Home LiteratureArticle Details
PMID: 9488413 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Expression of virulence of Mycobacterium tuberculosis within human monocytes: virulence correlates with intracellular growth and induction of tumor necrosis factor alpha but not with evasion of lymphocyte-dependent monocyte effector functions.

Infection and immunity ·Vol. 66 ·No. 3 ·1998-03-00 ·Pages 1190-9

Silver RF, Li Q, Ellner JJ

Abstract

We assessed the applicability of an in vitro model of low-level infection of human monocytes to the characterization of the virulence of strains of the Mycobacterium tuberculosis family. Peripheral blood monocytes were infected at a 1:1 ratio with the virulent M. tuberculosis strain H37Rv, the avirulent M. tuberculosis strain H37Ra, and the attenuated M. bovis strain BCG. Both the percentages of cells infected by the three strains and the initial numbers of intracellular organisms were equivalent, as were levels of monocyte viability up to 7 days following infection. Intracellular growth reflected virulence, as H37Rv replicated in logarithmic fashion throughout the assay, BCG growth reached a plateau at 4 days, and H37Ra did not grow at all. The same patterns of growth were observed following infection of human alveolar macrophages with H37Rv and H37Ra. Monocyte production of tumor necrosis factor alpha was significantly higher following infection with virulent H37Rv than with either BCG or H37Ra. In contrast, there was no clear correlation of interleukin 10 production with virulence. Nonadherent cells of purified-protein-derivative-positive donors mediated equivalent degrees of reduction of the intracellular growth of H37Rv, BCG, and H37Ra. Low-level infection of human monocytes with H37Rv, BCG, and H37Ra thus provides an in vitro model for assessment of the virulence of these M. tuberculosis family strains. Furthermore, it is suggested that the virulence of these strains is expressed primarily by their differing abilities to adapt to the intracellular environment of the mononuclear phagocyte.

