Profiling early lung immune responses in the mouse model of tuberculosis

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Kang, Dongwan D ^a,b   Lin, Yinyao ^b   Moreno, Javier Rangel ^c   Randall, Troy D ^c   Khader, Shabaana A ^b  

^a UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD14 ANTIGEN; CD209 ANTIGEN; CHEMOKINE; COLLAGENASE 3; DECTIN 1; DECTIN 2; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 30; GELATINASE B; GLYCOPROTEIN P 15095; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 10; INTERLEUKIN 12 RECEPTOR BETA1; INTERLEUKIN 12P35; INTERLEUKIN 12P40; INTERLEUKIN 4; INTERLEUKIN 6; MESSENGER RNA; NEUTROPHIL COLLAGENASE; STAT1 PROTEIN; STROMELYSIN 2; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 12; TOLL LIKE RECEPTOR 13; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; BONE MARROW CELL; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE MODEL; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; LUNG TUBERCULOSIS; MONOCYTE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INDUCTION; TH1 CELL; ANIMAL; BIOSYNTHESIS; GENE EXPRESSION PROFILING; IMMUNITY; IMMUNOLOGY; LUNG; MICROBIOLOGY; PATHOLOGY; TIME;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM TUBERCULOSIS;

ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; IMMUNITY; LUNG; MICE; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHIL INFILTRATION; RNA, MESSENGER; TH1 CELLS; TIME FACTORS; TUBERCULOSIS, PULMONARY;

EID: 79251589081     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016161     Document Type: Article

References (79)

1. Dye C, Scheele S, Dolin P, Pathania V, Raviglione M (1999) Global Burden of Tuberculosis. Estimated Incidence, Prevalence, and Mortality by Country. Journal of the American Medical Association 282: 677-686.
2. Koenig R (2008) Drug-resistant tuberculosis. In South Africa, XDR TB and HIV prove a deadly combination. Science 319: 894-897.
3. Flynn J, Chan J (2001) Immunology of tuberculosis. Annual Review of Immunology 19: 93-129.
4. Trinchieri G, Pflanz S, Kastelein R (2003) The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 19: 641-644.
5. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, et al. (1993) Disseminated tuberculosis in interferon gamma gene-disrupted mice. Journal of Experimental Medicine 178: 2243-2247.
6. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, et al. (1993) An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. Journal of Experimental Medicine 178: 2249-2254.
7. Casanova JL (2001) Mendelian susceptibility to mycobacterial infection in man. Swiss Med Wkly 131: 445-454.
8. Reiley WW, Calayag MD, Wittmer ST, Huntington JL, Pearl JE, et al. (2008) ESAT-6-specific CD4 T cell responses to aerosol Mycobacterium tuberculosis infection are initiated in the mediastinal lymph nodes. Proc Natl Acad Sci U S A 105: 10961-10966.
9. Cooper AM, Khader SA (2008) The role of cytokines in the initiation, expansion, and control of cellular immunity to tuberculosis. Immunol Rev 226: 191-204.
10. Khader SA, Rangel-Moreno J, Fountain JJ, Martino CA, Reiley WW, et al. (2009) In a murine tuberculosis model, the absence of homeostatic chemokines delays granuloma formation and protective immunity. J Immunol 183: 8004-8014.
11. Roberts A, Cooper A, Belisle J, Turner J, Gonzalez-Juarerro M, et al. (2002) Murine Models of Tuberculosis. In: Kaufmann S, Kabelitz D, eds. Methods in Microbiology. Second ed. London: Academic Press. pp 433-462.
12. Khader SA, Pearl JE, Sakamoto K, Gilmartin L, Bell GK, et al. (2005) IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFNgamma responses if IL-12p70 is available. J Immunol 175: 788-795.
13. Wu Z, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F (2004) A Model-Based Background Adjustment for Oligonucleotide Expression Arrays. journal of the American Statistical Association 99: 909-917.
14. Breitling R, Armengaud P, Amtmann A, Herzyk P (2004) Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 573: 83-92.
15. Jeffery IB, Higgins DG, Culhane AC (2006) Comparison and evaluation of methods for generating differentially expressed gene lists from microarray data. BMC Bioinformatics 7: 359.
16. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
17. Gonzalez-Juarrero M, Kingry LC, Ordway DJ, Henao-Tamayo M, Harton M, et al. (2009) Immune response to Mycobacterium tuberculosis and identification of molecular markers of disease. Am J Respir Cell Mol Biol 40: 398-409.
