Skip to main content

Advertisement

SpringerLink
Log in

The embryonic development of Schistosoma mansoni eggs: proposal for a new staging system

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

Schistosomiasis is a water-borne parasitic illness caused by neoophoran trematodes of the genus Schistosoma. Using classical histological techniques and whole-mount preparations, the present work describes the embryonic development of Schistosoma mansoni eggs in the murine host and compares it with eggs maintained under in vitro conditions. Two pre-embryonic stages occur inside the female worm: the prezygotic stage is characterized by the release of mature oocytes from the female ovary until its fertilization. The zygotic stage encompasses the migration of the zygote through the ootype, where the eggshell is formed, to the uterus. Fully formed eggs are laid still undeveloped, without having suffered any cleavage. In the outside environment, eight embryonic stages can be defined: stage 1 refers to early cleavages and the beginning of yolk fusion. Stage 2 represents late cleavage, with the formation of a stereoblastula and the onset of outer envelope differentiation. Stage 3 is defined by the elongation of the embryonic primordium and the onset of inner envelope formation. At stage 4, the first organ primordia arise. During stages 5 to 7, tissue and organ differentiation occurs (neural mass, epidermis, terebratorium, musculature, and miracidial glands). Stage 7 is characterized by the nuclear condensation of neurons of the central neural mass. Stage 8 refers to the fully formed larva, presenting muscular contraction, cilia, and flame-cell beating. This staging system was compared to a previous classification and could underlie further studies on egg histoproteomics (morphological localizome). The differentiation of embryonic structures and their probable roles in granulomatogenesis are discussed herein.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Andrade ZA, Barka T (1962) Histochemical observations on experimental schistosomiasis of mouse. Am J Trop Med Hyg 11:12–16

    PubMed  CAS  Google Scholar 

  • Andrade ZA, Sadigursky M (1978) Immunofluorescence studies of schistosome structures which share determinants with circulating schistosome antigens. Trans R Soc Trop Med Hyg 72:316–317

    Article  PubMed  CAS  Google Scholar 

  • Asahi H, Stadecker MJ (2003) Analysis of egg antigens inducing hepatic lesions in schistosome infection. Parasitol Int 52:361–367

    Article  PubMed  CAS  Google Scholar 

  • Ashton PD, Harrop R, Shah B, Wilson RA (2001) The schistosome egg: development and secretions. Parasitology 122:329–338

    Article  PubMed  CAS  Google Scholar 

  • Bahia D, Avelar LGA, Vigorosi F, Cioli D, Oliveira GC, Mortara RA (2006) The distribution of motor proteins in the muscles and flame cells of the Schistosoma mansoni miracidium and primary sporocyst. Parasitology 133:321–329

    Article  PubMed  CAS  Google Scholar 

  • Bancroft JD, Stevens A (1996) Theory and practice of histological techniques, 4th edn. Churchill Livingstone, New York

    Google Scholar 

  • Basch PF, Samuelson J (1990) Cell biology of schistosomes. I. Ultrastructure and transformations. In: Wyler DJ (ed) Modern parasite biology: cellular, immunological, and molecular aspects. Freeman, New York, pp 91–106

    Google Scholar 

  • Baskic D, Popovic S, Ristic P, Arsenijevic NN (2006) Analysis of cycloheximide-induced apoptosis in human leukocytes: fluorescence microscopy using annexin V/propidium iodide versus acridin orange/ethidium bromide. Cell Biol Int 30:924–932

    Article  PubMed  CAS  Google Scholar 

  • Bobek L, Rekosh DM, van Keulen H, LoVerde PT (1986) Characterization of a female-specific cDNA derived from a developmentally regulated mRNA in the human blood fluke Schistosoma mansoni. Proc Natl Acad Sci U S A 83:5544–5548

    Article  PubMed  CAS  Google Scholar 

  • Cardona A, Hartenstein V, Romero R (2005) The embryonic development of the triclad Schmidtea polychroa. Dev Genes Evol 215:109–131

