SERCA directs cell migration and branching across species and germ layers

Author:

Bower Danielle V.123ORCID,Lansdale Nick4,Navarro Sonia25,Truong Thai V.16,Bower Dan J.7,Featherstone Neil C.4,Connell Marilyn G.4,Al-Alam Denise2,Frey Mark R.2,Trinh Le A.16,Fernandez G. Esteban2,Warburton David2,Fraser Scott E.18,Bennett Daimark4,Jesudason Edwin C.129

Affiliation:

1. Division of Biological Sciences, California Institute of Technology, USA

2. The Saban Research Institute, Children's Hospital Los Angeles, USA

3. Department of Diagnostic, Interventional and Pediatric Radiology, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland

4. Department of Biochemistry & Centre for Cell Imaging, Institute of Integrative Biology, University of Liverpool, UK

5. Craniofacial Biology, Herman Ostrow School of Dentistry, University of Southern California, USA

6. Biological Sciences and Molecular and Computational Biology, Translational Imaging Center, University of Southern California, Los Angeles, USA

7. Institute of Geophysics, Department of Earth Sciences, ETH Zürich, Zürich, Switzerland

8. Biological Sciences and Biomedical Engineering, University of Southern California, Los Angeles, USA

9. NHS Lothian, Edinburgh, UK

Abstract

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.

Funder

National Institutes of Health

Pasadena Guild Endowment of Children's Hospital Los Angeles

Royal College of Surgeons of England

Wellcome Trust

Medical Research Council

Crohn's and Colitis Foundation of America

California Institute for Regenerative Medicine

Garland Foundation

Webb Foundation

St. Andrew's Society of Los Angeles

Publisher

The Company of Biologists

Subject

General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology

Reference66 articles.

1. Parallel adaptive feedback enhances reliability of the Ca2+ signaling system;Abell;Proc. Natl. Acad. Sci. USA,2011

2. Tissue remodeling through branching morphogenesis;Affolter;Nat. Rev. Mol. Cell Biol.,2009

3. Bcl-2 suppresses sarcoplasmic/endoplasmic reticulum Ca2+-ATPase expression in cystic fibrosis airways;Ahmad;Am. J. Respir. Crit. Care. Med.,2009

4. Endoplasmic reticulum calcium pumps and cancer;Arbabian;Biofactors,2011

5. Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung;Bellusci;Development,1997

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