1887

Abstract

The genus , whose members are Gram-negative non-fermentative rods, possesses ceramides and related sphingophospholipids (SPLs) with isoheptadecasphinganine and 2-hydroxy or non-hydroxy isopentadecanoic acid. This paper reports evidence that ceramides isolated from ATCC 33861 induce endonucleolytic DNA cleavage in human myeloid leukaemia HL-60 cells , which is the primary characteristic biochemical marker for apoptosis or programmed cell death. Ceramides and SPLs also induced DNA fragmentation and caspase-3 activation, followed by changes in morphology, such as alterations in the size of nuclei and cells, and cell cycle shortening. Apoptotic activity correlated with the ceramide structure. Ceramide with a 2-hydroxy fatty acid showed stronger apoptotic activity than ceramide with a non-hydroxy fatty acid. Furthermore, the major five SPLs (ceramide phosphorylethanolamine-1 and -2, ceramide phosphorylinositol-1 and -2, and ceramide phosphorylmannose-1) showed apoptosis-inducing activity in HL-60 cells, indicating that the ceramide moiety of the SPLs plays a crucial role as the intracellular second messenger but that their hydrophilicity is less important in this regard. The hydrophilic part of SPLs may play a role in other cellular response systems. The involvement of Fas antigen was implicated in the apoptotic event since Fas antigen expression was observed after 3 or 4 h stimulation of HL-60 cells with bacterial ceramides. However, a time-course study for caspase-3 activation indicated maximal activity at 1 h after stimulation with bacterial ceramides, suggesting that two (or possibly more) mechanisms of signal transduction, Fas-dependent and Fas-independent, may be involved. Fas antigen expression and caspase-3 activation by five kinds of SPLs were observed after 3 or 4 h. These results indicate that there is a difference in the response of HL-60 cells to bacterial ceramides and SPLs.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.25922-0
2003-08-01
2020-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/8/mic1492071.html?itemId=/content/journal/micro/10.1099/mic.0.25922-0&mimeType=html&fmt=ahah

References

  1. Allan D.. 2000; Lipid metabolic changes caused by short-chain ceramides and the connection with apoptosis. Biochem J345:603–610
    [Google Scholar]
  2. Damjanovski S., Amano T., Li Q., Ueda S., Shi Y. B., Ishizuya-Oka A.. 2000; Role of ECM remodeling in thyroid hormone-dependent apoptosis during anuran metamorphosis. Ann N Y Acad Sci926:180–191
    [Google Scholar]
  3. Decaudin D., Geley S., Hirsch T., Castedo M., Marchetti P., Macho A., Kofler R., Kroemer G.. 1997; Bcl-2 and Bcl-XL antagonize the mitochondrial dysfunction preceding nuclear apoptosis induced by chemotherapeutic agents. Cancer Res57:62–67
    [Google Scholar]
  4. Deng G., Podack E. R.. 1993; Suppression of apoptosis in a cytotoxic T-cell line by interleukin 2-mediated gene transcription and deregulated expression of the protooncogene bcl-2 . Proc Natl Acad Sci U S A90:2189–2193
    [Google Scholar]
  5. Eischen C. M., Schilling J. D., Lynch D. H., Krammer P. H., Leibson P. J.. 1996; Fc receptor-induced expression of Fas ligand on activated NK cells facilitates cell-mediated cytotoxicity and subsequent autocrine NK cell apoptosis. J Immunol156:2693–2699
    [Google Scholar]
  6. Ferrarini M., Imro M. A., Sciorati C., Heltai S., Protti M. P., Pellicciari C., Rovere P., Manfredi A. A., Rugarli C.. 1999; Blockade of the Fas-triggered intracellular signaling pathway in human melanomas is circumvented by cytotoxic lymphocytes. Int J Cancer81:573–579
    [Google Scholar]
