Suppression of dendritic cell-mediated responses by genes in calcium and cysteine protease pathways during Mycobacterium tuberculosis infection

Journal of Biological Chemistry

Volumn 287, Issue 14, 2012, Pages 11108-11121

  Singhal, Jhalak ^a   Agrawal, Neha ^a,d   Vashishta, Mohit ^a   Priya, N Gayatri ^b   Tiwari, Brijendra K ^c   Singh, Yogendra ^c   Raman, Rajagopal ^b   Natarajan, Krishnamurthy ^a  

^a UNIVERSITY OF DELHI   (India)

^b UNIVERSITY OF DELHI   (India)

^c CSIR INSTITUTE OF GENOMICS AND INTEGRATIVE BIOLOGY   (India)

^d INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE APPROACH; AUTOPHAGY; COSTIMULATORY MOLECULES; CYSTEINE PROTEASE; DENDRITIC CELLS; DRUG RESISTANCE; IMMUNE RESPONSE; INTRACELLULAR SURVIVAL; M. TUBERCULOSIS; MULTIPLE RESPONSE; MYCOBACTERIUM TUBERCULOSIS; OXIDATIVE BURSTS; SURFACE DENSITY; T CELLS;

AMINO ACIDS; ANTIGENS; CELLS; IMMUNOLOGY; LIBRARIES; TRANSCRIPTION FACTORS; TUBES (COMPONENTS);

GENE THERAPY;

B7 ANTIGEN; CALPAIN; CD40 ANTIGEN; CD86 ANTIGEN; CYSTEINE PROTEINASE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 12P40; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; AUTOPHAGY; BACTERIAL LOAD; BACTERIAL SURVIVAL; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; FEMALE; GENE; GENE IDENTIFICATION; GENE LIBRARY; GENE SILENCING; GENE TARGETING; GENETIC TRANSFECTION; IMMUNOMODULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN SYNTHESIS REGULATION; RNA INTERFERENCE; SENTRIN SPECIFIC PEPTIDASE 8 GENE; SNF RELATED KINASE GENE; TH1 CELL; TH2 CELL; TRANSCRIPTION REGULATION; TUBERCULOSIS; UBIQUITIN SPECIFIC PEPTIDASE 25 GENE;

ANIMALS; AUTOPHAGY; CALCIUM; CALMODULIN; CELL ADHESION MOLECULES; CYSTEINE PROTEASES; DENDRITIC CELLS; FEMALE; GENE KNOCKDOWN TECHNIQUES; IMMUNITY; INTERLEUKIN-12 SUBUNIT P40; MICE; MYCOBACTERIUM TUBERCULOSIS; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST; RNA, SMALL INTERFERING; SUPEROXIDE DISMUTASE; T-LYMPHOCYTES; TOLL-LIKE RECEPTOR 2;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS;

EID: 84859487856     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.300319     Document Type: Article

References (60)

