scholarly journals Non-immune Traits Triggered by Blood Intake Impact Vectorial Competence

2021 ◽  
Vol 12 ◽  
Author(s):  
Octavio A. C. Talyuli ◽  
Vanessa Bottino-Rojas ◽  
Carla R. Polycarpo ◽  
Pedro L. Oliveira ◽  
Gabriela O. Paiva-Silva

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.

Insects ◽  
2020 ◽  
Vol 11 (3) ◽  
pp. 201
Author(s):  
Jeremiah Reyes ◽  
Cuauhtemoc Ayala-Chavez ◽  
Arvind Sharma ◽  
Michael Pham ◽  
Andrew B. Nuss ◽  
...  

Ixodes scapularis is the major vector of Lyme disease in the Eastern United States. Each active life stage (larva, nymph, and adult) takes a blood meal either for developing and molting to the next stage (larvae and nymphs) or for oviposition (adult females). This protein-rich blood meal is the only food taken by Ixodes ticks and therefore efficient blood digestion is critical for survival. Studies in partially engorged ticks have shown that the initial stages of digestion are carried out by cathepsin proteases within acidic digestive cells. In this study, we investigated the potential role of serine proteases in blood digestion in replete ticks. RNA interference was used for functional analysis and a trypsin-benzoyl-D, L-arginine 4-nitoanilide assay was used to measure active trypsin levels. Hemoglobinolytic activity was determined in vitro, with or without a serine protease inhibitor. Our data suggest that trypsin levels increase significantly after repletion. Knockdown of serine proteases negatively impacted blood feeding, survival, fecundity, levels of active trypsin in the midgut, and resulted in lower hemoglobin degradation. Incubation of midgut extract with a trypsin inhibitor resulted in 65% lower hemoglobin degradation. We provide evidence of the serine proteases as digestive enzymes in fully engorged, replete females. Understanding the digestive profile of trypsin during blood meal digestion in I. scapularis improves our understanding of the basic biology of ticks and may lead to new methods for tick control.


2018 ◽  
Author(s):  
James Orsborne ◽  
Luis Furuya-Kanamori ◽  
Claire L. Jeffries ◽  
Mojca Kristan ◽  
Abdul Rahim Mohammed ◽  
...  

AbstractDifficulties with observing the dispersal of insect vectors in the field have hampered understanding of several aspects of their behaviour linked to disease transmission. Here, a novel method based on detection of blood-meal sources is introduced to inform two critical and understudied mosquito behaviours: plasticity in the malaria vector’s blood-host choice and vector dispersal. Strategically located collections of Anopheles coluzzii from a malaria-endemic village of southern Ghana showed statistically significant variation in host species composition of mosquito blood-meals. Trialling a new sampling approach gave the first estimates for the remarkably local spatial scale across which host choice is plastic. Using quantitative PCR, the blood-meal digestion was then quantified for field-caught mosquitoes and calibrated according to timed blood digestion in colony mosquitoes. We demonstrate how this new ‘molecular Sella score’ approach can be used to estimate the dispersal rate of blood-feeding vectors caught in the field.


Author(s):  
Jeremiah Reyes ◽  
Cuauhtemoc Ayala-Chavez ◽  
Michael Pham ◽  
Arvind Sharma ◽  
Andrew Nuss ◽  
...  

Ixodes scapularis is the major vector of Lyme disease in the eastern United States. Each active life stage (larva, nymph, and adult) takes a blood meal either for developing and molting to the next stage (larvae and nymphs) or for oviposition (adult females). This protein-rich blood meal is the only food taken by Ixodes ticks and therefore blood digestion is very important for tick survival. Most studies on blood digestion in ticks have shown that the initial stages of digestion are carried out by cathepsin proteases within acidic digestive cells. However, most of these studies have focused on partially engorged ticks. In other hematophagous arthropods, the serine proteases play an important role in blood protein degradation. In this study, we determined transcript expression of four I. scapularis serine proteases with previously characterized roles in blood digestion. RNA interference was used for functional analysis and a trypsin-benzoyl-D, L-arginine 4-nitoanilide assay was used to measure active trypsin levels. An in vitro hemoglobinolytic assay was performed with or without serine protease inhibitor. Our data suggest that trypsin levels increase significantly after blood feeding and peaked in larvae, nymphs, and adults at 3, 1, and 1 day post host detachment, respectively. The knockdown of three previously identified serine proteases by RNAi negatively impacted blood intake, survival, fecundity, levels of active trypsin in the gut and resulted in lower hemoglobin degradation in vitro. A trypsin inhibitor, PMSF, blocked the action of trypsin in the gut extract resulting in 65% lower hemoglobin degradation. We provide evidence of the serine proteases as digestive enzymes in fully engorged, replete females. Our data also demonstrated that in addition to blood digestion, these serine proteases might have a role in blood feeding success in I. scapularis.


