Tachykinin-related peptides modulate immune-gene expression in the mealworm beetle Tenebrio molitor L

Arkadiusz Urbański; Paul Johnston; Elisa Bittermann; Maryam Keshavarz; Véronique Paris; Karolina Walkowiak-Nowicka; Natalia Konopińska; Paweł Marciniak; Jens Rolff

doi:10.1038/s41598-022-21605-6

Tachykinin-related peptides modulate immune-gene expression in the mealworm beetle Tenebrio molitor L

Arkadiusz Urbański^*, Paul Johnston, Elisa Bittermann, Maryam Keshavarz, Véronique Paris, Karolina Walkowiak-Nowicka, Natalia Konopińska, Paweł Marciniak, Jens Rolff

^*Corresponding author for this work

School of Medicine

Research output: Contribution to journal › Article › peer-review

Abstract

Tachykinins (TKs) are a group of conserved neuropeptides. In insects, tachykinin-related peptides (TRPs) are important modulators of several functions such as nociception and lipid metabolism. Recently, it has become clear that TRPs also play a role in regulating the insect immune system. Here, we report a transcriptomic analysis of changes in the expression levels of immune-related genes in the storage pest Tenebrio molitor after treatment with Tenmo-TRP-7. We tested two concentrations (10-8 and 10-6 M) at two time points, 6 and 24 h post-injection. We found significant changes in the transcript levels of a wide spectrum of immune-related genes. Some changes were observed 6 h after the injection of Tenmo-TRP-7, especially in relation to its putative anti-apoptotic action. Interestingly, 24 h after the injection of 10-8 M Tenmo-TRP-7, most changes were related to the regulation of the cellular response. Applying 10-6 M Tenmo-TRP-7 resulted in the downregulation of genes associated with humoral responses. Injecting Tenmo-TRP-7 did not affect beetle survival but led to a reduction in haemolymph lysozyme-like antibacterial activity, consistent with the transcriptomic data. The results confirmed the immunomodulatory role of TRP and shed new light on the functional homology between TRPs and TKs.

Original language	English
Article number	17277
Number of pages	19
Journal	Scientific Reports
Volume	12
DOIs	https://doi.org/10.1038/s41598-022-21605-6
Publication status	Published - 14 Oct 2022

Keywords

Animals
Anti-Bacterial Agents/metabolism
Coleoptera/physiology
Gene Expression
Muramidase/metabolism
Neuropeptides/genetics
Tachykinins/genetics
Tenebrio/metabolism

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Cite this

@article{3cd243fa8e8d4ca296757b1205fbbce0,

title = "Tachykinin-related peptides modulate immune-gene expression in the mealworm beetle Tenebrio molitor L",

abstract = "Tachykinins (TKs) are a group of conserved neuropeptides. In insects, tachykinin-related peptides (TRPs) are important modulators of several functions such as nociception and lipid metabolism. Recently, it has become clear that TRPs also play a role in regulating the insect immune system. Here, we report a transcriptomic analysis of changes in the expression levels of immune-related genes in the storage pest Tenebrio molitor after treatment with Tenmo-TRP-7. We tested two concentrations (10-8 and 10-6 M) at two time points, 6 and 24 h post-injection. We found significant changes in the transcript levels of a wide spectrum of immune-related genes. Some changes were observed 6 h after the injection of Tenmo-TRP-7, especially in relation to its putative anti-apoptotic action. Interestingly, 24 h after the injection of 10-8 M Tenmo-TRP-7, most changes were related to the regulation of the cellular response. Applying 10-6 M Tenmo-TRP-7 resulted in the downregulation of genes associated with humoral responses. Injecting Tenmo-TRP-7 did not affect beetle survival but led to a reduction in haemolymph lysozyme-like antibacterial activity, consistent with the transcriptomic data. The results confirmed the immunomodulatory role of TRP and shed new light on the functional homology between TRPs and TKs.",

keywords = "Animals, Anti-Bacterial Agents/metabolism, Coleoptera/physiology, Gene Expression, Muramidase/metabolism, Neuropeptides/genetics, Tachykinins/genetics, Tenebrio/metabolism",

author = "Arkadiusz Urba{\'n}ski and Paul Johnston and Elisa Bittermann and Maryam Keshavarz and V{\'e}ronique Paris and Karolina Walkowiak-Nowicka and Natalia Konopi{\'n}ska and Pawe{\l} Marciniak and Jens Rolff",

note = "The research was partially supported by Grant No. 2021/41/B/NZ9/01054 from the National Science Centre (Poland). AU was supported by a scholarship from the Polish National Agency for Academic Exchange (NAWA) within the Bekker Programme, 2019 (personal stipend, PPN/BEK/2019/1/00167), a scholarship from the Deutscher Akademischer Austauschdienst (DAAD) within the program for Research Stays for University Academics and Scientists, 2018 (personal stipend, 91696887), and a scholarship from the Initiative of Excellence, Research University (ID-UB Project), within the International Junior and Senior Exchange, 2021 (personal stipend, 018/07/POB2/0001). The publication fee was supported by the ID-UB Project (040/08/POB2/0010). JR was funded by DFG FOR 5026.",

year = "2022",

month = oct,

day = "14",

doi = "10.1038/s41598-022-21605-6",

language = "English",

volume = "12",

journal = "Scientific Reports",

issn = "2045-2322",

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T1 - Tachykinin-related peptides modulate immune-gene expression in the mealworm beetle Tenebrio molitor L

