Truncated hemoglobin, HbN, is post-translationally modified in mycobacterium tuberculosis and modulates host-pathogen interactions during intracellular infection

Journal of Biological Chemistry

Volumn 288, Issue 41, 2013, Pages 29987-29999

  Arya, Swati ^a   Sethi, Deepti ^a   Singh, Sandeep ^a   Hade, Mangesh Dattu ^a   Singh, Vijender ^a   Raju, Preeti ^a   Chodisetti, Sathi Babu ^a   Verma, Deepshikha ^a   Varshney, Grish C ^a   Agrewala, Javed N ^a   Dikshit, Kanak L ^a  

^a INSTITUTE OF MICROBIAL TECHNOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED MACROPHAGES; HAZARDOUS ENVIRONMENT; HOST-PATHOGEN INTERACTIONS; INTRACELLULAR SURVIVAL; MYCOBACTERIUM TUBERCULOSIS; PERITONEAL MACROPHAGE; PRO-INFLAMMATORY CYTOKINES; TRUNCATED HEMOGLOBINS;

CYTOLOGY; HEMOGLOBIN; NITRIC OXIDE;

MACROPHAGES;

B7 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; CONCANAVALIN A; GLYCAN; HEMOGLOBIN; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; BACTERIAL CELL WALL; BACTERIAL INFECTION; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; CELL SURVIVAL; CELLULAR IMMUNITY; COLONY FORMING UNIT; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; GLYCOSYLATION; HOST PATHOGEN INTERACTION; IMMUNE SYSTEM; MACROPHAGE; MOUSE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NITROSATIVE STRESS; NONHUMAN; PERITONEUM MACROPHAGE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; SCANNING ELECTRON MICROSCOPY; WESTERN BLOTTING;

HEMOGLOBIN; HEMOGLOBIN MYOGLOBIN; HOST-PATHOGEN INTERACTIONS; MICROBIOLOGY; MYCOBACTERIUM TUBERCULOSIS; POST-TRANSLATIONAL MODIFICATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD80; ANTIGENS, CD86; BACTERIAL PROTEINS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL MEMBRANE; CELLS, CULTURED; CYTOKINES; FEMALE; FLOW CYTOMETRY; GLYCOSYLATION; HOST-PATHOGEN INTERACTIONS; HUMANS; INTRACELLULAR SPACE; MACROPHAGES; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MUTATION; MYCOBACTERIUM TUBERCULOSIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE HOMOLOGY, AMINO ACID; TRUNCATED HEMOGLOBINS;

EID: 84885670627     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.507301     Document Type: Article

References (49)

