The role of spleen macrophages in malaria: an ultrastructural study

Tosta, Carlos Eduardo; Ruiz, Greta; Wedderburn, Nina

doi:10.1590/S0037-86821984000100007

Abstracts

An electronmicroscopy study of the spleen from mice infected with Plasmodium berghei was carried out to investigate the types ofcells in volved in the removal of parasites from the blood, and the mechanisms by which this occurs. Macrophages, particularly from the red pulp and the marginal zone of the spleen, constituted the most important population of phagocytic cells in the spleen. At the height ofparasitaemia, macrophages in the periphery of the white pulp, especially in the mantle zone of secondary follicles, were also found to participate in phagocytosis, although to a limited extent. Our fingings suggest that phagocytosis of free parasites or parasitized erythrocytes in the spleen is an important mechanism of clearance of parasites from the circulation. Parasites removed from the erythrocytes when these cells cross the interendothelial slits are further phagocytosed by neighbouring macrophages. Evidence is presented suggesting that spleen macrophages may act against the parasite through a process of cytotoxicity.

Malaria; Plasmodium berghei; BALB/c mice; Spleen; Macrophages; Phagocytosis; Cytotoxicity

O presente estudo objetivou investigar através de microscopia eletrônica a natureza das células esplênicas envolvidas no processo de retirada do Plasmodium berghei do sangue de camundongos BALB/c infectados e os possíveis mecanismos utilizados. Os macrófagos, particularmente da polpa vermelha e da zona marginal, constituíram a mais importante população de células fagocitárias do baço. No pico da parasitemia, macrófagos da periferia da polpa branca, principalmente da zona do manto dos folículos secundários também participaram do processo de fagocitose. Células reticulares e interdigitais também apresentaram atividade fago- citária, embora em grau limitado. Nossas observações sugerem que a fagocitose de parasitos livres e de eritrócitos parasitados constitui o principal mecanismo de destruição intra-esplênica do plasmódio. Os parasitos podem ser retirados dos eritrócitos quando estes atravessam as pequenas fendas interendoteliais dos sinusóides e são em seguida fagocitados por macrófagos. São apresentadas evidências de que macrófagos esplênicos podem destruir parasitos através de mecanismos de citotoxicidade.

Malária; Plasmodium berghei; Camundongos BALB/c; Baço; Macrófagos; Fagocitose; Citotoxicidade

ARTICLES

The role of spleen macrophages in malaria: An ultrastructural study¹ 1 From the Department of Pathology, Royal College of Surgeons of England, London, England.

Carlos Eduardo Tosta^I; Greta Ruiz; Nina Wedderburn

^IPresent address and address for correspondence: Laboratório de Imunologia Celular, Departamento de Medicina Complementar, Universidade de Brasília, 70910 Brasília, DF, Brazil

ABSTRACT

An electronmicroscopy study of the spleen from mice infected with Plasmodium berghei was carried out to investigate the types ofcells in volved in the removal of parasites from the blood, and the mechanisms by which this occurs. Macrophages, particularly from the red pulp and the marginal zone of the spleen, constituted the most important population of phagocytic cells in the spleen. At the height ofparasitaemia, macrophages in the periphery of the white pulp, especially in the mantle zone of secondary follicles, were also found to participate in phagocytosis, although to a limited extent. Our fingings suggest that phagocytosis of free parasites or parasitized erythrocytes in the spleen is an important mechanism of clearance of parasites from the circulation. Parasites removed from the erythrocytes when these cells cross the interendothelial slits are further phagocytosed by neighbouring macrophages. Evidence is presented suggesting that spleen macrophages may act against the parasite through a process of cytotoxicity.

Keywords: Malaria. Plasmodium berghei. BALB/c mice. Spleen. Macrophages. Phagocytosis. Cytotoxicity.

RESUMO

O presente estudo objetivou investigar através de microscopia eletrônica a natureza das células esplênicas envolvidas no processo de retirada do Plasmodium berghei do sangue de camundongos BALB/c infectados e os possíveis mecanismos utilizados. Os macrófagos, particularmente da polpa vermelha e da zona marginal, constituíram a mais importante população de células fagocitárias do baço. No pico da parasitemia, macrófagos da periferia da polpa branca, principalmente da zona do manto dos folículos secundários também participaram do processo de fagocitose. Células reticulares e interdigitais também apresentaram atividade fago- citária, embora em grau limitado. Nossas observações sugerem que a fagocitose de parasitos livres e de eritrócitos parasitados constitui o principal mecanismo de destruição intra-esplênica do plasmódio. Os parasitos podem ser retirados dos eritrócitos quando estes atravessam as pequenas fendas interendoteliais dos sinusóides e são em seguida fagocitados por macrófagos. São apresentadas evidências de que macrófagos esplênicos podem destruir parasitos através de mecanismos de citotoxicidade.