MeSH Terms
Adult Humans Interleukin-10/biosynthesis Lymphocytes/physiology Middle Aged Monocytes/microbiology,physiology Mycobacterium tuberculosis/growth & development,immunology,pathogenicity Phagocytosis Tumor Necrosis Factor-alpha/biosynthesis Virulence
Chemicals
Tumor Necrosis Factor-alpha Interleukin-10
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Silver R F
Division of Pulmonary and Critical Care Medicine, Case Western Reserve University School of Medicine, Cleveland, Ohio 44106-4941, USA. rfs4@po.cwru.edu
Li Q
Ellner J J
References (58)
58 references, click to expand
  1. A comparative study of the virulence of mycobacterium tuberculosis measured in mice and guinea pigs.
    Am Rev Respir Dis. 1969 Nov;100(5):631-9 PMID: 4987090
  2. Inositol phosphate capping of the nonreducing termini of lipoarabinomannan from rapidly growing strains of Mycobacterium.
    J Biol Chem. 1995 May 26;270(21):12380-9 PMID: 7759478
  3. The effect of inoculum size on the immune response to BCG infection in mice.
    Immunology. 1971 Aug;21(2):369-81 PMID: 4999037
  4. Suppressor adherent cells in human tuberculosis.
    J Immunol. 1978 Dec;121(6):2573-9 PMID: 309907
  5. Preliminary demonstration of human tuberculoimmunity in vitro.
    Infect Immun. 1981 Jan;31(1):453-64 PMID: 7012004
  6. A simple method for counting adherent cells: application to cultured human monocytes, macrophages and multinucleated giant cells.
    J Immunol Methods. 1983 Jan 28;56(2):261-8 PMID: 6827097
  7. Replication of lyophilized and cultured BCG in human macrophages.
    Am Rev Respir Dis. 1983 Oct;128(4):673-9 PMID: 6354027
  8. Gamma interferon activates human macrophages to become tumoricidal and leishmanicidal but enhances replication of macrophage-associated mycobacteria.
    Infect Immun. 1985 Oct;50(1):1-8 PMID: 3930401
  9. Defective interleukin 2 production and responsiveness in human pulmonary tuberculosis.
    J Exp Med. 1986 May 1;163(5):1162-72 PMID: 2939169
  10. Natural mycobacteriostatic activity in human monocyte-derived adherent cells.
    Am Rev Respir Dis. 1986 Jul;134(1):44-8 PMID: 3014936
  11. Activation of macrophages to inhibit proliferation of Mycobacterium tuberculosis: comparison of the effects of recombinant gamma-interferon on human monocytes and murine peritoneal macrophages.
    Immunology. 1986 Nov;59(3):333-8 PMID: 3098676
  12. Cachectin: more than a tumor necrosis factor.
    N Engl J Med. 1987 Feb 12;316(7):379-85 PMID: 3543677
  13. The role of gamma-interferon, vitamin D3 metabolites and tumour necrosis factor in the pathogenesis of tuberculosis.
    Immunology. 1987 Oct;62(2):229-34 PMID: 3119471
  14. Inhibition of interferon-gamma-mediated activation in mouse macrophages treated with lipoarabinomannan.
    Clin Exp Immunol. 1990 Apr;80(1):141-8 PMID: 2138940
  15. Killing of Mycobacterium tuberculosis within human monocytes: activation by cytokines and calcitriol.
    Clin Exp Immunol. 1991 May;84(2):200-6 PMID: 1902761
  16. Effect of mycobacteria on sensitivity to the cytotoxic effects of tumor necrosis factor.
    Infect Immun. 1991 Aug;59(8):2567-72 PMID: 1906841
  17. Mechanisms involved in mycobacterial growth inhibition by gamma interferon-activated bone marrow macrophages: role of reactive nitrogen intermediates.
    Infect Immun. 1991 Sep;59(9):3213-8 PMID: 1908829
  18. The global tuberculosis situation and the new control strategy of the World Health Organization.
    Tubercle. 1991 Mar;72(1):1-6 PMID: 1882440
  19. An outbreak of tuberculosis with accelerated progression among persons infected with the human immunodeficiency virus. An analysis using restriction-fragment-length polymorphisms.
    N Engl J Med. 1992 Jan 23;326(4):231-5 PMID: 1345800
  20. Environmental signals controlling expression of virulence determinants in bacteria.
    J Bacteriol. 1992 Jan;174(1):1-7 PMID: 1729202
  21. Structural basis of capacity of lipoarabinomannan to induce secretion of tumor necrosis factor.
    Infect Immun. 1992 Mar;60(3):1249-53 PMID: 1541542
  22. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages.
    J Exp Med. 1992 Apr 1;175(4):1111-22 PMID: 1552282
  23. Lipoarabinomannan of Mycobacterium tuberculosis. Capping with mannosyl residues in some strains.
    J Biol Chem. 1992 Mar 25;267(9):6234-9 PMID: 1556132
  24. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice.
    Immunity. 1995 Jun;2(6):561-72 PMID: 7540941
  25. Down-regulation of the afferent phase of T cell-mediated pulmonary inflammation and immunity by a high melanin-producing strain of Cryptococcus neoformans.
    J Immunol. 1995 Oct 1;155(7):3507-16 PMID: 7561046
  26. On the expression of nitric oxide synthase by human macrophages. Why no NO?
    J Leukoc Biol. 1995 Dec;58(6):643-9 PMID: 7499961
  27. Nitric oxide production by human monocytes: evidence for a role of CD23.
    Immunol Today. 1995 Dec;16(12):574-80 PMID: 8579750
  28. Selective induction of transforming growth factor beta in human monocytes by lipoarabinomannan of Mycobacterium tuberculosis.
    Infect Immun. 1996 Feb;64(2):399-405 PMID: 8550183
  29. Evidence against a role for interleukin-10 in the regulation of growth of Mycobacterium avium in human monocytes.
    J Infect Dis. 1996 Feb;173(2):410-7 PMID: 8568303