1. World Health Organization (2008) Tuberculosis Facts. World Health Organization, Geneva, Switzerland
2. Dye, C. (2006) Global epidemiology of tuberculosis. Lancet 367, 938-940
3. Manca, C., Tsenova, L., Barry, C. E., 3rd, Bergtold, A., Freeman, S., Haslett, P. A., Musser, J. M., Freedman, V. H., and Kaplan, G. (1999) Mycobacterium tuberculosis CDC1551 induces a more vigorous host response in vivo and in vitro, but is not more virulent than other clinical isolates. J. Immunol. 162, 6740-6746
4. Smith, I. (2003) Mycobacterium tuberculosis pathogenesis and molecular determinants of virulence. Clin. Microbiol. Rev. 16, 463-496
5. Homolka, S., Niemann, S., Russell, D. G., and Rohde, K. H. (2010) Functional genetic diversity among Mycobacterium tuberculosis complex clinical isolates. Delineation of conserved core and lineage-specific transcriptomes during intracellular survival. PLoS Pathog. 6, e1000988
6. Hershberg, R., Lipatov, M., Small, P. M., Sheffer, H., Niemann, S., Homolka, S., Roach, J. C., Kremer, K., Petrov, D. A., Feldman, M. W., and Gagneux, S. (2008) High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 6, e311
7. Koo, M. S., Subbian, S., and Kaplan, G. (2012) Strain specific transcriptional response in Mycobacterium tuberculosis infected macrophages. Cell Commun. Signal. 10, 2
8. Ordway, D., Henao-Tamayo, M., Harton, M., Palanisamy, G., Troudt, J., Shanley, C., Basaraba, R. J., and Orme, I. M. (2007) The Hypervirulent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation. J. Immunol. 179, 522-531
9. Couture, M., Yeh, S. R., Wittenberg, B. A., Wittenberg, J. B., Ouellet, Y., Rousseau, D. L., and Guertin, M. (1999) A cooperative oxygen-binding hemoglobin from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 96, 11223-11228
10. Pathania, R., Navani, N. K., Gardner, A. M., Gardner, P. R., and Dikshit, K. L. (2002) Nitric oxide scavenging and detoxification by the Mycobacterium tuberculosis haemoglobin, HbN in Escherichia coli. Mol. Microbiol. 45, 1303-1314
11. Pawaria, S., Rajamohan, G., Gambhir, V., Lama, A., Varshney, G. C., and Dikshit, K. L. (2007) Intracellular growth and survival of Salmonella enterica serovar Typhimurium carrying truncated hemoglobins of Mycobacterium tuberculosis. Microb. Pathog. 42, 119-128
12. Ouellet, H., Ouellet, Y., Richard, C., Labarre, M., Wittenberg, B., Wittenberg, J., and Guertin, M. (2002) Truncated hemoglobin HbN protects Mycobacterium bovis from nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 99, 5902-5907
13. Pawaria, S., Lama, A., Raje, M., and Dikshit, K. L. (2008) Responses of Mycobacterium tuberculosis hemoglobin promoters to in vitro and in vivo growth conditions. Appl. Environ. Microbiol. 74, 3512-3522
14. Garbe, T. R., Barathi, J., Barnini, S., Zhang, Y., Abou-Zeid, C., Tang, D., Mukherjee, R., and Young, D. B. (1994) Transformation of mycobacterial species using hygromycin resistance as selectable marker. Microbiology 140, 133-138
15. Cowley, S. C., and Av-Gay, Y. (2001) Monitoring promoter activity and protein localization in Mycobacterium spp. using green fluorescent protein. Gene 264, 225-231
16. Michell, S. L., Whelan, A. O., Wheeler, P. R., Panico, M., Easton, R. L., Etienne, A. T., Haslam, S. M., Dell, A., Morris, H. R., and Reason, A. J. (2003) The MPB83 antigen from Mycobacterium bovis contains O-linked mannose and (133)-mannobiose moieties. J. Biol. Chem. 278, 16423-16432
17. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
18. Fimereli, D., Tsirigos, K., Litou, Z., Liakopoulos, T., Bagos, P., and Hamodrakas, S. (2012) CW-PRED. A HMM-based method for the classification of cell wall-anchored proteins of Gram-positive bacteria. in Artificial Intelligence: Theories and Applications (Maglogiannis, I., Plagianakos, V., and Vlahavas, I., eds) pp. 285-290, Springer, Berlin