1. World Health Organization (2009) World Health Organization Fact Sheet, Geneva, Switzerland
2. Young, D. (2009) Animal models of tuberculosis. Eur. J. Immunol. 39, 2011-2014
3. Ottenhoff, T. H. (2009) Overcoming the global crisis: "Yes, we can," but also for TB . . . ? Eur. J. Immunol. 39, 2014-2020
4. Fine, P. E. (1995) Variation in protection by BCG: Implications of and for heterologous immunity. Lancet 346, 1339-1345
5. Hess, J., Schaible, U., Raupach, B., and Kaufmann, S. H. (2000) Exploiting the immune system: Toward new vaccines against intracellular bacteria. Adv. Immunol. 75, 1-88 (Pubitemid 30436841)
6. Manabe, Y. C., and Bishai, W. R. (2000) Latent Mycobacterium tuberculosis persistence, patience, and winning by waiting. Nat. Med. 6, 1327-1329 (Pubitemid 32001014)
7. Foote, S. (1999) Mediating immunity to mycobacteria. Nat. Genet. 21, 345-346
8. Flynn, J. L., and Chan, J. (2001) Immunology of tuberculosis. Annu. Rev. Immunol. 19, 93-129 (Pubitemid 32368031)
9. Ganesan, A. K., Ho, H., Bodemann, B., Petersen, S., Aruri, J., Koshy, S., Richardson, Z., Le, L. Q., Krasieva, T., Roth, M. G., Farmer, P., and White, M. A. (2008) Genome-wide siRNA-based functional genomics of pigmentation identifies novel genes and pathways that impact melanogenesis in human cells. PLoS Genet. 4, e1000298
10. Luo, J., Emanuele, M. J., Li, D., Creighton, C. J., Schlabach, M. R., Westbrook, T. F., Wong, K. K., and Elledge, S. J. (2009) A genome-wide RNAi screen identifies multiple synthetic lethal interactions with the Ras oncogene. Cell 137, 835-848
11. Cullen, L. M., and Arndt, G. M. (2005) Genome-wide screening for gene function using RNAi in mammalian cells. Immunol. Cell Biol. 83, 217-223 (Pubitemid 40799549)
12. Steinman, R. M. (1999) Dendritic cells in Fundamental Immunology (William E. Paul, ed) pp. E47-72, Lippincott-Raven Publishers
13. Banchereau, J., and Steinman, R. M. (1998) Dendritic cells and the control of immunity. Nature 392, 245-252 (Pubitemid 28155090)
14. Reis e Sousa, C. (2001) Dendritic cells as sensors of infection. Immunity 14, 495-498
15. + T cell response to Mycobacterium tuberculosis and exacerbates the outcome of infection. J. Immunol. 175, 3268-3272
16. Pecora, N. D., Fulton, S. A., Reba, S. M., Drage, M. G., Simmons, D. P., Urankar-Nagy, N. J., Boom, W. H., and Harding, C. V. (2009) Mycobacterium bovis BCG decreases MHC-II expression in vivo on murine lung macrophages and dendritic cells during aerosol infection. Cell. Immunol. 254, 94-104
17. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Hoshino, K., Wagner, H., Takeda, K., and Akira, S. (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408, 740-745 (Pubitemid 32015992)
18. Bodnar, K. A., Serbina, N. V., and Flynn, J. L. (2001) Fate of Mycobacterium tuberculosis within murine dendritic cells. Infect. Immun. 69, 800-809 (Pubitemid 32109542)
19. Noble, A., Truman, J. P., Vyas, B., Vukmanovic-Stejic, M., Hirst, W. J., and Kemeny, D. M. (2000) The balance of protein kinase C and calcium signaling directs T cell subset development. J. Immunol. 164, 1807-1813 (Pubitemid 30108733)
20. 2+ signaling and phagosome maturation in human macrophages via specific inhibition of sphingosine kinase. J. Immunol. 170, 2811-2815
21. Hsing, L. C., and Rudensky, A. Y. (2005) The lysosomal cysteine proteases in MHC class II antigen presentation. Immunol. Rev. 207, 229-241 (Pubitemid 41415021)
22. Gupta, S., Salam, N., Srivastava, V., Singla, R., Behera, D., Khayyam, K. U., Korde, R., Malhotra, P., Saxena, R., and Natarajan, K. (2009) Voltage-gated calcium channels negatively regulate protective immunity to Mycobacterium tuberculosis. PLoS One 4, e5305
23. Gupta, D., Sharma, S., Singhal, J., Satsangi, A. T., Antony, C., and Natarajan, K. (2010) Suppression of TLR2-induced IL-12, reactive oxygen species, and inducible nitric oxide synthase expression by Mycobacterium tuberculosis antigens expressed inside macrophages during the course of infection. J. Immunol. 184, 5444-5455
24. Srivastava, V., Manchanda, M., Gupta, S., Singla, R., Behera, D., Das, G., and Natarajan, K. (2009) Toll-like receptor 2 and DC-SIGNR1 differentially regulate suppressors of cytokine signaling 1 in dendritic cells during Mycobacterium tuberculosis infection. J. Biol. Chem. 284, 25532-25541
