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Mycobacteria and innate cells: critical encounter for immunogenicity

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Abstract

Protective immunity against mycobacterial infections such as Mycobacterium tuberculosis is mediated by interactions between specific T cells and activated macrophages. To date, many aspects of mycobacterial immunity have shown that innate cells are the key elements that substantially influence the subsequent adaptive host response. During the early phases of infection, phagocytic cells and innate lymphocyte subsets play a pivotal role. Here we summarize the findings of recent investigations on macrophages, dendritic cells and γδ T lymphocytes in the response to mycobacteria.

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Abbreviations

APC:

antigen-presenting cell

ATP:

adenosine triphosphate

BCG:

bacille Calmette-Guérin

DC:

dendritic cell

DOXP:

1-deoxy-d-xylulose-5phosphate

GM-CSF:

granulocyte-macrophage colony-stimulating factor

IFN:

interferon

IL:

interleukin

imDC:

immature dendritic cell

LAM:

lipoarabinomannan

LPS:

lipopolysaccharide

MDM:

monocyte-derived macrophage

MHC:

major histocompatibility complex

MTB:

Mycobacterium tuberculosis

MVA:

mevalonate

Th:

T-helper

TLR:

toll-like receptors

TNF:

tumour necrosis factor

References

  • Bocchino M, Galati D, Sanduzzi A, Colizzi V, Brunetti E and Mancino G 2005 Role of mycobacteria-induced monocyte/macrophage apoptosis in the pathogenesis of human tuberculosis; Int. J. Tuberc. Lung. Dis. 9 375–383

    CAS  PubMed  Google Scholar 

  • Bodnar K A, Serbina N V and Flynn J L 2001 Fate of Mycobacterium tuberculosis within murine dendritic cells; Infec. Immun. 69 800–809

    Article  CAS  Google Scholar 

  • Boom WH 1999 γδ T cells and Mycobacterium tuberculosis; Microbes Infect. 1 187–195

    Article  CAS  Google Scholar 

  • Caccamo N, Sireci G, Meraviglia S, Dieli F, Ivanyi J and Salerno A 2006 Gammadelta T cells condition dendritic cells in vivo for priming pulmonary CD8 T cell responses against Mycobacterium tuberculosis; Eur. J. Immunol. 36 2681–2690

    Article  CAS  Google Scholar 

  • Cella M, Sallusto F and Lanzavecchia A 1997 Origin, maturation and antigen presenting function of dendritic cells; Curr. Opin. Immunol. 9 10–16

    Article  CAS  Google Scholar 

  • Chapuis F, Rosenzwajg M, Yagello M, Ekman M, Biberfeld P and Gluckman J C 1997 Differentiation of human dendritic cells from monocytes in vitro; Eur. J. Immunol. 27 431–441

    Article  CAS  Google Scholar 

  • Chomorat P, Banchereau J, Davoust J and Palucka A K 2000 IL-6 switches the differentiation of monocytes from dendritic cells to macrophages; Nat. Immunol. 1 510–514

    Article  Google Scholar 

  • Ciaramella A, Martino A, Cicconi R, Colizzi V and Fraziano M 2000 Mycobacterial 19-kDa lipoprotein mediates Mycobacterium tuberculosis-induced apoptosis in monocytes/macrophages at early stages of infection; Cell Death Differ. 7 1270–1272

    Article  CAS  Google Scholar 

  • Ciaramella A, Cavone A, Santucci M B, Amicosante M, Martino A, Auricchio G, Pucillo L P, Colizzi V and Fraziano M 2002 Proinflammatory cytokines in the course of Mycobacterium tuberculosis-induced apoptosis in monocytes/macrophages; J. Infect. Dis. 186 1277–1282

    Article  CAS  Google Scholar 

  • Ciaramella A, Cavone A, Santucci M B, Garg S K, Sanarico N, Bocchino M, Galati D, Martino A, Auricchio G, D’Orazio M, Stewart G M, Neyrolles O, Young D B, Colizzi V and Fraziano M 2004 Induction of apoptosis and release of interleukin-1 beta by cell wall-associated 19-kDa lipoprotein during the course of mycobacterial infection; J. Infect. Dis. 190 1167–1176

