Cilia-localized LKB1 regulates chemokine signaling, macrophage recruitment, and tissue homeostasis in the kidney

EMBO J. 2018 Aug 1;37(15):e98615. doi: 10.15252/embj.201798615. Epub 2018 Jun 19.

Abstract

Polycystic kidney disease (PKD) and other renal ciliopathies are characterized by cysts, inflammation, and fibrosis. Cilia function as signaling centers, but a molecular link to inflammation in the kidney has not been established. Here, we show that cilia in renal epithelia activate chemokine signaling to recruit inflammatory cells. We identify a complex of the ciliary kinase LKB1 and several ciliopathy-related proteins including NPHP1 and PKD1. At homeostasis, this ciliary module suppresses expression of the chemokine CCL2 in tubular epithelial cells. Deletion of LKB1 or PKD1 in mouse renal tubules elevates CCL2 expression in a cell-autonomous manner and results in peritubular accumulation of CCR2+ mononuclear phagocytes, promoting a ciliopathy phenotype. Our findings establish an epithelial organelle, the cilium, as a gatekeeper of tissue immune cell numbers. This represents an unexpected disease mechanism for renal ciliopathies and establishes a new model for how epithelial cells regulate immune cells to affect tissue homeostasis.

Keywords: cilia; macrophages; nephronophthisis; polycystic kidney disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases
  • Adaptor Proteins, Signal Transducing
  • Animals
  • Carrier Proteins / metabolism
  • Cell Line
  • Chemokine CCL2 / metabolism*
  • Cilia / pathology*
  • Cytoskeletal Proteins
  • Dogs
  • Epithelial Cells / metabolism
  • Female
  • HEK293 Cells
  • Humans
  • Kidney Diseases, Cystic / congenital*
  • Kidney Diseases, Cystic / pathology
  • Kidney Tubules / cytology
  • Kidney Tubules / pathology
  • Macrophages / metabolism
  • Madin Darby Canine Kidney Cells
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Phagocytosis / physiology
  • Polycystic Kidney, Autosomal Dominant / genetics
  • Polycystic Kidney, Autosomal Dominant / pathology*
  • Protein Kinase C / genetics*
  • Protein Kinase C / metabolism
  • Protein Serine-Threonine Kinases / genetics*
  • Protein Serine-Threonine Kinases / metabolism
  • Zebrafish

Substances

  • Adaptor Proteins, Signal Transducing
  • Carrier Proteins
  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Cytoskeletal Proteins
  • Nphp1 protein, mouse
  • protein kinase D
  • Protein Serine-Threonine Kinases
  • Stk11 protein, mouse
  • Protein Kinase C
  • AMP-Activated Protein Kinases

Supplementary concepts

  • Nephronophthisis, familial juvenile