    Article  PubMed  Google Scholar 

  • Cardona A, Hartenstein V, Romero R (2006) Early embryogenesis of planaria: a cryptic larva feeding on maternal resources. Dev Genes Evol 216:667–681

    Article  PubMed  Google Scholar 

  • Carson FL, Martin JH, Lynn JA (1973) Formalin fixation for electron microscopy: a re-evaluation. Am J Clin Pathol 59:365–373

    PubMed  CAS  Google Scholar 

  • Cass CL, Johnson JR, Califf LL, Xu T, Hernandez HJ, Stadecker MJ, Yates JR 3rd, Williams DL (2007) Proteomic analysis of Schistosoma mansoni egg secretions. Mol Biochem Parasitol 155:84–93

    Article  PubMed  CAS  Google Scholar 

  • Chen LL, Rekosh DM, LoVerde PT (1992) Schistosoma mansoni p48 eggshell protein gene: characterization, developmentally regulated expression and comparison to the p14 eggshell protein gene. Mol Biochem Parasitol 52:39–52

    Article  PubMed  CAS  Google Scholar 

  • Chernin E (1970) Behavioral responses of miracidia of Schistosoma mansoni and other trematodes to substances emitted by snails. J Parasitol 56:287–296

    Article  PubMed  CAS  Google Scholar 

  • Chernin E (1974) Some host-finding attributes of Schistosoma mansoni miracidia. Am J Trop Med Hyg 23:320–327

    PubMed  CAS  Google Scholar 

  • Chitsulo L, Engels D, Montresor A, Savioli L (2000) The global status of schistosomiasis and its control. Acta Trop 77:41–51

    Article  PubMed  CAS  Google Scholar 

  • Coelho MV (1957) Aspectos do desenvolvimento de formas larvárias de Schistosoma mansoni em Australorbis nigricans. Rev Bras Biol 17:325–337

    Google Scholar 

  • Coelho PMZ, Andrade ZA, Borges C, Ribeiro F, Barbosa L (2008) Evolução do Schistosoma mansoni no Hospedeiro Intermediário. In: Carvalho ODS, Coelho PMZ, Lenzi HL (eds) Schistosoma mansoni e Esquistossomose: uma visão multidisciplinar. Fiocruz, Rio de Janeiro, pp 147–160

    Google Scholar 

  • Conn DB, Swiderski Z (2008) A standardised terminology of the embryonic envelopes and associated developmental stages of tapeworms (Platyhelminthes: Cestoda). Folia Parasitol (Praha) 55:42–52

    Google Scholar 

  • Cunha AS, Pellegrino J, Oliveira CA, Alvarenga RJ (1962) Observations on the oogram in guinea pigs and rabbits experimentally infected with Schistosoma mansoni. Rev Inst Med Trop Sao Paulo 4:242–248

    PubMed  CAS  Google Scholar 

  • Dalton JP, Day SR, Drew AC, Brindley PJ (1997) A method for the isolation of schistosome eggs and miracidia free of contaminating host tissues. Parasitology 115(Pt 1):29–32

    Article  PubMed  Google Scholar 

  • de Araujo SC, de Mattos AC, Teixeira HF, Coelho PM, Nelson DL, de Oliveira MC (2007) Improvement of in vitro efficacy of a novel schistosomicidal drug by incorporation into nanoemulsions. Int J Pharm 337:307–315

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org. Accessed 7 Feb 2009

  • Dorsey CH, Cousin CE, Lewis FA, Stirewalt MA (2002) Ultrastructure of the Schistosoma mansoni cercaria. Micron 33:279–323

    Article  PubMed  Google Scholar 

  • Dresden MH, Payne DC (1981) A sieving method for the collection of schistosome eggs from mouse intestines. J Parasitol 67:450–452

    Article  PubMed  CAS  Google Scholar 

  • Ehlers U (1985) Das phylogenetische System der Plathelminthes. Fischer, Stuttgart

    Google Scholar 

  • Eklu-Natey DT, Wuest J, Swiderski Z, Striebel HP, Huggel H (1985) Comparative scanning electron microscope (SEM) study of miracidia of four human schistosome species. Int J Parasitol 15:33–42

