Mononuclear phagocyte-derived interleukin-10 suppresses the innate pulmonary granuloma cytokine response in aged mice

Am J Pathol. 2007 Sep;171(3):829-37. doi: 10.2353/ajpath.2007.061122. Epub 2007 Jul 13.

Abstract

Granulomas are sequestration responses observed in a wide variety of clinical conditions, including mycobacterial infection. We previously reported impaired adaptive, Th1 cell-mediated pulmonary granuloma formation in response to bead-immobilized Mycobacterium bovis-purified protein derivative in aged mice. To reveal determinants of age-related immune deficits, the present study examined the effect of aging on early innate stage pulmonary granuloma formation. Aged mice formed more neutrophil-rich innate granulomas with augmented CXCL2 expression followed by a pattern of rapid decay of tumor necrosis factor-alpha, interleukin (IL)-6, CCL3, and CXCL2. This was associated with enhanced IL-10 expression. Blockade of IL-10 signaling with anti-IL-10 receptor antibody reversed the age-related decay. Intracellular flow cytometric analysis revealed that CD11b(+)Gr-1(+/-) mononuclear phagocytes were the primary leukocyte sources of IL-10 in lungs, and their numbers were increased in aged mice. When exposed to purified protein derivative in vitro, young and old CD11b(+)Gr-1(+/-) mononuclear phagocytes from blood or lung had comparable IL-10 expression, suggesting in vivo signals in the aged environment enhanced the number of IL-10-producing cells in the aged lung. Our findings reveal a novel mechanism of age-associated IL-10 mediated pulmonary immune suppression with the potential to alter downstream adaptive immunity.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Aging / physiology*
  • Animals
  • Bacterial Proteins / immunology
  • CD11b Antigen / immunology
  • Chemokines / immunology
  • Cytokines / genetics
  • Cytokines / immunology*
  • Granuloma, Respiratory Tract* / immunology
  • Granuloma, Respiratory Tract* / pathology
  • Humans
  • Immune System / physiology
  • Interleukin-10 / genetics
  • Interleukin-10 / metabolism*
  • Leukocytes, Mononuclear / cytology
  • Leukocytes, Mononuclear / immunology*
  • Lung* / immunology
  • Lung* / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mycobacterium bovis / immunology
  • Phagocytes / cytology
  • Phagocytes / immunology*
  • Signal Transduction / physiology

Substances

  • Bacterial Proteins
  • CD11b Antigen
  • Chemokines
  • Cytokines
  • Interleukin-10