The same but different: The biology of Theileria sporozoite entry into bovine cells

International Journal for Parasitology

Volumn 27, Issue 5, 1997, Pages 457-474

  Shaw, Michael K ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Bovine cells; Host cell invasion; Sporozoites; Theileria; Theileria parva

Indexed keywords

CALCIUM ION; GUANINE NUCLEOTIDE BINDING PROTEIN; PHOSPHOTRANSFERASE;

CALCIUM MOBILIZATION; CATTLE DISEASE; CELL INVASION; FEVER; PARASITE DEVELOPMENT; REVIEW; SPOROZOITE; THEILERIA; THEILERIA PARVA; TICK BORNE DISEASE; TOXOPLASMA;

ANIMALS; CALCIUM; CATTLE; CYTOPLASM; CYTOSKELETON; ENDOPEPTIDASES; GTP-BINDING PROTEINS; HOST-PARASITE RELATIONS; LYMPHOCYTES; PROTEIN KINASES; SIGNAL TRANSDUCTION; THEILERIA; THEILERIASIS;

EID: 0030974627     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0020-7519(97)00015-5     Document Type: Review

References (120)

1. Aikawa M., Miller L. H., Johnson J. & Rabbege J. 1978. Erythrocyte entry by malarial parasites: a moving junction between erythrocyte and parasite. Journal of Cell Biology 77: 72-82.
2. Andrews N. W. & Portnoy D. A. 1994. Cytolysins from intracellular pathogens. Trends in Microbiology 2: 261-263.
3. Andrews N. W. & Webster P. 1991. Phagolysosomal escape by intracellular pathogens. Parasitology Today 7: 335-340.
4. Arrowood M. J., Sterling C. R. & Healey M. C. 1991. Immunofluorescent microscopical visualization of trails left by gliding Cryptosporidium parvum sporozoites. Journal of Parasitology 77: 315-317.
5. Baldwin C. W., Black S. J., Brown W. C., Conrad P. A., Goddeeris B. M., Kinuthia S. W., Lalor P. A., MacHugh N. D., Morrison W. I., Morzaria S. P., Naessens J. & Newson J. 1988. Bovine T cells, B cells, and Null cells are transformed by the protozoan parasite Theileria parva. Infection and Immunity 56: 462-467.
6. Bannister L. H. & Dluzewski A. R. 1990. The ultrastructure of red cell invasion in malaria infections. Blood Cells 16: 257-292.
7. Bannister L. H., Mitchell G. H., Butcher G. A., Dennis E. D. & Cohen S. 1986. Structure and development of the surface coat of erythrocytic merozoites of Plasmodium knowlesi. Cell and Tissue Research 245: 281-290.
8. Beckers C. J. M., Dubremetz J. F., Mercereau-Puijalon O. & Joiner K. A. 1994. The Toxoplasma gondii rhoptry protein ROP 2 is inserted into the parasitophorous vacuole membrane, surrounding the intracellular parasite, and is exposed to the host cell cytoplasm. Journal of Cell Biology 127: 947-961.
9. Bell G. I. 1978. Models for the specific adhesion of cells to cells: a theoretical framework for adhesion mediated by reversible bonds between cell surface molecules. Science (Washington) 200: 618-627.
10. Bliska J. B., Galan J. E. & Falkow S. 1993. Signal transduction in the mammalian cell during bacterial attachment and entry. Cell 73: 903-920.
11. Bootman M. D. & Berridge M. J. 1995. The elemental principles of calcium signaling. Cell 83: 675-678.
12. Boulter N., Knight P. A., Hunt P. D., Hennessey E. S., Katzer F., Tait A., Williamson S., Brown D., Baylis H. A. & Hall R. 1994. Theileria annulata sporozoite surface antigen (SPAG-1) contains neutralizing determinants in the C terminus. Parasite Immunology 16: 97-104.
13. Brown C. G. D., Stagg D. A., Purnell R. E., Kanhai G. K. & Payne R. C. 1973. Infection and transformation of bovine lymphoid cells in vitro by the infective particle of Theileria parva. Nature (London) 245: 101-103.
