The bacterial and host factors associated with extrapulmonary dissemination of Mycobacterium tuberculosis

Dong Yang,Ying Kong()

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Front. Biol. ›› 2015, Vol. 10 ›› Issue (3) : 252-261. DOI: 10.1007/s11515-015-1358-y
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REVIEW

The bacterial and host factors associated with extrapulmonary dissemination of Mycobacterium tuberculosis

  • Dong Yang,Ying Kong()
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Abstract

With high morbidity and mortality worldwide, tuberculosis (TB) is still an important public health threat. The majority of human TB cases are caused by Mycobacterium tuberculosis. Although pulmonary TB is the most common presentation, M. tuberculosis can disseminate into other organs and causes extrapulmonary TB (EPTB). The dissemination of bacteria from the initial site of infection to other organs can lead to fatal diseases, such as miliary and meningeal TB. Thoroughly understanding the mechanisms and pathways of dissemination would develop therapies to prevent the lethal prognosis of EPTB (miliary and meningeal TB) and vaccines to promote the development of adaptive immunity. This review focuses on risk factors of EPTB, bacterial and host genes involved in EPTB, and potential mechanisms of M. tuberculosis extrapulmonary dissemination.

Keywords

host genes / Mycobacterium tuberculosis / extrapulmonary / dissemination / risk factors / bacterial genes

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Dong Yang,Ying Kong. The bacterial and host factors associated with extrapulmonary dissemination of Mycobacterium tuberculosis. Front. Biol., 2015, 10(3): 252‒261 https://doi.org/10.1007/s11515-015-1358-y

References

1 Adams D O (1976). The granulomatous inflammatory response. A review. Am J Pathol, 84(1): 164–192
2 Alvarado-Esquivel C, García-Corral N, Carrero-Dominguez D, Enciso-Moreno J A, Gurrola-Morales T, Portillo-Gómez L, Rossau R, Mijs W (2009). Molecular analysis of Mycobacterium isolates from extrapulmonary specimens obtained from patients in Mexico. BMC Clin Pathol, 9(1): 1
3 American Thoracic Society, Infectious Diseases Society of America (2000). Diagnostic standards and classification of tuberculosis in adults and children. Am J Respir Crit Care Med, 161(4 Pt 1): 1376–1395
4 Antonucci G, Girardi E, Raviglione M C, Ippolito G (1995). Risk factors for tuberculosis in HIV-infected persons. A prospective cohort study. The Gruppo Italiano di Studio Tubercolosi e AIDS (GISTA). JAMA, 274(2): 143–148
5 Arias M, Zabaleta J, Rodríguez J I, Rojas M, París S C, García L F (1997). Failure to induce nitric oxide production by human monocyte-derived macrophages. Manipulation of biochemical pathways. Allergol Immunopathol (Madr), 25(6): 280–288
6 Arruda S, Bomfim G, Knights R, Huima-Byron T, Riley L W (1993). Cloning of an M. tuberculosis DNA fragment associated with entry and survival inside cells. Science, 261(5127): 1454–1457
7 Asghar R J, Pratt R H, Kammerer J S, Navin T R (2008). Tuberculosis in South Asians living in the United States, 1993–2004. Arch Intern Med, 168(9): 936–942
8 Barnes P F, Barrows S A (1993). Tuberculosis in the 1990s. Ann Intern Med, 119(5): 400–410
9 Barrios-Payán J, Saqui-Salces M, Jeyanathan M, Alcántara-Vazquez A, Casta?on-Arreola M, Rook G, Hernandez-Pando R (2012). Extrapulmonary locations of Mycobacterium tuberculosis DNA during latent infection. J Infect Dis, 206(8): 1194–1205
