Mycobacterium leprae activates toll-like receptor-4 signaling and expression on macrophages depending on previous bacillus Calmette-Guerin vaccination

Frontiers in Cellular and Infection Microbiology

Volumn 6, Issue JUL, 2016, Pages

  Polycarpou, Anastasia ^a   Holland, Martin J ^a   Karageorgiou, Ioannis ^a   Eddaoudi, Ayad ^b   Walker, Stephen L ^a   Willcocks, Sam ^a   Lockwood, Diana N J ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Bacillus Calmette Guerin; Leprosy; Macrophages; Mycobacterium leprae; Signaling; Toll like receptor 4; Trained immunity

Indexed keywords

ALKALINE PHOSPHATASE; CD14 ANTIGEN; CD16 ANTIGEN; CD68 ANTIGEN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 6; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; PROTEIN MD 2; RECOMBINANT COLONY STIMULATING FACTOR 1; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; BCG VACCINE; CYTOKINE; TLR4 PROTEIN, HUMAN;

ARTICLE; BCG VACCINATION; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOMODULATION; LEPROSY; MACROPHAGE ACTIVATION; MONOCYTE CULTURE; MYCOBACTERIUM LEPRAE; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BIOSYNTHESIS; DRUG EFFECTS; IMMUNOLOGY; MACROPHAGE; METABOLISM; MICROBIOLOGY; MONOCYTE; MOUSE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; BCG VACCINE; CELL DIFFERENTIATION; CYTOKINES; HEK293 CELLS; HUMANS; LEPROSY; MACROPHAGES; MICE; MONOCYTES; MYCOBACTERIUM LEPRAE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 85006184293     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2016.00072     Document Type: Article

References (57)