25. Srivastava, V., Vashishta, M., Gupta, S., Singla, R., Singla, N., Behera, D., and Natarajan, K. (2011) Suppressors of cytokine signaling inhibit effector T cell responses during Mycobacterium tuberculosis infection. Immunol. Cell Biol. 89, 786-791
26. Sinha, A., Singh, A., Satchidanandam, V., and Natarajan, K. (2006) Impaired generation of reactive oxygen species during differentiation of dendritic cells (DCs) by Mycobacterium tuberculosis secretory antigen (MTSA) and subsequent activation of MTSA-DCs by mycobacteria results in increased intracellular survival. J. Immunol. 177, 468-478 (Pubitemid 43939160)
27. Nguyen, A., Chen, P., and Cai, H. (2004) Role of CaMKII in hydrogen peroxide activation of ERK1/2, p38 MAPK, HSP27, and actin reorganization in endothelial cells. FEBS Lett. 572, 307-313 (Pubitemid 39092554)
28. Yan, B., Zemskova, M., Holder, S., Chin, V., Kraft, A., Koskinen, P. J., and Lilly, M. (2003) The PIM-2 kinase phosphorylates BAD on serine 112 and reverses BAD-induced cell death. J. Biol. Chem. 278, 45358-45367 (Pubitemid 37432672)
29. Jaleel, M., McBride, A., Lizcano, J. M., Deak, M., Toth, R., Morrice, N. A., and Alessi, D. R. (2005) Identification of the sucrose non-fermenting related kinase SNRK, as a novel LKB1 substrate. FEBS Lett. 579, 1417-1423 (Pubitemid 40289190)
30. Lee, J. W., Park, S., Takahashi, Y., and Wang, H. G. (2010) The association of AMPK with ULK1 regulates autophagy. PLoS One 5, e15394
31. Snapinn, K. W., Larson, E. B., Kawakami, H., Ujike, H., Borenstein, A. R., Izumi, Y., Kaji, R., Maruyama, H., Mata, I. F., Morino, H., Oda, M., Tsuang, D. W., Yearout, D., Edwards, K. L., and Zabetian, C. P. (2011) The UCHL1 S18Y polymorphism and Parkinson disease in a Japanese population. Parkinsonism Relat. Disord. 17, 473-475
32. Gawenda, J., Traub, F., Lück, H. J., Kreipe, H., and von Wasielewski, R. (2007) Legumain expression as a prognostic factor in breast cancer patients. Breast Cancer Res. Treat. 102, 1-6 (Pubitemid 46294961)
33. Barrett, A. J., and Kirschke, H. (1981) Cathepsin B, cathepsin H, and cathepsin L. Methods Enzymol. 80, 535-561
34. Gan-Erdene, T., Nagamalleswari, K., Yin, L., Wu, K., Pan, Z. Q., and Wilkinson, K. D. (2003) Identification and characterization of DEN1, a deneddylase of the ULP family. J. Biol. Chem. 278, 28892-28900 (Pubitemid 36939149)
35. Koh, K. W., Lehming, N., and Seah, G. T. (2009) Degradation-resistant protein domains limit host cell processing and immune detection of mycobacteria. Mol. Immunol. 46, 1312-1318
36. van Kooyk, Y., and Geijtenbeek, T. B. (2003) DC-SIGN: Escape mechanism for pathogens. Nat. Rev. Immunol. 3, 697-709
37. Yadav, U. C., Naura, A. S., Aguilera-Aguirre, L., Ramana, K. V., Boldogh, I., Sur, S., Boulares, H. A., and Srivastava, S. K. (2009) Aldose reductase inhibition suppresses the expression of Th2 cytokines and airway inflammation in ovalbumin-induced asthma in mice. J. Immunol. 183, 4723-4732
38. Virgin, H. W., and Levine, B. (2009) Autophagy genes in immunity. Nat. Immunol. 10, 461-470
39. Deretic, V., and Levine, B. (2009) Autophagy, immunity, and microbial adaptations. Cell Host Microbe 5, 527-549
40. Jagannath, C., Lindsey, D. R., Dhandayuthapani, S., Xu, Y., Hunter, R. L., Jr., and Eissa, N. T. (2009) Autophagy enhances the efficacy of BCG vaccine by increasing peptide presentation in mouse dendritic cells. Nat. Med. 15, 267-276
41. Koul, A., Herget, T., Klebl, B., and Ullrich, A. (2004) Interplay between mycobacteria and host signaling pathways. Nat. Rev. Microbiol. 2, 189-202 (Pubitemid 39490082)
42. Noss, E. H., Pai, R. K., Sellati, T. J., Radolf, J. D., Belisle, J., Golenbock, D. T., Boom, W. H., and Harding, C. V. (2001) Toll-like receptor 2-dependent inhibition of macrophage class IIMHCexpression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J. Immunol. 167, 910-918 (Pubitemid 32660847)
43. Latchumanan, V. K., Singh, B., Sharma, P., and Natarajan, K. (2002) Mycobacterium tuberculosis antigens induce the differentiation of dendritic cells from bone marrow. J. Immunol. 169, 6856-6864 (Pubitemid 36899271)