AU - Urbański, Arkadiusz

AU - Johnston, Paul

AU - Bittermann, Elisa

AU - Keshavarz, Maryam

AU - Paris, Véronique

AU - Walkowiak-Nowicka, Karolina

AU - Konopińska, Natalia

AU - Marciniak, Paweł

AU - Rolff, Jens

N1 - The research was partially supported by Grant No. 2021/41/B/NZ9/01054 from the National Science Centre (Poland). AU was supported by a scholarship from the Polish National Agency for Academic Exchange (NAWA) within the Bekker Programme, 2019 (personal stipend, PPN/BEK/2019/1/00167), a scholarship from the Deutscher Akademischer Austauschdienst (DAAD) within the program for Research Stays for University Academics and Scientists, 2018 (personal stipend, 91696887), and a scholarship from the Initiative of Excellence, Research University (ID-UB Project), within the International Junior and Senior Exchange, 2021 (personal stipend, 018/07/POB2/0001). The publication fee was supported by the ID-UB Project (040/08/POB2/0010). JR was funded by DFG FOR 5026.

PY - 2022/10/14

Y1 - 2022/10/14

N2 - Tachykinins (TKs) are a group of conserved neuropeptides. In insects, tachykinin-related peptides (TRPs) are important modulators of several functions such as nociception and lipid metabolism. Recently, it has become clear that TRPs also play a role in regulating the insect immune system. Here, we report a transcriptomic analysis of changes in the expression levels of immune-related genes in the storage pest Tenebrio molitor after treatment with Tenmo-TRP-7. We tested two concentrations (10-8 and 10-6 M) at two time points, 6 and 24 h post-injection. We found significant changes in the transcript levels of a wide spectrum of immune-related genes. Some changes were observed 6 h after the injection of Tenmo-TRP-7, especially in relation to its putative anti-apoptotic action. Interestingly, 24 h after the injection of 10-8 M Tenmo-TRP-7, most changes were related to the regulation of the cellular response. Applying 10-6 M Tenmo-TRP-7 resulted in the downregulation of genes associated with humoral responses. Injecting Tenmo-TRP-7 did not affect beetle survival but led to a reduction in haemolymph lysozyme-like antibacterial activity, consistent with the transcriptomic data. The results confirmed the immunomodulatory role of TRP and shed new light on the functional homology between TRPs and TKs.

AB - Tachykinins (TKs) are a group of conserved neuropeptides. In insects, tachykinin-related peptides (TRPs) are important modulators of several functions such as nociception and lipid metabolism. Recently, it has become clear that TRPs also play a role in regulating the insect immune system. Here, we report a transcriptomic analysis of changes in the expression levels of immune-related genes in the storage pest Tenebrio molitor after treatment with Tenmo-TRP-7. We tested two concentrations (10-8 and 10-6 M) at two time points, 6 and 24 h post-injection. We found significant changes in the transcript levels of a wide spectrum of immune-related genes. Some changes were observed 6 h after the injection of Tenmo-TRP-7, especially in relation to its putative anti-apoptotic action. Interestingly, 24 h after the injection of 10-8 M Tenmo-TRP-7, most changes were related to the regulation of the cellular response. Applying 10-6 M Tenmo-TRP-7 resulted in the downregulation of genes associated with humoral responses. Injecting Tenmo-TRP-7 did not affect beetle survival but led to a reduction in haemolymph lysozyme-like antibacterial activity, consistent with the transcriptomic data. The results confirmed the immunomodulatory role of TRP and shed new light on the functional homology between TRPs and TKs.

KW - Animals

KW - Anti-Bacterial Agents/metabolism

KW - Coleoptera/physiology

KW - Gene Expression

KW - Muramidase/metabolism

KW - Neuropeptides/genetics

KW - Tachykinins/genetics

KW - Tenebrio/metabolism

U2 - 10.1038/s41598-022-21605-6

DO - 10.1038/s41598-022-21605-6

M3 - Article

C2 - 36241888

SN - 2045-2322

VL - 12

JO - Scientific Reports

JF - Scientific Reports

M1 - 17277

ER -

Tachykinin-related peptides modulate immune-gene expression in the mealworm beetle Tenebrio molitor L

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Keywords

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