18. Underhill DM, Ozinsky A, Hajjar AM, Stevens A, Wilson CB, et al. (1999) The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401: 811-815.
19. Kincaid EZ, Wolf AJ, Desvignes L, Mahapatra S, Crick DC, et al. (2007) Codominance of TLR2-dependent and TLR2-independent modulation of MHC class II in Mycobacterium tuberculosis infection in vivo. J Immunol 179: 3187-3195.
20. Pompei L, Jang S, Zamlynny B, Ravikumar S, McBride A, et al. (2007) Disparity in IL-12 release in dendritic cells and macrophages in response to Mycobacterium tuberculosis is due to use of distinct TLRs. J Immunol 178: 5192-5199.
21. Bafica A, Scanga C, Feng C, Leifer C, Cheever A, et al. (2005) TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. Journal of Experimental Medicine 202: 1715-1724.
22. Bowdish DM, Sakamoto K, Kim MJ, Kroos M, Mukhopadhyay S, et al. (2009) MARCO, TLR2, and CD14 are required for macrophage cytokine responses to mycobacterial trehalose dimycolate and Mycobacterium tuberculosis. PLoS Pathog 5: e1000474.
23. Tailleux L, Schwartz O, Herrmann JL, Pivert E, Jackson M, et al. (2003) DCSIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J Exp Med 197: 121-127.
24. Rothfuchs AG, Bafica A, Feng CG, Egen JG, Williams DL, et al. (2007) Dectin- 1 interaction with Mycobacterium tuberculosis leads to enhanced IL-12p40 production by splenic dendritic cells. J Immunol 179: 3463-3471.
25. Zenaro E, Donini M, Dusi S (2009) Induction of Th1/Th17 immune response by Mycobacterium tuberculosis: role of dectin-1, Mannose Receptor, and DCSIGN. J Leukoc Biol 86: 1393-1401.
26. Ishikawa E, Ishikawa T, Morita YS, Toyonaga K, Yamada H, et al. (2009) Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by Ctype lectin Mincle. J Exp Med 206: 2879-2888.
27. Aoki N, Kimura Y, Kimura S, Nagato T, Azumi M, et al. (2009) Expression and functional role of MDL-1 (CLEC5A) in mouse myeloid lineage cells. J Leukoc Biol 85: 508-517.
28. Taylor JL, Hattle JM, Dreitz SA, Troudt JM, Izzo LS, et al. (2006) Role for matrix metalloproteinase 9 in granuloma formation during pulmonary Mycobacterium tuberculosis infection. Infect Immun 74: 6135-6144.
29. Appelberg R, Castro AG, Pedrosa J, Minoprio P (1994) Role of interleukin-6 in the induction of protective T cells during mycobacterial infections in mice. Immunology 82: 361-364.
30. Saunders BM, Tran S, Ruuls S, Sedgwick JD, Briscoe H, et al. (2005) Transmembrane TNF is sufficient to initiate cell migration and granuloma formation and provide acute, but not long-term, control of Mycobacterium tuberculosis infection. J Immunol 174: 4852-4859.
31. Ghosh S, Chackerian AA, Parker CM, Ballantyne CM, Behar SM (2006) The LFA-1 adhesion molecule is required for protective immunity during pulmonary Mycobacterium tuberculosis infection. J Immunol 176: 4914-4922.
32. Pasquinelli V, Quiroga MF, Martinez GJ, Zorrilla LC, Musella RM, et al. (2004) Expression of signaling lymphocytic activation molecule-associated protein interrupts IFN-gamma production in human tuberculosis. J Immunol 172: 1177-1185.
33. Boles KS, Nakajima H, Colonna M, Chuang SS, Stepp SE, et al. (1999) Molecular characterization of a novel human natural killer cell receptor homologous to mouse 2B4. Tissue Antigens 54: 27-34.
34. Pflugh DL, Maher SE, Bothwell AL (2000) Ly-6I, a new member of the murine Ly-6 superfamily with a distinct pattern of expression. J Immunol 165: 313-321.
35. Ravetch JV, Bolland S (2001) IgG Fc receptors. Annu Rev Immunol 19: 275-290.
36. Maglione PJ, Xu J, Casadevall A, Chan J (2008) Fc gamma receptors regulate immune activation and susceptibility during Mycobacterium tuberculosis infection. J Immunol 180: 3329-3338.
37. Ehrt S, Schnappinger D, Bekiranov S, Drenkow J, Shi S, et al. (2001) Reprogramming of the macrophage transcriptome in response to interferongamma and Mycobacterium tuberculosis: signaling roles of nitric oxide synthase- 2 and phagocyte oxidase. J Exp Med 194: 1123-1140.
