Schistosome egg production is dependent upon the activities of two developmentally regulated tyrosinases

FASEB Journal

Volumn 21, Issue 3, 2007, Pages 823-835

  Fitzpatrick, Jennifer M ^a   Hirai, Yuriko ^b   Hirai, Hirohisa ^b   Hoffmann, Karl F ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

Developmental regulation; Helminth; Kojic acid; Schistosoma

Indexed keywords

CATECHOL OXIDASE; KOJIC ACID; MONOPHENOL MONOOXYGENASE; TYROSINASE 1; TYROSINASE 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME 4; EGG PRODUCTION; EGG SHELL; ENZYME ACTIVITY; ENZYME STRUCTURE; FEMALE; GENE DUPLICATION; GENE LOCATION; GENETIC TRANSCRIPTION; IN VITRO STUDY; LINKAGE ANALYSIS; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SCHISTOSOMA MANSONI;

ANIMALS; MONOPHENOL MONOOXYGENASE; OVUM; SCHISTOSOMA; SCHISTOSOMIASIS;

PLATYHELMINTHES; SCHISTOSOMA; SCHISTOSOMA MANSONI; VERMES; VITELLARIA;

EID: 33847690240     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-7314com     Document Type: Article

References (48)

1. King, C. H., Dickman, K., and Tisch, D. J. (2005) Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365, 1561-1569
2. Bergquist, N. R., and Colley, D. G. (1998) Schistosomiasis vaccines: research to development. Parasitol. Today 14, 99-104
3. Hagan, P., Appleton, C. C., Coles, G. C., Kusel, J. R., and Tchuem-Tchuente, L. A. (2004) Schistosomiasis control: keep taking the tablets. Trends. Parasitol. 20, 92-97
4. Kabatereine, N. B., Vennervald, B. J., Ouma, J. H., Kemijumbi, J., Butterworth, A. E., Dunne, D. W., and Fulford, A. J. (1999) Adult resistance to schistosomiasis mansoni: age-dependence of reinfection remains constant in communities with diverse exposure patterns. Parasitology 118, 101-105
5. Cioli, D., and Pica-Mattoccia, L. (2003) Praziquantel. Parasitol. Res. 90 Supp. 1, S3-S9
6. Doenhoff, M. J., Kusel, J. R., Coles, G. C., and Cioli, D. (2002) Resistance of Schistosoma mansoni to praziquantel: is there a problem? Trans. R. Soc. Trop. Med. Hyg. 96, 465-469
7. 2+ channels targets of praziquantel action? Int. J. Parasitol. 35, 1-9
8. Ribeiro-Dos-Santos, G., Verjovski-Almeida, S., and Leite, L. C. (2006) Schistosomiasis-a century searching for chemotherapeutic drugs. Parasitol. Res. 99, 505-521
9. Hoffmann, K. F., Wynn, T. A., and Dunne, D. W. (2002) Cytokine-mediated host responses during schistosome infections; walking the fine line between immunological control and immunopathology. Adv. Parasitol. 52, 265-307
10. Hoffmann, K. F., Johnston, D. A., and Dunne, D. W. (2002) Identification of Schistosoma mansoni gender-associated gene transcripts by cDNA microarray profiling [Online]. Genome Biol. 3, RESEARCH0041
11. Fitzpatrick, J. M., Johnston, D. A., Williams, G. W., Williams, D. J., Freeman, T. C., Dunne, D. W., and Hoffmann, K. F. (2005) An oligonucleotide microarray for transcriptome analysis of Schistosoma mansoni and its application/use to investigate gender-associated gene expression. Mol. Biochem. Parasitol. 141, 1-13
12. Fitzpatrick, J. M., Johansen, M. V., Johnston, D. A., Dunne, D. W., and Hoffmann, K. F. (2004) Gender-associated gene expression in two related strains of Schistosoma japonicum. Mol. Biochem. Parasitol. 136, 191-209
13. Garcia-Borron, J. C., and Solano, F. (2002) Molecular anatomy of tyrosinase and its related proteins: beyond the histidine-bound metal catalytic center. Pigment. Cell. Res. 15, 162-173
14. Smyth, J. D., and Clegg, J. A. (1959) Egg-shell formation in trematodes and cestodes. Exp. Parasitol. 8, 286-323
15. Erasmus, D. A. (1973) A comparative study of the reproductive system of mature, immature and "unisexual" female Schistosoma mansoni. Parasitology 67, 165-183
16. Smithers, S. R., and Terry, R. J. (1965) The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology 55, 695-700
17. Nielsen, H., Engelbrecht, J., Brunak, S., and von Heijne, G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein. Eng. 10, 1-6
18. Claros, M. G., and von Heijne, G. (1994) TopPred II: an improved software for membrane protein structure predictions. Comput. Appl. Biosci. 10, 685-686
19. Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540-552
20. Huelsenbeck, J. P., and Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 17, 754-755
21. Whelan, S., and Goldman, N. (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18, 691-699
22. Page, R. D. M. (1996) TreeView: An application to display phylogenetic trees on personal computers. Computer. Applications. in. the. Biosciences. 12, 357-358
23. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, ME.