Author(s):  
Jeremiah Reyes ◽  
Cuauhtemoc Ayala-Chavez ◽  
Andrew Nuss ◽  
Monika Gulia-Nuss

Ixodes scapularis is the major vector of Lyme disease in the eastern United States. This species undergoes a life cycle consisting of eggs and three active stages: larva, nymph, and adult. Each active life stage takes a blood meal either for developing and molting to the next stage (larvae and nymphs) or for oviposition (adult females). This protein rich blood meal is the only food taken by Ixodes ticks. Most studies on blood digestion in ticks have shown that the initial stages of blood digestion are carried out by cathepsin proteases within endosomes of acidic digestive cells. However, in other hematophagous arthropods, the serine protease trypsin plays an important role in early protein degradation. In this study, we determined transcript expression of I. scapularis cathepsins and serine proteases, some with previously characterized roles in blood digestion. Gut pH was also determined and a trypsin-benzoyl-D, L-arginine 4-nitoanilide assay was used to measure active trypsin levels during blood digestion. Our data suggest that trypsin levels increase significantly after blood feeding and peaked in larvae, nymphs, and adults at 3, 1, and 1 days post host detachment, respectively. In addition, alkaline gut pH (8.0) conditions after I. scapularis blood feeding were similar to those required for trypsin activity in other arthropods suggesting these enzymes have an important and previously overlooked role in I. scapularis blood digestion.


2020 ◽  
Author(s):  
Yingjun Cui ◽  
Alexander W.E. Franz

AbstractMosquitoes are the most notorious hematophagous insects and due to their blood feeding behavior and genetic compatibility, numerous mosquito species are highly efficient vectors for certain human pathogenic parasites and viruses. The mosquito midgut is the principal organ of blood meal digestion and nutrient absorption. It is also the initial site of infection with blood meal acquired parasites and viruses. We conducted an analysis based on single-nucleus RNA sequencing (snRNA-Seq) to assess the cellular diversity of the midgut and how individual cells respond to blood meal ingestion to facilitate its digestion. Our study revealed the presence of 20 distinguishable cell-type clusters in the female midgut of Aedes aegypti. The identified cell types included intestinal stem cell (ISC), enteroblasts (EB), differentiating EB (dEB), enteroendocrine cells (EE), enterocytes (EC), EC-like cells, cardia cells, and visceral muscle (VM) cells. Blood meal ingestion dramatically changed the overall midgut cell type composition, profoundly increasing the proportions of ISC and three EC/EC like clusters. In addition, transcriptional profiles of all cell types were strongly affected while genes involved in various metabolic processes were significantly upregulated. Our study provides a basis for further physiological and molecular studies on blood digestion, nutrient absorption, and cellular homeostasis in the mosquito midgut.


1996 ◽  
Vol 86 (4) ◽  
pp. 351-354 ◽  
Author(s):  
Dave D. Chadee ◽  
John C. Beier ◽  
Raymond Martinez

AbstractThe cibarial armatures of Anopheles albitarsis Lynch Arribálzaga, A. aquasalis Curry, A. bellator Dyar & Knab and A. homunculus Komp are described for the first time. Ten to 15 minutes after blood feeding, higher levels of blood haemolysis were observed among A. bellator (14.9%) and A. homunculus (14.0%) mosquitoes which possessed type C cibarial armatures than among A. albitarsis (3.3%) and A. aquasalis (3.2%) which possessed type B cibarial armatures. In contrast, there were no significant differences among the four species in levels of extra-erythrocytic haemolysis when measured immediately and after one hour. The blood processing physiology observed for the four anopheline species is discussed at the enzymatic, mechanical and taxonomic levels as it relates to innate vector competence.


Author(s):  
Marvin S Godsey ◽  
Dominic Rose ◽  
Kristin L Burkhalter ◽  
Nicole Breuner ◽  
Angela M Bosco-Lauth ◽  
...  

Abstract Following the recent discovery of Bourbon virus (BRBV) as a human pathogen, and the isolation of the virus from Amblyomma americanum (L.) collected near the location of a fatal human case, we undertook a series of experiments to assess the laboratory vector competence of this tick species for BRBV. Larval ticks were infected using an immersion technique, and transstadial transmission of virus to the nymphal and then to the adult stages was demonstrated. Transstadially infected nymphs transmitted virus to adult ticks at very high rates during cofeeding, indicating the presence of infectious virus in the saliva of engorging ticks. Vertical transmission by transstadially infected females to their progeny occurred, but at a low rate. Rabbits fed on by infected ticks of all active life stages developed high titers of antibody to the virus, demonstrating host exposure to BRBV antigens/live virus during tick blood feeding. These results demonstrate that A. americanum is a competent vector of BRBV and indicate that cofeeding could be critical for enzootic maintenance.


Insects ◽  
2018 ◽  
Vol 9 (4) ◽  
pp. 177 ◽  
Author(s):  
Tereza Magalhaes ◽  
Alexis Robison ◽  
Michael Young ◽  
William Black ◽  
Brian Foy ◽  
...  