    Article  PubMed  CAS  Google Scholar 

  • Erasmus DA (1975) The subcellular localization of labelled tyrosine in the vitelline cells of Schistosoma mansoni. Z Parasitenkd 46:75–81

    Article  PubMed  CAS  Google Scholar 

  • Erasmus DA, Popiel I, Shaw JR (1982) A comparative study of the vitelline cell in Schistosoma mansoni, S. haematobium, S. japonicum and S. mattheei. Parasitology 84:283–287

    PubMed  CAS  Google Scholar 

  • Espin J (1941) La sustancia meplasmática en los nódulos producidos por Schistosoma mansoni. Rev Pol Caracas 10:73–90

    Google Scholar 

  • Fitzpatrick JM, Johansen MV, Johnston DA, Dunne DW, Hoffmann KF (2004) Gender-associated gene expression in two related strains of Schistosoma japonicum. Mol Biochem Parasitol 136:191–209

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatrick JM, Hirai Y, Hirai H, Hoffmann KF (2007) Schistosome egg production is dependent upon the activities of two developmentally regulated tyrosinases. FASEB J 21:823–835

    Article  PubMed  CAS  Google Scholar 

  • Freitas TC, Jung E, Pearce EJ (2007) TGF-beta signaling controls embryo development in the parasitic flatworm Schistosoma mansoni. PLoS Pathog 3:e52

    Article  PubMed  CAS  Google Scholar 

  • Gobert GN, Chai M, McManus DP (2007) Biology of the schistosome lung-stage schistosomulum. Parasitology 134:453–460

    Article  PubMed  CAS  Google Scholar 

  • Gonçalves T (2008) Correlação entre a difusão de material antigênico de ovo de Schistosoma mansoni com a expressão de moléculas de adesão de complexos juncionais em granulomas hepáticos murinos. Master's Dissertation, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro

  • Gonnert R (1955) Schistosomiasis-Studien, 1 Beitrage zur Anatomie und Histologie von Schistosoma mansoni. Z Tropenmed Parasitol 6:18–33

    PubMed  CAS  Google Scholar 

  • Gschwentner R, Ladurner P, Nimeth K, Rieger R (2001) Stem cells in a basal bilaterian. S-phase and mitotic cells in Convolutriloba longifissura (Acoela, Platyhelminthes). Cell Tissue Res 304:401–408

    Article  PubMed  CAS  Google Scholar 

  • Haas W, Haberl B, Schmalfuss G, Khayyal MT (1994) Schistosoma haematobium cercarial host-finding and host-recognition differs from that of S. mansoni. J Parasitol 80:345–353

    Article  PubMed  CAS  Google Scholar 

  • Haberl B, Kalbe M, Fuchs H, Ströbel M, Schmalfuss G, Haas W (1995) Schistosoma mansoni and S. haematobium: miracidial host-finding behaviour is stimulated by macromolecules. Int J Parasitol 25:551–560

    Article  PubMed  CAS  Google Scholar 

  • Hartenstein V, Ehlers U (2000) The embryonic development of the rhabdocoel flatworm Mesostoma lingua (Abildgaard, 1789). Dev Genes Evol 210:399–415

    Article  PubMed  CAS  Google Scholar 

  • Hartenstein V, Jones M (2003) The embryonic development of the body wall and nervous system of the cestode flatworm Hymenolepis diminuta. Cell Tissue Res 311:427–435

    PubMed  Google Scholar 

  • Hwang JS, Kobayashi C, Agata K, Ikeo K, Gojobori T (2004) Detection of apoptosis during planarian regeneration by the expression of apoptosis-related genes and TUNEL assay. Gene 333:15–25

    Article  PubMed  CAS  Google Scholar 

  • Johnson KS, Taylor DW, Cordingley JS (1987) Possible eggshell protein gene from Schistosoma mansoni. Mol Biochem Parasitol 22:89–100

    Article  PubMed  CAS  Google Scholar 

  • Jurberg AD, Oliveira AA, Lenzi HL, Coelho PM (2008a) A new miracidia hatching device for diagnosing schistosomiasis. Mem Inst Oswaldo Cruz 103:112–114