14. Brown E. M., Vassilev P. M. & Hebert S. C. 1995. Calcium ions as extracellular messengers. Cell 83: 679-682.
15. Burgoyne R. D. & Morgan A. 1993. Regulated exocytosis. Biochemical Journal 293: 305-316.
16. Campbell J. D., Brown D. J., Glass E. J., Hall F. R. & Spooner R. L. 1994. Theileria annulata sporozoite targets. Parasite Immunology 16: 501-505.
17. Carrington M., Allsop B., Baylis H., Malu N-M., Shochat Y. & Sohal S. 1995. Lymphoproliferation caused by Theileria parva and Theileria annulata. In: Molecular Approaches to Parasitology. MBL Lectures in Biology, Vol. 12 (Edited by Boothroyd J. C. & Komuniecki R.), pp. 43-56. Wiley-Liss, New York.
18. 4]Bl-Cer) and cholesterol-3-sulfate and its dependence on disulfide bond formation between cysteines in region II. Molecular and Biochemical Parasitology 54: 1-12.
19. Cesbron-Delauw M. F. 1994. Dense granule organelles of Toxoplasma gondii: their role in the host parasite relationship. Parasitology Today 10: 293-296.
20. Clapham D. E. 1995. Calcium signaling. Cell 80: 259-268.
21. Dennis E. D., Mitchell G. H., Butcher G. A. & Cohen S. 1975. In vitro isolation of Plasmodium knowlesi merozoites using polycarbonate sieves. Parasitology 71: 475-481.
22. Dobbelaere D. A. E., Spooner P. R., Barry W. C. & Irvin A. D. 1984. Monoclonal antibody neutralises the sporozoite stage of different Theileria parva stocks. Parasitology Immunology 6: 361-370.
23. Dobbelaere D. A. E., Shapiro S. Z. & Webster P. 1985a. Identification of a surface antigen on Theileria parva sporozoites by monoclonal antibody. Proceedings of the National Academy of Sciences U.S.A. 82: 1771-1775.
24. Dobbelaere D. A. E., Webster P., Leitch B. L., Voight W. P. & Irvin A. D. 1985b. Theileria parva: expression of a sporozoite surface coat antigen. Experimental Parasitology 60: 90-100.
25. Dobrowolski J. M. & Sibley L., D. 1996. Toxoplasma invasion of mammalian cells is powered by the actin cytoskeleton of the parasite. Cell 84: 933-939.
26. 2+ in the process of cell invasion by intracellular parasites. Parasitology Today 12: 61-65.
27. Dolan T. T. 1989. Theileriasis: a comprehensive review. Revue Scientifique et Technique (Office International des Epizooties) 8: 11-36.
28. Doury J. C., Bonnefoy S., Roger N., Dubremetz J. F. & Mercereau-Puijalon O. 1994. Analysis of the high molecular weight rhoptry complex of Plasmodium falciparum using monoclonal antibodies. Parasitology 108: 269-280.
29. Dubremetz J. F., Achbarou A., Bermudes D. & Joiner K. A. 1993. Kinetics and pattern of organelle exocytosis during Toxoplasma gondii/host cell interaction. Parasitology Research 79: 402-408.
30. Eichhorn M. & Dobbelaere D. A. E. 1994. Induction of signal transduction pathways in lymphocytes infected by Theileria parva. Parasitology Today 10: 469-472.
31. Emery D. L., MacHugh N. D. & Morrison W. I. 1988. Theileria parva (Muguga) infects bovine T lymphocytes in vivo and induces co-expression of BoT4 and BoT8. Parasite Immunology 10: 379-391.
32. Entzeroth R. 1985. Invasion and early development of Sarcocystis muri (Apicomplexa, Sarcocystidae) in tissue cultures. Journal of Protozoology 32: 446-453.
33. Eriksson J. E., Brautigan D. L., Vallee R., Olmsted J., Fujiki H. & Goldman R. D. 1992. Cytoskeletal integrity in interphase cells requires protein phosphatase activity. Proceedings of the National Academy of Sciences U.S.A. 89: 11,093-11,097.
34. Etges R., Bouvier J. & Bordier C. 1989. The promastigote surface protease of Leishmania: pH optimum and effects of protease inhibitors. In: Leishmaniasis: The Current Status and New Strategies for Control (Edited by Hart D. T.), pp. 627-633. NATO ASI Series A. Life Sciences, Vol. 163. Plenum Publishing, New York.
35. Falkow S., Isberg R. R. & Portnoy D. A. 1992. The interaction of bacteria with mammalian cells. Annual Review of Cell Biology 8: 333-363.