    Article  CAS  Google Scholar 

  • Di Virgilio F 1995 The P2Z purinoreceptors: an intriguing role in immunity, inflammation and cell death; Immunol. Today 16 524–528

    Article  Google Scholar 

  • Delneste Y, Charbonnier P, Herbault N, Magistrelli G, Caron G, Bonnefoy J Y and Jeannine P 2003 Interferon-{gamma} switches monocyte differentiation from dendritic cells to macrophages; Blood 101 143–150

    Article  CAS  Google Scholar 

  • Dudziak D, Kamphorst A O, Heidkamp G F, Buchholz V R, Trumpfheller C, Yamazaki S, Cheong C, Liu K, Lee H W, Park C G, Steinman R M and Nussenzweig M C 2007 Differential antigen processing by dendritic cell subsets in vivo; Science 315 107–111

    Article  CAS  Google Scholar 

  • Frattazzi C, Arbeit R D, Carini C and Remold H G 1997 Programmed cell death of Mycobacterium avium serovar 4-infected human macrophages prevents the mycobacteria from spreading and induces mycobacterial growth inhibition by freshly added, uninfected macrophages; J. Immunol. 164 389–397

    Google Scholar 

  • Gately M K, Renzetti L M, Magram J, Stern A S, Adorini L, Gubler U and Presky D H 1998 The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses; Annu. Rev. Immunol. 16 495–521

    Article  CAS  Google Scholar 

  • Giacobini E, Iona E, Ferroni L, Miettinen M, Fattorini L, Orefici G, Julkunen I and Coccia E M 2001 Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response; J. Immunol. 166 7033–7041

    Article  Google Scholar 

  • Girardi M 2006 Immunosurveillance and immuneregulation by γδ T cells; J. Invest. Dermatol. 126 25–31

    Article  CAS  Google Scholar 

  • Gober H J, Kistowska M, Angman L, Jeno P, Mori L and De Libero G 2003 Human T-cell receptor gammadelta cells recognize endogenous mevalonate metabolites in tumor cells; J. Exp. Med. 197 163–168

    Article  CAS  Google Scholar 

  • Hayday A C 2000 γδ cells: a right time and a right place for a conserved third way of protection; Annu. Rev. Immunol. 18 975–1026

    Article  CAS  Google Scholar 

  • Hickman S P, Chan J and Salgame P 2002 Mycobacterium tuberculosis induces differential cytokine production from dendritic cells and macrophages with divergent effects on naive T cell polarization; J. Immunol. 168 4636–4642

    Article  CAS  Google Scholar 

  • Hirsch C S, Elner J J, Russell D G and Rich E A 1994 Complement receptor-mediated uptake and tumor necrosis factor alpha-mediated growth inhibition of Mycobacteriumm tuberculosis infection in human tuberculosis; J. Infect. Dis. 183 779–788

    Article  Google Scholar 

  • Hoft D F, Brown R M and Roodman S T 1998 Bacille Calmette Guerin vaccination enhances human gamma delta T cell responsiveness to mycobacteria suggestive of a memory like phenotype; J. Immunol. 161 1045–1054

    CAS  PubMed  Google Scholar 

  • Houben E N, Nguyen L and Pieters J 2006 Interaction of pathogenic mycobacteria with the host immune system; Curr. Opin. Microbiol. 9 76–85

    Article  CAS  Google Scholar 

  • Hunter C I and Reiner S L 2000 Cytokines and T cells in host defense; Curr. Opin. Immunol. 12 413–418

    Article  CAS  Google Scholar 

  • Janis E M, Kaufmann S H E, Scwartz R H and Pardoll D M 1989 Activation of γδ T cells in the primary immune response to Mycobacterium tuberculosis; Science 244 713–716

