Peptide hormones regulate the physiological functions of reproductive organs in Tenebrio molitor males

Marciniak, Paweł; Urbański, Arkadiusz; Kudlewska, Milena; Szymczak, Monika; Rosiński, Grzegorz

doi:10.1016/j.peptides.2016.06.006

Cited by 14 publications

(22 citation statements)

References 33 publications

(13 reference statements)

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“…Similarly to previously described neuropeptides, sNPF also participates in the regulation of many physiological processes in the insect body, starting with the inhibition of food intake and ending with the regulation of reproduction (Castillo & Pietrantonio, ; Jiang et al ., ; Marciniak et al ., ). The effect of sNPF on the contraction frequency of the visceral organs was determined only for the heart, oviducts and ejaculatory duct of the tenebrionid beetles (Marciniak et al ., ; Marciniak et al ., ; Marciniak et al ., ). However, the expression of gene encoding sNPF receptor in gut of fruit fly D. melanogaster , mosquito A. gambiae and fire ant Solenopsis invicta were identified, which suggested direct effect of this peptide on insect digestive system (Mertens et al ., ; Chen & Pietrantonio, ; Garczynski et al ., ).…”

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Myotropic activity and immunolocalization of selected neuropeptides of the burying beetle Nicrophorus vespilloides (Coleoptera: Silphidae)

et al. 2018

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Burying beetles (Nicrophorus sp.) are necrophagous insects with developed parental care. Genome of Nicrophorus vespilloides has been recently sequenced, which makes them interesting model organism in behavioral ecology. However, we know very little about their physiology, including the functioning of their neuroendocrine system. In this study, one of the physiological activities of proctolin, myosuppressin (Nicve-MS), myoinhibitory peptide (Trica-MIP-5) and the short neuropeptide F (Nicve-sNPF) in N. vespilloides have been investigated. The tested neuropeptides were myoactive on N. vespilloides hindgut. After application of the proctolin increased hindgut contraction frequency was observed (EC value was 5.47 × 10 mol/L). The other tested neuropeptides led to inhibition of N. vespilloides hindgut contractions (Nicve-MS: IC = 5.20 × 10 mol/L; Trica-MIP-5: IC = 5.95 × 10 mol/L; Nicve-sNPF: IC = 4.08 × 10 mol/L). Moreover, the tested neuropeptides were immunolocalized in the nervous system of N. vespilloides. Neurons containing sNPF and MIP in brain and ventral nerve cord (VNC) were identified. Proctolin-immunolabeled neurons only in VNC were observed. Moreover, MIP-immunolabeled varicosities and fibers in retrocerebral complex were observed. In addition, our results have been supplemented with alignments of amino acid sequences of these neuropeptides in beetle species. This alignment analysis clearly showed amino acid sequence similarities between neuropeptides. Moreover, this allowed to deduce amino acid sequence of N. vespilloides proctolin (RYLPTa), Nicve-MS (QDVDHVFLRFa) and six isoforms of Nicve-MIP (Nicve-MIP-1-DWNRNLHSWa; Nicve-MIP-2-AWQNLQGGWa; Nicve-MIP-3-AWQNLQGGWa; Nicve-MIP-4-AWKNLNNAGWa; Nicve-MIP-5-SEWGNFRGSWa; Nicve-MIP-6- DPAWTNLKGIWa; and Nicve-sNPF-SGRSPSLRLRFa).

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Myotropic activity and immunolocalization of selected neuropeptides of the burying beetle Nicrophorus vespilloides (Coleoptera: Silphidae)

et al. 2018

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“…Apart from juvenile hormone (Wijesekera et al 2016 ; Wilson et al 2003 ) little is known about the hormonal and neurohormonal regulation of the functioning of the male reproductive system in insects (Klowden 2008 ). Thus far, only few studies have been performed on insects (Marciniak et al 2017 ; Rankin et al 2009 ; Van Wielendaele et al 2013 ).…”

