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PMID: 15908359 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Common and unique gene expression signatures of human macrophages in response to four strains of Mycobacterium avium that differ in their growth and persistence characteristics.

Infection and immunity ·Vol. 73 ·No. 6 ·2005-06-00 ·Pages 3330-41

Blumenthal A, Lauber J, Hoffmann R, Ernst M, Keller C, Buer J, Ehlers S, Reiling N

Abstract

Classification of pathogenic species according to the distinct host transcriptional responses that they elicit may become a relevant tool for microarray-based diagnosis of infection. Individual strains of Mycobacterium avium, an opportunistic pathogen in humans, have previously been shown to differ in terms of growth and persistence. In order to cover a wide spectrum of virulence, we selected four M. avium isolates (2151SmO, 2151SmT, SE01, TMC724) that have distinct intramacrophage replication characteristics and cause differential activation in human macrophages. Following infection with each of these strains, the expression of 12,558 genes in human macrophages was systematically analyzed by microarray technology. Fifty genes (including genes encoding proinflammatory cytokines, chemokines, signaling, and adhesion molecules) were differentially expressed more than twofold in response to all of the M. avium isolates investigated and therefore constitute a common macrophage signature in response to M. avium. The magnitude of regulation of most of these genes was directly correlated with the host cell-activating capacity of the particular M. avium strain. The regulation of a number of genes not previously associated with mycobacterial infections was apparent; these genes included genes encoding lymphocyte antigen 64 and myosin X. In addition, individual response patterns typical for some M. avium isolates could be defined by the pronounced upregulation of interleukin-12p40 (IL-12p40) (in the case of 2151SmO) or the specific upregulation of SOCS-1 and IL-10 (in the case of SE01) in macrophages. TMC724, a strain of avian origin, could not be classified by any one of these schemes, possibly indicating the limits of pathogen categorization solely by immune response signatures.