10 Bates M N, Khalakdina A, Pai M, Chang L, Lessa F, Smith K R (2007). Risk of tuberculosis from exposure to tobacco smoke: a systematic review and meta-analysis. Arch Intern Med, 167(4): 335–342
11 Be N A, Lamichhane G, Grosset J, Tyagi S, Cheng Q J, Kim K S, Bishai W R, Jain S K (2008). Murine model to study the invasion and survival of Mycobacterium tuberculosis in the central nervous system. J Infect Dis, 198(10): 1520–1528
12 Bekker L G, Moreira A L, Bergtold A, Freeman S, Ryffel B, Kaplan G (2000). Immunopathologic effects of tumor necrosis factor alpha in murine mycobacterial infection are dose dependent. Infect Immun, 68(12): 6954–6961
13 Boom W H, Canaday D H, Fulton S A, Gehring A J, Rojas R E, Torres M (2003). Human immunity to M. tuberculosis: T cell subsets and antigen processing. Tuberculosis (Edinb), 83(1-3): 98–106
14 Bouley D M, Ghori N, Mercer K L, Falkow S, Ramakrishnan L (2001). Dynamic nature of host-pathogen interactions in Mycobacterium marinum granulomas. Infect Immun, 69(12): 7820–7831
15 Brewer T F, Heymann S J (2005). Long time due: reducing tuberculosis mortality in the 21st century. Arch Med Res, 36(6): 617–621
16 Cailhol J, Decludt B, Che D (2005). Sociodemographic factors that contribute to the development of extrapulmonary tuberculosis were identified. J Clin Epidemiol, 58(10): 1066–1071
17 Campbell G R, Spector S A (2012). Vitamin D inhibits human immunodeficiency virus type 1 and Mycobacterium tuberculosis infection in macrophages through the induction of autophagy. PLoS Pathog, 8(5): e1002689
18 Camus J C, Pryor M J, Médigue C, Cole S T (2002). Re-annotation of the genome sequence of Mycobacterium tuberculosis H37Rv. Microbiology, 148(Pt 10): 2967–2973
19 Caruso A M, Serbina N, Klein E, Triebold K, Bloom B R, Flynn J L (1999). Mice deficient in CD4 T cells have only transiently diminished levels of IFN-gamma, yet succumb to tuberculosis. J Immunol, 162(9): 5407–5416
20 Casali N, Riley L W (2007). A phylogenomic analysis of the Actinomycetales mce operons. BMC Genomics, 8(1): 60
21 Castro-Garza J, King C H, Swords W E, Quinn F D (2002). Demonstration of spread by Mycobacterium tuberculosis bacilli in A549 epithelial cell monolayers. FEMS Microbiol Lett, 212(2): 145–149
22 Centers for Disease Control and Prevention (CDC) (2008). Trends in tuberculosis—United States, 2007. MMWR Morb Mortal Wkly Rep, 57(11): 281–285
23 Chan-Yeung M, Noertjojo K, Chan S L, Tam C M (2002). Sex differences in tuberculosis in Hong Kong. Int J Tuberc Lung Dis, 6(1): 11–18
24 Chang J C, Harik N S, Liao R P, Sherman D R (2007). Identification of Mycobacterial genes that alter growth and pathology in macrophages and in mice. J Infect Dis, 196(5): 788–795
25 Chawla M, Parikh P, Saxena A, Munshi M, Mehta M, Mai D, Srivastava A K, Narasimhulu K V, Redding K E, Vashi N, Kumar D, Steyn A J, Singh A (2012). Mycobacterium tuberculosis WhiB4 regulates oxidative stress response to modulate survival and dissemination in vivo. Mol Microbiol, 85(6): 1148–1165
26 Chiang C Y, Slama K, Enarson D A (2007). Associations between tobacco and tuberculosis. Int J Tuberc Lung Dis, 11(3): 258–262
27 Cirillo S L, Subbian S, Chen B, Weisbrod T R, Jacobs W R Jr, Cirillo J D (2009). Protection of Mycobacterium tuberculosis from reactive oxygen species conferred by the mel2 locus impacts persistence and dissemination. Infect Immun, 77(6): 2557–2567
28 Clay H, Davis J M, Beery D, Huttenlocher A, Lyons S E, Ramakrishnan L (2007). Dichotomous role of the macrophage in early Mycobacterium marinum infection of the zebrafish. Cell Host Microbe, 2(1): 29–39
29 Cole S T (2002). Comparative and functional genomics of the Mycobacterium tuberculosis complex. Microbiology, 148(Pt 10): 2919–2928
