Regulation of Parasitaemia in Mice Infected with Trypanosoma brucei

  • S. J. Black
  • C. N. Sendashonga
  • C. O’Brien
  • N. K. Borowy
  • M. Naessens
  • P. Webster
  • M. Murray
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 117)

Abstract

Salivarian trypanosomes are spindle-shaped Protozoa belonging to the class Zoomastigophorea, order Kinetoplastida and genus Trypanosoma (Hoare 1970). The parasites are the causative agents of human sleeping sickness (T. brucei) and of trypanosomiases (nagana) affecting domestic animals (T. vivax, T. congolense, T. simiae, T. brucei, T. suis). Salivarian trypanosomes are generally transmitted from mammal to mammal by tsetse flies (Glossina), and their distribution coincides with that of their vector. Tsetse flies are distributed throughout East, Central and West Africa over an area embracing 38 countries and covering approximately 10 million km2. Several control measures have been tried for trypanosomiasis, including eradication of tsetse fly habitats, eradication of tsetse flies, eradication of the reservoir hosts of trypanosomes (wild animals), chemoprophylaxis and/or diagnosis followed by chemotherapy. For a variety of social, political and practical reasons, none of these control measures has met with lasting success (Duggan 1970). Attempts to develop a vaccine against the parasites have been unsuccessful to date owing to extensive parasite antigenic diversity.

Keywords

Cholesterol Albumin Carbohydrate Adenosine Dehydration 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ashcroft MT (1957) The polymorphism of Trypanosoma brucei and Trypanosoma rhodesiense, its relationship to relapses and remissions of infections in white rats, and the effect of cortisone. Ann Trop Med Parasitol 51: 301–312PubMedGoogle Scholar
  2. Avrameas S, Leduc EH (1970) Detection of simultanous antibody synthesis in plasma cells and specialised lymphocytes in rabbit lymphnodes. J Exp Med 131: 1137–1168PubMedCrossRefGoogle Scholar
  3. Balber AE (1972) Trypanosoma brucei: Fluxes of the morphological variants in intact and x-irradiated mice. Exp Parasitol 31: 307–319PubMedCrossRefGoogle Scholar
  4. Balber AE (1983) Primary murine bone marrow cultures support continuous growth of infective human trypanosomes. Science 220: 421–423PubMedCrossRefGoogle Scholar
  5. Black SJ, Hewett RS, Sendashonga CN (1982) Trypanosoma brucei variable surface coat is released by degenerating parasites but not by actively dividing parasites. Parasite Immunol 4: 233–244PubMedCrossRefGoogle Scholar
  6. Black SJ, Jack RM, Morrison WI (1983a) Host: parasite interactions which influence the virulence of Trypanosoma (Trypanozoon) brucei brucei organisms. Acta Trop (Basel) 40: 11–18Google Scholar
  7. Black SJ, Sendashonga CN, Lalor PA, Whitelaw DD, Jack RM, Morrison WI, Murray M (1983b) Regulation of the growth and differentiation of Trypanosoma (Trypanozoon) brucei brucei in resistant (C57B1/6) and susceptible (C3H/He) mice. Parasite Immunol 5: 465–478PubMedCrossRefGoogle Scholar
  8. Bruce D, Hamerton AE, Bateman HR, Macie FP (1910) Trypanosome disease of domestic animals in Uganda. II: Trypanosoma brucei (Plimmer and Bradford). Proc R Soc B 80: 394–398CrossRefGoogle Scholar
  9. Bruce D, Hamerton AE, Watson DP, Bruce ME (1914) Morphology of various strains of the trypanosome causing disease in man in Nyasaland. Proc R Soc B 88: 190–205CrossRefGoogle Scholar
  10. Brun R, Schonenberger M (1979) Cultivation and in vitro cloning of procyclic culture forms of Trypanosoma brucei in a semidefined medium. Acta Trop (Basel) 36: 289–292Google Scholar