  7. Folch J., Lees M., Sloane Stanley G. H.. 1959; A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem226:497–509
    [Google Scholar]
  8. Furuya S., Ono K., Hirabayashi Y.. 1995; Sphingolipid biosynthesis is necessary for dendrite growth and survival of cerebellar Purkinje cells in culture. J Neurochem65:1551–1561
    [Google Scholar]
  9. Goodman Y., Mattson M. P.. 1996; Ceramide protects hippocampal neurons against excitotoxic and oxidative insults, and amyloid beta-peptide toxicity. J Neurochem66:869–872
    [Google Scholar]
  10. Gorczyca W., Gong J., Ardelt B., Traganos F., Darzynkiewicz Z.. 1993; The cell cycle related differences in susceptibility of HL-60 cells to apoptosis induced by various antitumor agents. Cancer Res53:3186–3192
    [Google Scholar]
  11. Hannun Y. A., Obeid L. M.. 1995; Ceramide: an intracellular signal for apoptosis. Trends Biochem Sci20:73–77
    [Google Scholar]
  12. Hannun Y. A., Loomis C. R., Merrill A. H. Jr, Bell R. M.. 1986; Sphingosine inhibition of protein kinase C activity and of phorbol dibutyrate binding in vitro and in human platelets. J Biol Chem261:12604–12609
    [Google Scholar]
  13. Harel R., Futerman A. H.. 1993; Inhibition of sphingolipid synthesis affects axonal outgrowth in cultured hippocampal neurons. J Biol Chem268:14476–14481
    [Google Scholar]
  14. Hartfield P. J., Mayne G. C., Murray A. W.. 1997; Ceramide induces apoptosis in PC12 cells. FEBS Lett401:148–152
    [Google Scholar]
  15. Ishizuya-Oka A.. 1996; Apoptosis of larval cells during amphibian metamorphosis. Microsc Res Tech34:228–235
    [Google Scholar]
  16. Ito A., Horigome K.. 1995; Ceramide prevents neuronal programmed cell death induced by nerve growth factor deprivation. J Neurochem65:463–466
    [Google Scholar]
  17. Iwata M., Hotta H., Higuchi N., Nishiuchi N., Fujiwara N., Arakawa T., Yano I., Kobayashi K.. 2002; Induction of thymic apoptosis by shigatoxin from Escherichia coli O157 : H7 in vivo and in vitro. Osaka City Med J47:11–22
    [Google Scholar]
  18. Karasavvas N., Erukulla R. K., Bittman R., Lockshin R., Zakeri Z.. 1996; Stereospecific induction of apoptosis in U937 cells by N -octanoyl-sphingosine stereoisomers and N -octyl-sphingosine. The ceramide amide group is not required for apoptosis. Eur J Biochem236:729–737
    [Google Scholar]
  19. Kawasaki S., Moriguchi R., Sekiya K., Nakai T., Ono E., Kume K., Kawahara K.. 1994; The cell envelope structure of the lipopolysaccharide-lacking gram-negative bacterium Sphingomonas paucimobilis . J Bacteriol176:284–290
    [Google Scholar]
  20. Kondo T., Matsuda T., Tashima M., Umehara H., Domae N., Yokoyama K., Uchiyama T., Okazaki T.. 2000a; Suppression of heat shock protein-70 by ceramide in heat shock-induced HL-60 cell apoptosis. J Biol Chem275:8872–8879
    [Google Scholar]
  21. Kondo T., Matsuda T., Kitano T.. 7 other authors 2000b; Role of c-jun expression increased by heat shock- and ceramide-activated caspase-3 in HL-60 cell apoptosis. Possible involvement of ceramide in heat shock-induced apoptosis. J Biol Chem275:7668–7676
    [Google Scholar]
  22. Lakics V., Vogel S. N.. 1998; Lipopolysaccharide and ceramide use divergent signaling pathways to induce cell death in murine macrophages. J Immunol161:2490–2500
    [Google Scholar]
  23. Lavie Y., Cao H., Volner A., Lucci A., Han T. Y., Geffen V., Giuliano A. E., Cabot M. C.. 1997; Agents that reverse multidrug resistance, tamoxifen, verapamil, and cyclosporin A, block glycosphingolipid metabolism by inhibiting ceramide glycosylation in human cancer cells. J Biol Chem272:1682–1687
    [Google Scholar]
  24. Linardic C. M., Hannun Y. A.. 1994; Identification of a distinct pool of sphingomyelin involved in the sphingomyelin cycle. J Biol Chem269:23530–23537