24. Hirai, H., and LoVerde, P. T. (1995) FISH techniques for constructing physical maps on schistosome chromosomes. Parasitol. Today 11, 310-314
25. Winder, A. J., and Harris, H. (1991) New assays for the tyrosine hydroxylase and dopa oxidase activities of tyrosinase. Eur. J. Biochem. 198, 317-326
26. Kim, Y. J., No, J. K., Lee, J. H., and Chung, H. Y. (2005) 4,4′-Dihydroxybiphenyl as a new potent tyrosinase inhibitor. Biol. Pharm. Bull. 28, 323-327
27. Lei, T. C., Virador, V. M., Vieira, W. D., and Hearing, V. J. (2002) A melanocyte-keratinocyte coculture model to assess regulators of pigmentation in vitro. Anal. Biochem. 305, 260-268
28. Gaykema, W. P., Volbeda, A., and Hol, W. G. (1986) Structure determination of Panulirus interruptus haemocyanin at 3.2 A resolution. Successful phase extension by sixfold density averaging. J. Mol. Biol. 187, 255-275
29. Klabunde, T., Eicken, C., Sacchettini, J. C., and Krebs, B. (1998) Crystal structure of a plant catechol oxidase containing a dicopper center. Nat. Struct. Biol. 5, 1084-1090
30. Neves, R. H., de Lamare Biolchini, C., Machado-Silva, J. R., Carvalho, J. J., Branquinho, T. B., Lenzi, H. L., Hulstijn, M., and Gomes, D. C. (2005) A new description of the reproductive system of Schistosoma mansoni (Trematoda: Schistosomatidae) analyzed by confocal laser scanning microscopy. Parasitol. Res. 95, 43-49
31. Olds, G. R., Olveda, R., Wu, G., Wiest, P., McGarvey, S., Aligui, G., Zhang, S., Ramirez, B., Daniel, B., Peters, P., Romulo, R., Fevidal, P., Tiu, W., Yuan, J., Domingo, E., and Blas, B. (1996) Immunity and morbidity in Schistosomiasis japonicum infection. Am. J. Trop. Med. Hyg. 55, 121-126
32. Seed, J. L., and Bennett, J. L. (1980) Schistosoma mansoni: phenol oxidase's role in eggshell formation. Exp. Parasitol. 49, 430-441
33. Seed, J. L., Boff, M., and Bennett, J. L. (1978) Phenol oxidase activity: induction in female schistosomes by in vitro incubation. J. Parasitol. 64, 283-289
34. Seed, J. L., Kilts, C. D., and Bennett, J. L. (1980) Schistosoma mansoni: tyrosine, a putative in vivo substrate of phenol oxidase. Exp. Parasitol. 50, 33-44
35. Wells, K. E., and Cordingley, J. S. (1991) Schistosoma mansoni: eggshell formation is regulated by pH and calcium. Exp. Parasitol. 73, 295-310
36. Ebersberger, I., Knobloch, J., and Kunz, W. (2005) Cracks in the shell-zooming in on eggshell formation in the human parasite Schistosoma mansoni. Dev. Genes. Evol. 215, 261-267
37. Fitzpatrick, J. M., and Hoffmann, K. F. (2006) Dioecious Schistosoma mansoni express divergent gene repertoires regulated by pairing. Int. J. Parasitol. 36, 1081-1089
38. Shaw, M. K. (1987) Schistosoma mansoni: vitelline gland development in females from single sex infections. J. Helminthol. 61, 253-259
39. Boonanuntanasarn, S., Yoshizaki, G., Iwai, K., and Takeuchi, T. (2004) Molecular cloning, gene expression in albino mutants and gene knockdown studies of tyrosinase mRNA in rainbow trout. Pigment. Cell. Res. 17, 413-421
40. Sturrock, R. F. (1966) Daily egg output of schistosomes. Trans. Roy. Soc. Trop. Med. Hyg. 60, 139-140
41. Gerdemann, C., Eicken, C., and Krebs, B. (2002) The crystal structure of catechol oxidase: new insight into the function of type-3 copper proteins. Acc. Chem. Res. 35, 183-191
42. Eshete, F., and LoVerde, P. T. (1993) Characteristics of phenol oxidase of Schistosoma mansoni and its functional implications in eggshell synthesis. J. Parasitol. 79, 309-317
43. Ribeiro-Paes, J. T., and Rodrigues, V. (1995) Electrophoretical and histochemical characterization of Schistosoma mansoni phenol oxidases. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 111, 69-74
44. Wang, F. L., Su, Y. F., Yang, G. M., Wang, X. Z., Qiu, Z. Y., Zhou, X. K., and Hu, Z. Q. (1986) Isoenzymes of phenol oxidase in adult female Schistosoma japonicum. Mol. Biochem. Parasitol. 18, 69-72
45. Colhoun, L. M., Fairweather, I., and Brennan, G. P. (1998) Observations on the mechanism of eggshell formation in the liver fluke, Fasciola hepatica. Parasitology 116 (Pt 6): 555-567
46. Pearce, E. J., Caspar, P., Grzych, J. M., Lewis, F. A., and Sher, A. (1992) Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma. mansoni. J. Exp. Med. 173, 159-162
47. Hill, D. E., and Fetterer, R. H. (1997) The effect of disulfiram on egg shell formation in adult Trichuris muris. J. Parasitol. 83, 938-942
48. Alverson, J. (2003) Effects of mycotoxins, kojic acid and oxalic acid, on biological fitness of Lygus hesperus (Heteroptera: Miridae). J. Invertebr. Pathol. 83, 60-62