A new intracellular pathway of haem detoxification in the midgut of the cattle tick Boophilus microplus: Aggregation inside a specialized organelle, the hemosome

Journal of Experimental Biology

Volumn 206, Issue 10, 2003, Pages 1707-1715

  Lara, Flavio Alves ^a   Lins, Ulysses ^a   Paiva Silva, Gabriela ^a   Almeida, Igor C ^b   Braga, Cláudia M ^c   Miguens, Flávio C ^d   Oliveira, Pedro L ^a   Dansa Petretski, Marílvia ^d  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c PETROBRAS   (Brazil)

^d NONE

Author keywords

Boophilus microplus; Cattle tick; Haem; Haemozoin; Tick

Indexed keywords

HEME;

ANIMAL; ARTICLE; BLOOD; CATTLE; CELL ORGANELLE; DIGESTION; DIGESTIVE SYSTEM; ELECTRON MICROSCOPY; FEMALE; HOST PARASITE INTERACTION; METABOLISM; PATHOGENICITY; TICK; ULTRASTRUCTURE;

ANIMALS; BLOOD; CATTLE; DIGESTION; DIGESTIVE SYSTEM; FEMALE; HEME; HOST-PARASITE RELATIONS; IXODIDAE; MICROSCOPY, ELECTRON; ORGANELLES;

ACARI; ANIMALIA; ARTHROPODA; BOOPHILUS MICROPLUS; BOS TAURUS; IXODIDAE;

EID: 0037506077     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.00334     Document Type: Article

References (29)