1. Andersen, J., VanScoy, S., Cheng, T. F., Gomez, D., and Reich, N. C. (2008). IRF-3-dependent and augmented target genes during viral infection. Genes Immun. 9, 168-175. doi: 10.1038/sj.gene.6364449
2. Arbour, N. C., Lorenz, E., Schutte, B. C., Zabner, J., Kline, J. N., Jones, M., et al. (2000). TLR4 mutations are associated with endotoxin hyporesponsiveness in humans. Nat. Genet. 25, 187-191. doi: 10.1038/76048
3. Basu, J., Shin, D. M., and Jo, E. K. (2012). Mycobacterial signaling through toll-like receptors. Front. Cell. Infect. Microbiol. 2:145. doi: 10.3389/fcimb.2012.00145
4. Bochud, P. Y., Sinsimer, D., Aderem, A., Siddiqui, M. R., Saunderson, P., Britton, S., et al. (2009). Polymorphisms in Toll-like receptor 4 (TLR4) are associated with protection against leprosy. Eur. J. Clin. Microbiol. Infect. Dis. 28, 1055-1065. doi: 10.1007/s10096-009-0746-0
5. Bosisio, D., Polentarutti, N., Sironi, M., Bernasconi, S., Miyake, K., Webb, G. R., et al. (2002). Stimulation of toll-like receptor 4 expression in human mononuclear phagocytes by interferon-gamma: a molecular basis for priming and synergism with bacterial lipopolysaccharide. Blood 99, 3427-3431. doi: 10.1182/blood.V99.9.3427
6. Britton, W. J., and Lockwood, D. N. (2004). Leprosy. Lancet 363, 1209-1219. doi: 10.1016/S0140-6736(04)15952-7
7. Bulut, Y., Michelsen, K. S., Hayrapetian, L., Naiki, Y., Spallek, R., Singh, M., et al. (2005). Mycobacterium tuberculosis heat shock proteins use diverse Toll-like receptor pathways to activate pro-inflammatory signals. J. Biol. Chem. 280, 20961-20967. doi: 10.1074/jbc.M411379200
8. Burguiere, A., Hitchen, P. G., Dover, L. G., Kremer, L., Ridell, M., Alexander, D. C., et al. (2005). LosA, a key glycosyltransferase involved in the biosynthesis of a novel family of glycosylated acyltrehalose lipooligosaccharides from Mycobacterium marinum. J. Biol. Chem. 280, 42124-42133. doi: 10.1074/jbc.M507500200
9. Byun, E. H., Kim, W. S., Kim, J. S., Won, C. J., Choi, H. G., Kim, H. J., et al. (2012). Mycobacterium paratuberculosis CobT activates dendritic cells via engagement of toll-like receptor 4 resulting in Th1 cell expansion. J. Biol. Chem. 287, 38609-38624. doi: 10.1074/jbc.M112.391060
10. Cehovin, A., Coates, A. R., Hu, Y., Riffo-Vasquez, Y., Tormay, P., Botanch, C., et al. (2010). Comparison of the moonlighting actions of the two highly homologous chaperonin 60 proteins of Mycobacterium tuberculosis. Infect. Immun. 78, 3196-3206. doi: 10.1128/IAI.01379-09
11. Chang, J. S., Huggett, J. F., Dheda, K., Kim, L. U., Zumla, A., and Rook, G. A. (2006). Myobacterium tuberculosis induces selective up-regulation of TLRs in the mononuclear leukocytes of patients with active pulmonary tuberculosis. J. Immunol. 176, 3010-3018. doi: 10.4049/jimmunol.176.5.3010
12. Choi, A., Legaspi, A., Hou, W., and Modlin, R. (2013). Identification of PE/PPE epitopes of Mycobacterium leprae recognised by peripheral blood mononuclear cells in leprosy (P3332). J. Immunol. 190, 134.19.
13. Cole, S. T., Eiglmeier, K., Parkhill, J., James, K. D., Thomson, N. R., Wheeler, P. R., et al. (2001). Massive gene decay in the leprosy bacillus. Nature 409, 1007-1011. doi: 10.1038/35059006
14. Covert, M. W., Leung, T. H., Gaston, J. E., and Baltimore, D. (2005). Achieving stability of lipopolysaccharide-induced NF-kappaB activation. Science 309, 1854-1857. doi: 10.1126/science.1112304
15. Daffe, M., McNeil, M., and Brennan, P. J. (1991). Novel type-specific lipooligosaccharides from Mycobacterium tuberculosis. Biochemistry 30, 378-388. doi: 10.1021/bi00216a011
16. Figueroa, L., Xiong, Y., Song, C., Piao, W., Vogel, S. N., and Medvedev, A. E. (2012). The Asp299Gly polymorphism alters TLR4 signaling by interfering with recruitment of MyD88 and TRIF. J. Immunol. 188, 4506-4515. doi: 10.4049/jimmunol.1200202
17. Fremond, C. M., Nicolle, D. M., Torres, D. S., and Quesniaux, V. F. (2003). Control of Mycobacterium bovis BCG infection with increased inflammation in TLR4-deficient mice. Microbes Infect. 5, 1070-1081. doi: 10.1016/j.micinf.2003.06.001
18. Gaydos, L. J., Wang, W., and Strome, S. (2014). Gene repression. H3K27me and PRC2 transmit a memory of repression across generations and during development. Science 345, 1515-1518. doi: 10.1126/science.1255023
19. Gilleron, M., Vercauteren, J., and Puzo, G. (1993). Lipooligosaccharidic antigen containing a novel C4-branched 3,6-dideoxy-alpha-hexopyranose typifies Mycobacterium gastri. J. Biol. Chem. 268, 3168-3179.
