Skip to main content

Advertisement

Log in

Effect of Mycoplasmas on Apoptosis of 32D Cells Is Species-Dependent

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

We previously showed that mycoplasmal infection effectively prevented apoptosis of infected cells, whereas other researchers have indicated that mycoplasmal infection promoted apoptosis. To understand the mechanism underlying this discrepancy, five different species of mycoplasmas were investigated for their effects on apoptosis of interleukin (IL)-3–dependent 32D cells. Results revealed that Mycoplasma fermentans and M. penetrans effectively supported continuous growth of 32D cells after IL-3 withdrawal. M. fermentans was more potent than M. penetrans. This effect was achieved by way of preventing apoptosis and stimulating cell proliferation. On the contrary, M. hominis and M. salivarium accelerated apoptosis of 32D cells. M. genitalium had no significant effect on apoptosis. The RNase protection assay indicated that the proapoptotic and antiapoptotic mycoplasmas altered the expression of major apoptosis regulatory genes differently. The difference in apoptosis regulatory gene expression induced by different species of mycoplasmas might be accountable for their effects on host cell apoptosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

Literature Cited

  1. Ben-Menachem G, Mousa A, Brenner T, Pinto F, Zahringer U, Rottem S (2001) Choline deficiency induced by Mycoplasma fermentans enhances apoptosis of rat astrocytes. FEMS Microbiol Lett 201:157–162

    Article  PubMed  CAS  Google Scholar 

  2. Bendjennat M, Blanchard A, Loutfi M, Montagnier L, Bahraoui E (1999) Role of Mycoplasma penetrans endonuclease P40 as a potential pathogenic determinant. Infect Immun 67:4456–4462

    PubMed  CAS  Google Scholar 

  3. Buzanska L, Zablocka B, Dybel A, Domanska-Janik K, Albrecht J (2000) Delayed induction of apoptosis by ammonia in C6 glioma cells. Neurochem Int 37:287–297

    Article  PubMed  CAS  Google Scholar 

  4. Compton MM (1992) A biochemical hallmark of apoptosis: Internucleosomal degradation of the genome. Cancer Metastasis Rev 11:105–119

    Article  PubMed  CAS  Google Scholar 

  5. Dedieu L, Chapey E, Balcer-Rodrigues V (2005) Mycoplasma mycoides ssp. mycoides biotype small colony-secreted components induce apoptotic cell death in bovine leucocytes. Scand J Immunol 62:528–538

    Article  PubMed  CAS  Google Scholar 

  6. Facchini LM, Penn LZ (1998) The molecular role of Myc in growth and transformation: Recent discoveries lead to new insights. FASEB J 12:633–651

    PubMed  CAS  Google Scholar 

  7. Feng SH, Tsai S, Rodriguez J, Lo SC (1999) Mycoplasmal infections prevent apoptosis and induce malignant transformation of interleukin-3-dependent 32D hematopoietic cells. Mol Cell Biol 19:7995–8002

    PubMed  CAS  Google Scholar 

  8. Gong H, Zolzer F, von Recklinghausen G, Rossler J, Breit S, Havers W, et al. (1999) Arginine deiminase inhibits cell proliferation by arresting cell cycle and inducing apoptosis. Biochem Biophys Res Commun 261:10–14

    Article  PubMed  CAS  Google Scholar 

  9. Greenberger JS, Sakakeeny MA, Humphries RK, Eaves CJ, Eckner RJ (1983) Demonstration of permanent factor-dependent multipotential (erythroid/neutrophil/basophil) hematopoietic progenitor cell lines. Proc Natl Acad Sci U S A 80:2931–2935

    Article  PubMed  CAS  Google Scholar 

  10. Hall RE, Agarwal S, Kestler DP (2000) Induction of leukemia cell differentiation and apoptosis by recombinant P48, a modulin derived from Mycoplasma fermentans. Biochem Biophys Res Commun 269:284–289

    Article  PubMed  CAS  Google Scholar 

  11. Hunt ME, Brown DR (2005) Mycoplasma alligatoris infection promotes CD95 (FasR) expression and apoptosis of primary cardiac fibroblasts. Clin Diagn Lab Immunol 12:1370–1377

    Article  PubMed  CAS  Google Scholar 

  12. Into T, Kiura K, Yasuda M, Kataoka H, Inoue N, Hasebe A, et al. (2004) Stimulation of human Toll-like receptor (TLR) 2 and TLR6 with membrane lipoproteins of Mycoplasma fermentans induces apoptotic cell death after NF-kappa B activation. Cell Microbiol 6:187–199

    Article  PubMed  CAS  Google Scholar 

  13. Komada Y, Zhang XL, Zhou YW, Ido M, Azuma E (1997) Apoptotic cell death of human T lymphoblastoid cells induced by arginine deiminase. Int J Hematol 65:129–141

    Article  PubMed  CAS  Google Scholar 

  14. Laneuville P, Timm M, Hudson AT (1994) bcr/abl expression in 32D cl3(G) cells inhibits apoptosis induced by protein tyrosine kinase inhibitors. Cancer Res 54:1360–1366

    PubMed  CAS  Google Scholar 

  15. Lee JC, Hapel AJ, Ihle JN (1982) Constitutive production of a unique lymphokine (IL 3) by the WEHI-3 cell line. J Immunol 128:2393–2398

