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The anti-haemostatic strategies of the human hookworm Necator americanus

Published online by Cambridge University Press:  06 April 2009

B. A. Furmidge
Affiliation:
Department of Life Science, University of Nottingham, University Park, Nottingham NG7 2RD
L. A. Horn
Affiliation:
Department of Therapeutics, Queen's Medical Centre, Nottingham
D. I. Pritchard
Affiliation:
Department of Life Science, University of Nottingham, University Park, Nottingham NG7 2RD

Summary

The human hookworm Necator americanus appears to have evolved a number of complementary strategies to overcome the host's haemostatic processes. These include the inhibition of blood coagulation, platelet aggregation and mediator release, and the secretion of fibrinogenolytic enzymes. These strategies presumably allow the parasite to establish the chronic infections so often documented in human populations.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Blackburn, C. C. & Selkirk, M. E. (1992). Inactivation of platelet-activating factor by a putative acetylhydrolase from the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunology 75, 41–6.Google ScholarPubMed
Board, P. G. (1982). The use of fluorogenic peptide substrates for the detection of coagulation factors II and X after electrolysis. Annals of Human Genetics 46, 293–8.CrossRefGoogle Scholar
Brown, A. & Pritchard, D. I. (1993). The immunogenicity of hookworm (N. americanus) acetylcholinesterase in man. Parasite Immunology 15, 195203.Google Scholar
Capello, M., Clyne, L. P., McPhedran, P. & Hotez, P. J. (1993). Ancylostoma Factor Xa Inhibitor: partial purification and its identification as a major hookworm-derived anticoagulant in vitro. Journal of Infectious Diseases 167, 1474–7.CrossRefGoogle Scholar
Cappello, M., Vlasuk, G. P., Bergum, P. W., Huang, S. & Hotez, P. J. (1995). Ancylostoma caninum anticoagulant peptide, a hookworm-derived inhibitor of human coagulation factor Xa. Proceedings of the National Academy of Sciences, USA 92, 6152–6.CrossRefGoogle ScholarPubMed
Carroll, S. M., Howse, D. J. & Grove, D. I. (1984). The anticoagulant effects of hookworm, Ancylostoma ceylanicum: Observations in human and dog blood in vitro and infected dogs in vivo. Thrombosis and Haemostasis 51, 222–7.Google Scholar
Eiff, J. A. (1966). Nature of an anticoagulant from the cephalic glands of Ancylostoma caninum. Journal of Parasitology 52, 833–47.Google Scholar
Farrell, D. H., Thiagarajan, P., Chung, D. W. & Davie, E. W. (1992). Role of fibrinogen α and γ chain sites in platelet aggregation. Biochemistry 89, 10729–32.Google Scholar
Gartner, T. K. & Bennet, J. S. (1985). The tetrapeptide analogue of the cell attachment site of fibronectin inhibits platelet aggregation and fibrinogen binding to activated platelets. Journal of Biological Chemistry 260, 11891–4.CrossRefGoogle ScholarPubMed
Hotez, P. J. (1989). Hookworm disease in children. Pediatric Infectious Diseases Journal 8, 516–20.CrossRefGoogle ScholarPubMed
Hotez, P. I. & Cerami, A. (1983). Secretion of a proteolytic anticoagulant by Ancylostoma worms. Journal of Experimental Medicine 157, 1594–603.CrossRefGoogle Scholar
Hotez, P. J. & Pritchard, D. I. (1995). Hookworm infection. Scientific American 272, 42–8.Google Scholar
Hotez, P. J., Le Trang, N., McKerrow, J. H. & Cerami, A. (1985). Isolation and characterisation of a proteolytic enzyme from the adult hookworm Ancylostoma caninum. Journal of Biological Chemistry 260, 7343–8.CrossRefGoogle ScholarPubMed
Hynes, R. O. (1991). The complexity of platelet adhesion to extracellular matrices. Thrombosis and Haemostasis 66, 40–3.Google ScholarPubMed
Kalkofen, U. P. (1974). Intestinal trauma resulting from feeding activities of Ancylostoma caninum. American Journal of Tropical and Medical Hygiene 23, 1046–53.CrossRefGoogle ScholarPubMed
Lagarde, M., Byron, P. A., Guichardant, M. & Dechavanne, M. (1980). A simple and efficient method for platelet isolation from their plasma. Thrombosis Research 17, 381–8.CrossRefGoogle ScholarPubMed