  11. Brun R, Jenni L, Schonenberger M, Schell KF (1981) In vitro cultivation of bloodstream forms of Trypanosoma brucei, T. rhodesiense and T. gambiense. J Protozool 28: 470–479PubMedGoogle Scholar
  12. Campbell GH, Esser KM, Weinbaum FI (1977) Trypanosoma rhodesiense infection in B-cell deficient mice. Infect Immun 18: 434–438PubMedGoogle Scholar
  13. Campbell GH, Esser KM, Phillips SM (1978) Trypanosoma rhodesiense infection in congenitally athymic (nude) mice. Infect Immun 20: 714–720PubMedGoogle Scholar
  14. Clayton CE, Sacks DL, Ogilvie BM, Askonas BA (1979a) Membrane fractions of trypanosomes mimic the immunosuppressive and mitogenic effects of living parasites on the host. Parasite Immunol 1: 241–249PubMedCrossRefGoogle Scholar
  15. Clayton CE, Ogilvie BM, Askonas BA (1979b) Trypanosoma brucei infection in nude mice: B-lymphocyte function is suppressed in the absence of T-lymphocytes. Parasite Immunol 1: 39–48PubMedCrossRefGoogle Scholar
  16. Corsini AC, Clayton C, Askonas BA, Ogilvie BM (1977) Suppressor cells and loss of B-cell potential in mice infected with Trypanosoma brucei. Clin Exp Immunol 29: 122–131PubMedGoogle Scholar
  17. Cunningham MP, Van Hoeve K, Lumsden WHR (1963) Variable infectivity of organisms of the T. brucei subgroup during acute relapsing infections in rats, related to parasitaemia, morphology and antibody response. Ann Rep EA Tryp Res Org 1962-1963, p 21Google Scholar
  18. Duggan AJ (1970) An historical perspective. In: Mulligan HW (ed) The African trypanosomiases. Allen and Unwin/Ministry of Overseas Development, London, pp XII–LXXXVIIIGoogle Scholar
  19. Flynn IW, Bowman IBR (1973) The metabolism of carbohydrate by pleomorphic African trypanosomes. Comp Biochem Physiol 45B: 25–42Google Scholar
  20. Goedbloed E, Kinyanjui H (1970) Development of African pathogenic trypanosomes in chicken embryos. Exp Parasitol 27: 464–478PubMedCrossRefGoogle Scholar
  21. Grabstein K, Chen YU (1980) Cell-mediated cytolytic responses. In: Mishell BB, Shiigi SM (eds) Selected methods in cellular immunology. Freeman, San Francisco, pp 129–130Google Scholar
  22. Gray AR (1962) The influence of antibody on serological variation in Trypanosoma brucei. Ann Trop Med Parasitol 56: 4–13PubMedGoogle Scholar
  23. Greenwood BM (1974) Possible role of a B-cell mitogen in hypergamma-globulinaemia in malaria and trypanosomiasis. Lancet I: 435CrossRefGoogle Scholar
  24. Greig WA, Murray M, Murray PK, McIntyre WIM (1979) Factors affecting blood sampling for anaemia and parasitaemia in Bovine Trypanosomiasis. Br Vet J 135: 130–141PubMedGoogle Scholar
  25. Hall T, Esser K (1984) Topologic mapping of protective and non-protective epitopes on the variant surface glycoprotein of the WRATat 1 clone of Trypanosoma brucei rhodesiense. J Immunol 132: 2059–2063PubMedGoogle Scholar
  26. Hill GC, Shimer S, Caughey B, Sauer S (1978a) Growth of infective forms of Trypanosoma (T.) brucei on buffalo lung and Chinese hamster lung tissue culture cells. Acta Trop (Basel) 35: 201–207Google Scholar
  27. Hill GC, Shimer S, Caughey B, Sauer S (1978b) Growth of infective forms of Trypanosoma rhodesiense in vitro, the causative agent of African trypanosomiasis. Science 202: 763–765PubMedCrossRefGoogle Scholar
  28. Hirumi H, Doyle JJ, Hirumi K (1977) African Trypanosomes: cultivation of animal infective Trypanosoma brucei in vitro. Science 196: 992–994PubMedCrossRefGoogle Scholar
  29. Hirumi H, Hirumi K, Nelson RT, Bwayo JJ (1980) Present status of in vitro cultivation of animal infective African trypanosomes. In: The in vitro cultivation of the pathogens of tropical diseases. Schwabe, Basel, pp 165–200 (Tropical diseases research series no. 3)Google Scholar
