IFN-γ- and TNF-independent vitamin D-inducible human suppression of mycobacteria: The role of cathelicidin LL-37

Journal of Immunology

Volumn 178, Issue 11, 2007, Pages 7190-7198

  Martineau, Adrian R ^a,b,c   Wilkinson, Katalin A ^a,c   Newton, Sandra M ^a   Floto, R Andres ^d   Norman, Anthony W ^e   Skolimowska, Keira ^a,c   Davidson, Robert N ^f   Sørensen, Ole E ^g   Kampmann, Beate ^a,c   Griffiths, Christopher J ^b   Wilkinson, Robert J ^a,c,f,h  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF CAPE TOWN   (South Africa)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f NORTHWICK PARK HOSPITAL   (United Kingdom)

^g LUND UNIVERSITY   (Sweden)

^h UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; CALCITRIOL; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CD14 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12P40; TUMOR NECROSIS FACTOR; VITAMIN D; VITAMIN D RECEPTOR;

ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; HUMAN CELL; INFECTION RESISTANCE; INFECTION SENSITIVITY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINOL DEFICIENCY; TUBERCULOSIS;

EID: 34249780526     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.11.7190     Document Type: Article

References (52)

1. Corbett, E. L., B. Marston, G. J. Churchyard, and K. M. De Cock. 2006. Tuberculosis in sub-Saharan Africa: opportunities, challenges, and change in the era of antiretroviral treatment. Lancet 367: 926-937.
2. Espinal, M. A., A. Laszlo, L. Simonsen, F. Boulahbal, S. J. Kim, A. Reniero, S. Hoffner, H. L. Rieder, N. Binkin, C. Dye, et al. 2001. Global trends in resistance to antituberculosis drugs: World Health Organization- International Union against Tuberculosis and Lung Disease Working Group on Anti-Tuberculosis Drug Resistance Surveillance. N. Engl. J. Med. 344: 1294-1303.
3. Corbett, E. L., C. J. Watt, N. Walker, D. Maher, B. G. Williams, M. C. Raviglione, and C. Dye. 2003. The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch. Intern. Med. 163: 1009-1021.
4. Altare, F., A. Durandy, D. Lammas, J. F. Emile, S. Lamhamedi, F. Le Deist, P. Drysdale, E. Jouanguy, R. Doffinger, F. Bernaudin, et al. 1998. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science 280: 1432-1435.
5. Keane, J., S. Gershon, R. P. Wise, E. Mirabile-Levens, J. Kasznica, W. D. Schwieterman, J. N. Siegel, and M. M. Braun. 2001. Tuberculosis associated with infliximab, a tumor necrosis factor α-neutralizing agent. N. Engl. J. Med. 345: 1098-1104.
6. Newport, M. J., C. M. Huxley, S. Huston, C. M. Hawrylowicz, B. A. Oostra, R. Williamson, and M. Levin. 1996. A mutation in the interferon γ-receptor gene and susceptibility to mycobacterial infection. N. Engl. J. Med. 335: 1941-1949.
7. Kampmann, B., C. Hemingway, A. Stephens, R. Davidson, A. Goodsall, S. Anderson, M. Nicol, E. Scholvinck, D. Relman, S. Waddell, et al. 2005. Acquired predisposition to mycobacterial disease due to autoantibodies to IFN-γ. J. Clin. Invest. 115: 2480-2488.
8. Flynn, J. L., and J. Chan. 2001. Immunology of tuberculosis. Annu. Rev. Immunol. 19: 93-129.
9. Rose, A. M., J. M. Watson, C. Graham, A. J. Nunn, F. Drobniewski, L. P. Ormerod, J. H. Darbyshire, and J. Leese. 2001. Tuberculosis at the end of the 20th century in England and Wales: results of a national survey in 1998. Thorax 56: 173-179.
10. Talbot, E. A., M. Moore, E. McCray, and N. J. Binkin. 2000. Tuberculosis among foreign-born persons in the United States, 1993-1998. J. Am. Med. Assoc. 284: 2894-2900.
11. British Thoracic Society. 2000. Control and prevention of tuberculosis in the United Kingdom: code of practice 2000: Joint Tuberculosis Committee of the British Thoracic Society. Thorax 55: 887-901.
12. 2006. Trends in tuberculosis - United States, 2005. Morb. Mortal Wkly. Rep. 55: 305-308.
