Mycobacterium bovis BCG interferes with miR-3619-5p control of cathepsin S in the process of autophagy

Frontiers in Cellular and Infection Microbiology

Volumn 6, Issue MAR, 2016, Pages

  Pawar, Kamlesh ^a   Sharbati, Jutta ^a   Einspanier, Ralf ^a   Sharbati, Soroush ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Autophagy; Cathepsin S; MicroRNA; MiR 3619 5p; Mycobacterium bovis BCG; Phagocytosis

Indexed keywords

CATHEPSIN S; GAMMA INTERFERON; MICRORNA; MICRORNA 3619; RAB11 PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; CATHEPSIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MEMBRANE PROTEIN; MESSENGER RNA; RAB11FIP4 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ALGORITHM; ARTICLE; ATYPICAL MYCOBACTERIOSIS; AUTOPHAGY; COMPUTER MODEL; DOWN REGULATION; GENE SILENCING; IMMUNOFLUORESCENCE; INNATE IMMUNITY; MONOCYTIC LEUKEMIA; MRNA EXPRESSION ASSAY; MYCOBACTERIUM BOVIS BCG; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; UPREGULATION; WESTERN BLOTTING; GENETICS; HELA CELL LINE; HUMAN; MACROPHAGE; METABOLISM; MICROBIOLOGY; MYCOBACTERIUM BOVIS; PHAGOSOME; RNA INTERFERENCE; TUMOR CELL LINE;

AUTOPHAGY; CARRIER PROTEINS; CATHEPSINS; CELL LINE, TUMOR; HELA CELLS; HUMANS; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MACROPHAGES; MEMBRANE PROTEINS; MICRORNAS; MYCOBACTERIUM BOVIS; PHAGOSOMES; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 85006228141     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2016.00027     Document Type: Article

References (61)