    [Google Scholar]
  25. Liu P., Anderson R. G.. 1995; Compartmentalized production of ceramide at the cell surface. J Biol Chem270:27179–27185
    [Google Scholar]
  26. Mansat V., Laurent G., Levade T., Bettaieb A., Jaffrezou J. P.. 1997; The protein kinase C activators phorbol esters and phosphatidylserine inhibit neutral sphingomyelinase activation, ceramide generation, and apoptosis triggered by daunorubicin. Cancer Res57:5300–5304
    [Google Scholar]
  27. McConkey D. J., Nicotera P., Orrenius S.. 1994; Signalling and chromatin fragmentation in thymocyte apoptosis. Immunol Rev142:343–363
    [Google Scholar]
  28. Mizushima N., Koike R., Kohsaka H., Kushi Y., Handa S., Yagita H., Miyasaka N.. 1996; Ceramide induces apoptosis via CPP32 activation. FEBS Lett395:267–271
    [Google Scholar]
  29. Nakamura S., Kozutsumi Y., Sun Y., Miyake Y., Fujita T., Kawasaki T.. 1996; Dual roles of sphingolipids in signaling of the escape from and onset of apoptosis in a mouse cytotoxic T-cell line, CTLL-2. J Biol Chem271:1255–1257
    [Google Scholar]
  30. Nakashima K., Ohtsuka A., Hayashi K.. 1998; Comparison of the effects of thyroxine and triiodothyronine on protein turnover and apoptosis in primary chick muscle cell cultures. Biochem Biophys Res Commun251:442–448
    [Google Scholar]
  31. Nakayama M.. 2000; Structure and apoptosis-inducing activity of sphingolipids isolated from Sphingobacterium spiritivorum . Seikatsu Eisei42:135–148
    [Google Scholar]
  32. Okazaki T.. 1999; Implications of “ceramide-regulating biostat system” from the discovery of “sphingomyelin cycle” [in Japanese]. Tanpakushitsu Kakusan Koso44:1052–1058
    [Google Scholar]
  33. Okazaki T., Domae N.. 1994; Physiological activity of sphingosine. J Clin Exp Med171:913–916
    [Google Scholar]
  34. Okazaki T., Bell R. M., Hannun Y. A.. 1989; Sphingomyelin turnover induced by vitamin D3 in HL-60 cells. Role in cell differentiation. J Biol Chem264:19076–19080
    [Google Scholar]
  35. Okazaki T., Bielawska A., Bell R. M., Hannun Y. A.. 1990; Role of ceramide as a lipid mediator of 1 alpha, 25-dihydroxyvitamin D3-induced HL-60 cell differentiation. J Biol Chem265:15823–15831
    [Google Scholar]
  36. Okazaki T., Bielawska A., Domae N., Bell R. M., Hannun Y. A.. 1994; Characteristics and partial purification of a novel cytosolic, magnesium-independent, neutral sphingomyelinase activated in the early signal transduction of 1 alpha, 25-dihydroxyvitamin D3-induced HL-60 cell differentiation. J Biol Chem269:4070–4077
    [Google Scholar]
  37. Ozeki Y., Kaneda K., Fujiwara N., Morimoto M., Oka S., Yano I.. 1997; In vivo induction of apoptosis in the thymus by administration of mycobacterial cord factor (trehalose 6,6′-dimycolate). Infect Immun65:1793–1799
    [Google Scholar]
  38. Parton R. G.. 1994; Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae. J Histochem Cytochem42:155–166
    [Google Scholar]
  39. Rothberg K. G., Heuser J. E., Donzell W. C., Ying Y. S., Glenney J. R., Anderson R. G.. 1992; Caveolin, a protein component of caveolae membrane coats. Cell68:673–682
    [Google Scholar]
  40. Saba J. D., Obeid L. M., Hannun Y. A.. 1996; Ceramide: an intracellular mediator of apoptosis and growth suppression. Philos Trans R Soc Lond B Biol Sci351:233–240 discussion 240–231
    [Google Scholar]
  41. Saito T., Kurasaki M.. 2000; Apoptosis and endocrine disrupters. Biomed Res21:353–359
    [Google Scholar]
  42. Sawai H., Okazaki T., Yamamoto H.. other authors 1995; Requirement of AP-1 for ceramide-induced apoptosis in human leukemia HL-60 cells. J Biol Chem270:27326–27331
    [Google Scholar]