13. Preece, M. A., S. Tomlinson, C. A. Ribot, J. Pietrek, H. T. Korn, D. M. Davies, J. A. Ford, M. G. Dunnigan, and J. L. O'Riordan. 1975. Studies of vitamin D deficiency in man. Q. J. Med. 44: 575-589.
14. Grenville-Mathers, R., and J. B. Clark. 1979. The development of tuberculosis in Afro-Asian immigrants. Tubercle 60: 25-29.
15. Wilkinson, R. J., M. Llewelyn, Z. Toossi, P. Patel, G. Pasvol, A. Lalvani, D. Wright, M. Latif, and R. N. Davidson. 2000. Influence of vitamin D deficiency and vitamin D receptor polymorphisms on susceptibility to tuberculosis amongst Gujarati Asians in west London: a case-control study. Lancet 355: 618-621.
16. Ustianowski, A., R. Shaffer, S. Collin, R. J. Wilkinson, and R. N. Davidson. 2005. Prevalence and associations of vitamin D deficiency in foreign-born persons with tuberculosis in London. J. Infect. 50: 432-437.
17. 3 of the multiplication of virulent tubercle bacilli in cultured human macrophages. Infect. Immun. 55: 2945-2950.
18. Davies, P., R. Brown, and J. Woodhead. 1985. Serum concentrations of vitamin D metabolites in untreated tuberculosis. Thorax 40: 187-190.
19. Bellamy, R., C. Ruwende, T. Corrah, K. P. McAdam, M. Thursz, H. C. Whittle, and A. V. Hill. 1999. Tuberculosis and chronic hepatitis B virus infection in Africans and variation in the vitamin D receptor gene. J. Infect. Dis. 179: 721-724.
20. Martineau, A. R., F. U. Honecker, R. J. Wilkinson, and C. J. Griffiths. 2007. Vitamin D in the treatment of pulmonary tuberculosis. J. Steroid Biochem. Mol. Biol. 103: 793-798.
21. Liu, P. T., S. Stenger, H. Li, L. Wenzel, B. H. Tan, S. Krutzik, M. T. Ochoa, J. Schauber, K. Wu, C. Meinken, et al. 2006. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311: 1770-1773.
22. 3-1α- hydroxylase in human monocytes. J. Bone Miner. Res. 21: 37-47.
23. Vidal, M., C. V. Ramana, and A. S. Dusso. 2002. Stat1-vitamin D receptor interactions antagonize 1,25-dihydroxyvitamin D transcriptional activity and enhance stat1-mediated transcription. Mol. Cell. Biol. 22: 2777-2787.
24. 3, γ interferon, and control of proliferation of Mycobacterium tuberculosis by human monocytes. Immunology 57: 159-163.
25. 3-induced monocyte antimycobacterial activity is regulated by phosphatidylinositol 3-kinase and mediated by the NADPH-dependent phagocyte oxidase. J. Biol. Chem. 276: 35482-35493.
26. 3-phosphoinositide 3-kinase pathway. J. Cell Sci. 117: 2131-2140.
27. 3. Mol. Cell. Endocrinol. 197: 1-13.
28. 3 induces nitric oxide synthase and suppresses growth of Mycobacterium tuberculosis in a human macrophage-like cell line. Infect. Immun. 66: 5314-5321.
29. MacMicking, J. D., G. A. Taylor, and J. D. McKinney. 2003. Immune control of tuberculosis by IFN-γ-inducible LRG-47. Science 302: 654-659.
30. Stewart, G. R., K. A. Wilkinson, S. M. Newton, S. M. Sullivan, O. Neyrolles, J. R. Wain, J. Patel, K. L. Pool, D. B. Young, and R. J. Wilkinson. 2005. Effect of deletion or overexpression of the 19-kilodalton lipoprotein Rv3763 on the innate response to Mycobacterium tuberculosis. Infect. Immun. 73: 6831-6837.
31. Turner, D. J., S. L. Hoyle, V. A. Snewin, M. P. Gares, I. N. Brown, and D. B. Young. 2002. An ex vivo culture model for screening drug activity against in vivo phenotypes of Mycobacterium tuberculosis. Microbiology 148: 2929-2936.
32. Snewin, V. A., M. P. Gares, P. O. Gaora, Z. Hasan, I. N. Brown, and D. B. Young. 1999. Assessment of immunity to mycobacterial infection with luciferase reporter constructs. Infect. Immun. 67: 4586-4593.
33. Kampmann, B., P. O. Gaora, V. A. Snewin, M. P. Gares, D. B. Young, and M. Levin. 2000. Evaluation of human antimycobacterial immunity using recombinant reporter mycobacteria. J. Infect. Dis. 182: 895-901.