    Article  PubMed  Google Scholar 

  • Jurberg AD, Pascarelli BM, Pelajo-Machado M, Maldonado A Jr, Mota EM, Lenzi HL (2008b) Trematode embryology: a new method for whole-egg analysis by confocal microscopy. Dev Genes Evol 218:267–271

    Article  PubMed  Google Scholar 

  • Knobloch J, Kunz W, Grevelding CG (2006) Herbimycin A suppresses mitotic activity and egg production of female Schistosoma mansoni. Int J Parasitol 36:1261–1272

    Article  PubMed  CAS  Google Scholar 

  • Koster B, Dargatz H, Schroder J, Hirzmann J, Haarmann C, Symmons P, Kunz W (1988) Identification and localisation of the products of a putative eggshell precursor gene in the vitellarium of Schistosoma mansoni. Mol Biochem Parasitol 31:183–198

    Article  PubMed  CAS  Google Scholar 

  • Kusel JR, Oliveira FA, Todd M, Ronketti F, Lima SF, Mattos AC, Reis KT, Coelho PM, Thornhill JA, Ribeiro F (2006) The effects of drugs, ions, and poly-l-lysine on the excretory system of Schistosoma mansoni. Mem Inst Oswaldo Cruz 101(Suppl 1):293–298

    PubMed  CAS  Google Scholar 

  • Larsson LI, Bjerregaard B, Talts JF (2008) Cell fusions in mammals. Histochem Cell Biol 129:551–561

    Article  PubMed  CAS  Google Scholar 

  • Lennert K (1978) Malignant lymphomas other than Hodgkin's disease. Springer, Berlin

    Google Scholar 

  • Lenzi HL, Lenzi JA, Sobral AC (1987) Eosinophils favor the passage of eggs to the intestinal lumen in schistosomiasis. Br J Med Biol Res 20:433–435

    CAS  Google Scholar 

  • Lenzi HL, Lenzi JA, Kerr IB, Antunes SL, Mota EM, Oliveira DN (1991) Extracellular matrix in parasitic and infectious diseases. Mem Inst Oswaldo Cruz 86:77–90

    Article  PubMed  Google Scholar 

  • Lenzi HL, Jurberg AD, Coelho PMZ, Lenzi JA (2008) Migração e Desenvolvimento do Schistosoma mansoni no Hospedeiro Definitivo. In: Carvalho ODS, Coelho PMZ, Lenzi HL (eds) Schistosoma mansoni e Esquistossomose: uma visão multidisciplinar. Fiocruz, Rio de Janeiro, pp 85–145

    Google Scholar 

  • Lewert RM, Lee CL (1954) Studies on the passage of helminth larvae through host tissues. I. Histochemical studies on the extracellular changes caused by penetrating larvae. II. Enzymatic activity of larvae in vitro and in vivo. J Infect Dis 95:13–51

    PubMed  CAS  Google Scholar 

  • Lewert RM, Para J, Ozcel MA (1970) Miracidial uptake of glucose in intact eggs of Schistosoma mansoni. J Parasitol 56:1250–1251

    Article  PubMed  CAS  Google Scholar 

  • Lillie RD, Fullmer HM (1976) Histopathological technique and practical histochemistry. McGraw Hill, New York

    Google Scholar 

  • Littlewood DTJ, Rohde K, Bray RA, Herniou EA (1999) Phylogeny of the Platyhelminthes and the evolution of parasitism. Biol J Linn Soc Lond 68:257–287

    Article  Google Scholar 

  • Machado-Silva JR, Pelajo-Machado M, Lenzi HL, Gomes DC (1998) Morphological study of adult male worms of Schistosoma mansoni Sambon, 1907 by confocal laser scanning microscopy. Mem Inst Oswaldo Cruz 93(Suppl 1):303–307

    PubMed  Google Scholar 

  • Maldonado JF, Acosta-Matienzo J (1947) Evolution del Schistosoma mansoni dentro de su hosped intermediário, el caracol Australorbis glabratus. P R J Public Health Trop Med 22:374–404

