Endocrine regulation of immunity in insects

Nunes, Catarina; Sucena, Élio; Kaburagi, Takashi

doi:10.1111/febs.15581

Cited by 51 publications

(55 citation statements)

References 205 publications

(248 reference statements)

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“…Indeed, the plasticity of the immune response requested to face pathogens during the insect life has maintenance costs [ 71 ] and leads to a systemic metabolic switch, redirecting the metabolic resources to the activated immune system. As neuropeptides play an important immunotropic role in the regulation of the insect cellular and humoral responses promoting the mobilisation of energetic sources, such as the breakdown of glycogen into circulating carbohydrates [ 72 , 73 ] and lipid [ 74 ], T. molitor may be a useful model to study the endocrine regulation of the immune responses in insects.…”

Section: Discussionmentioning

confidence: 99%

Morphological Characterisation of Haemocytes in the Mealworm Beetle Tenebrio molitor (Coleoptera, Tenebrionidae)

Vommaro

Kurtz

Giglio

2021

Insects

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The immunocompetence of the mealworm beetle Tenebrio molitor has been well investigated at molecular and physiological levels, but information on morphological and functional characteristics of its immune cells (haemocytes) is still scarce and fragmentary. This study provides an updated overview of the morphology of circulating immune cells from mealworm beetle adults, using light and transmission electron microscopy. Based on their affinities for May–Grünwald Giemsa stain, haemocytes were defined as either eosinophilic, basophilic or neutral. Ultrastructural descriptions allowed to detect four main cell types in the haemolymph: prohaemocytes, plasmatocytes, granular cells and oenocytoids. The morphological plasticity of haemocytes and the evidence of mitotic circulating cells, intermediate cell stages, as well as autophagic activities suggest haemocyte proliferation, turnover and transdifferentiation as constantly active processes in the haemolymph. Cytochemical tests revealed differences in the distribution of carbohydrates among cell types underling the great plasticity of the immune response and the direct involvement of circulating immune cells in the resource allocation. In addition, our results provide a detailed morphological description of vesicle trafficking, macro- and microautophagy, apoptotic and necrotic processes, confirming the suitability of T. molitor haemocytes as a model for studying evolutionarily conserved cellular mechanisms.

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Section: Discussionmentioning

confidence: 99%

Morphological Characterisation of Haemocytes in the Mealworm Beetle Tenebrio molitor (Coleoptera, Tenebrionidae)

Vommaro

Kurtz

Giglio

2021

Insects

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“…Generally, in Holometabola, the expression of AMPs is induced by sensing of specific molecular patterns that trigger the activation of the Toll or Imd pathways [10,[30][31][32][33]. However, there is increasing evidence of alternative regulators of innate immunity, including the moulting hormone, ecdysone [4][5][6][7][8][9]. In vertebrates, it has been known for many years that the immune system influences the secretion of hormones and that these, in turn, can influence immunity [3].…”

Section: Discussionmentioning

confidence: 99%

“…In vertebrates, steroid hormones and their nuclear receptors are key regulators of systemic immune responses, namely through the enhancement of inflammation [3]. Similarly, in insects, steroid hormones are also known to be involved in innate immunity [4][5][6][7][8][9]. In insects with complete metamorphosis (holometabolans), AMP genes are usually silent in the absence of an immune challenge and their expression is induced upon injury and/or infection [10].…”

Section: Introductionmentioning

confidence: 99%

Co-option of immune effectors by the hormonal signalling system triggering metamorphosis inDrosophila melanogaster