In urban settings, chikungunya, Zika, and dengue viruses are transmitted by Aedes aegypti mosquitoes. Since these viruses co-circulate in several regions, coinfection in humans and vectors may occur, and human coinfections have been frequently reported. Yet, little is known about the molecular aspects of virus interactions within hosts and how they contribute to arbovirus transmission dynamics. We have previously shown that Aedes aegypti exposed to chikungunya and Zika viruses in the same blood meal can become coinfected and transmit both viruses simultaneously. However, mosquitoes may also become coinfected by multiple, sequential feeds on single infected hosts. Therefore, we tested whether sequential infection with chikungunya and Zika viruses impacts mosquito vector competence. We exposed Ae. aegypti mosquitoes first to one virus and 7 days later to the other virus and compared infection, dissemination, and transmission rates between sequentially and single infected groups. We found that coinfection rates were high after sequential exposure and that mosquitoes were able to co-transmit both viruses. Surprisingly, chikungunya virus coinfection enhanced Zika virus transmission 7 days after the second blood meal. Our data demonstrate heterologous arbovirus synergism within mosquitoes, by unknown mechanisms, leading to enhancement of transmission under certain conditions.


Parasite ◽  
2018 ◽  
Vol 25 ◽  
pp. 61 ◽  
Author(s):  
Pavel Roudnický ◽  
Jiří Vorel ◽  
Jana Ilgová ◽  
Michal Benovics ◽  
Adam Norek ◽  
...  

Background: Serpins are a superfamily of serine peptidase inhibitors that participate in the regulation of many physiological and cell peptidase-mediated processes in all organisms (e.g. in blood clotting, complement activation, fibrinolysis, inflammation, and programmed cell death). It was postulated that in the blood-feeding members of the monogenean family Diplozoidae, serpins could play an important role in the prevention of thrombus formation, activation of complement, inflammation in the host, and/or in the endogenous regulation of protein degradation. Results: In silico analysis showed that the DNA and primary protein structures of serpin from Eudiplozoon nipponicum (EnSerp1) are similar to other members of the serpin superfamily. The inhibitory potential of EnSerp1 on four physiologically-relevant serine peptidases (trypsin, factor Xa, kallikrein, and plasmin) was demonstrated and its presence in the worm’s excretory-secretory products (ESPs) was confirmed. Conclusion: EnSerp1 influences the activity of peptidases that play a role in blood coagulation, fibrinolysis, and complement activation. This inhibitory potential, together with the serpin’s presence in ESPs, suggests that it is likely involved in host-parasite interactions and could be one of the molecules involved in the control of feeding and prevention of inflammatory responses.


Author(s):  
Seena Kumari ◽  
Tanwee Das De ◽  
Charu Chauhan ◽  
Jyoti Rani ◽  
Sanjay Tevatiya ◽  
...  

AbstractIn the adult female mosquito, successful blood meal acquisition is accomplished by salivary glands, which releases a cocktail of proteins to counteract vertebrate host’s immune-homeostasis. However, the biological relevance of many salivary proteins remains unknown. Here, we characterize a salivary specific Heme peroxidase family member HPX12, originally identified from Plasmodium vivax infected salivary RNAseq data of the mosquito Anopheles stephensi. We demonstrate that dsRNA silencing mediated mRNA depletion of salivary AsHPX12 (80-90%), causes enhanced host attraction but reduced blood-meal acquisition abilities, by increasing probing propensity (31%), as well as probing time (100–200s, P<0.0001) as compared to control (35-90s) mosquitoes group. Altered expression of the salivary secretory and antennal proteins may account for an unusual fast release of salivary cocktail proteins, but the slowing acquisition of blood meal, possibly due to salivary homeostasis disruption of AsHPX12 silenced mosquitoes. A parallel transcriptional modulation in response to blood feeding and P. vivax infection, further establish a possible functional correlation of AsHPX12 role in salivary immune-physiology and Plasmodium sporozoites survival/transmission. We propose that salivary HPX12 may have a vital role in the management of ‘pre- and post’-blood meal associated physiological-homeostasis and parasite transmission.Graphical abstractFigure 1:Schematic representation of mosquito’s blood meal acquisition and upshot on blood-feeding after silencing of salivary gland HPX-12. (A) After landing over host skin, mosquito mouthparts (proboscis) actively engaged to search, probe, and pierce the skin followed by a rapid release of the pre-synthesized salivary cocktail, which counteracts the host homeostasis, inflammation, and immune responses, during blood meal uptake. (B) Silencing of HPX-12 disrupts salivary gland homeostasis, enhancing mosquito attraction, possibly by up-regulating odorant-binding proteins genes-OBP-7,10 and OBP-20 expression in the Olfactory System. However, HPX-12 disruption may also cause significant effects on pre-blood meal associated probing abilities, which may be due to fast down-regulation of salivary cocktail proteins such as Anopheline, Apyrase, D7L proteins.


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