    Google Scholar 

  • McLaren DJ (1980) Schistosoma mansoni: the parasite surface in relation to host immunity. Research Studies, New York

    Google Scholar 

  • Michaels RM, Prata A (1968) Evolution and characteristics of Schistosoma mansoni eggs laid in vitro. J Parasitol 54:921–930

    Article  PubMed  CAS  Google Scholar 

  • Michel A, Knobloch J, Kunz W (2003) P19: a female and tissue specifically expressed gene in Schistosoma mansoni, regulated by pairing with the male. Parasitology 127:519–524

    Article  PubMed  CAS  Google Scholar 

  • Moore DV, Sandground JH (1956) The relative egg producing capacity of Schistosoma mansoni and Schistosoma japonicum. Am J Trop Med Hyg 5:831–840

    PubMed  CAS  Google Scholar 

  • Morris J, Nallur R, Ladurner P, Egger B, Rieger R, Hartenstein V (2004) The embryonic development of the flatworm Macrostomum sp. Dev Genes Evol 214:220–239

    Article  PubMed  Google Scholar 

  • Neill PJ, Smith JH, Doughty BL, Kemp M (1988) The ultrastructure of the Schistosoma mansoni egg. Am J Trop Med Hyg 39:52–65

    PubMed  CAS  Google Scholar 

  • Neves RH, de Lamare Biolchini C, Machado-Silva JR, Carvalho JJ, Branquinho TB, Lenzi HL, Hulstijn M, Gomes DC (2005) A new description of the reproductive system of Schistosoma mansoni (Trematoda: Schistosomatidae) analyzed by confocal laser scanning microscopy. Parasitol Res 95:43–49

    Article  PubMed  Google Scholar 

  • Nimeth K, Ladurner P, Gschwentner R, Salvenmoser W, Rieger R (2002) Cell renewal and apoptosis in Macrostomum sp. [Lignano]. Cell Biol Int 26:801–815

    Article  PubMed  CAS  Google Scholar 

  • Oren-Suissa M, Podbilewicz B (2007) Cell fusion during development. Trends Cell Biol 17:537–546

    PubMed  CAS  Google Scholar 

  • Ottolina C (1957) El miracidio del Schistosoma mansoni: anatomía, citología, fisiología. Rev Sanid Asist Soc 22:1–412 discussion 413–420

    PubMed  CAS  Google Scholar 

  • Pan SC (1980) The fine structure of the miracidium of Schistosoma mansoni. J Invertebr Pathol 36:307–372

    Article  PubMed  CAS  Google Scholar 

  • Pan SC (1996) Schistosoma mansoni: the ultrastructure of larval morphogenesis in Biomphalaria glabrata and of associated host–parasite interactions. Jpn J Med Sci Biol 49:129–149

    PubMed  CAS  Google Scholar 

  • Pellegrino J, Coelho PM (1978) Schistosoma mansoni: wandering capacity of a worm couple. J Parasitol 64:181–182

    Article  PubMed  CAS  Google Scholar 

  • Pellegrino J, Faria J (1965) The oogram method for the screening of drugs in schistosomiasis mansoni. Am J Trop Med Hyg 14:363–369

    PubMed  CAS  Google Scholar 

  • Pellegrino J, Oliveira CA, Faria J, Cunha AS (1962) New approach to the screening of drugs in experimental schistosomiasis mansoni in mice. Am J Trop Med Hyg 11:201–215

    PubMed  CAS  Google Scholar 

  • Peralta JM (1986) Obtenção e caracterização de anticorpos monoclonais para antígenos de Schistosoma mansoni. Ph.D. Thesis, Instituto de Microbiologia, Universidade Federal do Rio de Janeiro-UFRJ, Rio de Janeiro

  • Podbilewicz B (2006) Cell fusion. WormBook, pp 1–32

  • Prata A (1957) Biópsia retal na esquistossomose mansoni — bases e aplicações no diagnóstico e tratamento. Serviço Nacional de Educação Sanitária-Ministério da Saúde, Rio de Janeiro