    Article  CAS  Google Scholar 

  • Jo E K, Yang C S, Choi C H and Harding C V 2007 Intracellular signalling cascades regulating innate immune responses to mycobacteria: branching out from toll-like receptors; Cell Microbiol. 9 1087–1098

    Article  CAS  Google Scholar 

  • Keane J, Balcewicz-Sablinska M K, Remold H G, Chupp G L, Meek B B, Fenton M J and Kornfeld H 1997 Infection of Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis; Infect. Immun. 65 298–304

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kusner D J 2005 Mechanisms of mycobacterial persistence in tuberculosis; Clin. Immunol. 114 239–247

    Article  CAS  Google Scholar 

  • Lammas D A, Stober C, Harvey C J, Kendrick N, Panchalingam S and Kumararatne D S 1997 ATP-induced killing of mycobacteria by human macrophages is mediated by purinergic P2Z (P2X7) receptors; Immunity 7 433–444

    Article  CAS  Google Scholar 

  • Laochumroonvorapong P, Paul S, Elkin K B and Kaplan G 1996 H2O2 induces monocyte apoptosis and reduces viability of Mycobacterium avium-M intracellulare within cultured human monocytes; Infect. Immun. 64 452–459

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee J, Choi K, Olin M R, Cho S N and Molitor T W 2004 γδ T cells in immunity induced by Mycobacterium bovis bacillus Calmette Guerin vaccination; Infect. Immun. 72 1504–1511

    Article  CAS  Google Scholar 

  • Lopez M, Sly L M, Liu Y, Young D, Cooper H and Reiner N E 2003 The 19-kDa Mycobacterium tuberculosis protein induces macrophage apoptosis through toll-like receptor-2; J. Immunol. 170 2409–2416

    Article  CAS  Google Scholar 

  • Lyakh L A, Koski G K, Telford W, Gress R E, Cohen P A and Rice N R 2000 Bacterial lipopolysaccharide, TNF-{alpha} and calcium ionophore under serum-free conditions promote rapid dendritic cell-like differentiation in CD14+ monocytes through distinct pathways that activate NK-{kappa}B; J. Immunol. 165 3647–3655

    Article  CAS  Google Scholar 

  • Mariotti S, Teloni R, Iona E, Fattorini L, Giannoni F, Romagnoli G, Orefici G and Nisini R 2002 Mycobacterium tuberculosis subverts the differentiation of human monocytes into dendritic cells; Eur. J. Immunol. 32 3050–3058

    Article  CAS  Google Scholar 

  • Martino A, Sacchi A, Sanarico N, Spadaro F, Spadaro F, Ramoni C, Ciaramella A, Pucillo L P, Colizzi V and Vendetti S 2004 Dendritic cells derived from BCG-infected precursors induce Th2-like immune response; J. Leukoc. Biol. 76 827–834

    Article  CAS  Google Scholar 

  • Martino A, Sacchi A, Volpe E, Agrati C, De Santis R, Pucillo LP, Colizzi V and Vendetti S 2005 Non-pathogenic Mycobacterium smegmatis induces the differentiation of human monocytes directly into fully mature dendritic cells; J. Clin. Immunol. 25 365–375

    Article  CAS  Google Scholar 

  • Martino A, Casetti R, D’Alessandri A, Sacchi A and Poccia F 2005 Complementary function of gamma delta T-lymphocytes and dendritic cells in the response to isopentenyl-pyrophosphate and lipopolysaccharide antigens; J. Clin. Immunol. 25 230–237

    Article  CAS  Google Scholar 

  • Martino A and Poccia F 2005 Close encounters of different kinds: dendritic cells and gammadelta T cells heighten therapeutic applications; Immunol. Lett. 101 115

    Article  CAS  Google Scholar 

  • Martino A, Sacchi A, Colizzi V and Vendetti S 2006 Mycobacteria and dendritic cell differentiation: escape or control of immunity; Immunol. Lett. 102 115–117

    Article  CAS  Google Scholar 

  • Martino A, Casetti R and Poccia F 2007 Enhancement of BCG-induced Th1 immune response through Vgamma9V delta2 T cell activation with non-peptidic drugs; Vaccine 25 1023–1029