MeSH Terms
Cells, Cultured Gene Expression Profiling Humans Interleukin-12/genetics Interleukin-12 Subunit p40 Macrophages/metabolism,microbiology Membrane Glycoproteins/physiology Mitogen-Activated Protein Kinases/metabolism Mycobacterium tuberculosis/growth & development Myosins/genetics Protein Subunits/genetics Receptors, Cell Surface/physiology Toll-Like Receptors Tumor Necrosis Factor-alpha/biosynthesis
Chemicals
Interleukin-12 Subunit p40 MYO10 protein, human Membrane Glycoproteins Protein Subunits Receptors, Cell Surface Toll-Like Receptors Tumor Necrosis Factor-alpha Interleukin-12 Mitogen-Activated Protein Kinases Myosins
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Blumenthal Antje
Division of Molecular Infection Biology, Department of Immunochemistry and Biochemical Microbiology, Research Center Borstel, Parkallee 22, D-23845 Borstel, Germany.
Lauber Jörg
Hoffmann Reinhard
Ernst Martin
Keller Christine
Buer Jan
Ehlers Stefan
Reiling Norbert
References (55)
55 references, click to expand
  1. Immunopathogenesis of Mycobacterium avium infection.
    Front Biosci. 1998 Aug 5;3:e141-8 PMID: 9693155
  2. Different types of pulmonary granuloma necrosis in immunocompetent vs. TNFRp55-gene-deficient mice aerogenically infected with highly virulent Mycobacterium avium.
    J Pathol. 1999 Sep;189(1):127-37 PMID: 10451499
  3. [Horseradish peroxidase: kinetic studies and optimization of peroxidase activity determination using the substrates H2O2 and 3,3',5,5'-tetramethylbenzidine].
    J Clin Chem Clin Biochem. 1985 Aug;23(8):453-60 PMID: 3903027
  4. Mycobacterium avium complex and the normal host: the other side of the coin.
    N Engl J Med. 1989 Sep 28;321(13):896-8 PMID: 2770826
  5. The role of macrophage activation and of Bcg-encoded macrophage function(s) in the control of Mycobacterium avium infection in mice.
    Clin Exp Immunol. 1990 Jun;80(3):324-31 PMID: 2115416
  6. Mycobacterium avium complex infection in the acquired immunodeficiency syndrome.
    N Engl J Med. 1991 May 9;324(19):1332-8 PMID: 2017230
  7. Capacity of Mycobacterium avium isolates to grow well or poorly in murine macrophages resides in their ability to induce secretion of tumor necrosis factor.
    Infect Immun. 1992 Oct;60(10):4410-3 PMID: 1398951
  8. Rough morphological variants of Mycobacterium avium. Characterization of genomic deletions resulting in the loss of glycopeptidolipid expression.
    J Biol Chem. 1993 May 15;268(14):10517-23 PMID: 8486704
  9. The Mycobacterium avium complex.
    Clin Microbiol Rev. 1993 Jul;6(3):266-310 PMID: 8358707
  10. Disseminated tuberculosis in interferon gamma gene-disrupted mice.
    J Exp Med. 1993 Dec 1;178(6):2243-7 PMID: 8245795
  11. Phenotypical and functional characterization of Fc gamma receptor I (CD64)-negative monocytes, a minor human monocyte subpopulation with high accessory and antiviral activity.
    Eur J Immunol. 1993 Dec;23(12):3126-35 PMID: 7504990
  12. Effector mechanisms involved in cytokine-mediated bacteriostasis of Mycobacterium avium infections in murine macrophages.
    Immunology. 1993 Nov;80(3):352-9 PMID: 8288311
  13. Loci of Mycobacterium avium ser2 gene cluster and their functions.
    J Bacteriol. 1994 Aug;176(16):4803-8 PMID: 8050992
  14. Role of gamma interferon and tumor necrosis factor alpha during T-cell-independent and -dependent phases of Mycobacterium avium infection.
    Infect Immun. 1994 Sep;62(9):3962-71 PMID: 8063414
  15. Characterization of the virulence of Mycobacterium avium complex (MAC) isolates in mice.
    Clin Exp Immunol. 1994 Nov;98(2):210-6 PMID: 7955524
  16. Tumour necrosis factor-alpha (TNF-alpha) in the host resistance to mycobacteria of distinct virulence.
    Clin Exp Immunol. 1995 Aug;101(2):308-13 PMID: 7648714
  17. Relationship between virulence of Mycobacterium avium strains and induction of tumor necrosis factor alpha production in infected mice and in in vitro-cultured mouse macrophages.
    Infect Immun. 1995 Oct;63(10):3759-64 PMID: 7558277
  18. IL-12-deficient mice are defective in IFN gamma production and type 1 cytokine responses.
    Immunity. 1996 May;4(5):471-81 PMID: 8630732
  19. Involvement of reactive oxygen intermediates in tumor necrosis factor alpha-dependent bacteriostasis of Mycobacterium avium.
    Infect Immun. 1996 Aug;64(8):3224-30 PMID: 8757857
  20. Mechanisms of granuloma formation in murine Mycobacterium avium infection: the contribution of CD4+ T cells.
    Int Immunol. 1996 Aug;8(8):1299-310 PMID: 8918699
  21. Lipoarabinomannan of Mycobacterium tuberculosis promotes protein tyrosine dephosphorylation and inhibition of mitogen-activated protein kinase in human mononuclear phagocytes. Role of the Src homology 2 containing tyrosine phosphatase 1.
    J Biol Chem. 1998 Jan 2;273(1):645-52 PMID: 9417127
  22. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency.
    Science. 1998 May 29;280(5368):1432-5 PMID: 9603732
  23. Interferon-gamma and interleukin-12 pathway defects and human disease.
    Cytokine Growth Factor Rev. 2000 Dec;11(4):321-33 PMID: 10959079
  24. Latent Mycobacterium tuberculosis-persistence, patience, and winning by waiting.
    Nat Med. 2000 Dec;6(12):1327-9 PMID: 11100115
  25. Hijacking and exploitation of IL-10 by intracellular pathogens.
    Trends Microbiol. 2001 Feb;9(2):86-92 PMID: 11173248
