A05

The Wnt code: Deciphering early Wnt interactions in Hydra

Funding period: 2017-2029

Project A05

Project Leaders

Prof. Dr. Motomu Tanaka

Prof. Dr. Motomu Tanaka

 Project Leader A05

Prof. Dr. Thomas Holstein

 Project Leader A05

Abstract

Wnt genes are metazoan specific and play critical roles in embryonic patterning and cell differentiation. Using the Hydra regeneration model, we found that injury-induced MAPK activation primes the formation of a Wnt-driven signaling center (organizer). Physical cues and Hippo-Yap signaling are also essential for the establishment and maintenance of this organizer. Here we aim to reveal the spatiotemporal coupling of Wnt/Hippo-Yap signaling and mechanical forces through the de novo formation of the head organizer. Our data will help to understand how different Wnts and mechanical forces work together during animal evolution.

Project-related Publications

The origin and evolution of Wnt signalling

Holzem M, Boutros M, Holstein TW. Nat Rev Genet. 2024 Feb 19. Online ahead of print. PMID: 38374446

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A predatory gastrula leads to symbiosis-independent settlement in Aiptasia.

Maegele I, Rupp S, Özbek S, Guse A, Hambleton EA, Holstein TW. Proc Natl Acad Sci U S A. 2023 Oct 3;120(40):e2311872120. doi: 10.1073/pnas.2311872120. Epub 2023 Sep 25. PMID: 37748072

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Wnt/β-catenin signaling induces axial elasticity patterns of Hydra extracellular matrix

Veschgini M, Suzuki R, Kling S, Petersen HO, Bergheim BG, Abuillan W, Linke P, Kaufmann S, Burghammer M, Engel U, Stein F, Özbek S, Holstein TW, Tanaka M. iScience. 2023 Mar 16;26(4):106416. doi: 10.1016/j.isci.2023.106416. eCollection 2023 Apr 21. PMID: 37009232

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From injury to patterning-MAPKs and Wnt signaling in Hydra

Tursch A, Holstein TW. Curr Top Dev Biol. 2023;153:381-417. doi: 10.1016/bs.ctdb.2023.01.003. Epub 2023 Feb 9. PMID: 36967201 Review.

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Injury-induced MAPK activation triggers body axis formation in Hydra by default Wnt signaling

Tursch A, Bartsch N, Mercker M, Schlüter J, Lommel M, Marciniak-Czochra A, Özbek S, Holstein TW. Proc Natl Acad Sci U S A. 2022 Aug 30;119(35):e2204122119. doi: 10.1073/pnas.2204122119. Epub 2022 Aug 22. PMID: 35994642

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The role of cnidarian developmental biology in unraveling axis formation and Wnt signaling.

Holstein TW. Dev Biol. 2022 Apr 22;487:74-98. doi: 10.1016/j.ydbio.2022.04.005. Online ahead of print. PMID: 35461834

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Two plus one is almost three: a fast approximation for multi-view deconvolution

Hüpfel M, Fernández Merino M, Bennemann J, Takamiya M, Rastegar S, Tursch A, Holstein TW, Nienhaus GU. Biomed Opt Express. 2021 Dec 7;13(1):147-158. doi: 10.1364/BOE.443660. eCollection 2022 Jan 1. PMID: 35154860

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The Wnt-specific astacin proteinase HAS-7 restricts head organizer formation in Hydra

Ziegler B, Yiallouros I, Trageser B, Kumar S, Mercker M, Kling S, Fath M, Warnken U, Schnölzer M, Holstein TW, Hartl M, Marciniak-Czochra A, Stetefeld J, Stöcker W, Özbek S. BMC Biol. 2021 Jun 9;19(1):120. 
PMID: 34107975

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Wnt/β-Catenin Signaling Controls Spatio-Temporal Elasticity Patterns in Extracellular Matrix during Hydra Morphogenesis

Veschgini, M., H.O. Petersen, F. Rossetti, W. Abuillan, S. Kaufmann, R. Suzuki, M. Burghammer, S. Özbek, T.W. Holstein, and M. Tanaka. 2020. bioRxiv, preprint.

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MAPK signaling links the injury response to Wnt-regulated patterning in Hydra regeneration

Tursch, A., M. Lommel, N. Bartsch, and T.W. Holstein. 2020.  bioRxiv, preprint.

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Expansion of a single transposable element family is associated with genome-size increase and radiation in the genus Hydra

Wong WY, Simakov O, Bridge DM, Cartwright P, Bellantuono AJ, Kuhn A, Holstein TW, David CN, Steele RE, Martínez DE. Proc Natl Acad Sci U S A. 2019 Nov 12;116(46):22915-22917. PMID: 31659034

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What makes flatworms go to pieces

Holstein TW. Nature. 2019 Aug;572(7771):593-594. PMID: 31444489

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Hydra Mesoglea Proteome Identifies Thrombospondin as a Conserved Component Active in Head Organizer Restriction

Lommel M, Strompen J, Hellewell AL, Balasubramanian GP, Christofidou ED, Thomson AR, Boyle AL, Woolfson DN, Puglisi K, Hartl M, Holstein TW, Adams JC, Özbek S. Sci Rep. 2018 Aug 6;8(1):11753. PMID:30082916

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Making head or tail of cnidarian hox gene function

Rentzsch F, Holstein TW. Nat Commun. 2018 Jun 5;9(1):2187. PMID:29872045

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Tracking mechanical and morphological dynamics of regenerating Hydra tissue fragments using a two fingered micro-robotic hand

Veschgini, M., Gebert, F., Khangai, N., Ito, H., Suzuki, R., Holstein, T. W., Mae, Y., Arai, T. and Tanaka, M. 2016. Appl. Phys. Lett. 108, 103702

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A Comprehensive Transcriptomic and Proteomic Analysis of Hydra Head Regeneration.

Petersen, H.O., S.K. Hoger, M. Looso, T. Lengfeld, A. Kuhn, U. Warnken, C. Nishimiya-Fujisawa, M. Schnolzer, M. Kruger, S. Ozbek, O. Simakov, and T.W. Holstein. Mol Biol Evol. 2015 Aug;32(8):1928-47. doi: 10.1093/molbev/msv079. Epub 2015 Apr 3. PMID: 25841488

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Nodal signalling determines biradial asymmetry in Hydra

Watanabe H, Schmidt HA, Kuhn A, Höger SK, Kocagöz Y, Laumann-Lipp N, Ozbek S, Holstein TW. Nature. 2014 Nov 6;515(7525):112-5. doi: 10.1038/nature13666. Epub 2014 Aug 24.
PMID: 25156256

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Autoregulatory and repressive inputs localize Hydra Wnt3 to the head organizer

Nakamura Y, Tsiairis CD, Özbek S, Holstein TW. Proc Natl Acad Sci U S A. 2011 May 31;108(22):9137-42. doi: 10.1073/pnas.1018109108. Epub 2011 May 16. PMID: 21576458

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Unexpected complexity of the Wnt gene family in a sea anemone

Kusserow A, Pang K, Sturm C, Hrouda M, Lentfer J, Schmidt HA, Technau U, von Haeseler A, Hobmayer B, Martindale MQ, Holstein TW. Nature. 2005 Jan 13;433(7022):156-60. doi: 10.1038/nature03158.
PMID: 15650739

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

Hobmayer B, Rentzsch F, Kuhn K, Happel CM, von Laue CC, Snyder P, Rothbächer U, Holstein TW. Nature. 2000 Sep 14;407(6801):186-9. doi: 10.1038/35025063.
PMID: 11001056

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