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Histone monoaminylation

Histone monoaminylation refers to the post-translational modification in which monoamines are covalently attached to glutamine residue position 5 (Gln5) of histone H3 via transamidation. In general, monoaminylation refers to the overall class of post-translational modifications involving monoamines; however, these reactions are further classified by the individual monoamine reactant they describe.

Identification
Protein monoaminylation was first identified in 1957 by Heinrich Waelsch and colleagues at Columbia University. After discovering that primary amines could be covalently incorporated into proteins via transamidation at glutamine residues, the group went on to uncover the enzyme catalyzing these reactions, effectively naming it "transglutaminase" after its function. Despite its discovery in the mid-twentieth century, protein monoaminylation was not investigated as a post-translational modification until 2003, when Diego Walther and colleagues at the Max-Planck-Institute for Molecular Genetics revealed that serotonylation of small GTPases mediates ⍺-granule release during the activation and aggregation of platelets. Histone mnoaminylation was not uncovered as an epigenetic regulatory mechanism until 2019, when Lorna Farrelly and colleagues at the Icahn School of Medicine reported the H3Q5-serotonylation (H3Q5ser) modification for the first time. Later, in 2020, the H3Q5-dopaminylation (H3Q5dop) modification was identified in the striatum by Ashley Lepack and colleagues also at the Icahn School of Medicine. Five years later, Qingfei Zheng and colleagues at Ohio State University discovered the H3Q5-histaminylation (H3Q5his) modification in histaminergic neurons. == Mechanism ==
Mechanism
Histone monoaminylation is catalyzed by transglutaminase 2 (TGM2) in a calcium-dependent manner, and relies upon the intracellular bioavailability of monoamine substrates. Generally, protein monoaminylation occurs in the cytoplasm; however, histone monoaminylation only occurs within the nucleus. The active site itself is composed of a well conserved catalytic triad (Cys277–His335–Asp358) situated within a substrate binding channel, which is bordered by two conserved residues (Trp241 and Trp332) that facilitate catalysis through stabilization of the transition state. Once intracellular Ca2+ binds to TGM2 and exposes the substrate binding channel, the glutamine residue of the substrate protein (i.e., histone H3) is free to enter the enzyme active site. As a transamidation reaction, the mechanism for histone monoaminylation can be summarized in two parts: an initial thioester formation, followed by isopeptide bond formation. Fig. 1 Mechanism for Histone Monoaminylation Monoaminylation is a two step, Ca2+-dependent reaction in which TGM2 catalyzes the covalent attachment of a monoamine (i.e., dopamine, serotonin, histamine) onto the glutamine residue of histone proteins. (A) The catalytic cysteine residue (Cys277) of TGM2 facilitates an initial acyl transfer reaction, which is ultimately followed by isopeptide bond formation (B). When intracellular Ca2+ and monoamine concentrations are sufficient, TGM2-catalyzed monoaminylation of histone H3 can occur. First, the catalytic cysteine residue (Cys277) within the TGM2 active site nucleophilically attacks the 𝛾-carboxamido group of the glutamine residue in an acyl transfer reaction (Fig. 1A), forming a thioester intermediate and releasing one molecule of ammonia (NH3) as a result. Next, the deprotonated primary amine of the monoamine substrate nucleophilically attacks the 𝛾-thioester group of the intermediate, forming a stable isopeptide bond and ultimately releasing the enzyme (Fig. 1B). == Function ==
Function
With the discovery of histone monoaminylation in 2019, monoaminylation thus entered into the complex and ever-growing field of epigenetics, posing as a novel set of dynamic regulatory mechanisms. astrocytes of the olfactory bulb, the inferior alveolar nerve (i.e., of the lip and lower jaw), placenta, ependymomas (brain cancers), pancreatic ductal adenocarcinoma (PDAC) tissues, cancer-associated fibroblasts, hepatocellular carcinoma (HCC), and neutrophils. By comparison, H3Q5-dopaminylation (H3Q5dop) has remained a far less explored topic since its discovery in 2020. Nevertheless, H3Q5dop has been reported in dopaminergic neurons of the nucleus accumbens, the ventral tegmental area (VTA), and the amygdala. H3Q5-histaminylation (H3Q5his) remains the most recent (i.e., 2025) and thus least reported histone monoaminylation of all, which has been observed within histaminergic neurons of the posterior hypothalamic tuberomammillary nucleus (TMN), Dopaminylation Nucleus Accumbens (NAc) H3Q5dop Promotes cocaine-seeking behavior and regulates cocaine-induced gene expression programs (Stewart et al., 2023) Herein, failure to recognize novel odor was reportedly linked to increased dopamine transmission, decreased levels of TGM2, and increased histone trimethylation (H3K4me3) and dopaminylation (H3Q5dop) in the amygdala following exposure to early-life stressful social experience (SSE). It remains unclear whether the reported fluctuations in TGM2 levels could be attributed to changes in TGM2 expression levels or changes in TGM2 activity levels. Ambiguity aside, this data provides useful insight, as early-life adversity paradigms appear sufficient for reconfiguration of epigenetic signatures within the limbic system, thereby establishing stable, differential epigenetic programs which may contribute to lifelong susceptibility for affective psychopathologies (i.e., major depressive disorder, bipolar disorder, anxiety disorders). == See Also ==
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