Abstract
Litomosoides chagasfilhoi is a filariid nematode parasite of the abdominal cavity of the wild rodent Akodon cursor (Winge, 1887), that has been described and used in Brazil as a new model for human filariasis. The fine structure of the intestine of this nematode was analyzed based on observations made by light and transmission electron microscopies of serial sections along the body. Cytochemical analysis was carried out to investigate the composition of the intestinal wall. This structure consisted of a basal lamina and an epithelium of variable thickness, composed of cells that have an irregular shape. The cytoplasm of intestinal cells contains few organelles: vacuoles, lysosomal bodies, spheroid bodies, endoplasmic reticulum, and many large lipid droplets. In the anterior portion of the intestine, the lysosomal bodies, spheroid bodies, and vacuoles presented positive reaction for acid phosphatase, and carbohydrates were detected in lysosomal bodies. The midbody and posterior regions presented less organelles and lipid droplets, and nuclei were more abundant. Residues of l-fucose were detected by Ulex europaeus lectin binding in the midbody sections. Basic proteins were associated to lipid droplets, in the posterior region. In the whole extension of the intestine, carbohydrates were detected on tight junctions. These results indicate that the metabolized material in the epithelium can contribute to the microfilariae development and also probably can be involved with the excretory/secretory mechanism of these nematodes.
Similar content being viewed by others
References
Angermüller S, Fahimi DH (1982) Imidazole-buffered osmium tetroxide: an excellent stain for visualization of lipids in transmission electron microscopy. Histochem J 14:823–825
Araújo A, Souto-Padrón T, De Souza,W (1993) Cytochemical localization of carbohydrate residues in microfilariae of Wuchereria bancrofti and Brugia malayi. J Histochem Cytochem 41:571–578
Barka T, Anderson PJ (1962) Histochemistry methods for acid phosphatase using hexazoin pararosanilin as coupler. J Histochem Cytochem 10:741–753
Bendayan M (1984) Enzyme-gold electron microscopic cytochemistry: a new affinity approach for the ultrastructural localization of macromolecules. J Electron Microsc Tech 1:349–372
Bendayan M, Nancy A, Kan W (1987) Effect of tissue processing on colloidal gold cytochemistry. J Histochem Cytochem 35:983–986
Bendayan M, Benhamou N, Desjardins M (1990) Lectin-binding sites in diabetic glomeruli. J Submicrosc Cytol Pathol 22:173–184
Berryman MA, Rodewald RD (1990) An enhanced method for post-embedding immunocytochemical staining which preserves cell membranes. J Histochem Cytochem. 38:159–170
Bertram DS, Unsworth K, Gordon RM (1946) The biology and maintenance of Liponyssus bacoti Hirst, 1913, and an investigation into its role as a vector of Litomosoides carinii to cotton rats and white rats, together with some observations on the infection in the white rats. Ann Trop Med Parasitol 40:228–254
Bird AF, Bird J (1991) The structure of nematodes. Academic Press, San Diego, pp 1–95
Blaxter ML, Page AP, Rudin W, Maizels RM (1992) Nematode surface coats: actively evading immunity. Parasitol Today 8:243–247
Bonner TP, Etges FJ, Menefee MG (1971) Changes in the ultrastructure of Nematospiroides dubius (Nematoda) intestinal cells during development from fourth stage to adult. Z Zellforsch 119:526–533
Briggs RT, Draft DB, Karnovsky ML, Karnovsky MJ (1975) Localization of NADH oxidase on the surface of human polymorphonuclear leucocytes by a new cytochemical method. J Cell Biol 67:566–586
Franz M, Andrews P (1986a) Histology of adult Litomosoides carinii (Nematoda: Filarioidea). Z Parasitenkd 72:387–395
Franz M, Andrews P (1986b) Fine structure of adult Litomosoides carinii (Nematoda: Filarioidea). Z Parasitenkd 72:537–547
Franz M, Buttner DW (1983) The fine structure of adult Onchocerca volvulus. V. The digestive tract and the reproductive system of the female worm. Trop Med Parasitol 34:155–161
Franz M, Melles J, Buttner DW (1984) Electron microscope study of the body wall and the gut of adult Loa loa. Z Parasitenkd 70:525–536
Gordon M, Bensch KG (1968) Cytochemical differentiation of the guinea pig sperm flagellum with phosphotungstic acid. J Ultrastruct Res 24:33–50
Howels RE, Chen SN (1981) Brugia pahangi: feeding and nutrient uptake in vitro and in vivo. Exp Parasitol 51:42–58
Hulstaert CE, Kalicharan D, Hardonk MJ (1983) Cytochemical demonstration of phosphatases in the rat liver by a cerium-based method in combination with osmium tetroxide and potassium ferrocyanide post-fixation. Histochemistry 78:71–79
Johnstone IL (1994) The cuticle of the nematode Caenorhabditis elegans: a complex collagen structure. BioEssays 16:171–178
Jolodar A, Fischer P, Buttner DW, Miller DJ, Schmetz C, Brattig NW (2004) Onchocerca volvulus: expression and immunolocalization of a nematode cathepsin D-like lysosomal aspartic protease. Exp Parasitol 107:145–156
Kohler K, Zahraoui A (2005) Tight junction: a co-ordinator of cell signalling and membrane trafficking. Biol Cell 97:659–665
Lee DL, Wright KA, Shivers RR (1986) A freeze-fracture study of adult, in utero larval and infective stage larvae of the nematode Trichinella. Tissue Cell 16:819–828
