Semaphorin-Plexin Signaling Controls Mitotic Spindle Orientation during Epithelial Morphogenesis and Repair

Jingjing Xia; Jakub M. Swiercz; Inmaculada Bañón-Rodríguez; Ivana Matković; Giuseppina Federico; Tianliang Sun; Timo Franz; Cord Herbert Brakebusch; Atsushi Kumanogoh; Roland H. Friedel; Fernando Martín-Belmonte; Hermann-Josef Gröne; Stefan Offermanns; Thomas Worzfeld

doi:10.1016/j.devcel.2015.02.001

Semaphorin-Plexin Signaling Controls Mitotic Spindle Orientation during Epithelial Morphogenesis and Repair

Jingjing Xia, Jakub M. Swiercz, Inmaculada Bañón-Rodríguez, Ivana Matković, Giuseppina Federico, Tianliang Sun, Timo Franz, Cord Herbert Brakebusch, Atsushi Kumanogoh, Roland H. Friedel, Fernando Martín-Belmonte, Hermann-Josef Gröne, Stefan Offermanns, Thomas Worzfeld

27 Citations (Scopus)

Abstract

Morphogenesis, homeostasis, and regeneration of epithelial tissues rely on the accurate orientation of cell divisions, which is specified by the mitotic spindle axis. To remain in the epithelial plane, symmetrically dividing epithelial cells align their mitotic spindle axis with the plane. Here, we show that this alignment depends on epithelial cell-cell communication via semaphorin-plexin signaling. During kidney morphogenesis and repair, renal tubular epithelial cells lacking the transmembrane receptor Plexin-B2 or its semaphorin ligands fail to correctly orient the mitotic spindle, leading to severe defects in epithelial architecture and function. Analyses of a series of transgenic and knockout mice indicate that Plexin-B2 controls the cell division axis by signaling through its GTPase-activating protein (GAP) domain and Cdc42. Our data uncover semaphorin-plexin signaling as a central regulatory mechanism of mitotic spindle orientation necessary for the alignment of epithelial cell divisions with the epithelial plane.

Original language	English
Journal	Developmental Cell
Volume	33
Issue number	3
Pages (from-to)	299-313
Number of pages	15
ISSN	1534-5807
DOIs	https://doi.org/10.1016/j.devcel.2015.02.001
Publication status	Published - 4 May 2015

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Xia, J., Swiercz, J. M., Bañón-Rodríguez, I., Matković, I., Federico, G., Sun, T., Franz, T., Brakebusch, C. H., Kumanogoh, A., Friedel, R. H., Martín-Belmonte, F., Gröne, H.-J., Offermanns, S., & Worzfeld, T. (2015). Semaphorin-Plexin Signaling Controls Mitotic Spindle Orientation during Epithelial Morphogenesis and Repair. Developmental Cell, 33(3), 299-313. https://doi.org/10.1016/j.devcel.2015.02.001

Xia, J, Swiercz, JM, Bañón-Rodríguez, I, Matković, I, Federico, G, Sun, T, Franz, T, Brakebusch, CH, Kumanogoh, A, Friedel, RH, Martín-Belmonte, F, Gröne, H-J, Offermanns, S & Worzfeld, T 2015, 'Semaphorin-Plexin Signaling Controls Mitotic Spindle Orientation during Epithelial Morphogenesis and Repair', Developmental Cell, vol. 33, no. 3, pp. 299-313. https://doi.org/10.1016/j.devcel.2015.02.001

