Virulence-dependent alterations in the kinetics of immune cells during pulmonary infection by mycobacterium tuberculosis

PLoS ONE

Volumn 10, Issue 12, 2015, Pages

  Kim, Woo Sik ^a   Kim, Jong Seok ^a   Cha, Seung Bin ^a   Han, Seung Jung ^a   Kim, Hongmin ^a   Kwon, Kee Woong ^a   Kim, So Jeong ^a   Eum, Seok Yong ^b   Cho, Sang Nae ^a   Shin, Sung Jae ^a  

^a Yonsei University College of Medicine   (South Korea)

^b International Tuberculosis Research Center   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CD11 ANTIGEN; CD4 ANTIGEN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; INTERLEUKIN 2 RECEPTOR ALPHA;

ANIMAL; C57BL MOUSE; CELL CULTURE; DENDRITIC CELL; FEMALE; GENETICS; HELPER CELL; IMMUNOLOGY; INNATE IMMUNITY; LUNG; LUNG TUBERCULOSIS; METABOLISM; MICROBIOLOGY; MOUSE; MYCOBACTERIUM TUBERCULOSIS; PATHOGENICITY; REGULATORY T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD11; ANTIGENS, CD4; CELLS, CULTURED; DENDRITIC CELLS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; IMMUNITY, INNATE; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LUNG; MICE; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY; TUBERCULOSIS, PULMONARY;

EID: 84956618644     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0145234     Document Type: Article

References (49)

