Home LiteratureArticle Details
PMID: 17591775 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Exosomes released from infected macrophages contain Mycobacterium avium glycopeptidolipids and are proinflammatory.

The Journal of biological chemistry ·Vol. 282 ·No. 35 ·2007-08-31 ·Pages 25779-89

Bhatnagar S, Schorey JS

Abstract

Mycobacterium avium is a major opportunistic pathogen in HIV-positive individuals and is responsible for increased morbidity and mortality in AIDS patients. M. avium express glycopeptidolipids (GPLs) as a major cell wall constituent, and recent studies suggest that GPLs play an important role in M. avium pathogenesis. In the present study we show that M. avium-infected macrophages release GPLs, which are trafficked from the phagosome through the endocytic network to multivesicular bodies. Prior studies have shown that multivesicular bodies can fuse with the plasma membrane releasing small 50 to 100 nm vesicles known as exosomes. We found that M. avium-infected macrophages release exosomes containing GPLs leading to the transfer of GPLs from infected to uninfected macrophages. Interestingly, exosomes isolated from M. avium-infected but not from uninfected macrophages can stimulate a proinflammatory response in resting macrophages. This proinflammatory response is dependent on Toll like receptor (TLR) 2, TLR4, and MyD88 suggesting that released exosomes contain M. avium-expressed TLR ligands. Our studies are the first to demonstrate that exosomes isolated from mycobacteria-infected macrophages can induce a proinflammatory response, and we hypothesize that exosomes play an important role in immune surveillance during intracellular bacteria infections.