19. Cserzö, M., Wallin, E., Simon, I., von Heijne, G., and Elofsson, A. (1997) Prediction of transmembrane α-helices in prokaryotic membrane proteins. The dense alignment surface method. Protein. Eng. 10, 673-676
20. Herrmann, J. L., Delahay, R., Gallagher, A., Robertson, B., and Young, D. (2000) Analysis of post-translational modification of mycobacterial proteins using a cassette expression system. FEBS Lett. 473, 358-362
21. Lama, A., Pawaria, S., and Dikshit, K. L. (2006) Oxygen binding and NO scavenging properties of truncated hemoglobin, HbN, of Mycobacterium smegmatis. FEBS Lett. 580, 4031-4041
22. Karakousis, P. C., Bishai, W. R., and Dorman, S. E. (2004) Mycobacterium tuberculosis cell envelope lipids and the host immune response. Cell Microbiol. 6, 105-116
23. Mendelson, M., Walters, S., Smith, I., and Kaplan, G. (2005) Strain-specific mycobacterial lipids and the stimulation of protective immunity to tuberculosis. Tuberculosis 85, 407-413
24. Khan, N., Gowthaman, U., Pahari, S., and Agrewala, J. N. (2012) Manipulation of costimulatory molecules by intracellular pathogens. Veni, Vidi, Vici!! PLoS Pathog. 8, e1002676
25. Suvas, S., Singh, V., Sahdev, S., Vohra, H., and Agrewala, J. N. (2002) Distinct role of CD80 and CD86 in the regulation of the activation of B cell and B cell lymphoma. J. Biol. Chem. 277, 7766-7775
26. Schnappinger, D., Ehrt, S., Voskuil, M. I., Liu, Y., Mangan, J. A., Monahan, I. M., Dolganov, G., Efron, B., Butcher, P. D., Nathan, C., and Schoolnik, G. K. (2003) transcriptional adaptation of Mycobacterium tuberculosis within macrophages. Insights into the phagosomal environment. J. Exp. Med. 198, 693-704
27. Dutta, N. K., Mehra, S., Martinez, A. N., Alvarez, X., Renner, N. A., Morici, L. A., Pahar, B., Maclean, A. G., Lackner, A. A., and Kaushal, D. (2012) The stress-response factor SigH modulates the interaction between Mycobacterium tuberculosis and host phagocytes. PLoS One 7, e28958
28. Milani, M., Pesce, A., Ouellet, Y., Ascenzi, P., Guertin, M., and Bolognesi, M. (2001) Mycobacterium tuberculosis hemoglobin N displays a protein tunnel suited for O2 diffusion to the heme. EMBO J. 20, 3902-3909
29. Giffin, M. M., Modesti, L., Raab, R. W., Wayne, L. G., and Sohaskey, C. D. (2012) ald of Mycobacterium tuberculosis encodes both the alanine dehydrogenase and the putative glycine dehydrogenase. J. Bacteriol. 194, 1045-1054
30. Dahl, J. L., Wei, J., Moulder, J. W., Laal, S., and Friedman, R. L. (2001) Subcellular localization of the intracellular survival-enhancing Eis protein of Mycobacterium tuberculosis. Infect. Immun. 69, 4295-4302
31. Craney, A., Tahlan, K., Andrews, D., and Nodwell, J. (2011) Bacterial transmembrane proteins that lack N-terminal signal sequences. PLoS One 6, e19421
32. Borgese, N., Brambillasca, S., and Colombo, S. (2007) How tails guide tail-anchored proteins to their destinations. Curr. Opin. Cell Biol. 19, 368-375
33. Ragas, A., Roussel, L., Puzo, G., and Rivière, M. (2007) The Mycobacterium tuberculosis cell-surface glycoprotein apa as a potential adhesin to colonize target cells via the innate immune system pulmonary C-type lectin surfactant protein A. J. Biol. Chem. 282, 5133-5142
34. González-Zamorano, M., Mendoza-Hernández, G., Xolalpa, W., Parada, C., Vallecillo, A. J., Bigi, F., and Espitia, C. (2009) Mycobacterium tuberculosis glycoproteomics based on ConA-lectin affinity capture of mannosylated proteins. J. Proteome Res. 8, 721-733