Palavras-chave: Malária. Plasmodium berghei. Camundongos BALB/c. Baço. Macrófagos. Fagocitose. Citotoxicidade.

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Recebido para publicação em 30/11/1983.

1. Basten A, Mitchell J. Role of macrophages in T-cell-B cell collaboration in antibody production. In: Nelson DS (ed) Immunobiology of the macrophage. Academic Press, New York, p. 45-90, 1976.
2. Braendstrup O, Andersen V, WerdelinO. Macrophage - lymphocyte clusters in the immune response to soluble protein antigen in vitro. III. DNA synthesis of lymphocy- tes in clusters. Cellularlmmunology 25: 207-216, 1976.
3. Chen LT, Weiss L. The role of the sinus wall in the passage of erythrocytes through the spleen. Blood 41: 529-537, 1973.
4. Clark IA, Virelizier JL, Carswell EA, Wood PR. The possible importance of macrophage - derived mediators in acute malaria. Infection and Immunity 32:105 8-1065, 1981.
5. Hunter KW Jr, Winkelstein JA, Simpson TW. Serum opsonic activity in rodent malaria: functional and im- munochemical characteristics in vitro. Journal of Im- munology 123: 2582-2587, 1979.
6. La Celle PL. Alteration of membrane deformability in hemolytic anemias. Seminars in Hematology 6: 355- 371, 1970.
7. Mitchell J, Nossal GJV. Localization and fate of foreign antigens ifi tissues. In: Samter M (ed) Immunological Diseases, 3^rd edn, vol. I, Little Brown, Boston, p. 22-34, 1978.
8. Moran CJ, de Rivera VS, Turk JL. The immunological significance of histological changes in the spleen and liver in mouse malaria. Clinical and Experimental Immunolo- gy 13: 467-478, 1973.
9. Schnitzer B, Sodeman T, Mead ML, Contacos PG. An ultrastructural study of the red pulp of the spleen in malaria. Blood 41: 207-218, 1973.
10. Steinman RM, Chen LL, Witmer MD, Kaplan G, Nussenzweig MC, Adams JC, Cohn ZA. Dendritic cells and macrophages - current knowledge of their distincti- ve properties and functions. In: van Furth R (ed) Mono- nuclear phagocytes. Functional aspects. Martinus Nij- hoff, The Hague, p. 1781-1799, 1980.
11. Tosta CE, Wedderburn N. Immune phagocytosis of Plasmodium yoelii - infected erythrocytes by macrophages and eosinophils. Clinical and Experimental Im- munology 42: 114-120, 1980.
12. Tosta CE. The functions of macrophages in rodent malaria. PhD Thesis. University of London, London, 1981.
13. Tosta CE, Hermans MAA. Atypical reticulocytes in rats with malaria as a possible consequence of the pitting function of the spleen. Annals of Tropical Medicine and Parasitology 75: 363-365, 1981.
14. Tosta CE. Effects of immune and hyperimmune serum on the dynamics of phagocytosis of Plasmodium berghei - infected erythrocytes. Revista do Instituto de Medicina Tropical de São Paulo 24: 140-147, 1982.
15. Tosta CE, Ruiz G, Wedderburn N. Effects of lethal and non-lethal malaria on the mononuclear phagocyte system. Revista da Sociedade Brasileira de Medicina Tropical 16: 58-67, 1983.
16. Weiss LP, Tavassoli M. Anatomical hazards to the passage of erythrocytes through the spleen. Seminars in Hematology 7: 372-380, 1970.
17. Wyler DJ. Cellular aspects of immunoregulation in malaria. Bulletin of the World Health Organization 57 (suppl. 1): 239-243, 1979.
18. Wyler DJ, Oster CN, QuinnTC. The role of the spleen in malaria infections. In: The role of the spleen in the immunology of parasitic diseases. W. H. O. Tropical Diseases Research Series n° 1. Schwabe, Basel, p. 183-204, 1979.
19. Wyler DJ. Splenic functions in malaria. Lymphology 16: 121-127, 1983.