MeSH Terms
AIDS-Related Opportunistic Infections/immunology,microbiology,pathology Animals Biological Transport, Active/immunology Cell Line Cell Wall/immunology,metabolism Female Glycoconjugates/immunology,metabolism HIV Inflammation/immunology,microbiology Inflammation Mediators/immunology Macrophages/immunology,metabolism,microbiology Male Mice Mice, Inbred BALB C Mice, Knockout Mycobacterium avium Myeloid Differentiation Factor 88/immunology Phagosomes/immunology,microbiology Secretory Vesicles/immunology Toll-Like Receptor 2/immunology Toll-Like Receptor 4/immunology Tuberculosis/immunology,pathology
Chemicals
Glycoconjugates Inflammation Mediators Myd88 protein, mouse Myeloid Differentiation Factor 88 Tlr2 protein, mouse Tlr4 protein, mouse Toll-Like Receptor 2 Toll-Like Receptor 4
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Bhatnagar Sanchita
Department of Biological Sciences, Center for Global Health and Infectious Diseases, University of Notre Dame, Notre Dame, Indiana 46556, USA.
Schorey Jeffrey S
References (49)
49 references, click to expand
  1. Differential regulation of the mitogen-activated protein kinases by pathogenic and nonpathogenic mycobacteria.
    Infect Immun. 2002 Jun;70(6):3040-52 PMID: 12010996
  2. Different Toll-like receptor agonists induce distinct macrophage responses.
    J Leukoc Biol. 2001 Jun;69(6):1036-44 PMID: 11404392
  3. Exosomes: composition, biogenesis and function.
    Nat Rev Immunol. 2002 Aug;2(8):569-79 PMID: 12154376
  4. Exosomes: novel organelles implicated in immunomodulation and apoptosis.
    Yale J Biol Med. 2002 Mar-Apr;75(2):95-101 PMID: 12230314
  5. Indirect activation of naïve CD4+ T cells by dendritic cell-derived exosomes.
    Nat Immunol. 2002 Dec;3(12):1156-62 PMID: 12426563
  6. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest.
    Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5437-42 PMID: 12702770
  7. Identification and macrophage-activating activity of glycolipids released from intracellular Mycobacterium bovis BCG.
    Mol Microbiol. 2003 May;48(4):875-88 PMID: 12753183
  8. Exosome release is regulated by a calcium-dependent mechanism in K562 cells.
    J Biol Chem. 2003 May 30;278(22):20083-90 PMID: 12639953
  9. Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis.
    Nat Med. 2003 Aug;9(8):1039-46 PMID: 12872166
  10. Macrophage surface expression of annexins I and II in the phagocytosis of apoptotic lymphocytes.
    Mol Biol Cell. 2004 Jun;15(6):2863-72 PMID: 15064349
  11. Toll-like receptor pathways in the immune responses to mycobacteria.
    Microbes Infect. 2004 Aug;6(10):946-59 PMID: 15310472
  12. Exosomes for cancer immunotherapy.
    Ann Oncol. 2004;15 Suppl 4:iv141-4 PMID: 15477298
  13. Electron-transparent zone of mycobacteria may be a defence mechanism.
    Nature. 1970 Nov 28;228(5274):860-1 PMID: 4097724
  14. Isolation in high frequency of rough variants of Mycobacterium intracellulare lacking C-mycoside glycopeptidolipid antigens.
    J Bacteriol. 1982 Apr;150(1):381-4 PMID: 7061400
  15. Postphagocytic detection of glycopeptidolipids associated with the superficial L1 layer of Mycobacterium intracellulare.
    Infect Immun. 1983 Sep;41(3):1312-21 PMID: 6350184
  16. Evidence for inhibition of fusion of lysosomal and prelysosomal compartments with phagosomes in macrophages infected with pathogenic Mycobacterium avium.
    Infect Immun. 1986 Apr;52(1):252-62 PMID: 2870027
  17. The surface glycopeptidolipids of mycobacteria: structures and biological properties.
    Cell Mol Life Sci. 2001 Dec;58(14):2018-42 PMID: 11814054
  18. Intramacrophagic Mycobacterium avium bacilli are coated by a multiple lamellar structure: freeze fracture analysis of infected mouse liver.
    Infect Immun. 1991 Nov;59(11):3895-902 PMID: 1937749
  19. Mycobacterial glycopeptidolipid interactions with membranes: a monolayer study.
    FEBS Lett. 1995 Nov 20;375(3):254-8 PMID: 7498511
  20. B lymphocytes secrete antigen-presenting vesicles.
    J Exp Med. 1996 Mar 1;183(3):1161-72 PMID: 8642258
  21. Apoptosis of bcl-x-deficient telencephalic cells in vitro.
    J Neurosci. 1996 Mar 1;16(5):1753-8 PMID: 8774443
  22. Membrane transport from early to late endosomes.
    Cold Spring Harb Symp Quant Biol. 1995;60:205-9 PMID: 8824392
  23. Aggregation reroutes molecules from a recycling to a vesicle-mediated secretion pathway during reticulocyte maturation.
    J Cell Sci. 1997 Aug;110 ( Pt 16):1867-77 PMID: 9296387
  24. Risk assessment of opportunistic bacterial pathogens in drinking water.
    Rev Environ Contam Toxicol. 1997;152:57-83 PMID: 9297985
