Biomedical Science Letters (대한의생명과학회지)

The Korean Society for Biomedical Laboratory Sciences (대한의생명과학회)
권호 표지

Bfl-1/A1 Molecules are Induced in Mycobacterium Infected THP-1 Cells in the Early Time Points

  • Park, Sang-Jung (Department of Biomedical Laboratory Science, College of Health Sciences, Yonsei University) ;
  • Cho, Jang-Eun (Department of Biomedical Laboratory Science, Daegu Health College) ;
  • Kim, Yoon-Suk (Department of Biomedical Laboratory Science, College of Health Sciences, Yonsei University) ;
  • Cho, Sang-Nae (Department of Microbiology, Yonsei University College of Medicine) ;
  • Lee, Hye-Young (Department of Biomedical Laboratory Science, College of Health Sciences, Yonsei University)
  • Received : 2012.05.31
  • Accepted : 2012.09.04
  • Published : 2012.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Apoptosis is a physiological programmed cell death process. Tubercle bacilli inhibit apoptosis of alveolar macrophages and phagolysosome fusion. We investigated whether the Bcl-2 family anti-apoptotic member, Bfl-1/A1, plays an important role in the anti-apoptotic process during mycobacterial infection. PMA-treated human monocytoid THP-1 cells were infected with mycobacteria (H37Rv, BCG, and K-strain) at a multiplicity of infection (MOI) of 10 for 0, 1.5, 3, 6, 9, 12, 18, 24, 48, or 72 h. In addition, PMA-treated THP-1 cells were pretreated with specific inhibitors for 45 min before stimulation with mycobacteria at an MOI of 10 for 4 h. After the indicated time, the cells were subject to reverse transcription-polymerase chain reaction (RT-PCR) analysis, and a Bfl-1/A1-specific Western blot was performed. In PMA-differentiated THP-1 cells, the expression level of Bfl-1/A1 mRNA was increased by Mycobacterium tuberculosis (MTB) H37Rv infection. The mRNA level of Bfl-1/A1 peaked 3 h after MTB infection, then declined gradually until 9 h. However, Bfl-1/A1 mRNA induction gradually re-increased from 24 h to 72 h after MTB infection. No difference in Bfl-1/A1 expression was detected following infection with MTB H37Rv, K-strain, or M. bovis BCG. These results were not dependent on mycobacterial virulence. Moreover, mRNA levels of other anti-apoptotic molecules (Mcl-1, Bcl-2, and Bcl-xL) were not increased after MTB H37Rv or K-strain infection. These results suggest that mycobacteria induce the innate immune host defense mechanisms that utilize Bfl-1/A1 molecules at early time points, regardless of virulence.

