Schistosoma mansoni cercariae experience influx of macromolecules during skin penetration

Parasitology

Volumn 136, Issue 11, 2009, Pages 1257-1267

  Thornhill, J ^a   Coelho, P M Z ^b   McVeigh, P ^c   Maule, A ^c   Jurberg, A D ^b,d   Kusel, J R ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^d INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

Cercaria; Fluorescent dextrans; In vitro transformation; Lucifer Yellow; Propidium iodide; Schistosomulum; Skin penetration

Indexed keywords

CARMINIC ACID; LUCIFER YELLOW;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CERCARIA (TREMATODE LARVA); CONTROLLED STUDY; ESOPHAGUS; FLUORESCENCE MICROSCOPY; HOST; IN VITRO STUDY; MACROMOLECULE; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; SCHISTOSOMA MANSONI; SCHISTOSOMULUM; SKELETAL MUSCLE; SKIN PENETRATION;

ANIMALS; CARMINE; FLUORESCENT DYES; HOST-PARASITE INTERACTIONS; ISOQUINOLINES; LARVA; MACROMOLECULAR SUBSTANCES; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SKIN;

MUS; SCHISTOSOMA MANSONI;

EID: 70350569210     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182009990692     Document Type: Article

References (47)

1. Al Adhami, B. H., Doenho., M., Thornhill, J., Akhkha, A., White, E. and Kusel, J. R. (2001). A study of some characteristics of individual clones of Schistosoma mansoni with emphasis on the biological and metabolic activities. Parasitology 123, 563-572.
2. Alves, L. A., Coutinho-Silva, R., Persechini, P. M., Spray, D. C., Savino, W. and Campos de Carvalho, A. C. (1996). Are there functional gap junctions or junctional hemichannels in macrophages? Blood 88, 328-334.
3. 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.
4. Clegg, J. A. (1965). In vitro cultivation of Schistosoma mansoni. Experimental Parasitology 16, 133-147.
5. Clegg, J. A., Smithers, S. R. and Terry, R. J. (1971). Acquisition of human antigens by Schistosoma mansoni during cultivation in vitro. Nature, London 232, 653-654.
6. Colley, D. G. and Wikel, S. K. (1974). Schistosoma mansoni: simplified method for the production of schistosomules. Experimental Parasitology 35, 44-51.
7. Cousin, C. E., Stirewalt, M. A., Dorsey, C. H. and Watson, L. P. (1986). Schistosoma mansoni: comparative development of schistosomules produced by arti.cial techniques. The Journal of Parasitology 72, 606-609.
8. Dean, M. F., Cooper, J. A. and Stahl, P. (1988). Cell contact and direct transfer between co-cultured macrophages and fibroblasts. Journal of Leukocyte Biology 43, 539-546.
9. Eugenin, E. A., Branes, M. C., Berman, J. W. and Saez, J. C. (2003). TNF-alpha plus IFN-gamma induce connexin43 expression and formation of gap junctions between human monocytes/macrophages that enhance physiological responses. Journal of Immunology 170, 1320-1328.
10. Foley, M., Kusel, J. R. and Garland, P. B. (1988). Changes in the organization of the surface membrane upon transformation of cercariae to schistosomula of the helminth parasite Schistosoma mansoni. Parasitology 96, 85-97.
11. Fortes, F. S., Pecora, I. L., Persechini, P. M., Hurtado, S., Costa, V., Coutinho-Silva, R., Braga, M. B., Silva-Filho, F. C., Bisaggio, R. C., De Farias, F. P., Scemes, E., De Carvalho, A. C. and Goldenberg, R. C. (2004). Modulation of intercellular communication in macrophages: possible interactions between GAP junctions and P2 receptors. Journal of Cell Science 117, 4717-4726.
12. Gillan, L., Evans, G. and Maxwell, W. M. (2005). Flow cytometric evaluation of sperm parameters in relation to fertility potential. Theriogenology 63, 445-457.