30 Cole S T, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon S V, Eiglmeier K, Gas S, Barry C E 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, Quail M A, Rajandream M A, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston J E, Taylor K, Whitehead S, Barrell B G (1998). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature, 393(6685): 537–544
31 Cooper A M, Dalton D K, Stewart T A, Griffin J P, Russell D G, Orme I M (1993). Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med, 178(6): 2243–2247
32 Dannenberg A M Jr (1989). Immune mechanisms in the pathogenesis of pulmonary tuberculosis. Rev Infect Dis, 11(Suppl 2): S369–S378
33 Davis J M, Ramakrishnan L (2009). The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell, 136(1): 37–49
34 Davis N K, Chater K F (1992). The Streptomyces coelicolor whiB gene encodes a small transcription factor-like protein dispensable for growth but essential for sporulation. Mol Gen Genet, 232(3): 351–358
35 de Jong R, Altare F, Haagen I A, Elferink D G, Boer T, van Breda Vriesman P J, Kabel P J, Draaisma J M, van Dissel J T, Kroon F P, Casanova J L, Ottenhoff T H (1998). Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients. Science, 280(5368): 1435–1438
36 Dobos K M, Spotts E A, Quinn F D, King C H (2000). Necrosis of lung epithelial cells during infection with Mycobacterium tuberculosis is preceded by cell permeation. Infect Immun, 68(11): 6300–6310
37 Edwards D, Kirkpatrick C H (1986). The immunology of mycobacterial diseases. Am Rev Respir Dis, 134(5): 1062–1071
38 Farer L S, Lowell A M, Meador M P (1979). Extrapulmonary tuberculosis in the United States. Am J Epidemiol, 109(2): 205–217
39 Fenton M J, Vermeulen M W (1996). Immunopathology of tuberculosis: roles of macrophages and monocytes. Infect Immun, 64(3): 683–690
40 Fernando S L, Saunders B M, Sluyter R, Skarratt K K, Goldberg H, Marks G B, Wiley J S, Britton W J (2007). A polymorphism in the P2X7 gene increases susceptibility to extrapulmonary tuberculosis. Am J Respir Crit Care Med, 175(4): 360–366
41 Fiske C T, Griffin M R, Erin H, Warkentin J, Lisa K, Arbogast P G, Sterling T R (2010). Black race, sex, and extrapulmonary tuberculosis risk: an observational study. BMC Infect Dis, 10(1): 16
42 Flynn J L, Chan J (2001). Immunology of tuberculosis. Annu Rev Immunol, 19(1): 93–129
43 Forssbohm M, Zwahlen M, Loddenkemper R, Rieder H L (2008). Demographic characteristics of patients with extrapulmonary tuberculosis in Germany. Eur Respir J, 31(1): 99–105
44 Fortune S M, Solache A, Jaeger A, Hill P J, Belisle J T, Bloom B R, Rubin E J, Ernst J D (2004). Mycobacterium tuberculosis inhibits macrophage responses to IFN-gamma through myeloid differentiation factor 88-dependent and-independent mechanisms. J Immunol, 172(10): 6272–6280
45 Gioffré A, Infante E, Aguilar D, Santangelo M P, Klepp L, Amadio A, Meikle V, Etchechoury I, Romano M I, Cataldi A, Hernández R P, Bigi F (2005). Mutation in mce operons attenuates Mycobacterium tuberculosis virulence. Microbes Infect, 7(3): 325–334
46 Gombart A F, Borregaard N, Koeffler H P (2005). Human cathelicidin antimicrobial peptide (CAMP) gene is a direct target of the vitamin D receptor and is strongly up-regulated in myeloid cells by 1,25-dihydroxyvitamin D3. FASEB J, 19(9): 1067–1077
47 Gonzalez O Y, Adams G, Teeter L D, Bui T T, Musser J M, Graviss E A (2003). Extra-pulmonary manifestations in a large metropolitan area with a low incidence of tuberculosis. Int J Tuberc Lung Dis, 7(12): 1178–1185