1. Agerer, F., Waeckerle, S., and Hauck, C. R. (2004). Microscopic quantification of bacterial invasion by a novel antibody-independent staining method. J. Microbiol. Methods 59, 23-32. doi: 10.1016/j.mimet.2004.05.008.
2. Beers, C., Burich, A., Kleijmeer, M. J., Griffith, J. M., Wong, P., and Rudensky, A. Y. (2005). Cathepsin S controls MHC class II-mediated antigen presentation by epithelial cells in vivo. J. Immunol. 174, 1205-1212. doi: 10.4049/jimmunol.174.3.1205.
3. Behar, S. M., and Baehrecke, E. H. (2015). Tuberculosis: autophagy is not the answer. Nature 528, 482-483. doi: 10.1038/nature16324.
4. Billeskov, R., Grandal, M. V., Poulsen, C., Christensen, J. P., Winther, N., Vingsbo-Lundberg, C., et al. (2010). Difference in TB10.4 T-cell epitope recognition following immunization with recombinant TB10.4, BCG or infection with Mycobacterium tuberculosis. Eur. J. Immunol. 40, 1342-1354. doi: 10.1002/eji.200939830.
5. Blankenberg, D., Von Kuster, G., Coraor, N., Ananda, G., Lazarus, R., Mangan, M., et al. (2010). Galaxy: a web-based genome analysis tool for experimentalists. Curr. Protoc. Mol. Biol. 10, 11-21. doi: 10.1002/0471142727.mb1910s89.
6. Bucci, C., Thomsen, P., Nicoziani, P., McCarthy, J., and van Deurs, B. (2000). Rab7: a key to lysosome biogenesis. Mol. Biol. Cell 11, 467-480. doi: 10.1091/mbc.11.2.467.
7. Burgos-Portugal, J. A., Mitchell, H. M., Castano-Rodriguez, N., and Kaakoush, N. O. (2014). The role of autophagy in the intracellular survival of Campylobacter concisus. FEBS Open Bio 4, 301-309. doi: 10.1016/j.fob.2014.03.008.
8. Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., et al. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611-622. doi: 10.1373/clinchem.2008.112797.
9. Chen, K. L., Chang, W. S., Cheung, C. H., Lin, C. C., Huang, C. C., Yang, Y. N., et al. (2012). Targeting cathepsin S induces tumor cell autophagy via the EGFR-ERK signaling pathway. Cancer Lett. 317, 89-98. doi: 10.1016/j.canlet.2011.11.015.
10. Christoforidis, S., Miaczynska, M., Ashman, K., Wilm, M., Zhao, L., Yip, S. C., et al. (1999). Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat. Cell Biol. 1, 249-252. doi: 10.1038/12075.
11. Clemens, D. L., and Horwitz, M. A. (1995). Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J. Exp. Med. 181, 257-270. doi: 10.1084/jem.181.1.257.
12. Dennis, G. Jr., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C., et al. (2003). DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4:P3. doi: 10.1186/gb-2003-4-5-p3.
13. Driessen, C., Bryant, R. A., Lennon-Dumenil, A. M., Villadangos, J. A., Bryant, P. W., Shi, G. P., et al. (1999). Cathepsin S controls the trafficking and maturation of MHC class II molecules in dendritic cells. J. Cell Biol. 147, 775-790. doi: 10.1083/jcb.147.4.775.
14. Flannagan, R. S., Cosio, G., and Grinstein, S. (2009). Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat. Rev. Microbiol. 7, 355-366. doi: 10.1038/nrmicro2128.
15. Fratti, R. A., Backer, J. M., Gruenberg, J., Corvera, S., and Deretic, V. (2001). Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J. Cell Biol. 154, 631-644. doi: 10.1083/jcb.200106049.
16. Ghorpade, D. S., Leyland, R., Kurowska-Stolarska, M., Patil, S. A., and Balaji, K. N. (2012). MicroRNA-155 is required for Mycobacterium bovis BCG-mediated apoptosis of macrophages. Mol. Cell. Biol. 32, 2239-2253. doi: 10.1128/MCB.06597-11.
17. Gorvel, J. P., Chavrier, P., Zerial, M., and Gruenberg, J. (1991). rab5 controls early endosome fusion in vitro. Cell 64, 915-925. doi: 10.1016/0092-8674(91)90316-Q.
18. Gutierrez, M. G., Master, S. S., Singh, S. B., Taylor, G. A., Colombo, M. I., and Deretic, V. (2004). Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753-766. doi: 10.1016/j.cell.2004.11.038.
19. Hoeke, L., Sharbati, J., Pawar, K., Keller, A., Einspanier, R., and Sharbati, S. (2013). Intestinal Salmonella typhimurium infection leads to miR-29a induced caveolin 2 regulation. PLoS ONE 8:e67300. doi: 10.1371/journal.pone.0067300.
20. Houben, E. N., Walburger, A., Ferrari, G., Nguyen, L., Thompson, C. J., Miess, C., et al. (2009). Differential expression of a virulence factor in pathogenic and non-pathogenic mycobacteria. Mol. Microbiol. 72, 41-52. doi: 10.1111/j.1365-2958.2009.06612.x.
21. Huang, C. C., Chen, K. L., Cheung, C. H., and Chang, J. Y. (2013). Autophagy induced by cathepsin S inhibition induces early ROS production, oxidative DNA damage, and cell death via xanthine oxidase. Free Radic. Biol. Med. 65, 1473-1486. doi: 10.1016/j.freeradbiomed.2013.07.020.