1

From the Department of Pathology, Royal College of Surgeons of England, London, England.

Publication Dates

Publication in this collection
10 June 2013
Date of issue
Mar 1984

History

Received
30 Nov 1983
Accepted
30 Nov 1983

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

[1] 1. Basten A, Mitchell J. Role of macrophages in T-cell-B cell collaboration in antibody production. In: Nelson DS (ed) Immunobiology of the macrophage. Academic Press, New York, p. 45-90, 1976.

[2] 2. Braendstrup O, Andersen V, WerdelinO. Macrophage - lymphocyte clusters in the immune response to soluble protein antigen in vitro. III. DNA synthesis of lymphocy- tes in clusters. Cellularlmmunology 25: 207-216, 1976.

[3] 3. Chen LT, Weiss L. The role of the sinus wall in the passage of erythrocytes through the spleen. Blood 41: 529-537, 1973.

[4] 4. Clark IA, Virelizier JL, Carswell EA, Wood PR. The possible importance of macrophage - derived mediators in acute malaria. Infection and Immunity 32:105 8-1065, 1981.

[5] 5. Hunter KW Jr, Winkelstein JA, Simpson TW. Serum opsonic activity in rodent malaria: functional and im- munochemical characteristics in vitro. Journal of Im- munology 123: 2582-2587, 1979.

[6] 6. La Celle PL. Alteration of membrane deformability in hemolytic anemias. Seminars in Hematology 6: 355- 371, 1970.

[7] 7. Mitchell J, Nossal GJV. Localization and fate of foreign antigens ifi tissues. In: Samter M (ed) Immunological Diseases, 3^rd edn, vol. I, Little Brown, Boston, p. 22-34, 1978.

[8] 8. Moran CJ, de Rivera VS, Turk JL. The immunological significance of histological changes in the spleen and liver in mouse malaria. Clinical and Experimental Immunolo- gy 13: 467-478, 1973.

[9] 9. Schnitzer B, Sodeman T, Mead ML, Contacos PG. An ultrastructural study of the red pulp of the spleen in malaria. Blood 41: 207-218, 1973.

[10] 10. Steinman RM, Chen LL, Witmer MD, Kaplan G, Nussenzweig MC, Adams JC, Cohn ZA. Dendritic cells and macrophages - current knowledge of their distincti- ve properties and functions. In: van Furth R (ed) Mono- nuclear phagocytes. Functional aspects. Martinus Nij- hoff, The Hague, p. 1781-1799, 1980.

[11] 11. Tosta CE, Wedderburn N. Immune phagocytosis of Plasmodium yoelii - infected erythrocytes by macrophages and eosinophils. Clinical and Experimental Im- munology 42: 114-120, 1980.

[12] 12. Tosta CE. The functions of macrophages in rodent malaria. PhD Thesis. University of London, London, 1981.

[13] 13. Tosta CE, Hermans MAA. Atypical reticulocytes in rats with malaria as a possible consequence of the pitting function of the spleen. Annals of Tropical Medicine and Parasitology 75: 363-365, 1981.

[14] 14. Tosta CE. Effects of immune and hyperimmune serum on the dynamics of phagocytosis of Plasmodium berghei - infected erythrocytes. Revista do Instituto de Medicina Tropical de São Paulo 24: 140-147, 1982.

[15] 15. Tosta CE, Ruiz G, Wedderburn N. Effects of lethal and non-lethal malaria on the mononuclear phagocyte system. Revista da Sociedade Brasileira de Medicina Tropical 16: 58-67, 1983.

[16] 16. Weiss LP, Tavassoli M. Anatomical hazards to the passage of erythrocytes through the spleen. Seminars in Hematology 7: 372-380, 1970.

[17] 17. Wyler DJ. Cellular aspects of immunoregulation in malaria. Bulletin of the World Health Organization 57 (suppl. 1): 239-243, 1979.

[18] 18. Wyler DJ, Oster CN, QuinnTC. The role of the spleen in malaria infections. In: The role of the spleen in the immunology of parasitic diseases. W. H. O. Tropical Diseases Research Series n° 1. Schwabe, Basel, p. 183-204, 1979.

[19] 19. Wyler DJ. Splenic functions in malaria. Lymphology 16: 121-127, 1983.

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The role of spleen macrophages in malaria: an ultrastructural study

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