima / Winek, Katarzyna / Dudai, Amir / Adam, Gil / Schmidtner, Anna K / Tessier-Lavigne, Marc / Renier, Nicolas / Habib, Naomi / Segev, Idan / London, Michael / Soreq, Hermona

The EMBO journal

2022 , Page(s) e110565

Abstract: Cortical neuronal networks control cognitive output, but their composition and modulation remain elusive. Here, we studied the morphological and transcriptional diversity of cortical cholinergic VIP/ChAT interneurons (VChIs), a sparse population with a ... ...

Abstract	Cortical neuronal networks control cognitive output, but their composition and modulation remain elusive. Here, we studied the morphological and transcriptional diversity of cortical cholinergic VIP/ChAT interneurons (VChIs), a sparse population with a largely unknown function. We focused on VChIs from the whole barrel cortex and developed a high-throughput automated reconstruction framework, termed PopRec, to characterize hundreds of VChIs from each mouse in an unbiased manner, while preserving 3D cortical coordinates in multiple cleared mouse brains, accumulating thousands of cells. We identified two fundamentally distinct morphological types of VChIs, bipolar and multipolar that differ in their cortical distribution and general morphological features. Following mild unilateral whisker deprivation on postnatal day seven, we found after three weeks both ipsi- and contralateral dendritic arborization differences and modified cortical depth and distribution patterns in the barrel fields alone. To seek the transcriptomic drivers, we developed NuNeX, a method for isolating nuclei from fixed tissues, to explore sorted VChIs. This highlighted differentially expressed neuronal structural transcripts, altered exitatory innervation pathways and established Elmo1 as a key regulator of morphology following deprivation.
Language	English
Publishing date	2022-11-15
Publishing country	England
Document type	Journal Article
ZDB-ID	586044-1
ISSN	1460-2075 ; 0261-4189
ISSN (online)	1460-2075
ISSN	0261-4189
DOI	10.15252/embj.2021110565
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Article ; Online: Oxime-assisted reactivation of tabun-inhibited acetylcholinesterase analysed by active site mutations.

Katalinić, Maja / Šinko, Goran / Maček Hrvat, Nikolina / Zorbaz, Tamara / Bosak, Anita / Kovarik, Zrinka

Toxicology

2018 Volume 406-407, Page(s) 104–113

Abstract: The antidotal property of oximes is attributed to their ability to reactivate acetylcholinesterase (AChE) inhibited by organophosphorus compounds (OP) such as pesticides and nerve warfare agents. Understanding their interactions within the active site of ...

Abstract	The antidotal property of oximes is attributed to their ability to reactivate acetylcholinesterase (AChE) inhibited by organophosphorus compounds (OP) such as pesticides and nerve warfare agents. Understanding their interactions within the active site of phosphylated AChE is of great significance for the search for more efficient reactivators, especially in the case of the most resistant OP to reactivation, tabun. Therefore, herein we studied the interactions and reactivation of tabun-inhibited AChE by site-directed mutagenesis and a series of bispyridinium oximes. Our results indicated that the replacement of aromatic residues with aliphatic ones at the acyl pocket and choline binding site mostly interfered with the stabilisation of the oxime's pyridinium ring(s) within the active site gorge needed to obtain the proper orientation of the oxime group toward the phosphorylated active site serine. However, in the case of W286A, the mutation in the peripheral binding site by preventing a π-π interaction with one of the oxime's pyridinium rings allowed a more favourable position of the oxime for a nucleophilic attack on the phosphorylated catalytic serine. The mutation resulted in a 2-5 fold increase in the reactivation rates when compared to the AChE wild type. Therefore, it seems that aromatic amino acids at the peripheral binding site presented a limitation in bispyridinium oxime reactivation efficiency of tabun-phosphorylated AChE. Moreover, this is further corroborated by the reactivation by mono-pyridinium oxime 2-PAM, in which mutations at the peripheral site did not influence either the affinity or reactivation of tabun-inhibited AChE.
MeSH term(s)	Acetylcholinesterase/genetics ; Acetylcholinesterase/metabolism ; Animals ; Cholinesterase Inhibitors/chemistry ; Cholinesterase Inhibitors/metabolism ; Cholinesterase Inhibitors/toxicity ; Mice ; Molecular Docking Simulation/methods ; Mutation/drug effects ; Mutation/genetics ; Organophosphates/chemistry ; Organophosphates/metabolism ; Organophosphates/toxicity ; Oximes/chemistry ; Oximes/metabolism ; Oximes/toxicity
Chemical Substances	Cholinesterase Inhibitors ; Organophosphates ; Oximes ; Acetylcholinesterase (EC 3.1.1.7) ; tabun (S45M750QSH)
Language	English
Publishing date	2018-05-22
Publishing country	Ireland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	184557-3
ISSN	1879-3185 ; 0300-483X
ISSN (online)	1879-3185
ISSN	0300-483X
DOI	10.1016/j.tox.2018.05.008
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