TGF-β-activated kinase 1 is crucial in podocyte differentiation and glomerular capillary formation

J Am Soc Nephrol. 2014 Sep;25(9):1966-78. doi: 10.1681/ASN.2013030252. Epub 2014 Mar 20.

Abstract

TGF-β-activated kinase 1 (TAK1) is a key intermediate in signal transduction induced by TGF-β or inflammatory cytokines, such as TNF-α and IL-1, which are potent inducers of podocyte injury responses that lead to proteinuria and glomerulosclerosis. Nevertheless, little is known about the physiologic and pathologic roles of TAK1 in podocytes. To examine the in vivo role of TAK1, we generated podocyte-specific Tak1 knockout mice (Nphs2-Cre(+):Tak1(fx/fx); Tak1(∆/∆)). Targeted deletion of Tak1 in podocytes resulted in perinatal lethality, with approximately 50% of animals dying soon after birth and 90% of animals dying within 1 week of birth. Tak1(∆/∆) mice developed proteinuria from P1 and exhibited delayed glomerulogenesis and reduced expression of Wilms' tumor suppressor 1 and nephrin in podocytes. Compared with Tak1(fx/fx) mice, Tak1(∆/∆) mice exhibited impaired formation of podocyte foot processes that caused disruption of the podocyte architecture with prominent foot process effacement. Intriguingly, Tak1(∆/∆) mice displayed increased expression of vascular endothelial growth factor within the glomerulus and abnormally enlarged glomerular capillaries. Furthermore, 4- and 7-week-old Tak1(∆/∆) mice with proteinuria had increased collagen deposition in the mesangium and the adjacent tubulointerstitial area. Thus, loss of Tak1 in podocytes is associated with the development of proteinuria and glomerulosclerosis. Taken together, our data show that TAK1 regulates the expression of Wilms' tumor suppressor 1, nephrin, and vascular endothelial growth factor and that TAK1 signaling has a crucial role in podocyte differentiation and attainment of normal glomerular microvasculature during kidney development and glomerular filtration barrier homeostasis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Capillaries / enzymology
  • Capillaries / growth & development
  • Cell Differentiation / genetics
  • Cell Differentiation / physiology
  • Collagen / metabolism
  • Female
  • Glomerular Filtration Barrier / blood supply
  • Glomerular Filtration Barrier / enzymology
  • Glomerular Filtration Barrier / growth & development
  • Kidney Glomerulus / blood supply*
  • Kidney Glomerulus / enzymology*
  • Kidney Glomerulus / growth & development
  • MAP Kinase Kinase Kinases / deficiency
  • MAP Kinase Kinase Kinases / genetics
  • MAP Kinase Kinase Kinases / metabolism*
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Podocytes / cytology*
  • Podocytes / enzymology*
  • Pregnancy
  • Proteinuria / enzymology
  • Proteinuria / etiology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Signal Transduction
  • Vascular Endothelial Growth Factor A / genetics
  • Vascular Endothelial Growth Factor A / metabolism
  • WT1 Proteins / genetics
  • WT1 Proteins / metabolism

Substances

  • Membrane Proteins
  • RNA, Messenger
  • Vascular Endothelial Growth Factor A
  • WT1 Proteins
  • nephrin
  • vascular endothelial growth factor A, mouse
  • Collagen
  • MAP Kinase Kinase Kinases
  • MAP kinase kinase kinase 7