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Hyaluronidase of bloodsucking insects and its enhancing effect on leishmania infection in mice.

Volfova V, Hostomska J, Cerny M, Votypka J, Volf P - PLoS Negl Trop Dis (2008)

Bottom Line: No activity was found in kissing bug Rhodnius prolixus, mosquitoes Anopheles stephensi and Aedes aegypti, tse-tse fly Glossina fuscipes, stable fly Stomoxys calcitrans and human louse Pediculus humanus.Hyaluronidases of different insects vary substantially in their molecular weight, the structure of the molecule and the sensitivity to reducing conditions or sodium dodecyl sulphate.As this enzyme is present in all Phlebotomus and Lutzomyia species studied to date, it seems to be one of the factors responsible for enhancing activity present in sand fly saliva.

View Article: PubMed Central - PubMed

Affiliation: Department of Parasitology, Faculty of Science, Charles University in Prague, Czech Republic. volf@cesnet.cz

ABSTRACT

Background: Salivary hyaluronidases have been described in a few bloodsucking arthropods. However, very little is known about the presence of this enzyme in various bloodsucking insects and no data are available on its effect on transmitted microorganisms. Here, we studied hyaluronidase activity in thirteen bloodsucking insects belonging to four different orders. In addition, we assessed the effect of hyaluronidase coinoculation on the outcome of Leishmania major infection in BALB/c mice.

Principal findings: High hyaluronidase activity was detected in several Diptera tested, namely deer fly Chrysops viduatus, blackflies Odagmia ornata and Eusimilium latipes, mosquito Culex quinquefasciatus, biting midge Culicoides kibunensis and sand fly Phlebotomus papatasi. Lower activity was detected in cat flea Ctenocephalides felis. No activity was found in kissing bug Rhodnius prolixus, mosquitoes Anopheles stephensi and Aedes aegypti, tse-tse fly Glossina fuscipes, stable fly Stomoxys calcitrans and human louse Pediculus humanus. Hyaluronidases of different insects vary substantially in their molecular weight, the structure of the molecule and the sensitivity to reducing conditions or sodium dodecyl sulphate. Hyaluronidase exacerbates skin lesions caused by Leishmania major; more severe lesions developed in mice where L. major promastigotes were coinjected with hyaluronidase.

Conclusions: High hyaluronidase activities seem to be essential for insects with pool-feeding mode, where they facilitate the enlargement of the feeding lesion and serve as a spreading factor for other pharmacologically active compounds present in saliva. As this enzyme is present in all Phlebotomus and Lutzomyia species studied to date, it seems to be one of the factors responsible for enhancing activity present in sand fly saliva. We propose that salivary hyaluronidase may facilitate the spread of other vector-borne microorganisms, especially those transmitted by insects with high hyaluronidase activity, namely blackflies (Simuliidae), biting midges (Ceratopogonidae) and horse flies (Tabanidae).

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Substrate specificity of hyaluronidases tested on polyacrylamide gel with incorporated chondroitin sulfate.Protein content per 2 µl dot is indicated in brackets. Sh = sheep testicular hyaluronidase (10 µg), Cf = Ctenocephalides felis SGE (20 µg), Cq = Culex quinquefasciatus SGE (0.8 µg), Ck = Culicoides kibunensis BE (20 µg), Pp = Phlebotomus papatasi SGE (0.8 µg), Cv = Chrysops viduatus SGE (0.8 µg).
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pntd-0000294-g002: Substrate specificity of hyaluronidases tested on polyacrylamide gel with incorporated chondroitin sulfate.Protein content per 2 µl dot is indicated in brackets. Sh = sheep testicular hyaluronidase (10 µg), Cf = Ctenocephalides felis SGE (20 µg), Cq = Culex quinquefasciatus SGE (0.8 µg), Ck = Culicoides kibunensis BE (20 µg), Pp = Phlebotomus papatasi SGE (0.8 µg), Cv = Chrysops viduatus SGE (0.8 µg).

Mentions: The dot method on gels with copolymerized HA and chondroitin sulfate was used to study the presence of hyaluronidase activity and its substrate specificity. The highest hydrolysis of HA was observed in SGE of deer fly Chrysops viduatus. Pronounced hydrolysis was found in SGEs of blackflies Odagmia ornata and Eusimulium latipes, mosquito Culex quinquefasciatus, sand fly Phlebotomus papatasi and whole body extract of biting midge Culicoides kibunensis (syn. C. cubitalis). Lower activity was detected in BE of cat flea Ctenocephalides felis (Fig. 1). On the other hand, no detectable hydrolysis of HA occurred in SGEs of kissing bug Rhodnius prolixus, mosquitoes Anopheles stephensi and Aedes aegypti, tse-tse fly Glossina fuscipes, stable fly Stomoxys calcitrans and in thoracic extracts of human louse Pediculus humanus (Fig. 1). Positive samples were then tested also for chondroitin sulfate hydrolysis (Fig. 2). High activity was observed in Culex quinquefasciatus and Culicoides kibunensis, in other samples the hydrolysis of chondroitin sulfate was either moderate (Chrysops viduatus) or low (Phlebotomus papatasi, Ctenocephalides felis) (Fig. 2); clearly, HA is the preferred substrate for the enzymes of these three insects.


