Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1992 Nov;60(11):4475–4482. doi: 10.1128/iai.60.11.4475-4482.1992

A novel neutrophil-activating factor released by Trichomonas vaginalis.

M F Shaio 1, P R Lin 1, C S Lee 1, S C Hou 1, P Tang 1, K D Yang 1
PMCID: PMC258191  PMID: 1398962

Abstract

We have investigated the effects of a novel neutrophil-activating factor released by Trichomonas vaginalis (TV-NAF) on neutrophil chemotaxis. TV-NAF was present in the supernatant from 10(7) T. vaginalis (STV) cultured in 1 ml of serum-free Hanks' balanced salt solution (HBSS) at 37 degrees C for 30 min. With a multichamber chemotactic assay, we found that there were 112 +/- 15 migrated neutrophils (mean +/- standard deviation, n = 7) for STV and 11 +/- 4 for HBSS per high-power field (x 400). STV was also able to induce neutrophil actin assembly (increased 1.5-fold), enhance expression of complement receptor type 3 (increased 5-fold), and promote intracellular calcium mobilization (increased 2.5-fold). There was no chemotactic activity in the preparation of STV from killed trichomonads. The fact that heating up to 100 degrees C or deproteinization by treatment with proteinase K at 65 degrees C for 1 h did not abolish its chemotactic activity suggests that the TV-NAF involved was not a protein. The chemotactic activity of TV-NAF was associated with the fraction containing small molecules of less than 3,000 Da. Therefore, the possibility that eicosanoid production by trichomonads is responsible for neutrophil activation was investigated. Leukotriene B4 (LTB4; 500 pg/ml) but not thromboxane B2 (< 20 pg/ml) or prostaglandin E2 (< 8 pg/ml) was found in the STV by radioimmunoassay. Production of LTB4 by trichomonads was time dependent and increased twofold when arachidonic acid (100 microM) was added but was not decreased when eicosanoid inhibitors were present. Evidence for the presence of LTB4 in STV was further provided by the fact that rabbit anti-LTB4 antiserum could abolish the chemotactic activity of STV. These studies suggest that the spontaneous release of TV-NAF, which is most likely LTB4, may activate neutrophils, presumably through a different arachidonate metabolic pathway than that in mammalian cells.