36. Fawcett D. W., Musoke A. J. & Voight W. B. 1984. Interaction of sporozoites of Theileria parva with bovine lymphocytes in vitro. I. Early events after invasion. Tissue and Cell 16: 873-884.
37. Fawcett D. W., Young A. S. & Leitch B. L. 1985. Sporogony in Theileria (Apicomplexa: Piroplasmida). Journal of Submicroscopic Cytology 17: 299-314.
38. Fawcett D. W., Doxsey S., Stagg D. A. & Young A. S. 1982. The entry of sporozoites of Theileria parva into bovine lymphocytes in vitro. Electron microscopic observations. European Journal of Cell Biology 27: 10-21.
39. Fernandez M. A., Munoz-Fernandez M. A. & Fresno M. 1993. Involvement of β-1-integrins in the binding and entry of Trypanosoma cruzi into human macrophages. European Journal of Immunology 23: 552-557.
40. Frevert U., Sinnis P., Esko J. D. & Nussenzweig V. 1996. Cell surface glycosaminoglycans are not obligatory for Plasmodium falciparum sporozoite invasion in vitro. Molecular and Biochemical Parasitology 76: 257-266.
41. Galinski M. R. & Barnwell J. W. 1996. Plasmodium vivax: merozoites, invasion of reticulocytes and considerations for malaria vaccine development. Parasitology Today 12: 20-29.
42. Garcia-del Portillo F. & Finlay B. B. 1995. The varied life styles of intracellular pathogens within eukaryotic vacuolar compartments. Trends in Microbiology 3: 373-380.
43. Glass E. J., Innes E. A., Spooner R. L. & Brown C. G. D. 1989. Infection of bovine monocyte, macrophage populations with Theileria annulata and Theileria parva. Veterinary Immunology and Immunopathology 22: 355-368.
44. Hall R. 1994. Molecular mimicry. Advances in Parasitology 34: 81-132.
45. Hall R., Hunt P. D., Carrington M., Simmons D., Williamson S., Mecham R. P. & Tait A. 1992. Mimicry of elastin repetitive motifs by Theileria annulata sporozoite surface antigen. Molecular and Biochemical Parasitology 53: 105-112.
46. Haywood A. M. 1994. Virus receptors: binding, adhesion strengthening, and changes in viral structure. Journal of Virology 68: 1-5.
47. Heldin C.-H. 1995. Dimerization of cell surface receptors in signal transduction. Cell 80: 213-223.
48. Hemphill A., Gottstein B. & Kaufmann H. 1996. Adhesion and invasion of bovine endothelial cells by Neospora caninum. Parasitology 112: 183-197.
49. Holder A. A. 1994. Proteins on the surface of the malaria parasite and cell invasion. Parasitology 108: S5-S18.
50. Iams K. P., Young J. R., Nene V., Desai J., Webster P., Ole MoiYoi O. K. & Musoke A. J. 1990. Characterisation of the gene encoding a 104-kilodalton microneme-rhoptry protein of Theileria parva. Molecular and Biochemical Parasitology 39: 47-60.
51. Irvin A. D. & Morrison W. I. 1987. Immunopathology. immunology and immunoprophylaxis of Theileria infections. In: Immune Responses in Parasitic Infections: Immunology. Immunopathology and Immunoprophylaxis (Edited by Soulsby E. J. L.), pp. 223-274. CRC Press, Boca Raton.
52. Isberg R. R. & Tran Van Nhieu G. 1994. Binding and internalization of microorganisms by integrin receptors. Trends in Microbiology 2: 10-14.
53. Jarrett W. F. H., Crighton G. W. & Pirie H. W. 1969. Theileria parva: kinetics of replication. Experimental Parasitology 24: 9-25.
54. Johnson J. G., Epstein N., Shiroishi T. & Miller L. H. 1980. Factors affecting the ability of isolated Plasmodium knowlesi merozoites to attach to and invade erythrocytes. Parasitology 80: 539-550.
55. Jura W. G. Z. O. 1984. Factors affecting the capacity of Theileria annulata sporozoites to invade bovine peripheral blood lymphocytes. Veterinary Parasitology 16: 215-223.
56. Jura W. G. Z O., Brown C. G. D. & Kelly B. 1983. Fine structure and invasive behaviour of the early developmental stages of Theileria annulata in vitro. Veterinary Parasitology 12: 31-44.
