Transglutaminase-catalyzed incorporation of polyamines masks the DNA-binding region of the transcription factor Relish

Maki, Kouki; Shibata, Toshio; Kawabata, Shun Ichiro

doi:10.1074/jbc.m117.779579

Cited by 18 publications

(16 citation statements)

References 51 publications

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“…In contrast, we also detected a trend that TGase3 positively regulates sessile hemocyte attachment to the abdominal integument in uninfected mosquitoes. Based on these and other data 16 , 43 , 44 , we hypothesize that TGase3 negatively regulates periostial hemocyte aggregation by inhibiting the immune deficiency (IMD) pathway and altering hemocyte adhesion (Fig. 6 ).…”

Section: Discussionsupporting

confidence: 53%

“…The N-terminal region of Relish translocates into the nucleus, binds to DNA, and induces the expression of antimicrobial peptides and the activation of other immune responses that kill pathogens 45 . Interestingly, Drosophila transglutaminase negatively regulates the IMD pathway by crosslinking the N-terminal region of Relish and forming a polymer that prevents its translocation into the nucleus 43 , 44 . This transglutaminase also incorporates natural primary amines into the DNA binding site of Relish, thereby providing a second layer of IMD pathway inhibition 44 .…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, Drosophila transglutaminase negatively regulates the IMD pathway by crosslinking the N-terminal region of Relish and forming a polymer that prevents its translocation into the nucleus 43 , 44 . This transglutaminase also incorporates natural primary amines into the DNA binding site of Relish, thereby providing a second layer of IMD pathway inhibition 44 . Here, we did not test the direct relationship between A. gambiae TGase3 and the IMD pathway.…”

Section: Discussionmentioning

confidence: 99%

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Transglutaminase 3 negatively regulates immune responses on the heart of the mosquito, Anopheles gambiae

Yan

Ramakrishnan

Estévez‐Lao

et al. 2022

Sci Rep

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The immune and circulatory systems of insects are functionally integrated. Following infection, immune cells called hemocytes aggregate around the ostia (valves) of the heart. An earlier RNA sequencing project in the African malaria mosquito, Anopheles gambiae, revealed that the heart-associated hemocytes, called periostial hemocytes, express transglutaminases more highly than hemocytes elsewhere in the body. Here, we further queried the expression of these transglutaminase genes and examined whether they play a role in heart-associated immune responses. We found that, in the whole body, injury upregulates the expression of TGase2, whereas infection upregulates TGase1, TGase2 and TGase3. RNAi-based knockdown of TGase1 and TGase2 did not alter periostial hemocyte aggregation, but knockdown of TGase3 increased the number of periostial hemocytes during the early stages of infection and the sequestration of melanin by periostial hemocytes during the later stages of infection. In uninfected mosquitoes, knockdown of TGase3 also slightly reduced the number of sessile hemocytes outside of the periostial regions. Taken altogether, these data show that TGase3 negatively regulates periostial hemocyte aggregation, and we hypothesize that this occurs by negatively regulating the immune deficiency pathway and by altering hemocyte adhesion. In conclusion, TGase3 is involved in the functional integration between the immune and circulatory systems of mosquitoes.

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Section: Discussionsupporting

confidence: 53%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Transglutaminase 3 negatively regulates immune responses on the heart of the mosquito, Anopheles gambiae

Yan

Ramakrishnan

Estévez‐Lao

et al. 2022

Sci Rep

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“…An interaction analysis of social isolation and bacterial injection at all the four time points showed regulation of 20 genes across all time points in the bacteria‐injected isolated queens (Tables and ). These included down‐regulation at 4 hpi of the Toll receptor activator‐gene spätzle (LOC105678357), up‐regulation at 12 hpi of the Imd pathway signaling gene imd (LOC105672003) and down‐regulation, also at 12 hpi, of hemocyte protein–glutamine gamma‐glutamyl transferase‐like (LOC105670674) similar to transglutaminase (NP_609174, 37% identity, 90% coverage) in Drosophila that inhibits the Imd pathway transcription factor Relish (Maki, Shibata, & Kawabata, ).…”