Full text

PDF
4476

Selected References

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

  1. Barak L. S., Yocum R. R., Nothnagel E. A., Webb W. W. Fluorescence staining of the actin cytoskeleton in living cells with 7-nitrobenz-2-oxa-1,3-diazole-phallacidin. Proc Natl Acad Sci U S A. 1980 Feb;77(2):980–984. doi: 10.1073/pnas.77.2.980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blair R. J., Weller P. F. Uptake and esterification of arachidonic acid by trophozoites of Giardia lamblia. Mol Biochem Parasitol. 1987 Aug;25(1):11–18. doi: 10.1016/0166-6851(87)90013-2. [DOI] [PubMed] [Google Scholar]
  3. Chang J., Musser J. H., McGregor H. Phospholipase A2: function and pharmacological regulation. Biochem Pharmacol. 1987 Aug 1;36(15):2429–2436. doi: 10.1016/0006-2952(87)90512-0. [DOI] [PubMed] [Google Scholar]
  4. Clancy R. M., Dahinden C. A., Hugli T. E. Arachidonate metabolism by human polymorphonuclear leukocytes stimulated by N-formyl-Met-Leu-Phe or complement component C5a is independent of phospholipase activation. Proc Natl Acad Sci U S A. 1983 Dec;80(23):7200–7204. doi: 10.1073/pnas.80.23.7200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Clancy R. M., Hugli T. E. The extraction of leukotrienes (LTC4, LTD4, and LTE4) from tissue fluids: the metabolism of these mediators during IgE-dependent hypersensitivity reactions in lung. Anal Biochem. 1983 Aug;133(1):30–39. doi: 10.1016/0003-2697(83)90218-x. [DOI] [PubMed] [Google Scholar]
  6. Diamond L. S., Harlow D. R., Cunnick C. C. A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans R Soc Trop Med Hyg. 1978;72(4):431–432. doi: 10.1016/0035-9203(78)90144-x. [DOI] [PubMed] [Google Scholar]
  7. Fitzharris P., Cromwell O., Moqbel R., Hartnell A., Walsh G. M., Harvey C., Kay A. B. Leukotriene B4 generation by human neutrophils following IgG-dependent stimulation. Immunology. 1987 Aug;61(4):449–455. [PMC free article] [PubMed] [Google Scholar]
  8. Fouts A. C., Kraus S. J. Trichomonas vaginalis: reevaluation of its clinical presentation and laboratory diagnosis. J Infect Dis. 1980 Feb;141(2):137–143. doi: 10.1093/infdis/141.2.137. [DOI] [PubMed] [Google Scholar]
  9. Furlong S. T. Unique roles for lipids in Schistosoma mansoni. Parasitol Today. 1991 Feb;7(2):59–62. doi: 10.1016/0169-4758(91)90192-q. [DOI] [PubMed] [Google Scholar]
  10. Fusco A. C., Salafsky B., Kevin M. B. Schistosoma mansoni: eicosanoid production by cercariae. Exp Parasitol. 1985 Feb;59(1):44–50. doi: 10.1016/0014-4894(85)90055-4. [DOI] [PubMed] [Google Scholar]
  11. Goldman D. W., Goetzl E. J. Heterogeneity of human polymorphonuclear leukocyte receptors for leukotriene B4. Identification of a subset of high affinity receptors that transduce the chemotactic response. J Exp Med. 1984 Apr 1;159(4):1027–1041. doi: 10.1084/jem.159.4.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Goldman D. W., Goetzl E. J. Specific binding of leukotriene B4 to receptors on human polymorphonuclear leukocytes. J Immunol. 1982 Oct;129(4):1600–1604. [PubMed] [Google Scholar]
  13. Hill H. R., Augustine N. H., Newton J. A., Shigeoka A. O., Morris E., Sacchi F. Correction of a developmental defect in neutrophil activation and movement. Am J Pathol. 1987 Aug;128(2):307–314. [PMC free article] [PubMed] [Google Scholar]
  14. Hong S. L. The release of arachidonic acid from cellular lipids. Prog Allergy. 1988;44:99–139. [PubMed] [Google Scholar]
  15. Howard T. H., Meyer W. H. Chemotactic peptide modulation of actin assembly and locomotion in neutrophils. J Cell Biol. 1984 Apr;98(4):1265–1271. doi: 10.1083/jcb.98.4.1265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Korn E. D. Actin polymerization and its regulation by proteins from nonmuscle cells. Physiol Rev. 1982 Apr;62(2):672–737. doi: 10.1152/physrev.1982.62.2.672. [DOI] [PubMed] [Google Scholar]
  17. Krieger J. N., Wolner-Hanssen P., Stevens C., Holmes K. K. Characteristics of Trichomonas vaginalis isolates from women with and without colpitis macularis. J Infect Dis. 1990 Feb;161(2):307–311. doi: 10.1093/infdis/161.2.307. [DOI] [PubMed] [Google Scholar]
  18. Liu L. X., Weller P. F. Arachidonic acid metabolism in filarial parasites. Exp Parasitol. 1990 Nov;71(4):496–501. doi: 10.1016/0014-4894(90)90076-o. [DOI] [PubMed] [Google Scholar]
