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. 1991 Apr 15;275(Pt 2):407–411. doi: 10.1042/bj2750407

The inositol phosphate/diacylglycerol signalling pathway in Trypanosoma cruzi.

R Docampo 1, O P Pignataro 1
PMCID: PMC1150068  PMID: 2025225

Abstract

Using [32P]Pi and [3H]inositol as precursors, we have detected the presence of phosphatidylinositol, phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate, and their derivatives inositol phosphate, inositol 1,4-bisphosphate and inositol 1,4,5-trisphosphate respectively, in Trypanosoma cruzi epimastigotes. Using digitonin-permeabilized cells it was possible to detect a stimulation in the formation of inositol 1,4,5-trisphosphate and inositol 1,4-bisphosphate as well as an increased generation of diacylglycerol in the presence of 1 mM-CaCl2. These results are consistent with the operation of a functional inositol phosphate/diacylglycerol pathway in T. cruzi, and constitute the first demonstration of the presence and activation of this pathway in a parasitic protozoan. These results also indicate that this pathway is conserved during evolution from lower to higher eukaryotic organisms.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Andrews N. W., Robbins E. S., Ley V., Hong K. S., Nussenzweig V. Developmentally regulated, phospholipase C-mediated release of the major surface glycoprotein of amastigotes of Trypanosoma cruzi. J Exp Med. 1988 Feb 1;167(2):300–314. doi: 10.1084/jem.167.2.300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ascoli M., Pignataro O. P., Segaloff D. L. The inositol phosphate/diacylglycerol pathway in MA-10 Leydig tumor cells. Activation by arginine vasopressin and lack of effect of epidermal growth factor and human choriogonadotropin. J Biol Chem. 1989 Apr 25;264(12):6674–6681. [PubMed] [Google Scholar]
  3. Berridge M. J. Inositol trisphosphate and diacylglycerol: two interacting second messengers. Annu Rev Biochem. 1987;56:159–193. doi: 10.1146/annurev.bi.56.070187.001111. [DOI] [PubMed] [Google Scholar]
  4. Blum J. J. An adrenergic control system in Tetrahymena. Proc Natl Acad Sci U S A. 1967 Jul;58(1):81–88. doi: 10.1073/pnas.58.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Coppens I., Opperdoes F. R., Courtoy P. J., Baudhuin P. Receptor-mediated endocytosis in the bloodstream form of Trypanosoma brucei. J Protozool. 1987 Nov;34(4):465–473. doi: 10.1111/j.1550-7408.1987.tb03216.x. [DOI] [PubMed] [Google Scholar]
  6. Cross G. A. Eukaryotic protein modification and membrane attachment via phosphatidylinositol. Cell. 1987 Jan 30;48(2):179–181. doi: 10.1016/0092-8674(87)90419-3. [DOI] [PubMed] [Google Scholar]
  7. De Boiso J. F., De Cazzulo B. F., Stoppani A. O. Asimilación de fosfato por el Trypanosoma cruzi. Rev Soc Argent Biol. 1968 Aug-Nov;44(5):112–123. [PubMed] [Google Scholar]
  8. Docampo R., Vercesi A. E. Ca2+ transport by coupled Trypanosoma cruzi mitochondria in situ. J Biol Chem. 1989 Jan 5;264(1):108–111. [PubMed] [Google Scholar]
  9. Docampo R., Vercesi A. E. Characteristics of Ca2+ transport by Trypanosoma cruzi mitochondria in situ. Arch Biochem Biophys. 1989 Jul;272(1):122–129. doi: 10.1016/0003-9861(89)90202-6. [DOI] [PubMed] [Google Scholar]
  10. Exton J. H. Signaling through phosphatidylcholine breakdown. J Biol Chem. 1990 Jan 5;265(1):1–4. [PubMed] [Google Scholar]
  11. Ferguson M. A., Williams A. F. Cell-surface anchoring of proteins via glycosyl-phosphatidylinositol structures. Annu Rev Biochem. 1988;57:285–320. doi: 10.1146/annurev.bi.57.070188.001441. [DOI] [PubMed] [Google Scholar]
  12. Gadelha F. R., Moreno S. N., De Souza W., Cruz F. S., Docampo R. The mitochondrion of Trypanosoma cruzi is a target of crystal violet toxicity. Mol Biochem Parasitol. 1989 May 1;34(2):117–126. doi: 10.1016/0166-6851(89)90003-0. [DOI] [PubMed] [Google Scholar]