48 Gordon A H, Hart P D, Young M R (1980). Ammonia inhibits phagosome-lysosome fusion in macrophages. Nature, 286(5768): 79–80
49 Goren M B, D’Arcy Hart P, Young M R, Armstrong J A (1976). Prevention of phagosome-lysosome fusion in cultured macrophages by sulfatides of Mycobacterium tuberculosis. Proc Natl Acad Sci USA, 73(7): 2510–2514
50 Haas D W, Des Prez R M (1994). Tuberculosis and acquired immunodeficiency syndrome: a historical perspective on recent developments. Am J Med, 96(5): 439–450
51 Harris S S (2006). Vitamin D and African Americans. J Nutr, 136(4): 1126–1129
52 Hart P D, Young M R, Jordan M M, Perkins W J, Geisow M J (1983). Chemical inhibitors of phagosome-lysosome fusion in cultured macrophages also inhibit saltatory lysosomal movements. A combined microscopic and computer study. J Exp Med, 158(2): 477–492
53 Henao M I, Montes C, París S C, García L F (2006). Cytokine gene polymorphisms in Colombian patients with different clinical presentations of tuberculosis. Tuberculosis (Edinb), 86(1): 11–19
54 Henkle E, Winthrop K L (2015). Nontuberculous mycobacteria infections in immunosuppressed hosts. Clin Chest Med, 36(1): 91–99
55 Hoal-Van Helden E G, Epstein J, Victor T C, Hon D, Lewis L A, Beyers N, Zurakowski D, Ezekowitz A B, Van Helden P D (1999). Mannose-binding protein B allele confers protection against tuberculous meningitis. Pediatr Res, 45(4 Pt 1): 459–464
56 Holmes C B, Hausler H, Nunn P (1998). A review of sex differences in the epidemiology of tuberculosis. Int J Tuberc Lung Dis, 2(2): 96–104
57 Hopewell P (1994). Overview of Clinical Tuberculosis. In: Barry B(ed.). Tuberculosis: Pathogenesis, Protection and Control. ASM Press, Washington, DC. pp. 25–46
58 Hsu T, Hingley-Wilson S M, Chen B, Chen M, Dai A Z, Morin P M, Marks C B, Padiyar J, Goulding C, Gingery M, Eisenberg D, Russell R G, Derrick S C, Collins F M, Morris S L, King C H, Jacobs W R Jr (2003). The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc Natl Acad Sci USA, 100(21): 12420–12425
59 Hudelson P (1996). Gender differentials in tuberculosis: the role of socio-economic and cultural factors. Tuber Lung Dis, 77(5): 391–400
60 Jones B E, Young S M, Antoniskis D, Davidson P T, Kramer F, Barnes P F (1993). Relationship of the manifestations of tuberculosis to CD4 cell counts in patients with human immunodeficiency virus infection. Am Rev Respir Dis, 148(5): 1292–1297
61 Jouanguy E, Altare F, Lamhamedi S, Revy P, Emile J F, Newport M, Levin M, Blanche S, Seboun E, Fischer A, Casanova J L (1996). Interferon-gamma-receptor deficiency in an infant with fatal bacille Calmette-Guérin infection. N Engl J Med, 335(26): 1956–1961
62 Kapur V, Whittam T S, Musser J M (1994). Is Mycobacterium tuberculosis 15,000 years old? J Infect Dis, 170(5): 1348–1349
63 Kaufmann S H (2002). Protection against tuberculosis: cytokines, T cells, and macrophages. Ann Rheum Dis, 61(Suppl 2): ii54–ii58
64 Keane J, Gershon S, Wise R P, Mirabile-Levens E, Kasznica J, Schwieterman W D, Siegel J N, Braun M M (2001). Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N Engl J Med, 345(15): 1098–1104
65 Kim J H, Lee S Y, Lee S H, Sin C, Shim J J, In K H, Yoo S H, Kang K H (2003). NRAMP1 genetic polymorphisms as a risk factor of tuberculous pleurisy. Int J Tuberc Lung Dis, 7(4): 370–375
66 Kinhikar A G, Verma I, Chandra D, Singh K K, Weldingh K, Andersen P, Hsu T, Jacobs W R Jr, Laal S (2010). Potential role for ESAT6 in dissemination of M. tuberculosis via human lung epithelial cells. Mol Microbiol, 75(1): 92–106
