Limits...
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).

Show MeSH

Related in: MedlinePlus

Effect of hyaluronidase on Leishmania infection in mice.BALB/c mice were coinoculated intradermally into ear with 104 or 105 Leishmania major and hyaluronidase equivalent to 0, 2 and 10 salivary glands of Phlebotomus papatasi. Lesion size, given as a product of its area (mm2) and the degree of ulceration (1–5), was monitored for 6 weeks post infection. Points (▪) = mean values, boxes = 95% confidence intervals, whiskers = min-max values. The p values of corresponding Kruskal-Wallis ANOVA are provided.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2553483&req=5

pntd-0000294-g006: Effect of hyaluronidase on Leishmania infection in mice.BALB/c mice were coinoculated intradermally into ear with 104 or 105 Leishmania major and hyaluronidase equivalent to 0, 2 and 10 salivary glands of Phlebotomus papatasi. Lesion size, given as a product of its area (mm2) and the degree of ulceration (1–5), was monitored for 6 weeks post infection. Points (▪) = mean values, boxes = 95% confidence intervals, whiskers = min-max values. The p values of corresponding Kruskal-Wallis ANOVA are provided.

Mentions: Next we examined whether hyaluronidase altered the course of Leishmania major infection in BALB/c mice. We used intradermal inoculation into the ear and the disease burden was calculated from weekly measuring the lesion size. As shown in Fig. 6, mice coinjected with parasites and hyaluronidase developed bigger lesions. In all groups of mice, the onset of lesion development was at three weeks p.i. Thereafter, the lesions grew faster in coinoculated groups. The experiment was terminated six weeks post infection when, in some animals, ulcerating lesion spread over the majority of ear pinna. In mice inoculated by higher parasite numbers (105), both hyaluronidase treatments produced similar effects (Fig. 6A). In mice with an inoculation dose one order of magnitude lower (104), the effect of hyaluronidase was concentration-dependent: lesions were bigger in mice coinoculated with hyaluronidase activity equivalent of 10 P. papatasi salivary glands than in those coinoculated with equivalent of 2 glands (Fig. 6B). In both parasite numbers (104 and 105) over all considered weeks (3 to 6) post-inoculation, Kruskal- Wallis ANOVA showed significant differences among hyaluronidase treatments (p always≤0.025), with only one exception in week 3 of 104 parasites treatment (p = 0.23). Consequently, the post-hoc comparison of treatments tests confirmed the significant difference between controls (no hyaluronidase) and corresponding inoculated hyaluronidase doses (2 or 10 glands equivalents). We also tested the difference between the 2 and 10 gland equivalent doses: however, despite the common trends apparent in Fig. 6 indicating that there may be a systematic difference between 2 and 10 gland equivalents doses, the post-hoc comparison of treatments test did not prove it in any case but in week 5 of the 104 parasites treatment.


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)

Effect of hyaluronidase on Leishmania infection in mice.BALB/c mice were coinoculated intradermally into ear with 104 or 105 Leishmania major and hyaluronidase equivalent to 0, 2 and 10 salivary glands of Phlebotomus papatasi. Lesion size, given as a product of its area (mm2) and the degree of ulceration (1–5), was monitored for 6 weeks post infection. Points (▪) = mean values, boxes = 95% confidence intervals, whiskers = min-max values. The p values of corresponding Kruskal-Wallis ANOVA are provided.
© Copyright Policy
Related In: Results  -  Collection

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

pntd-0000294-g006: Effect of hyaluronidase on Leishmania infection in mice.BALB/c mice were coinoculated intradermally into ear with 104 or 105 Leishmania major and hyaluronidase equivalent to 0, 2 and 10 salivary glands of Phlebotomus papatasi. Lesion size, given as a product of its area (mm2) and the degree of ulceration (1–5), was monitored for 6 weeks post infection. Points (▪) = mean values, boxes = 95% confidence intervals, whiskers = min-max values. The p values of corresponding Kruskal-Wallis ANOVA are provided.
Mentions: Next we examined whether hyaluronidase altered the course of Leishmania major infection in BALB/c mice. We used intradermal inoculation into the ear and the disease burden was calculated from weekly measuring the lesion size. As shown in Fig. 6, mice coinjected with parasites and hyaluronidase developed bigger lesions. In all groups of mice, the onset of lesion development was at three weeks p.i. Thereafter, the lesions grew faster in coinoculated groups. The experiment was terminated six weeks post infection when, in some animals, ulcerating lesion spread over the majority of ear pinna. In mice inoculated by higher parasite numbers (105), both hyaluronidase treatments produced similar effects (Fig. 6A). In mice with an inoculation dose one order of magnitude lower (104), the effect of hyaluronidase was concentration-dependent: lesions were bigger in mice coinoculated with hyaluronidase activity equivalent of 10 P. papatasi salivary glands than in those coinoculated with equivalent of 2 glands (Fig. 6B). In both parasite numbers (104 and 105) over all considered weeks (3 to 6) post-inoculation, Kruskal- Wallis ANOVA showed significant differences among hyaluronidase treatments (p always≤0.025), with only one exception in week 3 of 104 parasites treatment (p = 0.23). Consequently, the post-hoc comparison of treatments tests confirmed the significant difference between controls (no hyaluronidase) and corresponding inoculated hyaluronidase doses (2 or 10 glands equivalents). We also tested the difference between the 2 and 10 gland equivalent doses: however, despite the common trends apparent in Fig. 6 indicating that there may be a systematic difference between 2 and 10 gland equivalents doses, the post-hoc comparison of treatments test did not prove it in any case but in week 5 of the 104 parasites treatment.

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