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title = "Semaphorin-Plexin Signaling Controls Mitotic Spindle Orientation during Epithelial Morphogenesis and Repair",

abstract = "Morphogenesis, homeostasis, and regeneration of epithelial tissues rely on the accurate orientation of cell divisions, which is specified by the mitotic spindle axis. To remain in the epithelial plane, symmetrically dividing epithelial cells align their mitotic spindle axis with the plane. Here, we show that this alignment depends on epithelial cell-cell communication via semaphorin-plexin signaling. During kidney morphogenesis and repair, renal tubular epithelial cells lacking the transmembrane receptor Plexin-B2 or its semaphorin ligands fail to correctly orient the mitotic spindle, leading to severe defects in epithelial architecture and function. Analyses of a series of transgenic and knockout mice indicate that Plexin-B2 controls the cell division axis by signaling through its GTPase-activating protein (GAP) domain and Cdc42. Our data uncover semaphorin-plexin signaling as a central regulatory mechanism of mitotic spindle orientation necessary for the alignment of epithelial cell divisions with the epithelial plane.",

author = "Jingjing Xia and Swiercz, {Jakub M.} and Inmaculada Ba{\~n}{\'o}n-Rodr{\'i}guez and Ivana Matkovi{\'c} and Giuseppina Federico and Tianliang Sun and Timo Franz and Brakebusch, {Cord Herbert} and Atsushi Kumanogoh and Friedel, {Roland H.} and Fernando Mart{\'i}n-Belmonte and Hermann-Josef Gr{\"o}ne and Stefan Offermanns and Thomas Worzfeld",

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T1 - Semaphorin-Plexin Signaling Controls Mitotic Spindle Orientation during Epithelial Morphogenesis and Repair

AU - Xia, Jingjing

AU - Swiercz, Jakub M.

AU - Bañón-Rodríguez, Inmaculada

AU - Matković, Ivana

AU - Federico, Giuseppina

AU - Sun, Tianliang

AU - Franz, Timo

AU - Brakebusch, Cord Herbert

AU - Kumanogoh, Atsushi

AU - Friedel, Roland H.

AU - Martín-Belmonte, Fernando

AU - Gröne, Hermann-Josef

AU - Offermanns, Stefan

AU - Worzfeld, Thomas

PY - 2015/5/4

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N2 - Morphogenesis, homeostasis, and regeneration of epithelial tissues rely on the accurate orientation of cell divisions, which is specified by the mitotic spindle axis. To remain in the epithelial plane, symmetrically dividing epithelial cells align their mitotic spindle axis with the plane. Here, we show that this alignment depends on epithelial cell-cell communication via semaphorin-plexin signaling. During kidney morphogenesis and repair, renal tubular epithelial cells lacking the transmembrane receptor Plexin-B2 or its semaphorin ligands fail to correctly orient the mitotic spindle, leading to severe defects in epithelial architecture and function. Analyses of a series of transgenic and knockout mice indicate that Plexin-B2 controls the cell division axis by signaling through its GTPase-activating protein (GAP) domain and Cdc42. Our data uncover semaphorin-plexin signaling as a central regulatory mechanism of mitotic spindle orientation necessary for the alignment of epithelial cell divisions with the epithelial plane.

AB - Morphogenesis, homeostasis, and regeneration of epithelial tissues rely on the accurate orientation of cell divisions, which is specified by the mitotic spindle axis. To remain in the epithelial plane, symmetrically dividing epithelial cells align their mitotic spindle axis with the plane. Here, we show that this alignment depends on epithelial cell-cell communication via semaphorin-plexin signaling. During kidney morphogenesis and repair, renal tubular epithelial cells lacking the transmembrane receptor Plexin-B2 or its semaphorin ligands fail to correctly orient the mitotic spindle, leading to severe defects in epithelial architecture and function. Analyses of a series of transgenic and knockout mice indicate that Plexin-B2 controls the cell division axis by signaling through its GTPase-activating protein (GAP) domain and Cdc42. Our data uncover semaphorin-plexin signaling as a central regulatory mechanism of mitotic spindle orientation necessary for the alignment of epithelial cell divisions with the epithelial plane.

U2 - 10.1016/j.devcel.2015.02.001

DO - 10.1016/j.devcel.2015.02.001

M3 - Journal article

C2 - 25892012

SN - 1534-5807

VL - 33

SP - 299

EP - 313

JO - Developmental Cell

JF - Developmental Cell

IS - 3

ER -

Semaphorin-Plexin Signaling Controls Mitotic Spindle Orientation during Epithelial Morphogenesis and Repair

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