67 Kumar A, Bose M, Brahmachari V (2003). Analysis of expression profile of mammalian cell entry (mce) operons of Mycobacterium tuberculosis. Infect Immun, 71(10): 6083–6087
68 Lado Lado F L, Barrio Gómez E, Carballo Arceo E, Cabarcos Ortíz de Barrón A, LadoF L, Barrio Gómez E (1999). Clinical presentation of tuberculosis and the degree of immunodeficiency in patients with HIV infection. Scand J Infect Dis, 31(4): 387–391
69 Lebrun P, Raze D, Fritzinger B, Wieruszeski J M, Biet F, Dose A, Carpentier M, Schwarzer D, Allain F, Lippens G, Locht C (2012). Differential contribution of the repeats to heparin binding of HBHA, a major adhesin of Mycobacterium tuberculosis. PLoS ONE, 7(3): e32421
70 Lee M P, Chan J W, Ng K K, Li P C (2000). Clinical manifestations of tuberculosis in HIV-infected patients. Respirology, 5(4): 423–426
71 Levin M, Newport M J, D’Souza S, Kalabalikis P, Brown I N, Lenicker H M, Agius P V, Davies E G, Thrasher A, Klein N, (1995). Familial disseminated atypical mycobacterial infection in childhood: a human mycobacterial susceptibility gene? Lancet, 345(8942): 79–83
72 Lin C Y, Chen T C, Lu P L, Lai C C, Yang Y H, Lin W R, Huang P M, Chen Y H (2013). Effects of gender and age on development of concurrent extrapulmonary tuberculosis in patients with pulmonary tuberculosis: a population based study. PLoS ONE, 8(5): e63936
73 Lin P L, Myers A, Smith L, Bigbee C, Bigbee M, Fuhrman C, Grieser H, Chiosea I, Voitenek N N, Capuano S V, Klein E, Flynn J L (2010). Tumor necrosis factor neutralization results in disseminated disease in acute and latent Mycobacterium tuberculosis infection with normal granuloma structure in a cynomolgus macaque model. Arthritis Rheum, 62(2): 340–350
74 Liu P T, Stenger S, Li H, Wenzel L, Tan B H, Krutzik S R, Ochoa M T, Schauber J, Wu K, Meinken C, Kamen D L, Wagner M, Bals R, Steinmeyer A, Zügel U, Gallo R L, Eisenberg D, Hewison M, Hollis B W, Adams J S, Bloom B R, Modlin R L (2006). Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science, 311(5768): 1770–1773
75 MacMicking J D, Taylor G A, McKinney J D (2003). Immune control of tuberculosis by IFN-gamma-inducible LRG-47. Science, 302(5645): 654–659
76 Malik Z A, Iyer S S, Kusner D J (2001). Mycobacterium tuberculosis phagosomes exhibit altered calmodulin-dependent signal transduction: contribution to inhibition of phagosome-lysosome fusion and intracellular survival in human macrophages. J Immunol, 166(5): 3392–3401
77 Manca C, Tsenova L, Bergtold A, Freeman S, Tovey M, Musser J M, Barry C E 3rd, Freedman V H, Kaplan G (2001). Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-alpha /beta. Proc Natl Acad Sci USA, 98(10): 5752–5757
78 Martineau A R, Wilkinson R J, Wilkinson K A, Newton S M, Kampmann B, Hall B M, Packe G E, Davidson R N, Eldridge S M, Maunsell Z J, Rainbow S J, Berry J L, Griffiths C J (2007). A single dose of vitamin D enhances immunity to mycobacteria. Am J Respir Crit Care Med, 176(2): 208–213
79 Martinez A N, Rhee J T, Small P M, Behr M A (2000). Sex differences in the epidemiology of tuberculosis in San Francisco. Int J Tuberc Lung Dis, 4(1): 26–31
80 McDonough K A, Kress Y (1995). Cytotoxicity for lung epithelial cells is a virulence-associated phenotype of Mycobacterium tuberculosis. Infect Immun, 63(12): 4802–4811
81 McDonough K A, Kress Y, Bloom B R (1993). Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages. Infect Immun, 61(7): 2763–2773
82 McKinney J D, H?ner zu Bentrup K, Mu?oz-Elías E J, Miczak A, Chen B, Chan W T, Swenson D, Sacchettini J C, Jacobs W R Jr, Russell D G (2000). Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature, 406(6797): 735–738
