SERCA directs cell migration and branching across species and germ layers

被引:5
作者
Bower, Danielle V. [1 ,2 ,11 ,12 ]
Lansdale, Nick [3 ,4 ,5 ]
Navarro, Sonia [2 ,6 ]
Truong, Thai V. [1 ,8 ]
Bower, Dan J. [9 ]
Featherstone, Neil C. [3 ,4 ]
Connell, Marilyn G. [3 ,4 ]
Al Alam, Denise [2 ]
Frey, Mark R. [2 ]
Trinh, Le A. [1 ,8 ]
Fernandez, G. Esteban [2 ]
Warburton, David [2 ]
Fraser, Scott E. [1 ,7 ,8 ]
Bennett, Daimark [3 ,4 ]
Jesudason, Edwin C. [1 ,2 ,10 ]
机构
[1] CALTECH, Div Biol Sci, Pasadena, CA 91125 USA
[2] Childrens Hosp Los Angeles, Saban Res Inst, Los Angeles, CA 90027 USA
[3] Univ Liverpool, Dept Biochem, Liverpool L69 7ZB, Merseyside, England
[4] Univ Liverpool, Ctr Cell Imaging, Inst Integrat Biol, Liverpool L69 7ZB, Merseyside, England
[5] Univ Liverpool, Inst Translat Med, Div Child Hlth, Liverpool L12 2AP, Merseyside, England
[6] Univ Southern Calif, Herman Ostrow Sch Dent, Craniofacial Biol, Los Angeles, CA 90089 USA
[7] Univ Southern Calif, Biol Sci & Biomed Engn, Los Angeles, CA 90089 USA
[8] Univ Southern Calif, Translat Imaging Ctr, Biol Sci & Mol & Computat Biol, Los Angeles, CA 90089 USA
[9] Univ Bern, Ctr Space & Habitabil, CH-3012 Bern, Switzerland
[10] NHS Lothian, Edinburgh EH14 1TY, Midlothian, Scotland
[11] Univ Bern, Bern Univ Hosp, Inselspital, Dept Diagnost Intervent & Pediat Radiol, CH-3010 Bern, Switzerland
[12] Univ Bern, Dept Biomed Res, CH-3008 Bern, Switzerland
基金
美国国家卫生研究院; 英国医学研究理事会; 英国惠康基金;
关键词
Branching morphogenesis; Cell migration; SERCA; Calcium dynamics; ENDOPLASMIC-RETICULUM CA2+-ATPASE; CONGENITAL DIAPHRAGMATIC-HERNIA; DROSOPHILA TRACHEAL SYSTEM; CALCIUM-PUMP EXPRESSION; LUNG DEVELOPMENT; AIRWAY PERISTALSIS; GENE-EXPRESSION; MOUSE LUNG; RAT LUNG; MORPHOGENESIS;
D O I
10.1242/bio.026039
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
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.
引用
收藏
页码:1458 / 1471
页数:14
相关论文
共 66 条
[1]   Parallel adaptive feedback enhances reliability of the Ca2+ signaling system [J].
Abell, Ellen ;
Ahrends, Robert ;
Bandara, Samuel ;
Park, Byung Ouk ;
Teruel, Mary N. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2011, 108 (35) :14485-14490
[2]   Tissue remodelling through branching morphogenesis [J].
Affolter, Markus ;
Zeller, Rolf ;
Caussinus, Emmanuel .
NATURE REVIEWS MOLECULAR CELL BIOLOGY, 2009, 10 (12) :831-842
[3]   Bcl-2 Suppresses Sarcoplasmic/Endoplasmic Reticulum Ca2+-ATPase Expression in Cystic Fibrosis Airways [J].
Ahmad, Shama ;
Ahmad, Aftab ;
Dremina, Elena S. ;
Sharov, Victor S. ;
Guo, Xiaoling ;
Jones, Tara N. ;
Loader, Joan E. ;
Tatreau, Jason R. ;
Perraud, Anne-Laure ;
Schoeneich, Christian ;
Randell, Scott H. ;
White, Carl W. .
AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE, 2009, 179 (09) :816-826
[4]   Endoplasmic reticulum calcium pumps and cancer [J].
Arbabian, Atousa ;
Brouland, Jean-Philippe ;
Gelebart, Pascal ;
Kovacs, Tuende ;
Bobe, Regis ;
Enouf, Jocelyne ;
Papp, Bela .
BIOFACTORS, 2011, 37 (03) :139-149
[5]  
Bellusci S, 1997, DEVELOPMENT, V124, P4867
[6]   Airway branching has conserved needs for local parasympathetic innervation but not neurotransmission [J].
Bower, Danielle V. ;
Lee, Hyung-Kook ;
Lansford, Rusty ;
Zinn, Kai ;
Warburton, David ;
Fraser, Scott E. ;
Jesudason, Edwin C. .
BMC BIOLOGY, 2014, 12
[7]  
BRAND AH, 1993, DEVELOPMENT, V118, P401
[8]   The asthma-associated ORMDL3 gene product regulates endoplasmic reticulum-mediated calcium signaling and cellular stress [J].
Cantero-Recasens, Gerard ;
Fandos, Cesar ;
Rubio-Moscardo, Fanny ;
Valverde, Miguel A. ;
Vicente, Ruben .
HUMAN MOLECULAR GENETICS, 2010, 19 (01) :111-121
[9]   The sarco/endoplasmic reticulum calcium-ATPase 2b is an endoplasmic reticulum stress-inducible protein [J].
Caspersen, C ;
Pedersen, PS ;
Treiman, M .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2000, 275 (29) :22363-22372
[10]   Staccato/Unc-13-4 controls secretory lysosome-mediated lumen fusion during epithelial tube anastomosis [J].
Caviglia, Sara ;
Brankatschk, Marko ;
Fischer, Elisabeth J. ;
Eaton, Suzanne ;
Luschnig, Stefan .
NATURE CELL BIOLOGY, 2016, 18 (07) :727-+