Fasting-Refeeding Impacts Immune Cell Dynamics and Mucosal Immune Responses

Cell. 2019 Aug 22;178(5):1072-1087.e14. doi: 10.1016/j.cell.2019.07.047.

Abstract

Nutritional status potentially influences immune responses; however, how nutritional signals regulate cellular dynamics and functionality remains obscure. Herein, we report that temporary fasting drastically reduces the number of lymphocytes by ∼50% in Peyer's patches (PPs), the inductive site of the gut immune response. Subsequent refeeding seemingly restored the number of lymphocytes, but whose cellular composition was conspicuously altered. A large portion of germinal center and IgA+ B cells were lost via apoptosis during fasting. Meanwhile, naive B cells migrated from PPs to the bone marrow during fasting and then back to PPs during refeeding when stromal cells sensed nutritional signals and upregulated CXCL13 expression to recruit naive B cells. Furthermore, temporal fasting before oral immunization with ovalbumin abolished the induction of antigen-specific IgA, failed to induce oral tolerance, and eventually exacerbated food antigen-induced diarrhea. Thus, nutritional signals are critical in maintaining gut immune homeostasis.

Keywords: B cell; CXCL13; IgA; Immunometabolism; Peyer's patch; bone marrow; fasting; mTOR signaling; mucosal immunity; nutritional signals; stroma cell.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens / immunology
  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism
  • B-Lymphocytes / physiology*
  • Bone Marrow / immunology
  • Bone Marrow / metabolism
  • Chemokine CXCL13 / genetics
  • Chemokine CXCL13 / metabolism
  • Fasting
  • Gene Expression Regulation
  • Glycolysis
  • Immunity, Mucosal*
  • Immunoglobulin A / metabolism
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Nutritional Status
  • Ovalbumin / immunology
  • Peyer's Patches / immunology
  • Peyer's Patches / metabolism
  • Peyer's Patches / pathology
  • Receptors, CXCR5 / genetics
  • Receptors, CXCR5 / metabolism
  • Signal Transduction
  • Stromal Cells / cytology
  • Stromal Cells / metabolism
  • TOR Serine-Threonine Kinases / metabolism

Substances

  • Antigens
  • Chemokine CXCL13
  • Immunoglobulin A
  • Receptors, CXCR5
  • Ovalbumin
  • mTOR protein, mouse
  • TOR Serine-Threonine Kinases