83 Menozzi F D, Bischoff R, Fort E, Brennan M J, Locht C (1998). Molecular characterization of the mycobacterial heparin-binding hemagglutinin, a mycobacterial adhesin. Proc Natl Acad Sci USA, 95(21): 12625–12630
84 Menozzi F D, Rouse J H, Alavi M, Laude-Sharp M, Muller J, Bischoff R, Brennan M J, Locht C (1996). Identification of a heparin-binding hemagglutinin present in mycobacteria. J Exp Med, 184(3): 993–1001
85 Musellim B, Erturan S, Sonmez Duman E, Ongen G (2005). Comparison of extra-pulmonary and pulmonary tuberculosis cases: factors influencing the site of reactivation. Int J Tuberc Lung Dis, 9(11): 1220–1223
86 Nathan C, Shiloh M U (2000). Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci USA, 97(16): 8841–8848
87 Nursyam E W, Amin Z, Rumende C M (2006). The effect of vitamin D as supplementary treatment in patients with moderately advanced pulmonary tuberculous lesion. Acta Med Indones, 38(1): 3–5
88 Peters W, Ernst J D (2003). Mechanisms of cell recruitment in the immune response to Mycobacterium tuberculosis. Microbes Infect, 5(2): 151–158
89 Pethe K, Alonso S, Biet F, Delogu G, Brennan M J, Locht C, Menozzi F D (2001). The heparin-binding haemagglutinin of M. tuberculosis is required for extrapulmonary dissemination. Nature, 412(6843): 190–194
90 Pitchenik A E, Fertel D, Bloch A B (1988). Mycobacterial disease: epidemiology, diagnosis, treatment, and prevention. Clin Chest Med, 9(3): 425–441
91 Raviglione M C, Narain J P, Kochi A (1992). HIV-associated tuberculosis in developing countries: clinical features, diagnosis, and treatment. Bull World Health Organ, 70(4): 515–526
92 Reed M B, Domenech P, Manca C, Su H, Barczak A K, Kreiswirth B N, Kaplan G, Barry C E 3rd (2004). A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature, 431(7004): 84–87
93 Rengarajan J, Bloom B R, Rubin E J (2005). Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci USA, 102(23): 8327–8332
94 Rieder H L, Snider D E Jr, Cauthen G M (1990). Extrapulmonary tuberculosis in the United States. Am Rev Respir Dis, 141(2): 347–351
95 Rook G A, Hernandez-Pando R (1996). The pathogenesis of tuberculosis. Annu Rev Microbiol, 50(1): 259–284
96 Sassetti C M, Rubin E J (2003). Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA, 100(22): 12989–12994
97 Schnappinger D, Ehrt S, Voskuil M I, Liu Y, Mangan J A, Monahan I M, Dolganov G, Efron B, Butcher P D, Nathan C, Schoolnik G K (2003). Transcriptional adaptation of Mycobacterium tuberculosis within Macrophages: Insights into the phagosomal environment. J Exp Med, 198(5): 693–704
98 Shafer R W, Kim D S, Weiss J P, Quale J M (1991). Extrapulmonary tuberculosis in patients with human immunodeficiency virus infection. Medicine (Baltimore), 70(6): 384–397
99 Shiloh M U, Nathan C F (2000). Reactive nitrogen intermediates and the pathogenesis of Salmonella and Mycobacteria. Curr Opin Microbiol, 3(1): 35–42
100 Sita-Lumsden A, Lapthorn G, Swaminathan R, Milburn H J (2007). Reactivation of tuberculosis and vitamin D deficiency: the contribution of diet and exposure to sunlight. Thorax, 62(11): 1003–1007
101 Sly L M, Hingley-Wilson S M, Reiner N E, McMaster W R (2003). Survival of Mycobacterium tuberculosis in host macrophages involves resistance to apoptosis dependent upon induction of antiapoptotic Bcl-2 family member Mcl-1. J Immunol, 170(1): 430–437
102 Snider D E Jr, Roper W L (1992). The new tuberculosis. N Engl J Med, 326(10): 703–705