Hyaluronidase of bloodsucking insects and its enhancing effect on leishmania infection in mice.

Volfova V, Hostomska J, Cerny M, Votypka J, Volf P - PLoS Negl Trop Dis (2008)

Substrate specificity of hyaluronidases tested on polyacrylamide gel with incorporated chondroitin sulfate.Protein content per 2 µl dot is indicated in brackets. Sh = sheep testicular hyaluronidase (10 µg), Cf = Ctenocephalides felis SGE (20 µg), Cq = Culex quinquefasciatus SGE (0.8 µg), Ck = Culicoides kibunensis BE (20 µg), Pp = Phlebotomus papatasi SGE (0.8 µg), Cv = Chrysops viduatus SGE (0.8 µg).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2553483&req=5

pntd-0000294-g002: Substrate specificity of hyaluronidases tested on polyacrylamide gel with incorporated chondroitin sulfate.Protein content per 2 µl dot is indicated in brackets. Sh = sheep testicular hyaluronidase (10 µg), Cf = Ctenocephalides felis SGE (20 µg), Cq = Culex quinquefasciatus SGE (0.8 µg), Ck = Culicoides kibunensis BE (20 µg), Pp = Phlebotomus papatasi SGE (0.8 µg), Cv = Chrysops viduatus SGE (0.8 µg).
Mentions: The dot method on gels with copolymerized HA and chondroitin sulfate was used to study the presence of hyaluronidase activity and its substrate specificity. The highest hydrolysis of HA was observed in SGE of deer fly Chrysops viduatus. Pronounced hydrolysis was found in SGEs of blackflies Odagmia ornata and Eusimulium latipes, mosquito Culex quinquefasciatus, sand fly Phlebotomus papatasi and whole body extract of biting midge Culicoides kibunensis (syn. C. cubitalis). Lower activity was detected in BE of cat flea Ctenocephalides felis (Fig. 1). On the other hand, no detectable hydrolysis of HA occurred in SGEs of kissing bug Rhodnius prolixus, mosquitoes Anopheles stephensi and Aedes aegypti, tse-tse fly Glossina fuscipes, stable fly Stomoxys calcitrans and in thoracic extracts of human louse Pediculus humanus (Fig. 1). Positive samples were then tested also for chondroitin sulfate hydrolysis (Fig. 2). High activity was observed in Culex quinquefasciatus and Culicoides kibunensis, in other samples the hydrolysis of chondroitin sulfate was either moderate (Chrysops viduatus) or low (Phlebotomus papatasi, Ctenocephalides felis) (Fig. 2); clearly, HA is the preferred substrate for the enzymes of these three insects.

Bottom Line: No activity was found in kissing bug Rhodnius prolixus, mosquitoes Anopheles stephensi and Aedes aegypti, tse-tse fly Glossina fuscipes, stable fly Stomoxys calcitrans and human louse Pediculus humanus.Hyaluronidases of different insects vary substantially in their molecular weight, the structure of the molecule and the sensitivity to reducing conditions or sodium dodecyl sulphate.As this enzyme is present in all Phlebotomus and Lutzomyia species studied to date, it seems to be one of the factors responsible for enhancing activity present in sand fly saliva.

View Article: PubMed Central - PubMed

Affiliation: Department of Parasitology, Faculty of Science, Charles University in Prague, Czech Republic. volf@cesnet.cz

ABSTRACT

Background: Salivary hyaluronidases have been described in a few bloodsucking arthropods. However, very little is known about the presence of this enzyme in various bloodsucking insects and no data are available on its effect on transmitted microorganisms. Here, we studied hyaluronidase activity in thirteen bloodsucking insects belonging to four different orders. In addition, we assessed the effect of hyaluronidase coinoculation on the outcome of Leishmania major infection in BALB/c mice.

Principal findings: High hyaluronidase activity was detected in several Diptera tested, namely deer fly Chrysops viduatus, blackflies Odagmia ornata and Eusimilium latipes, mosquito Culex quinquefasciatus, biting midge Culicoides kibunensis and sand fly Phlebotomus papatasi. Lower activity was detected in cat flea Ctenocephalides felis. No activity was found in kissing bug Rhodnius prolixus, mosquitoes Anopheles stephensi and Aedes aegypti, tse-tse fly Glossina fuscipes, stable fly Stomoxys calcitrans and human louse Pediculus humanus. Hyaluronidases of different insects vary substantially in their molecular weight, the structure of the molecule and the sensitivity to reducing conditions or sodium dodecyl sulphate. Hyaluronidase exacerbates skin lesions caused by Leishmania major; more severe lesions developed in mice where L. major promastigotes were coinjected with hyaluronidase.

Conclusions: High hyaluronidase activities seem to be essential for insects with pool-feeding mode, where they facilitate the enlargement of the feeding lesion and serve as a spreading factor for other pharmacologically active compounds present in saliva. As this enzyme is present in all Phlebotomus and Lutzomyia species studied to date, it seems to be one of the factors responsible for enhancing activity present in sand fly saliva. We propose that salivary hyaluronidase may facilitate the spread of other vector-borne microorganisms, especially those transmitted by insects with high hyaluronidase activity, namely blackflies (Simuliidae), biting midges (Ceratopogonidae) and horse flies (Tabanidae).

Show MeSH
Related in: MedlinePlus