38. Chang CH, Guerder S, Hong SC, van Ewijk W, Flavell RA (1996) Mice lacking the MHC class II transactivator (CIITA) show tissue-specific impairment of MHC class II expression. Immunity 4: 167-178.
39. MacMicking J, Taylor G, McKinney J (2003) Immune control of Tuberculosis by IFN-g-inducible LRG-47. Science 302: 654-659.
40. El Kasmi KC, Qualls JE, Pesce JT, Smith AM, Thompson RW, et al. (2008) Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat Immunol 9: 1399-1406.
41. Olakanmi O, Schlesinger LS, Ahmed A, Britigan BE (2004) The nature of extracellular iron influences iron acquisition by Mycobacterium tuberculosis residing within human macrophages. Infect Immun 72: 2022-2028.
42. Mellor A (2005) Indoleamine 2,3 dioxygenase and regulation of T cell immunity. Biochem Biophys Res Commun 338: 20-24.
43. Almeida AS, Lago PM, Boechat N, Huard RC, Lazzarini LC, et al. (2009) Tuberculosis is associated with a down-modulatory lung immune response that impairs Th1-type immunity. J Immunol 183: 718-731.
44. Deretic V, Singh S, Master S, Harris J, Roberts E, et al. (2006) Mycobacterium tuberculosis inhibition of phagolysosome biogenesis and autophagy as a host defence mechanism. Cell Microbiol 8: 719-727.
45. Kyei GB, Vergne I, Chua J, Roberts E, Harris J, et al. (2006) Rab14 is critical for maintenance of Mycobacterium tuberculosis phagosome maturation arrest. Embo J 25: 5250-5259.
46. Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, et al. (2000) Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 192: 1027-1034.
47. Jurado JO, Alvarez IB, Pasquinelli V, Martinez GJ, Quiroga MF, et al. (2008) Programmed death (PD)-1:PD-ligand 1/PD-ligand 2 pathway inhibits T cell effector functions during human tuberculosis. J Immunol 181: 116-125.
48. Riedel DD, Kaufmann SH (1997) Chemokine secretion by human polymorphonuclear granulocytes after stimulation with Mycobacterium tuberculosis and lipoarabinomannan. Infect Immun 65: 4620-4623.
49. Walz A, Burgener R, Car B, Baggiolini M, Kunkel SL, et al. (1991) Structureand neutrophil-activating properties of a novel inflammatory peptide (ENA-78) with homology to interleukin 8. J Exp Med 174: 1355-1362
50. Chang MS, McNinch J, Basu R, Simonet S (1994) Cloning and characterization of the human neutrophil-activating peptide (ENA-78) gene. J Biol Chem 269: 25277-25282.
51. Oliveira SH, Canetti C, Ribeiro RA, Cunha FQ (2008) Neutrophil migration induced by IL-1beta depends upon LTB4 released by macrophages and upon TNF-alpha and IL-1beta released by mast cells. Inflammation 31: 36-46.
52. Calkins CM, Bensard DD, Shames BD, Pulido EJ, Abraham E, et al. (2002) IL-1 regulates in vivo C-X-C chemokine induction and neutrophil sequestration following endotoxemia. J Endotoxin Res 8: 59-67.
53. Mayer-Barber KD, Barber DL, Shenderov K, White SD, Wilson MS, et al. (2010) Caspase-1 independent IL-1beta production is critical for host resistance to mycobacterium tuberculosis and does not require TLR signaling in vivo. J Immunol 184: 3326-3330.
54. Singh PP, Kaur S (2006) Serum amyloid P-component in murine tuberculosis: induction kinetics and intramacrophage Mycobacterium tuberculosis growth inhibition in vitro. Microbes Infect 8: 541-551.
55. de Beer FC, Nel AE, Gie RP, Donald PR, Strachan AF (1984) Serum amyloid A protein and C-reactive protein levels in pulmonary tuberculosis: relationship to amyloidosis. Thorax 39: 196-200.
56. Sommer G, Weise S, Kralisch S, Scherer PE, Lossner U, et al. (2008) The adipokine SAA3 is induced by interleukin-1beta in mouse adipocytes. J Cell Biochem 104: 2241-2247.
57. Hatanaka E, Pereira Ribeiro F, Campa A (2003) The acute phase protein serum amyloid A primes neutrophils. FEMS Immunol Med Microbiol 38: 81-84.
