Defense reactions of mosquitoes to filarial worms: Potential mechanism for avoidance of the response by Brugia pahangi microfilariae

Lafond, Michele M.; Christensen, Bruce M.; Lasee, Becky A.

doi:10.1016/0022-2011(85)90126-0

Cited by 16 publications

(4 citation statements)

References 12 publications

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“…Previous studies in our laboratory suggest that LF parasites either elicit an immune response, e.g., melanotic encapsulation, or go undetected and therefore unmolested by an immune response in certain mosquitoes [28],[40]. Although the interactions between these nematodes and the mosquito immune system are mechanistically undescribed, there is potential for LF parasites to evade and/or suppress the mosquito immune system [41]–[44]. In this study, we manipulated the mosquito immune system in an effort to activate immune response pathways to determine what effects, if any, they might have on parasite infection and development.…”

Section: Discussionmentioning

confidence: 97%

Mosquito Infection Responses to Developing Filarial Worms

Erickson

Mayhew

et al. 2009

PLoS Negl Trop Dis

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Human lymphatic filariasis is a mosquito-vectored disease caused by the nematode parasites Wuchereria bancrofti, Brugia malayi and Brugia timori. These are relatively large roundworms that can cause considerable damage in compatible mosquito vectors. In order to assess how mosquitoes respond to infection in compatible mosquito-filarial worm associations, microarray analysis was used to evaluate transcriptome changes in Aedes aegypti at various times during B. malayi development. Changes in transcript abundance in response to the different stages of B. malayi infection were diverse. At the early stages of midgut and thoracic muscle cell penetration, a greater number of genes were repressed compared to those that were induced (20 vs. 8). The non-feeding, intracellular first-stage larvae elicited few differences, with 4 transcripts showing an increased and 9 a decreased abundance relative to controls. Several cecropin transcripts increased in abundance after parasites molted to second-stage larvae. However, the greatest number of transcripts changed in abundance after larvae molted to third-stage larvae and migrated to the head and proboscis (120 induced, 38 repressed), including a large number of putative, immunity-related genes (∼13% of genes with predicted functions). To test whether the innate immune system of mosquitoes was capable of modulating permissiveness to the parasite, we activated the Toll and Imd pathway controlled rel family transcription factors Rel1 and Rel2 (by RNA interference knockdown of the pathway's negative regulators Cactus and Caspar) during the early stages of infection with B. malayi. The activation of either of these immune signaling pathways, or knockdown of the Toll pathway, did not affect B. malayi in Ae. aegypti. The possibility of LF parasites evading mosquito immune responses during successful development is discussed.

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Section: Discussionmentioning

confidence: 97%

Mosquito Infection Responses to Developing Filarial Worms

Erickson

Mayhew

et al. 2009

PLoS Negl Trop Dis

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“…This may be due to inability of the haemocytes to recognize the trypanosomes as being non-self as reported to occur with some parasitoid eggs, which become coated by substances recognized as self by their insect host haemocytes (Salt, 1968;Salt, 1973), and which are quickly destroyed by the insect cellular defences if the surface coat is removed. Sutherland et al (1984) and Lafond et al (1985) reported that when microfilariae of B. pahangi are allowed to penetrate A. aegypti midguts in vitro prior to their intrathoracic inoculation into A. aegypti, the microfilariae acquire a significantly increased ability to evade the host encapsulation reaction and they concluded that when the microfilariae penetrate through the gut, they become coated with mosquito host antigens which enable them to be recognized as self by the mosquito immune system and thus to escape encapsulation. Sutherland et al (1984) and Lafond et al (1985) reported that when microfilariae of B. pahangi are allowed to penetrate A. aegypti midguts in vitro prior to their intrathoracic inoculation into A. aegypti, the microfilariae acquire a significantly increased ability to evade the host encapsulation reaction and they concluded that when the microfilariae penetrate through the gut, they become coated with mosquito host antigens which enable them to be recognized as self by the mosquito immune system and thus to escape encapsulation.…”

Section: Discussionmentioning

confidence: 99%

A review of the progress made in recent years on research and understanding of immunity in insect vectors of human and animal diseases

Kaaya

1989

Int. J. Trop. Insect Sci.