57. Katzer F., Carrington M., Knight P., Williamson S., Tait A., Morrison W. I. & Hall R. 1994. Polymorphism of SPAG-1, a candidate antigen for inclusion in a sub-unit vaccine against Theileria annulata. Molecular and Biochemical Parasitology 67: 1-10.
58. King C. A. 1988. Cell motility of sporozoan parasites. Parasitology Today 4: 315-319.
59. Knight P., Musoke A. J., Gachanja J. N., Nene V., Katzer F., Boulter N., Hall R., Brown C. G. D., Williamson S., Kirvar E., Bell-Sakyi L., Hussain K. & Tait A. 1996. Conservation of neutralizing determinants between the sporozoite surface antigens of Theileria annulata and Theileria parva. Experimental Parasitology 82: 229-241.
60. Lawrence M. B. & Springer T. A. 1991. Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through intregrins. Cell 65: 859-873.
61. Matsumoto Y., Perry G., Scheibel L. W. & Aikawa M. 1987. Role of calmodulin in Plasmodium falciparum: implications for erythrocyte invasion by the merozoite. European Journal of Cell Biology 45: 36-43.
62. McCallum-Deighton N. & Holder A. A. 1992. The role of calcium in the invasion of human erythrocytes by Plasmodium falciparum. Molecular and Biochemical Parasitology 50: 317-324.
63. Menard R., Dehio C. & Sansonetti P. J. 1996. Bacterial entry into epithelial cells: the paradigm of Shigella. Trends in Microbiology 4: 220-226.
64. Michel R., Schupp K., Raether W. & Berther F. W. 1980. Formation of a close junction during invasion of erythrocytes by Toxoplasma gondii in vitro. International Journal for Parasitology 10: 309-313.
65. Miller L. H., Aikawa M., Johnson J. G. & Shiroishi T. 1979. Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Journal of Experimental Medicine 149: 172-184.
66. Mitchell G. H. & Bannister L. H. 1988. Malaria parasite invasion: interactions with the red cell membrane. CRC Critical Reriews in Oncology and Hematology 8: 255-310.
67. 2+-dependence of conoid extrusion in Toxoplasma gondii tachyzoites. Journal of Eukaryotic Microbiology 43: 120-127.
68. Mondragon R., Meza I. & Frixione E. 1994. Divalent cation and ATP dependent motility of Toxoplasma gondii tachyzoites after mild treatment with trypsin. Journal of Eukaryotic Microbiology 41: 330-337.
69. Morisaki J. H., Heuser J. E. & Sibley L. D. 1995. Invasion of Toxoplasma gondii occurs by active penetration of the host cell. Journal of Cell Science 108: 2457-2464.
70. Morrison W. I., MacHugh N. D. & Lalor P. A. 1996. Pathogenicity of Theileria parva is influenced by the host cell type infected by the parasite. Infection and Immunity 64: 557-562.
71. Moulder J. W. 1985. Comparative biology of intracellular parasitism. Microbiology Reviews 49: 298-337.
72. Mueller D. L., Jenkins M. K. & Schwartz R. H. 1989. Clonal expansion versus functional clonal inactivation: a costimulatory signalling pathway determines the outcome of T cell antigen receptor occupancy. Annual Review of Immunology 7: 445-480.
73. Mukhebi A. W., Perry B. D. & Kruska R. 1992. Estimated economics of theileriosis control in Africa. Preventive Veterinary Mediane 12: 73-85.
74. Musoke A. J., Nene V. & Morzaria S. P. 1993. A sporozoite-based vaccine for Theileria parva. Parasitology Today 9: 385-388.
75. Musoke A. J., Nantuyla V. M., Rurangirwa F. R. & Buscher G. 1984. Evidence for a common protective antigenic determinant on sporozoites of several Theileria parva strains. Immunology 52: 231-238.
76. Musoke A. J., Nantulya V. M., Buscher G., Masake R. A. & Otim B. 1982. Bovine immune response to Theileria parva: neutralizing antibodies to sporozoites. Immunology 45: 663-668.
77. Nagai Y. 1993. Protease-dependent virus tropism and pathogenicity. Trends in Microbiology 1: 81-87.
78. Nene V., Iams K. P., Gobright E. & Musoke A. J. 1992. Characterization of the gene encoding a candidate vaccine antigen of Theileria parva sporozoites. Molecular and Biochemical Parasitology 51: 17-28.