13. Haas, W., Grabe, K., Geis, C., Pach, T., Stoll, K., Fuchs, M., Haberl, B. and Loy, C. (2002). Recognition and invasion of human skin by Schistosoma mansoni cercariae: the key-role of L-arginine. Parasitology 124, 153-167.
14. 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.
15. Haeberlein, S. and Haas, W. (2008). Chemical attractants of human skin for swimming Schistosoma mansoni cercariae. Parasitology Research 102, 657-662.
16. Hansell, E., Braschi, S., Medzihradszky, K. F., Sajid, M., Debnath, M., Ingram, J., Lim, K. C. and McKerrow, J. H. (2008). Proteomic analysis of skin invasion by blood .uke larvae. PLoS Neglected Tropical Diseases 2, e262.
17. Heinrichs, S. (1985). Differential retrograde labelling with horseradish peroxidase (HRP) and Lucifer yellow (LY) in an invertebrate nervous system - HRP fluorescence andLY preservation limit choice of fixative. Journal of Neuroscience Methods 15, 85-93.
18. Hidalgo, C. and Latorre, R. (1970). Temperature dependence of non-electrolyte and sodium permeability in giant axon of squid. The Journal of Physiology 211, 173-191.
19. 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.
20. Kusel, J. R., Stones, L. and Harnett, W. (1982). The effects of retinol (vitamin A alcohol) and various non-ionic detergents on the surfaces of schistosomula and adult Schistosoma mansoni. Molecular and Biochemical Parasitology 5, 147-163.
21. Machado-Silva, J. R., Pelajo-Machado, M., Lenzi, H. L. and Gomes, D. C. (1998). Morphological study of adult male worms of Schistosoma mansoni Sambon, 1907 by confocal laser scanning microscopy. Memórias do Instituto Oswaldo Cruz 93 (Suppl. 1), 303-307.
22. McKerrow, J. H., Keene, W. E., Jeong, K. H. and Werb, Z. (1983). Degradation of extracellular matrix by larvae of Schistosoma mansoni. I. Degradation by cercariae as a model for initial parasite invasion of host. Laboratory Investigation 49, 195-200.
23. McLaren, D. J., Clegg, J. A. and Smithers, S. R. (1975). Acquisition of host antigens by young Schistosoma mansoni in mice: correlation with failure to bind antibody in vitro. Parasitology 70, 67-75.
24. McLaren, D. J. and Hockley, D. J. (1977). Blood flukes have a double outer membrane. Nature, London 269, 147-149.
25. Meyer, W., Poehling, H. M. and Neurand, K. (1991). Intraepidermal distribution of free amino acids in porcine skin. Journal of Dermatological Science 2, 383-392.
26. Peracchia, C. (1981). Direct communication between axons and sheath glial cells in crayfish. Nature, London 290, 597-598.
27. Ramachandran, H., Skelly, P. J. and Shoemaker, C. B. (1996). The Schistosoma mansoni epidermal growth factor receptor homologue, SER, has tyrosine kinase activity and is localized in adult muscle. Molecular and Biochemical Parasitology 83, 1-10.
28. Ramalho-Pinto, F. J., Gazzinelli, G., Howells, R. E., Mota-Santos, T. A., Figueiredo, E. A. and Pellegrino, J. (1974). Schistosoma mansoni: defined system for stepwise transformation of cercaria to schistosomule in vitro. Experimental Parasitology 36, 360-372.
29. Ribeiro, A. C., Maldonado Júnior, A., D'Andrea, P. S., Vieira, G. O. and Rey, L. (1998). Susceptibility of Nectomys rattus (Pelzen, 1883) to experimental infection with Schistosoma mansoni (Sambon, 1907): a potential reservoir in Brazil. Memórias do Instituto Oswaldo Cruz 93 (Suppl. 1), 295-299.
30. Schultz, G., Rotatori, D. S. and Clark, W. (1991). EGF and TGF-alpha in wound healing and repair. Journal of Cellular Biochemistry 45, 346-352.
31. Scott, I. R. and Harding, C. R. (1986). Filaggrin breakdown to water binding compounds during development of the rat stratum corneum is controlled by the water activity of the environment. Developmental Biology 115, 84-92.