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Different modes of immune reactions of insect vectors of human and animal diseases to nematode and protozoan parasites, fungi, bacteria, viruses and to other biological materials e.g. xenografts are discussed in this paper. Since most of the insect vectors of diseases are adult dipterans with low numbers of circulating haemocytes, their mode of defence against metazoan parasites and fungal pathogens is primarily by means of humoral encapsulation, with little haemocyte participation. Although earlier workers reported that humoral capsules in dipterans were formed without direct participation by haemocytes, this paper reveals increasing evidence of cellular involvement in the formation of humoral capsules, both at the initial and terminal stages of the encapsulation process. The role of phenoloxidase system in non-self recognition and in the process of melanization of haemolymph and capsules formed around parasites and fungal pathogens is also discussed. Immune defence of insect vectors against bacterial invasion by means of haemocytic reactions e.g. phagocytosis and nodule formation and by synthesis and release of humoral antibacterial factors e.g. lysozyme, attacins and cecropins is described and compared with similar reactions reported to occur in other insects. The role of lectins in defence of insect vectors against the parasites they transmit e.g. sandflies against Leishmania, blackflies against Onchocerca and tsetse against Trypanosomes is discussed and the possible mechanisms by which some parasites evade recognition and attack by the vector immune systems are also briefly discussed. Resume-Les differents modes de reactions immunisees des insectes vecteurs de maladies humaines et animates contre les nematodes et les protozoaires parasites, les champignons les bacteries, les viruses et autres materiels biologiques par exemple xenogratis sont discutes dans cette publication. Comme plus d' insectes vecteurs de maladies sont des dipteres adultes ayant un nombre inferieur d'hemocytes, leur mode de defense contre les metazoaires parasites et les champignons pathogenes est principalement par moyen d'encapsulation humorale, avec une moindre participation d'hemocyte. Bien que des recherches anterieures ont montre que les capsules humorales chez les dipteres etaient formees sans participation directe d'hemocytes, cette publication revele une Evidence accrue sur la participation cellulaire dans la formation des capsules humorales, au niveau initial et final du processus d'encapsulation. Le rdle du systeme phenoloxidase dans le processus de melanisation d'hemolymphe et les capsules formees autour des parasites et des champignons pathogenes est aussi discute. La defense immunisee des insectes vecteurs contre l'invasion bactlrienne par moyen de reactions hemocytaire par exemple la phagocy tose et la formation de nodules et par la synthese et la liberation des elements antibacteriens humoraux par example lysosomes, attacines et cecropines est decrite et com par ee aux reaction apparues chez d'autres insectes. Le rdle de l...

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“…The reasons why most of the mf of B. pahangi are not encapsulated are largely unknown. It has been suggested that mf acquire midgut antigens on their surface during migration through the midgut wall (Sutherland et al, 1984;LaFond et al, 1985). Christensen et al (1987), however, failed to detect midgut antigens on the surface of midgut-penetrated mf though a significant loss of microfilarial surface electronegativity was observed.…”

Section: Resultsmentioning

confidence: 88%

Surface lectin binding characteristics of developing stages of Brugia in Armigeres subalbatus: I. Brugia pahangi.

Zahedi

Denham

Ham

1990

Jap. J. Trop. Med. Hyg.

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Abstract:Surface characteristics of microfilariae and developing stages of Brugia pahangi in its natural vector, Armigeres subalbatus were assayed using fluorescein isothiocynate conjugated lectins. The following lectins were used: wheat germ agglutinins, lentil agglutinins, Helix aspersa agglutinins, Concanavalin A agglutinins, kidney bean agglutinins, asparagus pea agglutinins and pea nut agglutinins. It was observed that developing stages of B. pahangi the mosquito showed a dynamic surface carbohydrate characteristics.The larvae change their surface coat configuration frequently during the 10 day observation period. However, blood dwelling microfilariae and fully matured infective larvae obtained from the mosquito's head showed little or no binding affinity for the lectins tested. It's postulated that the rapid turnover of the surface carbohydrates, while development of the larvae is taking place, is the worm's response to a 'hostile' mosquito environment.

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Defense reactions of mosquitoes to filarial worms: Potential mechanism for avoidance of the response by Brugia pahangi microfilariae

Cited by 16 publications

References 12 publications

Mosquito Infection Responses to Developing Filarial Worms

Mosquito Infection Responses to Developing Filarial Worms

A review of the progress made in recent years on research and understanding of immunity in insect vectors of human and animal diseases

Surface lectin binding characteristics of developing stages of Brugia in Armigeres subalbatus: I. Brugia pahangi.

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