79. Nene V., Musoke A., Gobright E. & Morzana S. 1996. Conservation of the sporozoite p67 vaccine antigen in cattle-derived Theileria parva stocks with different cross-immunity profiles. Infection and Immunity 64: 2056-2061.
80. Norval R. A. I., Perry B. D. & Young A. S. 1992. The Epidemiology of Theileriosis in Africa. Academic Press, London.
81. Ole MoiYoi O. K. 1989. Theileria parva: an intracellular protozoan parasite that induces reversible lymphocyte transformation. Experimental Parasitology 69: 204-210.
82. 2+. Parasitology Today 12: 145-150.
83. Perkins M. E. 1992. Rhoptry organelles of Apicomplexan parasites. Parasitology Today 8: 28-32.
84. Rosenshine I. & Finlay B. B. 1993. Exploitation of host signal transduction pathways and cytoskeletal functions by invasive bacteria. BioEssays 15: 17-24.
85. Rosenshine I., Ruschkowski S., Foubister V. & Finlay B. B. 1994. Salmonella typhimurium invasion of epithelial cells: role of induced host cell tyrosine protein phosphorylation. Injection and Immunity 62: 4969-4974.
86. Russell D. G. 1994. Strategies for intracellular survival of microbes. Baillière's Clinical Infectious Diseases 1: 155-384.
87. Russell D. G. & Sinden R. E. 1981. The role of the cytoskeleton in the motility of coccidian sporozoites. Journal of Cell Science 50: 345-359.
88. Saffer L. D., Mercereau-Puijalon O., Dubremetz J. F. & Schwartzman J. D. 1992. Localization of a Taxoplasma gondii rhoptry protein by immunoelectron microscopy during and after host cell penetration. Journal of Protozoology 39: 526-530.
89. Sam-Yellowe T. Y. 1996. Rhoptry organelles of the Apicomplexa: their role in host cell invasion and intracellular survival. Parasitology Today 12: 308-316.
90. Sanders M. C. & Theriot J. A. 1996. Tails from the hall of infection: actin-based motility of pathogens. Trends in Microbiology 4: 211-213.
91. Scheibel L. W., Colombani P. M., Hess A. D., Aikawa M., Atkinson C. T. & Milhous W. K. 1987. Calcium and calmodulin antagonists inhibit human malaria parasites (Plasmodium falciparum): implications for drug design. Proceedings of the National Academy of Sciences U.S.A. 84: 7310-7314.
92. 2+ is essential for Theileria parva sporozoite invasion of bovine lymphocytes. European Journal of Cell Biology 68: 78-87.
93. Shaw M. K. 1996a. Characterization of the parasite host cell interactions involved in Theileria parva sporozoite invasion of bovine lymphocytes. Parasitology 113: 267-277.
94. Shaw M. K. 1996b. Theileria parva sporozoite entry into bovine lymphocytes involves both parasite and host cell signal transduction processes. Experimental Parasitology 84: 344-354.
95. Shaw M. K. & Tilney L. G. 1992. How individual cells develop from a syncytium: merogony in Theileria parva (Apicomplexa). Journal of Cell Science 101: 109-123.
96. Shaw M. K. & Tilney L. G. 1995. The entry of Theileria parva merozoites into bovine erythrocytes occurs by a process similar to sporozoite invasion of lymphocytes. Parasitology 111: 455-461.
97. Shaw M. K. & Young A. S. 1994. The biology of Theileria species in Ixodid ticks in relation to parasite transmission. Advances in Disease Vector Research 10: 23-63.
98. Shaw M. K. & Young A. S. 1995. Differential development and emission of Theileria parva sporozoites from the salivary gland of Rhipicephalus appendiculatus. Parasitology 111: 153-160.
99. Shaw M. K., Tilney L. G. & McKeever D. J. 1993. Tick salivary gland extract and interleukin-2 stimulation enhances susceptibility of lymphocytes to infection by Theileria parva sporozoites. Infection and Immunity 61: 1486-1495.
100. Shaw M. K., Tilney L. G. & Musoke A. J. 1991. The entry of Theileria parva sporozoites into bovine lymphocytes: evidence for MHC class I involvement. Journal of Cell Biology 113: 87-101.