44. Salam, N., Gupta, S., Sharma, S., Pahujani, S., Sinha, A., Saxena, R. K., and Natarajan, K. (2008) Protective immunity to Mycobacterium tuberculosis infection by chemokine and cytokine conditioned CFP-10 differentiated dendritic cells. PLoS One. 3, e2869
45. Moffat, J., and Sabatini, D. M. (2006) Building mammalian signaling pathways with RNAi screens. Nat. Rev. Mol. Cell Biol. 7, 177-187
46. Ito, M., Kawano, K., Miyagishi, M., and Taira, K. (2005) Genome-wide application of RNAi to the discovery of potential drug targets. FEBS Lett. 579, 5988-5995 (Pubitemid 41484144)
47. Ovcharenko, D., Kelnar, K., Johnson, C., Leng, N., and Brown, D. (2007) Genome-scale microRNA and small interfering RNA screens identify small RNA modulators of TRAIL-induced apoptosis pathway. Cancer Res. 67, 10782-10788 (Pubitemid 350145906)
48. Alenzi, F. Q. (2004) Links between apoptosis, proliferation and the cell cycle. Br. J. Biomed. Sci. 61, 99-102
49. Su, B., and Karin, M. (1996) Mitogen-activated protein kinase cascades and regulation of gene expression. Curr. Opin. Immunol. 8, 402-411 (Pubitemid 26229663)
50. Li, S., Wang, L., Berman, M. A., Zhang, Y., and Dorf, M. E. (2006) RNAi screen in mouse astrocytes identifies phosphatases that regulate NF-κB signaling. Mol. Cell 24, 497-509 (Pubitemid 350284222)
51. Kittler, R., Pelletier, L., Heninger, A. K., Slabicki, M., Theis, M., Miroslaw, L., Poser, I., Lawo, S., Grabner, H., Kozak, K., Wagner, J., Surendranath, V., Richter, C., Bowen, W., Jackson, A. L., Habermann, B., Hyman, A. A., and Buchholz, F. (2007) Genome-scale RNAi profiling of cell division in human tissue culture cells. Nat. Cell Biol. 9, 1401-1412 (Pubitemid 350201753)
52. Kumar, D., Nath, L., Kamal, M. A., Varshney, A., Jain, A., Singh, S., and Rao, K. V. (2010) Genome-wide analysis of the host intracellular network that regulates survival of Mycobacterium tuberculosis. Cell 140, 731-743
53. Connolly, S. F., and Kusner, D. J. (2007) The regulation of dendritic cell function by calcium signaling and its inhibition by microbial pathogens. Immunol. Res. 39, 115-127 (Pubitemid 47574879)
54. Fox, C. J., Hammerman, P. S., Cinalli, R. M., Master, S. R., Chodosh, L. A., and Thompson, C. B. (2003) The serine/threonine kinase Pim-2 is a transcriptionally regulated apoptotic inhibitor. Genes Dev. 17, 1841-1854 (Pubitemid 36944562)
55. Agrawal-Singh, S., Koschmieder, S., Gelsing, S., Stocking, C., Stehling, M., Thiede, C., Thoennissen, N. H., Köhler, G., Valk, P. J., Delwel, R., Mills, K., Bäumer, N., Tickenbrock, L., Hansen, K., Berdel, W. E., Müller-Tidow, C., and Serve, H. (2010) Pim2 cooperates with PML-RARα to induce acute myeloid leukemia in a bone marrow transplantation model. Blood 115, 4507-4516
56. Lin, P. T., Gleeson, J. G., Corbo, J. C., Flanagan, L., and Walsh, C. A. (2000) DCAMKL1 encodes a protein kinase with homology to doublecortin that regulates microtubule polymerization. J. Neurosci. 20, 9152-9161 (Pubitemid 32042918)
57. Pramanik, K., Chun, C. Z., Garnaas, M. K., Samant, G. V., Li, K., Horswill, M. A., North, P. E., and Ramchandran, R. (2009) Dusp-5 and Snrk-1 coordinately function during vascular development and disease. Blood 113, 1184-1191
58. Krausz, C., Degl'Innocenti, S., Nuti, F., Morelli, A., Felici, F., Sansone, M., Varriale, G., and Forti, G. (2006) Natural transmission of USP9Y gene mutations: A new perspective on the role of AZFa genes in male fertility. Hum. Mol. Genet. 15, 2673-2681
59. Kaufmann, S. H., and Schaible, U. E. (2003) A dangerous liaison between two major killers: Mycobacterium tuberculosis and HIV target dendritic cells through DC-SIGN. J. Exp. Med. 197, 1-5 (Pubitemid 36110252)
60. Soucy, T. A., Smith, P. G., Milhollen, M. A., Berger, A. J., Gavin, J. M., Adhikari, S., Brownell, J. E., Burke, K. E., Cardin, D. P., Critchley, S., Cullis, C. A., Doucette, A., Garnsey, J. J., Gaulin, J. L., Gershman, R. E., Lublinsky, A. R., McDonald, A., Mizutani, H., Narayanan, U., Olhava, E. J., Peluso, S., Rezaei, M., Sintchak, M. D., Talreja, T., Thomas, M. P., Traore, T., Vyskocil, S., Weatherhead, G. S., Yu, J., Zhang, J., Dick, L. R., Claiborne, C. F., Rolfe, M., Bolen, J. B., and Langston, S. P. (2009) An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 458, 732-736