1. Aft, R. L. and Muller, G. C. (1983). Haem-mediated DNA strand scission. J. Biol. Chem. 258, 12069-12072.
2. Agbede, R. I. S. and Kemp, D. H. (1985). Digestion in the cattle tick Boophilus microplus: light microscope study on the gut cells in nymphs and females. Int. J. Parasitol. 16, 35-41.
3. Agyei, A. D. and Runham, N. W. (1995). Studies on the morphological changes in the midguts of two ixodid tick species Boophilus microplus and Rhipicephalus appendiculatus during digestion of the blood meal. Int. J. Parasitol. 25, 56-62.
4. Braz, G. R. C., Coelho, H. S. L., Masuda, H. and Oliveira, P. L. (1999). A missing metabolic pathway in the cattle tick Boophilus microplus. Curr. Biol. 9, 703-706.
5. Braz, G. R. C., Moreira, M. F., Masuda, H. and Oliveira, P. L. (2002). Rhodnius baem-binding protein (RHBP) is a haem source for embryonic development in the blood-sucking bug Rhodnius prolixus (Hemiptera, Reduviidae). Insect Biochem. Mol. Biol. 32, 361-367.
6. Falk, J. E. (1964). Porphyrins and metalloporphyrins. Their general, physical and coordination chemistry, and laboratory methods. London: Elsevier Publishing Company.
7. Glauert, A. M. (1974). The high voltage electron microscope in biology. J. Cell Biol. 63, 717-748.
8. Goldberg, D. E., Slater, A. F., Cerami, A. and Henderson, G. B. (1990). Haemoglobin degradation in the malaria parasite Plasmodium falciparum: an ordered process in a unique organelle. Proc. Natl. Acad. Sci. USA 87, 2931-2935.
9. Gough, J. M. and Kemp, D. H. (1995). Acid phosphatase in midgut digestive cells in partially fed females of the cattle tick Boophilus microplus. J. Parasitol. 81, 341-349.
10. Graham, R. C., Jr and Karnovsky, M. J. (1966). The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J. Hist. Cytochem. 14, 291-302.
11. Gudderra, N. P., Sonenshine, D. E., Apperson, C. S. and Roe, R. M. (2002). Hemolymph proteins in ticks. J. Insect Physiol. 48, 269-278.
12. Logullo, C., Moraes, J., Dansa-Petretski, M., Vaz, I. S., Masuda, A., Sorgine, M. H. F., Braz, G. R., Masuda, H. and Oliveira, P. L. (2002). Binding and storage of haem by vitellin from the cattle tick, Boophilus microplus. Insect Biochem. Mol. Biol. 32, 1805-1811.
13. Maya-Monteiro, C. M., Daffre, S., Logullo, C., Lara, F. A., Alves, E. W., Capurro, M. L., Zingali, R., Almeida, I. C. and Oliveira, P. L. (2000). HeLp, a haem lipoprotein from the haemolymph of the cattle tick, Boophilus microplus. J. Biol. Chem. 275, 36584-36589.
14. Mendiola, J., Alonso, M., Marquetti, M. C. and Finlay, C. (1996). Boophilus microplus: multiple proteolitic activities in the midgut. Exp. Parasitol. 82, 27-33.
15. O'Hagan, J. E. (1974). Boophilus microplus: digestion of hemoglobin by the engorged female tick. Exp. Parasitol. 35, 110-118.
16. Oliveira, M. F., d' Ávila, J. C. P., Torres, C. R., Braga, C. M. S., Tempone, A. J., Rumjanek, F. D., Silva, J. R., Dansa-Petretski, M., Oliveira, M. A., Souza, W., Oliveira, P. L. and Ferreira, S. T. (2000). Haemozoin in Schistosoma mansoni. Mol. Biochem. Parasitol. 111, 217-221.
17. Oliveira, M. F., Silva, J. R., Dansa-Petretski, M., Souza, W., Lins, U., Braga, C. M. S., Masuda, H. and Oliveira, P. L. (1999). Haem detoxification by insect. Nature 400, 517-518.
18. Pagola, S., Stephens, P. W., Bohle, D. S., Kosar, A. D. and Madsen, S. K. (2000). The structure of malaria pigment beta-haematin. Nature 404, 307-310.
19. Ponka, P. (1997). Tissue-specific regulation of iron metabolism and haem synthesis: distinct control mechanisms in erythroid cells. Blood 89, 1-25.
20. Rosell, R. and Coons, L. B. (1991). Purification and partial characterization of vitellin from the eggs of the hard tick Dermacentor variabilis. Insect Biochem. 21, 871-885.
21. Ryter, S. W. and Tyrrell, R. M. (2000). The haem synthesis and degradation pathways: role in oxidant sensitivity; Haem oxygenase has both pro- and antioxidant properties. Free Rad. Biol. Med. 15, 289-309.
22. Sappington, T. W. and Raikhel, A. S. (1998). Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochem. Mol. Biol. 28, 277-300.
23. Schmitt, T. H., Frezzatti, W. A. and Schreier, S. (1993). Heroin-induced lipid membrane disorder and increased permeability: a molecular model for the mechanism of cell lysis. Arch. Biochem. Biophys. 307, 96-103.
24. Slater, A. F., Swiggard, W. J., Orton, B. R., Flitter, W. D., Goldberg, D. E., Cerami, A. and Henderson, G. B. (1991). An iron carboxylate bond links the haem units of malaria pigment. Proc. Natl. Acad. Sci. USA 88, 325-329.
25. Tarnowski, B. I. and Coons, L. B. (1989). Ultrastructure of the midgut and blood meal digestion in the adult tick Dermacentor variabilis. Exp. Appl. Acarol. 6, 263-289.
26. Vincent, S. H., Grady, R. W., Shaklai, N., Snider, J. M. and Muller-Eberhard, U. (1988). The influence of haem-binding proteins in haem-catalyzed oxidations. Arch. Biochem. Biophys. 265, 539-550.
27. Walker, A. R. and Fletcher, J. D. (1987). Histology of digestion in nymphs of Rhipicephalus appendiculatus on rabbits and cattle naive and resistant to the ticks. Int. J. Parasitol. 17, 1393-1411.
28. Wandersman, C. and Stojiljkovic, I. (2000). Bacterial haem sources: the role of haem, haemoprotein receptors and haemophores. Curr. Opin. Microbiol. 3, 215-220.
29. White, D. C. and Granick, S. (1963). Hemin biosynthesis in Haemophilus. J Bacteriol. 85, 842-850.