35. Galagan, J. E., Minch, K., Peterson, M., Lyubetskaya, A., Azizi, E., Sweet, L., Gomes, A., Rustad, T., Dolganov, G., Glotova, I., Abeel, T., Mahwinney, C., Kennedy, A. D., Allard, R., Brabant, W., Krueger, A., Jaini, S., Honda, B., Yu, W. H., Hickey, M. J., Zucker, J., Garay, C., Weiner, B., Sisk, P., Stolte, C., Winkler, J. K., Van de Peer, Y., Iazzetti, P., Camacho, D., Dreyfuss, J., Liu, Y., Dorhoi, A., Mollenkopf, H. J., Drogaris, P., Lamontagne, J., Zhou, Y., Piquenot, J., Park, S. T., Raman, S., Kaufmann, S. H., Mohney, R. P., Chelsky, D., Moody, D. B., Sherman, D. R., and Schoolnik, G. K. (2013) The Mycobacterium tuberculosis regulatory network and hypoxia. Nature 499, 178-183
36. Singh, A., Crossman, D. K., Mai, D., Guidry, L., Voskuil, M. I., Renfrow, M. B., and Steyn, A. J. (2009) Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathog. 5, e1000545
37. Neyrolles, O., and Guilhot, C. (2011) Recent advances in deciphering the contribution of Mycobacterium tuberculosis lipids to pathogenesis. Tuberculosis 91, 187-195
38. Astarie-Dequeker, C., Le Guyader, L., Malaga, W., Seaphanh, F.-K., Chalut, C., Lopez, A., and Guilhot, C. (2009) Phthiocerol dimycocerosates of Mycobacterium tuberculosis participate in macrophage invasion by inducing changes in the organization of plasma membrane lipids. PLoS Pathog. 5, e1000289
39. Astarie-Dequeker, C., N'Diaye, E.-N., Le Cabec, V., Rittig, M. G., Prandi, J., and Maridonneau-Parini, I. (1999) The mannose receptor mediates uptake of pathogenic and nonpathogenic mycobacteria and bypasses bactericidal responses in human macrophages. Infect. Immun. 67, 469-477
40. Schlesinger, L. (1993) Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors. J. Immunol. 150, 2920-2930
41. Brightbill, H. D., Libraty, D. H., Krutzik, S. R., Yang, R. B., Belisle, J. T., Bleharski, J. R., Maitland, M., Norgard, M. V., Plevy, S. E., Smale, S. T., Brennan, P. J., Bloom, B. R., Godowski, P. J., and Modlin, R. L. (1999) Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 285, 732-736
42. Brennan, P. J. (2003) Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis 83, 91-97
43. Herbst, S., Schaible, U. E., and Schneider, B. E. (2011) Interferon γ activated macrophages kill mycobacteria by nitric oxide induced apoptosis. PLoS One 6, e19105
44. Ragno, S., Romano, M., Howell, S., Pappin, D. J., Jenner, P. J., and Colston, M. J. (2001) Changes in gene expression in macrophages infected with Mycobacterium tuberculosis. A combined transcriptomic and proteomic approach. Immunology 104, 99-108
45. Wei, J., Dahl, J. L., Moulder, J. W., Roberts, E. A., O'Gaora, P., Young, D. B., and Friedman, R. L. (2000) Identification of a Mycobacterium tuberculosis gene that enhances mycobacterial survival in macrophages. J. Bacteriol. 182, 377-384
46. Agrewala, J. N., Suvas, S., Verma, R. K., and Mishra, G. C. (1998) Differential effect of anti-B7-1 and anti-M150 antibodies in restricting the delivery of costimulatory signals from B cells and macrophages. J. Immunol. 160, 1067-1077
47. Balkhi, M. Y., Latchumanan, V. K., Singh, B., Sharma, P., and Natarajan, K. (2004) Cross-regulation of CD86 by CD80 differentially regulates T helper responses from Mycobacterium tuberculosis secretory antigen-activated dendritic cell subsets. J. Leukoc. Biol. 75, 874-883
48. Gao, Q., Kripke, K. E., Saldanha, A. J., Yan, W., Holmes, S., and Small, P. M. (2005) Gene expression diversity among Mycobacterium tuberculosis clinical isolates. Microbiology 151, 5-14
49. Lama, A., Pawaria, S., Bidon-Chanal, A., Anand, A., Gelpí, J. L., Arya, S., Martí, M., Estrin, D. A., Luque, F. J., and Dikshit, K. L. (2009) Role of Pre-A motif in nitric oxide scavenging by truncated hemoglobin, HbN, of Mycobacterium tuberculosis. J. Biol. Chem. 284, 14457-14468