Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-28T14:23:57.016Z Has data issue: false hasContentIssue false
  • English
  • Français

Pathways for the influx of molecules into cercariae of Schistosoma mansoni during skin penetration

Published online by Cambridge University Press:  04 February 2010

J. A. THORNHILL ,
P. McVEIGH ,
A. D. JURBERG  and
J. R. KUSEL
J. A. THORNHILL
Affiliation:
Division of Infection and Immunity, Faculty of Biomedical and Life Sciences, Glasgow Biomedical Research Centre, University of Glasgow, 120 University Place, GlasgowG12 8TA, UK
P. McVEIGH
Affiliation:
Biomolecular Processes: Parasitology, School of Biological Sciences, Medical Biology Centre, 97 Lisburn Road, Queen's University Belfast, BelfastBT9 7BL, UK
A. D. JURBERG
Affiliation:
Instituto Gulbenkian de Ciência, Oeiras, Portugal
J. R. KUSEL*
Affiliation:
Division of Infection and Immunity, Faculty of Biomedical and Life Sciences, Glasgow Biomedical Research Centre, University of Glasgow, 120 University Place, GlasgowG12 8TA, UK
*
*Corresponding author: Division of Infection and Immunity, Faculty of Biomedical and Life Sciences, University of Glasgow, Level 5, Glasgow Biomedical Research Centre, 120 University Place, Glasgow G12 8TA, Scotland, UK. Tel: +44 (0)141 330 6968. Fax: +44 (0)141 330 4600. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

It has been observed that fluorescent membrane-impermeant molecules can enter the cercariae as they penetrate mouse skin. The hypothesis to be tested was that such molecules, which included Lucifer Yellow and a variety of fluorescent dextrans, entered the parasite through the nephridiopore and excretory tubules as well as through the surface membrane. FITC-labelled poly-L-lysine (molecular weight 10 kDa), added at 4°C during syringe transformation, was found to enter the nephridiopore and labelled the excretory bladder and sometimes the excretory tubules. This finding indicates that macromolecules (10 kDa) can enter the nephridiopore. It was found that linoleic acid (a normal constituent of skin) greatly stimulated uptake of Lucifer Yellow and dextrans into the excretory/subtegumental region of 2-h-old schistosomula. This correlated with an increased uptake of membrane-impermeant propidium iodide at 37°C. Since increased uptake of propidium iodide occurs when membranes become permeable, the surface membrane could also be a pathway of transport of the membrane-impermeant molecules into the schistosomulum.