  19. Marks P. W., Maxfield F. R. Transient increases in cytosolic free calcium appear to be required for the migration of adherent human neutrophils. J Cell Biol. 1990 Jan;110(1):43–52. doi: 10.1083/jcb.110.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mason P. R., Forman L. In vitro attraction of polymorphonuclear leucocytes by Trichomonas vaginalis. J Parasitol. 1980 Dec;66(6):888–892. [PubMed] [Google Scholar]
  21. McColl S. R., Hurst N. P., Cleland L. G. Modulation by phorbol myristate acetate of arachidonic acid release and leukotriene synthesis by human polymorphonuclear leukocytes stimulated with A23187. Biochem Biophys Res Commun. 1986 Dec 15;141(2):399–404. doi: 10.1016/s0006-291x(86)80186-3. [DOI] [PubMed] [Google Scholar]
  22. Nagy L., Lee T. H., Goetzl E. J., Pickett W. C., Kay A. B. Complement receptor enhancement and chemotaxis of human neutrophils and eosinophils by leukotrienes and other lipoxygenase products. Clin Exp Immunol. 1982 Mar;47(3):541–547. [PMC free article] [PubMed] [Google Scholar]
  23. Packman C. H., Lichtman M. A. Activation of neutrophils: measurement of actin conformational changes by flow cytometry. Blood Cells. 1990;16(1):193–207. [PubMed] [Google Scholar]
  24. Palmblad J., Gyllenhammar H., Ringertz B., Nilsson E., Cottell B. Leukotriene B4 triggers highly characteristic and specific functional responses in neutrophils: studies of stimulus specific mechanisms. Biochim Biophys Acta. 1988 Aug 19;971(1):92–102. doi: 10.1016/0167-4889(88)90165-6. [DOI] [PubMed] [Google Scholar]
  25. Palmblad J., Malmsten C. L., Udén A. M., Rådmark O., Engstedt L., Samuelsson B. Leukotriene B4 is a potent and stereospecific stimulator of neutrophil chemotaxis and adherence. Blood. 1981 Sep;58(3):658–661. [PubMed] [Google Scholar]
  26. Palmer R. M., Salmon J. A. Release of leukotriene B4 from human neutrophils and its relationship to degranulation induced by N-formyl-methionyl-leucyl-phenylalanine, serum-treated zymosan and the ionophore A23187. Immunology. 1983 Sep;50(1):65–73. [PMC free article] [PubMed] [Google Scholar]
  27. Philip A., Carter-Scott P., Rogers C. An agar culture technique to quantitate Trichomonas vaginalis from women. J Infect Dis. 1987 Feb;155(2):304–308. doi: 10.1093/infdis/155.2.304. [DOI] [PubMed] [Google Scholar]
  28. Psychoyos S., Uziel-Fusi S., Morrissey M. M., Ganu V., Smith C. W. Thick filter neutrophil chemotaxis performed in the absence of albumin. J Immunol Methods. 1991 Mar 1;137(1):37–46. doi: 10.1016/0022-1759(91)90391-r. [DOI] [PubMed] [Google Scholar]
  29. Rao K. M., Varani J. Actin polymerization induced by chemotactic peptide and concanavalin A in rat neutrophils. J Immunol. 1982 Oct;129(4):1605–1607. [PubMed] [Google Scholar]
  30. Rein M. F., Sullivan J. A., Mandell G. L. Trichomonacidal activity of human polymorphonuclear neutrophils: killing by disruption and fragmentation. J Infect Dis. 1980 Oct;142(4):575–585. doi: 10.1093/infdis/142.4.575. [DOI] [PubMed] [Google Scholar]
  31. Salafsky B., Fusco A. C. Schistosoma mansoni: cercarial eicosanoid production and penetration response inhibited by esculetin and ibuprofen. Exp Parasitol. 1985 Aug;60(1):73–81. doi: 10.1016/s0014-4894(85)80024-2. [DOI] [PubMed] [Google Scholar]
  32. Samuelsson B. Leukotrienes: mediators of immediate hypersensitivity reactions and inflammation. Science. 1983 May 6;220(4597):568–575. doi: 10.1126/science.6301011. [DOI] [PubMed] [Google Scholar]
  33. Shaio M. F., Chang F. Y., Hou S. C., Lee C. S., Lin P. R. The role of immunoglobulin and complement in enhancing the respiratory burst of neutrophils against Trichomonas vaginalis. Parasite Immunol. 1991 May;13(3):241–250. doi: 10.1111/j.1365-3024.1991.tb00279.x. [DOI] [PubMed] [Google Scholar]
  34. Shepherd J. C., Aitken A., McManus D. P. A protein secreted in vivo by Echinococcus granulosus inhibits elastase activity and neutrophil chemotaxis. Mol Biochem Parasitol. 1991 Jan;44(1):81–90. doi: 10.1016/0166-6851(91)90223-s. [DOI] [PubMed] [Google Scholar]
  35. Wallace P. J., Wersto R. P., Packman C. H., Lichtman M. A. Chemotactic peptide-induced changes in neutrophil actin conformation. J Cell Biol. 1984 Sep;99(3):1060–1065. doi: 10.1083/jcb.99.3.1060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Walsh C. E., Dechatelet L. R., Chilton F. H., Wykle R. L., Waite M. Mechanism of arachidonic acid release in human polymorphonuclear leukocytes. Biochim Biophys Acta. 1983 Jan 7;750(1):32–40. doi: 10.1016/0005-2760(83)90201-1. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES