SERCA Directs Cell Migration and Branching Across Species and Germ Layers

Overview

Journal Biol Open

Specialty Biology

Date 2017 Aug 20

PMID 28821490

Citations 4

Authors

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

Soon will be listed here.

Abstract

Branching morphogenesis underlies organogenesis in vertebrates and invertebrates, yet is incompletely understood. Here, we show that the sarco-endoplasmic reticulum Ca reuptake pump (SERCA) directs budding across germ layers and species. Clonal knockdown demonstrated a cell-autonomous role for SERCA in air sac budding. Live imaging of tracheogenesis revealed elevated Ca levels in migratory tip cells as they form branches. SERCA blockade abolished this Ca differential, aborting both cell migration and new branching. Activating protein kinase C (PKC) rescued Ca 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 ( nervous system) behaved similarly, suggesting a conserved requirement for cell-autonomous Ca signaling, established by SERCA, in iterative budding.

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References

Metzger R, Klein O, Martin G, Krasnow M . The branching programme of mouse lung development. Nature. 2008; 453(7196):745-50. PMC: 2892995. DOI: 10.1038/nature07005. View

Launay S, Gianni M, Kovacs T, Bredoux R, Bruel A, Gelebart P . Lineage-specific modulation of calcium pump expression during myeloid differentiation. Blood. 1999; 93(12):4395-405. View

Jesudason E, Connell M, Fernig D, Lloyd D, Losty P . Early lung malformations in congenital diaphragmatic hernia. J Pediatr Surg. 2000; 35(1):124-7; discussion 128. DOI: 10.1016/s0022-3468(00)80028-7. View

Bower D, Lee H, Lansford R, Zinn K, Warburton D, Fraser S . Airway branching has conserved needs for local parasympathetic innervation but not neurotransmission. BMC Biol. 2014; 12:92. PMC: 4255442. DOI: 10.1186/s12915-014-0092-2. View

Bellusci S, Grindley J, EMOTO H, Itoh N, Hogan B . Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development. 1998; 124(23):4867-78. DOI: 10.1242/dev.124.23.4867. View

Brand A, Perrimon N . Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 1993; 118(2):401-15. DOI: 10.1242/dev.118.2.401. View

Caspersen C, Pedersen P, Treiman M . The sarco/endoplasmic reticulum calcium-ATPase 2b is an endoplasmic reticulum stress-inducible protein. J Biol Chem. 2000; 275(29):22363-72. DOI: 10.1074/jbc.M001569200. View

Del Moral P, Sala F, Tefft D, Shi W, Keshet E, Bellusci S . VEGF-A signaling through Flk-1 is a critical facilitator of early embryonic lung epithelial to endothelial crosstalk and branching morphogenesis. Dev Biol. 2005; 290(1):177-88. DOI: 10.1016/j.ydbio.2005.11.022. View

Torralba S, Heath I . Cytoskeletal and Ca2+ regulation of hyphal tip growth and initiation. Curr Top Dev Biol. 2001; 51:135-87. DOI: 10.1016/s0070-2153(01)51005-4. View

10.

Lee H, Wright A, Zinn K . Live dissection of Drosophila embryos: streamlined methods for screening mutant collections by antibody staining. J Vis Exp. 2009; (34). PMC: 3149970. DOI: 10.3791/1647. View

11.

Caviglia S, Brankatschk M, Fischer E, Eaton S, Luschnig S . Staccato/Unc-13-4 controls secretory lysosome-mediated lumen fusion during epithelial tube anastomosis. Nat Cell Biol. 2016; 18(7):727-39. DOI: 10.1038/ncb3374. View

12.

Lacabaratz-Porret C, Launay S, Corvazier E, Bredoux R, Papp B, Enouf J . Biogenesis of endoplasmic reticulum proteins involved in Ca2+ signalling during megakaryocytic differentiation: an in vitro study. Biochem J. 2000; 350 Pt 3:723-34. PMC: 1221303. View

13.

Klambt C, Jacobs J, Goodman C . The midline of the Drosophila central nervous system: a model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell. 1991; 64(4):801-15. DOI: 10.1016/0092-8674(91)90509-w. View

14.

Arbabian A, Brouland J, Gelebart P, Kovacs T, Bobe R, Enouf J . Endoplasmic reticulum calcium pumps and cancer. Biofactors. 2011; 37(3):139-49. DOI: 10.1002/biof.142. View

15.

Strecker T, McGhee S, Shih S, Ham D . Permeabilization, staining and culture of living Drosophila embryos. Biotech Histochem. 1994; 69(1):25-30. DOI: 10.3109/10520299409106257. View

16.

Mammoto T, Ingber D . Mechanical control of tissue and organ development. Development. 2010; 137(9):1407-20. PMC: 2853843. DOI: 10.1242/dev.024166. View

17.

Affolter M, Zeller R, Caussinus E . Tissue remodelling through branching morphogenesis. Nat Rev Mol Cell Biol. 2009; 10(12):831-42. DOI: 10.1038/nrm2797. View

18.

Truong T, Supatto W, Koos D, Choi J, Fraser S . Deep and fast live imaging with two-photon scanned light-sheet microscopy. Nat Methods. 2011; 8(9):757-60. DOI: 10.1038/nmeth.1652. View

19.

Usachev Y, Marsh A, Johanns T, Lemke M, Thayer S . Activation of protein kinase C in sensory neurons accelerates Ca2+ uptake into the endoplasmic reticulum. J Neurosci. 2006; 26(1):311-8. PMC: 6674318. DOI: 10.1523/JNEUROSCI.2920-05.2006. View

20.

Malek A, Izumo S . Mechanism of endothelial cell shape change and cytoskeletal remodeling in response to fluid shear stress. J Cell Sci. 1996; 109 ( Pt 4):713-26. DOI: 10.1242/jcs.109.4.713. View