  25. Macrophages resistant to endogenously generated nitric oxide-mediated apoptosis are hypersensitive to exogenously added nitric oxide donors: dichotomous apoptotic response independent of caspase 3 and reversal by the mitogen-activated protein kinase kinase (MEK) inhibitor PD 098059.
    Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5045-50 PMID: 9560225
  26. The pathophysiology of disseminated Mycobacterium avium complex disease in AIDS.
    J Infect Dis. 1999 May;179 Suppl 3:S461-5 PMID: 10099120
  27. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells.
    Blood. 2004 Nov 15;104(10):3257-66 PMID: 15284116
  28. Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry.
    Proteomics. 2004 Dec;4(12):4019-31 PMID: 15478216
  29. In vivo activity of released cell wall lipids of Mycobacterium bovis bacillus Calmette-Guérin is due principally to trehalose mycolates.
    J Immunol. 2005 Apr 15;174(8):5007-15 PMID: 15814731
  30. Mycobacterium avium 104 deleted of the methyltransferase D gene by allelic replacement lacks serotype-specific glycopeptidolipids and shows attenuated virulence in mice.
    Mol Microbiol. 2005 Jun;56(5):1262-73 PMID: 15882419
  31. Involvement of ganglioside GM3 in G(2)/M cell cycle arrest of human monocytic cells induced by Actinobacillus actinomycetemcomitans cytolethal distending toxin.
    Infect Immun. 2005 Aug;73(8):4846-52 PMID: 16040998
  32. Mechanisms of group B streptococcal-induced apoptosis of murine macrophages.
    J Immunol. 2005 Aug 15;175(4):2555-62 PMID: 16081829
  33. Mature dendritic cells secrete exosomes with strong ability to induce antigen-specific effector immune responses.
    Blood Cells Mol Dis. 2005 Sep-Oct;35(2):89-93 PMID: 15990342
  34. Elevated mitogen-activated protein kinase signalling and increased macrophage activation in cells infected with a glycopeptidolipid-deficient Mycobacterium avium.
    Cell Microbiol. 2006 Jan;8(1):85-96 PMID: 16367868
  35. Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis.
    Immunity. 2006 Jan;24(1):105-17 PMID: 16413927
  36. Interaction of pathogenic mycobacteria with the host immune system.
    Curr Opin Microbiol. 2006 Feb;9(1):76-85 PMID: 16406837
  37. Role of exosomes in immune regulation.
    J Cell Mol Med. 2006 Apr-Jun;10(2):364-75 PMID: 16796805
  38. Glycopeptidolipids from Mycobacterium avium promote macrophage activation in a TLR2- and MyD88-dependent manner.
    J Leukoc Biol. 2006 Aug;80(2):415-23 PMID: 16760377
  39. Exosomes: a common pathway for a specialized function.
    J Biochem. 2006 Jul;140(1):13-21 PMID: 16877764
  40. Dynamic role of postsynaptic caspase-3 and BIRC4 in zebra finch song-response habituation.
    Neuron. 2006 Dec 21;52(6):1061-72 PMID: 17178408
  41. The high-affinity IgE receptor (FcepsilonRI) blocks apoptosis in normal human monocytes.
    J Clin Invest. 2000 Jan;105(2):183-90 PMID: 10642596
  42. ADP-ribosylation factor 6 regulates actin cytoskeleton remodeling in coordination with Rac1 and RhoA.
    Mol Cell Biol. 2000 May;20(10):3685-94 PMID: 10779358
  43. Exposure of human peripheral blood mononuclear cells to total lipids and serovar-specific glycopeptidolipids from Mycobacterium avium serovars 4 and 8 results in inhibition of TH1-type responses.
    Microb Pathog. 2000 Jul;29(1):9-16 PMID: 10873486
  44. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device.
    J Cell Sci. 2000 Oct;113 Pt 19:3365-74 PMID: 10984428
  45. Regulators of membrane trafficking and Mycobacterium tuberculosis phagosome maturation block.
    Electrophoresis. 2000 Oct;21(16):3378-85 PMID: 11079558
  46. Mycobacterial surface moieties are released from infected macrophages by a constitutive exocytic event.
    Eur J Cell Biol. 2001 Jan;80(1):31-40 PMID: 11211933
  47. Trafficking and release of mycobacterial lipids from infected macrophages.
    Traffic. 2000 Mar;1(3):235-47 PMID: 11208107
  48. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming.
    Nat Med. 2001 Mar;7(3):297-303 PMID: 11231627
  49. The exosome pathway in K562 cells is regulated by Rab11.
    J Cell Sci. 2002 Jun 15;115(Pt 12):2505-15 PMID: 12045221
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
0021-9258
Published
2007-08-31
Epub
2007-00-25
Pages
25779-89
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC3636815
Subset
IM
Grants
NIAID NIH HHS · AI052439 · United States
NIAID NIH HHS · R01 AI052439-04 · United States
NIAID NIH HHS · R01 AI056979-04 · United States
NIAID NIH HHS · R01 AI056979-05 · United States
NIAID NIH HHS · R01 AI056979 · United States
NIAID NIH HHS · R01 AI052439-05 · United States
NIAID NIH HHS · R01 AI052439 · United States
NIAID NIH HHS · AI056979 · 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