Nunes

Kaburagi

Sucena

2021

Preprint

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Insect metamorphosis is regulated by the production, secretion and degradation of two peripheral hormones: 20-hydroxyecdysone (ecdysone) and juvenile hormone (JH). In addition to their roles in developmental regulation, increasing evidence suggests that these hormones are involved in innate immunity processes, such as phagocytosis and the induction of antimicrobial peptide (AMP) production. AMP regulation includes systemic responses and local responses, at surface epithelia that contact with the external environments. At pupariation, Drosophila melanogaster increases dramatically the expression of three AMP genes: drosomycin (drs), drosomycin-like 2 (drsl2) and drosomycin-like 5 (drsl5). Using D. melanogaster, we show that the expression of drs at pupariation is dependent on ecdysone signalling in the fat body. This systemic immune response involving drs expression in the fat body operates via the ecdysone downstream target, Broad-Z4. In parallel, ecdysone also regulates local responses, specifically through the activation of drsl2 expression in the gut. Finally, we establish the relevance of this ecdysone dependent AMP expression for the control of bacterial persistence by showing that flies lacking drs expression in the fat body have higher bacterial persistence over metamorphosis. Together, our data establishes a new role for ecdysone during pupariation. We propose that the co-option of immune mechanisms by the hormonal cascade responsible for controlling metamorphosis constitutes a pre-emptive mechanism to control bacterial numbers in the pupa and increase developmental success.

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“…Most of the studies on signaling pathways and vector susceptibility/resistance to infection have focused on their role in the activation of immune pathways. These studies have been extensively discussed previously by others (Pakpour et al, 2013a(Pakpour et al, , 2014Urbanski and Rosinski, 2018;Sharma et al, 2019;Nunes et al, 2020). Among the best-known signaling pathways in insect vector species is the insulin/insulin-like growth factor signaling pathway (IIS), which is involved in the regulation of growth, longevity, reproduction and immunity.…”

Section: Blood Digestion and Metabolic Signalingmentioning

confidence: 99%

“…Several reports have shown hormonal effects on parasite infectivity, which, in Abbreviations: TG, triacylglycerol; TGFβ, transforming growth factor-beta; ILP, insulin-like peptides; PI3K, phosphoinositide 3-kinase; PKC, protein kinase C; ERK, extracellular signal-regulated kinase; MEK, MAPK/ERK kinase; NFκB, nuclear factor kappa-light-chain-enhancer of activated B cells; NRF-2, nuclear factor erythroid 2-related factor 2; OXR1, oxidation resistance protein 1; cGMP, cyclic guanosine monophosphate. some cases, have been attributed to a crosstalk between hormone signaling cascades and immune pathways (Nunes et al, 2020). Finally, for most blood-sucking insects, vertebrate hosts might be available more than once in a lifetime, and the effect of multiple blood meals have been shown to affect the life of pathogens by mechanisms that are not fully understood (Serafim et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Non-immune Traits Triggered by Blood Intake Impact Vectorial Competence

et al. 2021

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Blood-feeding arthropods are considered an enormous public health threat. They are vectors of a plethora of infectious agents that cause potentially fatal diseases like Malaria, Dengue fever, Leishmaniasis, and Lyme disease. These vectors shine due to their own physiological idiosyncrasies, but one biological aspect brings them all together: the requirement of blood intake for development and reproduction. It is through blood-feeding that they acquire pathogens and during blood digestion that they summon a collection of multisystemic events critical for vector competence. The literature is focused on how classical immune pathways (Toll, IMD, and JAK/Stat) are elicited throughout the course of vector infection. Still, they are not the sole determinants of host permissiveness. The dramatic changes that are the hallmark of the insect physiology after a blood meal intake are the landscape where a successful infection takes place. Dominant processes that occur in response to a blood meal are not canonical immunological traits yet are critical in establishing vector competence. These include hormonal circuitries and reproductive physiology, midgut permeability barriers, midgut homeostasis, energy metabolism, and proteolytic activity. On the other hand, the parasites themselves have a role in the outcome of these blood triggered physiological events, consistently using them in their favor. Here, to enlighten the knowledge on vector–pathogen interaction beyond the immune pathways, we will explore different aspects of the vector physiology, discussing how they give support to these long-dated host–parasite relationships.

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Endocrine regulation of immunity in insects

Cited by 51 publications

References 205 publications

Morphological Characterisation of Haemocytes in the Mealworm Beetle Tenebrio molitor (Coleoptera, Tenebrionidae)

Morphological Characterisation of Haemocytes in the Mealworm Beetle Tenebrio molitor (Coleoptera, Tenebrionidae)

Co-option of immune effectors by the hormonal signalling system triggering metamorphosis inDrosophila melanogaster

Non-immune Traits Triggered by Blood Intake Impact Vectorial Competence

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