Induction of necrosis and apoptosis of neutrophil granulocytes by Streptococcus pneumoniae
G. Zysk
Institute of Medical Microbiology and Virology, University of Düsseldorf, Düsseldorf, and
Search for more papers by this authorL. Bejo
Institute of Medical Microbiology and Virology, University of Düsseldorf, Düsseldorf, and
Search for more papers by this authorB. K. Schneider-Wald
Institute of Medical Microbiology and Virology, University of Düsseldorf, Düsseldorf, and
Search for more papers by this authorR. Nau
Department of Neurology, University of Göttingen, Göttingen, Germany
Search for more papers by this authorH.-P. Heinz
Institute of Medical Microbiology and Virology, University of Düsseldorf, Düsseldorf, and
Search for more papers by this authorG. Zysk
Institute of Medical Microbiology and Virology, University of Düsseldorf, Düsseldorf, and
Search for more papers by this authorL. Bejo
Institute of Medical Microbiology and Virology, University of Düsseldorf, Düsseldorf, and
Search for more papers by this authorB. K. Schneider-Wald
Institute of Medical Microbiology and Virology, University of Düsseldorf, Düsseldorf, and
Search for more papers by this authorR. Nau
Department of Neurology, University of Göttingen, Göttingen, Germany
Search for more papers by this authorH.-P. Heinz
Institute of Medical Microbiology and Virology, University of Düsseldorf, Düsseldorf, and
Search for more papers by this authorAbstract
Apoptosis followed by macrophage phagocytosis is the principal mechanism by which neutrophil granulocytes (PMN) are removed from the site of inflammation. To investigate whether Streptococcus pneumoniae causes apoptosis of PMN, we exposed PMN to viable and heat-killed pneumococci and purified pneumococcal cell walls (PCW). The occurrence of PMN cell death was quantified by flow cytometry using annexin V/propidium iodide labelling of the cells. Intracellular histone-associated DNA fragments were quantified by ELISA. The presence of apoptosis was confirmed by in situ tailing. Exposure of PMN to viable pneumococci caused necrosis of the cells. The pneumococcal cytotoxin pneumolysin, the bacterial production of hydrogen peroxide, and PCW contributed to necrosis. Heat-killed pneumococci accelerated the process of apoptosis observed in cultivated non-stimulated PMN in vitro. These results demonstrated that pneumococci induce PMN cell death. Depending on the intensity of the stimulus, PMN necrosis and apoptosis were observed.
References
- 1 Cox G, Crossley J, Xing Z. Macrophage engulfment of apoptotic neutrophils contributes to the resolution of acute pulmonary inflammation in vivo. Am J Respir Cell Mol Biol 1995; 12: 232 7.
- 2 Nau R, Zettl U, Gerber J et al. Granulocytes in the subarachnoid space of humans and rabbits with bacterial meningitis undergo apoptosis and are eliminated by macrophages. Acta Neuropathol 1998; 96: 472 80.DOI: 10.1007/s004010050921
- 3 Savill JS, Wyllie AH, Henson JE, Walport MJ, Henson PM, Haslett C. Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J Clin Invest 1989; 83: 865 75.
- 4 Sendo F, Tsuchida H, Takeda Y, Gon S, Takei H, Kato T, Hachiya O, Watanabe H. Regulation of neutrophil apoptosis—its biological significance in inflammation and the immune response. Hum Cell 1996; 9: 215 22.
- 5 Watson RW, Rotstein OD, Nathens AB, Parodo J, Marshall JC. Neutrophil apoptosis is modulated by endothelial transmigration and adhesion molecule engagement. J Immunol 1997; 158: 945 53.
- 6 Biffl WL, Moore EE, Moore FA, Barnett CCJ. Interleukin-6 delays neutrophil apoptosis via a mechanism involving platelet-activating factor. J Trauma 1996; 40: 575 8.
- 7 Cox G, Gauldie J, Jordana M. Bronchial epithelial cell-derived cytokines (G-CSF and GM-CSF) promote the survival of peripheral blood neutrophils in vitro. Am J Respir Cell Mol Biol 1992; 7: 507 13.
- 8 Cox G. IL-10 enhances resolution of pulmonary inflammation in vivo by promoting apoptosis of neutrophils. Am J Physiol 1996; 271: L566 71.
- 9 Gasmi L, McLennan AG, Edwards SW. The diadenosine polyphosphates Ap3A and Ap4A and adenosine triphosphate interact with granulocyte-macrophage colony-stimulating factor to delay neutrophil apoptosis: implications for neutrophil platelet interactions during inflammation. Blood 1996; 87: 3442 9.
- 10 Girard D, Paquet ME, Paquin R, Beaulieu AD. Differential effects of interleukin-15 (IL-15) and IL-2 on human neutrophils: modulation of phagocytosis, cytoskeleton rearrangement, gene expression, and apoptosis by IL-15. Blood 1996; 88: 3176 84.
- 11 Girard D, Paquin R, Beaulieu AD. Responsiveness of human neutrophils to interleukin-4: induction of cytoskeletal rearrangements, de novo protein synthesis and delay of apoptosis. Biochem J 1997; 325: 147 53.
- 12 Kettritz R, Gaido ML, Haller H, Luft FC, Jennette CJ, Falk RJ. Interleukin-8 delays spontaneous and tumor necrosis factor-alpha-mediated apoptosis of human neutrophils. Kidney Int 1998; 53: 84 91.