  30. Hoare CA (1970) Systematic description of the mammalian trypanomes of Africa. In: Mulligan HW (ed) The African trypanosomiases. Allen and Unwin/Ministry of Overseas Development, London, pp 41–48Google Scholar
  31. Hudson KM, Byner C, Freeman J, Terry RJ (1976) Immunodepression, high IgM levels and evasion of the immune response in murine trypanosomiasis. Nature 264: 256–258PubMedCrossRefGoogle Scholar
  32. Iscove NN, Melchers F (1978) Complete replacement of serum by albumin, transferrin and soybean lipid in cultures of lipopolysaccharide-reactive B-lymphocytes. J Exp Med 147: 923–933PubMedCrossRefGoogle Scholar
  33. Jack RM, Black SJ, Reed SL, Davis CE (1984) Indomethacin promotes differentiation of Trypanosoma brucei. Infect Immun 43: 445–448PubMedGoogle Scholar
  34. Jayawardena AN, Waksman BH (1977) Suppressor cells in experimental Trypanosomiasis. Nature 265: 539–541PubMedCrossRefGoogle Scholar
  35. Langreth SC, Balber AE (1975) Protein uptake and digestion in bloodstream and culture forms of Trypanosoma brucei. J Protozool 22: 40–53PubMedGoogle Scholar
  36. Lanham MS (1968) Separation of trypanosomes from the blood of infected rats and mice by anion-exchangers. Nature 218: 1273–1274PubMedCrossRefGoogle Scholar
  37. Levine RF, Mansfield JM (1984) Genetics of resistance to the African trypanosomes. III: Variant-specific antibody responses of H-2 compatible resistance and susceptible mice. J Immunol 133: 1564–1569PubMedGoogle Scholar
  38. MacAskill JA, Holmes PH, Jennings FW, Urquhart GM (1981) Immunological clearance of 75Se-labelled Trypanosoma brucei in mice. III: Studies in animals with acute infections. Immunology 43: 691–698PubMedGoogle Scholar
  39. Mancini PE, Patton CL (1981) Cyclic 3′,5′-adenosine monophosphate levels during the developmental cycle of Trypanosoma brucei brucei in the rat. Mol Biochem Physiol 3: 19–31Google Scholar
  40. Mao SJT, Downing MR, Kottke BA (1980) Physical, chemical and immunochemical studies of apolipoprotein A-1 from pigeon plasma high density lipoprotein. Biochim Biophys Acta 620: 100–110PubMedGoogle Scholar
  41. Mshelbwala AJ (1967) Infectivity of Trypanosoma rhodesiense to tsetse flies fed through animal membranes. Nature 215: 441PubMedCrossRefGoogle Scholar
  42. Murray M, Urquhart GM (1977) Immunoprophylaxis against African trypanosomiasis. In: Miller LH, Pino JA, McKelvey JJ Jr (eds) Immunity to blood parasites of animals and man. Plenum, New York, pp 209–241Google Scholar
  43. Murray M, Morrison WI, Murray PK, Clifford DJ, Trail JCM (1979a) Trypanotolerance: a review. Wld Anim Rev 31: 2–12Google Scholar
  44. Murray M, Huan CN, Lambert PH, Gerber H (1979b) The anaemia of african trypanosomiasis. In: Fifteenth Meeting of the International Scientific Council for Trypanosomiasis Research and Control, Banjul, The Gambia 1977. pp 460–469. Scientific Publications Division of Eleza Services, Nairobi, pp 460–469 (OAU/STRC no. 110)Google Scholar
  45. Murray M, Morrison WI, Whitelaw DD (1982) Host susceptibility to African trypanosomiases: Trypanotolerance. Adv Parasitol 21: 1–68PubMedCrossRefGoogle Scholar
  46. Nantulya VM, Musoke AJ, Barbet AF, Roelants GE (1979) Evidence for reappearance of Trypanosoma brucei variable antigen types in relapse populations. J Parasitol 65: 673–679PubMedCrossRefGoogle Scholar
  47. Nielsen K, Sheppard J, Holmes W, Tizard I (1978) Experimental bovine trypanosomiasis: Changes in the catabolism of serum immunoglobulins and complement components in infected cattle. Immunology 35: 811–816PubMedGoogle Scholar
