Interaction between neutrophils and Schistosoma mansoni larvae in vivo: a transmission electron-microscopic study

Melo, Alan Lane de; Machado, Conceição Ribeiro da Silva; Pereira, Leógenes Horácio

doi:10.1590/S0036-46651993000100005

Abstracts

Schistosoma mansoni cercariae were inoculated into the peritoneal cavity of naive mice and recovered 30 minutes later. Ultrastructural studies showed that neutrophils adhere to the larval surface and participate in the removal of glycocalyx by phagocytosis. This finding suggests that the neutrophils can play a role on the cercaria-schistosomulum transformation process.

Neutrophils; Schistosoma mansoni; Cercaria transformation

Cercárias de Schistosoma mansoni foram inoculadas na cavidade peritoneal de camundongos normais e recuperadas 30 minutos depois. Estudos ultra-estruturais mostraram que neutrófilos aderem à superfície da larva, participando da remoção do glicocálice através de fagocitose. Este achado sugere que neutrófilos possam ter papel no processo de transformação de cercária em esquistossômulo.

ORIGINAL ARTICLES

Interaction between neutrophils and Schistosoma mansoni larvae in vivo. A transmission electron-microscopic study

Interação entre neutrófilos e larvas de Schistosoma mansoni in vivo. Estudo ao microscópio eletrônico de transmissão

Alan Lane de Melo^I; Conceição Ribeiro da Silva Machado^II; Leógenes Horácio Pereira^I

^IDepartamento de Parasitologia e Grupo Interdepartamental de Estudos sobre Esquistossomose (GIDE)

^IIDepartamento de Morfologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901 - Belo Horizonte, Brasil

SUMMARY

Schistosoma mansoni cercariae were inoculated into the peritoneal cavity of naive mice and recovered 30 minutes later. Ultrastructural studies showed that neutrophils adhere to the larval surface and participate in the removal of glycocalyx by phagocytosis. This finding suggests that the neutrophils can play a role on the cercaria-schistosomulum transformation process.

Key words: Neutrophils; Schistosoma mansoni; Cercaria transformation.

RESUMO

Cercárias de Schistosoma mansoni foram inoculadas na cavidade peritoneal de camundongos normais e recuperadas 30 minutos depois. Estudos ultra-estruturais mostraram que neutrófilos aderem à superfície da larva, participando da remoção do glicocálice através de fagocitose. Este achado sugere que neutrófilos possam ter papel no processo de transformação de cercária em esquistossômulo.

Full text available only in PDF format.

Texto completo disponível apenas em PDF.

Recebido para publicação em 24/6/1992

Aceito para publicação em 24/08/1992.

Financial support has been provided by the Parasitic Diseases Programme, World Health Organization, Switzerland, and FINEP/CNPq, Brazil.