22. Huang, C. C., Lee, C. C., Lin, H. H., Chen, M. C., Lin, C. C., and Chang, J. Y. (2015). Autophagy-regulated ROS from xanthine oxidase acts as an early effector for triggering late mitochondria-dependent apoptosis in cathepsin S-targeted tumor cells. PLoS ONE 10:e0128045. doi: 10.1371/journal.pone.0128045.
23. Jung, M., Shin, M. K., Jung, Y. K., and Yoo, H. S. (2015). Modulation of macrophage activities in proliferation, lysosome, and phagosome by the nonspecific immunostimulator, mica. PLoS ONE 10:e0117838. doi: 10.1371/journal.pone.0117838.
24. Kanehisa, M., and Goto, S. (2000). KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27-30. doi: 10.1093/nar/28.1.27.
25. Kanehisa, M., Goto, S., Sato, Y., Kawashima, M., Furumichi, M., and Tanabe, M. (2014). Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 42, D199-D205. doi: 10.1093/nar/gkt1076.
26. Kimmey, J. M., Huynh, J. P., Weiss, L. A., Park, S., Kambal, A., Debnath, J., et al. (2015). Unique role for ATG5 in neutrophil-mediated immunopathology during M. tuberculosis infection. Nature 528, 565-569. doi: 10.1038/nature16451.
27. Klionsky, D. J., Cuervo, A. M., and Seglen, P. O. (2007). Methods for monitoring autophagy from yeast to human. Autophagy 3, 181-206. doi: 10.4161/auto.3678.
28. Kruger, J., and Rehmsmeier, M. (2006). RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Res. 34, W451-W454. doi: 10.1093/nar/gkl243.
29. Kumar, R., Halder, P., Sahu, S. K., Kumar, M., Kumari, M., Jana, K., et al. (2012). Identification of a novel role of ESAT-6-dependent miR-155 induction during infection of macrophages with Mycobacterium tuberculosis. Cell. Microbiol. 14, 1620-1631. doi: 10.1111/j.1462-5822.2012.01827.x.
30. Kumar, R., Sahu, S. K., Kumar, M., Jana, K., Gupta, P., Gupta, U. D., et al. (2015). MicroRNA 17-5p regulates autophagy in Mycobacterium tuberculosis-infected macrophages by targeting Mcl-1 and STAT3. Cell. Microbiol. doi: 10.1111/cmi.12540. [Epub ahead of print].
31. Lee, B. Y., Jethwaney, D., Schilling, B., Clemens, D. L., Gibson, B. W., and Horwitz, M. A. (2010). The Mycobacterium bovis bacille Calmette-Guerin phagosome proteome. Mol. Cell. Proteomics 9, 32-53. doi: 10.1074/mcp. M900396-MCP200.
32. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262.
33. Ma, F., Xu, S., Liu, X., Zhang, Q., Xu, X., Liu, M., et al. (2011). The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-gamma. Nat. Immunol. 12, 861-869. doi: 10.1038/ni.2073.
34. Pan, L., Li, Y., Jia, L., Qin, Y., Qi, G., Cheng, J., et al. (2012). Cathepsin S deficiency results in abnormal accumulation of autophagosomes in macrophages and enhances Ang II-induced cardiac inflammation. PLoS ONE 7:e35315. doi: 10.1371/journal.pone.0035315.
35. Pawar, K., Hanisch, C., Palma Vera, S. E., Einspanier, R., and Sharbati, S. (2016). Down regulated lncRNA MEG3 eliminates mycobacteria in macrophages via autophagy. Sci. Rep. 6:19416. doi: 10.1038/srep19416.
36. Rajaram, M. V., Ni, B., Morris, J. D., Brooks, M. N., Carlson, T. K., Bakthavachalu, B., et al. (2011). Mycobacterium tuberculosis lipomannan blocks TNF biosynthesis by regulating macrophage MAPK-activated protein kinase 2 (MK2) and microRNA miR-125b. Proc. Natl. Acad. Sci. U.S.A. 108, 17408-17413. doi: 10.1073/pnas.1112660108.
37. Riese, R. J., Mitchell, R. N., Villadangos, J. A., Shi, G. P., Palmer, J. T., Karp, E. R., et al. (1998). Cathepsin S activity regulates antigen presentation and immunity. J. Clin. Invest. 101, 2351-2363. doi: 10.1172/JCI1158.
38. Saegusa, K., Ishimaru, N., Yanagi, K., Arakaki, R., Ogawa, K., Saito, I., et al. (2002). Cathepsin S inhibitor prevents autoantigen presentation and autoimmunity. J. Clin. Invest. 110, 361-369. doi: 10.1172/JCI0214682.
39. Sanjuan, M. A., Dillon, C. P., Tait, S. W., Moshiach, S., Dorsey, F., Connell, S., et al. (2007). Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450, 1253-1257. doi: 10.1038/nature06421.
40. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675. doi: 10.1038/nmeth.2089.
41. Sharbati, J., Hanisch, C., Pieper, R., Einspanier, R., and Sharbati, S. (2015). Small molecule and RNAi induced phenotype transition of expanded and primary colonic epithelial cells. Sci. Rep. 5:12681. doi: 10.1038/srep12681.
42. Sharbati, J., Lewin, A., Kutz-Lohroff, B., Kamal, E., Einspanier, R., and Sharbati, S. (2011). Integrated microRNA-mRNA-analysis of human monocyte derived macrophages upon Mycobacterium avium subsp. hominissuis infection. PLoS ONE 6:e20258. doi: 10.1371/journal.pone.0020258.