20. Godal, T., Myklestad, B., Samuel, D. R., and Myrvang, B. (1971). Characterization of the cellular immune defect in lepromatous leprosy: a specific lack of circulating Mycobacterium leprae-reactive lymphocytes. Clin. Exp. Immunol. 9, 821-831.
21. Hart, B. E., and Tapping, R. I. (2012). Genetic Diversity of Toll-Like receptors and immunity to M. leprae Infection. J. Trop. Med. 2012:415057. doi: 10.1155/2012/415057
22. Hoebe, K., Du, X., Georgel, P., Janssen, E., Tabeta, K., Kim, S. O., et al. (2003). Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 424, 743-748. doi: 10.1038/nature01889
23. Hunter, S. W., Murphy, R. C., Clay, K., Goren, M. B., and Brennan, P. J. (1983). Trehalose-containing lipooligosaccharides. A new class of species-specific antigens from Mycobacterium. J. Biol. Chem. 258, 10481-10487.
24. Jung, I. D., Jeong, S. K., Lee, C. M., Noh, K. T., Heo, D. R., Shin, Y. K., et al. (2011). Enhanced efficacy of therapeutic cancer vaccines produced by co-treatment with Mycobacterium tuberculosis heparin-binding hemagglutinin, a novel TLR4 agonist. Cancer Res. 71, 2858-2870. doi: 10.1158/0008-5472.CAN-10-3487
25. Jung, S. B., Yang, C. S., Lee, J. S., Shin, A. R., Jung, S. S., Son, J. W., et al. (2006). The mycobacterial 38-kilodalton glycolipoprotein antigen activates the mitogen-activated protein kinase pathway and release of proinflammatory cytokines through Toll-like receptors 2 and 4 in human monocytes. Infect. Immun. 74, 2686-2696. doi: 10.1128/IAI.74.5.2686-2696.2006
26. Kleinnijenhuis, J., Quintin, J., Preijers, F., Benn, C. S., Joosten, L. A., Jacobs, C., et al. (2014). Long-lasting effects of BCG vaccination on both heterologous Th1/Th17 responses and innate trained immunity. J. Innate Immun. 6, 152-158. doi: 10.1159/000355628
27. Kleinnijenhuis, J., Quintin, J., Preijers, F., Joosten, L. A., Ifrim, D. C., Saeed, S., et al. (2012). Bacille Calmette-Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc. Natl. Acad. Sci. U.S.A. 109, 17537-17542. doi: 10.1073/pnas.1202870109
28. Krutzik, S. R., Ochoa, M. T., Sieling, P. A., Uematsu, S., Ng, Y. W., Legaspi, A., et al. (2003). Activation and regulation of Toll-like receptors 2 and 1 in human leprosy. Nat. Med. 9, 525-532. doi: 10.1038/nm864
29. Liu, M., John, C. M., and Jarvis, G. A. (2010). Phosphoryl moieties of lipid A from Neisseria meningitidis and N. gonorrhoeae lipooligosaccharides play an important role in activation of both MyD88-and TRIF-dependent TLR4-MD-2 signaling pathways. J. Immunol. 185, 6974-6984. doi: 10.4049/jimmunol.1000953
30. Means, T. K., Jones, B. W., Schromm, A. B., Shurtleff, B. A., Smith, J. A., Keane, J., et al. (2001). Differential effects of a Toll-like receptor antagonist on Mycobacterium tuberculosis-induced macrophage responses. J. Immunol. 166, 4074-4082. doi: 10.4049/jimmunol.166.6.4074
31. Means, T. K., Wang, S., Lien, E., Yoshimura, A., Golenbock, D. T., and Fenton, M. J. (1999). Human toll-like receptors mediate cellular activation by Mycobacterium tuberculosis. J. Immunol. 163, 3920-3927.
32. Medzhitov, R., Preston-Hurlburt, P., and Janeway, C. A. Jr. (1997). A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388, 394-397.
33. Munford, R. S. (2008). Sensing gram-negative bacterial lipopolysaccharides: a human disease determinant? Infect. Immun. 76, 454-465. doi: 10.1128/iai.00939-07
34. Murphy, J., Summer, R., Wilson, A. A., Kotton, D. N., and Fine, A. (2008). The prolonged life-span of alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 38, 380-385. doi: 10.1165/rcmb.2007-0224RC
35. Nicolle, D., Fremond, C., Pichon, X., Bouchot, A., Maillet, I., Ryffel, B., et al. (2004). Long-term control of Mycobacterium bovis BCG infection in the absence of Toll-like receptors (TLRs): investigation of TLR2-, TLR6-, or TLR2-TLR4-deficient mice. Infect. Immun. 72, 6994-7004. doi: 10.1016/j.celrep.2014.05.040
36. Nomura, F., Akashi, S., Sakao, Y., Sato, S., Kawai, T., Matsumoto, M., et al. (2000). Cutting edge: endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface toll-like receptor 4 expression. J. Immunol. 164, 3476-3479. doi: 10.4049/jimmunol.164.7.3476
37. Ohto, U., Yamakawa, N., Akashi-Takamura, S., Miyake, K., and Shimizu, T. (2012). Structural analyses of human Toll-like receptor 4 polymorphisms D299G and T399I. J. Biol. Chem. 287, 40611-40617. doi: 10.1074/jbc.M112.404608
38. Park, B. S., Song, D. H., Kim, H. M., Choi, B. S., Lee, H., and Lee, J. O. (2009). The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458, 1191-1195. doi: 10.1038/nature07830