    Google Scholar 

  • Ramachandra NB, Gates RD, Ladurner P, Jacobs DK, Hartenstein V (2002) Embryonic development in the primitive bilaterian Neochildia fusca: normal morphogenesis and isolation of POU genes Brn-1 and Brn-3. Dev Genes Evol 212:55–69

    Article  PubMed  CAS  Google Scholar 

  • Reis MG, Kuhns J, Blanton R, Davis AH (1989) Localization and pattern of expression of a female specific mRNA in Schistosoma mansoni. Mol Biochem Parasitol 32:113–119

    Article  PubMed  CAS  Google Scholar 

  • Saladin KS (1982) Schistosoma mansoni: cercarial responses to irradiance changes. J Parasitol 68:120–124

    Article  PubMed  CAS  Google Scholar 

  • Sarvel AK, Kusel JR, Araujo N, Coelho P, Katz N (2006) Comparison between morphological and staining characteristics of live and dead eggs of Schistosoma mansoni. Mem Inst Oswaldo Cruz 101(Suppl 1):289–292

    PubMed  Google Scholar 

  • Schramm G, Gronow A, Knobloch J, Wippersteg V, Grevelding CG, Galle J, Fuller H, Stanley RG, Chiodini PL, Haas H, Doenhoff MJ (2006) IPSE/alpha-1: a major immunogenic component secreted from Schistosoma mansoni eggs. Mol Biochem Parasitol 147:9–19

    Article  PubMed  CAS  Google Scholar 

  • Schussler P, Potters E, Winnen R, Bottke W, Kunz W (1995) An isoform of ferritin as a component of protein yolk platelets in Schistosoma mansoni. Mol Reprod Dev 41:325–330

    Article  PubMed  CAS  Google Scholar 

  • Sorour F (1929) Contribution a l'etude des tumeurs irratitives bénignes et malignes produites par les Bilharzies. Ann Parasit 7:381–398

    Google Scholar 

  • Stirewalt MA (1974) Schistosoma mansoni: cercaria to schistosomule. Adv Parasitol 12:115–182

    Article  PubMed  CAS  Google Scholar 

  • Stjernholm RL, Warren KS (1974) Schistosoma mansoni: utilization of exogenous metabolites by eggs in vitro. Exp Parasitol 36:222–232

    Article  PubMed  CAS  Google Scholar 

  • Swiderski Z (1994) Origin, differentiation and ultrastructure of egg envelopes surrounding the miracidia of Schistosoma mansoni. Acta Parasitol 39:64–72

    Google Scholar 

  • Tyler S, Tyler MS (1997) Origin of the epidermis in parasitic platyhelminths. Int J Parasitol 27:715–738

    Article  PubMed  CAS  Google Scholar 

  • Van de Vijver KK, Deelder AM, Jacobs W, Van Marck EA, Hokke CH (2006) LacdiNAc- and LacNAc-containing glycans induce granulomas in an in vivo model for schistosome egg-induced hepatic granuloma formation. Glycobiology 16:237–243

    Article  PubMed  CAS  Google Scholar 

  • Vogel H (1942) Über Entwicklung, Lebensdauer und Tod der Eier vom Bilharzia japonica im Wirtsgewebe. Dtsch Tropenmed Ztsch 46:57–91

    Google Scholar 

  • Warren KS (1978) The pathology, pathobiology and pathogenesis of schistosomiasis. Nature 273:609–612

    Article  PubMed  CAS  Google Scholar 

  • Wells KE, Cordingley JS (1991) Schistosoma mansoni: eggshell formation is regulated by pH and calcium. Exp Parasitol 73:295–310

    Article  PubMed  CAS  Google Scholar 

  • Williams DL, Asahi H, Botkin DJ, Stadecker MJ (2001) Schistosome infection stimulates host CD4(+) T helper cell and B-cell responses against a novel egg antigen, thioredoxin peroxidase. Infect Immun 69:1134–1141

    Article  PubMed  CAS  Google Scholar 

  • Wilson RA (1987) Cercariae to liver worms: development and migration in the mammalian host. In: Rollinson D, Simpson AJG (eds) The biology of schistosomes: from genes to latrines. Academic, London, pp 115–146

