DOI QR코드

DOI QR Code

Endotoxins of Enteric Pathogens Modulate the Functions of Human Neutrophils and Lymphocytes

  • Islam, Laila N. (Department of Biochemistry and Molecular Biology, University of Dhaka) ;
  • Nabi, A.H.M. Nurun (Department of Biochemistry and Molecular Biology, University of Dhaka)
  • Received : 2003.04.08
  • Accepted : 2003.06.04
  • Published : 2003.11.30

Abstract

The locomotor responses of human peripheral blood neutrophils and lymphocytes were measured by the change from spherical to polarized shapes in the presence of endotoxins (lipopolysaccharide, LPS) of enteric pathogens: S. dysenteriae type 1, V. cholerae Inaba 569B, S. typhimurium, and K. pneumoniae. We reported earlier that these endotoxins are chemotactic factors for the neutrophils since they stimulated cell polarization within a few minutes of incubation. Endotoxins had an inhibitory effect upon neutrophil phagocytosis of opsonized yeast and the cells engulfed fewer yeasts. Interestingly, endotoxins increased neutrophil adhesion to clean glass surfaces, but stimulated the cells to exhibit increased random locomotion (chemokinesis) through cellulose nitrate filters and show an enhanced ability to reduce nitroblue tetrazolium (NBT) dye. Unlike neutrophils, lymphocytes direct from blood do not show polarized morphology towards chemotactic factors but the cells acquire locomotor capacity during 24-72 h culture with mitogens such as phytohemagglutinin (PHA), phorbol myristate acetate or concanavalin A. Stimulation of blood lymphocytes with endotoxins did not induce cell polarization in short-term but long-term culture resulted in an increase in the proportion of polarized cells that acquired locomotor morphologies. The majority of these cells were identified as esterase negative B-lymphocytes that migrated through filters. Despite the optimum time of incubation for each of these cell types being different, we found that lymphocytes respond to much lower concentrations of endotoxins than the neutrophils. These findings suggest that endotoxins of enteric pathogens modulate the functions of human blood neutrophils and lymphocytes.