32. Shimizu, N. and Kawazoe, Y. (1996). A new method for permeabilization of the plasma membrane of cultured mammalian cells. III. Internalization of .uorescent dextrans into cultured mammalian cells by vortex-stirring in the presence of high molecular weight polyacrylic acid. Biological and Pharmaceutical Bulletin 19, 1023-1025. (Pubitemid 26303360)
33. Shoemaker, C. B., Ramachandran, H., Landa, A., dos Reis, M. G. and Stein, L. D. (1992). Alternative splicing of the Schistosoma mansoni gene encoding a homologue of epidermal growth factor receptor. Molecular and Biochemical Parasitology 53, 17-32.
34. Skelly, P. J., Da'dara, A. and Harn, D. A. (2003). Suppression of cathepsin B expression in Schistosoma mansoni by RNA interference. International Journal for Parasitology 33, 363-369.
35. Skelly, P. J. and Shoemaker, C. B. (1996). Rapid appearance and asymmetric distribution of glucose transporter SGTP4 at the apical surface of intramammalian-stage Schistosoma mansoni. Proceedings of the National Academy of Sciences, USA 93, 3642-3646.
36. Skelly, P. J. and Shoemaker, C. B. (2001). The Schistosoma mansoni host-interactive tegument forms from vesicle eruptions of a cyton network. Parasitology 122, 67-73.
37. Smith, H. V. and Kusel, J. R. (1979). The acquisition of antigens in the intercellular substance of mouse skin by schistosomula of Schistosoma mansoni. Clinical and Experimental Immunology 36, 430-435.
38. Steinberg, T. H., Newman, A. S., Swanson, J. A. and Silverstein, S. C. (1987). Macrophages possess probenecid-inhibitable organic anion transporters that remove .uorescent dyes from the cytoplasmic matrix. The Journal of Cell Biology 105, 2695-2702.
39. Stirewalt, M. A. (1974). Schistosoma mansoni: cercaria to schistosomule. Advances in Parasitology 12, 115-182.
40. Stirewalt, M. A., Cousin, C. E. and Dorsey, C. H. (1983). Schistosoma mansoni: stimulus and transformation of cercariae into schistosomules. Experimental Parasitology 56, 358-368.
41. Swanson, J., Bushnell, A. and Silverstein, S. C. (1987). Tubular lysosome morphology and distribution within macrophages depend on the integrity of cytoplasmic microtubules. Proceedings of the National Academy of Sciences, USA 84, 1921-1925.
42. Sweet, W. D. and Schroeder, F. (1986). Charged anaesthetics alter LM-flbroblast plasma-membrane enzymes by selective fluidization of inner or outer membrane leaffets. The Biochemical Journal 239, 301-310.
43. Takahashi, M. and Tezuka, T. (2004). The content of free amino acids in the stratum corneum is increased in senile xerosis. Archives of Dermatological Research 295, 448-452.
44. Tanaka, A., Nagate, T. and Matsuda, H. (2005). Acceleration of wound healing by gelatin fllm dressings with epidermal growth factor. The Journal of Veterinary Medical Science 67, 909-913.
45. Tassin, M. T., Lang, T., Antoine, J. C., Hellio, R. and Ryter, A. (1990). Modified lysosomal compartment as carrier of slowly and non-degradable tracers in macrophages. European Journal of Cell Biology 52, 219-228.
46. Taylor, K. R., Trowbridge, J. M., Rudisill, J. A., Termeer, C. C., Simon, J. C. and Gallo, R. L. (2004). Hyaluronan fragments stimulate endothelial recognition of injury through TLR4. The Journal of Biological Chemistry 279, 17079-17084.
47. Whitfield, P. J., Bartlett, A., Khammo, N., Brain, A. P., Brown, M. B., Marriott, C. and Clothier, R. (2003). Delayed tail loss during the invasion of human skin by schistosome cercariae. Parasitology 126, 135-140. (Pubitemid 36308249)