Deficiency of the planar cell polarity protein Vangl2 in podocytes affects glomerular morphogenesis and increases susceptibility to injury
The planar cell polarity (PCP) signaling pathway is crucial for tissue morphogenesis. Van Gogh-like protein 2 (Vangl2) is central in the PCP pathway; in mice, Vangl2 loss is embryonically lethal because of neural tube defects, and mutations in Vangl2 are associated with human neural tube defects. In...
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Published in | Journal of the American Society of Nephrology Vol. 26; no. 3; pp. 576 - 586 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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American Society of Nephrology
01.03.2015
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Abstract | The planar cell polarity (PCP) signaling pathway is crucial for tissue morphogenesis. Van Gogh-like protein 2 (Vangl2) is central in the PCP pathway; in mice, Vangl2 loss is embryonically lethal because of neural tube defects, and mutations in Vangl2 are associated with human neural tube defects. In the kidney, PCP signaling may be important for tubular morphogenesis and organization of glomerular epithelial cells (podocytes) along the glomerular basement membrane. Podocyte cell protrusions (foot processes) are critical for glomerular permselectivity; loss of foot process architecture results in proteinuria and FSGS. Previously, we showed a profound effect of PCP signaling on podocyte shape, actin rearrangement, cell motility, and nephrin endocytosis. To test our hypothesis that the PCP pathway is involved in glomerular development and function and circumvent lethality of the ubiquitous Vangl2 mutation in the Looptail mouse, we generated a mouse model with a podocyte-specific ablation of the Vangl2 gene. We report here that podocyte-specific deletion of Vangl2 leads to glomerular maturation defects in fetal kidneys. In adult mice, we detected significantly smaller glomeruli, but it did not affect glomerular permselectivity in aging animals. However, in the context of glomerular injury induced by injection of antiglomerular basement membrane antibody, deletion of Vangl2 resulted in exacerbation of injury and accelerated progression to chronic segmental and global glomerular sclerosis. Our results indicate that Vangl2 function in podocytes is important for glomerular development and protects against glomerular injury in adult animals. |
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AbstractList | The planar cell polarity (PCP) signaling pathway is crucial for tissue morphogenesis. Van Gogh-like protein 2 (Vangl2) is central in the PCP pathway; in mice, Vangl2 loss is embryonically lethal because of neural tube defects, and mutations in Vangl2 are associated with human neural tube defects. In the kidney, PCP signaling may be important for tubular morphogenesis and organization of glomerular epithelial cells (podocytes) along the glomerular basement membrane. Podocyte cell protrusions (foot processes) are critical for glomerular permselectivity; loss of foot process architecture results in proteinuria and FSGS. Previously, we showed a profound effect of PCP signaling on podocyte shape, actin rearrangement, cell motility, and nephrin endocytosis. To test our hypothesis that the PCP pathway is involved in glomerular development and function and circumvent lethality of the ubiquitous Vangl2 mutation in the
Looptail
mouse, we generated a mouse model with a podocyte-specific ablation of the Vangl2 gene. We report here that podocyte-specific deletion of Vangl2 leads to glomerular maturation defects in fetal kidneys. In adult mice, we detected significantly smaller glomeruli, but it did not affect glomerular permselectivity in aging animals. However, in the context of glomerular injury induced by injection of antiglomerular basement membrane antibody, deletion of Vangl2 resulted in exacerbation of injury and accelerated progression to chronic segmental and global glomerular sclerosis. Our results indicate that Vangl2 function in podocytes is important for glomerular development and protects against glomerular injury in adult animals. The planar cell polarity (PCP) signaling pathway is crucial for tissue morphogenesis. Van Gogh-like protein 2 (Vangl2) is central in the PCP pathway; in mice, Vangl2 loss is embryonically lethal because of neural tube defects, and mutations in Vangl2 are associated with human neural tube defects. In the kidney, PCP signaling may be important for tubular morphogenesis and organization of glomerular epithelial cells (podocytes) along the glomerular basement membrane. Podocyte cell protrusions (foot processes) are critical for glomerular permselectivity; loss of foot process architecture results in proteinuria and FSGS. Previously, we showed a profound effect of PCP signaling on podocyte shape, actin rearrangement, cell motility, and nephrin endocytosis. To test our hypothesis that the PCP pathway is involved in glomerular development and function and circumvent lethality of the ubiquitous Vangl2 mutation in the Looptail mouse, we generated a mouse model with a podocyte-specific ablation of the Vangl2 gene. We report here that podocyte-specific deletion of Vangl2 leads to glomerular maturation defects in fetal kidneys. In adult mice, we detected significantly smaller glomeruli, but it did not affect glomerular permselectivity in aging animals. However, in the context of glomerular injury induced by injection of antiglomerular basement membrane antibody, deletion of Vangl2 resulted in exacerbation of injury and accelerated progression to chronic segmental and global glomerular sclerosis. Our results indicate that Vangl2 function in podocytes is important for glomerular development and protects against glomerular injury in adult animals. |
Author | Torban, Elena Leung, Vicki Gros, Philippe Cybulsky, Andrey V Babayeva, Sima Rocque, Brittany L Li, Jane Nezvitsky, Lisa |
Author_xml | – sequence: 1 givenname: Brittany L surname: Rocque fullname: Rocque, Brittany L organization: Departments of Medicine and Physiology, McGill University and McGill University Health Centre, Montreal, Quebec, Canada; and – sequence: 2 givenname: Sima surname: Babayeva fullname: Babayeva, Sima organization: Departments of Medicine and Physiology, McGill University and McGill University Health Centre, Montreal, Quebec, Canada; and – sequence: 3 givenname: Jane surname: Li fullname: Li, Jane organization: Departments of Medicine and Physiology, McGill University and McGill University Health Centre, Montreal, Quebec, Canada; and – sequence: 4 givenname: Vicki surname: Leung fullname: Leung, Vicki organization: Departments of Human Genetics and Complex Traits Group, McGill University, Montreal, Quebec, Canada – sequence: 5 givenname: Lisa surname: Nezvitsky fullname: Nezvitsky, Lisa organization: Departments of Medicine and Physiology, McGill University and McGill University Health Centre, Montreal, Quebec, Canada; and – sequence: 6 givenname: Andrey V surname: Cybulsky fullname: Cybulsky, Andrey V organization: Departments of Medicine and Physiology, McGill University and McGill University Health Centre, Montreal, Quebec, Canada; and – sequence: 7 givenname: Philippe surname: Gros fullname: Gros, Philippe organization: Complex Traits Group, McGill University, Montreal, Quebec, Canada Biochemistry and – sequence: 8 givenname: Elena surname: Torban fullname: Torban, Elena email: elena.torban@mcgill.ca organization: Departments of Medicine and Physiology, McGill University and McGill University Health Centre, Montreal, Quebec, Canada; and elena.torban@mcgill.ca |
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Snippet | The planar cell polarity (PCP) signaling pathway is crucial for tissue morphogenesis. Van Gogh-like protein 2 (Vangl2) is central in the PCP pathway; in mice,... |
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SubjectTerms | Animals Basic Research Cell Polarity Female Kidney Glomerulus - embryology Kidney Glomerulus - physiology Male Mice, Inbred C57BL Mice, Transgenic Morphogenesis Nerve Tissue Proteins - metabolism Podocytes - metabolism |
Title | Deficiency of the planar cell polarity protein Vangl2 in podocytes affects glomerular morphogenesis and increases susceptibility to injury |
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