  13. Goldman M. E., Gundersen R. E., Erickson C. K., Thompson G. A., Jr High performance liquid chromatographic analysis of catecholamines in growing and non-growing Tetrahymena pyriformis. Biochim Biophys Acta. 1981 Aug 17;676(2):221–225. doi: 10.1016/0304-4165(81)90190-2. [DOI] [PubMed] [Google Scholar]
  14. Gonzales-Perdomo M., Romero P., Goldenberg S. Cyclic AMP and adenylate cyclase activators stimulate Trypanosoma cruzi differentiation. Exp Parasitol. 1988 Aug;66(2):205–212. doi: 10.1016/0014-4894(88)90092-6. [DOI] [PubMed] [Google Scholar]
  15. Gómez M. L., Erijman L., Arauzo S., Torres H. N., Téllez-Iñn M. T. Protein kinase C in Trypanosoma cruzi epimastigote forms: partial purification and characterization. Mol Biochem Parasitol. 1989 Sep;36(2):101–108. doi: 10.1016/0166-6851(89)90182-5. [DOI] [PubMed] [Google Scholar]
  16. Hide G., Gray A., Harrison C. M., Tait A. Identification of an epidermal growth factor receptor homologue in trypanosomes. Mol Biochem Parasitol. 1989 Aug;36(1):51–59. doi: 10.1016/0166-6851(89)90199-0. [DOI] [PubMed] [Google Scholar]
  17. Irvine R. F., Letcher A. J., Heslop J. P., Berridge M. J. The inositol tris/tetrakisphosphate pathway--demonstration of Ins(1,4,5)P3 3-kinase activity in animal tissues. Nature. 1986 Apr 17;320(6063):631–634. doi: 10.1038/320631a0. [DOI] [PubMed] [Google Scholar]
  18. Janakidevi K., Dewey V. C., Kidder G. W. The biosynthesis of catecholamines in two genera of protozoa. J Biol Chem. 1966 Jun 10;241(11):2576–2578. [PubMed] [Google Scholar]
  19. Le Roith D., Shiloach J., Roth J., Lesniak M. A. Evolutionary origins of vertebrate hormones: substances similar to mammalian insulins are native to unicellular eukaryotes. Proc Natl Acad Sci U S A. 1980 Oct;77(10):6184–6188. doi: 10.1073/pnas.77.10.6184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Majerus P. W., Connolly T. M., Deckmyn H., Ross T. S., Bross T. E., Ishii H., Bansal V. S., Wilson D. B. The metabolism of phosphoinositide-derived messenger molecules. Science. 1986 Dec 19;234(4783):1519–1526. doi: 10.1126/science.3024320. [DOI] [PubMed] [Google Scholar]
  21. Martin T. F. Hormone-regulated phosphoinositide turnover in permeabilized cells and membranes. Methods Enzymol. 1987;141:111–126. doi: 10.1016/0076-6879(87)41060-4. [DOI] [PubMed] [Google Scholar]
  22. Martin T. F. Thyrotropin-releasing hormone rapidly activates the phosphodiester hydrolysis of polyphosphoinositides in GH3 pituitary cells. Evidence for the role of a polyphosphoinositide-specific phospholipase C in hormone action. J Biol Chem. 1983 Dec 25;258(24):14816–14822. [PubMed] [Google Scholar]
  23. Maruo T., Cohen H., Segal S. J., Koide S. S. Production of choriogonadotropin-like factor by a microorganism. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6622–6626. doi: 10.1073/pnas.76.12.6622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McGowan K., Kane A., Asarkof N., Wicks J., Guerina V., Kellum J., Baron S., Gintzler A. R., Donowitz M. Entamoeba histolytica causes intestinal secretion: role of serotonin. Science. 1983 Aug 19;221(4612):762–764. doi: 10.1126/science.6308760. [DOI] [PubMed] [Google Scholar]
  25. Nandini-Kishore S. G., Thompson G. A., Jr Increased levels of adenosine 3',5'-cyclic monophosphate in Tetrahymena stimulated by glucose and mediated by Ca2+ and epinephrine. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2708–2711. doi: 10.1073/pnas.76.6.2708. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nishizuka Y. Studies and perspectives of protein kinase C. Science. 1986 Jul 18;233(4761):305–312. doi: 10.1126/science.3014651. [DOI] [PubMed] [Google Scholar]