  30. Genome sequencing. Europeans move on from yeast to TB.
    Science. 1996 Apr 5;272(5258):27 PMID: 8600529
  31. A stationary-phase stress-response sigma factor from Mycobacterium tuberculosis.
    Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2790-4 PMID: 8610119
  32. Interleukin-10 downregulates Mycobacterium tuberculosis-induced Th1 responses and CTLA-4 expression.
    Infect Immun. 1996 Mar;64(3):913-8 PMID: 8641800
  33. Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis.
    J Bacteriol. 1996 Mar;178(5):1274-82 PMID: 8631702
  34. Elements of signal transduction in Mycobacterium tuberculosis: in vitro phosphorylation and in vivo expression of the response regulator MtrA.
    J Bacteriol. 1996 Jun;178(11):3314-21 PMID: 8655513
  35. Comparable growth of virulent and avirulent Mycobacterium tuberculosis in human macrophages in vitro.
    J Infect Dis. 1996 Jul;174(1):105-12 PMID: 8655979
  36. Lymphocyte-dependent inhibition of growth of virulent Mycobacterium tuberculosis H37Rv within human monocytes: requirement for CD4+ T cells in purified protein derivative-positive, but not in purified protein derivative-negative subjects.
    J Immunol. 1998 Mar 1;160(5):2408-17 PMID: 9498784
  37. Multiplication and survival of tubercle bacilli in the organs of mice.
    J Exp Med. 1953 Feb 1;97(2):189-206 PMID: 13022873
  38. Cytokine production induced by Mycobacterium tuberculosis lipoarabinomannan. Relationship to chemical structure.
    J Immunol. 1992 Jul 15;149(2):541-7 PMID: 1624801
  39. 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
  40. The effect of Mycobacterium tuberculosis on the susceptibility of human cells to the stimulatory and toxic effects of tumour necrosis factor.
    Immunology. 1992 Dec;77(4):505-9 PMID: 1362962
  41. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors.
    J Immunol. 1993 Apr 1;150(7):2920-30 PMID: 8454864
  42. Colonial morphotype as a determinant of cytokine expression by human monocytes infected with Mycobacterium avium.
    J Immunol. 1993 Apr 1;150(7):2945-54 PMID: 8454866
  43. Exogenous reinfection with multidrug-resistant Mycobacterium tuberculosis in patients with advanced HIV infection.
    N Engl J Med. 1993 Apr 22;328(16):1137-44 PMID: 8096066
  44. Mycobacterial virulence. Virulent strains of Mycobacteria tuberculosis have faster in vivo doubling times and are better equipped to resist growth-inhibiting functions of macrophages in the presence and absence of specific immunity.
    J Exp Med. 1993 Jun 1;177(6):1723-33 PMID: 8496688
  45. Identification and cloning of genes differentially expressed in the virulent strain of Mycobacterium tuberculosis.
    Gene. 1993 Sep 6;131(1):113-7 PMID: 7690337
  46. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection.
    J Exp Med. 1993 Dec 1;178(6):2249-54 PMID: 7504064
  47. Structure and antigenicity of lipoarabinomannan from Mycobacterium bovis BCG.
    J Gen Microbiol. 1993 Nov;139(11):2649-58 PMID: 8277248
  48. Complement receptor-mediated uptake and tumor necrosis factor-alpha-mediated growth inhibition of Mycobacterium tuberculosis by human alveolar macrophages.
    J Immunol. 1994 Jan 15;152(2):743-53 PMID: 8283049
  49. Human monocytes are stimulated for nitric oxide release in vitro by some tumor cells but not by cytokines and lipopolysaccharide.
    Eur J Immunol. 1994 Feb;24(2):435-9 PMID: 8299693
  50. Salmonella typhimurium loci involved in survival within macrophages.
    Infect Immun. 1994 May;62(5):1623-30 PMID: 8168923
  51. The epidemiology of tuberculosis in San Francisco. A population-based study using conventional and molecular methods.
    N Engl J Med. 1994 Jun 16;330(24):1703-9 PMID: 7910661
  52. Transmission of tuberculosis in New York City. An analysis by DNA fingerprinting and conventional epidemiologic methods.
    N Engl J Med. 1994 Jun 16;330(24):1710-6 PMID: 7993412
  53. Differential release of tumor necrosis factor-alpha from murine peritoneal macrophages stimulated with virulent and avirulent species of mycobacteria.
    FEMS Immunol Med Microbiol. 1994 Mar;8(3):225-32 PMID: 8004059
  54. Defective antigen presentation by Mycobacterium tuberculosis-infected monocytes.
    Infect Immun. 1994 Aug;62(8):3472-8 PMID: 8039918
  55. Further characterization of the PhoP regulon: identification of new PhoP-activated virulence loci.
    Infect Immun. 1994 Nov;62(11):5095-101 PMID: 7927792
  56. Triggering of human monocyte activation through CD69, a member of the natural killer cell gene complex family of signal transducing receptors.
    J Exp Med. 1994 Nov 1;180(5):1999-2004 PMID: 7964477
  57. Bacterial evasion of host immune defense: Yersinia enterocolitica encodes a suppressor for tumor necrosis factor alpha expression.
    Infect Immun. 1995 Apr;63(4):1270-7 PMID: 7890384
  58. The relation between infecting ndosage and median survival in tuberculous guinea pigs.
    Am Rev Respir Dis. 1971 Aug;104(2):206-14 PMID: 4997673
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
1998-03-00
Pages
1190-9
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC108033
Subset
IM
Grants
NIAID NIH HHS · N01 AI045244 · United States
NIAID NIH HHS · AI35207 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com