    Article  CAS  Google Scholar 

  • Martino A, Casetti R, Sacchi A and Poccia F 2007 Central Memory v{gamma}9V{delta}2 T lymphocytes primed and expanded by bacillus Calmette-Guerin-infected dendritic cells kill mycobacterial-infected monocytes; J. Immunol. 179 3057–3064

    Article  CAS  Google Scholar 

  • Mueller P and Pieters J 2006 Modulation of macrophage antimicrobial mechanisms by pathogenic mycobacteria; Immunobiology 211 549–556

    Article  CAS  Google Scholar 

  • Nigou J, Zelle-Rieser C, Gilleron M, Thurnher M and Puzo G 2001 Mannosylated lipoarabinomannans inhibit IL-12 production by human dendritic cells: evidence for a negative signal delivered through the mannose receptor; J. Immunol. 166 7477–7485

    Article  CAS  Google Scholar 

  • Oliveira R B, Ochoa M T, Sieling P A, Rea T H, Rambukkana A, Sarno E N and Modlin R L 2003 Expression of toll-like receptor on human Schwann cells: a mechanism of nerve damage in leprosy; Infect. Immun. 71 1427–1433

    Article  CAS  Google Scholar 

  • Placido R, Mancino G, Amendola A, Placido R, Mancino G, Amendola A, Mariani F, Vendetti S, Piacentini M, Sanduzzi A, Bocchino M L, Zembala M and Colizzi V 1997 Apoptosis of human monocytes/macrophages in Mycobacterium tuberculosis infection; J. Pathol. 181 31–38

    Article  CAS  Google Scholar 

  • Reis e Sousa C 2004 Activation of dendritic cells: translating innate into adaptive immunity; Curr. Opin. Immunol. 16 21–25

    Article  CAS  Google Scholar 

  • Shen Y, Zhou D, Qiu L, Lai X, Simon M, Shen L, Kou Z, Wang Q, et al 2002 Adaptive immune response of Vgamma2V delta2+ T cells during mycobacterial infections; Science 295 2255–2258

    Article  CAS  Google Scholar 

  • Tanaka Y, Sano S, Nieves E, De Libero G, Rosa D, Modlin R L, Brenner M B, Bloom B R and Morita C T 1994 Non peptide ligands for human gamma delta T-cells; Proc. Natl. Acad. Sci. USA 91 8175–8179

    Article  CAS  Google Scholar 

  • Thoma-Uszynski S, Stenger S and Modlin R L 2000 CTL-mediated killing of intracellular Mycobacterium tuberculosis is independent of target cell nuclear apoptosis; J. Immunol. 165 5773–5779

    Article  CAS  Google Scholar 

  • Vordermeier H M, Zhu X and Harris D P 1997 Induction of CD8+ CTL recognizing mycobacterial peptides; Scand. J. Immunol. 45 521–526

    Article  CAS  Google Scholar 

  • Winau F, Weber S, Sad S, de Diego J, Hoops SL, Breiden B, Sandhoff K, Brinkmann V, Kaufmann S H and Schaible U E 2006 Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis; Immunity 24 105–117

    Article  CAS  Google Scholar 

  • Zhang Y, Doertfler M, Lee T C, Guillemin B and Rom W N 1993 Mechanisms of stimulation of interleukin-1 beta and tumor necrosis factor-alpha by Mycobacterium tuberculosis components; J. Clin. Invest. 91 2076–2083

    Article  CAS  Google Scholar 

  • Zhou LJ and Tedder TF 1996 CD14+ blood monocytes can differentiate into functionally mature CD83+ dendritic cells; Proc. Natl. Acad. Sci. USA 93 2588–2592

    Article  CAS  Google Scholar 

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Correspondence to Angelo Martino.

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Martino, A. Mycobacteria and innate cells: critical encounter for immunogenicity. J Biosci 33, 137–144 (2008). https://doi.org/10.1007/s12038-008-0029-4

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