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SERCA directs cell migration and branching across species and germ layers

Bower, Danielle V. and Lansdale, Nick and Navarro, Sonia and Truong, Thai V. and Bower, Dan J. and Featherstone, Neil C. and Connell, Marilyn G. and Al Alam, Denise and Frey, Mark R. and Trinh, Le A. and Fernandez, G. Esteban and Warburton, David and Fraser, Scott E. and Bennett, Daimark and Jesudason, Edwin C. (2017) SERCA directs cell migration and branching across species and germ layers. Biology Open, 6 (10). pp. 1458-1471. ISSN 2046-6390. PMCID PMC5665464. https://resolver.caltech.edu/CaltechAUTHORS:20171103-082000956

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Abstract

Branching morphogenesis underlies organogenesis in vertebrates and invertebrates, yet is incompletely understood. Here, we show that the sarco-endoplasmic reticulum Ca^(2+) 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 Ca^(2+) levels in migratory tip cells as they form branches. SERCA blockade abolished this Ca^(2+) differential, aborting both cell migration and new branching. Activating protein kinase C (PKC) rescued Ca^(2+) 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 Ca^(2+) signaling, established by SERCA, in iterative budding.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1242/bio.026039DOIArticle
http://bio.biologists.org/content/6/10/1458PublisherArticle
http://bio.biologists.org/content/6/10/1458.supplementalPublisherSupplementary Information
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5665464PubMed CentralArticle
ORCID:
AuthorORCID
Bower, Danielle V.0000-0002-4469-4855
Bower, Dan J.0000-0002-0673-4860
Fraser, Scott E.0000-0002-5377-0223
Additional Information:© 2017 Published by The Company of Biologists Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. Received April 26, 2017; Accepted August 14, 2017; Published online October 15, 2017. We thank Sean McCann for his assistance with the migration and shedding assays, and Kai Zinn and Hyung-Kook Lee for advice on the Drosophila embryo studies. The authors declare no competing or financial interests. Author contributions: Conceptualization: E.C.J., D.V.B.; Methodology: D.V.B., N.L., S.N., T.V.T., N.C.F., M.G.C., D.A., M.R.F., L.A.T., G.E.F., D.W., S.E.F., D.B., E.C.J.; Software: D.V.B., D.J.B.; Validation: D.V.B., N.L., D.B., E.C.J.; Formal analysis: D.V.B., N.L., S.N., N.C.F., M.G.C., D.A., M.R.F., G.E.F., D.B., E.C.J.; Investigation: D.V.B., N.L., S.N., T.V.T., N.C.F., M.G.C., D.A., M.R.F., G.E.F., E.C.J.; Resources: D.V.B., N.L., T.V.T., N.C.F., M.G.C., M.R.F., L.A.T., D.W., S.E.F., D.B., E.C.J.; Data curation: D.V.B., N.L., S.N., N.C.F., M.G.C., D.A., M.R.F., G.E.F., E.C.J.; Writing - original draft: D.V.B., E.C.J.; Writing - review & editing: D.V.B., N.L., S.N., M.R.F., L.A.T., G.E.F., D.W., S.E.F., D.B., E.C.J.; Visualization: D.V.B., D.J.B., E.C.J.; Supervision: D.W., S.E.F., D.B., E.C.J.; Project administration: D.V.B., E.C.J.; Funding acquisition: D.V.B., D.W., S.E.F., D.B., E.C.J. Funding: D.V.B. was funded by the National Institutes of Health (NHLBI) grant no. NRSA 1F30 HL110723, National Institutes of Health FaceBase grant no. U01 DE020063 and the Pasadena Guild Endowment of Children's Hospital Los Angeles. N.L. was funded by the Royal College of Surgeons of England and The Wellcome Trust, UK grant no. WT090124MA. S.N. was funded by a HURM graduate student supplement to the National Institutes of Health grant no. NIGMS R01GM096195 (D.W. as co-PI) and DE training grant T90 DE021982. N.C.F. was funded by The Royal College of Surgeons of England and the Medical Research Council, UK. M.R.F. is funded by National Institutes of Health award R03DK090295, and a Senior Research Award from the Crohn's and Colitis Foundation of America. D.W. was funded by the National Institutes of Health HL44060, 44977, 60231 and 12268, California Institute for Regenerative Medicine Training Grant TG2-01168 and Shared Laboratory Grant CL1-00507, the Garland Foundation, the Webb Foundation, the Pasadena Guild Endowment of Children's Hospital Los Angeles and the St Andrew's Society of Los Angeles. D.B. was funded by the Medical Research Council, UK grant no. MR/K015931/1. E.C.J. was funded by a Medical Research Council New Investigator Award grant no. G0802057, a Medical Research Council Centenary Award and an American Asthma Foundation Early Excellence Award grant no. 11-0051.
Funders:
Funding AgencyGrant Number
NIH Postdoctoral Fellowship1F30 HL110723
NIHU01 DE020063
Children’s Hospital Los Angeles Pasadena GuildUNSPECIFIED
Royal College of Surgeons of EnglandUNSPECIFIED
Wellcome TrustWT090124MA
NIHR01GM096195
NIH Predoctoral FellowshipT90 DE021982
Medical Research Council (UK)MR/K015931/1
NIHR03DK090295
Crohn's and Colitis Foundation of AmericaUNSPECIFIED
NIHHL44060
NIHHL44977
NIHHL60231
NIHHL12268
California Institute for Regenerative MedicineTG2-01168
Children's Hospital Los AngelesCL1-00507
John Jewett and Helen Chandler Garland FoundationUNSPECIFIED
Del Webb FoundationUNSPECIFIED
St Andrew's Society of Los AngelesUNSPECIFIED
Medical Research Council (UK)G0802057
American Asthma Foundation11-0051
Subject Keywords:Branching morphogenesis; Cell migration; SERCA; Calcium dynamics
Issue or Number:10
PubMed Central ID:PMC5665464
Record Number:CaltechAUTHORS:20171103-082000956
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20171103-082000956
Official Citation: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 Biology Open 2017 6: 1458-1471; doi: 10.1242/bio.026039
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:82928
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:03 Nov 2017 17:01
Last Modified:09 Mar 2020 13:18

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