1. ANWAR, A.R.E.; SMITHERS, S.R. & KAY, A.B. - Killing of schistosomula of Schistosoma mansoni coated with antibody and/or complement by human leucocytes in vitro: requirement for complement in preferential killing by eosinophils. J. Immunol., 122: 628-637, 1979.
2. CAULFIELD, J.P.; KORMAN, G.; BUTTERWORTH, A.E.; KOOGAN, M. & DAVID, J.R. - The adherence of human neutrophils and eosinophils to schistosomula: evidence for membrane fusion between cells and parasites. J. Cell Biol., 86: 46-63, 1980.
3. CLEGG, J.A. - In vitro cultivation of Schistosoma mansoni. Exp. Parasit., 16: 133-147, 1965.
4. CLEGG, J.A. & SMITHERS, R. - Death of schistosome cercariae during penetration of the skin. II. Penetration of mammalian skin by Schistosoma mansoni. Parasitology, 58: 111-128, 1968.
5. DESSEIN, A.; SAMUELSON, J.C.; BUTTERWORTH, A.E.; HOOGAN, M.; SINGERY, B.A.; VADAS, M.A. & DAVID, J.R. - Immune evasion by Schistosoma mansoni: loss of susceptibility to antibody or complement-dependent eosinophil attack by schistosomula cultured in medium free of macromolecules. Parasitology, 82: 357-374, 1981.
6. GILBERT, B.; DA ROSA, M.N.; BOROJEVIC, R. & PELLEGRINO, J. - Schistosoma mansoni in vitro transformation of cercariae into schistosomule. Parasitology, 64: 333-339, 1972.
7. HOCKLEY, D.J. & McLAREN, D.J. - The outer membrane of Schistosoma mansoni. Trans. roy. Soc. trop. Med. Hyg., 65: 432, 1971.
8. HOCKLEY, D.J. & McLAREN, D.J. - Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. Int. J. Parasit, 3: 13-25, 1973.
9. HOFFSTEIN, S.T.; FRIEDMAN, R.S. & WEISSMANN, G. - Degranulation, membrane addition, and shape change during chemotactic factor - induced aggregation of human neutrophils. J. Cell Biol., 95: 234-241, 1982.
10. INCANI, R.N. & McLAREN, D.J. - Neutrophil-mediated cytotoxicity to schistosomula of Schistosoma mansoni in vitro: studies on the kinetics of complement and/or antibody-dependent adherence and killing. Paras. Immunol., 3: 107-126, 1981.
11. INCANI, R.N. & McLAREN, D.J. - Ultrastructural observations on the in vitro interactions of rat neutrophils with schistosomula of Schistosoma mansoni in the presence of antibody and/or complement. Parasitology, 86: 345-357, 1983.
12. MACHADO, A.J.; GAZZINELLI, G.; PELLEGRINO, J. & DIAS DA SILVA, W. - Schistosoma mansoni: the role of the complement C₃ activating system in the cercaricidal action of normal serum. Exp. Parasit., 38: 20-29, 1975.
13. McKEAN, J.R.; ANWAR, A.R.E. & KAY, A.B. - Schistosoma mansoni: complement and antibody damage, mediated by human eosinophils and neutrophils, in killing schistosomula in vitro. Exp. Parasit., 51: 307-317, 1981.
14. McLAREN, D.J.; CLEGG, J.A. & SMITHERS, S.R. - Acquisition of host antigens by young Schistosoma mansoni in mice: correlation with failure to bind antibody in vitro. Parasitology, 70: 67-75, 1975.
15. MELO, A.L. - Efeitos da oxamniquina sobre a transformaçăo da cercária de Schistosoma mansoni em esquistossômulo in vivo. Belo Horizonte, 1979. (Tese de Mestrado - Instituto de Cięncias Biológicas da UFMG).
16. MELO, A.L. & PEREIRA, L.H. - Kinetics of the cercaria schistosomulum transformation, in vivo. Rev. Soc. bras. Med. trop., 18: 17-21, 1985.
17. MELO, A.L.; MACHADO, C.R.S. & PEREIRA, L.H. - Differences between in vitro and in vivo obtained schistosomules. Rev. Inst. Med. trop. S. Paulo, 32: 84-85, 1990.
18. MELO, A.L.; MACHADO, C.R.S. & PEREIRA, L.H. - Host cell adhesion to Schistosoma mansoni larvae in the peritoneal cavity of naive mice. Histological and scanning electron microscopic studies. Rev. Inst. Med. trop. S. Paulo, 35 (1): 1993.
19. PEREIRA, L.H.; PELLEGRINO, J.; VALADARES, T.E.; MELLO, R.T. & COELHO, P.M.Z. - A new approach for screening prophylactic agents in schistosomiasis. Rev. Inst. Med. trop. S. Paulo, 16: 123-126, 1974.
20. RAMALHO-PINTO, F.J.; McLAREN, D.J. & SMITHERS, S.R. - Complement-mediated killing of schistosomula of Schistosoma mansoni by rat eosinophils in vitro. J. exp. Med., 147: 147-156, 1978.
21. SINGER, I.I.; SCOTT, S.; KAWKA, D.W. & KAZAZIS, D.M. - Adhesomes: specific granules containing receptors for laminin, C3bi/fibrinogen, fibronectin, and vitronectin in human polymorphonuclear leukocytes and monocytes. J. Cell Biol., 109: 3169-3182, 1989.
22. STIREWALT, M.A. - Schistosomule vs cercariae. J. Parasit., 47: 47, 1961.
23. STIREWALT, M.A. - Schistosoma mansoni: cercaria to schistosomule. Advanc. Parasit., 12: 115-182, 1974.
24. STIREWALT, M.A.; MINNICK, D.R. & FREGEAU, W.A. - Definition and collection in quantity of schistosomules of Schistosoma mansoni. Trans. roy. Soc. trop. Med. Hyg., 60: 352-360, 1966.
25. STIREWALT, M.A. & UY, A. - Schistosoma mansoni: cercarial penetration and schistosomule collection in an in vitro system. Exp. Parasit., 26: 17-28, 1969.
26. VON LICHTENBERG, F.; SHER, A.; GIBBONS, N. & DOUGHTY, B.L. - Eosinophil enriched inflammatory response to schistosomula in the skin of mice immune to Schistosoma mansoni. Amer. J. Path., 84: 479-500, 1976.