1. World Health Organization (2014) Global tuberculosis report 2014. World Health Organization, WHO/ HTM/TB. 2014.08.
2. Leung AN. Pulmonary tuberculosis: the essentials. Radiology. 1999; 210 (2): 307-22. doi: 10.1148/radiology.210.2.r99ja34307 PMID: 10207408.
3. Reiling N, Homolka S, Walter K, Brandenburg J, Niwinski L, Ernst M, et al. Clade-specific virulence patterns of Mycobacterium tuberculosis complex strains in human primary macrophages and aerogenically infected mice. MBio. 2013; 4 (4). doi: 10.1128/mBio.00250-13 PMID: 23900170; PubMed Central PMCID: PMC3735190.
4. Hunter RL, Actor JK, Hwang SA, Karev V, Jagannath C. Pathogenesis of post primary tuberculosis: immunity and hypersensitivity in the development of cavities. Ann Clin Lab Sci. 2014; 44 (4): 365-87. PMID: 25361920.
5. Guidry TV, Hunter RL Jr, Actor JK. Mycobacterial glycolipid trehalose 6,6'-dimycolate-induced hypersensitive granulomas: contribution of CD4+ lymphocytes. Microbiology. 2007; 153 (Pt 10): 3360-9. doi: 10.1099/mic.0.2007/010850-0 PMID: 17906135; PubMed Central PMCID: PMCPMC2583334.
6. Chakraborty P, Kulkarni S, Rajan R, Sainis K. Drug resistant clinical isolates of Mycobacterium tuberculosis from different genotypes exhibit differential host responses in THP-1 cells. PLoS One. 2013; 8 (5): e62966. doi: 10.1371/journal.pone.0062966 PMID: 23667550; PubMed Central PMCID: PMC3646887.
7. Beisiegel M, Mollenkopf HJ, Hahnke K, Koch M, Dietrich I, Reece ST, et al. Combination of host susceptibility and Mycobacterium tuberculosis virulence define gene expression profile in the host. Eur J Immunol. 2009; 39 (12): 3369-84. doi: 10.1002/eji.200939615 PMID: 19795415.
8. Kamath AB, Alt J, Debbabi H, Behar SM. Toll-like receptor 4-defective C3H/HeJ mice are not more susceptible than other C3H substrains to infection with Mycobacterium tuberculosis. Infect Immun. 2003; 71 (7): 4112-8. PMID: 12819102; PubMed Central PMCID: PMCPMC162027.
9. Ehlers S. Role of tumour necrosis factor (TNF) in host defence against tuberculosis: implications for immunotherapies targeting TNF. Ann Rheum Dis. 2003; 62 Suppl 2: ii37-42. PMID: 14532147; PubMed Central PMCID: PMCPMC1766754.
10. Green AM, Difazio R, Flynn JL. IFN-gamma from CD4 T cells is essential for host survival and enhances CD8 T cell function during Mycobacterium tuberculosis infection. J Immunol. 2013; 190 (1): 270-7. doi: 10.4049/jimmunol.1200061 PMID: 23233724; PubMed Central PMCID: PMCPMC3683563.
11. Beamer GL, Flaherty DK, Assogba BD, Stromberg P, Gonzalez-Juarrero M, de Waal Malefyt R, et al. Interleukin-10 promotes Mycobacterium tuberculosis disease progression in CBA/J mice. J Immunol. 2008; 181 (8): 5545-50. PMID: 18832712; PubMed Central PMCID: PMC2728584.
12. Weiser JN, Roche AM, Hergott CB, LaRose MI, Connolly T, Jorgensen WL, et al. Macrophage migration inhibitory factor (MIF) is detrimental in pneumococcal pneumonia and a target for therapeutic immunomodulation. J Infect Dis. 2015. doi: 10.1093/infdis/jiv262 PMID: 25943202.
13. Vilaplana C, Prats C, Marzo E, Barril C, Vegue M, Diaz J, et al. To achieve an earlier IFN-gamma response is not sufficient to control Mycobacterium tuberculosis infection in mice. PLoS One. 2014; 9 (6): e100830. doi: 10.1371/journal.pone.0100830 PMID: 24959669; PubMed Central PMCID: PMC4069189.
14. Ali A. Mycobacterium tuberculosis and Molecular Epidemiology: An Overview. Journal of Microbiology Research. 2014; 4 (6A): 25-31. doi: 10.5923/s.microbiology.201401.04
15. Gagneux S, Small PM. Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect Dis. 2007; 7 (5): 328-37. doi: 10.1016/S1473-3099 (07) 70108-1 PMID: 17448936.
16. Buu TN, van Soolingen D, Huyen MN, Lan NT, Quy HT, Tiemersma EW, et al. Increased transmission of Mycobacterium tuberculosis Beijing genotype strains associated with resistance to streptomycin: a population-based study. PLoS One. 2012; 7 (8): e42323. doi: 10.1371/journal.pone.0042323 PMID: 22912700; PubMed Central PMCID: PMC3418256.
17. Hanekom M, van der Spuy GD, Streicher E, Ndabambi SL, McEvoy CR, Kidd M, et al. A recently evolved sublineage of the Mycobacterium tuberculosis Beijing strain family is associated with an increased ability to spread and cause disease. J Clin Microbiol. 2007; 45 (5): 1483-90. doi: 10.1128/ JCM.02191-06 PMID: 17360841; PubMed Central PMCID: PMC1865897.