Keywords

References

  1. Armstrong JA, Hart PD. Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J Exp Med. 1971. 134: 713-740. https://doi.org/10.1084/jem.134.3.713
  2. Bocchino M, Galati D, Sanduzzi A, Colizzi V, Brunetti E, Mancino G. Role of mycobacteria-induced monocyte/macrophage apoptosis in the pathogenesis of human tuberculosis. Int J Tuberc Lung Dis. 2005. 9: 375-383.
  3. Chan J, Xing Y, Magliozzo RS, Bloom BR. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J Exp Med. 1992. 175: 1111-1122. https://doi.org/10.1084/jem.175.4.1111
  4. Clemens DL, Horwitz MA. Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J Exp Med. 1995. 181: 257-270. https://doi.org/10.1084/jem.181.1.257
  5. Deretic V, Singh S, Master S, Harris J, Roberts E, Kyei G, Davis A, de Haro S, Naylor J, Lee HH, Vergne I. Mycobacterium tuberculosis inhibition of phagolysosome biogenesis and autophagy as a host defence mechanism. Cell Microbiol. 2006. 8: 719-727. https://doi.org/10.1111/j.1462-5822.2006.00705.x
  6. Dhiman R, Kathania M, Raje M, Majumdar S. Inhibition of bfl-1/A1 by siRNA inhibits mycobacterial growth in THP-1 cells by enhancing phagosomal acidification. Biochim Biophys Acta. 2008. 1780: 733-742. https://doi.org/10.1016/j.bbagen.2007.12.010
  7. Dhiman R, Raje M, Majumdar S. Differential expression of NF-kappaB in mycobacteria infected THP-1 affects apoptosis. Biochim Biophys Acta. 2007. 1770: 649-658. https://doi.org/10.1016/j.bbagen.2006.11.016
  8. Dockrell DH. Apoptotic cell death in the pathogenesis of infectious diseases. J Infect. 2001. 42: 227-234. https://doi.org/10.1053/jinf.2001.0836
  9. Dye C, Scheele S, Dolin P, Pathania V, Raviglione MC. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. JAMA. 1999. 282: 677-686. https://doi.org/10.1001/jama.282.7.677
  10. Dye C, Watt CJ, Bleed DM, Hosseini SM, Raviglione MC. Evolution of tuberculosis control and prospects for reducing tuberculosis incidence, prevalence, and deaths globally. JAMA. 2005. 293: 2767-2775. https://doi.org/10.1001/jama.293.22.2767
  11. Ge Y, Yoshiie K, Kuribayashi F, Lin M, Rikihisa Y. Anaplasma phagocytophilum inhibits human neutrophil apoptosis via upregulation of bfl-1, maintenance of mitochondrial membrane potential and prevention of caspase 3 activation. Cell Microbiol. 2005. 7: 29-38.
  12. Gross A, Terraza A, Ouahrani-Bettache S, Liautard JP, Dornand J. In vitro Brucella suis infection prevents the programmed cell death of human monocytic cells. Infect Immun. 2000. 68: 342-351. https://doi.org/10.1128/IAI.68.1.342-351.2000
  13. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004. 119: 753-766. https://doi.org/10.1016/j.cell.2004.11.038
  14. Gutierrez MG, Mishra BB, Jordao L, Elliott E, Anes E, Griffiths G. NF-kappa B activation controls phagolysosome fusionmediated killing of mycobacteria by macrophages. J Immunol. 2008. 181: 2651-2663.
  15. Kawamura I. Advances in understanding of the virulence mechanism of Mycobacterium tuberculosis. Nihon Hansenbyo Gakkai Zasshi 2008. 88: 219-224.
  16. Keane J, Remold HG, Kornfeld H. Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol. 2000. 164: 2016-2020.
  17. Kim SJ, Bai GH, Lee H, Kim HJ, Lew WJ, Park YK, Kim Y. Transmission of Mycobacterium tuberculosis among high school students in Korea. Int J Tuberc Lung Dis. 2001. 5: 824-830.
  18. Kremer K, Glynn JR, Lillebaek T, Niemann S, Kurepina NE, Kreiswirth BN, Bifani PJ, van Soolingen D. Definition of the Beijing/W lineage of Mycobacterium tuberculosis on the basis of genetic markers. J Clin Microbiol. 2004. 42: 4040-4049. https://doi.org/10.1128/JCM.42.9.4040-4049.2004
  19. Kurepina NE, Sreevatsan S, Plikaytis BB, Bifani PJ, Connell ND, Donnelly RJ, van Sooligen D, Musser JM, Kreiswirth BN. Characterization of the phylogenetic distribution and chromosomal insertion sites of five IS6110 elements in Mycobacterium tuberculosis: non-random integration in the dnaA-dnaN region. Tuber Lung Dis. 1998. 79: 31-42. https://doi.org/10.1054/tuld.1998.0003
  20. Liu PT, Stenger S, Li H, Wenzel L, Tan BH, Krutzik SR, Ochoa MT, Schauber J, Wu K, Meinken C, Kamen DL, Wagner M, Bals R, Steinmeyer A, Zugel U, Gallo RL, Eisenberg D, Hewison M, Hollis BW, Adams JS, Bloom BR, Modlin RL. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 2006. 311: 1770-1773. https://doi.org/10.1126/science.1123933
  21. MacMicking JD, North RJ, LaCourse R, Mudgett JS, Shah SK, Nathan CF. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc Natl Acad Sci U S A. 1997. 94: 5243-5248. https://doi.org/10.1073/pnas.94.10.5243
  22. Maiti D, Bhattacharyya A, Basu J. Lipoarabinomannan from Mycobacterium tuberculosis promotes macrophage survival by phosphorylating Bad through a phosphatidylinositol 3-kinase/Akt pathway. J Biol Chem. 2001. 276: 329-333.
  23. Oddo M, Renno T, Attinger A, Bakker T, MacDonald HR, Meylan PR. Fas ligand-induced apoptosis of infected human macrophages reduces the viability of intracellular Mycobacterium tuberculosis. J Immunol. 1998. 160: 5448-5454.
  24. Opferman JT, Korsmeyer SJ. Apoptosis in the development and maintenance of the immune system. Nat Immunol. 2003. 4: 410-415. https://doi.org/10.1038/ni0503-410
  25. Perskvist N, Long M, Stendahl O, Zheng L. Mycobacterium tuberculosis promotes apoptosis in human neutrophils by activating caspase-3 and altering expression of Bax/Bcl-xL via an oxygen-dependent pathway. J Immunol. 2002. 168: 6358-6365.
  26. Riendeau CJ, Kornfeld H. THP-1 cell apoptosis in response to Mycobacterial infection. Infect Immun. 2003. 71: 254-259. https://doi.org/10.1128/IAI.71.1.254-259.2003
  27. Simmons MJ, Fan G, Zong WX, Degenhardt K, White E, Gelinas C. Bfl-1/A1 functions, similar to Mcl-1, as a selective tBid and Bak antagonist. Oncogene 2008. 27: 1421-1428. https://doi.org/10.1038/sj.onc.1210771
  28. Sly LM, Hingley-Wilson SM, Reiner NE, McMaster WR. Survival of Mycobacterium tuberculosis in host macrophages involves resistance to apoptosis dependent upon induction of antiapoptotic Bcl-2 family member Mcl-1. J Immunol. 2003. 170: 430-437.
  29. Spira A, Carroll JD, Liu G, Aziz Z, Shah V, Kornfeld H, Keane J. Apoptosis genes in human alveolar macrophages infected with virulent or attenuated Mycobacterium tuberculosis: a pivotal role for tumor necrosis factor. Am J Respir Cell Mol Biol. 2003. 29: 545-551. https://doi.org/10.1165/rcmb.2002-0310OC
  30. Vergne I, Singh S, Roberts E, Kyei G, Master S, Harris J, de Haro S, Naylor J, Davis A, Delgado M, Deretic V. Autophagy in immune defense against Mycobacterium tuberculosis. Autophagy 2006. 2: 175-178.
  31. Zhang J, Jiang R, Takayama H, Tanaka Y. Survival of virulent Mycobacterium tuberculosis involves preventing apoptosis induced by Bcl-2 upregulation and release resulting from necrosis in J774 macrophages. Microbiol Immunol. 2005. 49: 845-852.