B-1a Cells Protect Mice from Sepsis: Critical Role of CREB

J Immunol. 2017 Jul 15;199(2):750-760. doi: 10.4049/jimmunol.1602056. Epub 2017 Jun 19.

Abstract

Bacterial sepsis is a serious life-threatening condition caused by an excessive immune response to infection. B-1 cells differ from conventional B-2 cells by their distinct phenotype and function. A subset of B-1 cells expressing CD5, known as B-1a cells, exhibits innate immune activity. Here we report that B-1a cells play a beneficial role in sepsis by mitigating exaggerated inflammation through a novel mechanism. Using a mouse model of bacterial sepsis, we found that the numbers of B-1a cells in various anatomical locations were significantly decreased. Adoptive transfer of B-1a cells into septic mice significantly attenuated systemic inflammation and improved survival, whereas B-1a cell-deficient CD19-/- mice were more susceptible to infectious inflammation and mortality. We also demonstrated B-1a cells produced ample amounts of IL-10 which controlled excessive inflammation and the mice treated with IL-10-deficient B-1a cells were not protected against sepsis. Moreover, we identified a novel intracellular signaling molecule, cAMP-response element binding protein (CREB), which serves as a pivotal transcription factor for upregulating IL-10 production by B-1a cells in sepsis through its nuclear translocation and binding to putative responsive elements on IL-10 promoter. Thus, the benefit of B-1a cells in bacterial sepsis is mediated by CREB and the identification of CREB in B-1a cells reveals a potential avenue for treatment in bacterial sepsis.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adoptive Transfer
  • Animals
  • Antigens, CD19 / genetics
  • Antigens, CD19 / immunology
  • B-Lymphocyte Subsets / immunology*
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / metabolism
  • Cyclic AMP Response Element-Binding Protein / genetics
  • Cyclic AMP Response Element-Binding Protein / metabolism*
  • Disease Models, Animal
  • Inflammation / immunology
  • Interleukin-10 / biosynthesis
  • Interleukin-10 / immunology
  • Mice
  • Sepsis / immunology*

Substances

  • Antigens, CD19
  • CD19 antigen, mouse
  • Creb1 protein, mouse
  • Cyclic AMP Response Element-Binding Protein
  • IL10 protein, mouse
  • Interleukin-10