SERCA directs cell migration and branching across species and germ layers

Danielle V. Bower; Nick Lansdale; Sonia Navarro; Thai V. Truong; Dan J. Bower; Neil C. Featherstone; Marilyn G. Connell; Denise Al Alam; Mark R. Frey; Le A. Trinh; G. Esteban Fernandez; David Warburton; Scott E. Fraser; Daimark Bennett; Edwin C. Jesudason

doi:10.1242/bio.026039

Biology Open (Oct 2017)

SERCA directs cell migration and branching across species and germ layers

Danielle V. Bower,
Nick Lansdale,
Sonia Navarro,
Thai V. Truong,
Dan J. Bower,
Neil C. Featherstone,
Marilyn G. Connell,
Denise Al Alam,
Mark R. Frey,
Le A. Trinh,
G. Esteban Fernandez,
David Warburton,
Scott E. Fraser,
Daimark Bennett,
Edwin C. Jesudason

Affiliations

Danielle V. Bower: Division of Biological Sciences, California Institute of Technology, Pasadena, CA 91125, USA
Nick Lansdale: Department of Biochemistry & Centre for Cell Imaging, Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, UK
Sonia Navarro: The Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, CA 90027, USA
Thai V. Truong: Division of Biological Sciences, California Institute of Technology, Pasadena, CA 91125, USA
Dan J. Bower: Center for Space and Habitability, University of Bern, 3012 Bern, Switzerland
Neil C. Featherstone: Department of Biochemistry & Centre for Cell Imaging, Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, UK
Marilyn G. Connell: Department of Biochemistry & Centre for Cell Imaging, Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, UK
Denise Al Alam: The Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, CA 90027, USA
Mark R. Frey: The Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, CA 90027, USA
Le A. Trinh: Division of Biological Sciences, California Institute of Technology, Pasadena, CA 91125, USA
G. Esteban Fernandez: The Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, CA 90027, USA
David Warburton: The Saban Research Institute, Children's Hospital Los Angeles, Los Angeles, CA 90027, USA
Scott E. Fraser: Division of Biological Sciences, California Institute of Technology, Pasadena, CA 91125, USA
Daimark Bennett: Department of Biochemistry & Centre for Cell Imaging, Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, UK
Edwin C. Jesudason: Division of Biological Sciences, California Institute of Technology, Pasadena, CA 91125, USA

DOI: https://doi.org/10.1242/bio.026039
Journal volume & issue: Vol. 6, no. 10
pp. 1458 – 1471

Abstract

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Branching morphogenesis underlies organogenesis in vertebrates and invertebrates, yet is incompletely understood. Here, we show that the sarco-endoplasmic reticulum Ca2+ reuptake pump (SERCA) directs budding across germ layers and species. Clonal knockdown demonstrated a cell-autonomous role for SERCA in Drosophila air sac budding. Live imaging of Drosophila tracheogenesis revealed elevated Ca2+ levels in migratory tip cells as they form branches. SERCA blockade abolished this Ca2+ differential, aborting both cell migration and new branching. Activating protein kinase C (PKC) rescued Ca2+ in tip cells and restored cell migration and branching. Likewise, inhibiting SERCA abolished mammalian epithelial budding, PKC activation rescued budding, while morphogens did not. Mesoderm (zebrafish angiogenesis) and ectoderm (Drosophila nervous system) behaved similarly, suggesting a conserved requirement for cell-autonomous Ca2+ signaling, established by SERCA, in iterative budding.

Published in Biology Open

ISSN: 2046-6390 (Online)
Publisher: The Company of Biologists
Country of publisher: United Kingdom
LCC subjects: Science: Biology (General)
Website: https://journals.biologists.com/bio

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