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. 1981 Sep 15;198(3):467–473. doi: 10.1042/bj1980467

Properties of a series of tegumental membrane-bound phosphohydrolase activities of Schistosoma mansoni.

I M Cesari, A J Simpson, W H Evans
PMCID: PMC1163290  PMID: 6275849

Abstract

1. Incubation of Schistosoma mansoni for 5 min in a phosphate-buffered medium, pH 7.4, released tegumental material containing the following phosphohydrolase activities: alkaline phosphatase, 5'-nucleotidase, glycerol-2-phosphatase, glucose 6-phosphatase, phosphodiesterase and ATPase. 2. Maximum activity of these enzymes was measured at pH 9.5; however, the phosphodiesterase and ATPase activities were also appreciable at pH 7.0. 3. Solubilization of the released tegumental material in 1% Triton X-100 followed by gel filtration distinguished three peaks of enzyme activity: an ATPase (mol.wt. greater than 1000 000), a phosphodiesterase (mol.wt. 1 000 000) and an alkaline phosphomonoesterase with broad specificity (mol.wt. 232 000). 4. The ATPase activity was highly activated by 10 mM-Mg2+ or 1 mM-Ca2+ and was inhibited by chelating agents. Ouabain, Na+ and K+ had little effect on enzyme activity, whereas activity was increased by 50% in the presence of calmodulin. The phosphodiesterase activity was highest in the presence of 100 mM-Na+ or -K+, and 10 mM-Mg2+ or -Ca2+. Alkaline phosphatase activity was also stimulated by 100 mM-Na+ or -K+, and 10 mM-Mg2+; however Ca2+ inhibited at greater than 1 mM. 5. Surface iodination of parasites followed by detergent solubilization and gel filtration of the released tegumental membranes indicated that these enzymes were not accessible. A major surface component, apparent mol.wt. 80 000, was iodinated. 6. Rabbit anti-(mouse liver 5'-nucleotidase) antibodies did not inhibit the phosphohydrolase activities. However, an immunoglobulin G fraction from sera of mice chronically infected with S. mansoni partially inhibited alkaline phosphatase activity, but was without effect on the phosphodiesterase and ATPase activities. 7. The location of the enzymes in the double membrane of the tegument and their significance in host-parasite interactions is discussed.

