Semaphorin3A, Neuropilin-1, and PlexinA1 are required for lymphatic valve formation

Circ Res. 2012 Aug 3;111(4):437-45. doi: 10.1161/CIRCRESAHA.112.269316. Epub 2012 Jun 21.

Abstract

Rationale: The lymphatic vasculature plays a major role in fluid homeostasis, absorption of dietary lipids, and immune surveillance. Fluid transport depends on the presence of intraluminal valves within lymphatic collectors. Defective formation of lymphatic valves leads to lymphedema, a progressive and debilitating condition for which curative treatments are currently unavailable. How lymphatic valve formation is regulated remains largely unknown.

Objective: We investigated if the repulsive axon guidance molecule Semaphorin3A (Sema3A) plays a role in lymphatic valve formation.

Methods and results: We show that Sema3A mRNA is expressed in lymphatic vessels and that Sema3A protein binds to lymphatic valves expressing the Neuropilin-1 (Nrp1) and PlexinA1 receptors. Using mouse knockout models, we show that Sema3A is selectively required for lymphatic valve formation, via interaction with Nrp1 and PlexinA1. Sema3a(-/-) mice exhibit defects in lymphatic valve formation, which are not due to abnormal lymphatic patterning or sprouting, and mice carrying a mutation in the Sema3A binding site of Nrp1, or deficient for Plxna1, develop lymphatic valve defects similar to those seen in Sema3a(-/-) mice.

Conclusions: Our data demonstrate an essential direct function of Sema3A-Nrp1-PlexinA1 signaling in lymphatic valve formation.

Publication types

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

MeSH terms

  • Animals
  • Animals, Newborn
  • Antibodies, Neutralizing / administration & dosage
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Cells, Cultured
  • Endothelial Cells / metabolism
  • Gene Expression Regulation, Developmental
  • Genotype
  • Gestational Age
  • Humans
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Lymphatic Vessels / embryology
  • Lymphatic Vessels / metabolism*
  • Mice
  • Mice, Knockout
  • Mice, Transgenic
  • Morphogenesis
  • Nerve Tissue Proteins / deficiency
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Neuropilin-1 / deficiency
  • Neuropilin-1 / genetics
  • Neuropilin-1 / immunology
  • Neuropilin-1 / metabolism*
  • Phenotype
  • RNA, Messenger / metabolism
  • Receptors, Cell Surface / deficiency
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*
  • Semaphorin-3A / deficiency
  • Semaphorin-3A / genetics
  • Semaphorin-3A / metabolism*
  • Vascular Endothelial Growth Factor Receptor-3 / genetics
  • Vascular Endothelial Growth Factor Receptor-3 / metabolism

Substances

  • Antibodies, Neutralizing
  • Bacterial Proteins
  • Luminescent Proteins
  • Nerve Tissue Proteins
  • PLXNA1 protein, human
  • Plxna1 protein, mouse
  • RNA, Messenger
  • Receptors, Cell Surface
  • SEMA3A protein, human
  • Sema3a protein, mouse
  • Semaphorin-3A
  • yellow fluorescent protein, Bacteria
  • Neuropilin-1
  • Vascular Endothelial Growth Factor Receptor-3