Publication Dates

Publication in this collection
11 Sept 2006
Date of issue
Feb 1993

History

Accepted
24 Aug 1992
Received
24 June 1992

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] 1. ANWAR, A.R.E.; SMITHERS, S.R. & KAY, A.B. - Killing of schistosomula of Schistosoma mansoni coated with antibody and/or complement by human leucocytes in vitro: requirement for complement in preferential killing by eosinophils. J. Immunol., 122: 628-637, 1979.

[2] 2. CAULFIELD, J.P.; KORMAN, G.; BUTTERWORTH, A.E.; KOOGAN, M. & DAVID, J.R. - The adherence of human neutrophils and eosinophils to schistosomula: evidence for membrane fusion between cells and parasites. J. Cell Biol., 86: 46-63, 1980.

[3] 3. CLEGG, J.A. - In vitro cultivation of Schistosoma mansoni. Exp. Parasit., 16: 133-147, 1965.

[4] 4. CLEGG, J.A. & SMITHERS, R. - Death of schistosome cercariae during penetration of the skin. II. Penetration of mammalian skin by Schistosoma mansoni. Parasitology, 58: 111-128, 1968.

[5] 5. DESSEIN, A.; SAMUELSON, J.C.; BUTTERWORTH, A.E.; HOOGAN, M.; SINGERY, B.A.; VADAS, M.A. & DAVID, J.R. - Immune evasion by Schistosoma mansoni: loss of susceptibility to antibody or complement-dependent eosinophil attack by schistosomula cultured in medium free of macromolecules. Parasitology, 82: 357-374, 1981.

[6] 6. GILBERT, B.; DA ROSA, M.N.; BOROJEVIC, R. & PELLEGRINO, J. - Schistosoma mansoni in vitro transformation of cercariae into schistosomule. Parasitology, 64: 333-339, 1972.

[7] 7. HOCKLEY, D.J. & McLAREN, D.J. - The outer membrane of Schistosoma mansoni. Trans. roy. Soc. trop. Med. Hyg., 65: 432, 1971.

[8] 8. HOCKLEY, D.J. & McLAREN, D.J. - Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. Int. J. Parasit, 3: 13-25, 1973.

[9] 9. HOFFSTEIN, S.T.; FRIEDMAN, R.S. & WEISSMANN, G. - Degranulation, membrane addition, and shape change during chemotactic factor - induced aggregation of human neutrophils. J. Cell Biol., 95: 234-241, 1982.

[10] 10. INCANI, R.N. & McLAREN, D.J. - Neutrophil-mediated cytotoxicity to schistosomula of Schistosoma mansoni in vitro: studies on the kinetics of complement and/or antibody-dependent adherence and killing. Paras. Immunol., 3: 107-126, 1981.

[11] 11. INCANI, R.N. & McLAREN, D.J. - Ultrastructural observations on the in vitro interactions of rat neutrophils with schistosomula of Schistosoma mansoni in the presence of antibody and/or complement. Parasitology, 86: 345-357, 1983.