  48. Oehler R (1913) Zur Gewinnung reiner Trypanosomastämme. Zentralblatt für Bakteriologie, Parasitenkunde und Infektionskrankheiten 70: 110–111Google Scholar
  49. Oehler R (1914) Der Dimorphismus des Trypanosoma brucei bei experimentellen Behandlung. Zeitschrift für Hygiene und Infectionskrankheit 78: 188–191CrossRefGoogle Scholar
  50. Oi VT, Herzenberg LA (1980) Immunoglobulin-producing hybrid cell lines. In: Mishell BB, Shiigi SM (eds) Selected methods in cellular immunology. Freeman, San Francisco, pp 351–372Google Scholar
  51. Ormerod WE (1958) A comparative study of cytoplasmic inclusions (volutin granules) in different species of trypanosomes. J Gen Microbiol 19: 271–288PubMedGoogle Scholar
  52. Paris J, Murray M, McOdimba F (1982) A comparative evaluation of the parasitological techniques currently available for the diagnosis of African trypanosomiasis in cattle. Acta Trop (Basel) 37: 307–316Google Scholar
  53. Pearson TW, Roelants GE, Pinder M, Lundin LB, Mayor-Withey KS (1979) Immunodepression in trypanosome infected mice. III: Suppressor cells. Eur J Immunol 9: 200–204PubMedCrossRefGoogle Scholar
  54. Pearson TW, Pinder M, Roelants GE, Kar SK, Lundin LB, Mayor-Withey KS, Hewett RS (1980) Methods for derivation and analysis of anti-parasite monoclonal antibodies. J Immunol Methods 34: 141–154PubMedCrossRefGoogle Scholar
  55. Rickman L, Mwanza S, Kanyangala S, Kolala F (1982) The isolation of T. brucei-like organisms from man. Ann Trop Med Parasitol 76: 223–224PubMedGoogle Scholar
  56. Rifkin MR (1978) Identification of the trypanocidal factor in normal human serum: High-density lipoprotein. Proc Natl Acad Sci USA 75: 3450–3454PubMedCrossRefGoogle Scholar
  57. Robertson M (1913) Notes on the behaviour of a polymorphic trypanosome in the bloodstream of the mammalian host. Report of the Sleeping Sickness Commission of the Roy Society 13: 111–119Google Scholar
  58. Rose LM, Goldman M, Lambert PH (1982) Simultaneous induction of an idiotype, corresponding anti-idiotypic antibodies and immune complexes during African trypanosomiasis in mice. J Immunol 128: 79–84PubMedGoogle Scholar
  59. Sacks DL, Askonas BA (1980) Trypanosome-induced suppression of antiparasite responses during experimental African trypanosomiasis. Eur J Immunol 10: 971–974PubMedCrossRefGoogle Scholar
  60. Sacks DL, Selkirk ME, Ogilvie BM, Askonas BA (1980) Intrinsic immunosuppressive activity varies with parasite virulence. Nature 283: 476–478PubMedCrossRefGoogle Scholar
  61. Schalm OW, Jain WC, Carrol EJ (1975) Veterinary hematology, 3rd edition. Lea and Febiger, Philadelphia, pp 26–27Google Scholar
  62. Selkirk ME, Sacks DL (1980) Trypanotolerance in inbred mice: An immunological basis for variation in susceptibility to infection with Trypanosoma brucei. Tropenmed Parasitol 31: 435–438PubMedGoogle Scholar
  63. Sendashonga CN (1983) Induction, expression and regulation of antibody responses against Trypanosoma brucei brucei in mice. PhD Thesis, ILRAD LibraryGoogle Scholar
  64. Sendashonga CN, Black SJ (1982) Humoral immune responses against Trypanosoma brucei variable surface antigens are induced by degenerating parasites. Parasite Immunol 4: 245–257PubMedCrossRefGoogle Scholar
  65. Shapiro SZ, Naessens J, Leisegang B, Moloo SK, Magondu J (1984) Analysis by flow cytometry of DNA synthesis during the life cycle of African trypanosomes. Acta Trop (Basel) 41: 313–323Google Scholar
  66. Ssenyonga GSZ, Adam KMG (1975) The number and morphology of trypanosomes in the blood and lymph of rats infected with Trypanosoma brucei and T. congolense. Parasitology 70: 255–261PubMedCrossRefGoogle Scholar
