Skip to main content
SpringerLink
Log in

The role of the bone marrow in bovine trypanotolerance II. Macrophage function inTrypanosoma congolense-infected cattle

  • Original Article
  • Published:
Comparative Haematology International Aims and scope Submit manuscript

Abstract

Sequential biopsies of sternal bone marrow (BM) of three trypanosusceptible Boran and three trypanotolerant N'Dama cattle were examined by light and transmission electron microscopy before and up to 112 days postinfection (DPI) withTrypanosoma congolense. Before infection, the percentage of cells of the mononuclear phagocyte system (MPS) including the macrophage (Mϕ) and the calculated index of Mϕ volume in the BM were similar in both breeds, whereas the mean Mϕ surface area was significantly higher (p<0.0001) in the Boran than in the N'Dama. DuringT. congolense infection, the MPS cell counts, the Mϕ surface area and the calculated Mϕ volume index increased significantly in both breeds particularly in the N'Dama.

Macrophages phagocytosed only a few erythrocytes and mature neutrophils in both breeds before infection. During infection, Mϕ engulfed many erythrocytes, reticulocytes, normoblasts, granulocytes and their precursors, and thrombocytes, as well as few lymphocytes and monocytes. Many Mϕ phagocytosed cells from more than one cell lineage, and phagocytosis of nucleated cells was preceded by attraction of the target cell and subsequent adhesion to the Mϕ, suggesting a common mechanism of cell destruction. The Mϕ of cattle maintained contact, through reciprocal U- or V-shaped microvilli or filiform processes, with haemopoietic cells. These contacts increased during the acute phase ofT. congolense infection in both breeds and remained elevated in the N'Dama until 112 DPI, whereas they dropped to preinfection levels in the chronic phase (98, 112 DPI) in the Boran.

Cumulatively, the absolute numbers, surface area, organelle contents and calculated volume index of the Mϕ, percentage of Mϕ with phagocytosed cells, the total cells engulfed, adhesion of target cell to Mϕ prior to phagocytosis, phagocytosis of multiple cell lines, as well as the percentage of Mϕ in contact with haemopoietic cells, and the total haemopoietic cells in contact with Mϕ were significantly higher in the N'Dama than in the Boran. Cell phagocytosis and contact with haemopoietic cells decreased in Boran cattle during the chronic phase but remained elevated in the N'Dama.

The positive balance between the beneficial effects of Mϕ activation in the BM (enhanced haematopoiesis, and presumably parasite clearance and antigen processing) and its deleterious effect (cytophagia) was greater in the trypanotolerant N'Dama than in the Boran, enabling the N'Dama to resist infection better. This study therefore demonstrates that superior BM responses, pivoted on vital Mϕ functions, play a major role in trypanotolerance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abebe G, Shaw MK, Eley RM (1993)Trypanosoma congolense in the microvasulature of the pituitary gland in experimentally infected Boran (Bos indicus) cattle. Vet Pathol 30:401–409

    PubMed  CAS  Google Scholar 

  • Anosa VO, Isoun TT (1983) Pathology of experimentalTrypanosoma vivax infection in sheep and goats. Zentralbl Veterinarmed B 30:685–700

    PubMed  CAS  Google Scholar 

  • Anosa VO, Kaneko JJ (1983a) Pathogenesis ofTrypanosoma brucei infection in deer mice (Peromyscus maniculatus). Light and electron microscopic studies on erythrocyte pathologic changes and phagocytosis. Am J Vet Res 44:645–651

    PubMed  CAS  Google Scholar 

  • Anosa VO, Kaneko JJ (1983b) Pathogenesis ofTrypanosoma brucei infection in deer mice (Peromyscus maniculatus). V. Macrophage ultrastructure and function. Vet Pathol 20:617–631