  43. Schlegel J., Peters I., Orrenius S., Miller D. K., Thornberry N. A., Yamin T. T., Nicholson D. W.. 1996; CPP32/apopain is a key interleukin 1 beta converting enzyme-like protease involved in Fas-mediated apoptosis. J Biol Chem271:1841–1844
    [Google Scholar]
  44. Schnitzer J. E., Oh P., McIntosh D. P.. 1996; Role of GTP hydrolysis in fission of caveole directly from plasma membranes. Science274:239–242
    [Google Scholar]
  45. Schutze S., Potthoff K., Machleidt T., Berkovic D., Wiegmann K., Kronke M.. 1992; TNF activates NF-kappa B by phosphatidylcholine-specific phospholipase C-induced “acidic” sphingomyelin breakdown. Cell71:765–776
    [Google Scholar]
  46. Schwarz A., Futerman A. H.. 1997; Distinct roles for ceramide and glucosylceramide at different stages of neuronal growth. J Neurosci17:2929–2938
    [Google Scholar]
  47. Shimizu S., Eguchi Y., Kamiike W., Matsuda H., Tsujimoto Y.. 1996; Bcl-2 expression prevents activation of the ICE protease cascade. Oncogene12:2251–2257
    [Google Scholar]
  48. Suzuki A., Tsutomi Y., Miura M., Akahane K.. 1999; Caspase 3 inactivation to suppress Fas-mediated apoptosis: identification of binding domain with p21 and ILP and inactivation machinery by p21. Oncogene18:1239–1244
    [Google Scholar]
  49. Taylor I. W.. 1980; A rapid single step staining technique for DNA analysis by flow microfluorimetry. J Histochem Cytochem28:1021–1024
    [Google Scholar]
  50. Tepper C. G., Jayadev S., Liu B., Bielawska A., Wolff R., Yonehara S., Hannun Y. A., Seldin M. F.. 1995; Role for ceramide as an endogenous mediator of Fas-induced cytotoxicity. Proc Natl Acad Sci U S A92:8443–8447
    [Google Scholar]
  51. Tessitore L., Valente G., Bonelli G., Costelli P., Baccino F. M.. 1989; Regulation of cell turnover in the livers of tumour-bearing rats: occurrence of apoptosis. Int J Cancer44:697–700
    [Google Scholar]
  52. Verheij M., Bose R., Lin X. H.. 10 other authors 1996; Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature380:75–79
    [Google Scholar]
  53. Wang B., Ohyama H., Haginoya K., Odaka T., Itsukaichi H., Yukawa O., Yamada T., Hayata I.. 2000; Adaptive response in embryogenesis. III. Relationship to radiation-induced apoptosis and Trp53 gene status. Radiat Res154:277–282
    [Google Scholar]
  54. Wiegmann K., Schutze S., Machleidt T., Witte D., Kronke M.. 1994; Functional dichotomy of neutral and acidic sphingomyelinases in tumor necrosis factor signaling. Cell78:1005–1015
    [Google Scholar]
  55. Yang Z., Costanzo M., Golde D. W., Kolesnick R. N.. 1993; Tumor necrosis factor activation of the sphingomyelin pathway signals nuclear factor kappa B translocation in intact HL-60 cells. J Biol Chem268:20520–20523
    [Google Scholar]
  56. Yano I., Tomiyasu I., Yabuuchi E.. 1982; Long chain base comparison of strains of three species of Sphingobacterium gen. nov. FEMS Microbiol Lett15:303–307
    [Google Scholar]
  57. Yano I., Imaizumi S., Tomiyasu I., Yabuuchi E.. 1983; Separation and analysis of free ceramides containing 2-hydroxy fatty acids in Sphingobacterium species. FEMS Microbiol Lett20:449–453
    [Google Scholar]
  58. Yonehara S., Ishii A., Yonehara M.. 1989; A cell-killing monoclonal antibody (anti-Fas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J Exp Med169:1747–1756
    [Google Scholar]
  59. Zhang Y. H., Takahashi K., Jiang G. Z., Kawai M., Fukada M., Yokochi T.. 1993; In vivo induction of apoptosis (programmed cell death) in mouse thymus by administration of lipopolysaccharide. Infect Immun61:5044–5048
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.25922-0
Loading
/content/journal/micro/10.1099/mic.0.25922-0
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error