  27. Oliveira M. M., Antunes A., De Mello F. G. Growth of Trypanosoma cruzi epimastigotes controlled by shifts in cyclic AMP mediated by adrenergic ligands. Mol Biochem Parasitol. 1984 Apr;11:283–292. doi: 10.1016/0166-6851(84)90072-0. [DOI] [PubMed] [Google Scholar]
  28. Palmer F. B. Lipids of Crithidia fasciculata. The occurrence and turnover of phosphoinositides. Biochim Biophys Acta. 1973 Sep 25;316(3):296–304. [PubMed] [Google Scholar]
  29. Pan J. X., Mikkelsen R. B., Wallach D. F., Asher C. R. Synthesis of a somatostatin-like peptide by Plasmodium falciparum. Mol Biochem Parasitol. 1987 Aug;25(1):107–111. doi: 10.1016/0166-6851(87)90023-5. [DOI] [PubMed] [Google Scholar]
  30. Pignataro O. P., Ascoli M. Epidermal growth factor increases the labeling of phosphatidylinositol 3,4-bisphosphate in MA-10 Leydig tumor cells. J Biol Chem. 1990 Jan 25;265(3):1718–1723. [PubMed] [Google Scholar]
  31. Pignataro O. P., Ascoli M. Studies with insulin and insulin-like growth factor-I show that the increased labeling of phosphatidylinositol-3,4-bisphosphate is not sufficient to elicit the diverse actions of epidermal growth factor on MA-10 Leydig tumor cells. Mol Endocrinol. 1990 May;4(5):758–765. doi: 10.1210/mend-4-5-758. [DOI] [PubMed] [Google Scholar]
  32. Rangel-Aldao R., Triana F., Fernández V., Comach G., Abate T., Montoreano R. Cyclic AMP as an inducer of the cell differentiation of Trypanosoma cruzi. Biochem Int. 1988 Aug;17(2):337–344. [PubMed] [Google Scholar]
  33. Renard D., Poggioli J., Berthon B., Claret M. How far does phospholipase C activity depend on the cell calcium concentration? A study in intact cells. Biochem J. 1987 Apr 15;243(2):391–398. doi: 10.1042/bj2430391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Roth J., LeRoith D., Shiloach J., Rosenzweig J. L., Lesniak M. A., Havrankova J. The evolutionary origins of hormones, neurotransmitters, and other extracellular chemical messengers: implications for mammalian biology. N Engl J Med. 1982 Mar 4;306(9):523–527. doi: 10.1056/NEJM198203043060907. [DOI] [PubMed] [Google Scholar]
  35. Schenkman S., Yoshida N., Cardoso de Almeida M. L. Glycophosphatidylinositol-anchored proteins in metacyclic trypomastigotes of Trypanosoma cruzi. Mol Biochem Parasitol. 1988 Jun;29(2-3):141–151. doi: 10.1016/0166-6851(88)90069-2. [DOI] [PubMed] [Google Scholar]
  36. Strickler J. E., Patton C. L. Adenosine 3',5'-monophosphate in reproducing and differentiated trypanosomes. Science. 1975 Dec 12;190(4219):1110–1112. doi: 10.1126/science.171773. [DOI] [PubMed] [Google Scholar]
  37. Trager W., Gill G. S. Plasmodium falciparum gametocyte formation in vitro: its stimulation by phorbol diesters and by 8-bromo cyclic adenosine monophosphate. J Protozool. 1989 Sep-Oct;36(5):451–454. doi: 10.1111/j.1550-7408.1989.tb01079.x. [DOI] [PubMed] [Google Scholar]
  38. Volpe P., Krause K. H., Hashimoto S., Zorzato F., Pozzan T., Meldolesi J., Lew D. P. "Calciosome," a cytoplasmic organelle: the inositol 1,4,5-trisphosphate-sensitive Ca2+ store of nonmuscle cells? Proc Natl Acad Sci U S A. 1988 Feb;85(4):1091–1095. doi: 10.1073/pnas.85.4.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. WARREN L. G. Metabolism of Schizotrypanum cruzi Chagas. I. Effect of culture age and substrate concentration on respiratory rate. J Parasitol. 1960 Oct;46:529–539. [PubMed] [Google Scholar]
  40. Walter R. D., Buse E., Ebert F. Effect of cyclic AMP on transformation and proliferation of leishmania cells. Tropenmed Parasitol. 1978 Dec;29(4):439–442. [PubMed] [Google Scholar]
  41. Weikel C. S., Murphy C. F., Orozco E., Ravdin J. I. Phorbol esters specifically enhance the cytolytic activity of Entamoeba histolytica. Infect Immun. 1988 Jun;56(6):1485–1491. doi: 10.1128/iai.56.6.1485-1491.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

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