- 13 Leuenroth S, Lee C, Grutkoski P, Keeping H, Simms HH. Interleukin-8-induced suppression of polymorphonuclear leukocyte apoptosis is mediated by suppressing CD95 (Fas/Apo-1) Fas-1 interactions. Surgery 1998; 124: 409 17.
- 14 Andonegui G, Trevani AS, López DH, Raiden S, Giordano M, Geffner JR. Inhibition of human neutrophil apoptosis by platelets. J Immunol 1997; 158: 3372 7.
- 15 Lee A & Haslett C. Human monocyte-conditioned medium inhibits neutrophil apoptosis in vitro. Biochem Soc Trans 1994; 22: 254S.
- 16 Cox G. Glucocorticoid treatment inhibits apoptosis in human neutrophils. Separation of survival and activation outcomes. J Immunol 1995; 154: 4719 25.
- 17 Kato T, Takeda Y, Nakada T, Sendo F. Inhibition by dexamethasone of human neutrophil apoptosis in vitro. Nat Immun 1995; 14: 198 208.
- 18 Gon S, Gatanaga T, Sendo F. Involvement of two types of TNF receptor in TNF-alpha induced neutrophil apoptosis. Microbiol Immunol 1996; 40: 463 5.
- 19 Takeda Y, Watanabe H, Yonehara S, Yamashita T, Saito S, Sendo F. Rapid acceleration of neutrophil apoptosis by tumor necrosis factor-alpha. Int Immunol 1993; 5: 691 4.
- 20 Cox G. IL-10 enhances resolution of pulmonary inflammation in vivo by promoting apoptosis of neutrophils. Am J Physiol 1996; 271: L566 71.
- 21 William R, Watson G, Redmond HP, Wang JH, Condron C, Bouchier-Hayes D. Neutrophils undergo apoptosis following ingestion of Escherichia coli. J Immunol 1996; 156: 3986 92.
- 22 Watson RW, Redmond HP, Wang JH, Bouchier-Hayes D. Bacterial ingestion, tumor necrosis factor-alpha, and heat induce programmed cell death in activated neutrophils. Shock 1996; 5: 47 51.
- 23 Yang YF, Sylte MJ, Czuprynski MJ. Apoptosis: a possible tactic of Haemophilus somnus for evasion of killing by bovine neutrophils? Microb Pathog 1998; 24: 351 9.DOI: 10.1006/mpat.1998.0205
- 24 Matsuda T, Saito H, Inoue T et al. Ratio of bacteria to polymorphonuclear neutrophils (PMNs) determines PMN fate. Shock 1999; 12: 365 72.
- 25 Rubins JB & Janoff EN. Pneumolysin: a multifunctional pneumococcal virulence factor. J Lab Clin Med 1998; 131: 21 27.
- 26 Duane PG, Rubins JB, Weisel HR, Janoff EN. Identification of hydrogen peroxide as a Streptococcus pneumoniae toxin for rat alveolar epithelial cells. Infect Immun 1993; 61: 4392 7.
- 27 Hirst RA, Sikand KS, Rutman A, Mitchell TJ, Andrew PW, O'callaghan C. Relative roles of pneumolysin and hydrogen peroxide from Streptococcus pneumoniae in inhibition of ependymal ciliary beat frequency. Infect Immun 2000; 68: 1557 62.
- 28 Geelen S, Bhattacharyya C, Tuomanen E. The cell wall mediates pneumococcal attachment to and cytopathology in human endothelial cells. Infect Immun 1993; 61: 1538 43.
- 29 Tiraby JG & Fox MS. Marker discrimination in transformation and mutation of pneumococcus. Proc Natl Acad Sci USA 1973; 70: 3541 5.
- 30 Chen JD & Morrison DA. Construction and properties of a new insertion vector, pJDC9, that is protected by transcriptional terminators and useful for cloning of DNA from Streptococcus pneumoniae. Gene 1988; 64: 155 64.
- 31 Benton A, Paton JC, Briles DE. Differences in virulence for mice among Streptococcus pneumoniae strains of capsular types 2, 3, 4, 5, and 6 are not attributable to differences in pneumolysin production. Infect Immun 1997; 65: 1237 44.
- 32 Vermes I, Haanen C, Steffens-Nakken H, Reutlingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods 1995; 184: 39 51.DOI: 10.1016/0022-1759(95)00072-i
- 33 Fischer H & Tomasz A. Production and release of peptidoglycan and wall teichoic acid polymers in pneumococci treated with beta-lactam antibiotics. J Bacteriol 1984; 157: 507 13.
- 34 Stuertz K, Schmidt H, Eiffert H, Schwartz P, Mäder M, Nau R. Differential release of lipoteichoic and teichoic acids from Streptococcus pneumoniae as a result of exposure to beta-lactam antibiotics, rifamycins, trovafloxacin, and quinupristin-dalfopristin. Antimicrob Agents Chemother 1998; 42: 277 81.
- 35 Steinfort C, Wilson R, Mitchell T et al. Effect of Streptococcus pneumoniae on human respiratory epithelium in vitro. Infect Immun 1989; 57: 2006 13.
- 36 Leblebicioglu B & Walters J. Alkaline conditions accelerate polymorphonuclear leukocyte apoptosis in vitro. Infect Immun 1999; 67: 2019 21.