[12] 12. MACHADO, A.J.; GAZZINELLI, G.; PELLEGRINO, J. & DIAS DA SILVA, W. - Schistosoma mansoni: the role of the complement C₃ activating system in the cercaricidal action of normal serum. Exp. Parasit., 38: 20-29, 1975.

[13] 13. McKEAN, J.R.; ANWAR, A.R.E. & KAY, A.B. - Schistosoma mansoni: complement and antibody damage, mediated by human eosinophils and neutrophils, in killing schistosomula in vitro. Exp. Parasit., 51: 307-317, 1981.

[14] 14. McLAREN, D.J.; CLEGG, J.A. & SMITHERS, S.R. - Acquisition of host antigens by young Schistosoma mansoni in mice: correlation with failure to bind antibody in vitro. Parasitology, 70: 67-75, 1975.

[15] 15. MELO, A.L. - Efeitos da oxamniquina sobre a transformaçăo da cercária de Schistosoma mansoni em esquistossômulo in vivo. Belo Horizonte, 1979. (Tese de Mestrado - Instituto de Cięncias Biológicas da UFMG).

[16] 16. MELO, A.L. & PEREIRA, L.H. - Kinetics of the cercaria schistosomulum transformation, in vivo. Rev. Soc. bras. Med. trop., 18: 17-21, 1985.

[17] 17. MELO, A.L.; MACHADO, C.R.S. & PEREIRA, L.H. - Differences between in vitro and in vivo obtained schistosomules. Rev. Inst. Med. trop. S. Paulo, 32: 84-85, 1990.

[18] 18. MELO, A.L.; MACHADO, C.R.S. & PEREIRA, L.H. - Host cell adhesion to Schistosoma mansoni larvae in the peritoneal cavity of naive mice. Histological and scanning electron microscopic studies. Rev. Inst. Med. trop. S. Paulo, 35 (1): 1993.

[19] 19. PEREIRA, L.H.; PELLEGRINO, J.; VALADARES, T.E.; MELLO, R.T. & COELHO, P.M.Z. - A new approach for screening prophylactic agents in schistosomiasis. Rev. Inst. Med. trop. S. Paulo, 16: 123-126, 1974.

[20] 20. RAMALHO-PINTO, F.J.; McLAREN, D.J. & SMITHERS, S.R. - Complement-mediated killing of schistosomula of Schistosoma mansoni by rat eosinophils in vitro. J. exp. Med., 147: 147-156, 1978.

[21] 21. SINGER, I.I.; SCOTT, S.; KAWKA, D.W. & KAZAZIS, D.M. - Adhesomes: specific granules containing receptors for laminin, C3bi/fibrinogen, fibronectin, and vitronectin in human polymorphonuclear leukocytes and monocytes. J. Cell Biol., 109: 3169-3182, 1989.

[22] 22. STIREWALT, M.A. - Schistosomule vs cercariae. J. Parasit., 47: 47, 1961.

[23] 23. STIREWALT, M.A. - Schistosoma mansoni: cercaria to schistosomule. Advanc. Parasit., 12: 115-182, 1974.

[24] 24. STIREWALT, M.A.; MINNICK, D.R. & FREGEAU, W.A. - Definition and collection in quantity of schistosomules of Schistosoma mansoni. Trans. roy. Soc. trop. Med. Hyg., 60: 352-360, 1966.

[25] 25. STIREWALT, M.A. & UY, A. - Schistosoma mansoni: cercarial penetration and schistosomule collection in an in vitro system. Exp. Parasit., 26: 17-28, 1969.

[26] 26. VON LICHTENBERG, F.; SHER, A.; GIBBONS, N. & DOUGHTY, B.L. - Eosinophil enriched inflammatory response to schistosomula in the skin of mice immune to Schistosoma mansoni. Amer. J. Path., 84: 479-500, 1976.

Brasil

Brasil

Interaction between neutrophils and Schistosoma mansoni larvae in vivo: a transmission electron-microscopic study

Interação entre neutrófilos e larvas de Schistosoma mansoni in vivo: estudo ao microscópio eletrônico de transmissão

Abstracts

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History