58. Bjorkman L, Karlsson J, Karlsson A, Rabiet MJ, Boulay F, et al. (2008) Serum amyloid A mediates human neutrophil production of reactive oxygen species through a receptor independent of formyl peptide receptor like-1. J Leukoc Biol 83: 245-253.
59. Pechkovsky DV, Zalutskaya OM, Ivanov GI, Misuno NI (2000) Calprotectin (MRP8/14 protein complex) release during mycobacterial infection in vitro and in vivo. FEMS Immunol Med Microbiol 29: 27-33.
60. Ryckman C, Vandal K, Rouleau P, Talbot M, Tessier PA (2003) Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion. J Immunol 170: 3233-3242.
61. Vandal K, Rouleau P, Boivin A, Ryckman C, Talbot M, et al. (2003) Blockade of S100A8 and S100A9 suppresses neutrophil migration in response to lipopolysaccharide. J Immunol 171: 2602-2609.
62. Rahimi F, Hsu K, Endoh Y, Geczy CL (2005) FGF-2, IL-1beta and TGF-beta regulate fibroblast expression of S100A8. FEBS J 272: 2811-2827.
63. Maus UA, Waelsch K, Kuziel WA, Delbeck T, Mack M, et al. (2003) Monocytes are potent facilitators of alveolar neutrophil emigration during lung inflammation: role of the CCL2-CCR2 axis. J Immunol 170: 3273-3278.
64. Kipnis A, Basaraba R, Orme I, Cooper A (2003) Role of chemokine CCL2 in the protective response to early murine pulmonary tuberculosis. Immunology 109: 547-551.
65. Mordue DG, Sibley LD (2003) A novel population of Gr-1+-activated macrophages induced during acute toxoplasmosis. J Leukoc Biol 74: 1015-1025.
66. Robben PM, LaRegina M, Kuziel WA, Sibley LD (2005) Recruitment of Gr-1+ monocytes is essential for control of acute toxoplasmosis. J Exp Med 201: 1761-1769.
67. Landsman L, Varol C, Jung S (2007) Distinct differentiation potential of blood monocyte subsets in the lung. J Immunol 178: 2000-2007.
68. Lin Y, Ritchea S, Logar A, Slight S, Messmer M, et al. (2009) Interleukin-17 Is Required for T Helper 1 Cell Immunity and Host Resistance to the Intracellular Pathogen Francisella tularensis. Immunity 31: 799-810.
69. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE (2008) Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 83: 64-70.
70. Wolf AJ, Desvignes L, Linas B, Banaiee N, Tamura T, et al. (2008) Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J Exp Med 205: 105-115.
71. Noss EH, Harding CV, Boom WH (2000) Mycobacterium tuberculosis inhibits MHC class II antigen processing in murine bone marrow macrophages. Cell Immunol 201: 63-74.
72. Fulton SA, Reba SM, Pai RK, Pennini M, Torres M, et al. (2004) Inhibition of major histocompatibility complex II expression and antigen processing in murine alveolar macrophages by Mycobacterium bovis BCG and the 19- kilodalton mycobacterial lipoprotein. Infect Immun 72: 2101-2110.
73. Jung YJ, Ryan L, LaCourse R, North RJ (2005) Properties and protective value of the secondary versus primary T helper type 1 response to airborne Mycobacterium tuberculosis infection in mice. J Exp Med 201: 1915-1924.
74. Khader SA, Bell GK, Pearl JE, Fountain JJ, Rangel-Moreno J, et al. (2007) IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol 8: 369-377.
75. Sadek MI, Sada E, Toossi Z, Schwander SK, Rich EA (1998) Chemokines induced by infection of mononuclear phagocytes with mycobacteria and present in lung alveoli during active pulmonary tuberculosis. Am J Respir Cell Mol Biol 19: 513-521.
76. Jones GS, Amirault HJ, Andersen BR (1990) Killing of Mycobacterium tuberculosis by neutrophils: a nonoxidative process. J Infect Dis 162: 700-704.
77. May ME, Spagnuolo PJ (1987) Evidence for activation of a respiratory burst in the interaction of human neutrophils with Mycobacterium tuberculosis. Infect Immun 55: 2304-2307.
78. Denis M (1991) Human neutrophils, activated with cytokines or not, do not kill virulent Mycobacterium tuberculosis. J Infect Dis 163: 919-920.
79. Seiler P, Aichele P, Bandermann S, Hauser AE, Lu B, et al. (2003) Early granuloma formation after aerosol Mycobacterium tuberculosis infection is regulated by neutrophils via CXCR3-signaling chemokines. Eur J Immunol 33: 2676-2686.