Loeb, L. & Fleisher, M. S. (1910). The influence of extracts of Ancylostoma caninum on the coagulation of the blood haemolysis. Journal of Infectious Diseases 7, 625–31.CrossRefGoogle Scholar
Loeb, L. & Smith, A. J. (1904). The presence of a substance inhibiting the coagulation of the blood in Ancylostoma. Proceedings of the Pathological Society 7, 173–87.Google Scholar
Louden, K. A., Broughton, Pipkin F., Heptinstall, S., Fox, S. C., Mitchell, J. R. A. & Symonds, E. M. (1990). A longitudinal study of platelet behaviour and thromboxane production in whole blood in normal pregnancy and the puerpium. British Journal of Obstetrics and Gynaecology 97, 1108–14.CrossRefGoogle Scholar
Lowry, D., Rosebrough, N., Farr, A. & Randall, R. (1951). Protein measurement with the Folin-phenol reagent. Journal of Biological Chemistry 193, 265–75.Google Scholar
Malinconico, S. M., Katz, J. B. & Budzynski, A. Z. (1984). Fibrinogen degradation by hementin, a fibrinogenolytic anticoagulant from the salivary glands of the leech Haementeria ghilianii. Journal of Laboratory and Clinical Medicine 104, 842–54.Google ScholarPubMed
McEver, R. P., Bennet, E. M. & Martin, M. N. (1983). Identification of two structurally and functionally distinct sites on human platelet membrane glycoprotein IIb-IIIa using monoclonal antibodies. Journal of Biological Chemistry 258, 5269–75.CrossRefGoogle ScholarPubMed
Miletich, J. P., Jackson, C. M. & Majeru, P. W. (1977). Interaction of coagulation Factor Xa with human platelets. Proceedings of the National Academy of Sciences, USA 47, 4033–6.CrossRefGoogle Scholar
Morita, T., Kato, H., Iwanaga, S., Takada, K., Kimwa, T. & Sakakibara, S. (1977). New fluorogenic substrates for a-Thrombin, factor Xa, kallikreins and urokinase. Journal of Biochemistry 82, 1495–8.CrossRefGoogle Scholar
Moyle, M., Foster, D. L., McGarth, D. E., Brown, S. M., Laroche, Y., Demeutter, J., Stanssens, P., Bogowitz, C. A., Fried, V. A., Ely, J. A., Soule, H. R. & Vlasuk, G. P. (1994). A hookworm glycoprotein that inhibits neutrophil function is a ligand of the integrin CD 11b/CD 18. Journal of Biological Chemistry 269, 10008–15.CrossRefGoogle Scholar
Nachman, R. L. & Leung, R. L. (1982). Complex formation of platelet membrane glycoproteins IIb and IIIa with fibrinogen. Journal of Clinical Investigation 69, 263–9.CrossRefGoogle ScholarPubMed
Nurden, A. T. & Caen, J. P. (1974). An abnormal platelet glycoprotein pattern in three cases of Glanzmann's thrombastenia. British Journal of Haematology 28, 253–9.CrossRefGoogle Scholar
Savage, B., Marzec, U. M., Chao, B. H., Harker, L. A., Maraganore, J. M. & Ruggeri, Z. M. (1990). Binding of the snake venom-derived proteins applagin and echistatin to the arginine-glycine-aspartic acid recognition site(s) as platelet glycoprotein IIb/IIIa complex inhibits receptor function. Journal of Biochemistry 265, 11766–72.Google Scholar
Sawyer, R. (1991). Thrombolytics and anti-coagulants from leeches. Biotechnology 9, 513–14.Google ScholarPubMed
Shattil, S. J. (1993). Regulation of platelet anchorage and signalling by integrin αIIbβ3. Thrombosis and Haemostasis 70, 224–8.Google Scholar
Shattil, S. J., Hoxie, J. A., Cunningham, M. & Brass, L. F. (1985). Changes in the platelet membrane glycoprotein IIb/IIIa complex during platelet activation. Journal of Biological Chemistry 260, 11107–14.CrossRefGoogle ScholarPubMed
Spellman, G. G. & Nossell, H. L. (1971). Anticoagulant activity of dog hookworm. American Journal of Physiology 4, 922–7.Google Scholar
Steen, V. M. & Holmsen, H. (1987). Current aspects on human platelet activation and responses. European Journal of Haematology 38, 383–99.CrossRefGoogle ScholarPubMed
Thorson, R. E. (1955). Proteolytic activity in extracts of the oesophagus of adults of Ancylostoma caninum and the effect of immune serum on this activity. Journal of Parasitology 7, 2130.Google Scholar