  67. Steiger RF (1973) On the ultrastructure of Trypanosoma (Trypanozoon) brucei in the course of its life cycle and some related aspects. Acta Trop (Basel) 30: 1–168Google Scholar
  68. Swellengrebel NH (1912) Zur Kenntnis des Dimorphismus von Trypanosoma gambiense (var. rhodesiense). Zentralblatt für Bakteriologie, Parasitenkunde und Infectionskrankheiten 61: 193–206Google Scholar
  69. Tanner M, Jenni L, Hecker H, Brun R (1980) Characterization of Trypanosoma brucei isolated from lymph nodes of rats. Parasitology 80: 383–391PubMedCrossRefGoogle Scholar
  70. Tarktakoff A, Hoessli D, Vassali P (1981) Intracellular transport of lymphoid surface glycoproteins: role of the Golgi complex. J Mol Biol 150: 525 - 535CrossRefGoogle Scholar
  71. Tsu TT, Herzenberg LA (1980) Solid-phase radioimmunoassay. In: Mishell BB, Shiigi SM (eds) Selected methods in cellular immunology. Freeman, San Francisco, pp 373–397Google Scholar
  72. Van Meirvenne N, Magnus E, Janssens PG (1976) The effect of normal human serum on trypanosomes of distinct antigenic type (ETAT 1 to 12) isolated from a strain of Trypanosoma brucei rhodesiense. Ann Soc Belge Med Trop 1: 55–63Google Scholar
  73. Van Prewazek S (1913) Überreine Trypanosomenstamme. Zentralblatt für Bakteriologie, Parasitenkunde und Infektionskrankheiten 68: 498–501Google Scholar
  74. Venkatesan S, Ormerod WE (1976) Lipid content of the slender and stumpy forms of Trypanosoma brucei rhodesiense: a comparative study. Comp Biochem Physiol 53B: 481–487CrossRefGoogle Scholar
  75. Venkatesan S, Bird RG, Ormerod WE (1977) Intracellular enzymes and their localization in slender and stumpy forms of Trypanosoma brucei rhodesiense. Int J Parasitol 7: 139–147PubMedCrossRefGoogle Scholar
  76. Vickerman K (1962) The mechanism of cyclical development in Trypanosoma brucei subgroup: an hypothesis based on ultrastructural observations. Trans R Soc Trop Med Hyg 56: 487–495PubMedCrossRefGoogle Scholar
  77. Vickerman K (1965) Polymorphism and mitochondrial activity in sleeping sickness trypanosomes. Nature (Lond) 208: 762–766CrossRefGoogle Scholar
  78. Vickerman K (1971) Morphological and physiological considerations of extracellular blood protozoa. In: Fallis AM (ed) Ecology and physiology of parasites. University of Toronto Press, Toronto, pp 58–91Google Scholar
  79. Weiss L (1972) The cells and tissues of the immune system: structure, functions, interactions Prentice-Hall. Englewood Cliffs, pp 157–159. (Foundations of immunology series)Google Scholar
  80. Wellhausen SR, Mansfield JM (1979) Lymphocyte function in experimental African trypanosomiasis. II: Splenic suppressor cell activity. J Immunol 122: 818–824PubMedGoogle Scholar
  81. WHO (1978) Immunodeficiency report of a WHO scientific group. World Health Organization, Geneva (Technical report series, no 630 )Google Scholar
  82. Wijers DJB (1959) Polymorphism in Trypanosoma gambiense and Trypanosoma rhodesiense and the significance of intermediate forms. Ann Trop Med Parasitol 53: 59PubMedGoogle Scholar
  83. Wijers DJB, Willett KC (1960) Factors that may influence the infection rate of Glossina palpalis with Trypanosoma gambiense. II: The number and morphology of the trypanosomes present in the blood of the host at the time of the infected feed. Ann Trop Med Parasitol 54: 341–346PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1985

Authors and Affiliations

  • S. J. Black
    • 1
  • C. N. Sendashonga
    • 1
  • C. O’Brien
    • 1
  • N. K. Borowy
    • 1
  • M. Naessens
    • 1
  • P. Webster
    • 1
  • M. Murray
    • 1
  1. 1.ILRADNairobiKenya

Personalised recommendations