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Selected References

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  1. Asch H. L., Read C. P. Transtegumental absorption of amino acids by male Schistosoma mansoni. J Parasitol. 1975 Apr;61(2):378–379. [PubMed] [Google Scholar]
  2. Avruch J., Wallach D. F. Preparation and properties of plasma membrane and endoplasmic reticulum fragments from isolated rat fat cells. Biochim Biophys Acta. 1971 Apr 13;233(2):334–347. doi: 10.1016/0005-2736(71)90331-2. [DOI] [PubMed] [Google Scholar]
  3. Bogitsh B. J., Krupa P. L. Schistosoma mansoni and Haematoloechus medioplexus: nuclosidediphosphatase localization in tegument. Exp Parasitol. 1971 Dec;30(3):418–425. doi: 10.1016/0014-4894(71)90106-8. [DOI] [PubMed] [Google Scholar]
  4. Bolton A. E., Hunter W. M. The labelling of proteins to high specific radioactivities by conjugation to a 125I-containing acylating agent. Biochem J. 1973 Jul;133(3):529–539. doi: 10.1042/bj1330529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carson S. D. Ammonium molybdate-stannous chloride determination of orthophosphate in the presence of Triton X-100. Anal Biochem. 1976 Oct;75(2):472–477. doi: 10.1016/0003-2697(76)90102-0. [DOI] [PubMed] [Google Scholar]
  6. Cesari I. M. Schistosoma mansoni: distribution and characteristics of alkaline and acid phosphatase. Exp Parasitol. 1974 Dec;36(3):405–414. doi: 10.1016/0014-4894(74)90080-0. [DOI] [PubMed] [Google Scholar]
  7. Fetterer R. H., Pax R. A., Bennett J. L., Bennett J. L. Na+-K+ transport, motility and tegumental membrane potential in adult male Schistosoma mansoni. Parasitology. 1981 Feb;82(1):97–109. doi: 10.1017/s0031182000041895. [DOI] [PubMed] [Google Scholar]
  8. Fetterer R. H., Pax R. A., Bennett J. L. Schistosoma mansoni: characterization of the electrical potential from the tegument of adult males. Exp Parasitol. 1980 Jun;49(3):353–365. doi: 10.1016/0014-4894(80)90071-5. [DOI] [PubMed] [Google Scholar]
  9. Ghijsen W. E., van Os C. H. Ca-stimulated ATPase in brush border and basolateral membranes of rat duodenum with high affinity sites for Ca ions. Nature. 1979 Jun 28;279(5716):802–803. doi: 10.1038/279802a0. [DOI] [PubMed] [Google Scholar]
  10. Grand R. J., Perry S. V., Weeks R. A. Troponin C-like proteins (calmodulins) from mammalian smooth muscle and other tissues. Biochem J. 1979 Feb 1;177(2):521–529. doi: 10.1042/bj1770521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gurd J. W., Evans W. H. Distribution of liver plasma membrane 5' nucleotidase as indicated by its reaction with anti-plasma membrane serum. Arch Biochem Biophys. 1974 Sep;164(1):305–311. doi: 10.1016/0003-9861(74)90035-6. [DOI] [PubMed] [Google Scholar]
  12. Hayunga E. G., Murrell K. D., Taylor D. W., Vannier W. E. Isolation and characterization of surface antigens from Schistosoma mansoni. I. Evaluation of techniques for radioisotope labeling of surface proteins from adult worms. J Parasitol. 1979 Aug;65(4):488–496. [PubMed] [Google Scholar]
  13. Hockley D. J., McLaren D. J. Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. Int J Parasitol. 1973 Jan;3(1):13–25. doi: 10.1016/0020-7519(73)90004-0. [DOI] [PubMed] [Google Scholar]
  14. Kusel J. R. Protein composition and protein synthesis in the surface membranes of Schistosoma mansoni. Parasitology. 1972 Aug;65(1):55–69. doi: 10.1017/s0031182000044231. [DOI] [PubMed] [Google Scholar]
  15. Lane S. M., Lawson D. E. Differentiation of the changes in alkaline phosphatase from calcium ion-activated adenosine triphosphatase activities associated with increased calcium absorption in chick intestine. Biochem J. 1978 Sep 15;174(3):1067–1070. doi: 10.1042/bj1741067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Levy M. G., Read C. P. Relation of tegumentary phosphohydrolase to purine and pyrimidine transport in Schistosoma mansoni. J Parasitol. 1975 Aug;61(4):648–656. [PubMed] [Google Scholar]
  17. Moog F., Glazier H. S. Phosphate absorption and alkaline phosphatase activity in the small intestine of the adult mouse and of the chick embryo and hatched chick. Comp Biochem Physiol A Comp Physiol. 1972 Jun 1;42(2):321–336. doi: 10.1016/0300-9629(72)90113-2. [DOI] [PubMed] [Google Scholar]
  18. Morris G. P., Threadgold L. T. Ultrastructure of the tegument of adult Schistosoma mansoni. J Parasitol. 1968 Feb;54(1):15–27. [PubMed] [Google Scholar]
  19. Narayanan S., Appleton H. D. Specificity studies on human intestinal alkaline phosphatase. Biochim Biophys Acta. 1972 Sep 19;284(1):175–182. doi: 10.1016/0005-2744(72)90056-3. [DOI] [PubMed] [Google Scholar]
  20. Nechay B. R., Hillman G. R., Dotson M. J. Properties and drug sensitivity of adenosine triphosphatases from Schistosoma mansoni. J Parasitol. 1980 Aug;66(4):596–600. [PubMed] [Google Scholar]
  21. Rogers S. H., Bueding E. Anatomical localization of glucose uptake by Schistosoma mansoni adults. Int J Parasitol. 1975 Jun;5(3):369–371. doi: 10.1016/0020-7519(75)90086-7. [DOI] [PubMed] [Google Scholar]
  22. Shirazi S. P., Colston K. W., Butterworth P. J. Alkaline phosphatase: a possible transport protein for inorganic phosphate. Biochem Soc Trans. 1978;6(5):933–935. doi: 10.1042/bst0060933. [DOI] [PubMed] [Google Scholar]
  23. Simpson A. J., Schryer M. D., Cesari I. M., Evans W. H., Smithers S. R. Isolation and partial characterization of the tegumental outer membrane of adult Schistosoma mansoni. Parasitology. 1981 Aug;83(Pt 1):163–177. doi: 10.1017/s0031182000050137. [DOI] [PubMed] [Google Scholar]
  24. Skillen A. W., Rahbani-Nobar M. ATPase and alkaline phosphatase activities of chick and rat small intestinal mucosa. Biochim Biophys Acta. 1979 Nov 9;571(1):86–93. doi: 10.1016/0005-2744(79)90228-6. [DOI] [PubMed] [Google Scholar]
  25. Smithers S. R., Terry R. J. Naturally acquired resistance to experimental infections of Schistosoma mansoni in the rhesus monkey (Macaca mulatta). Parasitology. 1965 Nov;55(4):701–710. [PubMed] [Google Scholar]
  26. Snary D., Smith M. A., Clegg J. A. Surface proteins of Schistosoma mansoni and their expression during morphogenesis. Eur J Immunol. 1980 Jul;10(7):573–575. doi: 10.1002/eji.1830100716. [DOI] [PubMed] [Google Scholar]
  27. Wheater P. R., Wilson R. A. The tegument of Schistosoma mansoni: a histochemical investigation. Parasitology. 1976 Feb;72(1):99–109. doi: 10.1017/s0031182000043237. [DOI] [PubMed] [Google Scholar]

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