    Google Scholar 

  • World Health Organization (2006) Report of the Scientific Working Group meeting on Schistosomiasis. WHO, Geneva

    Google Scholar 

  • Younossi-Hartenstein A, Hartenstein V (2000a) Comparative approach to developmental analysis: the case of the dalyellid flatworm, Gieysztoria superba. Int J Dev Biol 44:499–506

    PubMed  CAS  Google Scholar 

  • Younossi-Hartenstein A, Hartenstein V (2000b) The embryonic development of the polyclad flatworm Imogine mcgrathi. Dev Genes Evol 210:383–398

    Article  PubMed  CAS  Google Scholar 

  • Younossi-Hartenstein A, Hartenstein V (2001) The embryonic development of the temnocephalid flatworms Craspedella pedum and Diceratocephala boschmai. Cell Tissue Res 304:295–310

    Article  PubMed  CAS  Google Scholar 

  • Younossi-Hartenstein A, Ehlers U, Hartenstein V (2000) Embryonic development of the nervous system of the rhabdocoel flatworm Mesostoma lingua (Abilgaard, 1789). J Comp Neurol 416:461–474

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors acknowledge the staff of the Laboratório de Patologia-IOC/Fiocruz and of the Laboratório de Esquistossomose-CPqRR/Fiocruz for technical assistance, Mr. Bruno Eschenazi from the Setor de Produção e Tratamento de Imagens-IOC/Fiocruz for the schematic drawing of S. mansoni egg embryonic development, Dr. Jane Arnt Lenzi from the Laboratório de Patologia-IOC/Fiocruz and Dr. John R Kusel from the Glasgow University for critical review of the manuscript, and Dr. Jennifer Rowland from the Laboratory of Patterning and Morphogenesis-Instituto Gulbenkian de Ciência for the English review. ADJ and TG received fellowships from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)—Brazil. TAC and ACA de M received fellowships from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)—Brazil. The work was supported by the Fundação Oswaldo Cruz (Fiocruz).

Author information

Author notes

  1. Arnon D. Jurberg & Tiana Gonçalves

    Present address: Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, 2781-901, Oeiras, Portugal

Authors and Affiliations

  1. Laboratório de Patologia, Instituto Oswaldo Cruz (IOC)/Fundação Oswaldo Cruz (Fiocruz), Pavilhão Gomes de Faria. Av. Brasil, 4365—Manguinhos, CEP: 21040-900, Rio de Janeiro, RJ, Brazil

    Arnon D. Jurberg, Tiana Gonçalves, Tatiane A. Costa, Bernardo M. Pascarelli, Pedro Paulo A. de Manso, Marcelo Pelajo-Machado & Henrique L. Lenzi

  2. Laboratório de Esquistossomose, Instituto René Rachou (CPqRR)/Fiocruz, Belo Horizonte, MJ, Brazil

    Ana Carolina A. de Mattos & Paulo Marcos Z. Coelho

  3. Centro de Desenvolvimento Tecnológico em Saúde (CDTS)/Fiocruz, Rio de Janeiro, RJ, Brazil

    Marcelo Ribeiro-Alves

  4. Instituto de Microbiologia/Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

    José M. Peralta

Authors
  1. Arnon D. Jurberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tiana Gonçalves
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tatiane A. Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ana Carolina A. de Mattos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bernardo M. Pascarelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Pedro Paulo A. de Manso
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marcelo Ribeiro-Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marcelo Pelajo-Machado
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. José M. Peralta
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Paulo Marcos Z. Coelho
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Henrique L. Lenzi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Arnon D. Jurberg or Henrique L. Lenzi.

