Light-activated Frizzled7 reveals a permissive role of non-canonical wnt signaling in mesendoderm cell migration

被引:35
作者
Capek, Daniel [1 ]
Smutny, Michael [1 ,2 ,3 ]
Tichy, Alexandra-Madelaine [4 ,5 ]
Morri, Maurizio [1 ]
Janovjak, Harald [1 ,4 ,5 ]
Heisenberg, Carl-Philipp [1 ]
机构
[1] IST Austria, Klosterneuburg, Austria
[2] Univ Warwick, Warwick Med Sch, Ctr Mechnochem Cell Biol, Coventry, W Midlands, England
[3] Univ Warwick, Warwick Med Sch, Div Biomed Sci, Coventry, W Midlands, England
[4] Monash Univ, Fac Med Nursing & Hlth Sci, Clayton, Vic, Australia
[5] Monash Univ, European Mol Biol Lab Australia EMBL Australia, Clayton, Vic, Australia
基金
欧洲研究理事会;
关键词
CONVERGENT EXTENSION MOVEMENTS; PLANAR POLARITY; OPTOGENETIC CONTROL; GASTRULATION; ORIENTATION; DROSOPHILA; LOCALIZATION; ENDOCYTOSIS; DIVISION; DYNAMICS;
D O I
10.7554/eLife.42093
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
Non-canonical Wnt signaling plays a central role for coordinated cell polarization and directed migration in metazoan development. While spatiotemporally restricted activation of noncanonical Wnt-signaling drives cell polarization in epithelial tissues, it remains unclear whether such instructive activity is also critical for directed mesenchymal cell migration. Here, we developed a light-activated version of the non-canonical Wnt receptor Frizzled 7 (Fz7) to analyze how restricted activation of non-canonical Wnt signaling affects directed anterior axial mesendoderm (prechordal plate, ppl) cell migration within the zebrafish gastrula. We found that Fz7 signaling is required for ppl cell protrusion formation and migration and that spatiotemporally restricted ectopic activation is capable of redirecting their migration. Finally, we show that uniform activation of Fz7 signaling in ppl cells fully rescues defective directed cell migration in fz7 mutant embryos. Together, our findings reveal that in contrast to the situation in epithelial cells, non-canonical Wnt signaling functions permissively rather than instructively in directed mesenchymal cell migration during gastrulation.
引用
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页数:24
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共 88 条
[1]   Temporally precise in vivo control of intracellular signalling [J].
Airan, Raag D. ;
Thompson, Kimberly R. ;
Fenno, Lief E. ;
Bernstein, Hannah ;
Deisseroth, Karl .
NATURE, 2009, 458 (7241) :1025-1029
[2]   Design and functional evaluation of an optically active μ-opioid receptor [J].
Barish, Philip A. ;
Xu, Ying ;
Li, Jianxin ;
Sun, Jiao ;
Jarajapu, Yagna P. R. ;
Ogle, William O. .
EUROPEAN JOURNAL OF PHARMACOLOGY, 2013, 705 (1-3) :42-48
[3]   An Effective Feedback Loop between Cell-Cell Contact Duration and Morphogen Signaling Determines Cell Fate [J].
Barone, Vanessa ;
Lang, Moritz ;
Krens, S. F. Gabriel ;
Pradhan, Saurabh J. ;
Shamipour, Shayan ;
Sako, Keisuke ;
Sikora, Mateusz ;
Guet, Calin C. ;
Heisenberg, Carl-Philipp .
DEVELOPMENTAL CELL, 2017, 43 (02) :198-+
[4]   Secreted Frizzled-related Protein 2 (sFRP2) Redirects Non-canonical Wnt Signaling from Fz7 to Ror2 during Vertebrate Gastrulation [J].
Brinkmann, Eva-Maria ;
Mattes, Benjamin ;
Kumar, Rahul ;
Hagemann, Anja I. H. ;
Gradl, Dietmar ;
Scholpp, Steffen ;
Steinbeisser, Herbert ;
Kaufmann, Lilian T. ;
Oezbek, Suat .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2016, 291 (26) :13730-13742
[5]   Evolutionary conservation of early mesoderm specification by mechanotransduction in Bilateria [J].
Brunet, Thibaut ;
Bouclet, Adrien ;
Ahmadi, Padra ;
Mitrossilis, Demosthene ;
Driquez, Benjamin ;
Brunet, Anne-Christine ;
Henry, Laurent ;
Serman, Fanny ;
Bealle, Gaelle ;
Menager, Christine ;
Dumas-Bouchiat, Frederic ;
Givord, Dominique ;
Yanicostas, Constantin ;
Le-Roy, Damien ;
Dempsey, Nora M. ;
Plessis, Anne ;
Farge, Emmanuel .
NATURE COMMUNICATIONS, 2013, 4
[6]   Spatial and temporal analysis of PCP protein dynamics during neural tube closure [J].
Butler, Mitchell T. ;
Wallingford, John B. .
ELIFE, 2018, 7
[7]   Prickle 1 regulates cell movements during gastrulation and neuronal migration in zebrafish [J].
Carreira-Barbosa, F ;
Concha, ML ;
Takeuchi, M ;
Ueno, N ;
Wilson, SW ;
Tada, M .
DEVELOPMENT, 2003, 130 (17) :4037-4046
[8]   Mechanical Strain Determines the Axis of Planar Polarity in Ciliated Epithelia [J].
Chien, Yuan-Hung ;
Keller, Ray ;
Kintner, Chris ;
Shook, David R. .
CURRENT BIOLOGY, 2015, 25 (21) :2774-2784
[9]   Crystal structure of metarhodopsin II [J].
Choe, Hui-Woog ;
Kim, Yong Ju ;
Park, Jung Hee ;
Morizumi, Takefumi ;
Pai, Emil F. ;
Krauss, Norbert ;
Hofmann, Klaus Peter ;
Scheerer, Patrick ;
Ernst, Oliver P. .
NATURE, 2011, 471 (7340) :651-U137
[10]   Wnt proteins can direct planar cell polarity in vertebrate ectoderm [J].
Chu, Chih-Wen ;
Sokol, Sergei Y. .
ELIFE, 2016, 5