Phenoloxidase activity in the reproductive system of Biomphalaria glabrata: role in egg production and effect of schistosome infection.
Infection by larval trematodes often causes a cessation of egg production in its molluscan intermediate host and is referred to as parasitic castration. Because phenoloxidase (PO) has been shown to be involved in egg formation in other invertebrate species, we investigated the role of PO in normal egg production in the snail, Biomphalaria glabrata, and the effects of Schistosoma mansoni infection on the PO pathway in this snail. Our data showed that PO activity in the albumen gland (AG) is initially expressed when snails reach a size of approximately 8 mm in shell diameter and continues to increase as snails grow, indicating a developmental link between snail size and AG PO expression. Egglaying was also shown to be coincidental with the onset of PO expression in the AG, thereby supporting a direct association between PO activity and egg production. In addition, exposure of snails to diethyldithiocarbamate (DDC), a PO inhibitor, affected normal in vivo egg production, as evidenced by a significant decrease in the numbers of eggs laid in DDC-treated groups compared to nontreated groups. Normal resumption of egg-laying activity in treated snails following withdrawal of the drug indicated that inhibition was reversible. Taken together, the results of our developmental and DDC-exposure studies provide strong support for a crucial role of PO in normal egg production in this animal. Finally, AG PO activities of infected and uninfected control snails were measured over the course of S. mansoni infection. Our results showed that both total and specific enzyme activities in the AG of infected snails were significantly decreased at 28 and 33 days postinfection (PI) when compared to those of control snails. Results of subsequent experiments assessing the effects of larval infection on L-tyrosine (PO substrate) levels in AG and ovotestis revealed a significant increase in the levels of this compound in both organs over the course of infection. It is concluded that AG PO activity is functionally linked to egg formation in normal snails and that a strong association exists between parasite-mediated decrease in AG PO activity and parasitic castration. However, from the data presented, a direct causal relationship linking infection, decreased PO, and castration has yet to be established.
Bai
G
G
Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin, Madison 53706, USA.
Johnston
L A
LA
Watson
C O
CO
Yoshino
T P
TP
D000818:Animals; D001700:Biomphalaria / Q000201:enzymology* / Q000469:parasitology* / Q000502:physiology; D004199:Disease Vectors; D004050:Ditiocarb / Q000494:pharmacology; D004791:Enzyme Inhibitors / Q000494:pharmacology; D005260:Female; D005835:Genitalia / Q000201:enzymology; D007814:Larva / Q000201:enzymology / Q000469:parasitology; D014442:Monophenol Monooxygenase / Q000037:antagonists & inhibitors / Q000378:metabolism / Q000502:physiology*; D010058:Oviposition / Q000187:drug effects / Q000502:physiology*; D012550:Schistosoma mansoni / Q000502:physiology*; D014443:Tyrosine / Q000032:analysis
D004791:Enzyme Inhibitors; D014443:Tyrosine; D004050:Ditiocarb; D014442:Monophenol Monooxygenase