    PubMed  CAS  Google Scholar 

  • Anosa VO, Kaneko JJ (1984a) Pathogenesis ofTrypanosoma brucei infection in deer mice (Peromyscus maniculatus). Ultrastructural pathology of the spleen, liver, heart and kidney. Vet Pathol 21:229–237

    PubMed  CAS  Google Scholar 

  • Anosa VO, Kaneko JJ (1984b) Pathogenesis ofTrypanosoma brucei infection in deer mice (Peromyscus maniculatus). Light and electron microscopic study of testicular lesions. Vet Pathol 21:238–246

    PubMed  CAS  Google Scholar 

  • Anosa VO, Kaneko JJ (1989) Ultrastructural pathology of haemopoietic organs inTrypanosoma vivax infection in goats. Vet Pathol 26:78–83

    PubMed  CAS  Google Scholar 

  • Anosa VO, Obi TU (1980) Haematological studies on domestic animals in Nigeria. III. The effects of age breed and haemoglobin type on bovine haematology and anaemia. Zentral Veterinarmed B 27:773–788

    CAS  Google Scholar 

  • Anosa VO, Logan-Henfrey LL, Shaw MK (1992) A light and electron microscopic study of changes in blood and bone marrow in acute haemorrhagicTrypanosoma vivax infection in calves. Vet Pathol 29:33–45

    PubMed  CAS  Google Scholar 

  • Anosa VO, Logan-Henfrey LL, Wells CW (1997a) The haematology ofTrypanosoma congolense infection in cattle. I. Sequential cytomorphologic changes in the blood and bone marrow of adult Boran cattle. Comp Haematol Inter 7:14–22

    Article  Google Scholar 

  • Anosa VO, Logan-Henfrey LL, Wells CW (1997b) The haematology ofTrypanosoma congolense infection in cattle. II. Macrophage structure and function in the bone marrow of Boran cattle. Comp Haematol int 7:23–29

    Article  Google Scholar 

  • Askomas BA (1985) Macrophages as mediators of immunsuppression in murine African trypanosomiasis. Curr Top Microbiol Immunol 117:119–127

    Google Scholar 

  • Crocker PR, Milon G (1992) Macrophages in the control of haematopoiesis. In: Lewis CE, McGee JOD (eds) The macrophage: the natural immune system. Oxford University Press, Oxford, pp 116–156

    Google Scholar 

  • Crocker PR, Morris L, Gordon S (1988) Novel cell surface adhesion receptors involved in interactions between stromal macrophages and haematopoietic cells. J Cell Sci Suppl 9:185–206

    PubMed  CAS  Google Scholar 

  • Dargie JD, Murray PK, Murray M et al. (1979) Bovine trypanosomiasis. I. The red cell kinetics of N'Dama and Zebu cattle infected withTrypanosoma congolense. Parasitology 78:271–286

    Article  PubMed  CAS  Google Scholar 

  • Desowitz RS (1959) Studies on the immunity and host parasite relationships. I. The immunological response of resistant and susceptible breeds of cattle to typanosome challenge. Ann Trop Med Parasitol 53:293–313

    PubMed  CAS  Google Scholar 

  • Ezekowitz RAB, Austyn J, Stahl PD et al. (1981) Surface properties of BCG-activated mouse macrophages. J Exp Med 154:60–76

    Article  PubMed  CAS  Google Scholar 

  • Fierer J, Askonas BA (1982)Trypanosoma brucei infection stimulates receptor-mediated phagocytosis by murine peritoneal macrophages. Infect Immun 37:1282–1284

    PubMed  CAS  Google Scholar 

  • Gordon S, Perry VH, Rabinowitz S et al. (1988) Plasma membrane receptors of the mononuclear phagocyte system. J Cell Sci Suppl 9:1–26

    PubMed  CAS  Google Scholar 

  • Greenblatt HC, Diggs CL, Aikawa M (1983) Antibody-dependent phagocytosis ofTrypanosoma rhodesiense by murine macrophages. Am J Trop Med Hyg 321:33–45