Martinez AMB, De Souza W (1995) A quick-frozen, freeze-fracture, and deep-etch study of the cuticle of adult forms of Strongyloides venezuelensis (Nematoda). Parasitology 111:523–529
Martinez AMB, De Souza W (1997) A freeze-fracture and deep-etch study of the cuticle and hypodermis of infective larvae of Strongyloides venezuelensis (Nematoda). Int J Parasitol 27:289–297
McGonigle S, Yoho ER, James ER (2001) Immunization of mice with fractions derived from the intestines of Dirofilaria immitis. Int J Parasitol 31:1459–1466
Moraes Neto AHA, Lanfredi RM, De Souza W (1997) Litomosoides chagasfilhoi sp. nov. (Nematoda: Filarioidea) parasitizing the abdominal cavity of Akodon cursor (Winge, 1887) (Rodentia: Muridae) from Brazil. Parasitol Res 83:137–143
Moraes Neto AHA, Lanfredi RM, De Souza W (2001) Fine structure, freeze-fracture and deep-etch views of the sheath and cuticle of microfilariae of Litomosoides chagasfilhoi (Nematoda: Filarioidea). Parasitol Res 87:1035–1042
Moraes Neto AHA, Lanfredi RM, De Souza W (2002) Deep-etched view of the cuticle of adults of Litomosoides chagasfilhoi (Nematoda: Filarioidea). Parasitol Res 88:849–854
Moraes Neto AHA, Lanfredi RM, Gadelha C, Cunha-e-Silva NL, Simão RA, Achete C, De Souza W (2003) Further studies on the structural analysis of the cuticle of Litomosoides chagasfilhoi (Nematoda: Filarioidea). Parasitol Res 89:397–406
Ogbogu VC, Storey DM (1996) Ultrastructure of the alimentary tract of third-stage larvae of Litomosoides carinii. J Helminthol 70:223–229
Peixoto CA, Kramer JM, De Souza (1997) Caenorhabditis elegans cuticle: a description of new elements of the fibrous layer. J Parasitol 54:351–358
Peixoto CA, Norões J, Rocha A, Dreyer G (1999) Immunocytochemical localization and distribution of human albumin in Wuchereria bancrofti adult worms. Arch Pathol Lab Med 123:173–177
Peixoto CA, Silva LF, Teixeira KM, Rocha A (2001) Ultrastructural characterization of intracellular bacteria of Wuchereria bancrofti. Trans R Soc Trop Med Hyg 95:566–568
Rao UR, Chandrashekar R, Subrahmanyam D (1987) Litomosoides carinii: characterization of surface carbohydrates of microfilariae and infective larvae. Trop Med Parasitol 38:15–18
Robinson J, Karnovsky M (1983) Ultrastructural localization of several phosphatases with cerium. J Histochem Cytochem 10:1197–1208
Schraermeyer U, Peters W, Zahner H (1987a) Formation by the uterus of a peripheral layer of the sheath in microfilariae of Litomosoides carinii and Brugia malayi. Parasitol Res 73:557–564
Schraermeyer U, Peters W, Zahner H (1987b) Lectin binding studies on adult filariae, intrauterine developing stages and microfilariae of Brugia malayi and Litomosoides carinii. Parasitol Res 73:550–556
Selkirk ME, Gregory WF, Yasdanbakhsh M, Jenkins RE, Maizels RM (1990) Cuticular localisation and turnover of the major surface glycoprotein (gp29) of adult Brugia malayi. Mol Biochem Parasitol 42:31–43
Taylor MJ, Bandi C, Hoerauf AM, Lazdins J (2000) Wolbachia bacteria of filarial nematodes: a target for control? Parasitol Today 16:179–180
Thiery JP (1967) Mise en evidence des polysaccharides sur coupes fines en microscopie electronic. J Microsc 6:987–1018
Vincent AL, Ash LR, Frommes SP (1975) The ultrastructure of adult Brugia malayi (Brug, 1927), (Nematoda: Filarioidea). J Parasitol 61:499–512
Weber P (1985) Electron microscope study on the developmental stages of Wuchereria bancrofti in the intermediate host: structure of the digestive tract. Trop Med Parasitol 36:109–116
Wildenburg G, Henkle-Duhrsen K (1999) Onchocerca volvulus: immunolocalization of the extracellular CuZn superoxide dismutase using antibodies raised against a 15-mer epitope of this enzyme. Exp Parasitol 91:1–6
Wright KA, Lee DL, Shivers RR (1985) A freeze-fracture study of the digestive tract of the parasitic nematode Trichinella. Tissue Cell 17:189–198
Zhang Y, Foster JM, Kumar S, Fougere M, Carlow CK (2004) Cofactor-independent phosphoglycerate mutase has an essential role in Caenorhabditis elegans and is conserved in parasitic nematodes. J Biol Chem 279:37185–37190
Acknowledgements
We are grateful to Ms. Beatriz Ferreira Ribeiro, Márcia Adriana Dutra, and Giovana Alves de Moraes from the Laboratório de Biologia Celular e Tecidual, CBB, UENF, and Izaias Aparecido Pimenta, from the Departamento de Biologia, IOC, FIOCRUZ, for technical assistance; to Dr Renato Augusto DaMatta and Dr João CA Almeida, for critical review of the manuscript; and to Ms. Maria de Fátima Leal Alencar for secretarial assistance.
This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) grant 150.115/2003-2, Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Universidade Estadual do Norte Fluminense Darcy Ribeiro, and Departamento de Biologia, Instituto Oswaldo Cruz, FIOCRUZ.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
de Moraes Neto, A.H.A., Cunha, G.S.P., Ferreira, T.F. et al. Fine structure and cytochemical analysis of the intestinal wall along the body of adult female of Litomosoides chagasfilhoi (Nematoda: Filarioidea). Parasitol Res 98, 525–533 (2006). https://doi.org/10.1007/s00436-005-0092-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-005-0092-9