Keywords

linoleic acidLucifer Yellownephridioporeschistosomulumsurface membrane
Type
Research Article
Information
Parasitology , Volume 137 , Issue 7 , June 2010 , pp. 1089 - 1098
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Booth, I. R., Edwards, M. D., Black, S., Schumann, U. and Miller, S. (2007). Mechanosensitive channels in bacteria: signs of closure? Nature Reviews Microbiology 5, 431–440.CrossRefGoogle ScholarPubMed
Braschi, S. and Wilson, R. A. (2006). Proteins exposed at the adult schistosome surface revealed by biotinylation. Molecular & Cellular Proteomics 5, 347–356.Google Scholar
Cao, C., Steinberg, T. H., Neu, H. C., Cohen, D., Horwitz, S. B., Hickman, S. and Silverstein, S. C. (1993). Probenecid-resistant J774 cell expression of enhanced organic anion transport by a mechanism distinct from multidrug resistance. Infectious Agents and Disease 2, 193–200.Google Scholar
Curwen, R. S., Ashton, P. D., Sundaralingam, S. and Wilson, R. A. (2006). Identification of novel proteases and immunomodulators in the secretions of schistosome cercariae that facilitate host entry. Molecular & Cellular Proteomics 5, 835–844.CrossRefGoogle ScholarPubMed
Dong, Z., Patel, Y., Saikumar, P., Weinberg, J. M. and Venkatachalam, M. A. (1998). Development of porous defects in plasma membranes of adenosine triphosphate-depleted Madin-Darby canine kidney cells and its inhibition by glycine. Laboratory Investigation 78, 657–668.Google ScholarPubMed
Dorsey, C. H., Cousin, C. E., Lewis, F. A. and Stirewalt, M. A. (2002). Ultrastructure of the Schistosoma mansoni cercaria. Micron 33, 279–323.CrossRefGoogle ScholarPubMed
Fusco, A. C., Salafsky, B. and Delbrook, K. (1986). Schistosoma mansoni: production of cercarial eicosanoids as correlates of penetration and transformation. The Journal of Parasitology 72, 397–404.CrossRefGoogle ScholarPubMed
Gillan, L., Evans, G. and Maxwell, W. M. (2005). Flow cytometric evaluation of sperm parameters in relation to fertility potential. Theriogenology 63, 445–457.CrossRefGoogle ScholarPubMed
Goksor, M., Diez, A., Enger, J., Hanstorp, D. and Nystrom, T. (2003). Analysis of molecular diffusion in ftsK cell-division mutants using laser surgery. EMBO Reports 4, 867–871.CrossRefGoogle ScholarPubMed
Graca, D. S., Vitoria, S. R., Loureiro-Dias, M. C., Rombouts, F. M. and Abee, T. (2002). Flow cytometric assessment of membrane integrity of ethanol-stressed Oenococcus oeni cells. Applied and Environmental Microbiology 68, 6087–6093.CrossRefGoogle Scholar
Haas, W. (1984). Schistosoma mansoni: cercaricidal effect of 2-tetradecenoic acid, a penetration stimulant. Experimental Parasitology 58, 215–222.CrossRefGoogle ScholarPubMed
Haas, W., Haeberlein, S., Behring, S. and Zoppelli, E. (2008). Schistosoma mansoni: human skin ceramides are a chemical cue for host recognition of cercariae. Experimental Parasitology 120, 94–97.Google Scholar
Haeberlein, S. and Haas, W. (2008). Chemical attractants of human skin for swimming Schistosoma mansoni cercariae. Parasitology Research 102, 657–662.CrossRefGoogle ScholarPubMed
Hockley, D. J. and McLaren, D. J. (1973). Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. International Journal for Parasitology 3, 13–25.CrossRefGoogle ScholarPubMed
Jones, J. T., Breeze, P. and Kusel, J. R. (1989). Schistosome fecundity: influence of host genotype and intensity of infection. International Journal for Parasitology 19, 769–777.CrossRefGoogle ScholarPubMed
Jones, J. T., Helm, C. N. and Kusel, J. R. (1988). Variation in susceptibility of Schistosoma mansoni to damage by polycations. Molecular and Biochemical Parasitology 30, 35–44.CrossRefGoogle ScholarPubMed
Kennedy, S. M., Ji, Z., Hedstrom, J. C., Booske, J. H. and Hagness, S. C. (2008). Quantification of electroporative uptake kinetics and electric field heterogeneity effects in cells. Biophysical Journal 94, 5018–5027.CrossRefGoogle ScholarPubMed
Kusel, J. R., Al Adhami, B. H. and Doenhoff, M. J. (2007). The schistosome in the mammalian host: understanding the mechanisms of adaptation. Parasitology 134, 1477–1526.CrossRefGoogle ScholarPubMed
LaPlaca, M. C., Prado, G. R., Cullen, D. K. and Irons, H. R. (2006). High rate shear insult delivered to cortical neurons produces heterogeneous membrane permeability alterations. Conference Proceedings IEEE Engineering in Medicine and Biology Society 1, 2384–2387.CrossRefGoogle Scholar
Leypoldt, J. K. and Henderson, L. W. (1993). Molecular charge influences transperitoneal macromolecule transport. Kidney International 43, 837–844.Google Scholar
McLaren, D. J., Peterson, C. G. and Venge, P. (1984). Schistosoma mansoni: further studies of the interaction between schistosomula and granulocyte-derived cationic proteins in vitro. Parasitology 88, 491–503.CrossRefGoogle ScholarPubMed
Mikes, L., Zidkova, L., Kasny, M., Dvorak, J. and Horak, P. (2005). In vitro stimulation of penetration gland emptying by Trichobilharzia szidati and T. regenti (Schistosomatidae) cercariae. Quantitative collection and partial characterization of the products. Parasitology Research 96, 230–241.CrossRefGoogle Scholar
Milici, A. J., L'Hernault, N. and Palade, G. E. (1985). Surface densities of diaphragmed fenestrae and transendothelial channels in different murine capillary beds. Circulation Research 56, 709–717.Google Scholar
Oliveira, V. H., Nascimento, K. S., Freire, M. M., Moreira, O. C., Scofano, H. M., Barrabin, H. and Mignaco, J. A. (2008). Mechanism of modulation of the plasma membrane Ca(2+)-ATPase by arachidonic acid. Prostaglandins & other Lipid Mediators 87, 47–53.CrossRefGoogle ScholarPubMed
Ribeiro, F., Coelho, P. M. Z., Vieira, L. Q., Powell, K. and Kusel, J. R. (1998). Membrane internalization processes in different stages of Schistosoma mansoni as shown by a styryl dye (Frei Mao 1–43). Parasitology 116, 51–59.CrossRefGoogle ScholarPubMed
Shiu, C., Barbier, E., Di Cello, F., Choi, H. J. and Stins, M. (2007). HIV-1 gp120 as well as alcohol affect blood-brain barrier permeability and stress fiber formation: involvement of reactive oxygen species. Alcoholism, Clinical and Experimental Research 31, 130–137.Google Scholar
Silver, F. H. and Siperko, L. M. (2003). Mechanosensing and mechanochemical transduction: how is mechanical energy sensed and converted into chemical energy in an extracellular matrix? Critical Reviews in Biomedical Engineering 31, 255–331.CrossRefGoogle Scholar
Skelly, P. J. and Wilson, R. A. (2006). Making sense of the schistosome surface. Advances in Parasitology 63, 185–284.Google Scholar
Tallima, H., Salah, M. and El Ridi, R. (2005). In vitro and in vivo effects of unsaturated fatty acids on Schistosoma mansoni and S. haematobium lung-stage larvae. The Journal of Parasitology 91, 1094–1102.CrossRefGoogle ScholarPubMed
Tan, H. H., Thornhill, J. A., Al Adhami, B. H., Akhkha, A. and Kusel, J. R. (2003). A study of the effect of surface damage on the uptake of Texas Red-BSA by schistosomula of Schistosoma mansoni. Parasitology 126, 235–240.CrossRefGoogle ScholarPubMed
Thornhill, J., Coelho, P. M., McVeigh, P., Maule, A., Jurberg, A. D. and Kusel, J. R. (2009). Schistosoma mansoni cercariae experience influx of macromolecules during skin penetration. Parasitology 136, 1257–1267.CrossRefGoogle ScholarPubMed
Valiunas, V. (2002). Biophysical properties of connexin-45 gap junction hemichannels studied in vertebrate cells. The Journal of General Physiology 119, 147–164.CrossRefGoogle ScholarPubMed
Vlahakis, N. E. and Hubmayr, R. D. (2003). Response of alveolar cells to mechanical stress. Current Opinion in Critical Care 9, 2–8.Google Scholar
Wilson, R. A. and Webster, L. A. (1974). Protonephridia. Biological Reviews of the Cambridge Philosophical Society 49, 127–160.CrossRefGoogle ScholarPubMed