103 Sohn H, Kim J S, Shin S J, Kim K, Won C J, Kim W S, Min K N, Choi H G, Lee J C, Park J K, Kim H J (2011). Targeting of Mycobacterium tuberculosis heparin-binding hemagglutinin to mitochondria in macrophages. PLoS Pathog, 7(12): e1002435
104 Sreeramareddy C T, Panduru K V, Verma S C, Joshi H S, Bates M N (2008). Comparison of pulmonary and extrapulmonary tuberculosis in Nepal- a hospital-based retrospective study. BMC Infect Dis, 8(1): 8
105 Sudre P, ten Dam G, Kochi A (1992). Tuberculosis: a global overview of the situation today. Bull World Health Organ, 70(2): 149–159
106 Tascon R E, Soares C S, Ragno S, Stavropoulos E, Hirst E M, Colston M J (2000). Mycobacterium tuberculosis-activated dendritic cells induce protective immunity in mice. Immunology, 99(3): 473–480
107 Theuer C P, Hopewell P C, Elias D, Schecter G F, Rutherford G W, Chaisson R E (1990). Human immunodeficiency virus infection in tuberculosis patients. J Infect Dis, 162(1): 8–12
108 Thuong N T, Hawn T R, Thwaites G E, Chau T T, Lan N T, Quy H T, Hieu N T, Aderem A, Hien T T, Farrar J J, Dunstan S J (2007). A polymorphism in human TLR2 is associated with increased susceptibility to tuberculous meningitis. Genes Immun, 8(5): 422–428
109 Tsenova L, Ellison E, Harbacheuski R, Moreira A L, Kurepina N, Reed M B, Mathema B, Barry C E 3rd, Kaplan G (2005). Virulence of selected Mycobacterium tuberculosis clinical isolates in the rabbit model of meningitis is dependent on phenolic glycolipid produced by the bacilli. J Infect Dis, 192(1): 98–106
110 van Pinxteren L A, Cassidy J P, Smedegaard B H, Agger E M, Andersen P (2000). Control of latent Mycobacterium tuberculosis infection is dependent on CD8 T cells. Eur J Immunol, 30(12): 3689–3698
111 Verway M, Bouttier M, Wang T T, Carrier M, Calderon M, An B S, Devemy E, McIntosh F, Divangahi M, Behr M A, White J H (2013). Vitamin D induces interleukin-1β expression: paracrine macrophage epithelial signaling controls M. tuberculosis infection. PLoS Pathog, 9(6): e1003407
112 Wang T T, Nestel F P, Bourdeau V, Nagai Y, Wang Q, Liao J, Tavera-Mendoza L, Lin R, Hanrahan J W, Mader S, White J H (2004). Cutting edge: 1,25-dihydroxyvitamin D3 is a direct inducer of antimicrobial peptide gene expression. J Immunol, 173(5): 2909–2912
113 Weir M R, Thornton G F (1985). Extrapulmonary tuberculosis. Experience of a community hospital and review of the literature. Am J Med, 79(4): 467–478
114 WHO (2014). Global tuberculosis control 2013.
115 Wilkinson R J, Llewelyn M, Toossi Z, Patel P, Pasvol G, Lalvani A, Wright D, Latif M, Davidson R N (2000). Influence of vitamin D deficiency and vitamin D receptor polymorphisms on tuberculosis among Gujarati Asians in west London: a case-control study. Lancet, 355(9204): 618–621
116 Wilkinson R J, Patel P, Llewelyn M, Hirsch C S, Pasvol G, Snounou G, Davidson R N, Toossi Z (1999). Influence of polymorphism in the genes for the interleukin (IL)-1 receptor antagonist and IL-1beta on tuberculosis. J Exp Med, 189(12): 1863–1874
117 Wolf A J, Linas B, Trevejo-Nu?ez G J, Kincaid E, Tamura T, Takatsu K, Ernst J D (2007). Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J Immunol, 179(4): 2509–2519
118 Yang Z, Kong Y, Wilson F, Foxman B, Fowler A H, Marrs C F, Cave M D, Bates J H (2004). Identification of risk factors for extrapulmonary tuberculosis. Clin Infect Dis, 38(2): 199–205
119 Zhang X, Andersen A B, Lillebaek T, Kamper-J?rgensen Z, Thomsen V O, Ladefoged K, Marrs C F, Zhang L, Yang Z (2011). Effect of sex, age, and race on the clinical presentation of tuberculosis: a 15-year population-based study. Am J Trop Med Hyg, 85(2): 285–290
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