Section: Resultsmentioning

confidence: 99%

“…identity, 90% coverage) in Drosophila that inhibits the Imd pathway transcription factor Relish (Maki, Shibata, & Kawabata, 2017).…”

Section: Interaction Effect Of Social Isolation and Bacterial Injecmentioning

confidence: 99%

Social environment affects the transcriptomic response to bacteria in ant queens

Viljakainen

Jurvansuu

Holmberg

et al. 2018

Ecology and Evolution

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Social insects have evolved enormous capacities to collectively build nests and defend their colonies against both predators and pathogens. The latter is achieved by a combination of individual immune responses and sophisticated collective behavioral and organizational disease defenses, that is, social immunity. We investigated how the presence or absence of these social defense lines affects individual‐level immunity in ant queens after bacterial infection. To this end, we injected queens of the ant Linepithema humile with a mix of gram+ and gram− bacteria or a control solution, reared them either with workers or alone and analyzed their gene expression patterns at 2, 4, 8, and 12 hr post‐injection, using RNA‐seq. This allowed us to test for the effect of bacterial infection, social context, as well as the interaction between the two over the course of infection and raising of an immune response. We found that social isolation per se affected queen gene expression for metabolism genes, but not for immune genes. When infected, queens reared with and without workers up‐regulated similar numbers of innate immune genes revealing activation of Toll and Imd signaling pathways and melanization. Interestingly, however, they mostly regulated different genes along the pathways and showed a different pattern of overall gene up‐regulation or down‐regulation. Hence, we can conclude that the absence of workers does not compromise the onset of an individual immune response by the queens, but that the social environment impacts the route of the individual innate immune responses.

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Type 2 transglutaminase in the nucleus: the new epigenetic face of a cytoplasmic enzyme

Rossin

Ciccosanti

D’Eletto

et al. 2023

Cell. Mol. Life Sci.

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One of the major mysteries in science is how it is possible to pack the cellular chromatin with a total length of over 1 m, into a small sphere with a diameter of 5 mm “the nucleus”, and even more difficult to envisage how to make it functional. Although we know that compaction is achieved through the histones, however, the DNA needs to be accessible to the transcription machinery and this is allowed thanks to a variety of very complex epigenetic mechanisms. Either DNA (methylation) or post-translational modifications of histone proteins (acetylation, methylation, ubiquitination and sumoylation) play a crucial role in chromatin remodelling and consequently on gene expression. Recently the serotonylation and dopaminylation of the histone 3, catalyzed by the Transglutaminase type 2 (TG2), has been reported. These novel post-translational modifications catalyzed by a predominantly cytoplasmic enzyme opens a new avenue for future investigations on the enzyme function itself and for the possibility that other biological amines, substrate of TG2, can influence the genome regulation under peculiar cellular conditions. In this review we analyzed the nuclear TG2’s biology by discussing both its post-translational modification of various transcription factors and the implications of its epigenetic new face. Finally, we will focus on the potential impact of these events in human diseases.

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Transglutaminase-catalyzed incorporation of polyamines masks the DNA-binding region of the transcription factor Relish

Abstract: Edited by Joel GottesfeldIn Drosophila, the final immune deficiency (IMD) pathwaydependent signal is transmitted through proteolytic conversion of the nuclear factor-B (

Cited by 18 publications

References 51 publications

Transglutaminase 3 negatively regulates immune responses on the heart of the mosquito, Anopheles gambiae

Transglutaminase 3 negatively regulates immune responses on the heart of the mosquito, Anopheles gambiae

Social environment affects the transcriptomic response to bacteria in ant queens

Type 2 transglutaminase in the nucleus: the new epigenetic face of a cytoplasmic enzyme

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