Keywords

References

  1. Al-Bahry, S. N. and Pistole, T. G. (1997) Adherence ofSalmonella typhimurium to murine peritoneal macrophages ismediated by lipopolysaccharide and complement receptors.Zentralbl. Bakteriol. 286, 83-92. https://doi.org/10.1016/S0934-8840(97)80080-1
  2. Brooks, K. H. and Vitetta, E. S. (1987) Activation of murine Bcells with Salmonella typhimurium mitogen (STM),lipopolysaccharide (LPS), and dextran sulfate (DxS). I. Cellcycle analysis and induction of cytoplasmic immunoglobulin. J.Mol. Cell Immunol. 3, 215-219.
  3. Castro, A., Bemer, V., Nobrega, A., Coutinho, A. and Truffa-Bachi, P. (1998) Administration to mouse of endotoxin fromgram-negative bacteria leads to activation and apoptosis of Tlymphocytes. Eur. J. Immunol. 28, 488-495. https://doi.org/10.1002/(SICI)1521-4141(199802)28:02<488::AID-IMMU488>3.0.CO;2-R
  4. Detmers, P. A., Zhou, D. and Powell, D. E. (1994). Differentsignaling pathways for CD18-mediated adhesion and Fc-mediatedphagocytosis. Response of neutrophils to LPS. J.Immunol. 153, 2137-2145.
  5. Finn. A., Strobel. S., Levin. M. and klein. N. (1994) Endotox-ininducedneutrophil adherence to endothelium: relationship toCD11b/CD18 and L-selectin expression and matrix disruption.Ann. N. Y. Acad. Sci. 725, 173-182. https://doi.org/10.1111/j.1749-6632.1994.tb39799.x
  6. Forehand, J. R., Pabst, M. J., Phillips, W. A. and Johnston Jr., R.B. (1989) Lipopolysaccharide priming of human neutrophils foran enhanced respiratory burst. Role of intracellular freecalcium. J. Clin. Invest. 83, 74-83. https://doi.org/10.1172/JCI113887
  7. Francis, J. W., Todd, R. F. 3rd, Boxer, L. A. and Petty, H. R.(1989) Sequential expression of surface C3bi receptors duringneutrophil locomotion. J. Cell Physiol. 140, 519-523. https://doi.org/10.1002/jcp.1041400317
  8. Gonzalez, C. R., Isibasi, A., Ortiz-Navarrete, V., Paniagua, J.,Garcia, J. A., Blanco, F. and Kumate, J. (1993) Lymphocyticproliferative response to outer-membrane proteins isolated fromSalmonella. Microbiol. Immunol. 37, 793-799. https://doi.org/10.1111/j.1348-0421.1993.tb01707.x
  9. Greaves, M., Jannosy, G. and Doenhoff, M. (1974) Slectivetriggering of human T- and B-lymphocytes in vitro bypolyclonal mitogens. J. Exp. Med. 140, 1-18. https://doi.org/10.1084/jem.140.1.1
  10. Grey, I., Krueger, K. and Spiesel S. Z. (1972) Stimulation of B-lymphocytesby endotoxin. J. Immunol. 108, 1088-1091.
  11. Howard, T. H., Wang, D. and Berkow, R. L. (1990)Lipopolysaccharide modulates chemotactic peptide inducedactin polymerization in neutrophils. J. Leukoc. Biol. 47, 13-24.
  12. Islam, L. N., Ahmed, K. M. and Shammy, S. (1997) Modulationof human neutrophil function by Vibrio choleraelipopolysaccharide. Bangladesh J. Biochem. 3, 75-86.
  13. Islam, L. N., Nabi, A. H. M. N., Ahmed, K. M. and Sultana, N.(2002) Endotoxins of enteric pathogens are chemotactic factorsfor human neutrophils. J. Biochem. Mol. Biol. 30, 482-487.
  14. Islam, L. N. and Wilkinson, P. C. (1989) Evaluation of methodsfor isolating human peripheral blood monocytes. Studies onchemotactic locomotion and other functional characteristics. J.Immunol. Meth. 121, 75-84. https://doi.org/10.1016/0022-1759(89)90422-5
  15. Malhotra, R., Priest, R. and Bird, M. I. (1996) Role for L-selectinin lipopolysaccharide-induced activation of neutrophils. J.Biochem. 320, 589-593.
  16. Monno, R., Valenza, M. A., Panaro, M. A., Lisi, S., Marcuccio,L., De Vito, D. and Mitolo, V. (1996) Spontaneous binding ofVibrio cholerae to human leucocytes. Microbios. 88, 169-176.
  17. Nakano, M., Tanabe, M. J., Hori, H., Kondo, S. and Hisatsune, K.(1977) Immunological properties of Vibrio choleraelipopolysaccharides. Microbiol. Immunol. 21, 611-619. https://doi.org/10.1111/j.1348-0421.1977.tb00329.x
  18. Proctor, R. A. (1979) Endotoxin in vitro interactions with humanneutrophils: depression of chemiluminescence, oxygenconsumption, superoxide production, and killing. Infect. Immun.25, 912-921.
  19. Ringden, O. (1976) Activation of human lymphocytesubpopulations by rabbit anti human ${\beta}2-microglobulin$ and bylipopolysaccharide. Scand. J. Immunol. 5, 891- 900. https://doi.org/10.1111/j.1365-3083.1976.tb03039.x
  20. Seheli, K., Kanta, H. Y. and Islam, L. N. (2002) Activation bymitogens and endotoxins of human peripheral bloodlymphocytes: morphological polarization, locomotion and celltype study. Dhaka Univ. J. Biol. Sci. 11, 49-58.
  21. Sha’afi, R. I. and Molski, T. F. (1988) Activation of theneutrophil. Prog. Allergy 42, 1- 64.
  22. Shields, J. M. and Haston, W. S. (1985) Behaviour of neutrophilleukocytes in uniform concentrations of chemotactic factors:contraction waves, cell polarity and persistence. J. Cell Sci. 74,75-93.
  23. Simms, H. H. and D’Amico, R. (1994) Regulation of intracellularpolymorphonuclear leukocyte Fc receptors bylipopolysaccharide. Cell. Immunol. 157, 525-541. https://doi.org/10.1006/cimm.1994.1247
  24. Stickle, J. E. (1996) The neutrophil. Function, disorders andtesting. Vet. Clin. North. Am. Small Anim. Pract. 26, 1013-1021. https://doi.org/10.1016/S0195-5616(96)50053-7
  25. Tennenberg, S. D. and Weller, J. J. (1997) Endotoxin-inducedneutrophil-mediated endothelial cytotoxicity is enhanced by T-lymphocytes.J. Surg. Res. 69, 11-13. https://doi.org/10.1006/jsre.1996.4996
  26. Valenza, M. A., Monno, R., De Vito, D., Mitolo, V., Lisi, S.,Marcuccio, C., Marcuccio, L. and Panaro, M. A. (1997)Polarizing response of human polymorphonuclear cells toVibrio cholerae. Cytobios. 90, 193-201.
  27. Westphal, O. and Jann, K. (1965) Bacterial lipopolysaccharides:extraction with phenol water and further application of theprocedure; in Methods in Carbohydrate Chemistry, Whister, R.L. and Wolfrom, M. L. (eds.), Vol. 5, p. 88, Academic PressInc., New York, USA.
  28. Wilkinson, P. C. (1986) The locomotor capacity of humanlymphocytes and its enhancement by cell growth. Immunol. 57,281-289.
  29. Wilkinson, P. C. and Higgins, A. (1987) OKT3-activatedlocomotion of human blood lymphocytes: a phenomenonrequiring contact of T cells with Fc receptor-bearing cells.ImmunoI. 60, 445-451.
  30. Wilkinson, P. C., Lackie, J. M., Haston, W. S. and Islam, L. N.(1988) Effects of phorbol esters on shape and locomotion of human blood lymphocytes. J. Cell Sci. 90, 645-655.
  31. Wilson, M. E. (1985) Effects of bacterial endotoxins on neutrophilfunction. Rev. Infect. Dis. 7, 404-418. https://doi.org/10.1093/clinids/7.3.404
  32. Zarewych, D. M., Kindzelskii, A. L., Todd, R. F. 3rd and Petty, H.R. (1996) LPS induces CD14 association with complement receptor type 3, which is reversed by neutrophil adhesion. J.Immunol. 156, 430-433.
  33. Zimmerli, W., Reber, A. M. and Dahinden, C. A. (1990) The roleof formylpeptide receptors, C5a receptors, and cytosolic-freecalcium in neutrophil priming. J. Infect. Dis. 161, 242-249. https://doi.org/10.1093/infdis/161.2.242

Cited by

  1. Neutrophil dysfunction induced by hyperglycemia: modulation of myeloperoxidase activity vol.30, pp.7, 2012, https://doi.org/10.1002/cbf.2840
  2. Effect of Deoxynivalenol and Other Type B Trichothecenes on the Intestine: A Review vol.6, pp.5, 2014, https://doi.org/10.3390/toxins6051615