    Google Scholar 

  • Grossinsky CM, Askonas BA (1981) Macrophages as primary target cells and mediators of immune dysfunction in African trypanosomiasis. Infect Immun 33:149–155

    Google Scholar 

  • Ikede BO, Losos GJ (1972) Pathogensesis of the disease in sheep produced byTrypanosoma brucei. Vet Pathol 9:278–289

    Article  PubMed  CAS  Google Scholar 

  • Logan-Henfrey LL, Anosa VO, Wells CM (2000) The role of the bone marrow in bovine trypanotolerance I. Changes in blood and bone marrow inTrypanosoma congolense-infected in cattle. Comp Haematol Int 10:??-??

    Google Scholar 

  • Mackenzie PKI, Cruickshank JG (1973) Phagocytosis of erythrocytes and leucocytes in sheep infected withTrypanosoma congolense (Broden 1904). Res Vet Sci 15:256–262

    PubMed  CAS  Google Scholar 

  • Murray M, Morrison WI, Whitelaw DD (1982) Host specificity to African trypanosomiasis: trypanotolerance. Adv Parasitol 21:1–67

    Article  PubMed  CAS  Google Scholar 

  • Paling RW, Moloo SK, Scott JR et al. (1991a) Susceptibility of N'Dama and Boran cattle to a tsetse-transmitted primary and rechallenge infections with a homologous serodeme ofTrypanosoma congolense. Parasite Immunol 13:413–425

    PubMed  CAS  Google Scholar 

  • Paling RW, Moloo SK, Scott JR (1991b) Susceptibility of N'Dama and Boran cattle to sequential challenges with tsetse-transmitted clones ofTrypanosoma congolense. Parasite Immunol 13:427–445

    PubMed  CAS  Google Scholar 

  • Sileghem M, Flynn JN, Darji A et al. (1994). African trypanosomiasis. In: Kierszenbaum (ed) Parasitic infections and the immune system. Academic Press, London, pp 1–51

    Google Scholar 

  • Snedecor GW, Cochran WG (1980) Statistical methods, 7th edn. Iowa State University Press, Ames

    Google Scholar 

  • Stevens DR, Moulton JE (1978) Ultrastructural and immunological aspects of the phagocytosis ofTrypanosoma brucei by mouse peritoneal macrophages. Infect Immun 19:972–982

    PubMed  CAS  Google Scholar 

  • Valli VEO, Forsberg CM (1979) The pathogenesis ofTrypanosoma congolense infection in valves. Quantitative histological changes. Vet Pathol 16:334–368

    PubMed  CAS  Google Scholar 

  • Weiss L. (1983) Haemopoietic tissue in malaria: facilitation of erythrocyte recycling by bone marrow inPlasmodium berghei-infected mice. J Parasitol 69:307–308

    Article  PubMed  CAS  Google Scholar 

  • Whitelaw DG, Mackaskil JA, Holmes PH et al. (1980) Genetic resistance toTrypanosoma congolense infections in mice. Infect Immun 27:707–713

    PubMed  CAS  Google Scholar 

  • Williams DJ, Logan-Henfrey LL, Authie E et al. (1992) Experimental infection with a haemorrhage-causingTrypanosoma vivax in N'Dama and Boran cattle. Scand J Immunol 36: suppl 11, 34–36

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. International Livestock Research Institute, Nairobi, Kenya

    V. O. Anosa, L. L. Logan-Henfrey & C. W. Wells

Authors
  1. V. O. Anosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. L. Logan-Henfrey
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. W. Wells
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to V. O. Anosa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Anosa, V.O., Logan-Henfrey, L.L. & Wells, C.W. The role of the bone marrow in bovine trypanotolerance II. Macrophage function inTrypanosoma congolense-infected cattle. Comp Haematol Int 9, 208–218 (1999). https://doi.org/10.1007/BF02585507

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02585507

Keywords

Search

Navigation