Soluble β-glucan from Grifola frondosa induces proliferation and Dectin-1/Syk signaling in resident macrophages via the GM-CSF autocrine pathway

J Leukoc Biol. 2012 Apr;91(4):547-56. doi: 10.1189/jlb.0711386. Epub 2011 Oct 25.

Abstract

MD-Fraction, a highly purified, soluble β-(1,3) (1,6)-glucan obtained from Grifola frondosa (an oriental edible mushroom), has been reported to inhibit tumor growth by modulating host immunity. β-Glucan, a major component of the fungal cell wall, is generally recognized by PRRs expressed on macrophages and DCs, such as Dectin-1, and the ability of β-glucans to modulate host immunity is influenced by their structure and purity. Most cellular studies have used particulate β-glucans, such as yeast zymosan (crude β-glucan) and curdlan (purified β-glucan). However, little is known about the cellular mechanism of soluble β-glucans, including MD-Fraction, despite significant therapeutic implications. In this study, we investigated the cellular mechanism of MD-Fraction in murine resident macrophages and compared it with two well-known β-glucan particles. MD-Fraction induced GM-CSF production rapidly through Dectin-1-independent ERK and p38 MAPK activation. Subsequently, MD-Fraction-induced GM-CSF enhanced proliferation and Dectin-1 expression, which permitted Dectin-1-mediated TNF-α induction through the Syk pathway. Curdlan induced not only the proliferation and activation of Dectin-1/Syk signaling in a manner similar to MD-Fraction but also the uncontrolled, proinflammatory cytokine response. Contrastingly, zymosan reduced proliferation and Dectin-1 expression significantly, indicating that the mechanism of macrophage activation by MD-Fraction differs from that of zymosan. This is the first study to demonstrate that purified β-glucans, such as MD-Fraction and curdlan, induce GM-CSF production directly, resulting in Dectin-1/Syk activation in resident macrophages. In conclusion, we demonstrated that MD-Fraction induces cell proliferation and cytokine production without excessive inflammation in resident macrophages, supporting its immunotherapeutic potential.

MeSH terms

  • Agaricales / chemistry*
  • Agaricales / immunology
  • Animals
  • Autocrine Communication / drug effects*
  • Autocrine Communication / immunology
  • Cell Proliferation / drug effects
  • Cell Wall / chemistry
  • Cell Wall / immunology
  • Enzyme Activation / drug effects
  • Enzyme Activation / immunology
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / immunology
  • Granulocyte-Macrophage Colony-Stimulating Factor / immunology*
  • Granulocyte-Macrophage Colony-Stimulating Factor / metabolism
  • Intracellular Signaling Peptides and Proteins / immunology*
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Lectins, C-Type / biosynthesis
  • Lectins, C-Type / immunology*
  • MAP Kinase Signaling System / drug effects*
  • MAP Kinase Signaling System / immunology
  • Macrophages, Peritoneal / cytology
  • Macrophages, Peritoneal / immunology*
  • Macrophages, Peritoneal / metabolism
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred DBA
  • Protein-Tyrosine Kinases / immunology*
  • Protein-Tyrosine Kinases / metabolism
  • Syk Kinase
  • beta-Glucans / chemistry
  • beta-Glucans / immunology
  • beta-Glucans / pharmacology*
  • p38 Mitogen-Activated Protein Kinases / immunology
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Intracellular Signaling Peptides and Proteins
  • Lectins, C-Type
  • beta-Glucans
  • dectin 1
  • Granulocyte-Macrophage Colony-Stimulating Factor
  • Protein-Tyrosine Kinases
  • Syk Kinase
  • Syk protein, mouse
  • p38 Mitogen-Activated Protein Kinases