18. Palanisamy GS, Smith EE, Shanley CA, Ordway DJ, Orme IM, Basaraba RJ. Disseminated disease severity as a measure of virulence of Mycobacterium tuberculosis in the guinea pig model. Tuberculosis (Edinb). 2008; 88 (4): 295-306. doi: 10.1016/j.tube.2007.12.003 PMID: 18321783; PubMed Central PMCID: PMC2572689.
19. Manca C, Tsenova L, Bergtold A, Freeman S, Tovey M, Musser JM, et al. 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 U S A. 2001; 98 (10): 5752-7. doi: 10. 1073/pnas.091096998 PMID: 11320211; PubMed Central PMCID: PMC33285.
20. Amaral EP, Ribeiro SC, Lanes VR, Almeida FM, de Andrade MR, Bomfim CC, et al. Pulmonary infection with hypervirulent Mycobacteria reveals a crucial role for the P2X7 receptor in aggressive forms of tuberculosis. PLoS Pathog. 2014; 10 (7): e1004188. doi: 10.1371/journal.ppat.1004188 PMID: 24991816; PubMed Central PMCID: PMC4081775.
21. Kim SJ, Bai GH, Lee H, Kim HJ, Lew WJ, Park YK, et al. Transmission of Mycobacterium tuberculosis among high school students in Korea. Int J Tuberc Lung Dis. 2001; 5 (9): 824-30. PMID: 11573893.
22. Jeon BY, Kwak J, Hahn MY, Eum SY, Yang J, Kim SC, et al. In vivo characteristics of Korean Beijing Mycobacterium tuberculosis strain K1 in an aerosol challenge model and in the Cornell latent tuberculosis model. J Med Microbiol. 2012; 61 (Pt 10): 1373-9. doi: 10.1099/jmm.0.047027-0 PMID: 22820694.
23. Peters W, Scott HM, Chambers HF, Flynn JL, Charo IF, Ernst JD. Chemokine receptor 2 serves an early and essential role in resistance to Mycobacterium tuberculosis. Proc Natl Acad Sci U S A. 2001; 98 (14): 7958-63. doi: 10.1073/pnas.131207398 PMID: 11438742; PubMed Central PMCID: PMC35450.
24. Byun EH, Kim WS, Kim JS, Jung ID, Park YM, Kim HJ, et al. Mycobacterium tuberculosis Rv0577, a novel TLR2 agonist, induces maturation of dendritic cells and drives Th1 immune response. FASEB J. 2012; 26 (6): 2695-711. doi: 10.1096/fj.11-199588 PMID: 22415304.
25. Mihret A. The role of dendritic cells in Mycobacterium tuberculosis infection. Virulence. 2012; 3 (7): 654-9. doi: 10.4161/viru.22586 PMID: 23154283; PubMed Central PMCID: PMCPMC3545947.
26. Obregon-Henao A, Henao-Tamayo M, Orme IM, Ordway DJ. Gr1 (int)CD11b+ myeloid-derived suppressor cells in Mycobacterium tuberculosis infection. PloS one. 2013; 8 (11): e80669. doi: 10.1371/ journal.pone.0080669 PMID: 24224058; PubMed Central PMCID: PMCPMC3815237.
27. Smith I. Mycobacterium tuberculosis pathogenesis and molecular determinants of virulence. Clin Microbiol Rev. 2003; 16 (3): 463-96. PMID: 12857778; PubMed Central PMCID: PMC164219.
28. Gideon HP, Phuah J, Myers AJ, Bryson BD, Rodgers MA, Coleman MT, et al. Variability in tuberculosis granuloma T cell responses exists, but a balance of pro- and anti-inflammatory cytokines is associated with sterilization. PLoS Pathog. 2015; 11 (1): e1004603. doi: 10.1371/journal.ppat.1004603 PMID: 25611466; PubMed Central PMCID: PMCPMC4303275.
29. van Crevel R, Ottenhoff TH, van der Meer JW. Innate immunity to Mycobacterium tuberculosis. Clin Microbiol Rev. 2002; 15 (2): 294-309. PMID: 11932234; PubMed Central PMCID: PMC118070.
30. Meraviglia S, El Daker S, Dieli F, Martini F, Martino A. gammadelta T cells cross-link innate and adaptive immunity in Mycobacterium tuberculosis infection. Clin Dev Immunol. 2011; 2011: 587315. doi: 10. 1155/2011/587315 PMID: 21253470; PubMed Central PMCID: PMC3022180.
31. Ahmad S. Pathogenesis, immunology, and diagnosis of latent Mycobacterium tuberculosis infection. Clin Dev Immunol. 2011; 2011: 814943. doi: 10.1155/2011/814943 PMID: 21234341; PubMed Central PMCID: PMCPMC3017943.
32. Tundup S, Mohareer K, Hasnain SE. Mycobacterium tuberculosis PE25/PPE41 protein complex induces necrosis in macrophages: Role in virulence and disease reactivation? FEBS Open Bio. 2014; 4: 822-8. doi: 10.1016/j.fob.2014.09.001 PMID: 25379378; PubMed Central PMCID: PMCPMC4219985.
33. Carlsson F, Kim J, Dumitru C, Barck KH, Carano RA, Sun M, et al. Host-detrimental role of Esx-1-mediated inflammasome activation in mycobacterial infection. PLoS Pathog. 2010; 6 (5): e1000895. doi: 10. 1371/journal.ppat.1000895 PMID: 20463815; PubMed Central PMCID: PMCPMC2865529.
34. Zhang L, Zhang H, Zhao Y, Mao F, Wu J, Bai B, et al. Effects of Mycobacterium tuberculosis ESAT-6/ CFP-10 fusion protein on the autophagy function of mouse macrophages. DNA Cell Biol. 2012; 31 (2): 171-9. doi: 10.1089/dna.2011.1290 PMID: 21740189.