    PubMed  CAS  Google Scholar 

  16. Li YH, Chen M, Brauner A, Zheng C, Skov Jensen J, Tullus K (2002) Ureaplasma urealyticum induces apoptosis in human lung epithelial cells and macrophages. Biol Neonate 82:166–173

    Article  PubMed  CAS  Google Scholar 

  17. Lo SC, Hayes MM, Tully JG, Wang RY, Kotani H, Pierce PF, et al. (1992) Mycoplasma penetrans sp. nov., from the urogenital tract of patients with AIDS. Int J Syst Bacteriol 42:357–364

    Article  PubMed  CAS  Google Scholar 

  18. Lo SC, Shih JW, Newton PBD, Wong DM, Hayes MM, Benish JR, et al. (1989) Virus-like infectious agent (VLIA) is a novel pathogenic mycoplasma: Mycoplasma incognitus. Am J Trop Med Hyg 41:586–600

    PubMed  CAS  Google Scholar 

  19. Maniloff J, McElhaney RN, Flinch LR, Baseman JB (1992) Mycoplasmas, molecular biology, pathogenesis. Washington DC, American Society for Microbiology

    Google Scholar 

  20. Mesner PW, Winters TR, Green SH (1992) Nerve growth factor withdrawal-induced cell death in neuronal PC12 cells resembles that in sympathetic neurons. J Cell Biol 119:1669–1680

    Article  PubMed  CAS  Google Scholar 

  21. Nunez G, London L, Hockenbery D, Alexander M, McKearn JP, Korsmeyer SJ (1990) Deregulated Bcl-2 gene expression selectively prolongs survival of growth factor-deprived hemopoietic cell lines. J Immunol 144:3602–3610

    PubMed  CAS  Google Scholar 

  22. Paddenberg R, Weber A, Wulf S, Mannherz HG (1998) Mycoplasma nucleases able to induce internucleosomal DNA degradation in cultured cells possess many characteristics of eukaryotic apoptotic nucleases. Cell Death Diff 5:517–528

    Article  CAS  Google Scholar 

  23. Paddenberg R, Wulf S, Weber A, Heimann P, Beck LA, Mannherz HG (1996) Internucleosomal DNA fragmentation in cultured cells under conditions reported to induce apoptosis may be caused by mycoplasma endonucleases. Eur J Cell Biol 71:105–119

    PubMed  CAS  Google Scholar 

  24. Raff MC (1992) Social controls on cell survival and cell death. Nature 356:397–400

    Article  PubMed  CAS  Google Scholar 

  25. Shibata K, Watanabe T (1997) Mycoplasma fermentans enhances concanavalin A-induced apoptosis of mouse splenic T cells. FEMS Immunol Med Microbiol 17:103–109

    Article  PubMed  CAS  Google Scholar 

  26. Sokolova IA, Vaughan AT, Khodarev NN (1998) Mycoplasma infection can sensitize host cells to apoptosis through contribution of apoptotic-like endonuclease(s). Immunol Cell Biol 76:526–534

    Article  PubMed  CAS  Google Scholar 

  27. Thatte HS, Rhee JH, Zagarins SE, Treanor PR, Birjiniuk V, Crittenden MD, et al. (2004) Acidosis-induced apoptosis in human and porcine heart. Ann Thorac Surg 77:1376–1383

    Article  PubMed  Google Scholar 

  28. Tsai S, Wear DJ, Shih JW, Lo SC (1995) Mycoplasmas and oncogenesis: Persistent infection and multistage malignant transformation. Proc Natl Acad Sci U S A 92:10197–10201

    Article  PubMed  CAS  Google Scholar 

  29. Tully JG (1983) The Emmy Klieneberger-Nobel Award lecture. Reflections on recovery of some fastidious mollicutes with implications of the changing host patterns of these organisms. Yale J Biol Med 56:799–813

    PubMed  CAS  Google Scholar 

  30. Vanden Bush TJ, Rosenbusch RF (2002) Mycoplasma bovis induces apoptosis of bovine lymphocytes. FEMS Immunol Med Microbiol 32:97–103

    Article  PubMed  CAS  Google Scholar 

  31. Wyllie AH (1992) Apoptosis and the regulation of cell numbers in normal and neoplastic tissues: An overview. Cancer Metastasis Rev 11:95–103

    Article  PubMed  CAS  Google Scholar 

  32. Zhang S, Tsai S, Lo SC (2006) Alteration of gene expression profiles during mycoplasma-induced malignant cell transformation. BMC Cancer 6:116

    Article  PubMed  CAS  Google Scholar 

  33. Zhang S, Wear DJ, Lo S (2000) Mycoplasmal infections alter gene expression in cultured human prostatic and cervical epithelial cells. FEMS Immunol Med Microbiol 27:43–50

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Tamara Newsome and Joe F. Rodriguez for their critical reviews of this manuscript. This work was supported by grants (UBUY, UBPA, UBIM, and UBZZ) from American Registry of Pathology/Armed Forces Institute of Pathology.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shimin Zhang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, S., Lo, SC. Effect of Mycoplasmas on Apoptosis of 32D Cells Is Species-Dependent. Curr Microbiol 54, 388–395 (2007). https://doi.org/10.1007/s00284-006-0491-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-006-0491-x

Keywords

Navigation