  26. Mycobacteria-induced TNF-alpha and IL-10 formation by human macrophages is differentially regulated at the level of mitogen-activated protein kinase activity.
    J Immunol. 2001 Sep 15;167(6):3339-45 PMID: 11544323
  27. Reprogramming of the macrophage transcriptome in response to interferon-gamma and Mycobacterium tuberculosis: signaling roles of nitric oxide synthase-2 and phagocyte oxidase.
    J Exp Med. 2001 Oct 15;194(8):1123-40 PMID: 11602641
  28. Alphabeta T cell receptor-positive cells and interferon-gamma, but not inducible nitric oxide synthase, are critical for granuloma necrosis in a mouse model of mycobacteria-induced pulmonary immunopathology.
    J Exp Med. 2001 Dec 17;194(12):1847-59 PMID: 11748285
  29. Activation of the mitogen-activated protein kinase signaling pathway is instrumental in determining the ability of Mycobacterium avium to grow in murine macrophages.
    J Immunol. 2002 Jan 15;168(2):825-33 PMID: 11777978
  30. Stereotyped and specific gene expression programs in human innate immune responses to bacteria.
    Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):972-7 PMID: 11805339
  31. Human macrophage activation programs induced by bacterial pathogens.
    Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1503-8 PMID: 11805289
  32. Genetic dissection of immunity to mycobacteria: the human model.
    Annu Rev Immunol. 2002;20:581-620 PMID: 11861613
  33. Human herpesvirus 8-derived viral IL-6 induces PTX3 expression in Kaposi's sarcoma cells.
    AIDS. 2002 May 24;16(8):F9-18 PMID: 12004288
  34. Control of mycobacterial replication in human macrophages: roles of extracellular signal-regulated kinases 1 and 2 and p38 mitogen-activated protein kinase pathways.
    Infect Immun. 2002 Sep;70(9):4961-7 PMID: 12183542
  35. Toll-like receptor 4 expression is required to control chronic Mycobacterium tuberculosis infection in mice.
    J Immunol. 2002 Sep 15;169(6):3155-62 PMID: 12218133
  36. Cutting edge: Toll-like receptor (TLR)2- and TLR4-mediated pathogen recognition in resistance to airborne infection with Mycobacterium tuberculosis.
    J Immunol. 2002 Oct 1;169(7):3480-4 PMID: 12244136
  37. Mycobacterium avium infection and modulation of human macrophage gene expression.
    J Immunol. 2002 Dec 1;169(11):6286-97 PMID: 12444135
  38. In vivo IL-10 production reactivates chronic pulmonary tuberculosis in C57BL/6 mice.
    J Immunol. 2002 Dec 1;169(11):6343-51 PMID: 12444141
  39. Characterization of virulence, colony morphotype and the glycopeptidolipid of Mycobacterium avium strain 104.
    Tuberculosis (Edinb). 2002;82(6):293-300 PMID: 12623272
  40. Novel IL-12 family members shed light on the orchestration of Th1 responses.
    Trends Immunol. 2003 Apr;24(4):207-12 PMID: 12697453
  41. Unique gene expression profiles of human macrophages and dendritic cells to phylogenetically distinct parasites.
    Blood. 2003 Jul 15;102(2):672-81 PMID: 12663451
  42. Proposed pathway for the biosynthesis of serovar-specific glycopeptidolipids in Mycobacterium avium serovar 2.
    Microbiology. 2003 Oct;149(Pt 10):2797-807 PMID: 14523113
  43. Mice lacking myeloid differentiation factor 88 display profound defects in host resistance and immune responses to Mycobacterium avium infection not exhibited by Toll-like receptor 2 (TLR2)- and TLR4-deficient animals.
    J Immunol. 2003 Nov 1;171(9):4758-64 PMID: 14568952
  44. Identification of genes expressed in tumor-associated macrophages.
    Immunobiology. 2003;207(5):351-9 PMID: 14575150
  45. Role of TLR4/MD-2 and RP105/MD-1 in innate recognition of lipopolysaccharide.
    Scand J Infect Dis. 2003;35(9):568-72 PMID: 14620136
  46. The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses.
    Immunity. 2003 Nov;19(5):641-4 PMID: 14614851
  47. Toll-like receptor 4 plays no role in susceptibility of mice to Mycobacterium tuberculosis infection.
    Tuberculosis (Edinb). 2003;83(6):367-71 PMID: 14623167
  48. Suppressors of cytokine signaling and immunity.
    Nat Immunol. 2003 Dec;4(12):1169-76 PMID: 14639467
  49. Chemokine secretion of rheumatoid arthritis synovial fibroblasts stimulated by Toll-like receptor 2 ligands.
    J Immunol. 2004 Jan 15;172(2):1256-65 PMID: 14707104
  50. The power of combinatorial immunology: IL-12 and IL-12-related dimeric cytokines in infectious diseases.
    Med Microbiol Immunol. 2004 Feb;193(1):1-17 PMID: 12836019
  51. Tuberculosis: a problem with persistence.
    Nat Rev Microbiol. 2003 Nov;1(2):97-105 PMID: 15035039
  52. Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients.
    Science. 1998 May 29;280(5368):1435-8 PMID: 9603733
  53. Mutation in the signal-transducing chain of the interferon-gamma receptor and susceptibility to mycobacterial infection.
    J Clin Invest. 1998 Jun 1;101(11):2364-9 PMID: 9616207
  54. Mycobacterium avium infection of mouse macrophages inhibits IFN-gamma Janus kinase-STAT signaling and gene induction by down-regulation of the IFN-gamma receptor.
    J Immunol. 1999 Aug 15;163(4):2041-8 PMID: 10438942
  55. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g.
    Scand J Clin Lab Invest Suppl. 1968;97:77-89 PMID: 4179068
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
2005-06-00
Pages
3330-41
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC1111816
Subset
IM
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