39. Poltorak, A., He, X., Smirnova, I., Liu, M. Y., Van Huffel, C., Du, X., et al. (1998). Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282, 2085-2088.
40. Prohinar, P., Rallabhandi, P., Weiss, J. P., and Gioannini, T. L. (2010). Expression of functional D299G.T399I polymorphic variant of TLR4 depends more on coexpression of MD-2 than does wild-type TLR4. J. Immunol. 184, 4362-4367. doi: 10.4049/jimmunol.0903142
41. Richardus, R. A., Butlin, C. R., Alam, K., Kundu, K., Geluk, A., and Richardus, J. H. (2015). Clinical manifestations of leprosy after BCG vaccination: an observational study in Bangladesh. Vaccine 33, 1562-1567. doi: 10.1016/j.vaccine.2015.02.017
42. Ridley, D. S., and Jopling, W. H. (1966). Classification of leprosy according to immunity. A five-group system. Int. J. Lepr. Other. Mycobact. Dis. 34, 255-273.
43. Rombouts, Y., Burguiere, A., Maes, E., Coddeville, B., Elass, E., Guerardel, Y., et al. (2009). Mycobacterium marinum lipooligosaccharides are unique caryophyllose-containing cell wall glycolipids that inhibit tumor necrosis factor-alpha secretion in macrophages. J. Biol. Chem. 284, 20975-20988. doi: 10.1074/jbc.M109.011429
44. Saeed, S., Quintin, J., Kerstens, H. H., Rao, N. A., Aghajanirefah, A., Matarese, F., et al. (2014). Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science 345, 1251086. doi: 10.1126/science.1251086
45. Sampson, S. L. (2011). Mycobacterial PE/PPE proteins at the host-pathogen interface. Clin. Dev. Immunol. 2011:497203. doi: 10.1155/2011/497203
46. Shalova, I. N., Kajiji, T., Lim, J. Y., Gomez-Pina, V., Fernandez-Ruiz, I., Arnalich, F., et al. (2012). CD16 regulates TRIF-dependent TLR4 response in human monocytes and their subsets. J. Immunol. 188, 3584-3593. doi: 10.4049/jimmunol.1100244
47. Singh, P., and Cole, S. T. (2011). Mycobacterium leprae: genes, pseudogenes and genetic diversity. Future Microbiol. 6, 57-71. doi: 10.2217/fmb.10.153
48. Stephenson, H. N., John, C. M., Naz, N., Gundogdu, O., Dorrell, N., Wren, B. W., et al. (2013). Campylobacter jejuni lipooligosaccharide sialylation, phosphorylation, and amide/ester linkage modifications fine-tune human Toll-like receptor 4 activation. J. Biol. Chem. 288, 19661-19672. doi: 10.1074/jbc.M113.468298
49. Teles, R. M., Graeber, T. G., Krutzik, S. R., Montoya, D., Schenk, M., Lee, D. J., et al. (2013). Type I interferon suppresses type II interferon-triggered human anti-mycobacterial responses. Science 339, 1448-1453. doi: 10.1126/science.1233665
50. Tiwari, B., Ramakrishnan, U. M., and Raghunand, T. R. (2015). The Mycobacterium tuberculosis protein pair PE9 (Rv1088)-PE10 (Rv1089) forms heterodimers and induces macrophage apoptosis through Toll-like receptor 4. Cell. Microbiol. 17, 1653-1669. doi: 10.1111/cmi.12462
51. Walker, S. L., Roberts, C. H., Atkinson, S. E., Khadge, S., Macdonald, M., Neupane, K. D., et al. (2012). The effect of systemic corticosteroid therapy on the expression of toll-like receptor 2 and toll-like receptor 4 in the cutaneous lesions of leprosy Type 1 reactions. Br. J. Dermatol. 167, 29-35. doi: 10.1111/j.1365-2133.2012.10891.x
52. Wilson, A. A., Murphy, G. J., Hamakawa, H., Kwok, L. W., Srinivasan, S., Hovav, A. H., et al. (2010). Amelioration of emphysema in mice through lentiviral transduction of long-lived pulmonary alveolar macrophages. J. Clin. Invest. 120, 379-389. doi: 10.1172/JCI36666
53. Yamamoto, M., Sato, S., Hemmi, H., Hoshino, K., Kaisho, T., Sanjo, H., et al. (2003). Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301, 640-643. doi: 10.1126/science.1087262
54. Yamamura, M., Uyemura, K., Deans, R. J., Weinberg, K., Rea, T. H., Bloom, B. R., et al. (1991). Defining protective responses to pathogens: cytokine profiles in leprosy lesions. Science 254, 277-279.
55. Yanez, A., Hassanzadeh-Kiabi, N., Ng, M. Y., Megias, J., Subramanian, A., Liu, G. Y., et al. (2013). Detection of a TLR2 agonist by hematopoietic stem and progenitor cells impacts the function of the macrophages they produce. Eur. J. Immunol. 43, 2114-2125. doi: 10.1002/eji.201343403
56. Yona, S., Kim, K. W., Wolf, Y., Mildner, A., Varol, D., Breker, M., et al. (2013). Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38, 79-91. doi: 10.1016/j.immuni.2012.12.001
57. Zughaier, S. M., Zimmer, S. M., Datta, A., Carlson, R. W., and Stephens, D. S. (2005). Differential induction of the toll-like receptor 4-MyD88-dependent and-independent signaling pathways by endotoxins. Infect. Immun. 73, 2940-2950. doi: 10.1128/IAI.73.5.2940-2950.2005