101. Shaw M. K., Tilney L. G., Musoke A. J. & Teale A. J. 1995. MHC class I molecules are an essential cell surface component involved in Theileria parva sporozoite binding to bovine lymphocytes. Journal of Cell Science 108: 1587-1596.
102. Sibley L. D. 1995. Invasion of vertebrate cells by Toxoplasma gondii. Trends in Cell Biology 5: 129-132.
103. Sonnenshine D. E. 1993. Biology of Ticks, Vol. 2. Oxford University Press, Oxford.
104. Speer C. A., Tilley M., Temple M. E., Blixt J. A., Dubey J. P. & White M. W. 1995. Sporozoites of Toxoplasma gondii lack dense-granule protein GRA3 and form a unique parasitophorous vacuole. Molecular and Biochemical Parasitology 75: 75-86.
105. Spooner R. L., Innes E. A., Glass E. J. & Brown C. G. D. 1989. Theileria annulata and T. parva infect and transform different bovine mononuclear cells. Immunology 66: 284-288.
106. Stagg D. A., Dolan T. T., Latch B. L. & Young A. S. 1981. The initial stage of infection of cattle cells with Theileria parva sporozoites in vitro. Parasitology 83: 191-197.
107. Stagg D. A., Fawcett D. W., Young A. S. & Leitch B. L. 1984. Superinfection of established Theileria-infected bovid cell lines with Theileria parva sporozoites. Annals of Tropical Medicine and Parasitology 78: 335-337.
108. Stagg D. A., Young A. S., Leitch B. L., Grootenhuis J. G. & Dolan T. T. 1983. Infection of mammalian cells with Theileria parva. Parasitology 86: 243-254.
109. Stewart M. J. & Vanderberg J. P. 1991. Malaria sporozoites release circumsporozoite protein from their apical end and translocate it along their surface. Journal of Protozoology 38: 411-421.
110. Tilney L. G., Tilney M. S. & Shaw M. K. 1994. Theileria: strategy of infection and survival. Baillière's Clinical Infectious Diseases 1: 335-350.
111. Toye P. G., Goddeeris B. M., Iams K., Musoke A. J. & Morrison W. I. 1991. Characterization of a polymorphic immunodominant molecule in sporozoites and schizonts of Theileria parva. Parasite Immunology 13: 49-62.
112. Toye P. G., Metzelaar M. J., Wijngaard P. L., Nene V., Iams K., Roose J., Nyanjui J. K., Gobright E., Musoke A. J. & Clevers H. C. 1995. Characterization of the gene encoding the polymorphic immunodominant molecule, a neutralizing antigen of Theileria parva. Journal of Immunology 155: 1370-1381.
113. Ward G. E., Chitnis C. E. & Miller L. H. 1994a. The invasion of erythrocytes by malarial merozoites. Baillière's Clinical Infectious Diseases 1: 155-190.
114. Ward G. E., Fujioka H., Aikawa M. & Miller L. H. 1994b. Staurosporine inhibits invasion of erythrocytes by malarial merozoites. Experimental Parasitology 79: 480-487.
115. 2+ depletion on asexual cell cycle of Plasmodium falciparum. American Journal of Tropical Medicine and Hygiene 31: 711-717.
116. Wasserman M., Vernot J. P. & Mendoza P. 1990. Role of calcium and erythrocyte cytoskeleton phosphorylation in the invasion of Plasmodium falciparum. Parasitology Research 16: 681-688.
117. Webster P., Dobbelaere D. A. E. & Fawcett D. W. 1985. The entry of sporozoites of Theileria parva into bovine lymphocytes in vitro: immunoelectron microscopic observations. European Journal of Cell Biology 36: 157-162.
118. Weiss A. & Littman D. R. 1994. Signal transduction by lymphocyte antigen receptors. Cell 76: 263-274.
119. Williamson S., Tait A., Brown D., Walker A., Beck P., Shiels B., Fletcher J. & Hall R. 1989. Theileria annulata sporozoite surface antigen expressed in Escherichia coli elicits neutralizing antibody. Proceedings of the National Academy of Sciences U.S.A. 86: 4639-4643.
120. Yayon A., Klagsbrun M., Esko J. D., Leder P. & Ornitz D. M. 1991. Cell surface, heparin-like molecules are required for binding of basic fibroblast-growth factor to its high affinity receptor. Cell 64: 841-848.