35. Sreejit G, Ahmed A, Parveen N, Jha V, Valluri VL, Ghosh S, et al. The ESAT-6 protein of Mycobacterium tuberculosis interacts with beta-2-microglobulin (beta2M) affecting antigen presentation function of macrophage. PLoS Pathog. 2014; 10 (10): e1004446. doi: 10.1371/journal.ppat.1004446 PMID: 25356553; PubMed Central PMCID: PMCPMC4214792.
36. Romagnoli A, Etna MP, Giacomini E, Pardini M, Remoli ME, Corazzari M, et al. ESX-1 dependent impairment of autophagic flux by Mycobacterium tuberculosis in human dendritic cells. Autophagy. 2012; 8 (9): 1357-70. doi: 10.4161/auto.20881 PMID: 22885411; PubMed Central PMCID: PMCPMC3442882.
37. Lee JS, Krause R, Schreiber J, Mollenkopf HJ, Kowall J, Stein R, et al. Mutation in the transcriptional regulator PhoP contributes to avirulence of Mycobacterium tuberculosis H37Ra strain. Cell Host Microbe. 2008; 3 (2): 97-103. doi: 10.1016/j.chom.2008.01.002 PMID: 18312844.
38. Shin AR, Shin SJ, Lee KS, Eom SH, Lee SS, Lee BS, et al. Improved sensitivity of diagnosis of tuberculosis in patients in Korea via a cocktail enzyme-linked immunosorbent assay containing the abundantly expressed antigens of the K strain of Mycobacterium tuberculosis. Clin Vaccine Immunol. 2008; 15 (12): 1788-95. doi: 10.1128/CVI.00231-08 PMID: 18945883; PubMed Central PMCID: PMCPMC2593165.
39. Kipnis A, Irwin S, Izzo AA, Basaraba RJ, Orme IM. Memory T lymphocytes generated by Mycobacterium bovis BCG vaccination reside within a CD4 CD44lo CD62 ligand (hi) population. Infect Immun. 2005; 73 (11): 7759-64. doi: 10.1128/IAI.73.11.7759-7764.2005 PMID: 16239580; PubMed Central PMCID: PMC1273888.
40. Ancelet LR, Aldwell FE, Rich FJ, Kirman JR. Oral vaccination with lipid-formulated BCG induces a long-lived, multifunctional CD4 (+) T cell memory immune response. PLoS One. 2012; 7 (9): e45888. doi: 10.1371/journal.pone.0045888 PMID: 23049885; PubMed Central PMCID: PMC3457949.
41. Ordway D, Henao-Tamayo M, Harton M, Palanisamy G, Troudt J, Shanley C, et al. The hypervirulent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation. J Immunol. 2007; 179 (1): 522-31. PMID: 17579073.
42. Semple PL, Binder AB, Davids M, Maredza A, van Zyl-Smit RN, Dheda K. Regulatory T cells attenuate mycobacterial stasis in alveolar and blood-derived macrophages from patients with tuberculosis. Am J Respir Crit Care Med. 2013; 187 (11): 1249-58. doi: 10.1164/rccm.201210-1934OC PMID: 23590266.
43. Satchidanandam V, Kumar N, Jumani RS, Challu V, Elangovan S, Khan NA. The glycosylated Rv1860 protein of mycobacterium tuberculosis inhibits dendritic cell mediated TH1 and TH17 polarization of T cells and abrogates protective immunity conferred by BCG. PLoS Pathog. 2014; 10 (6): e1004176. doi: 10.1371/journal.ppat.1004176 PMID: 24945624; PubMed Central PMCID: PMC4055742.
44. Verwaerde C, Debrie AS, Dombu C, Legrand D, Raze D, Lecher S, et al. HBHA vaccination may require both Th1 and Th17 immune responses to protect mice against tuberculosis. Vaccine. 2014; 32 (47): 6240-50. doi: 10.1016/j.vaccine.2014.09.024 PMID: 25252198.
45. Mayer-Barber KD, Andrade BB, Oland SD, Amaral EP, Barber DL, Gonzales J, et al. Host-directed therapy of tuberculosis based on interleukin-1 and type I interferon crosstalk. Nature. 2014; 511 (7507): 99-103. doi: 10.1038/nature13489 PMID: 24990750.
46. Antonelli LR, Gigliotti Rothfuchs A, Goncalves R, Roffe E, Cheever AW, Bafica A, et al. Intranasal Poly- IC treatment exacerbates tuberculosis in mice through the pulmonary recruitment of a pathogen-permissive monocyte/macrophage population. J Clin Invest. 2010; 120 (5): 1674-82. doi: 10.1172/ JCI40817 PMID: 20389020; PubMed Central PMCID: PMC2860920.
47. McKenna K, Beignon AS, Bhardwaj N. Plasmacytoid dendritic cells: linking innate and adaptive immunity. J Virol. 2005; 79 (1): 17-27. doi: 10.1128/JVI.79.1.17-27.2005 PMID: 15596797; PubMed Central PMCID: PMC538703.
48. Gupta V, Jaiswal A, Behera D, Prasad HK. Disparity in circulating peripheral blood dendritic cell subsets and cytokine profile of pulmonary tuberculosis patients compared with healthy family contacts. Hum Immunol. 2010; 71 (7): 682-91. doi: 10.1016/j.humimm.2010.03.010 PMID: 20381566.
49. Tsiganov EN, Verbina EM, Radaeva TV, Sosunov VV, Kosmiadi GA, Nikitina IY, et al. Gr-1dimCD11b+ immature myeloid-derived suppressor cells but not neutrophils are markers of lethal tuberculosis infection in mice. J Immunol. 2014; 192 (10): 4718-27. doi: 10.4049/jimmunol.1301365 PMID: 24711621.