43. Sharbati, S., Friedlander, M. R., Sharbati, J., Hoeke, L., Chen, W., Keller, A., et al. (2010). Deciphering the porcine intestinal microRNA transcriptome. BMC Genomics 11:275. doi: 10.1186/1471-2164-11-275.
44. Sharbati, S., Sharbati, J., Hoeke, L., Bohmer, M., and Einspanier, R. (2012). Quantification and accurate normalisation of small RNAs through new custom RT-qPCR arrays demonstrates Salmonella-induced microRNAs in human monocytes. BMC Genomics 13:23. doi: 10.1186/1471-2164-13-23.
45. Sharbati-Tehrani, S., Kutz-Lohroff, B., Bergbauer, R., Scholven, J., and Einspanier, R. (2008). miR-Q: a novel quantitative RT-PCR approach for the expression profiling of small RNA molecules such as miRNAs in a complex sample. BMC Mol. Biol. 9:34. doi: 10.1186/1471-2199-9-34.
46. Sharbati-Tehrani, S., Meister, B., Appel, B., and Lewin, A. (2004). The porin MspA from Mycobacterium smegmatis improves growth of Mycobacterium bovis BCG. Int. J. Med. Microbiol. 294, 235-245. doi: 10.1016/j.ijmm.2004.02.001.
47. Stewart, G. R., Patel, J., Robertson, B. D., Rae, A., and Young, D. B. (2005). Mycobacterial mutants with defective control of phagosomal acidification. PLoS Pathog. 1:e33. doi: 10.1371/journal.ppat.0010033.
48. Sturgill-Koszycki, S., Schlesinger, P. H., Chakraborty, P., Haddix, P. L., Collins, H. L., Fok, A. K., et al. (1994). Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263, 678-681. doi: 10.1126/science.8303277.
49. Sun, J., Deghmane, A. E., Soualhine, H., Hong, T., Bucci, C., Solodkin, A., et al. (2007). Mycobacterium bovis BCG disrupts the interaction of Rab7 with RILP contributing to inhibition of phagosome maturation. J. Leukoc. Biol. 82, 1437-1445. doi: 10.1189/jlb.0507289.
50. Tanida, I., Yamaji, T., Ueno, T., Ishiura, S., Kominami, E., and Hanada, K. (2008). Consideration about negative controls for LC3 and expression vectors for four colored fluorescent protein-LC3 negative controls. Autophagy 4, 131-134. doi: 10.4161/auto.5233.
51. Tili, E., Michaille, J. J., Cimino, A., Costinean, S., Dumitru, C. D., Adair, B., et al. (2007). Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J. Immunol. 179, 5082-5089. doi: 10.4049/jimmunol.179.8.5082.
52. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., et al. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3:RESEARCH0034. doi: 10.1186/gb-2002-3-7-research0034.
53. Vejnar, C. E., and Zdobnov, E. M. (2012). MiRmap: comprehensive prediction of microRNA target repression strength. Nucleic Acids Res. 40, 11673-11683. doi: 10.1093/nar/gks901.
54. Vergne, I., Chua, J., Singh, S. B., and Deretic, V. (2004). Cell biology of mycobacterium tuberculosis phagosome. Annu. Rev. Cell Dev. Biol. 20, 367-394. doi: 10.1146/annurev.cellbio.20.010403.114015.
55. Vieira, O. V., Bucci, C., Harrison, R. E., Trimble, W. S., Lanzetti, L., Gruenberg, J., et al. (2003). Modulation of Rab5 and Rab7 recruitment to phagosomes by phosphatidylinositol 3-kinase. Mol. Cell. Biol. 23, 2501-2514. doi: 10.1128/MCB.23.7.2501-2514.2003.
56. Walburger, A., Koul, A., Ferrari, G., Nguyen, L., Prescianotto-Baschong, C., Huygen, K., et al. (2004). Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science 304, 1800-1804. doi: 10.1126/science.1099384.
57. Wang, J., Yang, K., Zhou, L., Minhaowu, Wu, Y., Zhu, M., et al. (2013). MicroRNA-155 promotes autophagy to eliminate intracellular mycobacteria by targeting Rheb. PLoS Pathog. 9:e1003697. doi: 10.1371/journal.ppat.1003697.
58. Xu, S., Cooper, A., Sturgill-Koszycki, S., van Heyningen, T., Chatterjee, D., Orme, I., et al. (1994). Intracellular trafficking in Mycobacterium tuberculosis and Mycobacterium avium-infected macrophages. J. Immunol. 153, 2568-2578.
59. Zhang, L., Wang, H., Xu, J., Zhu, J., and Ding, K. (2014). Inhibition of cathepsin S induces autophagy and apoptosis in human glioblastoma cell lines through ROS-mediated PI3K/AKT/mTOR/p70S6K and JNK signaling pathways. Toxicol. Lett. 228, 248-259. doi: 10.1016/j.toxlet.2014.05.015.
60. Zhou, J., Tan, S. H., Nicolas, V., Bauvy, C., Yang, N. D., Zhang, J., et al. (2013). Activation of lysosomal function in the course of autophagy via mTORC1 suppression and autophagosome-lysosome fusion. Cell Res. 23, 508-523. doi: 10.1038/cr.2013.11.
61. Zur Bruegge, J., Hanisch, C., Einspanier, R., Alter, T., Golz, G., and Sharbati, S. (2014). Arcobacter butzleri induces a pro-inflammatory response in THP-1 derived macrophages and has limited ability for intracellular survival. Int. J. Med. Microbiol. 304, 1209-1217. doi: 10.1016/j.ijmm.2014.08.017.