Section: Introductionmentioning

confidence: 99%

“…In Tenebrio molitor , these peptides also delay the moulting process of larvae, accelerate pupal moulting and increase growth in pre-starved and non-starved larvae, which again shows that they regulate growth and development in beetles (Marciniak et al 2013 ). Further studies with T. molitor have shown that sNPFs inhibit the oviduct muscle contractility (Marciniak et al 2013 ) and stimulate the contractions of the ejaculatory duct in this species (Marciniak et al 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Short neuropeptide F signaling regulates functioning of male reproductive system in Tenebrio molitor beetle

et al. 2020

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Neuropeptides of short neuropeptides F family (sNPF) have been identified in various arthropods. They are pleiotropic neuromolecules which so far have been mainly associated with regulation of feeding and metabolism, as well as growth and development, locomotion, circadian rhythm or learning and memory. Here, we describe the effects of Tenebrionid sNPF peptide (SGRSPSLRLRFa) on various aspects of the male reproductive physiology in the Tenebrio molitor beetle. We identified in silico the putative sNPF receptor Tenmo-sNPFR. Based on RT-PCR technique, it was shown that the receptor might be present in the male reproductive tissues of this beetle. The analysis of receptor amino acid sequence showed that it is similar to other beetle sNPFRs, as well as other insect species, and belongs rhodopsin-like G-protein-coupled receptors (GPCRs). Injections of Trica-sNPF and its shorter form Trica-sNPF (4-11) caused differentiated effects in T. molitor male reproductive tissues. After 24 h post injections, the peptides decreased the concentration of the soluble protein fraction in testes of 4-and 8-day-old beetles as well as the dry mass of these organs but only in 8-day-old individuals. The same effects were shown with regard to accessory glands. Both peptides decrease the concentration of the soluble protein fraction but do not affect the dry mass of this organ. Furthermore, injections of Trica-sNPF at the 10-7 M concentration decrease the total sperm number in the reproductive system. Surprisingly, the same concentration of the shorter form, Trica-sNPF (4-11) increased the sperm number. It was also shown that both peptides in different manner influence contractions of ejaculatory duct. The data presented in this article give new evidence that sNPFs are involved in the regulation of reproductive events in beetles, which might be the part of a larger neuropeptide network combining feeding, growth and development with the physiology of reproduction.

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“…Therefore, the effect on male fecundity might be less severe because a poor metabolic condition of the beetles plays a minor role here. However, insect peptide hormones have been implicated in the regulation of testes development and sperm number [56]. In addition, neuropeptides are involved in regulating male sexual behaviour [9].…”

Section: Pc-dependent Neuropeptide Signalling Is Required For Female mentioning

confidence: 99%

Individual function of the ancestral prohormone convertase PC1/3 in Tribolium larval growth and moulting highlights major evolutionary changes between beetle and fly neuroendocrine systems

Fritzsche¹,

Hunnekuhl²

2020

Preprint

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Background: The insect neuroendocrine system acts in the regulation of physiology, development and growth. Molecular evolution of this system hence has the potential to allow for major biological differences between insect groups. Two prohormone convertases, PC1/3 and PC2, are found in animals and both function in the processing of neuropeptide precursors in the vertebrate neurosecretory pathway. Whereas PC2-function is conserved between the fly Drosophila and vertebrates , ancestral PC1/3 was lost in the fly lineage and has not been functionally studied in any protostome. Results: In order to understand its original functions and the changes accompanying the gene loss in the fly, we investigated PC1/3 and PC2 expression and function in the beetle Tribolium castaneum. We found that PC2 is broadly expressed in the nervous system, whereas surprisingly, PC1/3 expression is restricted to specific cell groups in the posterior brain and suboesophageal ganglion. Both proteases have parallel but non-redundant functions in adult beetles’ viability and fertility. Female infertility following RNAi is caused by a failure to deposit sufficient nutritive material to the developing oocytes. Larval RNAi of both genes produced moulting defects where the larvae were not able to shed their old cuticle and became ‘locked-in’. Unexpectedly, PC1/3 RNAi larvae went through supernumerary larval moults despite minimal to zero weight gain. Conclusions: Our results indicate a yet unknown molecular mechanism for the coupling of moulting and growth in insect larvae. Conservation of the evolutionary ancient PC1/3 gene in most insect groups suggests conserved function and that its loss in dipterans may have been accompanied by major changes in the coordination of larval growth and moulting.

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Peptide hormones regulate the physiological functions of reproductive organs in Tenebrio molitor males

Cited by 14 publications

References 33 publications

Myotropic activity and immunolocalization of selected neuropeptides of the burying beetle Nicrophorus vespilloides (Coleoptera: Silphidae)

Myotropic activity and immunolocalization of selected neuropeptides of the burying beetle Nicrophorus vespilloides (Coleoptera: Silphidae)

Short neuropeptide F signaling regulates functioning of male reproductive system in Tenebrio molitor beetle

Individual function of the ancestral prohormone convertase PC1/3 in Tribolium larval growth and moulting highlights major evolutionary changes between beetle and fly neuroendocrine systems

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