Literature DB >> 19237582

Wnt/beta-catenin and noncanonical Wnt signaling interact in tissue evagination in the simple eumetazoan Hydra.

Isabelle Philipp1, Roland Aufschnaiter, Suat Ozbek, Stefanie Pontasch, Marcell Jenewein, Hiroshi Watanabe, Fabian Rentzsch, Thomas W Holstein, Bert Hobmayer.   

Abstract

In and evaginations of 2D cell sheets are major shape generating processes in animal development. They result from directed movement and intercalation of polarized cells associated with cell shape changes. Work on several bilaterian model organisms has emphasized the role of noncanonical Wnt signaling in cell polarization and movement. However, the molecular processes responsible for generating tissue and body shape in ancestral, prebilaterian animals are unknown. We show that noncanonical Wnt signaling acts in mass tissue movements during bud and tentacle evagination and regeneration in the cnidarian polyp Hydra. The wnt5, wnt8, frizzled2 (fz2), and dishevelled-expressing cell clusters define the positions, where bud and tentacle evaginations are initiated; wnt8, fz2, and dishevelled remain up-regulated in those epithelial cells, undergoing cell shape changes during the entire evagination process. Downstream of wnt and dsh expression, JNK activity is required for the evagination process. Multiple ectopic wnt5, wnt8, fz2, and dishevelled-expressing centers and the subsequent evagination of ectopic tentacles are induced throughout the body column by activation of Wnt/beta-Catenin signaling. Our results indicate that integration of axial patterning and tissue morphogenesis by the coordinated action of canonical and noncanonical Wnt pathways was crucial for the evolution of eumetazoan body plans.

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Year:  2009        PMID: 19237582      PMCID: PMC2646623          DOI: 10.1073/pnas.0812847106

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  44 in total

Review 1.  Mechanisms of convergence and extension by cell intercalation.

Authors:  R Keller; L Davidson; A Edlund; T Elul; M Ezin; D Shook; P Skoglund
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2000-07-29       Impact factor: 6.237

2.  JNK functions in the non-canonical Wnt pathway to regulate convergent extension movements in vertebrates.

Authors:  Hiroaki Yamanaka; Tetsuo Moriguchi; Norihisa Masuyama; Morioh Kusakabe; Hiroshi Hanafusa; Ritsuko Takada; Shinji Takada; Eisuke Nishida
Journal:  EMBO Rep       Date:  2001-12-19       Impact factor: 8.807

3.  WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra.

Authors:  B Hobmayer; F Rentzsch; K Kuhn; C M Happel; C C von Laue; P Snyder; U Rothbächer; T W Holstein
Journal:  Nature       Date:  2000-09-14       Impact factor: 49.962

Review 4.  Convergent extension: the molecular control of polarized cell movement during embryonic development.

Authors:  John B Wallingford; Scott E Fraser; Richard M Harland
Journal:  Dev Cell       Date:  2002-06       Impact factor: 12.270

5.  SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase.

Authors:  B L Bennett; D T Sasaki; B W Murray; E C O'Leary; S T Sakata; W Xu; J C Leisten; A Motiwala; S Pierce; Y Satoh; S S Bhagwat; A M Manning; D W Anderson
Journal:  Proc Natl Acad Sci U S A       Date:  2001-11-20       Impact factor: 11.205

Review 6.  Shaping the vertebrate body plan by polarized embryonic cell movements.

Authors:  Ray Keller
Journal:  Science       Date:  2002-12-06       Impact factor: 47.728

7.  Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton.

Authors:  C G Winter; B Wang; A Ballew; A Royou; R Karess; J D Axelrod; L Luo
Journal:  Cell       Date:  2001-04-06       Impact factor: 41.582

8.  A mutational analysis of dishevelled in Drosophila defines novel domains in the dishevelled protein as well as novel suppressing alleles of axin.

Authors:  Andrea Penton; Andreas Wodarz; Roel Nusse
Journal:  Genetics       Date:  2002-06       Impact factor: 4.562

9.  Small-molecule antagonists of the oncogenic Tcf/beta-catenin protein complex.

Authors:  Maina Lepourcelet; Ying-Nan P Chen; Dennis S France; Huisheng Wang; Phillip Crews; Frank Petersen; Charles Bruseo; Alexander W Wood; Ramesh A Shivdasani
Journal:  Cancer Cell       Date:  2004-01       Impact factor: 31.743

10.  HyAlx, an aristaless-related gene, is involved in tentacle formation in hydra.

Authors:  K M Smith; L Gee; H R Bode
Journal:  Development       Date:  2000-11       Impact factor: 6.868

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  53 in total

1.  In vivo imaging of basement membrane movement: ECM patterning shapes Hydra polyps.

Authors:  Roland Aufschnaiter; Evan A Zamir; Charles D Little; Suat Özbek; Sandra Münder; Charles N David; Li Li; Michael P Sarras; Xiaoming Zhang
Journal:  J Cell Sci       Date:  2011-12-01       Impact factor: 5.285

Review 2.  Cellular and molecular processes leading to embryo formation in sponges: evidences for high conservation of processes throughout animal evolution.

Authors:  Alexander V Ereskovsky; Emmanuelle Renard; Carole Borchiellini
Journal:  Dev Genes Evol       Date:  2012-04-29       Impact factor: 0.900

3.  The evolution of the Wnt pathway.

Authors:  Thomas W Holstein
Journal:  Cold Spring Harb Perspect Biol       Date:  2012-07-01       Impact factor: 10.005

4.  Turing's theory of morphogenesis of 1952 and the subsequent discovery of the crucial role of local self-enhancement and long-range inhibition.

Authors:  Hans Meinhardt
Journal:  Interface Focus       Date:  2012-02-08       Impact factor: 3.906

5.  A small molecule screen identifies a novel compound that induces a homeotic transformation in Hydra.

Authors:  Kristine M Glauber; Catherine E Dana; Steve S Park; David A Colby; Yukihiko Noro; Toshitaka Fujisawa; A Richard Chamberlin; Robert E Steele
Journal:  Development       Date:  2013-12       Impact factor: 6.868

Review 6.  Evolutionary crossroads in developmental biology: Cnidaria.

Authors:  Ulrich Technau; Robert E Steele
Journal:  Development       Date:  2011-03-09       Impact factor: 6.868

7.  Autoregulatory and repressive inputs localize Hydra Wnt3 to the head organizer.

Authors:  Yukio Nakamura; Charisios D Tsiairis; Suat Özbek; Thomas W Holstein
Journal:  Proc Natl Acad Sci U S A       Date:  2011-05-16       Impact factor: 11.205

8.  Dynamic expression of a Hydra FGF at boundaries and termini.

Authors:  Ellen Lange; Stephanie Bertrand; Oliver Holz; Nicole Rebscher; Monika Hassel
Journal:  Dev Genes Evol       Date:  2014-10-14       Impact factor: 0.900

9.  Regeneration and transdetermination: the role of wingless and its regulation.

Authors:  Margrit Schubiger; Anne Sustar; Gerold Schubiger
Journal:  Dev Biol       Date:  2010-09-21       Impact factor: 3.582

10.  Frizzled-Induced Van Gogh Phosphorylation by CK1ε Promotes Asymmetric Localization of Core PCP Factors in Drosophila.

Authors:  Lindsay K Kelly; Jun Wu; Wang A Yanfeng; Marek Mlodzik
Journal:  Cell Rep       Date:  2016-06-23       Impact factor: 9.423

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