34. Ratledge, C. 2004. Iron, mycobacteria and tuberculosis. Tuberculosis 84: 110-130.
35. Wilkinson, R. J., L. E. DesJardin, N. Islam, B. M. Gibson, R. A. Kanost, K. A. Wilkinson, D. Poelman, K. D. Eisenach, and Z. Toossi. 2001. An increase in expression of a M. tuberculosis mycolyl transferase gene (fbpB) occurs early after infection of human monocytes. Mol. Microbiol. 39: 813-821.
36. Sorensen, O., J. B. Cowland, J. Askaa, and N. Borregaard. 1997. An ELISA for hCAP-18, the cafhelicidin present in human neutrophils and plasma. J. Immunol. Methods 206: 53-59.
37. Sorensen, O., T. Bratt, A. H. Johnsen, M. T. Madsen, and N. Borregaard. 1999. The human antibacterial cathelicidin, hCAP-18, is bound to lipoproteins in plasma. J. Biol. Chem. 274: 22445-22451.
38. MacMicking, J. D., R. J. North, R. LaCourse, J. S. Mudgett, S. K. Shah, and C. F. Nathan. 1997. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. USA 94: 5243-5248.
39. 3 is a direct inducer of antimicrobial peptide gene expression. J. Immunol. 173: 2909-2912.
40. Dorschner, R. A., B. Lopez-Garcia, A. Peschel, D. Kraus, K. Morikawa, V. Nizet, and R. L. Gallo. 2006. The mammalian ionic environment dictates microbial susceptibility to antimicrobial defense peptides. FASEB J. 20: 35-42.
41. Wilkinson, K. A., G. R. Stewart, S. M. Newton, H. M. Vordermeier, J. R. Wain, H. N. Murphy, K. Horner, D. B. Young, and R. J. Wilkinson. 2005. Infection biology of a novel α-crystallin of Mycobacterium tuberculosis: Acr2. J. Immunol. 174: 4237-4243.
42. Wilkinson, R. J., and D. B. Young. 2004. Novel vaccines against tuberculosis. In New Generation Vaccines, 3rd Ed. M. Levine, J. Kaper, R. Rappuoli, M. Liu, and M. Good, eds. Marcel Dekker, New York, pp. 519-535.
43. Bekpen, C., J. P. Hunn, C. Rohde, I. Parvanova, L. Guethlein, D. M. Dunn, E. Glowalla, M. Leptin, and J. C. Howard. 2005. The interferon-inducible p47 (IRG) GTPases in vertebrates: loss of the cell autonomous resistance mechanism in the human lineage. Genome Biol. 6: R92.
44. Wah, J., A. Wellek, M. Frankenberger, P. Unterberger, U. Welsch, and R. Bals. 2006. Antimicrobial peptides are present in immune and host defense cells of the human respiratory and gastrointestinal tracts. Cell Tissue Res. 324: 449-456.
45. Sorensen, O. E., P. Follin, A. H. Johnsen, J. Calafat, G. S. Tjabringa, P. S. Hiemstra, and N. Borregaard. 2001. Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood 97: 3951-3959.
46. De, Y., Q. Chen, A. P. Schmidt, G. M. Anderson, J. M. Wang, J. Wooters, J. J. Oppenheim, and O. Chertov. 2000. LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J. Exp. Med. 192: 1069-1074.
47. Scott, M. G., D. J. Davidson, M. R. Gold, D. Bowdish, and R. E. Hancock. 2002. The human antimicrobial peptide LL-37 is a multifunctional modulator of innate immune responses. J. Immunol. 169: 3883-3891.
48. Henzler-Wildman, K. A., G. V. Martinez, M. F. Brown, and A. Ramamoorthy. 2004. Perturbation of the hydrophobic core of lipid bilayers by the human antimicrobial peptide LL-37. Biochemistry 43: 8459-8469.
49. 3 indicates that the 6-s-cis conformation is preferred for rapid nongenomic biological responses and that neither 6-s-cis- nor 6-s-trans-locked analogs are preferred for genomic biological responses. Mol. Endocrinol. 11: 1518-1531.
50. 3 analog structure-function assessment of the rapid stimulation of intestinal calcium absorption (transcaltachia). J. Bone Miner. Res. 7: 457-463.
51. Bula, C. M., J. E. Bishop, S. Ishizuka, and A. W. Norman. 2000. 25-Dehydro-1α-hydroxyvitamin D3-26,23S-lactone antagonizes the nuclear vitamin D receptor by mediating a unique noncovalent conformational change. Mol. Endocrinol. 14: 1788-1796.
52. 3. J. Biol. Chem. 268: 20022-20030.