Additional information

Communicated by D. A. Weisblat

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary methods (DOC 30 kb)

Supplementary results (DOC 27 kb)

Fig. S1

Interaction plots between each evaluated main effect. a Egg maturation stages at its source. b Egg source at its maturation stage. The nonparallel nature of lines connecting the mean area at levels of one main source put into a hierarchy by the levels of the other main source suggests interaction, as mentioned in the text. (GIF 62 kb)

High-Resolution Image (TIFF 18 kb)

Fig. S2

Model good fitting diagnostics. a Plot of residual quantiles against theoretical normal quantiles (Q–Q norm plot) shows a moderate tail and about 97% of data fitting the straight line, which suggests its normal distribution. b Box plot of padronized residuals shows a median value equal to null and a symmetric interquantile range (box), also suggesting a normal residual distribution. (GIF 47 kb)

High-Resolution Image (TIFF 13 kb)

Fig. S3

Distribution of the main effect levels of egg estimated areas during maturation. a Box plot of estimated areas of eggs for the source main effect levels, cultivated and isolated. Cultivated eggs are significant bigger than those eggs isolated from the murine host (P = 0.00017). b Box plot of estimated area of eggs for the maturation stage main effect levels, ordered in roman numerals(I to V). Eggs increase in size as embryos develop. (GIF 40 kb)

High-Resolution Image (TIFF 25 kb)

Fig. S4

Statistical analysis of egg growth. a, b Only the biologically relevant relationships were plotted, i.e., M-I:M-II, M-II:M-III, M-III:M-IV, and M-IV:M-V, where M is the maturation stage in roman numerals (according to Vogel and Prata's classification). a Simultaneous 95% confidence intervals for comparing estimated mean areas of cultivated eggs during growth under in vitro conditions (RPMI-1640 medium). b Simultaneous 95% confidence intervals for comparing estimated mean areas of isolated eggs during growth in the murine host. The overlapping of confidence intervals with the vertical dotted line at abscissa 0 indicates no pairwise difference between maturation stages at a level of confidence set as 0.05. Positive significant mean differences are higher than 0 for the lower intervals, while negative significant mean differences are lower than 0 for higher intervals. See details in the text. c Box plot of egg area during different stages of maturation (M) in regard to egg source (S). S1 refers to eggs obtained from the host and S2 refers to eggs maintained in culture. d Simultaneous 95% confidence intervals for comparing estimated mean areas of each matching stages for both sources (isolated and cultivated), i.e. M-I:M-I, M-II: M-II, M-III:M-III, M-IV:M-IV, and M-V:M-V. (GIF 92 kb)

High-Resolution Image (TIFF 67 kb)

Fig. S5

Oogram technique by bright field and confocal microscopies. a, b Bright field micrographs of compressed fragments of S. mansoni-infected mouse intestines. a Classical oogram. Three mature eggs are shown. b Compressed intestinal fragment stained with hydrochloric carmine analyzed by BM. It is difficult to identify the stages of maturation in each egg. c–e Confocal laser scanning microscope images of carmine-stained fragments of compressed intestines. c Sagittal section of two mature eggs (stage 8) and a third egg in an oblique view. nm, neural mass; np, neuropile; lg, lateral glands; gc, germinal cells. d Stage 2 egg, with the developing embryo (em). The stereoblastula and the yolk are visible. e Stage 3 egg, with an elongated embryo (em) and some yolk (yk). Scale bars 100 µm (GIF 69 kb)

High-Resolution Image (TIFF 962 kb)

Supplementary Table 1

Number of eggs counted per each Vogel and Prata's stage. The eggs were obtained from S. mansoni-infected mice and from culture. (DOC 29 kb)

Supplementary Table 2

Estimated mean areas (µm2) during S. mansoni egg growth in mice (isolated) and under in vitro conditions (cultivated). (DOC 169 kb)

Schistosoma mansoni embryo at stage 3 (MPG 3670 kb)

Schistosoma mansoni embryo at stage 6 (MPG 5014 kb)

Schistosoma mansoni embryo at stage 8 (mature miracidium) (MPG 3080 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jurberg, A.D., Gonçalves, T., Costa, T.A. et al. The embryonic development of Schistosoma mansoni eggs: proposal for a new staging system. Dev Genes Evol 219, 219–234 (2009). https://doi.org/10.1007/s00427-009-0285-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-009-0285-9

Keywords

Search

Navigation